advances in ecological research, volume 12

Advances in

ECOLOGICAL RESEARCH

VOLUME 12

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Advances in

ECOLOGICAL RESEARCH

Edited by

A. MACFADYEN School of Biological and Environmental Studies, New University of Ulster,

Coleraine, County Londonderry. Northern Ireland

E. D. FORD Institute of Terrestrial Ecology, Bush Estate, Penicuik, Midlothian

VOLUME 12

1982

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Contributors to Volume 12

W. ARTHUR, Department of Biology, Sunderland Polytechnic, Sunderland, SRI 3SD, UK

J. P. DEMPSTER, Institute of Terrestrial Ecology, Monks Wood Experi- mental Station, Abbots Ripton. Huntingdon. Cambridgeshire, PEI 7 2LS. U K

Z. NAVEH, Faculty of Agricultural Engineering, Technion-Israel Institute of Technology, Haifa, Israel

D. H. N. SPENCE, Deparrment of Botany. University of St Andrew, Fife, Scotland, KY16 9AL, U K

Preface

Readers already familiar with this series will, I am sure, be glad to see that Dr David Ford of the Institute of Terrestrial Ecology, Edinburgh, has joined me as co-editor with effect from the present volume. Not only are his fields of ecological expertise complementary to mine but he has world-wide knowledge of ecological research, both academic and applied. This move, as will be evident from the contents of Volume 13, will certainly broaden the range of articles which we can solicit from experienced authors. We would both like to emphasize that we welcome proposals from those who can write about their research fields in such a way as to interest and inform colleagues across the whole range of ecology.

The present volume serves to indicate the wideness of that field and the fruitfulness of the union at an ecological level between plant and animal biology.

Dr Dempster’s contribution on the Cinnabar moth and its food plant, ragwort, reviews more than a decade’s work and underlines the extent to which these two organisms have evolved together. One result of this is that the moth, while wholly dependent on the food-plant, makes virtually no impact on the density of the latter.

Dr Spence’s review, covering an even longer time-span, uses a wealth of examples to demonstrate the complexity of the interaction between physical factors and the epiphytic plant communities in lakes. The framework which he constructs will surely enlighten not only botanical limnologists but all who have observed zonation phenomena in lakes and their influence on the fauna and on lake processes.

Dr Arthur takes us into the rapidly developing and sometimes controversial field in which ecology, genetics and evolutionary studies overlap. He draws examples from a range of plants and animals and, needless to say, goes a long way beyond the classical ecological approach to competition in which the members of a population are deemed to differ only in age and sex.

Finally, Dr Naveh reviews a field which has been for too long neglected by Anglo-Saxon readers, namely Landschaftsokologie (Landscape ecology) as understood by workers in Central Europe and, to some extent, in the Netherlands. His article extends that of Young in Volume 8 and links many of the ideas of theoretical ecology with studies relevant to land use and its cultural implications. The approach will be new to many who do not read the German language literature.

Present conditions do not favour the production of articles such as we

... Vll l PREFACE

publish in this series but the need for a medium by which the thoughts and activities of workers across the whole spectrum of ecology are exchanged becomes more important as primary research is starved of time and resources. This is borne out by the support which our readers give to the series and the healthy list which has accumulated for the forthcoming volumes. As a result we intend to publish, from now onwards, an increasing range of articles more regularly and more frequently.

October 1981 AMYAN MACFADYEN DAVID FORD

Contents

Contributors to Volume 12 . . . . . . . . . v Preface . . . . . . . . . . . . . vii

The Ecology of the Cinnabar Moth, T'riajacobaeae L. (Lepidoptera: Arctiidae)

J. P. DEMPSTER

I. Introduction . . . . . . . . . . . . 1 11. General Biology of the Moth . . . . . . , I

111. The Moth's Food Plant . . . . . . . . . . 4 IV. Natural Enemies of the Moth. . . . . . . 7

A. Predators . . . . . . . . . . 7 B. Parasitoids. . . . . . . . . . 11 C. Disease Organisms . . . . . . . . . 13

V. Food Quality and Quantity . . . . . . . . 14 VI. Dispersion and Dispersal of the Moth . . . . . . . 18

VIII. Concluding Remarks . . . . . . . . . 32 Acknowledgements . . . . . . . . 34 References . . . . . . . . . . . 34

VII. Population Ecology of the Moth . . . . . 24

The Zonation of Plants in Freshwater Lakes

D. H. N. SPENCE

I. Introduction . . . . . . . . . . . . 37 A. Aquatic Vegetation . . . . . . . . . . 38 B. The Groups of Plants, and Overall Depth Distribution . . . 38 C. Habitat and Zonation Variables Distinguished . . . . 44

11. Habitat Variables . . . . . . . . . . . 4 9 A. Vertical Environmental Variables . . . . . . . 4 9 B. Vertical and Horizontal Environmental Variables; Turbulent and

Molecular Motion in the Littoral . . . . . . . 60 C. Conclusions; Effects on Sediment and Plant Distribution . . . 70

. 71 A. Vertical Zonation . . . . . . . . 7 1 B. Vertical and Horizontal Components of Zonation . . . . 80 C. Sediments and Plant Responses . . . . . . . . 86

111. Causal Analysis of Within-lake Distribution at any Instant of Time

IV. Causal Analysis of changes of Within-lake Distribution with Time; Depositional Shores and the Hydrosere . . . . . . . 9 2

V. Plant Adaptations . . . . . . . . . . 9 5 A. Flow, Substrate and Plant Distribution . . . . . 9 5

X CONTENTS

B. Photomorphogenesis, Photosynthesis and Zonation . . . . 97

by Substrate or by Light . . . . . . . 108 A. Competition with Microalgae and Extent of zc . . . 108 B. The Macrophyte Biomass/Depth Curve; some Implications . . 110

C. Growth Forms, Plant Strategies and Interspecific Competition . . 103 VI. Competition with Microalgae and the Control of Macrophyte Zonation

VII. Concluding Hypothesis: when Substrate or Light controls the Distri- bution of Macrophytes in Lakes . .

Acknowledgements . . . . . . . . References . . . . . Notes . . . . Appendix: List of Symbols . . .

The Evolutionary Consequences of Interspecific Competition

WALLACE ARTHUR

I . Introduction . . . . 11. Proposed Patterns of Competitively-induced Evolution .

A. Character Displacement . . . . B. Character Convergence. . C. Character Release . D. Evolution of Competitive Ability. . E. Genetic Feedback. . . . F. Effects of Competition on Polymorphic Loci . .

A. Introduction. . . . . . . B. The Models . . . .

IV. Criteria for Demonstrating ComDetitive Selection .

111. Some Coevolutionary Models . . . . . .

112 , 114

1 I5 . 124 , 124

, 127 . 129 . 129 . 131 . 131 . 132 . 133 , 134 . 136 , 136 . 131

145 A. Criteria for Conclusive Demonstration of Character Displacement

B. Criteria for Conclusive Demonstration of the Evolution of Inter- in Natural Populations . . . . . . 145

specific Competitive Ability in Experimental Populations . . . 149 V. The Evidence . . . . . . . 150

A. Changes in the Mean of Quantitative Characters. . . 150 B. Changes in the Variance of Quantitative Characters . . 173 C. Changes in Heterozygosity and Gene-frequency . . . 174

VI. Conclusions . , 181 Acknowledgements . . . . . . . 182 References . . . , 182

Landscape Ecology as an Emerging Branch of Human Ecosystem Science

ZEV NAVEH

I . Introduction . . 189 11. The Conceptual and Theoretical Basis of Landscape Ecology . . . 190

A. Some Definitions of Landscape and Landscape Ecology . , 190 B. Some Relevant Conceptual and Methodological Contributions . . 193

CONTENTS xi

C. Towards a General Biosystems Theory. . . . . . 197

111. Practical Contributions of Landscape Ecology . . . . . 210 A. Major Contributions in Central Europe . . 210 B. Landscape Ecological Studies in Israel . . . . . . 222

V. Summary and Conclusions . . . . . . . . 2 2 9

D. The Role of Landscape Ecology as a Human Ecosystem Science. . 204

IV. Landscape Ecology and Environmental Education . . . . 228

Acknowledgements . . . . . . . . . . 230 References . . . . . . . . . 230

Author Index . . . . . . . 239 Subject Index . . . . . . . . . . 245 Cumulative List of Titles . . . . . . . 251

The Ecology of the Cinnabar Moth, Tyria jacobaeae L. (Lepidoptera: Arctiidae)

J. P. DEMPSTER

I. Introduction . . . . . . . . . . . . . . . 1 11. General Biology of the Moth . . . . . . . . . . . 1

111. The Moth’s Food Plant . . . . . . . . . . . . 4 IV. Natural Enemies of the Moth . . . . . . . . . . . 7

A. Predators . . . . . . . . . . . . . . . 7 B. Parasitoids. . . . . . . . . . . . . . . 1 1 C. Disease Organisms. . . . . . . . . . . . . 13

V. Food Quality and Quantity . . . . . . . . . . . 14

VIII. Concluding Remarks . . . . . . . . . . . . . 32 Acknowledgements . . . . . . . . . . . . . . . 34 References . . . . . . . . . . . . . . . . . 34

VI. Dispersion and Dispersal of the Moth . . . . . . . . . 18 VII. Population Ecology of the Moth . . . . . . . . . . 24

I. INTRODUCTION

The cinnabar moth has attracted the attention of research biologists for the past 50 years, because of its conspicuous, warning coloration, its distastefulness to vertebrate predators, and the spectacular defoliation which its caterpillars periodically cause to its food plant, ragwort (Senecio jacobaea L.). Study of the moth has also been greatly stimulated by attempts to use it for biological control of ragwort, a poisonous weed of pasture, which has been accidentally introduced by man to many parts of the world. As a result, few insects have been studied more extensively than this moth.

11. GENERAL BIOLOGY OF THE MOTH

The cinnabar moth occurs naturally throughout Europe, except for the extreme north, and in the east its distribution extends into Asia. It is univoltine

2 I. P. DEMPSTER

throughout its range, with an obligatory diapause in the pupal stage. The adult moths emerge in late spring from the overwintering pupae and lay their eggs in clusters on the underside of the basal leaves of the food plant, ragwort (Senecio jacobaea L.). The moth has also been recorded laying on groundsel, Senecio vulgaris L. (Aplin and Rothschild, 1972). The moths are frequently active by day, but have peaks in flight activity around dusk and dawn (Fig. 1). Although it is not a strong flier, the cinnabar moth is capable of considerable dispersal (van der Meijden, 1979); individual moths having been taken at lightships up to 30 miles from the coast (Williams et al., 1942). The males are attracted to light, but the females are not.

14-

13-

12-

11-

p 10-

5 9- (D

suntet I

I I

I

I ,

00 01 02 03 04 05 06 07 08 09 10 11 12 13 14 I5 16 17 18 19 2 0 21 22 23 24

time of day

Fig. 1. Diurnal activity of the cinnabar moth. These data are based on 354 records of flight on film with a 5 min time-lapse exposure of 18 moths in cages over a period of 4 days. (See Dempster 1971a for details.)

Mating occurs soon after emergence, normally around sunrise. Males are attracted to virgin females, but mated females are unattractive, so that most are mated only once (Rose, 1978). Females live for 2-3 weeks under normal field conditions, with larger individuals tending to live longer than small ones (Dempster, 1971a). In the laboratory, unmated females usually live longer than fertilized females, and they frequently lay a few infertile eggs in the last 2-3 days of their life (Rose, 1978).

The number of eggs laid per female varies considerably between years and

THE ECOLOGY OF THE CINNABAR MOTH 3

populations. Up to 600 eggs per female have been obtained in the laboratory, but this is rarely approached in the field. During nine years at Weeting Heath, Norfolk, the mean fecundity ranged from 73-295 eggs per female (Dempster, 1975). This large variation was brought about by variations in adult size, which resulted from differences in the availability of food for the caterpillars in different years. As with many insects, fecundity is closely related to size of female (Dempster, 1971a; van der Meijden, 1976).

Up to 150 eggs may be laid in a cluster, but more usually the number is between 30 and 40. The mean number per cluster varies between years and populations; at Weeting Heath it has ranged from 19.243.1 over 10 years (Dempster, unpublished data), whilst Myers and Campbell (1976b) record similar differences between localities in the same year (256-58.1). Egg batch size tends to decrease with age of female, so that the first laid egg batches are the biggest (Rose, 1978). Also, larger adults lay on average more eggs per batch ( I = 0.3790, d.f. 26, P -= 0.05) (Dempster, unpublished data).

The eggs are bright yellow when laid, but just prior to hatching, they become greyish, and the black head of the developing larva can be seen through the shell. Hatching takes place after 4-20 days depending on temperature (Rose, 1978), usually about two weeks in the field. The young caterpillars are grey-green in colour when they hatch and they stay together during the first instar, feeding on the leaf on which they hatched. Unlike many Lepidoptera, they do not eat their eggshells, and these may remain on the plant for several weeks after hatching. After the first moult, the larvae start to develop their characteristic black and orange banding. As they grow, they tend to move to the top of the plants and feed on the developing flower buds. With increasing age, the distribution of the larvae becomes more spaced out, there being a considerable amount of movement between plants. This occurs even when the plants are not defoliated, although the rate of movement increases when plants become badly damaged (van der Meijden, 1976). There are five larval instars and the total larval period takes about a month in the field. Each moult may take up to one day and larvae frequently leave the ragwort plant on which they have been feeding to moult on surrounding vegetation, particularly when densities are high.

The first stage larva weighs about 0 . 2 4 3 mg on hatching whilst the fully grown larva must weigh a minimum of 140-150 mg to pupate successfully (Dempster, 1971a; van der Meijden, 1976). Over half of the final weight (usually about 250 mg) is put on during the last larval stage, and this stage lasts about twice as long as the previous stages, which are of about equal duration.

When fully grown the caterpillars leave their food plant to pupate in the superficial layers of the soil, often under a small stone, or amongst moss or grass roots. The fully grown larvae are capable of dispersal of several hundred

4 J . P. DEMPSTER

yards, and this is particularly common when food is in short supply (see p. 23). An obligatory pupal diapause ensures that adults do not emerge until the following spring. Philogene (1975) showed that this diapause is unaffected by the temperature and photoperiod experienced by the developing larva. When introducing the moth to Australia for biological control of ragwort, attempts to break the pupal diapause, so as to synchronize the moth's life cycle with conditions in the southern hemisphere, led to a reduced fecundity amongst the emerging moths (Bornemissza, 1961, 1966).

Pupae can gain or lose water at any time during their development. If pupae are exposed to dry air, they lose water rapidly, but this can be replaced if they are wetted. They can lose up to about a third of their weight from desiccation before they die, but over-moist conditions soon lead to death (Dempster, 1971a). This susceptibility of the moth's pupae to wet conditions results in the moth being restricted to well-drained soils in Britain (Dempster, loc. cit.). Van der Meijden (1974) failed, however, to find such a relationship in the distribution of the moth in Holland. On the other hand, failures of introduced populations of cinnabar have been noted in over-wet localities in California (Frick and Holloway, 1964; Hawkes, 1973) and Australia (Borne- missza, 1966).

111. THE MOTH'S FOOD PLANT

Ragwort, Senecio jacobaea L. (Compositae), is a native of Europe from 62'30" in Norway to as far south as Asia Minor. In the east, its distribution extends into Siberia (Harper and Wood, 1957; Harper, 1958). The plant has, however, been introduced by man into Canada, the USA, Argentina, South Africa, Australia and New Zealand (see p. 6). It is essentially a plant of well-drained soils, of medium to high pH (Cameron, 1935; van der Meijden, 1974).

Ragwort is usually a biennial, which passes the first year as a rosette, flowers in its second year and then dies. Occasional plants may be annuals, flowering and dying in one year, or they may behave as perennials, particularly if they are damaged and prevented from flowering. Schmidl (1972) records the fate of 176 plants in Victoria, Australia, as 3 annuals, 1 1 1 biennials, 46 perennials and 16 which died without flowering. Van der Meijden and van der Waals-Kooi (1979) have shown that the size of a plant, rather than its age, determines whether or not it flowers and it seems likely that plants can stay as rosettes for several years until they have reached a size which enables them to flower.

The majority of seed germinates in autumn, but some germination may


be delayed until the following spring. Seed is dispersed by wind, but most fertile seed falls within 10 m of the parent plant (Poole and Cairns, 1940). Seed may also be dispersed by water. The seed can retain its viability for eight or more years within the soil, but a covering of 1 cm of soil is sufficient to prevent germination (Cameron, 1935; van der Meijden and van der Waals- Kooi, 1979). The young seedling requires a disturbed soil surface for establishment, and recruitment is greatly reduced in long grass, or in a closed sward. Only a small proportion of seedlings and young plants survive, depending upon plant competition and shading, soil type, climate, etc. (Schmidl, 1972). Van der Meijden (1971) estimated that over 98% of the seed produced in a Dutch dune area failed to germinate. He also found that drought and frost led to very high mortality of seedlings. Forbes (1977) has published similar data for one year for a ragwort population in Scotland. He estimated that under 1% of the seed produced actually germinated, and that a minimum of 57% of all germinating plants died as seedlings. Dempster and Lakhani (1979) showed that the changes in the numbers of ragwort plants at Weeting Heath, England, were almost totally dependent upon summer rainfall (July- September). During their 9-year study, summer rainfall accounted for 95.8% of the observed variation in the annual change in the logarithms of plant numbers.

Ragwort plants vary considerably in size, depending upon soil type and climate. On a poor sandy soil, such as that at Weeting Heath (Dempster, 1971a), where rainfall is limiting, plants will normally produce only a single flower stalk of about 20-30 cm in height. On richer soils, receiving adequate rainfall a single plant may produce a dozen stems and grow up to 180 cm (Schmidl, 1972). For this reason, there are huge variations in the number of seeds produced per plant in different localities (1000-250 OOO seeds/plant; Cameron, 1935; Harper and Wood, 1957; Schmidl, 1972; van der Meijden and van der Waals-Kooi, 1979).

Ragwort has enormous powers of regeneration, if it is damaged. Although it is usually a biennial, it frequently becomes perennial if it is cut, or defoliated, and prevented from flowering. Regeneration may take one of two forms. If the plant is large and has ample food reserves, regrowth occurs from the crown of the plant. Secondary flower shoots are then produced in late summer, but seed production is usually less than from undamaged plants. Again there appears to be considerable variation in the effect of cutting, or defoliation, on seed production. For example, Cameron (1935) estimated a 65% reduction in seed production by damaged plants compared with undamaged ones, whilst Bornemissza (1966) estimated a 98% reduction. The effects of defoliation probably depend heavily upon climatic factors and the speed with which the plant can recover. Stimac and Isaacson (1978) report that secondary flower shoots can be produced within two weeks of defoliation in Oregon,

6 J. P. DEMPSTER

USA, whereas Wilkinson et al. (1970) consider that secondary flowering is unlikely in Nova Scotia because the growing season is so short.

Besides this regrowth from the crowns of damaged plants, regeneration may also occur from root buds. This type of regeneration is particularly vigorous from the young roots of rosette plants (Poole and Cairns, 1940), but roots of flowering plants can also regenerate this way. The young plants resulting from root buds are not easily distinguishable from seedlings, since their connection with the parent root-fragment may soon be lost. As with secondary flowering, the extent of regeneration from root buds is dependent upon the weather. With adequate warmth and rainfall, the number of plants may increase markedly as a result of regeneration (Dempster, 1971a). How- ever, the data presented by Dempster and Lakhani (1979) show that at Weeting Heath, England, it made little difference whether new plants were produced mainly from seed or from root buds, changes in the number of ragwort plants from one year to the next depended upon the amount of summer/autumn rainfall. In other words, defoliation had a negligible effect on plant numbers in the following year. In contrast, Harris et al. (1978) showed that defoliation led to a decline in plant numbers in the Canadian Maritimes, because regenerating rosettes were killed by frosts soon after the start of regrowth. They showed that plants required a minimum of 70 days to build up their carbohydrate reserves, if they were to survive winter temperatures.

Ragwort is toxic to cattle and horses, causing cirrhosis of the liver. The disease symptoms are known as “Pictou disease” in Canada, “Winton disease” in New Zealand, “Sirasyke” in Norway and “Molten0 disease” in South Africa. This toxicity, combined with the plant’s powers of regeneration, makes it a serious weed of pasture in many parts of the world. The plant’s toxicity is due to the presence of at least six alkaloids, jacobine, jacozine, jacoline, senecionine, seneciphylline and integerrimine (Leonard, 1950, 1960; Warren, 1970). The total alkaloid content of the plant changes during the growing season and reaches a peak in June and July. Different populations of the plant differ in their alkaloid content. The importance of the individual alkaloids also varies seasonally, with seneciphylline and jacozine making up a high proportion of the alkaloid content during summer, and jacobine being particularly important during winter and spring (Aplin and Rothschild, 1972). The toxic alkaloids are not lost on drying, and deaths of cattle and horses may result from them eating hay or silage containing ragwort. Sheep appear to be far more resistant to the plant and they eat it readily. The introduction of sheep into infected pasture is often recommended as a means of controlling the weed, although the efficacy of this is doubtful (see p. 33).


IV. NATURAL ENEMIES OF THE MOTH

A. Predators

The caterpillars, pupae and adults of cinnabar moth are distasteful to a wide range of vertebrate predators (Windecker, 1939). The moth's caterpillars ingest and store poisonous alkaloids from their food plant (Aplin et al., 1968; Aplin and Rothschild, 1972). These alkaloids are absent from the eggs of cinnabar, but they are stored by the larvae, so that they may be present in a far higher concentration than in the food plant. All six plant alkaloids have been recorded in cinnabar pupae, together with a metabolite (Aplin and Rothschild, 1972), but the relative concentrations of the individual alkaloids are different from those in the plant, suggesting a selective absorption and/or storage by the moth.

When disturbed the adult moth ejects a pungent secretion from its pro- thoracic glands. A further metabolite of the alkaloids, not found in the plant, is present in this defensive secretion (Aplin et al., 1968).

It is difficult to assess the role of these ingested alkaloids in the insect's defence. Windecker (1939) showed that the repellent qualities reside in the larval skin and in the haemolymph of the pupa and adult. He also showed that there is a latent period lasting about eight weeks after pupation, when the pupa is readily eaten by the same range of vertebrate predators which reject the moth earlier and later in its life cycle. Dempster (1971a) recorded a heavy mortality during the first few weeks of pupal life at Weeting Heath, which was almost certainly due to predation by vertebrates, in this case, moles (Tulpa europaea L.). Since alkaloids cannot be ingested after the fully grown larva has stopped feeding, it seems unlikely that they are the active repellent, at least in older pupae and adults. Nevertheless, as Aplin and Rothschild (1972) point out, the fact that the aposematic cinnabar stores Senecio alkaloids, whereas two cryptic species of moth fed on Senecio vulgaris do not (Spodoptera littoralis (Boisduval) and Melanchra persicariae L.) suggests that these substances play some part in the cinnabar's defence mechanisms.

Besides storing poisonous alkaloids from its food plant, the cinnabar moth also manufactures some toxic substances itself. Very high levels of histamine (750 pg g- ' freeze-dried body tissue) have been demonstrated in the adult moth (Bisset et al., 1960; Frazer and Rothschild, 1962), a substance frequently associated with poison glands of invertebrates. Histamine is a far more rapid poison than are the alkaloids and is therefore more likely to deter a predator before it has killed and eaten the moth. Obviously, far more research needs

8 J . P. DEMPSTER

to be done to sort out the roles of the various toxins present in the cinnabar moth.

Besides being distasteful, the cinnabar moth is warningly coloured. The adult moth has a brilliant red and black coloration, whilst the caterpillar has black and yellow stripes. When feeding amongst ragwort flowerheads, the caterpillars are surprisingly cryptic from a distance, at least to the human eye (Rothschild, 1975), but at close quarters and on foliage they are strongly aposematic. If disturbed, the caterpillars display a lateral “flicking” movement in which the anterior part of the body is jerked from side to side. When several larvae are present on one plant, they will often “flick” in unison in an agitated fashion (Bornemissza, 1966; Myers and Campbell, 1976~). Further disturbance usually leads to the larvae dropping from the plant.

In spite of the defence mechanisms of the cinnabar moth, a small number of vertebrate predators will feed on the caterpillars and adults. Those recorded tend to be species which specialize in distasteful prey, for example, the Euro- pean cuckoo (Cuculus canorus L.). However, these probably make very little impact upon populations of the moth. Of far more importance is the predation by vertebrates on the newly developed pupae. Dempster (1971a, 1975) estimated that between 51-960/, of fully grown larvae leaving ragwort to pupate were killed in the first 6 8 weeks of pupal life. This mortality was attributed mainly to moles and is possibly abnormally high at Weeting Heath, because of the tendency for cinnabar larvae to enter the ground through the soft disturbed soil on the sides of superficial mole runs.

The available evidence suggests that, apart from this susceptible period immediately after pupation, the effects of vertebrate predators on moth populations within its natural distribution are insignificant. Populations of the moth, introduced to other parts of the world to control ragwort, have however, sometimes been heavily attacked by vertebrate predators. Thus, Miller (1970) records adults and larvae being taken in large numbers by the native cuckoo (Chrysococcyx lucidus Vieillot) in New Zealand. He also recorded the house sparrow (Passer domesticus L.) and starling (Sturnus oulgaris L.) feeding on the moth. Bornemissza (1 966) says that no insectivorous birds or lizards fed on the early introductions of the moth to Australia, but Schmidl(l972) reported that the fan-tailed brush cuckoo (Cacomantis pyrrhophanus Gmelin) was seen preying on larvae. I think that instances such as these are likely to be important only during the initial period of establishment of the moth, when small populations can be eliminated by the odd individual predators concentrating on them.

Compared with vertebrate predators, predacious invertebrates are far more important. These do not appear to be deterred by the moth’s distastefulness, nor by its warning coloration. Many are nocturnal and so presumably do not hunt by sight. Very many species have been recorded feeding on cinnabar


eggs, larvae, pupae and adults, but those feeding on the newly hatched larvae probably have the biggest impact. These include mites, phalangids, spiders and ground beetles (Carabidae). All are polyphagous, taking many types of prey besides cinnabar moth.

In general, the predatory fauna depends upon the type of vegetation in which the ragwort plants are growing. Dempster (1971b) studied the arthropod predators of cinnabar moth serologically and identified nine species which had fed on the moth at Weeting Heath. Of these, by far the most important was a mite, Erythraeus phalangoides de Geer. Variation between years in the mortality attributed to arthropod predators was correlated with changes in the numbers of this mite (Dempster and Lakhani, 1979). The vegetation at Weeting Heath is heavily overgrazed by rabbits (Oryctolagus cuniculus (L.)), is dominated by lichens and fine grasses, and supports a poor arthropod fauna. In contrast, a study of a population of the moth at Monks Wood identified 30 species of arthropod feeding on cinnabar (Dempster, 1971b). Here the ragwort was growing at the base of a hedge, amongst tall, dense herbaceous vegetation. In this situation, mortality from arthropod predators was estimated as 87.8, 88.8 and 82.7% over three years, compared with estimates ranging from 28649.1% (mean 56.9%) over a nine-year period at Weeting Heath. Another population of the moth in a lightly grazed field (Monks Wood, East Field) had intermediate numbers of predators and mortality attributed to predation.

Since most of the predatory arthropods recorded feeding on cinnabar moth are polyphagous, the presence of one particular predator does not necessarily mean that it will be taking the moth. This will depend upon what alternative prey are present. Thus, van der Meijden (1973) has shown that cinnabar larvae are heavily preyed upon by the ant, Lasius alienus Forst., on the sand dunes of Wassenaar (The Netherlands). This same species of ant is present in large numbers at Weeting Heath, but many hours observation of the foraging activity of Lasius recorded only a single cinnabar larva taken. Added to this, serological tests of over 100 L. alienus failed to give a single positive reaction to anti-cinnabar serum (Dempster, 1971a). The different behaviour of the ants in the two localities may possibly be explained by a greater availability of other sources of protein at Weeting Heath.

A similar range of egg-predators has been recorded from Britain (Dempster, 1971a) and from the USA (Hawkes, 1973; Isaacson, 1973). These include omnivorous species, such as woodlice (Armadillidium oulgare Latreille, Por- cellio scaber Latreille, Philoscia muscorum (Scopoli)) and earwigs (ForJcula auricularia L.) as well as true predators (e.g. Anthocoris nemorum (L.), Nabis rugosus (L.) (Hemiptera, Heteroptera) and Bembidion lampros (Herbst) (Cole- optera, Carabidae)). Bornemissza (1966) recorded a pentatomid bug (Chaero- coris paganus Fabr.) taking eggs in Australia, whilst Harris et al. (1975)

10 J. P. DEMPSTER

estimated that a 46% egg loss was due to predation by cantharid beetles in Canada. The cantharid, Rhagonycha, was shown to take young larvae of cinnabar in Britain (Dempster, 1971a).

Most authors agree that egg predation is normally low compared with that on the very young larvae of cinnabar moth. Mortalities of between 5040% are commonly recorded between hatching and the end of the second instar (see p. 24) and this is likely to be mainly due to arthropod predators. It is very difficult to obtain estimates of the effects of predators on any insect population because individuals which are taken are usually lost without trace. However, Dempster (1971a) was able to find a predator which gave a positive reaction with anti-cinnabar serum on just over 60% of the occasions when larvae were missing from plants, during a three-year intensive study. This was achieved by daily searches and there is little doubt that the percentage would have been even higher, if the searches had been made more frequently, since many of the predators were nocturnal.

During the first instar the caterpillars are clustered together on the underside of the leaf on which they hatched. When attacked by a predator they react by dropping from the leaf on silk threads. In each of the three years of Dempster’s more intensive study at Monks Wood, there was a significant positive correlation between survival during the first instar and the number in the cluster. This, he suggested, was due to a higher proportion escaping attacks by predators when they occurred in large clusters. Other advantages of clustering have, however, been suggested by other authors (see p. 21).

As the caterpillars grow, they become immune from attack by all but the largest arthropods, or those, such as ants, which attack a prey in large numbers. Mortality from arthropod predation therefore tends to be lower during the third to fifth instars. In some circumstances, however, arthropods can still cause high mortalities. Van der Meijden (1971, 1973) showed that the ants, Formica polyctena Forst. and Lasius alienus Forst., caused such high mortalities of larvae that the moth was absent from plants near the ants’ nests. By putting out marked caterpillars, he showed that these ants readily took fully grown larvae. Myers and Campbell (1976a) recorded a similar heavy predation by carpenter ants (Camponotus sp.) on an introduced population of the moth in Canada. Bornemissza (1966) found that a large scorpion fly, Harpobittacus nigriceps (Selys) (Mecoptera), switched from its normal prey of tipulid flies to attack an introduced population of cinnabar larvae in Victoria, Australia, with such an effect that this, combined with a viral disease, led to extinction of the moth. Again, this species was capable of taking fully grown larvae. Failure of an earlier introduction of the moth to Victoria was also attributed to the action of this predator (Currie and Fyfe, 1938).

Once the fully grown larvae leave the plants to pupate they become avail-

THE ECOLOGY OF THE CINNABAR MOTH 1 1

able to other ground-living, arthropod predators. This is also true when younger larvae move between plants. Wilkinson (1965) attributed the failure of introduced cinnabar moths to establish a population at Abbotsford, British Columbia, to predation of newly formed pupae by the ground-beetles (Carabidae), Feronia (Pterostichus) melanuria (Illiger) and Calathus fuscipes Goeze.

Arthropod predators occasionally take adult moths, e.g. the crab spider, Xysticus cristatus Clerck (Dempster, 1971a), but this is normally so infrequent as to be insignificant in population terms.

In spite of its defence mechanisms, the cinnabar moth is attacked by a wide range of predators. All stages may be attacked, but the moth is particularly susceptible as an early larva and at the time of pupation. Very heavy mortalities can be caused at these times. All of the predators so far recorded are polyphagous, feeding on a wide range of prey, and from the limited data so far available, mortality caused by them is unrelated to the moth’s density.

B. Parasitoids

The eggs of cinnabar moth are large and exposed, but surprisingly, they do not appear to be normally attacked by insect parasitoids. Harris et al. (1975) record a species of Telenomus attacking the eggs of an introduced population of the moth in Nova Scotia, Canada, but this is the only record that I am aware of, in spite of many thousands of eggs which must have been observed during studies of the moth. In contrast, the moth’s larvae and pupae may be attacked by a large number of species.

Introduced populations of the moth are usually established without their normal parasitoids, since these are screened out before release. Even so, insect parasitoids can cause high mortalities in introduced populations of the moth. These are presumably all non-specific parasitoids which have moved on to cinnabar moth from other prey species. Thus, Miller (1970) records up to 78% parasitism by the tachinid fly, Cerosomyia casta Hutt., in New Zealand. He also records the pupae being attacked by an ichneumonid, Echthromorpha intricatoria F. A low percentage parasitism by tachinids and ichneumonids was reported in Australia (Bornemissza, 1966) and the USA (Hawkes, 1973; Isaacson, 1973).

In Europe, the caterpillars of the cinnabar moth are attacked by a specific braconid parasitoid, Apanteles popularis Hal. (Daviault, 1929; Cameron, 1935; Dempster, 1971a). This small wasp lays its eggs in the first or second stage

12 J . P. DEMPSTER

caterpillars. Up to 15 larvae can develop in a single caterpillar, but the number is usually five or six. These kill the host in its fifth instar, usually when the latter is fully grown. After leaving their host, Apunteles larvae spin up in cocoons and hibernate until the following spring. They pupate shortly before emerging as adults in May or early June, thus having a single generation each year. Apanteles is itself frequently attacked by a hyperparasitoid, Meso- chorus facialis Bridg. (Ichneumonidae).

v v V v v

A z 1.0 J , 1

1966 67 68 69 70 71 72 73 74

Fig. 2. Showing the relationship between the number of fully grown Apanteles larvae emerging each year and the number of their hosts available at the time of egg-laying by Apanteles. The arrows indicate years when cinnabar larvae ran out of food, and the figures in parenthesis show the mean number of Apanteles larvae per parasitized host.

The relationship between the numbers of Apanteles emerging from cinnabar and the numbers of its host at Weeting Heath is shown in Fig. 2. It must be remembered that some of these Apanteles larvae will themselves be parasitized by Mesochorus. The number of Apanteles leaving their hosts broadly followed the number of hosts available to them between 1966-1974, but it was depressed in years when the cinnabar caterpillars defoliated their food plant. In those years, shortage of food led to the death of many Apanteles, whose hosts died of starvation before completion of their development, and to a reduction in the mean number of Apunteles emerging per host, as host size was reduced. The latter was particularly marked in the years when food ran out earliest (i.e. 1968 and 1973).

THE ECOLOGY OF T H E CINNABAR MOTH 13

The percentage of fifth stage caterpillars killed by Apanteles varied from 5.2-35.7% at Weeting Heath between 1966-1974 (Dempster, 1975). The percentage attacked appeared to be inversely related to the density of the moth during the first five years of this study, but after that, Apanteles killed a low percentage which did not respond to changes in cinnabar numbers (Dempster and Lakhani, 1979). The impact of Apanteles is discussed further on p. 33.

Cameron (1935) records a number of other parasitoids which have been reared from cinnabar moth pupae. Ichneumon (Melanichneurnon) perscrutator Wsm. was found in 2-15% of pupae collected in Norfolk, England, whilst P sychophayus omniuorus Walker (Pteromalidae) occurred in 3 4 % of these pupae. During regular sampling of pupae at Weeting Heath, I found only a single pupa (1.0%) parasitized by P. omniuorus in 1970 and five (7.9%) in 1974. None was found in the other seven years. Either this species must occur at very low densities in most years, or it must be dependent upon other species of prey. As with all of the other parasitoids recorded from cinnabar moth, with the exception of Apanteles popularis, P . omnivorus is polyphagous, attacking the pupae of many Lepidoptera.

C. Disease Organisms

A number of diseases has been isolated from cinnabar moth and high mortalities have been reported. However, it is difficult to assess the incidence of disease in field populations, because studies have invariably involved laboratory rearing of field-caught individuals and this is likely to have increased the incidence of infection. However, although quantitative data are of uncertain reliability, there is no doubt that field mortalities from disease can be high. For example, a virus epizootic virtually eliminated an introduced population over a period of five days in Australia, under a climatic stress of high temperatures (over 35°C) and high relative humidities (Bornemissza, 1966).

Although parasitoids were excluded when using cinnabar moth for biological control of ragwort, few of the earliest introductions attempted to use disease-free stock. Much of the evidence of outbreaks of disease in populations of the moth come from these early introductions and it is likely that release of diseased individuals into a new environment may have produced ideal conditions for the disease to spread, since the moth may have been stressed by the unusual environmental conditions it encountered.

Microsporidial, viral and fungal diseases have been identified in cinnabar populations. Viruses and microsporidians are particularly troublesome when rearing the moth, since they can be passed from one generation to the next through the egg.

14 J. P. DEMPSTER

The microsporidian belongs to the genus Nosema (Bucher and Harris, 1961). This develops in the fat body, midgut epithelium, silk glands and Malpighian tubules of larvae. The disease progresses slowly, but most infected larvae die before pupation. It can also cause high mortalities in the pupal stage, however. As the gut epithelium becomes infected, the disease probably spreads through contamination of the food with infected faeces. The early introductions of the moth to California, USA, appear to have carried this disease (Hawkes, 1973).

Two viral diseases have been reported in the literature, a nuclear polyhedrosis (Steinhaus and Marsh, 1962; Bornemissza, 1966), and a cytoplasmic polyhedrosis (Bucher and Harris, 1961). The former appears to be transmitted through the egg, but the latter does not. The early introductions of the moth to Australia carried the nuclear polyhedrosis virus from Europe.

During the study of the moth at Weeting Heath (Dempster, 1971a, 1975) microsporidian and virus diseases were looked for but no evidence of their occurrence was ever found even in those years when the moth population was very high and stressed by starvation.

A number of fungi has been identified attacking cinnabar larvae and pupae, i.e. Beauueria bassiana (Bols) Vuill, Spicaria gracilis Petch, and Fusarium sp. (Cameron, 1935; Bornemissza, 1966; Dempster, 1971a). Dempster (loc. cit.) also recorded Penicillium sp. growing on larvae which died, probably from starvation, during a population crash in 1968 (see p. 25), but considered this fungus to be saprophytic. He also found Fusarium sp. developing on pupae kept in the laboratory in damp conditions, but again questioned whether this fungus was pathogenic or saprophytic. Fusarium species are rather weak parasites of insects, but Beauueria and Spicaria are far stronger pathogens.

For the reasons given above, it is very difficult to assess the importance of disease organisms in the population dynamics of the moth. The methods of studying disease in field populations are invariably unsatisfactory, and the interplay between “stress” and disease frequently imposes uncertainty as to the real cause of death. Data from natural populations in Europe suggest that epizootics are surprisingly rare. On the other hand, populations of the moth introduced to other parts of the world, appear sometimes to have taken disease organisms with them, from which epizootics can develop in the new environment to which they are exposed. There is a need for more research into the impact of disease under natural field conditions.

V. FOOD QUALITY AND QUANTITY

Most eggs of the cinnabar moth are laid on large, flowering-sized plants and the larvae feed preferentially on the developing flower buds. A number of


studies have been made comparing the performance of cinnabar larvae fed on different parts of the plant.

Van der Meijden (1976) reared larvae on leaves only and on leaves plus flowers and showed that rate of larval development, pupal size and the percentage of moths emerging from pupae, were all higher when larvae were fed on flowers. Dempster (unpublished data) did a similar experiment and showed that pupal size was not significantly greater when larvae were fed on flowers (pupal diameter, 0.513 f 0-0274 cm), than when fed on the basal leaves of second year plants (diameter, 0.500 f 0.0168 cm). These, however, were significantly bigger than pupae obtained by rearing larvae on leaves from rosette plants (diameter, 0.412 f 0.0278 cm). Rose (1978) repeated these experiments, but compared a wider range of diets. She compared the performance of caterpillars reared on leaves from first-year rosettes, leaves from second-year flowering plants, leaves from plants grown in shade, the floral parts and a mixture of all of these. She found that pupae reared on a floral diet were significantly bigger than those reared on leaves from shaded plants, though not significantly different from those reared on other diets. Adults reared on flowers emerged significantly later than those reared on other diets, but unlike van der Meijden, she showed no effect on percentage emergence, or on developmental time.

The results from these experiments are somewhat contradictory, but all workers obtained larger pupae when larvae were fed on flowers, rather than leaves, although with the numbers tested, this was not always statistically significant. This increased size is probably linked with the greater nitrogen content of the flowering stems compared with the leaves of ragwort (Table 1).

Table 1 Showing the nitrogen content of ragwort

(percentage dry weight of bulked sample of 30 plants).

Weeting Heath Monks Wood (22 June 1971) (17 June 1971)

First year rosette leaves 2.44 2.16 Second year basal leaves 1.94 2.60 Second year flowering shoots 3.20 3.30

In the field, the proportion of plants flowering varies between years. At Weeting Heath, it depends upon early summer rainfall, and it is always low in years following defoliation by cinnabar caterpillars (Dempster and Lakhani, 1979). The percentage flowering has a considerable effect on the availability of food for cinnabar moth, because flowering plants are far larger

16 J . P. DEMPSTER

Table 2 Showing variations in the amount of ragwort present at Weeting Heath

between 1966-1974.

1966 1967 1968 1969 1970 1971 1972 1973 1974

Mean no. plantslm’ 9.7 8.1 5.6 68.1 52.3 25.8 18.1 22.3 29.5 % flowering 45.5 50.6 1.8 12.3 35.2 29.8 1.7 13.9 12.5 Wt ragwort (g)/m’ 16.9 15.2 3.8 67.0 90.3 33.5 9.4 23.9 35.4 Wt ragwort (g)/larva 1.36 0.14 0.04 162.07 4.79 0.25 0.91 0.78 0.94

+ - + + Complete defoliation - + + - -

than rosettes. This can be seen from Table 2 which summarizes the plant data from Weeting Heath between 19661974 (Dempster, 1975). During that time the availability of food, measured each year at the time of cinnabar hatch, ranged from 0.04-162.07 g per larva, due partly to variations in the percentage of plants flowering.

In many years, shortage of food leads to complete defoliation of ragwort before many of the caterpillars have completed their development, and when this happens there may be a high mortality from starvation. Dempster (1975) showed that starvation was a key factor determining fluctuations in population size of the moth at Weeting Heath (see p. 25).

Besides causing high mortalities, starvation also leads to a reduced size of those individuals which survive to pupation. At Weeting Heath, mean pupal width has ranged from 0.4254527 cm between 19661974 (Table 3). The

Table 3 Factors affecting egg batch and plant size at Weeting Heath.

Complete Mean no. Mean biomass/ Mean eggs/ Mean pupal defoliation eggs/batch plant batch per width (cm)

(wet wt g) unit plant in previous biomass generation

~ ~~ ~~ ~~ ~~

1966 - 26.8 1.7 15.8 -

1967 + 43.1 1.9 22.7 0.5 12 1968 + 27.7 0.7 39.6 0.454 1969 - 31.0 1 .o 31.0 0.425 1970 - 33.3 1.7 19.6 0.51 1 1971 + 38.5 1.3 29.6 0.527 1972 - 20.1 0.5 40.2 0.445 1973 + 23.4 1.1 21.3 0.496 1974 + 20.4 1.2 17.0 0.4 5 5 1977 - 19.2 1.7 11.3 -


size of the resulting adult is closely correlated with pupal size (r = 08280, P c 0.001: Dempster, 1971a) and this has a marked effect on length of adult life and on fecundity (Dempster, loc. cit.; van der Meijden, 1976). Figure 3 shows the relationship between pupal size and fecundity. Because of this relationship, starvation leads to a delayed density-dependent reduction in the number of eggs laid (see p. 27).

600

400

. .

Fig. 3. Showing the number of eggs laid in the laboratory by females from different sized pupae. (0 Dempster, 1971a; o van der Meijden, 1976.)

The effects of food shortage are further complicated by the reaction of the ragwort plants to defoliation. Although this probably has little effect on the number of plants (see p. 6), the size of plants, and hence the biomass of food available to the next generation of the moth, is usually greatly reduced in the year following defoliation.

Short periods of starvation are not readily made good. Dempster (1971a) showed that if first instar larvae were starved for three days, the resulting pupae were reduced in size even when excess food was available for the rest of their development. Van der Meijden (1976) found that the same was true if fifth stage caterpillars were starved for a few days.

18 J. P. DEMPSTER

VI. DISPERSION AND DISPERSAL OF THE MOTH

The cinnabar moth lays its eggs in clusters and the newly emerged caterpillars do not disperse, but stay together in a compact mass, often heaped on top of one another. If these first stage larvae are separated from each other, they reform into dense aggregations again within a few hours (Bornemissza, 1966). After the first moult, the larvae move from the basal leaves to the top of the plant, where they feed on the developing flower buds. As they grow, their gregarious behaviour is gradually lost, so that by the fifth instar there is a positive agonistic response by one individual to the presence of another, and a marked spacing out of the larvae. Van der Meijden (1976) attempted to study this change in the pattern of dispersion during larval growth quantitatively by calculating Lloyd’s (1967) mean crowding, h, for each instar (i.e. the mean number of individuals per individual per surface unit). Un- fortunately, one cannot separate the effects on mean crowding of movement from those of mortality, but van der Meijden did show a rapid drop in dl per leaf, which coincided with the end of the first instar, and a more gradual drop in h per plant during the later instars.

The number of egg batches per plant is related to plant size; more egg batches being laid on the largest plants (van der Meijden, 1976). This tendency is seen in the significant positive correlations obtained between the number of egg batches/m2 and the biomass of ragwort/m2 (estimated at the time of hatch of cinnabar), in 8 out of 10 years at Weeting Heath (Table 4). In the two years when this correlation was not statistically significant (1969, 1970), the density of eggs was so low compared with the density of plants that many quadrats containing large plants were not laid in. Such correlations do not necessarily imply that the female moth is actively selecting the largest plants on which to lay her eggs. If she lays her eggs on ragwort leaves at random, more eggs would still be laid on large plants, simply because these have more leaves on which eggs can be deposited. To test whether selection is occurring, one needs to know the number of eggs laid on individual plants of known biomass, but such data are not available.

Myers and Campbell (1976b) have suggested that the cinnabar moth has the genetic, or phenotypic, flexibility to adjust egg batch size, egg distribution and larval dispersion to variations in plant density. This suggestion stems from a theoretical study by means of a simulation model (Myers, 1976) of the influence of distribution and dispersal on the population size and stability of an insect which is capable of exhausting its food supply. Myers concludes from this study that both population size and stability will be highest when egg batch size is as large as can be supported by an average food plant, or


Table 4 Showing various measures of dispersions of cinnabar moth at Weeting Heath.

~~ ~~

Mean no. Correl. coef. Indices of Log. (no. egg batches egg batches/m2 dispersion larvae/

/m2 v. plant biomass/m2 egg batches/m2 kg ragwort) l/k l a

1966 1967 1968 1969 1970 1971 1972 1973 1974 1977

0.54 2.59 3.8 1 0.01 0 6 3 3.75 0.57 1.35 2.00 0.2 1

0.2257” 0.5195b 0.5067b 0.0671 n.s. 0.1718 ns. 0.6734b 06242b 0.5342b 0.3989b 0.4261b

4.1286 0.9852 2.01 17

1.3928 1.2057 5.3496 2.40 1 8 1.6695 4.3950

-

3.43 16 1.8321 2.8465

2.4860 2.3865 5.2101 3.1605 2.8729 6.9556

-

2.8665 3.8539 4.3979 0.7903 2.3 198 3.602 1 3.041 1 3.1079 3.0276 2.3674

P < 0.05; P < 0.001.

slightly larger if larval dispersal occurs. Clumping of egg batches on food plants increases population stability when egg batches are small by ensuring that some food plants will not be overcrowded. She has tested these ideas with data for the cinnabar moth (Myers and Campbell, 1976b) and claims that they support the findings of her model. However, these conclusions are based upon a number of pieces of evidence which, in my opinion, do not stand up to rigorous inspection.

First, Myers and Campbell (1976b) claim that egg batches are more clumped when cinnabar density is high. To test this idea, they use variance/ mean as a measure of clumping, and Myers (1978b) attempts to justify this by means of a simulation model. The study ofdispersion in animal populations is notoriously difficult because so many indices of clumping are not independent of population size. Field counts of egg batches per square metre at Weeting Heath were described adequately by the negative binomial distribution in 9 out of 10 years. The exception was the year when egg numbers were exceedingly low (1969: Table 4). Egg clumping, as measured by l/k of the negative binomial is not positively correlated with density (log number of larvae per kg of ragwort) ( r = - 0.4072, d.f. = 7, n.s.), nor is Morisita’s index of dispersion, l a (Morisita, 1962) ( r = -0.5063, d.f. = 7, n.s.) (Table 4). Thus, these data do not support Myers and Campbell’s views that egg batches are more clumped when density is high, and it seems likely that the relationship with density which they demonstrate is an artefact caused by the inappropriate use of variance/mean as a measure of clumping. As

20 J. P. DEMPSTER

they found, variance/mean is positively correlated with density in the Weeting data ( I = 08220, d.f. = 8, P c 0.01).

Myers’ model (Myers, 1976) also predicts that populations in which egg batches are small in relation to the average size of a food plant should have a more contagious egg batch distribution. In any one population of cinnabar moth, egg batch size can vary considerably between years. At Weeting Heath the mean number of eggs per batch has varied from 19-43 over 10 years. During this time, the mean size of the food plants has also varied, since the plant population contains few large plants in years following defoliation by the moth (Table 3). However, if the mean egg batch size per unit of plant biomass is calculated, it shows no correlation with the indices of clumping l/k ( r = 0.0509, d.f. = 7, n.s.) and l a ( r = -0.1515, d.f. = 7, n.s.). Added to this, van der Meijden (1976) and Green (1974) showed that the number of eggs per batch is independent of the size of the plant on which they are laid.

The third prediction from Myers’ model is that larval dispersal should be lower in populations in areas where plants are widely spaced. Evidence of this is given by Myers and Campbell (1976b). First, they measured the proportions of first and fifth instar larvae to drop from plants when disturbed, but failed to show any significant relationship with plant density. Next, they looked at the distribution of fourth and fifth instar larvae and estimated the amount of food available to them on the occupied plant and the nearest neighbouring plant. From this they argued that if the tendency for dispersal was low, more food would be available if the larvae moved to the adjacent plant. In contrast, populations with a high tendency for dispersal should have readjusted their distribution, so that few would be better off if they moved. I do not believe that it is possible to make judgements of this sort from a single measure of dispersion, at one point in time. Where plants are far apart, many larvae may disperse but fail to find another plant and so die. These would then be unrecorded and one would get a false impression that dispersal had been low. One can overcome this difficulty only by knowing the initial number on a plant and by following their subsequent dispersal. Lastly, Myers and Campbell (loc. cit.) used a high frequency of single larvae and pairs of larvae on plants as an indication of a high rate of dispersal in a population. Akain, without detailed knowledge of the original number of larvae, and of their death rates, interpretation of these types of data is impossible.

Taking all of this evidence into account, there is, in my opinion, nothing to suggest that the cinnabar moth is able to adjust its egg batch size, egg distribution, or larval dispersal to food plant density. Instead, I believe that the patterns of dispersion seen in the field result from the tendency for more eggs to be laid on large plants (though not necessarily through active selection


on the part of the female moth), and from the subsequent reaction of individual larvae to one another’s presence.

If egg distribution is unrelated to the distribution of food, what then are the advantages of laying eggs in clusters, when food for the larvae is likely to be limited? Rose (1978) found that there was a lower percentage hatch of eggs in the laboratory from small than from large egg batches. She attributed this to the greater hatchability of the first laid eggs, which tend to be in larger batches. Added to this, any infertile eggs laid by non-fertilized females will normally be in small batches, though these are probably rare in the field. Van der Meijden (1976) also reported that hatching success from the smallest egg batches was a little lower in the field. However, larvae occurring in ones and twos are far more difficult to find on a large plant than are normal sized clusters, which might give a false impression of poor hatch from small batches.

Ghent’s (1960) study of Neodiprion has led several authors to suggest that the advantage of laying eggs in batches rests with the greater difficulty which solitary larvae have in penetrating the plant cuticle when starting to feed. However, there is no evidence of this in the cinnabar moth, and larvae kept singly in the laboratory survive just as well as those kept in groups (van der Meijden, 1976). It seems more likely that the advantage of gregarious behaviour in the first instar is that it leads to better survival from predation. It is during the first instar that the caterpillars are most heavily attacked by arthropod predators, and when a cluster of larvae is attacked, they react by dropping from the leaf on silk threads. Dempster (1971a) showed that there was a significant correlation between survival and the number in a cluster ( r = +0*6270, P < 0.01) and suggested that the most likely reason for this was that a higher proportion of larvae escape when a large cluster is attacked by a predator than when a small cluster is attacked.

Food is not normally in short supply during the early instars, so that first stage larvae can afford to aggregate without this adversely affecting food supply. It is only during the older larval stages, and particularly the fifth instar, that aggregation may lead to increased competition for food. As we have seen (p. 18), gregarious behaviour is replaced by agonistic behaviour by the fifth instar and this leads to a spacing out of the caterpillars. By that time, the likelihood of predation by arthropods is greatly reduced.

Variations in egg batch size between years and between populations (see p. 3 and Table 3) are probably brought about largely by variations in the size of females, which in turn depends upon the availability of food during their larval development. Dempster (unpublished data) found that large females laid on average more eggs per batch in the laboratory (p. 3), and this view is further supported by the positive correlation between number of eggs per batch and the mean size of pupae (Table 3) from which the

22 J. P. DEMPSTER

females emerged ( I = 0.8296, d.f. = 5, P < 0.05: excluding data for 1969 when only two egg batches were recorded in 150 m’).

Besides these effects of egg and larval dispersion, the distribution of cinnabar moth is further clumped by the patchy distribution of its food plant, ragwort. This is a relatively short-lived plant and it is dependent upon gaps in the vegetation for seedling establishment. This makes its distribution both patchy and variable from year to year. This can be seen from Fig. 4, which shows the changes in the mean numbers of plants within 25 sub-plots, of 20 m x 30m, at Weeting Heath between 1968-1974. These data were obtained by counting the number of plants within 6 m2-quadrats in each area. The site at Weeting Heath is extremely homogeneous compared to many areas where cinnabar moth occurs, but even here there are considerable changes in plant density and distribution in the course of a few years. Ragwort can become greatly reduced in areas where it was abundant and spread into other areas where its density was previously low.

The moth adjusts its own dispersion to these changes by movements to areas of high plant density. During an intensive mark and recapture study on the adult moth, Dempster (1971a) found that there was a significant

44 r

I 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

Sub-plot

Fig. 4. Changes in the mean number of ragwort plants per m2 on 25 sub-plots at Weeting Heath 1968-1974.


correlation between the number of adults caught and the density of plants (r = 0.7432, d.f. = 7, P c 0*05), but no correlation between the distribution of adults and the distribution of pupae in the previous winter (r = 0.4419, d.f. = 7), showing that there had been a readjustment of dispersion.

Van der Meijden (1979) describes a similar variation in the distribution of the plant and the moth on a larger scale within coastal sand dunes in Holland. In an area of about 1 km2 he identified 150 populations of ragwort, more or less separated from one another. He studied just over 100 of these for five years and showed that the moth’s distribution was continually changing, as it attacked new populations of the plant, but became extinct on others. At the same time, extinction of plant populations frequently occurred, thus causing an everchanging mosaic of plant and moth abundance. Approximately half of the plant populations contained no plants during at least one year of the study, and almost 17% contained no plants during the last three years of observation. Similarly, attacks by the moth lasted for only a single year in many populations, although one plant population was attacked throughout the five years.

Interpretation of van der Meijden’s findings depends upon one’s definition of a population. It is arguable that the whole dune system should be considered as a single “population” of the plant and of the moth, since in one year (1976) every plant population was defoliated by cinnabar, whether or not it had eggs laid on it. Migrating caterpillars were able to find and defoliate all of the plant populations studied. Large caterpillars can survive for more than two weeks without food and they can move considerable distances in that time, perhaps up to 800 m (van der Meijden, 1971). Few animal populations are totally independent of one another, since they are mostly subject to immigration and emigration. However, the ability of caterpillars to move from one plant population to another suggests a lack of the discontinuity required by most definitions of “population”.

However one views this, van der Meijden’s study demonstrates the dynamic nature of the dispersion of cinnabar moth and its food plant beautifully. It also clearly shows the need for the moth to be able to disperse effectively between aggregations of the plant. As van der Meijden (1979) points out, this need is increased by the adverse effect of defoliation by the moth’s caterpillars on the food supply for its next generation (see p. 17).

It is extremely difficult to obtain estimates of the effects of dispersal on insect populations. The limited dispersal of caterpillars is density-dependent (see above), but there is also some evidence that adult dispersal is density- dependent in the cinnabar moth. First, the number of eggs laid in 1968,1971 and 1974 at Weeting Heath was lower than that expected from pupal size (Dempster, 1975), and this suggests that there was either an exceptionally high death rate of adults, or that many emigrated. There was no evidence for

24 J. P. DEMPSTER

increased mortality in those years, but in 1968 and 1971 large numbers of adults were seen flying out of the area. The three years in question were all years when adult numbers were exceedingly high.

Secondly, the effect of adult density on flight activity was studied in the laboratory (Dempster, 1971a) and this showed that moths flew significantly more when kept at high densities. This study failed to show any effect of size of adult, or of rearing density, on flight activity: density of adults alone appeared to be important. The significance of density-dependent emigration is discussed further on p. 27.

VII. POPULATION ECOLOGY OF THE MOTH

The most detailed study of the population dynamics of the cinnabar moth is that at Weeting Heath, England, covering the years 1966-1974. Life tables describing changes in the moth’s population up to 1973 are given by Dempster (1971a, 1975).

During this study, the moth’s numbers fluctuated widely, with egg numbers ranging from 62-21,699/150 m2 and adult numbers ranging from 1.5-362/150 m2. The caterpillars completely defoliated the ragwort over the whole site (19 ha) in 1967, 1968, 1971, 1973 and 1974.

The pattern of mortality during the young stages of the moth was similar in most years. Egg mortality was always low and relatively constant, with an average of 7.6% dying (range 1.2-13*1%). This was due to infertility (0.8-4.4%), failure to hatch successfully (0.4-2-9%), and factors, such as predation and damage to the plants by rabbits and phytophagous insects, including cinnabar moth itself. Once the larvae hatched, mortality increased considerably, so that between 3245% had died by the end of the second instar. This was due largely to arthropod predators. Nine species were identified by means of serology as feeding on the moth’s young stages, but by far the most important was a mite, Erythraeus phalangoides. Estimated mortality due to predation was shown to be closely related to the density of this predatory mite (Dempster and Lakhani, 1979). As the caterpillars grew they became immune from attack by arthropod predators, but there was another peak in mortality in the fifth instar, when the parasitoid, Apanteles popularis, killed its hosts. This killed between 5.2-35.7% of the fully grown caterpillars. There was a further period of high mortality at the time of pupation, due probably to predation by moles (Talpa europaea). This mortality was estimated to range from 51.4-96.1% over the 9 years of the study, but there is reason to think that it may have been overestimated owing to difficulty in assessing the number of larvae entering pupation, particularly in years when many were dying of starvation (Dempster and Lakhani, loc. cit.).


Superimposed on this pattern of mortality was the very high mortality caused by starvation of larvae in those years when food was in short supply (Table 2). In most of these years, deaths from starvation occurred in the later larval stages, but in some, such as 1968, when close to 50% of the caterpillars starved, food ran out when many larvae were still hatching.

Food shortage had a marked effect on the fecundity of female moths emerging in the following year. The estimated number of eggs per female was between 280-300 following years when no starvation occurred, but was under 100 in years following those when the food supply was inadequate. Mean fecundity was further reduced in years when adult numbers were high (1968, 1971, 1974), because of emigration of adult moths.

Dempster (1975) presents a k-factor analysis of the life table data (Varley and Gradwell, 1960). In this, k-values were calculated for losses during each developmental stage of the moth. Figure 5 shows a similar analysis carried out in a slightly different way, so that deaths from any one mortality factor have been combined, irrespective of the stage on which they act. Thus, deaths from arthropod predators plus unknown causes (i.e. complete disappearance of the individuals) in the egg and larval stages have been combine as k s . To enable this to be done, each mortality factor is taken as operating in succession during the moth’s development. Thus infertility, failure to hatch, arthropod predation, Apanteles, starvation, and pupal loss are taken as discrete mortalities with no overlap in effect. This is not strictly true, since starvation, for example, can cause high mortalities at any time during larval development, although it does affect mainly older instars. However, this approach gives a clearer picture of the impact of the various factors affecting the population, than one based on different age classes.

The analysis in Fig. 5 also differs from previously published analyses, in that immigration of adult moths onto the study area, resulting from a small scale movement within the site in 1970, has been included into estimates of dispersal, thus giving a negative k-value in that year. Dempster (1975) restricted analysis of dispersal to estimates of emigration out of the site.

Inspection of Fig. 5 shows that total K is determined largely by variations in k6 (starvation: r = 0.7991), ks (pupal loss: r = 0.8954) and kl (adult dispersal and mortality: r = 0.6706). Adult numbers are inversely related to K.

Because of the impact of starvation, total larval mortality is positively correlated with larval density, though this is clearly not a linear relationship (Fig. 6). At around 1000 larvae per kg of ragwort there is a marked increase in mortality as food supply becomes limiting. As pointed out by Dempster and Lakhani (1979), pupal mortality is also correlated with larval density, though not with pupal density. It is difficult to see any biological explanation for this, since pupal loss is thought to be due mainly to predation. It therefore seems likely that the relationship between pupal mortality and larval density

0 -

-1

z:' -

01 - k. 1966 1W7 1968 1969 1970 1971 1972 1973 1974

Fig. 5. K-factor analysis of population data for cinnabar moth from 19661974 at Weeting Heath. k l = adult dispersal and mortality; kz = variations in adult fecundity; k3 = infertility of eggs; kq = failure to hatch; ks = larval predation and unknown causes; k g = starvation; k7 = Apanteles; k s = pupal loss; K = total generation loss.

THE ECOLOGY OF THE CINNABAR MOTH

50

27

0 70 -

100

901 0 74

066

is an artefact caused by the method of study failing to separate larval and pupal mortality adequately.

Variations in natality are brought about by two factors, both of which are related to density, i.e. fecundity and dispersal. Fecundity is determined by larval density and the supply of food (see p. 16). Because of the effects of food supply on the size of individuals, estimates of fecundity can be obtained from the mean pupal width each year. These estimates can then be subtracted from the total reduction in natality, calculated from the maximum possible fecundity times the number of moths, to give an estimate of the combined effect of variations in dispersal and mortality of adults (kl). Losses due to variations in fecundity ( k z ) are positively related to density in the previous generation, and so are acting as a delayed density-dependent factor. Varia- tions in kl are thought to be due largely to variations in dispersal (see p. 23) and are correlated with adult density, emigration tending to occur when moth numbers are high.

The conclusions from these analyses were tested by Dempster and Lakhani (1979) by constructing a simple model of the interacting populations of cinnabar and ragwort, to see whether those factors identified as being important could account for the bulk of the observed variation in the population size between years. This model was built from three sub-models describing (1) the effects of rainfall and defoliation by cinnabar moth on the number and biomass of ragwort plants; (2) the effects of food supply and adult density on the moth's natality; and (3) the effects of larval density on mortality. By taking the number of plants, the number of cinnabar moth eggs, and the percentage of plants flowering in 1966, together with rainfall data for subse-

28 J . P. DEMPSTER

quent years, reasonable estimates of plant and moth numbers were obtained from the model for each year up to 1974. The model was further tested by running it on past 1974 to predict the numbers which should be present in 1977, for comparison with actual field counts. Remarkably close agreement was obtained, showing that the study had probably identified the more important elements of the moth’s population dynamics at Weeting Heath.

Although the factors determining the abundance of the moth and its food plant at Weeting Heath, are well understood, the question must be asked as to how applicable the findings are to other localities. Myers (1978a) has argued that because specific mortality factors will vary from place to place, the enumeration of them will not yield a general understanding of the population dynamics of the moth. Instead of the more classical population study, she suggests that the biological aspects of the insect which are important generally to population regulation may be identified by studying the ways in which the moth has adapted to different environmental conditions. Before comparing the findings at Weeting Heath with those from elsewhere, let us first consider this proposal.

Myers suggests three characters which might respond to changes in plant density and which would lead to greater population stability of the moth, namely reduction in moth size, reduction in egg batch size and increased density-dependent dispersal by larvae between plants. The evidence presented by Myers and Campbell (1976b) concerning adaptation of egg batch size and larval dispersal is discussed on p. 18, where it is concluded that there is no evidence to suggest that the moth is capable of adjusting its dispersion in the way suggested by Myers (1978a). Let us now look at the possibility that reduced adult size may be an adaptation which would lead to greater population stability.

Myers (loc. cit.) suggests that the larval weight required for successful pupation will be a constant characteristic of moth populations established over a long period of time. Selection pressures at times of starvation will lead to a reduction in the minimum weight required for pupation and this will lead to greater population stability, since it will tend to buffer the effects of starvation. Two pieces of evidence suggest that this is not true. First, fluctuating (unstable) populations show a wide range in pupal size; small pupae resulting from starvation. In contrast, non-fluctuating populations tend to occur at low density and tend to have a constant, large pupal size, since they are not subject to the violent impact of starvation. This is the reverse to what Myers proposes. Secondly, it seems unlikely that selection pressures on the minimum weight required for pupation are large at times of starvation, because the heterogeneity in moth density and timing ensures that many individuals pupate at “normal” size in years of starvation. This can be seen in Fig. 7 where the distribution of pupal size at Weeting Heath in years of


Pupal width (Em)

Fig. 7. The distribution of pupal sizes of cinnabar moth in years of no food shortage (a) and of food shortage (b) at Weeting Heath.

starvation is compared with that in years when food supply was ample. In spite of this disagreement with the proposals of Myers, it is tempting

to think that there must be considerable variations in the “quality” of individuals, brought about by genetic changes during the large fluctuations in some populations of the moth, which should be taken into account in any population model. What evidence there is, however, suggests that such genetic effects are insignificant compared with the direct impact of environmental variations on moth numbers.

Richards (1978) studied the genetic and non-genetic effects of maternal size on the size of offspring and concluded that such maternal effects were un- important under normal field conditions compared with the effects of larval crowding and food availability. Dempster (unpublished data) did a similar study of survival, under crowded and uncrowded conditions, of offspring from high and low density field populations, but found no detectable genetic effect (Table 5). In this experiment, eggs were collected in 1966 from Weeting Heath and Monks Wood (East Field) (Dempster, 197 la), distributed systematically between treatments, and reared at different densities. Fresh food was put into the cages each day, but there was probably some shortage of food at the highest densities. Larvae from both sites survived better at low density, but there was no significant difference between sites. These studies indicate that genetic effects on fecundity (size) and survival are so small that they can be safely ignored in any population model of the moth.

30 J. P. DEMPSTER

Table 5 Survival of larvae from a high (Weeting Heath) and a low density (Monks Wood)

population when reared at different densities.

No. of No. of No. of larvae pupating larvae/cage replicates Weeting stock Monks Wood stock

1 24 18 10 3 8, 6, 7 40 3 10, 14, 8

19 7, 8, 8

14, 20, 8

The model proposed by Dempster and Lakhani (1979) is based solely upon the interaction between the populations of the moth and its food plant. Sufficiently detailed data from other localities are not yet available to test the whole model, but some idea of its generality can be obtained from two studies in North America.

First, there are data from an introduced population of the moth at Nanaimo, B.C., Canada, obtained by Dr P. Harris and Mr A. T. S. Wilkinson. Using these data, Lakhani and Dempster (1981) showed that the Weeting model gave reasonable estimates of both plant and moth numbers. Nanaimo is on a gravelly, sandy loam, in an area which is often subject to severe summer drought, so that rainfall is often limiting to the multiplication of ragwort. As at Weeting Heath, regeneration by ragwort after defoliation appears to be mainly from root buds.

In contrast, data from an introduced population of the moth at Jordan in Oregon, USA, gave a very poor fit with the Weeting model. This site is an unimproved pasture, which was cleared of woodland in 1963-1965. Rainfall during early summer is appreciably higher than at Nanaimo and Weeting. Isaacson (1973) has published life tables for two years (1970, 1971), for this introduced population of the moth, and Stimac and Isaac- son (1978) have compared the population dynamics of the moth at Jordan with that in England. The factors affecting the population dynamics of the moth in Oregon are broadly similar to those identified at Weeting Heath, except that Apanteles is not present in this introduced population. In two years, 1970 and 1971, egg mortality was 12.4 and 30.3%, due to embryonic failure (infertility and failure to hatch), predation, and defoliation by larval feeding, i.e. somewhat higher than that recorded at Weeting. Young larvae appear to be taken by a similar range of arthropod predators and a high mortality from starvation occurred in 1971. Stimac and Isaacson (1978), summarizing five years’ data from Oregon, considered that larval mortality was the key factor determining total generation survival, and that both starvation and arthropod predation were acting as density-dependent factors, although insufficient data were available to show this conclusively. The main


differences between the Oregon population and that at Weeting Heath were the low pupal mortality (over five years it ranged from 1540%) and the smaller variation in the availability of food for the moth’s caterpillars at the Oregon site. Stimac and Isaacson (loc. cit.) record only a four-fold variation in ragwort biomass (g dry wt/m2) over a six-year period in Oregon, compared with a 24-fold variation (g wet wt/m2) over nine years at Weeting Heath.

Some idea of the likely impact of those differences that have been found can be obtained from further study of the Weeting Heath model. By varying the size of the various parameters used, one can study their impact on the cinnabar moth and ragwort abundance. Lakhani and Dempster (1981) have done this and have shown that the model is exceedingly robust, in that large variations in some parameters have rather little effect on the output of the model. Increased mortality in the egg stage to about 30% had a negligible effect on the size of adult moth and ragwort populations. Similarly, a reduced pupal mortality, similar to that found in Oregon, produced larger fluctuations in adult numbers, but had little effect on plant numbers and biomass. In the model, the effects of increases in adult numbers were damped by adult dispersal. Changes in the biomass of ragwort available to cinnabar moth larvae had a bigger effect, since in the model, this is the main determinant offluctuations in the moth’s abundance, and it seems likely that the differences between the findings at Weeting Heath and Oregon rest more with differences in the dynamics of the plant populations than with the moth. This view is supported by the fact that reasonable estimates of the moth’s numbers at Jordan are obtained from the Weeting model if its plant sub-model is bypassed by using estimates of ragwort biomass obtainable from data published by Stimac and Isaacson (1978), Myers (1978), Stimac (1978) and Lakhani and Dempster (1981). Stimac and Isaacson (1978) state that there is a rapid recovery of the plants following defoliation in Oregon, with both rosettes and mature plants making regrowth. Regeneration by mature plants may reduce the variation in biomass of ragwort in different years. A large part of that recorded at Weeting Heath was caused by the fact that very few flowering sized plants were present in years following defoliation (Table 2). The Weeting model produces smaller fluctuations in the moth’s abundance, when there is less variation in ragwort biomass, which is what Stimac and Isaacson found.

Although both larval mortality and adult dispersal are density-dependent, they are unable to regulate the moth’s population below the carrying capacity of the habitat. This is probably due to the very large variations in carrying capacity which can occur as a result of changes in the biomass of ragwort present. Studies with the Weeting model suggest that in more stable environments, far greater stability will occur in the moth’s population (Lakhani and Dempster, 1981). It is perhaps worth pointing out that many studies of

32 J. P. DEMPSTER

the population dynamics of herbivorous animals totally overlook variations in the carrying capacity of the habitats they occupy, yet this can have a huge effect on the stability of populations.

The moth’s population is buffered against extinction by the heterogeneity within the habitat and in the moth’s timing and density. Survival tends to be best in those areas where early-hatching larvae occur at low density, or where food supply is particularly good. The probability of persistence is, of course, also dependent upon the size of suitable habitat available and hence the size of the moth’s population. In spite of this, however, local extinction is a common feature of cinnabar moth populations.

The moth has good powers of dispersal, so that recolonization after extinction is frequently rapid. As one would expect, however, the likelihood of recolonization is dependent upon distances involved and will be greatest in years of high density, since dispersal is density-dependent. Although the distribution of adult moths at the time of their emergence is very patchy in years following a population crash at Weeting Heath (Dempster, 1971a), the moth rapidly reoccupies the whole site. Van der Meijden (1979) describes a situation where the plant occurs in discrete patches separated by several hundred metres. These patches are found and exploited by the moth for a few years, before local extinction occurs, so that not all patches of the plant are exploited in any one year. On an even larger scale, Dempster (1971a) described the extinction of an isolated population of the moth at Monks Wood (East Field) in 1968. The nearest known population of the moth was about five miles (eight km) away, and the site was not reoccupied by the moth until 1978, ten years later. In that year, a single batch of eggs was found, indicating that probably a single fertilized female had recolonized the site.

VIII. CONCLUDING REMARKS

Studies of the cinnabar moth and its food plant, ragwort, suggest a remarkable degree of co-evolution of the two species. The activities of the moth appear to have been an important selective force in the evolution of the plant, so that the latter can survive periodic defoliation with little or no effect on its numbers. It is, of course, partly this evolved ability to withstand damage which makes ragwort such a difficult weed to control. In turn, the moth has evolved the ability to cope with the poisonous alkaloids produced by the plant, and in fact the moth stores these poisons itself, probably as a defence against its predators.

The role of these plant alkaloids in the ecology of the moth is especially


interesting, since the moth is one of a very small number of specialist herbi- vores feeding on ragwort, and compared with other Lepidoptera, the moth is attacked by relatively few predators, and it has only one specific natural enemy, namely Apanteles.

In most situations, ragwort abundance appears to be unaffected by the attacks of cinnabar moth. On the other hand, the numbers of the moth are very dependent upon the abundance of ragwort. Similarly, the specific parasitoid, A. popularis appears to have little effect on the population size of the moth, although its abundance is closely dependent on the availability of cinnabar hosts (see Fig. 2). We appear then to have the situation where food supply is determining the population size of both cinnabar moth and Apanteles, although neither species is having a significant impact on the population size of its food organisms. I t would be interesting to know whether the same applies to the parasitoid, Mesochorus facialis, which is attacking Apanteles.

The population studies which have been made on cinnabar moth suggest that there is no intrinsic, or extrinsic, factor which limits numbers below the carrying capacity of the plant population. Although aspects of the moth’s behaviour, such as density-dependent dispersal and the spacing out of the older larvae, will tend to reduce the effects of overcrowding, the scramble-type competition for food which occurs between the larvae ensures that there are very high death rates from starvation when food supplies are inadequate. Added to this, those individuals which survive starvation are smaller and less fecund than normal, so that the effects of food shortage are carried over into the next generation.

In localities with poor soil and limited rainfall, few plants reach a flowering size in years following defoliation, since regeneration from root buds produces only small rosette plants. In these situations the carrying capacity of the site for the moth may fluctuate violently, as a result of periodic defoliation, as seen at Weeting Heath. Here the population crashes of the moth often occur in the second year of defoliation, as a result of the reduced carrying capacity of the site (e.g. 1967 + 1968, 1973 + 1974; Dempster, 1975). In other localities, with richer soils and ample rainfall, where the plant regenerates by secondary flowering rather than from root buds, defoliation by the moth does not produce such violent fluctuations in its food supply, and the moth population will be more stable, as seen in Oregon (p. 30). In neither situation, however, is it likely that cinnabar moth will control ragwort numbers.

It is clear from this that the cinnabar moth is unlikely to prove successful, by itself, in the biological control of ragwort (Stimac, 1978). It is possible, however, that adequate control of ragwort may be obtainable if some other factor operates against the plant whilst it is weakened by defoliation from the moth. An example of this has been reported from Nova Scotia (Harris

34 J . P. DEMPSTER

et al., 1978) where frosts frequently kill plants which are regenerating after attack by cinnabar moth.

ACKNOWLEDGEMENTS

I wish to thank Dr M. G. Morris, Mr K. H. Lakhani and Dr E. Pollard for their helpful comments and criticism during the preparation of this article.

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36 J. P. DEMPSTER

Myers, J. H. (1976). Distribution and dispersal in populations capable of resource depletion. A simulation model. Oecologia (Berl.) 23, 255-269.

Myers, J. H. (1978a). Biological control introductions as grandiose field experiments: adaptations of the cinnabar moth to new surroundings. Int . Symp. Biol. Contr. Weeds 4th. 181-188.

Myers. J. H. (1978b). Selecting a measure of dispersion. Enoiron. Entomol. 6, 101-106. Myers, J. H. and Campbell, B. J. (1976a). Predation by carpenter ants: a deterrent

to the spread of cinnabar moth. J. ent. Soc. Br. Columbia 73, 7-9. Myers, J. H. and Campbell, B. J. (1976b). Distribution and dispersal in populations

capable of resource depletion. A field study on cinnabar moth. Oecologia (Berl.)

Myers, J. H. and Campbell, B. J. (1976~). Indirect measures of larval dispersal in the cinnabar moth, Tyria jacobaeae (Lepidoptera: Arctiidae). Canad. Ent. 108,967-972.

Philogene, B. J. R. (1975). Responses of the cinnabar moth, Hypocrita jacobaeae, to various temperatures/photoperiod regimes. J. Insect Physiol. 21, 1415-1417.

Poole, A. L. and Cairns, D. (1940). Botanical aspects of ragwort (Senecio jacobaea L.) control. Bull. N.Z. Dep. Scient. ind. Res. 82, 1-61.

Richards, L. J. (1978). Maternal influences on size in the cinnabar moth. M.Sc. Thesis, University of British Columbia, vi + 53 pp.

Rose, S. D. (1978). Effect of diet on larval development, adult emergence and fecundity of the cinnabar moth, Tyria jacobaeae (L.) (Lepidoptera: Arctiidae). M.Sc. Thesis, Oregon State Univ. 88 pp.

Rothschild, M. (1975). Remarks on carotenoids in the evolution of signals. In “Co- evolution of Animals and Plants” (Eds L. E. Gilbert and P. H. Raven), pp. 2&51. University of Texas Press, Austin and London.

Schmidl, L. (1972). Biology and control of ragwort, Senecio jacobaea L., in Victoria Australia. Weed Res. 12, 3745.

Steinhaus, E. A. and Marsh, G. A. (1962). Report of diagnoses of diseased insects 1951-1961. Hilgardia 33, 349-490.

Stimac, J. L. (1978). A model study of a plant-herbivore system. Ph.D. Thesis, Oregon State Univ. 240 pp.

Stimac, J. L. and Isaacson, D. L. (1978). Cinnabar moth as a biological control of tansy ragwort: comparison of population dynamics in England and Oregon. I n t . Symp. Biol. Contr. Weeds 4th. 155-162.

Varley, G. C. and Gradwell, G. R. (1960). Key factors in population studies. J . h i m . Ecol. 29, 399401.

Warren, F. L. (1970). Senecio Alkaloids. I n “The Alkaloids”, Vol. 12 (Ed. R. H. F. Manske), pp. 246331. Academic Press, New York and London.

Wilkinson, A. T. S. (1965). Releases of cinnabar moth (Hypocrita jacobaeae L.) on tansy ragwort in British Columbia. Proc. ent. Soc. Br. Columb. 62, 1&12.

Wilkinson, A. T. S., Harris, P., Neary, M. E. and Thompson, L. S. (1970). Control of stinking Willie with cinnabar moth Canad. Agric. 15, 9-1 1.

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24, 7-20.

The Zonation of Plants in Freshwater Lakes

D . H . N . SPENCE

I . Introduction . . . . . . . . . . . . . . . A . Aquatic Vegetation . . . . . . . . . . . . .

C . Habitat and Zonation Variables Distinguished . . . . . . I1 . Habitat Variables . . . . . . . . . . . . . .

A . Vertical Environmental Variables . . . . . . . . . B . Vertical and Horizontal Environmental Variables; Turbulent and

. . . . . . . . . C . Conclusions; Effects on Sediment and Plant Distribution . . .

. A . Vertical Zonation . . . . . . . . . . . . . B . Vertical and Horizontal Components of Zonation . . . . . C . Sediments and Plant Responses . . . . . . . . . .

IV . Causal Analysis of Changes of Within-lake Distribution with Time; Depositional Shores and the Hydrosere . . . . . . . . .

V . Plant Adaptations . . . . . . . . . . . . . . A . Flow, Substrate and Plant Distribution . . . . . . . . B . Photomorphogenesis, Photosynthesis and Zonation . . . . . C . Growth Forms, Plant Strategies and Interspecific Competition . .

VI . Competition with Microalgae and the Control of Macrophyte Zonation by Substrate or by Light . . . . . . . . . . . .

B . The Macrophyte Biomass/Depth Curve: some Implications . . . VII . Concluding Hypothesis: when Substrate or Light Controls the Distribu-

tion of Macrophytes in Lakes . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . Notes . . . . . . . . . . . . . . . . . Appendix: List of Symbols . . . . . . . . . . . . .

B . The Groups of Plants. and Overall Depth Distribution . . . .

Molecular Motion in the Littoral

111 . Causal Analysis of Within-lake Distribution at any Instant of Time

A . Competition with Microalgae and Extent of zc . . . . . .

I . INTRODUCTION

37 38 38 44 49 49

60 70 71 71 80 86

92 95 95 97

103

108 108 110

112 114 115 124 124

This paper presents a critical review of factors controlling the zonation of freshwater plants . In the Introduction I first outline the groups of plants which are classed as macrophytes. and comprise aquatic vegetation. and define their

38 D. H. N. SPENCE

overall depth distribution. Specific examples are then provided of the zonation of vegetation in a range of lakes, particularly to emphasize the distinction between environmental factors varying solely in the vertical plane and those that have both vertical and horizontal components. This distinction underlies my causal analysis of zonation.

A. Aquatic Vegetation

Numerous schemes of classification of water plants have been devised, and are reviewed by Sculthorpe (1967) and Hutchinson (1975). Sculthorpe also gives a comprehensive list of the descriptive literature on zonation and floristics of aquatic habitats in many parts of the world while Gessner (1955, 1959) and Hutchinson (1975) provide selections of published examples in some detail.

These accounts tend to consider as “aquatic” only those types of vegetation of which the underground parts at least are permanently submerged. While most attention in the present paper is paid to plants comprising such vegetation, aquatic vegetation is also taken to include those “wetland” types such as fen, fen woodland or much swamp-forest which occur on seasonally flooded land. This definition follows, for example, Tansley (1949), Curtis (1959), Walker (1950), Lind and Morrison (1974), Hook and Scholtens (1978) and Husak and Hejny (1978). The swamp forests of the tropics and North America, for instance, are typical of aquatic and wetland sites (e.g. Eggeling, 1947; Godfrey and Wooten, 1979) and emphasize the habitat gradations which exist within areas dominated by a single life form.

B. The Groups of Plants, and Overall Depth Distribution

It is necessary first of all to outline the various plant forms which inhabit fresh water and to indicate which of these are classed as macrophytes. There are three overlapping groups of plants:

(1) Free-floating plants. The bulk comprises a photosynthesizing suspension of phytoplankton, microalgae or microphytes. Some free-floating macrophytes, all Tracheophyta, occur on the water surface-species of Lemna, Azolla, Salvinia, Pistia and Eichornia--and a few below it, such as Cerato- phyllum and most Utricularia species.

(2) Thalloid, filamentous, colonial, unicellular algae: lying on or attached to the stones, sands or muds of the late bottom, or to the above-ground parts of larger attached plants. Thalloid species like Enteromorpha, along with many of the larger filamentous algae, such as species of Cladophora and Rhizo- clonium, may be classed as macrophytes.

THE ZONATION OF PLANTS IN FRESHWATER LAKES 39

(3) Larger attached plants, mainly Tracheophyta. Plants in this group include members of the stonewort or muskgrass family, the Characeae, which are large algae confined to fresh and brackish water. Frequently members of the Bryophyta, mosses and liverworts, become important but most macrophyte cover is probably supplied by the Tracheophyta, which includes ferns and fern-allies like Pilularia and Isoetes, and the predominant angiosperms.

The depth of water colonized by macrophytes is referred to as zC (Spence, 1976a) (see List of Symbols, p. 124). In certain clear waters, unicellular and colonial microalgae colonize sediments, at least seasonally, to depths below z, (for examples, see Hutchinson, 1975; Spence, 1976a) but, as a rule, z, occupies most if not all the littoral. The depth of water occupied by green plants-macrophytes and microalgae-is the euphotic zone zeu. zC is always less than zev.

Attached aquatic vegetation occurs along a more or less continuous gradient from deep water to at least seasonally dry land, from underwater plants to forest. This vegetation can be grouped into five main classes by combining the depth of the water table below or above the soil surface during the growing season, with the predominant life form on a particular section of the water table gradient (modified from Tansley, 1949 and Spence, 1964). Throughout this review it is assumed that the water table during the growing season is only intermittently variable so no account is made of impoundments, reservoirs etc. and their vegetation (and see, for example, Quennerstedt, 1958).

1. Swamp Forest

Stands dominated by phanerophytes:’ the water table may vary from as much as 2 m below the soil surface during the growing season and above it for the rest of the year (seasonal swamp forest); or it may always lie at or above the soil surface (permanent swamp forest). Many areas of swamp forest have an uneven surface so that drier, firmer patches occupied by phanerophytes alternate with more or less permanent swamps and pools which may contain some phanerophytes, but are mainly colonized by hydrophytes’ (mixed swamp forest). Included in swamp forest are the fragments of woodland or scrub of Alnus and Salix species etc. which occur in the United Kingdom amongst the helophytes3 and hydrophytes of fens and, sometimes, of swamps also. In Scotland, for example, they are found on stretches of ground dominated by the large tussocks of Carex paniculata4. In ungrazed, undisturbed sites these tussocks can exceed 2.3 m in height, the rhizome “trunk” accounting for up to 0.5 m and often being colonized by Salix or Betula species, in East Anglia by Alnus too, by many herbs and by ferns like Dryop- teris dilatata. The ground between tussocks in some places supports Salix species, which form a closed canopy overhead, whilst water in summer lies

40 D. H. N. SPENCE

Sheltered bay,

west end

-6b

Berula pubescens I

Mynca - Cal/una - -

Myrim - Carex ~ lasiacarpo

C lasocarpa -Myrim

Carer roslrala

-- -

Menyadhes -- Nvmphaea

P ~ o g e r a n nafans

I 100 2

Depth of water ( c m )

0

Fig. 1. Zonation of vegetation, represented by dominant species, in relation to summer water level: sheltered bay at west end of Loch an Choin, Inverness. After Spence (1964).

at the soil surface, or in other places this ground is dominated by hydrophytes such as Schoenoplectus, with the water surface as much as 15 cm above it (Spence, 1964, p. 349 and Plates 62, 63). Another example is provided by Betula-Myrica gale carr (Fig. 1) (Spence, 1964, Plates 59 to 61).

In Britain this swamp-forest or woodland is called “carr”, which is Old Norse for a copse on boggy ground. According to Godwin and Bharucha (1936), woody plants only survive in, for example, Wicken Fen if the water table lies more than 10 cm below the soil surface in winter and more than 40 cm below the soil surface in summer. By woody plants Godwin is referring to shrubs or trees of Alnus, Salix and Frangula normal components of carr in that area. Quercus robur, for instance, would be excluded because knowledge of its general distribution indicates its intolerance of wet ground. However, depth of water is only one aspect of flooding: its duration and its rate of flow are also important (Gil, 1970) and, in the tropics, the overall effects of climatic conditions on transpiration rates (Lind and Morrison, 1974). If a broader range of species in more continuous forest can be drawn upon, then a whole range of flooding tolerances are observed. In the southern United States, for example, species such as Populus deltoides can withstand no more than three to four days flooding whereas others like Nyassa aquatica or Fraxinuspennsylvanica can tolerate very long periods of deep flooding (Hook and Brown, 1973).

Fifteen of the 80 phanerophytes of low-altitude swamp-forest in Uganda are unique (Eggeling, 1947) and should be regarded as woody hydrophytes.


In the present account, however, the term “hydrophyte” will be restricted to non-woody hydrophytes.

2. Fen Vegetation

Stands are typically dominated by tall grasses like Phragmites spp., tall sedges such as Carex paniculata and herbs, all growing as helophytes and stands usually have a moss carpet. Water table during the growing season lies down to 0.4 m below the soil surface. Stands are liable to varying periods of flooding during the winter or wet season (Table 1).

Table 1

Summary of mean and range in depth of water table (cm) below ( - ) or above (+) the soil surface during the growing season of samples occupied by some typical fen dominants: data for Scotland, from Spence (1964: Table 39 and synoptic tables).

n is number of samples.

Depth of growing season water table (cm) below ( - ) or above (+ ) the soil

surface mean range n

Glyceria maxima-Iris -25 -3OtO -11 I Filipendula-Calliergon“ -14 -30to 1 4 Phragmites-Galium palustre -10 -40 to 2 20

Carex nigra-Calliergon -5 - 1 5 to 1 4 Carex rostrata-Calliergon -5 -37 to 10 11 Equisetum fluviatile-Calliergon -2 - I t 0 3 4 Carex paniculata-Angelica (in Salix Carr) 0 -50 to 36 4

Sphagnum-Juncus bulbosus 0 - 5 t o 5 5

Potentilla palustris-Calliergon - 8 -26 to 8 8

Carex lasiocarpa-Myrica gale 0 - 5 t o I 15

_ _ _ _ _ _ _ _ _ ~

Formerly Acrocladium.

3. Reed Swamp

Stands are dominated by reeds or herbs, growing as emergent hydrophytes. There is no moss carpet, although submerged mosses may be present. Water table during the growing season varies from a few centimetres below the soil surface to 1.5 m or 2 m above it (e.g. Denmark, Scotland (Fig. l), Boye- Petersen, 1917; Spence, 1964). It is noted that only Schoenoplectus in Table 2, amongst these dominants, is confined to fully submerged soils (in Scotland, Canada and East Africa) and that many grasses, or grass-like species dominate

42 D. H. N. SPENCE

Table 2 Summary of mean and range in depth of water above the soil surface during the growing season of samples occupied by some swamp community-types in Scotland (Spence, 1964, Table 39 and synoptic tables). All the emergents except Schoenoplectus lacustris

can also occur as dominants in fens. n is number of samples.

Depth of growing season water table (cm) above the soil surface

mean range n

Carex rostrata-Menyanthes trifoliata 19 3 to 43 8 Eleocharis palustris-Littorella 28 8 to 55 11 Phraymites communis-Sparyanium emersum 56 8 to 110 10

var. Jluitans 88 30 to 150 8

Equisetum Jluviatile-Littorella 85 40 to 150 6 Schoenoplectus lacustris-Juncus bulbosus

in both swamp and fen but with different subordinate species. One swamp dominant, Hippuris vulgaris, also occurs as a fully submerged plant to water depths of 6 m (Fig. 3).

Just as “swamp-forest’’ includes permanently and seasonally submerged sites, so the stands without trees interdigitate as fen and reedswamp in, for example, areas dominated by Phragmites communis or Carex rostrata. Pearsall (1918, p. 76) compromised by calling reedswamp “the climax aquatic community and the pioneer fen community”. Indeed, the presence of carpeting mosses like Calliergon (Acrocladium) cuspidatum or flood-sensitive herbs like Galium palustre in Scotland may help distinguish fen from the adjacent swamp which lacks such species. In temperate regions at least, it seems likely that only Schoenoplactus species are exclusively swamp dominants.

4. Floating-leaved Vegetation

A relatively small group of species are totally submerged outside their growing season and in their immature phases of growth. They produce floating leaves during most of their growing season. Many are heterophyllous, some homo- phyllous. Others again can survive for some time with the water table during the growing season below the soil surface (Nymphaea alba, Potamogeton polygonifolius). Maximum reported water depths for these plants range from 3.5 m in northern Europe to 4 m in East Africa (Spence, 1964; Spence et al. 197 1 a; Denny, 1972). Potamogeton natans, a heterophyllous floating-leaved species, reaches depths exceeding 4 m in some limestone lakes, like Loch Balnagowan (Baille na Ghobhainn) (Fig. 17), and produces floating-type leaves down to 1 m below the water surface. Many species with entirely submerged leaves (Potamogeton lucens, P. amplifolius) can produce dense leaf


cover just under the water surface and thus “mimic” true floating-leaved vegetation.

5. Submerged (Open Water) Vegetation

Dominated by hydrophytes which, with a few exceptions (Lobelia, Littorella and Subularia species, for example) are permanently submerged. Dominant hydrophytes in different lakes range from angiosperms and other Tracheo- phyta, to bryophytes, stoneworts and Cladophora species, although the latter are confined as dominants to brackish water.

The question of immediate interest here is the depth of the zone colonized by macrophytes in standing water, zC. Before looking at estimates of zc, however, it is necessary to examine briefly the possible sources of error in such estimates, a question studied in detail by Spence (1976a, pp. 114 et seq.). After

Fig. 2. Zonation of submerged vegetation in Lake Windermere: west shore between Wray Crag and Wetbarrow Point. After previously unpublished map of W. H. Pearsall, reproduced by Macan (1972).

44 D. H. N. SPENCE

a comparison of data on macrophyte depth limits collected by observation or by grab from a boat, and by diver, it was concluded that, unless data have been gathered on a detailed survey of small areas such as those carried out on parts of the English Lakes by Pearsall (1918, 1920 and Fig. 2), the most satisfactory records for vegetation that is invisible from the water surface are those collected by divers who are, preferably, botanists. By “diver” is meant a person equipped with Scuba.

It was admitted that, even then, errors in estimating lower macrophyte depth limits can be considerable; low available light and scattering limit both visibility and field of vision, which may be tolerable where slopes are steep and the vegetation “cut-off” is an obvious line but less tolerable where vegetation is scattered and slopes are gentle. Also, in the latter situations, it may be difficult even for a diver examining plant material in situ to decide whether a clump of, say, the moss Fontinalis antipyretica is growing at its “real” depth or whether it has been carried down by currents to rest in deeper water at or below its light compensation point. It did, however, prove possible to check the accuracy of diver-estimated zc values in a number of Scottish lochs where biomass or % cover had been measured in relation to water depth (Section VI): namely, with the point of intersection of the y axis (depth) by extrapolation of the straight-line logarithmic plot of standing crop. Values of zc obtained by this extrapolation lay within 3-7% of the estimates obtained by diving. It was concluded that underwater sampling like that from a boat can be inadequate but is less likely to be incorrect.

Where possible, diver-collected estimates of zc have been used in the examples set out in Table 3 but it will be appreciated that there remain unknown amounts of error in these data of mixed origin, and especially in the very deep examples. In summary, data for 36 lakes over 130 degrees of latitude indicate that zC ranges from less than 1 to more than 100 m. Tracheophyta do not penetrate beyond 12 m, Charophyta reportedly reach 65 m and bryophytes 120 m. The isolated position of Lake Tahoe and Crater Lake is emphasized in relation to other zc values; for example, of the 13 Scottish lochs in Table 3, 10 have a mean zc of 3.7 m, compared with a mean of 14.3 m in the three with the highest zc values. These frequency distributions, however, partly reflect the emphasis on the display of “record” depth zones colonized, and on giving examples for which comparable light data are available (Table 5).

C. Habitat and Zonation Variables Distinguished

The distinction between environmental factors varying solely in the vertical plane and those that have both vertical and horizontal components underlies the present analysis of causal distribution of macrophytes. Lack of such a


distinction in the past has probably contributed to the confusion between the roles of light and of substrate in controlling the distribution of these plants.

A few examples are first given to illustrate, at particular sites, vertical sequences of growth form or individual dominants in relation to gradients in water table which form the basis of the classification just outlined. The aquatic vegetation in Fig. 1 ranges along this gradient from woodland to submerged plant communities, while Fig. 2 maps underwater vegetation in part of Lake Windermere in what may be regarded as a typical series of zones along the depth contours. Figure 3 also represents underwater zonation, but as a transect down the south shore of Loch Borralie, Sutherland. The transect shows the usual restriction of angiosperms to water depths less than 6.5 m and a predominance of Charophya below this depth: indeed Loch Borralie is probably colonized by macrophytes to the greatest depth of any British lake.

Ppect Myrio spic Nitella-Chara Charo-Nitella Nitella Cham aspera Hippuris Pprae,pect Pprae ,pect (wintergreen ) beyond

Cham Hipp ,Cham -10 m

Colonized to 15m \

12 c Fig. 3. Zonation of submerged vegetation in Loch Borralie, as transect down the south shore, July 1975. (Horizontal scale about 1/10 x vertical scale.) Data collected, while diving, by the author. (P.pect = Potamogeton pectinatus, P.prae = Potamogeton praelongus, Myrio. spic = Myriophyllurn spicaturn.)

The principal vertical environmental variables are now distinguished. The most landward aquatic vegetation may be much altered by felling, cutting, burning and grazing, and such land use is depth-dependent because, for example, access of domesticated grazing animals is determined by the height of the water table. Also, periodic fires help maintain certain kinds of wetland vegetation and fen peat may be, or have been, removed for fuel. Within the

Table 3 Maximal depth of water (m) colonized by attached submerged angiosperms or vascular cryptogams in 37 freshwater lakes. The greater depth in any lake represents depth zone colonized by attached macrophytes, zc (m), in that lake. Data gathered by diver (D) or from

boat by grab (G). An expansion ot I able 5.6 in Spence, 1Y76, where notes are provided on many ot the British lakes listed.

Lake

~~~

Lake Tahoe, California

Crater Lake, Oregon Lake of Geneva, 1931 Lake Vattern, Sweden Lake Vrana, Yugoslavia Lake Latnjajaure, Sweden Lakes on south Georgia Lake Titicaca, Peru Lunzer Untersee, Austria Crystal Lake, Wisconsin

Loch Avon Loch Borralie Lake George, New York Loch Balnagowan Weber Lake Wiirmsee (Starnbergersee) Long Lake, Minnesota Wastwater

Maximal Maximal Genus (Charophyta or depth (m) depth (m) Bryophyta)

Angiosperm Charophyta (C) or vascular or cryptogam Bryophyta (B)

-~ ~

6-5 122 B 65 C

?b 120 B ? 60 B ? 40 C

7.7 38 C 11.0 32 B

30 B 11.0 29 B 6.0 25 B 4.0 20 B

(I -

- 15 B 6.0 15 C

12.0 15 B 6.5 13 B ? 13 B ? 12 c ? 11 c

6.0 12 c

Fontinalis and 5 others Chara Fontinalis Thamnium Nitella Nitella Marsupella Drepanocladus

Fontinalis Fontinalis, Drepanocladus

Sphagnum Nitella Fon tinalis Fontinalis Fontinalis, Drepanocladus Nitella Nitella Nitella

Data coll. by diver (D) or

from boat (G)

____

G

G G G G G D G G G

D D D D G G D D

Frantz and Cordone. 1967

Hasler, 1938 Monkemeyer, 1931 Stalberg, 1939 GolubiC, 1961 Bodin and Nauwerck, 1968 Light and Heywood, 1973 Tutin, 1940 Fuchsig, 1924 Fassett, 1930 Williams,

1930; Juday, 1934 Light, 1975 Spence, 1980, unpublished' Sheldon and Boylen, 1977 West, 1910 Spence, 1976b Juday, 1934 Brand, 1896 Schmid, 1965 J. W. G. Lund in litt.:

see Spence, 1976a

Table 3 (contd)

Lake Maximal Maximal Genus (Charophyta or depth (m) depth (m) Bryophyta)

Angiosperm Charophyta (C) or vascular or cryptogam Bryophyta (B)

Data coll. by diver (D) or

from boat (G)

Ennerdale Water Fureso

Wastwater Lake Bunyoni, Uganda Lake Mutanda, Uganda Loch Croispol Trout Lake, Wisconsin Derwentwater Lake Windermere

Loch Lanlish Loch Clunie Loch Uanagan Loch of Lowes Loch Spiggie Loch Drumore Lake of Menteith Esthwajte Water Loch Urigill Loch Leven

? 7.5

6.0 8.0 6.0 6.0 6.5 5.0 4.6

4.5 4.0 3.9 3.9 3.2 3.5 3.7 3.1 3.0 1 .o

10 c 8 C

8 B (6 C) (5 C) (3 C) (5 C) 6 C

5.7 c 7

(2.0 C) 4.3 c 4.1 C 3.9 c 3.2 C/B

(3.0 C) 3.7 c

(2.8 C) (1.5 C) 1.0 c

Nitella Nitella

Fontinalis Chara Chara Chara Nitella Nitella Nitella Nitella Chara Nitella Nitella Nitella Fontinalis, Nitella Chara Nitella Nitella Chara Nitella

G G

D G G D G G D G D D D D D D D D D D

Pearsall, 1918 Seidelin-Raunkaier and

Boye-Petersen, 1917 Spence, 1976a Spence, 1976a Spence, 1976a Spence, 1976a Wilson, 1941 Pearsall, 1920 J. W. G. Lund in litt. Pearsall, 1918. Spence, 1976a Spence, 1976a Spence, 1976a Spence, 1976a Spence, 1976a Unpublished Unpublished Spence, 1976a Spence and Allen, 1979 Jupp and Spence, 1977a

“ A dash means that angiosperms and vascular cryptogams are absent. * A question mark means that there is no information in the cited reference. ‘Supersedes 1 1 m in Spence, 1976; new figure based on 12 dives in different parts of the loch gave Z, of 12.4 m and a range of 1 1 to 15 m.

48 D. H. N. SPENCE

lake itself, vertical gradients occur in light, temperature, water density and pressure. Of these, it will be argued that light is the single most important factor .

Gradients in turbulent motion are also mainly vertical but, in the littoral, changes occur in turbulent motion and in sediment type which are only partly depth-dependent. Horizontal changes are imposed on these littoral depth gradients in any lake because sharp changes in turbulent motion and in sediment type can take place on different parts of a shore, at least in water up to a few metres deep. It will be argued that, like light, these factors also have profound effects on the distribution and nature of macrophyte vegetation in lakes. Figure 4 shows broadly how macrophyte zonation in shallow water varies with the aspect of a stretch of shore and with the prevailing sediments. For instance, the carr, fen and swamp at the west end of Loch an Ordain are similar to those at the west end of Loch an Choin, referred to earlier (Fig. l), but Loch an Ordain also provides an example of an exposed rocky shore with sparse submerged Lobelia dortmanna and Littorella unlpora in

Loch on Ordoin

open shore I

P proelonpus ~

Mynophyllum C rosfroto P norons

Sporgonium offine, Equisefum fluviofife

---

-60 0 100 200

*Scboenoplectus locusrris

)O cm

Fig. 4. Zonation of vegetation, represented by dominant species, in relation to summer water level in Loch Uanagan and Loch an Ordain, Inverness-shire. After Spence (1964). C = Corex, P. = Potomogeton and S = Schoenoplectus.


place of the Carex lasiocarpa swamp. From that part of the fen where the water table lies less than 20 cm below the soil surface, and on its rocky shore, Loch Uanagan resembles Loch an Ordain. Generally, one is comparing fen and swamp vegetation in sheltered bays with sparse, submerged vegetation on exposed rocky or stony shores.

All the given examples show how vegetation varies vertically down any shore while the examples discussed in the previous paragraph show how vegetation and gradients in any one lake can vary horizontally as well as vertically. An aim of this article is to find ways of distinguishing these vertical and horizontal components quantitatively.

11. HABITAT VARIABLES

A. Vertical Environmental Variables

1. Underwater Light Climate

PAR (see p. 124) is equated with light, or radiant energy of visible wavelengths, 400-700 nm, and the photochemical reaction involved in the conversion of phytochrome from the far red to the red form needs radiation at 730 nm. There now follow a few general observations about the underwater light climate. Firstly, underwater light has three components, sunlight, skylight and scattered light, the latter being produced by all beams projecting in natural water. Secondly, water is a predominantly shade habitat since it darkens as it deepens. The downwelling vector irradiance, E d (m-2 nm- l ) , of sunlight and skylight diminishes with increasing depth because of scattering and absorption. Following Beer’s Law, the decrease is logarithmic in an optically homogeneous medium. Thirdly, when viewed over the side of a boat or bridge on a bright day, and out of sight of the bottom, most waters seem to be flooded with light. This upwelling vector irradiance, E,,, results from scattering of sunlight and skylight. Fourthly, all natural water is coloured blue, green, yellow, brown or grey when, again out of sight of the bottom, it is viewed from above a surface that is non-reflecting or, when viewed underwater, horizontally. The next section examines these properties, shows how underwater light comes to vary in colour and clarity and outlines the relevance of these variations to macrophyte growth.

(a) Scattering and its effect on the colour of natural water. Scattering has three components: (1) light is deviated from rectilinear propagation (diffraction) by the action of particles; (2) light penetrates particles and can emerge with one or more internal reflections (refraction); (3) light is reflected by particles.

50 D. H. N. SPENCE

Diffraction is independent of particle composition while refraction and reflection vary with the refractive index of the particle. Particle size is the major variable in scattering. A particle scatters light if it is bigger than the impinging wavelengths and scattering is selective until particles exceed 700 nm in diameter. Thereafter scattering is non-selective.

In pure water, scattering is caused by water molecules and increases with the fourth power of the frequency, 04, or with the negative fourth power ofthe wavelength, K4. So blue light is scattered more than red and the clearest natural freshwaters like Crater Lake or Lake Tahoe in the USA are indeed blue (Fig. 5) . Clear calcareous freshwaters are green or blue-green, possibly because of selective scattering by CaC03 (Jerlov, 1968). As far as water colour is concerned, then, it seems likely that scattering is only important in very clear water.

,"""

5 95 metres

n

Wavelength ( n m )

Fig. 5. Downwelling spectral irradiance (pW cm-' n m - ' ) (37&725 nm) measured with submerged spectroradiometer at different depths in Crater Lake, Oregon. Data collected on 25 and 26 July 1969 under clear sunny sky in calm water. Elevation of the sun between 62" and 67". Data of Smith et al. (1973).

Turbidity or "muddiness" is caused by scattering from suspended silts and clays in water, although the term is also used of dense phytoplankton blooms (uiz. Westlake, 1966). In the main these inorganic particles act as neutral density filters or diffusion screens. Secchi disc transparency, measured as the depth at which a white disc 25 cm in diameter is just visible from the water surface, can show very good agreement with the turbidity of inorganic particles, estimated gravimetrically. This relationship is illustrated by the


calculated regression curves for eight widely separated lakes in Dokulil(l979, Fig. 15.6). Turbidity of inorganic origin is likely to be most significant as a factor in shallow lakes, specifically those where the bottom sediments lie wholly within the wave-mixed zone.

Overall, the biological importance of scatter centres on vision rather than on water colour per se, since it affects target or predator or prey visibility and colour contrast (Muntz, 1976). Even in clear coastal waters of the Moray Firth (Jerlov’s oceanic type 11) and in clear Loch Borralie on the Durness limestone, horizontal black body visibility in full sunlight is only 10 m, at water depths of 1.8 and 10 m (Hemmings, 1966; Spence, 1976a).

(b) Selective absorption: its effect on water colour. In its passage through water Ed decreases because of scattering and absorption by phytoplankton, epiphytes, macrophytes, dissolved substances and water itself. All but the clearest water becomes coloured through selective absorption and this factor predominates in inorganically turbid water.

Colour normally varies with the amount of dissolved and colloidal substance of organic origin. This “yellow substance” or “gelbstoff” consists of various heteropolycondensates of phenolic compounds, coupled by an oxida- tive polymerising mechanism (Christmann and Ghasseni, 1966; Hall and Lee, 1974). For present purposes, dissolved yellow substances represent about 95% total organic carbon (TOC), absorb strongly in blue and ultraviolet and may be assumed to be present in all natural waters (Hutchinson, 1957; Kalle, 1966; Jerlov, 1968). Kirk (1976b) estimated absorption coefficients at 440 pm (G440) of five lakes in south-western Australia, using absorption coefficients as a measure of concentration of yellow substance. Table 4 shows a seven-fold difference between the yellow water of Lake Gimminderra and the relatively uncoloured water from Cotter Dam, and Lake Gimminderra is 30 times more coloured than the sea in Bateman’s Bay. Absorption by dissolved yellow substances is, then, highly selective in short visible wavelengths. In all but a very few clear waters this selective absorption must exceed the combined effects of scattering of shorter wavelengths and absorption of longer wavelengths which is brought about by water itself, since yellow and brown freshwaters are the commonest types. Suspended particles in the form of phytoplankton also affect water brightness and colour because they scatter light and their chlorophyll acts as a selective light filter.

2. Attenuation and Attenuation Coefficients Light attenuation underwater results from its scattering and absorption and with radiation from sun and sky can be described as diffuse. In a homogeneous medium attenuation takes place logarithmically, a statement which can be verified by simple field measurement. Firstly, to describe what is measured as both vertical and diffuse light attenuation, the collector or sensor is placed

52 D. H. N. SPENCE

Table 4 Absorption coefficient (base-I0 logarithm) at 440 nm (G440) due to yellow substance in freshwater (first 5 samples), brackish water (Clyde River), the sea within Bateman’s Bay and the nearby open sea (the last figure, an estimate); South-eastern Australia. All samples taken between 13 May and 19 September

1974. Data of Kirk (1976b).

Water body G440 m-l

Lake Gimminderra 2.90 Burrinjuck Dam 1.57 Lake George 1.32

Cotter Dam 0.42 Clyde River (Nelligen) 0.38 Sea in Bateman’s Bay 0.08 Open sea beyond Bateman’s Bay - 0.01

Lake Burley Griffin 1.11

horizontally and has a corrected cosin response; also, through use of a collector above the water surface, allowance is made for variations in skylight and sunlight while attenuation readings are being carried out. In such conditions a semi-logarithmic plot of these readings, corrected for any surface variation, upon depth will quickly show significant departures from linearity; departures due to “surface errors” (Berger, 1961; Westlake, 1965) are avoided by taking readings only below 0.1 m, or deeper in very clear water. For example, a straight line was drawn through each of a series of semi-logarithmic plots relating surface-corrected readings of downwelling irradiance (400-700 nm) to depth; the readings were taken with a quantum sensor down a 6.5 m water column in Drumore Loch, Angus, at 14-day intervals over six months. The r values for these slopes, with five degrees of freedom, ranged from 0.833 to 0.951 and were all therefore highly significant (P. Chambers, unpublished data).

The slope of a truly linear plot of this type describes the vertical diffuse attenuation coefficient of downwelling irradiance, Kd. To estimate K d , values from this plot are substituted in either of the following formulae which are based on the negative exponential:

In I, - In z, I, = l o . ~ - K z or K, =

Z


where I, is the intensity at subsurface, I , the intensity at depth z(m) and K is the vertical diffuse attenuation coefficient m- l (for vector irradiance E ; p. 49), and E = the base of natural logarithms. Since readings are not taken in less than 0.1 m water depth, the semi-logarithmic plots are extrapolated to zero depth. The figure at zero depth is regarded as the true subsurface value (I,) and the data can be replotted as percentages of this value (Westlake, 1966).

(a) Range in quality of light underwater. When water colour and clarity are measured with selenium photocells and blue, green and red filters freshwaters fall into two classes (Table 5). For clear freshwaters like Ennerdale, Wastwater and Borralie which lie on hard, acid rocks or limestone, and lack peat, K B is always less than K R , and K R less than 0.45. There is little phytoplankton and allochthonous organic matter in such waters so that colour is determined by scattering. In the remaining freshwaters K B is greater than K R , presumably because there is more organic matter in the catchment or in the lakes themselves. K B increases as the amount of organic matter rises and K R always exceeds 0.45. Colour is determined by selective absorption. Light penetration has decreased compared with the first group and decreases throughout the series; that is, K G becomes greater.

Data for Loch Obisary and Loch Balnagowan (Table 5 ) illustrate these points. Loch Obisary is a brazkish deep-water loch in the Outer Hebrides, lying in a peaty catchment on Lewisian gneiss, and has a permanently stratified north basin, connected by a narrow inlet to the sea, and an unstratified south basin. In summer the unstratified south basin and the epilimnion above the thermocline and halocline in the north basin belong to the second group of waters where K B is greater than K R but in the saltier hypolimnion of the north basin K B is less than K R , as in the clearest, least organic freshwaters in the United Kingdom. This suggests that the higher K B value in the less salty waters of Loch Obisary is due to allochthonous organic matter in its freshwater inflows, a deduction strengthened by the far higher attenuation values, of K B particularly, throughout the loch in the wetter, winter month of January (Spence et al., 1979a). Loch Balnagowan on the limestone island of Lismore provides a less complex example (Bodkin, 1979). In August 1978 this loch was in the clear-water class with K B less than K R . A year earlier (sample 2) it belonged to the darker, brown-water class and in April 1978 the loch was even browner. While it is a solution lake, this loch has large fens at each end which, like the fens of Lawrence Lake, Michigan (Wetzel, 1975), are the source of allochthonous organic matter. The amount of organic matter presumably depends on the extent and duration of rainfall prior to the taking of light readings. Loch Borralie, another solution lake, has few such fens and remains clear throughout similar parts of the year.

The euphotic zone (zeu) in freshwater can be defined by in situ profiles of phytoplankton photosynthesis in relation to water depth. Its boundary

54 D. H . N. SPENCE

Table 5 Vertical diffuse attenuation coefficients, K d In units m- I , for downwelling blue ( K B ) , green ( K G ) and red ( K R ) light measured with appropriate Chance or Schott optical glass filters (see text) in a number of British lakes. Data taken from Spence, 1976a (Table 5.2, with citations) with additional data for Loch Balnagowan from Bodkin (l979), Loch Obisary from Spence et al. (1979a). Loch Urigill from Spence and Allen (1979) and previously unpublished data for Lochs Drumore, Fingask, Rae and

Stenness.

Lake or Loch Date K d In units m - K B K c K R

Stenness Loch an Eun Wastwater Ennerdale Water Balnagowan (1) Borralie

Croispol Borralie

south Derwentwater Uanagan Windermere South Balnagowan (2) Lanlish Esthwaite Water Clunie Lowes Drumore na Thull Balnagowan (3) Fingask Rae Obisary, north

south Urigill Leven Leven Urigill

June 1978 0.16 0.16 0.18 July 1979 0.14 0.12 0.33 June-September 1952 0.18 0.12 0.38 June-September 1952 0.25 0.1 3 0.3 1 August 1978 0.29 0.13 0.43 June 1971, 1972, 1974 0.29 0.16 0.42 March 1977 0.28 0.17 0.45 July 1977 0.30 0.19 0.40 June 1971, 1974 0.29 0.18 0.43 September 1977 0.36 0.26 0.44 July 1978 0.41 0.26 0.44 July 1978 0.56 0.26 0.36 July 1978 0.59 0.26 0.40 June-September 1952 0.47 0.32 0.42 July 1967 0.62 0.37 0.43 June-September 1952 0.66 0.35 0.58 August 1977 0.74 0.47 0.67 August 1974 0.77 0.36 0.56 June-September 1952 0.77 0.48 0.52 June 1967 0.84 0.46 0.47 June 1967 0.97 0.60 0.54 January 1976 1.06 0.40 0.56 June 1974 1.19 0.55 0.54 April 1978 1.23 0.94 0.95 January 1978 1.38 0.94 1.12 January 1978 1.46 0.65 0.69 January 1979 1.50 0.80 0.63 January 1979 1.65 0.97 0.68 June 1977 1.95 0.86 0.92 September 1974 2.01 1.07 1.04 August 1975 2.53 1.42 1.48 June 1978 2.85 1.65 1.10

coincides with the lower limit of net photosynthesis which, usually, is that water depth at which 1% subsurface PAR is found. The least absorbed wavelength, generally green, defines Kmin (In units m- l ) which in turn has been used empirically to define zeU. A relationship established by Talling (1971)


for waters of the English Lake District and Lake Victoria etc. in East Africa is:

zeU x 3*7/Kmi..

This factor compares with a factor of 4.2 derived by Balon and Coche (1974) for Lake Kariba and 4.8 by Dokulil(l979) for Neusiedlersee. Broadly, therefore, Kd for the least attenuated light may indicate the depth of the euphotic zone. Like Talling (1971) for Esthwaite Water, Bindloss (1974) demonstrated a correlation ( I = 0.84) for Loch Leven between Kmin and B, the phytoplankton density in mg chlorophyll a m-3. Where B exceeded 200 mg chlorophyll a m-3, phytoplankton absorbed more than 75% PAR. In certain circumstances (Spence, 1976a and this paper Section 1II.C) the depth zone colonized by macrophytes, zc, is also related empirically to Kmin:

ZC w 14/Kmin,

so measurements of Kd of the least attenuated light may also indicate the extent of zc.

A Leven I b..

I I I I I I 400 500 600 700

X(nm)

Fig. 6. Spectroradiometrically determined vertical diffuse attenuation coefficients of downwelling irradiance (Kd loglo units nm-') for named lakes. Data for Loch Leven, Blelham Tarn and Crater Lake redrawn from Spence (1976, Fig. 5.2), those for Blelham Tarn and Crater Lake being derived originally from Talling (1970) and Tyler and Smith (1967) respectively. Data for Loch Borralie, converted to log,, basis for comparison, from Spence (1981).

56 D. H. N. SPENCE

3. Underwater Spectral Intensity

A spectroradiometer, which measures spectral intensity ( p W cm-2 nm- l ) ,

allows a precise quantitative definition of the colour and amount of underwater light and is a useful method for estimating red and far-red irradiance. Scans made with a submersed spectroradiometer in one of the clearest of fresh waters, Crater Lake (Tyler and Smith, 1967), show more rapid loss of the longer visible wave-lengths with increasing water depth, and progressive monochromacity, in this case blueness (Fig. 5). It is probably more useful, however, to express these spectral features as the vertical attenuation coefficients of each wavelength, or Kd m-'. Regression lines of irradiance at 25 nm intervals in relation to depth, which were fitted to the data of Fig. 5, gave the plot of K d nm- ' upon wavelength for Crater Lake in Fig. 6. Scans taken at 1 m depth intervals with a submersed spectroradiometer provided

X l n m )

Fig. 7. Relative contribution of chlorophyll a (-0) and of yellow substance (.-. ) in Loch Leven during bloom of Synechococcus species (0.7-0.9 pm diameter), 19th June 1968. The yellow substance curve, with absorbance predominating in short waves, is that of a filtered, chlorophyll-free sample while the chlorophyll curve represents the filtrate to which 199 mg chlorophyll a m - ' has been re-added. Based on data of Talling (1970, Fig. 5).


the plots of Kd nm-' for Loch Balnagowan, Borralie and Leven (Spence et al., unpublished data).

In terms of such coefficients, Crater Lake illustrates the spectral selectivity of water itself while limestone Loch Borralie approaches these properties of water over longer wavelengths. Because of the least attenuation in short wavelengths, Crater Lake is blue and, with least attenuation around 550 nm, Loch Borralie is blue-green. Although its overall attenuation is higher, Loch Leven during a bloom has a similar curve to that of Blelham Tarn, also measured during a phytoplankton bloom. The presence of a bloom in each lake is signified by the attenuation increases at 665 nm, the in vivo absorption peak for chlorophyll a. The relative contributions of yellow substance and phytoplankton to attenuation can be gauged from Fig. 7, which is based on data of Talling (1970, Fig. 5 , p. 442), and shows that addition of 188 mg chlorophyll a m - 3 produces 4 times the shortwave attenuation due to yellow substance alone, with a large subsidiary peak at 675 nm. (For a theoretical analysis of the contribution of algal cells to light attenuation in waters see Kirk 1975a, b, 1976a.) These curves supplement the finding that phytoplankton at high densities in Loch Leven absorbed more than 75% PAR. Data in Table 6, derived partly from Fig. 6, emphasize the point that in clear, as in distilled water, FR is attenuated more rapidly than R and that, presumably as the amount of yellow substance increases, attenuation of both FR and R

rises, again more rapidly in the case of FR. At the limits of angiosperm occurrence (4 m) in Loch Uanagan, R irradiance at noon in summer was l op5 a surface value of 6 W m-* nm-' (Spence, 1976a).

An approximate figure for the range of PAR to be expected at a given depth between the clearest and intermittently darkest standing water in the UK is given by comparing the value of K p A R * (In units 400-700 nm) of 0-14 for Ennerdale Water, derived from optical glass filters and Emin (Talling, 1957), with a K P A R value of 2.9 for nutrient-rich Loch Leven during a dense phyto-

Table 6 Kd (In units m- l ) for R (660 nm) and FR (730 nm) irradiance in five Scottish lochs, calculated from measurements made with a submersed spectroradiometer (Bodkin

et al., 1980 Spence, 1981).

Loch Borralie Balnagowan Uanagan Black Leven Date 2 July 10 August 17 July 23 May 9 August

1977 1978 1970 1979 1975

660 nm 0.62 0.50 0.74 0.80 1.70 730 nm 1.07 1.38 1.88 3.37 2.10

* Called E p A R in Spence (1976).

58 D. H. N. SPENCE

Table 7 Integrated values of PAR, as p E m-2 s - l , at subsurface (0 m) and 1 m in Loch Croispol on 4 August 1970, in Loch Leven on 2 July 1970, with estimates of light energy entering, and being absorbed by, a horizontally positioned, fresh leaf of Potamogeton crispus (for

derivation of data, see Spence 1976a, pp. 99 et seq.).

pE m-’s-l Loch Croispol Loch Leven

~ ~

Subsurface 0 m 835 1155 l m 485 92

Entering leaf 480 90 Absorbed by leaf 351 63

percentage

43 5 Subsurface light energy Absorbed by leaf

plankton bloom; this value is based on integrated spectroradiometric data (Spence et al., 1971). These figures yield a 20-fold range which is a con- servative one because it lacks an example from extremely turbid water, e.g. Sauberer (1952) recorded KpAR of 18 during a storm in Neusiedlersee. Table 7 (from Spence, 1976a) shows that a clear leaf of Potamogeton crispus, lying in a plane parallel to, and at a depth 1 m below, the water surface would have available for absorbtion 43% of the subsurface irradiance in calcareous Loch Croispol (spectrally similar to nearby L. Borralie) but a mere 5% in Loch Leven during a moderate phytoplankton bloom.

Epiphytes reduce the light reaching a host’s chloroplasts, but the significance of such reductions for the host are difficult to assess because leaf senescence and epiphyte density may be positively correlated. Epiphyte demand may effectively increase the internal diffusive resistance for COa to the host’s chloroplasts so that an apparent light limitation may be a carbon limitation. However, Sand-Jensen (1977) has demonstrated that the reduction by epiphytes of Zostera marina photosynthesis in 1 a7 m-equiv 1 - HCO; was caused by shading at surface irradiances below 7.2 mW crn-’, that the reduction was linear and, at 0.44 mW cm-2, reached 58%. Sand-Jensen also notes that because photosynthesis of 2. marina was never light-saturated in winter in the Danish lake he studied, the shading effect of epiphytes was likely to be very important at the prevailing alkalinities.

In Neusiedlersee, surface radiation loss is high (mean 13.8%) because of considerable back-scattering due to turbidity, which is caused by wind disturbance of the sediments in this very shallow lake. Turbidity and windspeed account for more than 50% of the observed variance in the percentage albido (Dokulil, 1979).


Scattering

Another factor which reduces irradiance for evergreen plants in winter is the increased path-length of sunlight in water at low sun-angles in high latitudes but, as pointed out in Spence (1976a), there are good reasons for regarding the optical light path underwater as fairly constant and the result mainly of sky radiation and so for referring to vertical diffuse attenuation and its appropriate coefficients. Low solar angle may be more critical for reflectivity because, as Anderson (1952) has shown, for considerable periods on either side of the winter solstice in latitudes over about 57", almost a third of the total sun and sky radiation may be lost to the underwater environment. Factors affecting the light climate underwater are summarized in Fig. 8.

Absorbtion

solar angles and

Non-selective silts and clays

(particles phytoplankton >700 nm I

Selective yellow substances

< 700 nm )

and other plant surfaces

water molecules dissolved salts

Selective phytoplankton, epiphytes mocrophytes

yellow substances water molecules

Scattering predominant in controlling water colour

Scattering Absorbtion important predominant in controlling in controlling water colour water colour

coloured water,

KpARhigh-lowest+

granitic water yellow substances phyto- blue-green to green +phytoplankton plankton

dense - very low - increasing -high

60 D. H. N. SPENCE

4. Density Gradients, Thermal StratlJication, Pressure

In many lakes in temperate climates, heating in spring from low temperatures causes a separation of the water into the epilimnion, an upper layer of cir- culating, turbulent water, and the hypolimnion, which is a deeper, colder, relatively undisturbed layer. The zone of sharpest temperature change per unit depth between these layers is the thermocline. A lake with these three horizontal layers is thermally stratified; this may or may not be accompanied by chemical stratification in the concentrations of certain dissolved substances such as oxygen. Such freshwater lakes may be what Hutchinson (1957) calls “dimictic” or “monomictic”: that is, respectively, thermally stratified in summer and winter or in summer only.

The basic factors governing thermal stratification and the possible chemical consequences for nutrient exchange, for instance, between lake sediments and overlying water can be studied in a standard text like Hutchinson (1957). The occurrence of thermal stratification depends on the relative strengths of turbulent mixing and thermally induced density gradients. Given the sharp falls in temperature below the epilimnion during the summer in stratified lakes, questions of direct relevance to macrophytes are the stability of the epilimnion and whether its base does or does not extend below z,. There is evidence that steep temperature gradients are set up during summer amongst weed beds in shallow lakes (Dale and Gillespie, 1977) but no evidence that such localized stratification is connected, except in its physical nature, with any regular stratification of the main water body of a lake itself. If the epilimnion is stable and if its base lies at or above the macrophyte depth limits then a principle effect envisaged would be that of the limiting of growth by low temperature.

Pressure is directly depth-dependent and increases by 1 Atmosphere ( lo5 Pascals) per 10 m water depth. Evidence for the involvement of these depth- dependent factors in macrophyte distribution is examined in Section 1II.A. Of indirect relevance in the present context are the depth of the euphotic zone (zeJ and the epilimnion or turbulent, mixed zone (z , ) in relation to phytoplankton production, discussed briefly in the final Section.

B. Vertical and Horizontal Environmental Variables; Turbulent and Molecular Motion in the Littoral Water movement in the littoral presents a complex and important set of environmental factors for macrophytes in lakes. The motion of water in a lake varies from large scale turbulence involving almost all the lake volume to purely laminar flow very close to the lake bed or around plants attached


to it. In this Section I examine how these interacting factors influence the distribution of sediments and draw attention to ways in which they may also affect the distribution of plant cover. The aspects of fluid dynamics outlined here are those that deal with events relatively near surfaces rather than with details of water circulation in lakes, or other matters covered by, e.g. Hutchinson (1957) and Wetzel(l975). Introductory texts on which the present physical account is based are those of Monteith (1973) and Smith (1975).

1. Turbulent Motion

Turbulent motion, in which the applied force is wind or gravity, consists of mean motion or general flow in one direction with superimposed velocity fluctuations or eddies of varying intensity in all directions. This current flow is an order of magnitude greater than the fluctuations. Molecular motion is responsible for the transfer of momentum in moving water which is in turn responsible for viscosity, or viscous forces.

Windspeed withvelocity U acting in x direction -

Distance above lake bed ( 2 )

close to stationary surface of lake bed

Momentum transfer inducing

force

Force of current - acting on bed ( T~ )

Friction velocity

fffd =fi

Fig. 9. Transfer of momentum from moving water in a lake to an apparently stationary surface at or near the lake bed, and related forces.

In isothermal conditions, with a wind blowing on a lake surface to induce a current velocity U , the velocity of molecular movement will be similar at all distances above the lake bed, except very close to it. However, the horizontal component of velocity U in the x direction decreases with decrease in the vertical distance, z, above the bed. Because of molecular motion, a constant exchange of molecules occurs between adjacent horizontal layers with a corresponding uertical exchange of horizontal momentum. Such a transfer of momentum between adjacent layers of water produces viscous forces which tend to oppose changes in velocity (Fig. 9). These viscous forces are proportional to the rate of change of velocity with depth, dUfdz. At a

62 D. H. N. SPENCE

distance z from the bed, the viscous force per unit area, z, otherwise known as the shear stress or Reynold’s stress, can be written

where N is the eddy viscosity or coefficient of turbulent transfer (s m-2). The force of current acting on the lake bed is opposed by the frictional drag of the bed on the fluid. The friction velocity, denoted as Ufd, is a component of the current force which acts on the bed, while to means the stress exerted as frictional drag by the bed.

where p is the density of water. For particles of a given size and density, ufd determines the critical velocity at which bed erosion starts, a point returned to once some properties of waves and then laminar flow have been outlined.

(a) Waves. Free turbulent or wave motion is a particularly important aspect of the littoral environment for both macrophytes and lake sediment although, at present, there is virtually no quantitative information about the direct effects of waves on plant growth in lakes. Free turbulence is turbulent motion at an interface between two fluids of different densities and, on the surface of lakes, its typical feature is the formation of waves because fast air is moving over slower water.

Waves consist of oscillations of the water surface and wave form can be described as a curve traced by a point on a disc of radius r rolling on a horizontal surface. Crests travel at some velocity, c, the phase velocity or windspeed, in such a way that 2, (wavelength) equals c x t , the duration of one orbit, while H (wave height) is 2r. As water deepens, the orbital radius of waves below the surface decreases in a predictable way-for a wavelength of 1 m, an orbital radius of 20 cm at the water surface becomes 10 cm at a depth of 1 1 cm and 5 cm at a depth of 22 cm. Towards the shore in shallower water the circular orbits become elliptical and, near the bed itself, the water- particle motion is one of pure oscillation at constant level. Waves produce downslope flow or long-shore currents. These actions predominate in the wave-mixed depth (Fig. lo), which may be taken as equal to half the wavelength (Smith, 1979), and are discussed later in relation to erosion and sorting of bed particles.

2. Molecular Motion in the Boundary or Laminar Sub-layer

The bulk of water in a lake is subject to turbulence and, near the lake surface, waves. However, close to the lake bed and around plants there exists a


Fig. 10. water.)

Shore zone Deep woter : mo ormaynot

Wave incrude some of the mixed littoral zone

j Erosion and some deposition j Deposition only \ D

The influence of waves on lake shores (after Smith, 1979). (D = depth of

boundary layer where flow is not turbulent, is low, and cannot be detected by standard measurements of current velocity. This feature (Fig. 11) is caused by the existence of a thin layer of fluid near solid objects like rocks or individual plants protruding from the lake bed, or over the lake bed itself, where flow is entirely laminar and motion molecular.

Distance above lake bed z

Loaarithmic

I

/ _---

velocity profile

tronsit ion T profile

bulk solution

boundaryor laminar sublayer

Velocity u acting in x direction

Fig.11. Velocity profile in a lake with reference to type of flow and to Reynold's numbers.

A relationship between turbulent and laminar flow is provided by the Reynold's number, Re, which expresses the ratio of inertial forces in a fluid (producing changes in velocity) to viscous forces (tending to oppose changes in velocity). With a small ratio or Re, viscous forces predominate so that flow tends to remain laminar but, when the ratio increases beyond a critical

64 D. H. N . SPENCE

value, inertial forces dominate and the system and flow become turbulent.

Re = ~ L / v

where is current mean velocity down the velocity/depth profile, L is a characteristic length dimension, say depth above bed or z in a well-mixed lake, and v is kinematic viscosity, or fluid flow without reference to force. Flow is definitely laminar where Re is less than 500, definitely turbulent where R, exceeds 2000 and between these numbers flow is transitional (Fig. 11).

The laminar sub-layer or boundary layer is termed 6. The usual expression for 6 involves shear velocity, U f d , and kinematic viscosity, v:

6 = 11.5 v /Uld .

A mathematical treatment of boundary layers in lakes is given by Bretscheider (1952). Here it is noted that, while the thickness of 6 is influenced by the shape and roughness of the solid surface, it also depends on flow conditions. Table 8 gives anexample of the dimensions of 6 on a bed relative to current mean velocity U . To derive this relationship between 6 and U , a mean ratio of E/U,-, of 20 has been coupled with the expression for 6 given above (Smith, 1975).

Table 8 Relationship between mean velocity, 0, and the thickness of the laminar sub-layer,

6', in rivers. Water temperature 15°C (from Smith, 1975).

0 (cm SKI) 1 5 10 50 100 6' (mm) 27 5.4 2.1 0.54 0.21

The significance of boundary layers and laminar flow for plants centres on questions of mass transfer across this layer between the bulk solution and the inner wall of the leaf epidermal cells. Mass transfer is also important in some circumstances between sediment surfaces and overlying water. Laminar flow is involved in the movement and deposition of finer particles and it is this aspect about which the most relevant information is available.

Rate-limitation of photosynthesis of macrophytes is likely to occur frequently in relatively deep and therefore still water as a result of the development of large boundary layers over leaves, especially since C 0 2 diffuses lo4 times more slowly in water than in air. For a given boundary layer thickness, such limitation will be most severe in poorly buffered waters with, that is, low total carbon concentrations. Calculated diffusive resistance of isolated leaves of broad-leaved Potarnogeton species to C02 fixation in well-stirred solutions at low pH is about 2500 s cm-', with thickness of the boundary layer of about 300 pm (Black et al., unpublished data). These values compare


with an estimated diffusive resistance of 20 s cm-' for leaves of a terrestrial mesophyte, Impatiens paroijlora, in well-stirred air (Rackham, 1966) and 48 pm for the boundary layer of the submerged macrophyte Egeria densa (Browse et al., 1979).

It seems likely that flow within dense weed beds is laminar, a supposition borne out by the records of very steep temperature gradients within such beds made by Dale and Gillespie (1977). However, no observations appear to have been published on laminar boundary layers in or above submerged weed beds, in lakes, and it is impossible to say anything that might have a bearing on zonation.

For a number of years, more has been known about the extent of boundary layers overlying sediments in the hypolimnion of stratified lakes and, in particular, the significance of this layer when the redox potential of the mud surface is sufficiently low to allow nutrient release into the water above (Mortimer, 1941, 1942). Such eutrophic lake processes, however, have little direct relevance to macrophyte zonation, although they may help to determine zc: see Section VI.

(a) Criticalerosion andsettling velocities. Of more relevance to macrophytes and zonation are the velocities which start movement of shore material or bed particles, and their settling velocities. An approximate relationship between particle size and the critical velocity for the onset of erosion of material of uniform density (2.65 g ~ m - ~ ) is shown in Fig. 12 (from Sundborg, 1956). The limits for consolidated or cohesive clays and silts are very uncertain,

'\_Consolidated clay and silt

qoc Unconsolidated clay and silt

I I I I I I 0.001 0.01 0.10 1.0 10.0 100 1000

Groin diameter ( m m )

Fig. 12. The critical velocity for the onset of erosion of uniform material of density 2.65 g cm-3. The solid line refers to velocities measured at a height of 1 m above the bed and the dotted lines indicate the limits of the critical erosion velocity. After Smith (1975), from Sundborg (1956).

66 D. H. N. SPENCE

while unconsolidated clays and silts may be eroded at lower limiting velocities than those indicated.

The critical erosion velocity of organic matter of density 1.05 g cm-3 will be even lower. Smith (1975) points out that the stresses at the onset of erosion will be in the ratio (2.65-1.0)/( 1.05-1.0): that is, under identical conditions, organic matter is moved by a stress 1/33 that required by a mineral particle of the same size and shape. Since -= ufd and u/ufd is constant at constant velocity, the critical erosion velocity for organic matter is a or almost 1/6 of that of mineral particles. So a stable bed of organic sediment with particles which, for the sake of argument, are the same size as mineral particles must occur at 1/6th of the current which permits a stable mineral bed.

From the previous paragraph it may be concluded that, on any one shore, a stable bed of organic particles always occurs in deeper water than a bed of similarly sized inorganic particles. In shallow water on two different shores, the organic particles will only be found (if at all) on the more sheltered one. The whole question of erosion, deposition, turbulent and laminar flow can be looked at in terms of particle Reynold’s numbers.

The particle Reynold’s number is defined by:

Re = V,d/v

where V, is settling velocity, d is diameter of particle and v is kinematic viscosity. If particle Re is less than 0.5, flow around a falling particle is entirely laminar and V, follows Stokes’ Law governing rates of sedimentation. As particle Re increases above this value flow becomes entirely turbulent. Data in Table 9 (from Smith, 1975) illustrate some of these relationships for particles of sp. gr. = 2.65.

3. Erosion, Sorting and Deposition in Lakes

The relationships established in preceding paragraphs are now applied to the development of lake shores and aspects of plant cover. Two important

Table 9 The relationship between the size of spherical particles (diameter cm), their settling velocity ( V s ) and the particle Reynold’s number (Re) (sp. gr. 2.65). Water temperature

15°C. Based on Smith, 1975.

Particle diameter (cm) < lo-’ 10-2 lo-’ 1 10

cm s - ’ (Stokes’ Law) 1 10 50 100 Particle Re (sp. gr. 2.65) ~ 0 . 5 1 102 103.5 105

Wentworth Silt Very fine sand Coarse sand Pebbles V,: settling velocity


effects of waves and long-shore currents are erosion, or the onset of movement of bed particles, and sorting or elutriation, which leads to in situ deposition, and down-shore transport and deposition. Substances in a lake upon which waves act in the process of erosion vary in size from bare, jointed rock surfaces to previously deposited or weathered clays and silts, and erosion occurs because of wave-cutting and fragmentation across the axis of mean motion. In lakes in temperate climates which are subject to annual freezing, wave action in the shore zone may be augmented by ice-scouring.

A beach is cut and particles are eroded when subjected to their critical erosion velocities; they are then sorted-a combination of wave action, turbulent mixing and longshore currents. The greater the wave height the larger is the orbital radius of the wave and the larger the particles displaced. Heavy material down to 10 cm diameter is deposited in situ; or lifted up the beach, in extreme examples as on parts of the east shore of the Bruce Peninsula, Lake Huron, or the south end of Loch Ness forming a storm beach of boulders. Finer material, less than 10 cm in diameter (Re -= lo’), is carried out and deposited in deeper water by longshore currents. Governed by their respective settling velocities (Table 9), pebbles are carried the least distance, coarse then fine sands rather further whilst silts, clays and, finally, organic particles, travel furthest and are deposited under progressively deeper water. Thus particles in sediments usually become finer with increasing distance from the lake edge and with deepening water.

Smith (1979) noted that the wave-mixed depth which also defines the shore zone may be taken as equal to half the wavelength (Fig. 10). Also “the lower limit of the wave-distorted depth, or wave-mixed zone, on any shore would seem to be defined by the depth at which orbital velocity due to wave action equals the vertical velocity fluctuations of the current flow”.

Indirect evidence for the existence of downslope flow, induced by wind and longshore currents, over a submerged weed bed is provided by the direction in which shoots were found to be laid over a range of depths on 15 September 1975 in Loch Borralie (Fig. 13, from the author’s unpublished data), Solid arrows in that diagram indicate the direction of “lie” recorded, while diving, by means of an underwater compass. Dense vegetation starts on this shore at 2.5 m, the probable base of the wave-mixed zone, and penetrates to more than 12 m depth of water (Fig. 3). The dotted arrows on the “wave-mixed zone” are conjectural. Wind on the sampling and preceding day was light south-westerly and it is assumed that the vegetation, perhaps like a laid cornfield, continued to show evidence of a surge or surges from an earlier gale, in this case from the north-west.

Returning now to the question of particle sorting. On gentle slopes facing a long fetch, where fetch is the distance a wind has blown uninterrupted over open water, particle sizes are likewise gently graded. On steeper slopes,

68 D. H. N. SPENCE

Bare or sparse veg Liltorelfa Pot f i l inshallow water with more, short Chora aspero in deeper

approx 5 0 m

I // /’

I // /’ // I ; //’ /’ 2 5m

Po!omoge!on ___---- Om praelongus err

-135’

A /------- 6 5 m Cham-Nitella

possible causal wind direction 1 N -=T- 6-

Fig. 13. Evidence for the existence of downslope flow, induced by wind and long-shore currents, affecting the direction in which shoots of submerged macrophytes were laid in Loch Borralie on 15th September 1975. Wind was light, south-westerly at the time of sampling. Unpublished data of the author. Pot. fil. = Potamogeton,filiformis.

terracing develops. Sand cut from the beach is deposited among coarser particles, with little lakeward movement, to form the littoral shelf; beyond and below lies the bottom mud, deposited on the original unaltered lake basin (Fig. 14). Terracing is an extreme expression of the sorting effects of waves; terraces form the longest composite shoreline in UK freshwaters and, it is reasonable to suppose, in freshwaters generally.

Size of lake, and aspect of shore. Around the edge of a lake where the depth of water is less than half the wavelength of waves, the “shore” zone, erosion caused by wave action is likely to be more severe than that due to any current flow. As I shall show, the critical question in relation to the depth zone colonized by macrophytes on any shore is the depth of this wave-mixed zone (zw). The extent of zw depends on the aspect of that shore and, in turn, on lake size.

The height of the highest waves observed in a lake at a given windspeed appears, without a good theoretical explanation, to vary with the square root of the fetch of the waves. Thus the maximum height

H=kJF

where k = 0.0105 and F = fetch (m) at the point of measurement downwind. The maximum height observed in Lake Superior was 6-9 m with a fetch

THE ZONATION OF PLANTS IN FRESHWATER LAKES

Wave-mixed zone - Erosion and in Deposition ond Bottom or profundal sifu deposition some erosion sediment

69

Fig. 14. Erosion and depositional areas along a wave-cut terrace, littoral shelf and the start of bottom sediment, and the decreasing particle-size on the depositional areas as distance from the shore increases. This change is quantified in terms of particle Reynold’s numbers (Table 9).

of 482 km and this agrees well with a maximum of 7.3 m derived from the equation (Wetzel, 1975, p. 95 who gives k = 0.105). But fetch varies with the width of the water body and with irregularities of shoreline as well as with its length; to account for such effects, Bretschneider (1952) proposed the use of a “weighted mean fetch” and Smith (1979) gives a simple method of computing this quantity for a given wind direction and shore. Approximately, however, as area and depth of a lake increase so do the maximum height of the waves breaking on the shore and the depth of the wave-mixed zone; also, the greater does the length and depth of the lake shore occupied by the wave-mixed zone become, the more exaggerated is the difference between these exposed shores and the less common sheltered shores.

Whenever a body of water becomes large enough for strong development of waves, the aspect of any shore assumes importance because it may modify erosion and sorting effects through diminishing I and H values and the onset of movement of bed particles. For example, the sheltered south-west shore of Loch Maberry possesses fine-particled sediments which occur several metres deeper on the exposed north-east shore of the same lake (Fig. 15). That sheltered shore also possesses a more diverse flora and much more plant cover, which approaches 85% at a water depth in which the exposed shore has less than 5%.

70

-

- Silty Sandy Sandy Silty mud mud mud mud - -

D. H. N. SPENCE

100

200

300

Outline m a p o f Loch Moberry Sect ion A

'7 j'.o ( c m )

lsoetes Littorella

200 Mud Rocks Sand and gravel

"/o plant 80 nil 5 nil cover of soil surface

( c m )

c o v e r a t soil surface

Fig. 15. Outline map and transects of portions of the shores of Loch Maberry (horizontal scale about 1/7 x vertical scale). Note (1) a broad correlation between soil- particle size on a shore and its likely degree of exposure to wave action; (2) the absence of emergent and floating-leaved vegetation from relatively coarse-particled, and exposed, shores; (3) a roughly inverse relationship between the size of soil particles and the percentage total plant cover at the soil surface. After Spence (1964).

C. Conclusions; Effects on Sediment and Plant Distribution

Eventually it may be possible to relate the critical erosion velocities and settling velocities of mixtures of particles on a given shore to the amount and type of plant cover they carry, bearing in mind the possible adaptive significance of different growth forms of both shoot and root (a point returned to in Section V). Simple methods already exist (Smith, 1979) for establishing the depth of the wave-mixed zone on any shore and, like the contrasted examples in Loch Maberry, this could be studied with particular reference to the vegetation.

The observation that plant cover on the sheltered shore of that lake is obviously more species-rich and more extensive than on the exposed one is qualitative. Indeed, just as no data are available on laminar sublayers in the weed-beds of lakes, neither do measurements exist of critical erosion velocities below which any macrophyte cover can be established or maintained; nor of features of waves which deform shoots and leaves as well as causing


frictional stress on them, nor on the ability of roots to remain anchored. Recently, however, Haslam (1978) has attempted to measure responses of shoot and root-systems of river plants to physical factors which together amount to “turbulence-tolerance” and which are discussed for some river plants common to standing waters in Section V.

Qualitative interpretations of some interactions between exposure, sediment and plant cover are made in Section 1II.B. Here it is concluded that, following any shore from shallow to deep water, one crosses the wave-mixed zone where erosion, sorting and some deposition occur and one enters the purely depositional, and most fine-particled zone. Rarely, the wave-mixed zone is absent. The depth and breadth of each zone depends on the slope and aspect of the shore and on the lake size, principally its fetch. An exposed shore may be entirely wave-mixed, with few plants, while a sheltered bay in the same lake may have a depositional shore with continuous and more diverse plant cover. It is inferred that the existence of dense macrophyte cover in lakes depends on the absence of wave action.

111. CAUSAL ANALYSIS OF WITHIN-LAKE DISTRIBUTION AT ANY INSTANT OF TIME

A. Vertical Zonation

I . Emergent Vegetation

The upper end of these water-depth gradients-swamp-forest, carr, fen and reedswamps- have been subjected over large areas of the world to tree-felling, clearing of scrub, draining, peat-cutting, reed-cutting or grazing, usually by cattle. Many of the East Anglian Broads are mediaeval or earlier peat-cuttings which have subsequently been flooded (Lambert et al., 1960). Phragmites communis is cropped for a variety of economic uses in the Danube delta, around Czechoslovakian and Hungarian fish ponds, on the Norfolk Broads etc. (Dykyjova and Kvtt, 1978; Haslam, 1972, for example). This species is also very susceptible to trampling and grazing. On unenclosed areas in the United Kingdom it can be trampled, grazed and eliminated by cattle from all ground drier than swamps; it only survives unenclosed where the water table is too high and the substrate too unstable for cattle to tolerate (Spence, 1964). In these latter examples Phragmites is replaced by Juncus species and Carex nigra and it seems likely that the prevalence of groups of communities dominated by these and related species in damp or waterlogged sites around lake shores all over upland Britain is the direct result of trampling and grazing, in some places since Neolithic times (Spence, 1979). Also, periodic fires may

72 D. H. N. SPENCE

be important in maintaining certain kinds of wetland vegetation: e.g. the open pine savannas, with many associated herbs, in the south-eastern United States (Godfrey and Wooten, 1979). But these and other modifications constitute a topic within themselves and examples have only been given here to draw attention to the existence in this habitat of anthropogenic factors as far- reaching in effect as any of the more obvious edaphic factors.

Of these edaphic factors, the degree of soil aeration during the growing season in swamp-forest, carr and fen may be particularly important, coupled with the degree to which plants can aerate their root system and/or employ metabolic devices to counter the normally toxic effects of anoxia. Aeration problems are likely to be aggravated by insufficient turbulence or overlarge laminar sublayers around roots. It is clear that many species in these habitats are well-endowed with aerenchyma (Arber, 1920; Sculthorpe, 1967), or have developed metabolic adaptations to anaerobiosis (e.g. Laing, 1940a, b; Hood and Crawford, 1978; Smith and ap Rees, 1979; and reviews by Crawford, 1981, 1982).

The root systems of some species like Phragmites, which dominate in ungrazed fen and in swamp, can be either seasonally or permanently submerged and thrive in either situation. The root systems of other emergents, such as Schoenoplectus lacustris, or of floating-leaved plants like Nymphaea alba or Potamogeton natans are in general permanently submerged. In winter, when shoots and leaves are dead, such plants are indistinguishable in habit from fully submerged species with overwintering organs under water and soil, like Potamogeton perfoliatus or P. richardsonii. Their roots will suffer a seasonal loss of oxygen supply from their shoots and their rhizomes etc. must be able to resist flooding when shoots die back.

No experimental work appears to have been done on what determines the limits of beds of emergent (reedswamp) species in deep water. In this context, reference is made to an experiment involving seeds of Phragmites cornmunis sown outdoors in winter (Spence, 1964, p. 341). The seeds were sown in various sediments with constant water tables lying just below and up to 15 cm above the sediment surface. Germination did not occur the following summer on any sediment held under more than 5 cm depth of water. This suggests that seeds of P. communis have a much lower flooding tolerance than whole plants, that P. communis swamps must be the result of vegetative spread, except in the shallowest water, and that environmental limits on this spread, rather than on germination and seedling growth, determine the greatest depth of water in which the species can grow.

Given vegetative reproduction in deeper water, suitable sediments for colonization and a (related) absence of wave-induced turbulence, limits for emergent species may be set by susceptibility of perennial parts to water entry from dying shoots which is enhanced by higher pressure: or limits may be


set by insufficient overwintering carbohydrate reserves to sustain shoot extension through deep water in spring. The last assumption implies inadequate translocation from shoots rooted in shallower water. Some explanations are offered in Section V.B in terms of possible morphological adaptations and include a reference to light requirements for seed germination.

2. Submerged Vegetation

Angiosperm and vascular cryptogams (Tracheophyta) penetrate fresh waters down to depths of 12 m. Their more usual maximum is less than this: indeed, for the 36 lakes of Table 3, the mean value for depth limits of angiosperms and vascular cryptogams is 4.6 m. Charophyta penetrate to 65 m and bryophytes are reported to grow at depths of 120 m in very clear water.

There are two interrelated questions: (1) what factors limit depth penetration of members of the Tracheophyta; and (2) what controls the overall depth penetration of macrophytes? The possible environmental factors involved in influencing these limits are summarized in Fig. 16.

(a) Temperature limitations. Pearsall(l920) concluded that temperature did not limit the downward penetration of water plants in the English Lakes and, with the possible exception of Loch Balnagowan in Lismore, Spence

I ~ &q&, I toounstoble too rocky

I u

factor of macrophyte

Pressure 1

hydrostatic pressure limits angiosperms at water depth of 6 m (sea level) even in very

Fig. 16. Possible factors influencing lower depth limits of freshwater macrophytes. In this diagram a standard zc is assumed in terms of underwater light climate.

74 D. H. N. SPENCE

(1964) reached the same conclusion with respect to macrophytes in Scottish freshwater lochs; either the lakes are unstratified, at least in summer, or else the epilimnion extends many metres below the lower limits reached by attached plants.

In Loch Balnagowan, a steep-sided solution lake on limestone, there is some evidence that vegetation limits in deeper water are set by low summer temperatures associated with layers below the epilimnion. As determined by diving, continuous vegetation and angiosperm growth around the loch cease at a depth of 6.7 m (Fig. 17). Below that contour at each end of the loch, plant cover is composed almost entirely of Fontinalis antipyretica which decreases from about 50% at 6.7 m to less than 1% at 14 m, the limits of Fontinalis and macrophytes in this loch. No vegetation at all grows along

Maximum

HlppUrJS with Poforno nofans (at4 5rn deoth 1

1 Choro 1 Fanfinals papilloro with fpure some stands PofpuSlIh

Slope

Fig. 17. Sketch of zonation at the south end of Loch Balnagowan, August 1974. Data collected by diver. Between 0 and 6.7 m, the depth limit of angiosperms and of continuous plant cover, the boxes represent the various community types encountered round the loch end. Unpublished data of E. D. Allen and the author.


the steep sides of the loch below 6.7 m which could imply that, compared with the ends of the loch, the sediment has too unstable an angle of rest. 6.7 m is also the depth at which the base of a well-defined epilimnion lay on 12 August 1904 (Murray and Pullar, 1910) and on 23 June 1969 (Spence, 1976b, Fig. 6) but no stratification occurred in August 1974 or August 1976 over 15 m depth ofwater (Allen et al., unpublished data). Although apparently unstable during summer, temperature stratification is the most probable reason why the lower limit of continuous plant cover lies at 6.7 m.

In Lake George, New York, the depth of colonization by vascular plants was found by diver to coincide precisely with the base of the epilimnion in August, or 12 m (Sheldon and Boylen, 1977). Over this period the authors report that light intensity at 12 m was 10% of surface values. It is still possible that low temperature rather than light was limiting angiosperm growth in the deeper water of this lake. Apparently low temperature was not limiting Nitella flexilis to the same extent since this charophyte continued to form beds from 12 down to 15 m, which constitutes the macrophyte depth limit. While 1% surface light intensity still existed at 18 m, according to Sheldon and Boylen, it seems likely that the lower limit of Nitella and therefore of macrophytes in this lake are set by underwater PAR.

A third example is provided by data, again collected by diving, from Mirror Lake, New Hampshire (Moeller, 1980). This oligotrophic, clear-water lake is dimictic, or thermally stratified in summer and winter. Utricularia purpurea, an unattached submerged plant which can be moved around by currents, is a typical species of Mirror Lake and Moeller found that it did not grow there below 6 m of water. Through in situ measurements of extension growth, carried out on plants artificially attached to transects at selected depths, Moeller concluded that temperature stratification limited the species’ growing season to eight weeks at this depth compared with 17 weeks at 2 m depth. Low light did not depress growth at 4 m but it might interact with low temperature to depress growth at the species’ depth limit of 6 m.

Several sets of diver-collected data therefore indicate that low summer temperatures may limit the downward penetration of angiosperms beneath the intermediate and final depths at which the base of epilimnia occur in clear-water, stratified lakes.

(b) Substrate limitations. Unsuitable sediments for rooting may limit colonization even when light and temperature can be deduced as adequate for growth. Like the sides of Loch Balnagowan, just mentioned, Loch Croispol on the Durness limestone also seems to have unstable sediments that limit zc. Between 3 and 6 m depth of water there is a steep mud slope which supports a sparse plant cover of mainly tall Potarnogeton perfoliatus on an otherwise bare substratum. Most of the shore of the neighbouring Loch Borralie slopes more gently and the sediments there from 2.4 to 6 m bear rich beds of angio-

76 D. H. N. SPENCE

sperms, with an understorey of Chara and Nitella species, and the stoneworts persist to 15 m depth in places (Fig. 3). Both lochs have water with similar optical properties and are unstratified over at least 15 m, so it follows that zE in Loch Croispol is limited by a substrate effect such as too rapid a rate of sedimentation on its steep slopes (and see Section 1II.C). The littoral zone may also be uncolonized where boulders predominate to depths below those at which growth can occur on adjacent finer-particled shores, e.g. Loch Urigill (Fig. 18).

Aspect-I Point I Open I Bays shore exposed sheltered

Predominant substrate

Em = CZI 0

Plant

I0

L O

I

L

S

P

Boulders, stones

Gravel

Sand

Mud

cover

open lsoefes

open Liftorella

dense lsoefes ( to 30% cover)

dense Liffore//a

Schoenoplectus lacusfris

Pofamogefon spp mainly

P perfohatus, Ppraelongus

Pnafans locally, between

1 5 and 2 7 m

Chara, Nitella

Fig. 18. Zonation of mainly submerged vegetation in Loch Urigill in relation to exposure and type of substrate. Data collected by wading along shore and by diving in three separate parts of loch in July 1977 and 1978. The nine resulting transects are arranged from left to right in terms of progressively shallower water depths at which colonized sediment can accumulate, which is inferred to indicate decreasing free turbulence. After Spence and Allen (1979).

(c) Limitations due to pressure or to light. Until very recently, the increasing atmospheric pressure which accompanies increasing water depth has been considered a limiting factor in the downward spread of members of the Tracheophyta in fresh water, although an angiosperm like Posidonia oceanica in the Mediterranean (Gessner, 1959; Drew and Jupp, 1974) reaches, at 40 m, more than three times the depth of any angiosperm in fresh water. The case for the prime importance of pressure for freshwater angiosperms relies heavily


on experimental evidence of Gessner (1952, 1955) and Ferling (1957), and on some distributional evidence from lakes in various parts of the world. Gessner studied the growth of cut shoots of Hippuris vulgaris in closed bottles under pressures of up to 2 atm. With the unspecified levels of illumination, shoot diameters were reduced at 1.5 atm but the rate of shoot extension was unaffected until pressure reached 1.75 atm, whereupon growth ceased, which corresponds to a water depth at sea level of 7 m.

Let us look at depth limits where neither low temperatures nor unsuitable sediments are involved, as for Hippuris uulgaris at 6.5 m in the clear, unstratified water of Loch Borralie (Fig. 3). Stems collected at this depth are as thin, and have the same proportions of lacunar and non-lacunar tissue, as those subjected to similar pressures by Gessner. In the even clearer waters of Lake Vrana, Yugoslavia, Golubii: (1961, 1963) established the angiosperm depth limit at 7.7 m (Charophyta reaching 40 m in some years). Golubii: reported that the laboratory-determined light compensation points of two of the main species of Chara was 1.6 times those occurring at their depth limits; for Myriophyllum spicatum the discrepancy was near 4.7. (In addition, M. spicatum did not occur in the lake at a depth receiving less than one-quarter of PAR incident on the lake surface.) It was deduced that low light was an unlikely limiting factor although extrapolations from laboratory compensation points are doubtful; temperature too was discounted because the lower limit of the epilimnion lay at 10 m. At the angiosperm depth limit of 7.7 m, pressure is 1.8 atm, experimentally determined as limiting growth of H . vulgaris, and GolubiC concluded that this is what limits M. spicatum in Lake Vrana.

The coincidence in clear waters of the maximal depth of penetration by angiosperms with a pressure at sea level of less than 1.8 atm, and the experimental evidence for effects of pressures of these values on growth and anatomy may seem strongly to implicate this factor in producing a limit to growth in the natural environment. Hutchinson (1975) also points out that the occurrence of angiosperms at 1 1 m in Lake Titicaca can be explained on the basis of reduced atmospheric pressure at the altitude of this lake (3815 m), equivalent to 7.5 m at sea level.

Recently, however, Sheldon and Boylen (1977) found by diving that several angiosperms grow in low-altitude Lake George, New York State, at 10 m with Elodea canadensis reaching 12 m, and further doubts about the role of pressure are raised by the work of Bodkin (1979). Like Gessner, Bodkin studied effects of pressure on H . uulgaris but he also looked at interactions with PAR. This species reaches a depth of 6.5 m in Loch Borralie and Loch Balnagowan. In the laboratory, H . uulgaris shoots were rooted in chambers, bathed in bicarbonate-enriched solution, and then subjected to additional pressure of 1 or 1.8 atm at a range of PAR in an 8 or 16 h day and tem-

78 D. H. N. SPENCE

peratures of 5 or 15°C. It was found that plants in a 16 h day, at 15"C, and receiving at least 140 pE s - ' m-' PAR, achieved normal shoot elongation and diameter, even though they were held at 1, 1.8 or 2.3 atm, equivalent to water depths of 5 m, 8 m, and 13.3 m. Lacunae in shoots grown at 2.3 atm were as large as those in control shoots, implying that pressure does not restrict air spaces. Both lower PAR and temperature inhibited growth. It may be noted that on a clear day at noon in midJune, PAR at 6.5 m in Loch Borralie was 100 ,uE s - ' m-2, which must be a maximum in a lake of which the water is always plankton-poor and relatively free of yellow substance (Fig. 6).

In summary, underwater plants of H. uulgaris growing at their lower depth limits of 6.5 m typically produce short, thin shoots and such effects have hither- to been attributed to pressure exerted by the overlying water column at these depths. It has now been found that underwater plants of this species grew normally at their natural summer temperatures, and when subjected to pressures the same as or greater than those exerted by the water column at their depth limits of 6 5 m, but only if levels of PAR were about the same as the maxima to which the naturally occurring plants are known to be subjected at these depth limits. In other words, inadequate PAR rather than excess pressure sets the lower depth limit of the angiosperm H. uulgaris.

( d ) Relationship between zc and Kmin. Field data are now examined which attempt to relate the depth of the zone colonized by macrophytes to light levels underwater. Maristo (1 941) established a linear correlation between the transparency of 27 Finnish lakes, measured with a Secchi disc, and zc. Mosses reached the greatest depths in 17 of the lakes, in 10 cases the species being Fontinalis antipyretica and Drepanocladus sendteri. Spence (1976a) demonstrated that zc x 1.4/Kmi. in eight British lakes where phytoplankton density never exceeded 20 mg chlorophyll a m-3 in any year. In a second group of lakes, phytoplankton density had a far greater annual range, and reached much higher maxima-up to 250 mg chlorophyll a m-3, and zc is unlikely at any instant of time to be predictable from Kmin.

Figure 19 illustrates the relationship between zc and Kmin for 15 British lakes. Fontinalis lies at the base of one of the deepest zC values and various Potamogeton species are the deepest colonists in three other lakes. However, the base of zc is shared in Loch Drumore and occupied exclusively in nine others by Nitella. The Nitella values are distinguished on the graph which represents an extinction curve, in terms of the least attenuated light, for these macroph ytes.

Attention was drawn on p. 57 to the far larger contribution of phytoplankton than yellow substance to short wave attenuation with around 200 mg chlorophyll a m-3 in the water, but this applies to none of the lakes in Fig. 19. Rather the problem centres on seasonal variation in amount of yellow sub-

THE ZONATION OF PLANTS IN FRESHWATER LAKES

2 -

1 - 0

79

10 0

0

stance itself for which, amongst the present data, KB values provide a guide. In Loch Balnagowan, for example, the K B values varied on three visits from 0.29 to 1.23, the lowest being similar to that recorded in Loch Borralie and the highest comparable with that found in a brown lake such as Loch na Thuill (Table 5). Kmin values showed a corresponding range, from 013 to 0.94.

These Balnagowan data illustrate the danger of extrapolating from light readings based on single visits, even when phytoplankton density is always low. Further, there may be substrate limitation in a particular lake. Recent diver-collected data indicate that low summer temperature can be an important factor for macrophyte depth limits, specifically the intermediate and final depths at which the base of epilimnia occur in clear stratified lakes. In these circumstances, however, low light levels may still be involved. The two factors both interact to inhibit shoot growth in both Hippuris vulgaris (Bodkin, 1979) and Utriculariu purpurea (Moeller, 1980). More data like these are needed on the depth limits of Tracheophyta from clear-water lakes with moderately rich sediments, where these plants may be expected to occur below 6 m depth. At present this lake class is apparently rare-note the shallow mean depth limits for angiosperms and indeed all macrophytes in the 36 lakes of Table 3.

80 D. H. N. SPENCE

(e) Conclusions. Recent field and laboratory evidence suggests that, contrary to widely held views in the literature, pressure is probably not involved in limiting the water depths to which submerged angiosperms may penetrate. While low temperature appears to be an important modifying factor for such plants in some clear, stratified lakes and unsuitable substrates may inhibit macrophyte colonization in deep water where there is adequate light, light is nevertheless the main determinant of ultimate depth limits.

It is concluded that broad relationships can be established between submerged macrophyte depth-limits and underwater light intensity in particular lakes but that detailed relationships are best studied at the physiological level, by laboratory and field investigations of photosynthesis, photomorphogenesis and the overall growth and survival of selected species.

B. Vertical and Horizontal Components of Zonation

I . Reedswamp and Submerged Plant Distribution

In the shallow water of a lake, an exposed, wave-mixed shore having sparse plant cover may be contrasted with a sheltered bay having continuous plant cover. Horizontal variation in wave action and sediment type may occur between the exposed and the sheltered shore and be superimposed on vertical variation in both of these factors. Diminished wave action or turbulent motion is accompanied by smaller particled and therefore, usually, more nutrient-rich sediments. Either factor, or both, could result in better plant growth and, in the absence of experimental data to separate them, these factors should be grouped together.

In this section, first of all, the effects of wave action and sediment type on reedswamp distribution around lakes are briefly studies using Scottish data (Spence, 1964, but see also, for example, Bernatowicz and Zachwieja, 1966). Kilconquhar Loch, a shallow eutrophic lake of 39 ha in Fife, is almost completely surrounded by reedswamp (except where it has been removed by man), with several patches of floating-leaved vegetation close to the shore and it is inferred that the wave-mixed zone is very narrow. Consider two further lakes of comparable size, one in acidic fluvio-glacial deposits, the other in a rock basin of gneiss. In the first, the west end of Loch Stack in Sutherland, there is sparse but fairly continuous reedswamp. In the second, typical of any small glacial ice-scour lake in Scotland, there is an abundance of rocks and boulders which severely restricts reedswamp irrespective of any other factor. Reedswamp may also be absent from small and sheltered rock basins in blanket-peat catchments because the substrate is too nutrient-poor for establishment or growth. Loch Lurgainn in Sutherland is a larger rock basin (area 327 ha, mean depth 19 m), with cliffs and stony shores, and reedswamp is

0 X 50- r

3 40-

f 1 i 3 0 g-20

I? 10- 3 6

0 .-

Depth of water Icm)

/I) -

-

/x X I 1 1 I I I 1 ,

( b )

c

40 40 0

Plant cover

Depth of water (cm 1

Depth of water (cm )

Fig. 20. Plant-sediment interactions with waves. (a) Increase in shoot height of Equiseturn fluviatile above the water surface as water depth increases and sediments grade from gravel to mud in Loch Hacoin; (b) submerged shoots of Myriophyllum alternijorum and underlying sediments showing the same trends on an open shore of Loch Kinardochy; and this example also demonstrates increasing plant cover with increasing water depth; (c) an increase in plant cover and a corresponding decrease in the amount of sand in the sediment as water deepens are illustrated for an open bay in Loch Tarff. Redrawn from Spence (1964).

82 D. H. N. SPENCE

confined to three sandy inlets on the north shore. Finally in Loch Ness, with an area of 5650 ha, length 32 km and mean depth 132 m, there are only three areas of reedswamp, Inchnacardoch Bay, Borlum and the delta of the River Urquhart. In both lochs the wave-mixed zone predominates in the littoral.

Submerged vegetation is now considered in relation to the interacting effects of turbulence and sediment type on its growth. The data in Fig. 20 were collected in the shallow water of open bays of three small lochs, where the sediments were gently graded towards deeper water. Shoot height of individual species and overall plant cover increase as the sediments become finer and wave action lessens. A broad comparison has already been made in Fig. 4 (p. 48) between vegetation in the shallow water of an exposed and a sheltered shore of Loch Uanagan, another small lake.

The combined effects of variation in wave action and sediment type on plant biomass is shown well in Fig. 21 for the exposed shore of the same loch, but in this case down to a depth of 4 m. Data were collected in August,

Pot praelongus

$ 0

Pot perfoliatus Pot x ZIZII

c

Pot pusillus

80 160 240 320 400 Depth of water (cm)

Fig. 21. Zonation of submerged vegetation in Loch Uanagan on 13th August 1967. Data collected by diving. As standing crop (roots and shoots) of all submerged species in relation to water depth (cm) above the surface of the sediment in which they were rooted (arrow indicates base of littoral shelf) and as relative species’ dry weight. Redrawn from Spence (1972).


while snorkelling with a weight belt, from quadrats placed along a depth transect (Spence, 1972). A typical gravel terrace with sparse Littorella and Lobelia extends to a water depth of 0.6 m, drops steeply over large stones to the start of the bottom sediment at 0.8 m (marked in Fig. 20 by an arrow) and thereafter the sediment surface drops gently to more than 4 m depth. The fine-leaved Potamogeton pusillus is the deepest angiosperm but Nitella opaca was found, whilst diving on a later visit, in patches to a depth of 4.1 m. Plant biomass increases very sharply once the bottom sediment is reached, rising to a maximum in water just over 1 m deep. Most of this biomass is contributed by the large pondweeds, Potamogeton praelongus, P. perfoliatus and P . x zizii, which predominates in these more sheltered and finer sediments.

Another instance of the interactions between wave action, sediments and plants is provided by the distribution of vegetation in Loch Urigill, Suther- land (Spence and Allen, 1979), a lake lying on an open plateau at an altitude of 145 m. Figure 18 gives some results obtained by wading along the shore and by diving in three widely separated parts of the loch. Sparse Isoetes and some Lobelia occur amongst rocks, boulders or gravel. Mud less than 1 cm deep is uncolonized and lsoetes or Littorella only form dense cover on muds at least 5 cm deep. The pondweed beds, mainly of Potamogeton perfoliatus and P. praelongus, with P . natans locally between 1.5 and 2.7 m depth of water, occur on muds not less than 8 cm deep. These beds lack an understorey of vegetation and consist of 2-3 shoots m-2 (rarely up to 9 shoots m-2) and cease abruptly at 3 m depth in this brown water. The ability of broad- leaved species to root in shallow water in this exposed loch is perhaps a function of the extent to which the sediment can anchor these potentially large plants. Also a relationship may be inferred between a decline in the depth of the wave-mixed zone and the increasingly shallower water depths at which colonizable sediment can accumulate.

Again implicating differences in both wave action and sediment there is usually, in the shallow water of a lake, an increase in species diversity between an exposed and a sheltered shore. Figure 15 shows this for contrasted shores transects in Loch Maberry. Thunmark (1931) also illustrates this increase in species diversity between two shores of Lake Fiolen in Finland. With deposition starting at 3.75 m water depth, the exposed eastern shore had 18 species and these were entirely emergent or rosette type whereas deposition started at 1.25 m on the sheltered shore and supported 32 species of diverse growth forms.

Waves may have a direct effect on plant growth: a natural population of Potamogeton richardsonii growing in silty sand on the exposed shore of Sparrow Lake, Ontario at 0 5 m depth of water achieved an LAI of 0.4. At the same water depth in similar soil but with the vegetation in an experi-

84 D. H. N. SPENCE

mental bin where the only turbulence was convectional, LAI = 4 (Spence and Dale, 1978).

Both wave action and grazing by waterfowl can reduce biomass in shallow water. The depth zone colonized by macrophytes in a eutrophic lake, Loch Leven, is 1 m and less than 5% of this zone bears plant cover (Jupp and Spence, 1977a). The seasonal integrated biomass on the sandy east shore of the loch, representing its commonest habitat, was 15% of values on the rarer clays north of St Serf’s Island (Table 10). Wave action was considered to be the main cause of this difference. The loch however is also noted for its large migrant and resident waterfowl population and some of the low macrophyte biomass might have been partly the result of waterfowl grazing, which includes the uprooting involved in searching for the underground tubers. Plots were enclosed with broad-mesh wire netting which excluded waterfowl but caused little reduction in turbulence (Jubb and Spence, 1977b). Unenclosed plant biomass at St Serf’s was then found to be 80% of that achieved with enclosure and the 20% reduction was attributed to waterfowl grazing. This is a minimal figure since the enclosures were removed before the full effect on the pondweed beds of the late autumn tuber “grazing” could be estimated. However, even the ungrazed biomass was only 40% of that reached in perspex tubes with complete protection from both waves and grazing so, at that time, losses through grazing were less than those caused by wave action.

Qualitatively, some of the interrelationships of waves, sediments and vegetation can be summarized in terms of three broad types of littoral (after Bernatowicz and Zachwieja, 1966):

(1) Litholittoral, where beach and shelf are cut in rock or formed from boulders and some gravel but, in shallow water, there is no sand. Sparse plant cover may occur in gravel pockets (in northern Europe, open Littorella- Lobelia or Isoetes):

(2) Psammo-littoral, where beach and shelf are sandy and mainly devoid of plants although stretches of sparse or moderate plant cover occur locally (in northern Europe, open reedswamp of Phragmites communis, Equisetum fluviatile, Eleocharis spp., Schoenoplectus lacustris, some floating-leaved communities like Polygonum amphibium and submerged Lobelia-Littorella or Chara-Myriophyllum-Potamogeton jiliformis): if (1) or (2) or a combination of both comprise the littoral then zc must lie wholly within the wave-mixed zone.

(3) Phytolittoral, where the whole littoral is covered in submerged floating- leaved and reedswamp vegetation. Possible dominant species are too numerous to list. The wave-mixed zone is likely to be minimal or absent.

Conclusions. Reedswamp distribution around a lake is controlled by the degree of wind-induced wave motion. Accepting that the shape of the lake may modify any simple relationship this means approximately that the pro-

Table 10 Integrated seasonal biomass of Potamogeton jiliformis in relation to strong wave action (east shore: sandy) and some shelter (St Serf’s: ciay), and to exclusion of water fowl and to complete protection from wave action at St Serf’s (derived irom Jupp and Spence,

1977b).

Unenclosed biomass as ”/, Unenclosed biomass as :4 max. Wire-enclosed biomass as :/” unenclosed biomass wire-enclosed biomass perspex-enclosed biomass

~~ ~~~ ~~~~~~ ~~~~~~ ~~~~~~ ~~~~ ~ ~~~ ~

St Serf’s clay’s (rare) 100 St Serf’s clays: wire enclosed 100 St Serf‘s clays: perspex-enclosed 100 East shore sands (common) 15 St Serf’s clays: unenclosed 80 St Serf’s clays: wire-enclosed 40 % biomass reduction 85 20 60 Deduced cause Waves Waterfowl Waves

mainly grazing

86 D. H. N. SPENCE

portion of colonized shoreline is inversely related to mean fetch. Shoot density, biomass etc., are thereafter likely to vary with the nutrient status of the sediments in the available sites. It follows that, above an undetermined degree of exposure, there is no reedswamp because of direct effects on the establishment and spread of the plants themselves or because the sediments within colonizable depths are too coarse particled for adequate growth.

The same broad conclusions can be drawn for submerged plants, basing this view on measurements of their growth along depth gradients on exposed shores and in deeper, sheltered water, and on examples which discriminate between the influence of waves, sediment and grazing by waterfowl. The most suitable overall explanation of the differences in macrophyte vegetation which occur around a lake does seem to be that horizontal variations in the environment are imposed on vertical variations.

In the littoral of any lake, species diversity and plant cover increase with shelter, and dense cover depends on the absence of wave action. Such shelter may extend to the whole of a pond and to increasingly fewer stretches of the shores of increasingly larger lakes. Shelter in shallow water is the exception not the rule so that the litholittoral, lying wholly within the wave-exposed zone, is probably the commonest shoreline. To limitations set by wave action are added, in most palaeogenic regions, those imposed by the low nutrient status of the rock type from which catchment and lake basin are made. While interactions of wave action and sediment have been emphasized here, these deductions indicate why sediment itself appears to be so important in controlling the distribution of macrophytes in lakes, a point returned to in Sections 1II.c and V.

C. Sediments and Plant Responses

1. Root and Shoot Uptake of Nutrients

Since this review deals with aquatic plants in the widest sense, the distinction should be emphasized that exists between most emergent species and most submerged species, with floating-leaved species occupying an intermediate position. That is, emergent species are fully submerged only during their dormant phase: their photosynthetic tissue is mainly or exclusively exposed via stomata to the air and, allowing that they can tolerate some degree of anoxia around and in their roots, such plants are not functionally different from other “land” plants. Permanently submerged plants are generally furnished with root hairs or other absorbing surfaces in the sediment, like rhizoids; and from growth experiments over many years (Pond, 1905; Snell, 1908; Bourne, 1932; Roll, 1936; Misra, 1938; Moyle, 1945; Mulligan and Baranowski, 1969; Peltier and Welch, 1969; Denny, 1972) it has been deduced


that aquatic angiosperms in particular can take up nutrients via their roots; for example, better growth in the same container has generally been observed of such plants rooted in mud rather than sand. The use of various radio- isotopes has established that specific ions are taken up by roots of a range of species (Bristowe and Whitcornbe, 1971; McRoy and Barsdale, 1970; Campbell, 1971; DeMarte and Hartman, 1974; Nichols and Keeney, 1976a, b; Best and Mantai, 1978; Carignan and Kalff, 1979; Welsh and Denny, 1979) and by the basal parts of Ceratophyllum demersum (Toetz, 1974; see also Denny, 1980).

In evolutionary terms the submergence of angiosperms in fresh water has led, among other features, to reduction in leaf cuticle thickness; such a reduction must follow from the known effects of reduced oxygen diffusion, light intensity (UV in particular) and increased humidity on cutin development (Clowes and Juniper, 1968). For example, a fresh leaf of Potamogeton praelongus, stained in Sudan IV, had a cuticle thickness of 0.24 pm, on a cellulose wall 0.09 pm deep; this compares with a similarly prepared Prunus laurocerasus leaf having a cuticle thickness of 0.70 pm on a wall 6-00 pm deep (Spence, unpublished data). The main functional difference that distinguishes most permanently submerged angiosperms is their apparent ability, in the first place because of this thin cuticle, to exchange ions dissolved between the surrounding solution and their photosynthesizing tissue (Rosen- fels, 1953; Gessner and Kaukal, 1952; Arisz, 1953, 1963, 1964; Winter, 1961; Denny and Weeks, 1970; Jeschke, 1976). The fact that the green “giant cells” of members of the Charophyta exchange ions with their bathing solution has of course resulted in a detailed understanding of the regulation of salt uptake in plant cells generally (e.g. Hope and Walker, 1975). In addition, members of the Tracheophyta, Charophyta and Bryophyta exhibit varying ability to take up bicarbonate ion from the bathing solution for use in photosynthesis (e.g. Raven, 1968; Allen and Spence, 1981).

Submerged plants can take up nutrients via their above and below-ground parts. The mechanism of salt uptake in submerged angiosperms by leaves and roots, the solute movement between these organs, and the extent of dependence on sediment or bathing solution have recently been reviewed in detail by Denny (1980); the concern here is with the ecological consequences, if any, of this “dual ability” of submerged plants.

2. Signijicance of Sediment as a Source of Nutrients for M acrop hytes

Under certain conditions nutrient uptake by submerged macrophytes can only occur directly from the sediment. These conditions exist in lakes with water that is poor in nutrients, especially phosphorus, and which have a per-

88 D. H. N. SPENCE

manently oxidized microzone at the sediment surface. The sediment then acts as a nutrient “sink” and levels of phosphorus such as the interstitial concentrations of phosphate-phosphorus, for example, are always higher than those in the lake water.

On erosional shores there are interactions between waves, sediments and plants; waves coarsen sediments, in effect lowering their nutrient status while plants may be damaged as well as having a poor medium for establishment and rooting. To test the effects of sediment alone on plant growth in nature, sheltered, depositional sites must be examined or else shelter must be created. Naturally sheltered sites may lie in shallow water, as in the narrow bays of Lake Opinicon, Ontario (Crowder et a/., 1977), or in water several metres deep, as in Loch Borralie. The calcareous water in the latter lake is always clear (Table 5 ) and thermally unstratified, and contains less than 5 mg m-3 PO4-P while the interstitial PO4-P concentration in the sediment is relatively high at 2.4 g m-3. Levels of nitrate and ammonium are also very low in the water but NH’ reaches 22 g m-3 in the interstitial water of the sediment. The nutrient supply needed to sustain the large maximal biomass of 400 g organic dry weight m-2, which occurs at 3.5 m depth of water (Fig. 3), can only reach the plants by direct uptake from the sediment. Macrophyte growth which must also depend in the main on sediment, unaffected by exposure on the one hand, by low light on the other, may also be observed beyond the wave-mixed zone in clear, acid or low-alkalinity lakes: although, on a sediment containing 10 mg m-3 interstitial P04-P, maximal biomass is only 35 g organic dry weight m-2.

Loch Leven is eutrophic, its waters during summer containing variable but generally high concentrations of PO4-P (up to 90 mg mP3). These levels should be adequate for the growth of Potamogetonfiliformis which is the principal species in its shallow macrophyte zone and which, in these circumstances, might be expected to utilize phosphate in water or sediment. To find out if sediment affected growth independently of waves, Jupp and Spence (1977b) placed perspex tubes around plants growing on a sheltered (clay) and an exposed (sandy) shore, where the initial maximal biomass was respectively 100 and 25 g organic dry weight m-2. Within eight weeks, the increase in both shoot length and shoot weight was 60% greater on the clay than the sandy shore, where clay contained 28.3 If: 8.5 and sand 5.5 k 0.01 mg P per 100 g oven dry sediment.

This result does not preclude the possibility of phosphate uptake by shoots in this nutrient-rich lake but it is quoted because of an analogy with a situation recently examined by Best and Mantai (1978). Using natural sediments and, in separate containers, natural or enriched lake water as sources of P and N for Myriophyllum spicatum, these authors showed that P levels in tissue tended to be higher in plants grown in a sandy silt than those grown


in sand from the same lake, regardless of the nutrient levels in the (separated) lake water, even where PO4-P levels are raised to 55 mg m-3. Carignan and Kalff (1979) bathed the shoots of three submerged species including M . spicatum in lake water at various phosphate concentrations and the attached roots in separate containers of lake sediments. They showed that mobile sediment phosphorus, as determined by isotopic dilution, represents the total P available to plants rooted in these sediments. For one lake at least, with concentrations of 10 to 15 mg m-3 in the water, macrophytes obtain all their P from sediments. However, Best and Mantai found that, if N content around the shoots was high, then M . spicatum rooted in an N-rich medium obtained N from either source with equal facility. A neat corollary is provided by work of Nichols and Keeney (1976a, b) on M . spicatum, utilizing lSN- labelled compounds (and not quoted by Best and Mantai); the species had a greater facility for shoot absorption of nitrogen but, when this source was limited, root absorption supplied its N requirements.

For submerged and rooted macrophytes in eutrophic waters, it is likely that P is supplied by roots from the sediment. However, while shoot uptake may augment nutrient supply where the plant is growing in a coarse, low phosphorus sediment, phytoplankton or epiphytes in these eutrophic waters would usually represent alternative “sinks” around shoots and, depending on relative rates of demand, might reduce direct supplies to them. As to nitrogen, when its content is high in the bathing solution, uptake by the shoot is as important as that by the root and, when that source is low, root uptake from the sediment predominates. Again the usual presence of many microalgae and bacteria in natural waters of this type may still mean that sediments also provide the major source of nitrogen for angiosperms.

In Loch Borralie (Fig. 3) where the water has less than 5 mg PO4-P m-3 but the mud interstitial water 2.4 g m-3, Chara contraria can exceed heights of 1 m, and form very dense beds. Given the capability for nutrient uptake by rhizoids (Vouk, 1929), the high velocity of cytoplasmic streaming observed in Chara cells (Pickard, 1974) and the known long-distance nutrient fluxes displayed in these plants (see, for example, Raven, 1979), nutrient uptake from the bathing solution by green shoots would indeed be unnecessary although ions may enter the portions of the shoots lying below the sediment surface.

Therefore, field and experimental evidence point to sediment as the major source of nutrients for submerged macrophytes, at least for angiosperms, vascular cryptogams and Charophyta with roots or other organs buried in the sediment. Filamentous algae like Cladophora glomerata provide examples of macrophytes where an association with fine, deep-water sediment probably relates to lack of strong turbulence rather than to any ability of the sediment to provide nutrients directly to these plants. Growth of algae such as these will tend to vary with the amounts of soluble phosphorus and nitrogen in

90 D. H. N. SPENCE

the water. There is some evidence that the same situation applies to the rootless angiosperm Ceratophyllum demersum (Goulder and Boatman, 197 1).

A further contrast lies with the bryophytes which tend to occur as dominants on a wide physical range of sediments in granitic lakes from which all submerged angiosperms, or at least the larger ones, are absent: or, in less nutrient-poor lakes, on rocks in shallow water and on sediments below the depths colonized by angiosperms and Charophyta. Since the common factor for bryophyte dominance is not, for instance, growth on a fine sediment but minimal or no competition from such plants, sediment generally may be less important for bryophytes as a nutrient source than lake water. However, high rates of deposition may also exclude them from certain sites.

3. Sedimentation and Plant Response

Sediment can be deposited at greatly differing rates, even on adjacent stretches of a single shore, and macrophyte survival may depend on the capacity of plants to respond, to burial, by vertical growth. Further, the actual presence of living plants on a depositional shore will, through entrapment, enhance sedimentation rates. When plants are not killed by such deposition but interact with it, a hydrosere can be started, successional aspects of which are discussed in Section IV.

A broken reed provides an example of the passive trapping of sediment. Shoots of Phragmites communis grow, for instance in the Tay Estuary, with densities of 90 to 150 mW2 and, on dying in winter, break to produce erect hollow cylinders which, on the outer swamp margin, entrap up to 2 kg sediment m-2 yr-' (Alizai and McManus, 1980). This method accounts for much of the annual accretion. Most of the deposition, however, occurs directly amongst the plant shoots and similar processes probably take place in underwater vegetation also.

Arber (1920) was the first to report that plants of Littorella unifora could alter their rooting levels in response to burial by sediment. Under glasshouse conditions in summer, Webster (1975) buried matched rosettes of Littorella, with intact roots, with sand at rates of 0.5, 1 and 2 cm depth per month. At the lowest rate of deposition, Littorella spread horizontally by a branching, rhizome-like structure. With sand additions of 2 cm depth per month, a wholly vertical, sparsely-branched system developed, of a type frequently found in plants gathered from silts near stream inflows. Eleocharis palustris was found to respond to experimental burial in the same way; like Littorella, specimens can be found in nature with similar underground parts to those produced by laboratory burial.

From his observation of vegetation and habitat in the English Lakes, Pearsall (1921) concluded that rates of silting, or sediment deposition, had important consequences for the distribution of plants. Zsoetes lacustris and


Fontinalis antipyretica were stated to be found on bottom muds where silting was least, otherwise being typical of stony or other coarse substrata; Nitella opaca could withstand some sedimentation but not as much as Juncus bulbosus f. ,fluitans, Elodea canadensis or Potamogeton perfoliatus. So, where local topography or aspect causes horizontal variation in a mainly depth- dependent pattern of silt deposition, beds of Nitella on fine silt may occur in shallow water of one shore; while, in deeper water on another shore of the same lake, beds of Zsoetes may grow in coarse-particled sediment.

Strictly, these responses of different species to silting should only be deduced from sites where rates of vegetation change are known. Confirmation of at least some of these responses comes from Pearsall’s own maps of the North Bay of Esthwaite Water which were drawn in 1914 and 1929 and published in Tansley (1949). Where silting is considerable as judged by decrease in water depth over 15 years, Fontinalis is either succeeded by Nitella which in turn is followed by Elodea, or Fontinalis is replaced directly by Elodea. Sayre (1945) noted that, in Colorado lakes, the deposition of fine sediment in shallow water caused the replacement of Fontinalis by angiosperms.

In Lake Fiolen Zsoetes lacustris is typical in deeper water of areas of minimal deposition (Thunmark, 1931) while in Loch Uanagan Juncus bulbosus f.$uitans has replaced Chara species, where silting has occurred at a stream entry in 1 to 2 m depth of water (p. 93). Pearsall (1921) points out that Zsoetes lacustris cannot alter its rooting level in response to rapid silting; there is indeed no mechanism for vertical stem or rhizome growth like that described above for Littorella.

It is assumed that these different responses are in part the result of species’ having different growth responses to burial and partly the result of their having different relative growth rates. Clearly any apparent correlation between species and substrate type must take account of these largely unknown attributes of the plants themselves. The subject will be referred to again when discussing the hydrosere (Section IV) and in relation to plant adaptation (Section V).

4. Conclusions

Pearsall(l918, 1921, 1922) concluded that the distribution of aquatic plants in the English Lakes was primarily governed by the nature of the substratum, specifically (Pearsall, 1921, p. 181) “sediments become finer as water deepens; since sediments are zoned along lake shores and since they differ in chemical composition, we are justified in assuming that zonation of vegetation is a result of differences in soil conditions”. Pearsall indeed considered certain species to be associated with particular soil properties like percentage organic matter or percentage fine silt (e.g. K’) but Spence (1964,

92 D. H. N. SPENCE

1967) was unable to endorse these findings for the same species after a survey of aquatic vegetation in Scottish lochs and stated that, while edaphic conditions could directly or indirectly control the distribution of rooted aquatic plants in lakes, it had still to be proved that any species was causally associated, even in a single lake, with one circumscribed soil type.

Thirteen years later this proof is still awaited, in spite of much new evidence implicating sediment as the main source of nutrients for submerged macrophytes with their roots or other organs buried in sediment, and some new evidence that macrophytes vary greatly in their capacity to respond to high rates of sedimentation. This last point suggests where one paradox lies; a species occurs in a lake on sediments which have a range of chemical attributes at any instant of time but its limits may be set by its tolerance of rapid silt deposition (and, further, where silting is less, by competition from another species). The overall question of control of zonation is looked at again once light and plant response, and interspecific competition, have been discussed (Section VI).

IV. CAUSAL ANALYSIS OF CHANGES OF

DEPOSITIONAL SHORES AND THE HYDROSERE WITHIN-LAKE DISTRIBUTION WITH TIME

It has already been observed that shelter or lack of strong turbulence% a common feature of all well-colonized habitats, either the whole of a small lake or increasingly less of the shoreline of larger and larger lakes. These sheltered shores are essentially depositional, that is, subject to minimal wind- induced currents and wave action, and the remaining part of this section concentrates on further aspects of plant growth and community development on depositional shores.

The zonation of plant communities at the edge of an expanse of water from, say floating-leaved vegetation to reedswamp is often called a hydrosere. Only knowledge of change at one site and, better, the rate of change can confirm that a spatial sequence is also an example of a hydrosere, or plant succession. In this section, evidence for such succession is examined, along with study of causes and rates.

We may study short-term photographic or cartographic evidence and long- term evidence preserved in lacustrine muds. Let us first look at the vegetation on nutrient-rich organic silts of the fens of East Anglia. A typical example is provided by Godwin's maps of parts of Wicken Fen, drawn in 1923-1924 and 1934 (Godwin and Bharucha, 1936). At the time of the first mapping, an area of Cladium-Molinia (mixed fen) was colonized in places by nearly closed carr of Rhamnus catharticus and Salix atrocinerea or by small bushes


of Frangula alnus. Ten years later the carr had become closed and had extended: Salix had largely given way to Rhamnus and Cladium beneath the trees was suppressed. Also, closed Frangula now occupied much of the rest of the area although Cladium here still survived beneath the bushes.

Scottish loch-margins generally provide a contrasting picture to this evidence of rapid change. Many sites which included emergent and floating- leaved vegetation were photographed in 1904 by West (1905,1910). A number of these sites were re-photographed by the present author more than 50 years later, in 1959 or 1960 (Spence, 1964, Plates 66-77 and pp. 378-381). Most of the photograph pairs illustrate no change in the extent or position of emergent and floating-leaved vegetation. The implication is that insufficient additional material had accumulated on the substrate to cause change; the communities represented an edaphic climax over this 60 year period and there was no evidence of autogenic succession.

All these lochs occur in the palaeogenic regions of Scotland, the Highlands mainly, and their inflows tend to lack finer and more nutrient-rich sediments. I have previously suggested (Spence, 1964) that, even where turbulence is slight, autogenic factors have little or no effect on plant succession in the absence of finer fractions in inwashed sediment. However, where in these palaeogenic regions, sediment has accumulated from depositions made by in- flowing rivers and streams there is evidence of considerable change. Thus the delta of the River Urquhart at its entry to Loch Ness has built up during this 56-year period and plant succession from hydrophyte to reedswamp and from reedswamp to fen carr and Alder woodland has occurred. For example (as Plates 66 and 67 in Spence, 1964 show):

1904 1960

Shallow water No emergents Shallow water Carex rostrata Water at soil Carex rostrata Water below Carex rostrata-

surface soil surface Calliergon (Acrocladium)

Water below Carex rostrata Alisma plantago-aquatica soil surface Alisma plantago-aquatica Phalaris

Phalaris Salix fen-carr and Phalaris

Another example of change is found at the stream entry into Loch Uanagan in the Great Glen near Fort Augustus (Plates 68 and 69 in Spence, 1964). Apart from the obvious spread and expansion of Schoenoplectus lacustris on the delta fan, beds of Chara species in water up to 2 m deep beyond Schoeno- plectus have been replaced by Juncus bulbosus f. Juitans with Utricularia vulgar is.

94 D. H. N. SPENCE

Detailed mapping of the vegetation of the North Bay of Esthwaite Water was carried out by Pearsall in 1914 and 1929 (Figs 114 and 115 in Tansley, 1949). During this 15-year period, Phragmites swamp had advanced between 17 and 34 m into the lake while, on its landward side, much of the Phrag- mites had been succeeded by Carex rostrata, C. elata and Salix cinera, this last species also forming more closed carr to lakeward of its previous areas. Silt accumulation in deeper parts of the bay had resulted in Fontinalis being succeeded by Nitella and then Elodea or directly by Elodea (and see p. 91).

In 1967-1969 Pigott and Wilson (1978) re-surveyed the vegetation of North Fen which adjoins North Bay. Since Pearsall’s survey of 1929 the Phragmites swamp had advanced up to a further 25 m into Esthwaite Water and Carex rostrata had again succeeded Phragmites along the latter’s landward edge. So, too, had closed carr or woodland of Ainus glutinosa and Salix cinerea continued to advance lakeward on alluvium. Other notable changes between 1929 and 1967-1969 were the recent spread of Betula pubescens and Fraxinus excelsior into the sedge-fen and the establishment of a few saplings of Quercus petraea beneath dying trees of B. pubescens on the oldest part of the carr.

In the least turbulent parts of lochs such as Lindores or Carlingwark, which are kettle lakes in fluvio-glacial clays, comparison by Spence (1964) with West’s (1910) photographs indicated accumulation during the intervening 55 years of silt, clay and dead plant material as fen peat, with consequent rapid allogenic-autogenic successions of the East Anglian fen pattern: but this vegetation change could not be accurately recorded.

It therefore appears that succession is normally brought about over this time scale by an allogenic factor, the net accumulation of inorganic sediment. Pearsall(1918,1920,1921) reached the same general conclusion from his study of the vegetation of the lakes of the English Lake District.

If the net accumulation of inorganic sediment is essential to the hydrosere, the rate at which this accumulation takes place may also be very important because it may determine, for a given range of water depth, which species can colonize a particular site. This point has already been discussed in the section on sediment and plant response, along with a second point, that species’ growth response may help determine the rate of net accumulation; Littorella uniflora and Eleocharis palustris can grow vertically if buried but Isoetes lacustris cannot. Pearsall (1920) infers successional relationships between 12 underwater plant communities on the basis of type and amount of sediment, or deduced rates of sedimentation. It is concluded, 60 years later, that measurement of sedimentation rates and substrate changes would be one of the more profitable ways of studying these interactions with underwater vegetation, as well as what occurs on lake margins beyond the reach of anthropogenic factors like grazing or trampling by farm stock.


Walker (1970) used the pollen evidence of mud cores collected round 66 British lakes to test the hypothesis that the in-filling of lakes results from the action of plant communities appearing in a predictable, orderly sequence; that is, from autogenic succession. Confirming the conclusions from short- term studies, Walker found that the infilling of most lakes was inwashed material and not autochthonous organic matter deposited by the plant communities themselves. Plants had responded to the infilling rather than causing it. It was also found that the plant communities did not appear in a predictable sequence, perhaps not surprisingly since individual hydroseres should reflect responses to different types of sediment and to differing rates of silting.

A further cause of variation, however, could be fluctuation with time in the water chemistry of a lake. A fairly rapid change from nutrient-rich to nutrient-poor sediments is a well-known feature of lakes in Palaeogenic regions, in early post-glacial times, being reflected in qualitative changes in their macrophyte and microalgal floras (for example, Pennington, 1943; Round, 1961; Mackereth, 1966; Walker, 1970). Many cases have been reported of recent qualitative changes in macrophyte floras which have accompanied the chemical enrichment of lake waters in Europe and North America (for instance, Edmonson, 1961; Jupp et al., 1974; Philips et al., 1978; Dale and Miller, 1978). While such changes may have no obvious effects on any local hydroseres in these lakes they may in the medium or long term influence the plant record in their sediments.

V. PLANT ADAPTATIONS

A. Flow, Substrate and Plant Distribution

First, some field observations: Eleocharis palustris is often the sole reedswamp species in British lakes where the finest shallow-water sediment is sand (Fig. 15, L. Maberry: Table 2). EquisetumJluoiatile forms an open reedswamp on sandy soils a full metre deeper than Eleocharis (Fig. 4, L. an Ordain: Table 2) while Schoenoplectus lacustris never occurs in less than 0.3 m water depth, at least in Scotland, and typically to lakeward of, for instance, Phragmites communis (Table 2). The same relationship holds for these species, or their vicariads, in North America and East Africa. Species like Sparganium erectum are typical of sheltered bays and very fine sediments with low critical erosion velocities. These observations suggest that terete-stemmed genera-leafless like Eleocharis palustris or without emergent leaves like Schoenoplectus lacustris-are all more wave-tolerant than grasses such as Phragmites or sedges like Carex rostrata. While Polygonum amphibium appears to be one of the more wave tolerant floating-leaved species, alone occurring in rippled

96 D. H. N. SPENCE

sand, the general status of this group relative to emergents is not known. Haslam (1978) has categorized plants of British water courses in terms of

their measured relative responses to water currents. “Hydraulic resistance” of shoots to flow was measured as the drag exerted on a spring balance by shoots, attached to this balance, in a flume tank at a standard surface velocity; and “anchoring strength” where pull on a naturally anchored plant was applied, through a spring balance. Responses were recorded on a 3-point scale, from 1 (high) to 3 (low) resistance and anchoring strength respectively. “Erosion susceptibility” was tested by response of naturally sited root systems to a constant-velocity jet of water and “turbulence susceptibiliby” was recorded as visible damage to shoots exposed to a constant velocity current in a flume tank: these responses were scored on a 4 and 5 point scale respectively. In Table 11 I have summarized these findings for a number of species common to lakes and rivers. I have, however, altered Haslam’s last two categories by referring to exposure and erosion tolerance, not susceptibility. The total score for each species then provides a relative measure of its tolerance of “turbulence”; low flow-resistance (3 points), high anchoring- strength (3 points), high erosion-tolerance (5 points) and high exposure- tolerance (4 points) give a maximum tolerance of turbulence amounting to 15 points or 100%.

Table 11 Some emergent, floating-leaved and submergent species, common to rivers and lakes, classified in terms of their tolerance of turbulence, derived from data of Haslam (1978); see above. Turbulence-tolerance has a maximum of 15 (loo%), made up as fol1ows: ( I ) hydraulic resistance (HR) on a 3-point scale from 1, high, to 3, low; (2) anchoring strength (AS) from 1, low, to 3, high; (3) erosion-tolerance (Er-T) on a 5-point scale from 1, low, to 5, high; and (4) exposure-tolerance (Ex-T) on a 4-point scale from

I , low, to 4, high.

HR AS Er-T Ex-T u o

max. 3 3 5 4 100

Phragmites communis Schoenoplectus lacustris Sparganium erectum Nuphar lutea Sparganium emersum Potamogeton natans Polygonum amphihium Elodea canadensis Potamogeton pectinatus Myriophyllum ulternifiorum Ranunculus peltatus Potamoyeton ohtusifolius

2 3

2

3

2 5 3 4

2 2 5

3 i

~

i i 5

3

3 5 1

4 (100) 3 92 2 13 4 80 3 66

(87)


Complete data sets only exist for four out of twelve of these species and six of the remainder have just one or two values. Schoenoplectus lacustris has almost maximal tolerance of turbulence while Potamogeton natans and Nuphar lutea have less and the two Sparganium species least, findings which are in broad agreement with knowledge of the distribution of these species in lakes. Ranunculus aquatilis (as R. peltatus and R. baudotii) colonizes wave- exposed shores where plant cover is less than 10% and Elodea canadensis is typical of fine sediments, and therefore some degree of shelter, in lakes. Finally, the only figure for P. obtusifolius conforms to its occurrence in lakes as a species of soft muds in deep water. Whilst they have been developed for rivers, Haslam's findings clearly have some relevance to lake studies and indicate an approach that is worth further study.

B. Photomorphogenesis, Photosynthesis and Zonation

1. Photomorphogenetic Responses Underwater (a) Emergent species, some of which also grow fully submerged. Most emer-

gent hydrophytes cannot exist at more than 2 m depth of water and the limit, in Scotland at least, is 1.5 m (p. 42). There are several possible reasons for these shallow limits, some of which were discussed earlier (p. 72), and those based on light requirements are dealt with here.

(1) In so far as reproduction occurs by germinating seeds rather than by vegetative spread there may be a light requirement which is only met in shallow water. Under conditions of reduced aeration, Typha latifolia is an emergent species of this type (Sifton, 1959). Alternatively, without an apparent light requirement, seeds may be able to withstand only shallow flooding, as is the case with Phragmites communis (p. 72).

(2) When Phragmites communis was recorded at its deepest, 1.1 m, it produced about the same shoot height above water (Spence, 1964). Leaves of this species are aerial only which might suggest that morphology is limiting, especially as a leafless species such as Equisetumfluviatile can grow in water 13 m deep, with more than three-quarters of its mature shoot submerged (Fig. 20). Does part of the difference lie in the relative contributions made to photosynthesis by the emergent and submerged parts of these species?

Eleocharis palustris and E . multicaulis, leafless emergent species of swamps which, like Equisetum fluviatile, also occur in fens, might seem ecologically similar to that species, although their smaller overall height apparently restricts them to about 0.5 m water depth (Table 2). In Loch na Thull, Suther- land, E. multicaulis forms part of a sparse reedswamp on its stony shores down to 0 2 5 m. Uncolonized rocks and boulders then extend to 0 7 5 m, and bottom sediments occupy the rest of the loch from that water depth down

98 D. H. N. SPENCE

to the maximum at 1.4 m. When diving recently in this loch, I observed E. multicaulis with shoots about 0.5 m high, growing amongst dense Juncus bulbosus var.Juitans, Lobelia and Littorella, in 1 to 1.4 m depth of water. Occurring in clumps, it formed about 10% of the total plant cover of 80%. (The species was overlooked in an earlier study illustrated as Fig. 48 in Spence, 1964, and it is not recorded as a submerged species in Clapham et al., 1962.) So, for this leafless species growing as an emergent, inadequate photosynthesis by its underwater parts seems an unlikely cause of depth limitation in shallow water.

(3) All the emergents so far considered have lacked underwater leaves, and a third reason for depth restriction might arise from such a lack. Schoeno- plectus lacustris has a leafless emergent stem and a rosette of strap-shaped submerged leaves. In Scotland it forms reedswamp to a maximum depth of 1.5 m, compared with 1.1 m for Phragmites, and the mean water depth of 0-9 m for S. lacustris swamps compares with 0 4 m for P. communis swamps (Table 2). S. lacustris can produce submerged-type leaves only, when it is reported to occur at water depths of 2 m (Haslam et al., 1975), while the fully submerged North American S. subterminalis Torr. reaches a water depth of 6 m in Lawrence Lake, Michigan (Rich et af., 1971).

Hippuris uulgaris is a familiar fen and swamp species which also, however, occurs as a fully submerged plant down to a depth of 6 5 m, the maximum recorded angiosperm limit in British waters (Figs 3 and 17). By contrast with S. lacustris, of which the submerged leaves are only produced as a basal rosette, H. uulgaris develops shoots with short aerial-type leaves and long, strap- shaped submerged-type leaves. The ability of emergent species to produce morphologically distinct underwater leaves is correlated with their ability to grow in deeper water than those that lack this ability. An exception like E. multicaulis might repay further study.

(4) This section has so far dealt with observations about depth limits and speculation about causes. Two photomorphogenetic processes are now examined which have been subjected to experimental analysis. The first concerns the mechanism controlling heterophylly in Hippuris uulgaris (Bodkin et al., 1980). In the clear water of limestone lakes, the aerial-type leaves of H . uulgaris occur down to more than 1 m below the surface. There is laboratory and field evidence that the switch from submerged to aerial-type leaves is photoreversible and, therefore, phytochrome mediated and depends on a R/FR ratio below 13.5 combined with high levels of PAR, only found below the surface of unusually transparent water (Bodkin et al., 1980). The second process concerns germination of submerged species.

(b) Germination and other light responses of mainly submerged species. A few submerged macrophytes need light to germinate, e.g. Potamogeton h e n s (Forsberg, 1966), and this need was studied in detail in P. schweinfurthii


A. Benn and P . richardii Solms. by Spence et al. (1971). Germination in nature only occurs once the fruit (a drupe) has sunk and the pericarp and mesocarp have rotted. Germination was promoted by R and reversed by FR and experiments indicated that P. richardii, which rarely grows in more than 0.5 m depth of water, needed three times the photon flux density required by P. schweinfurthii which occurs in water 0.75 to 6 m deep. So different light requirements for germination could contribute to zonation, although it may be argued that spread of perennial species like these will be achieved, at least within a lake, by stem turions or root tubers which our laboratory experiments show do not need light for initial growth. However, any light requirement for germination by annuals like Elatine hexandra or Subularia aquatica might well contribute to zonation.

Lobelia dortmanna has a rosette of leaves which are normally submerged and it bears a flowering stem which, according to Clapham et al. (1962) for example, grows up to 60 cm high and carries an emersed raceme. These data suggest that flowering rosettes are restricted to water less than 0 5 m deep, which agrees with general observation that this is a species of the upper littoral. Recently, however, while diving in the brown water of Loch na Thull, I found plants producing flowers, fruit and viable seed underwater, on stems 50 cm to 1 m tall from rosettes in water as deep as 1.2 m. Underwater flowering shoots as tall as 1 m are also recorded for L. dortmanna, by diving, in Mirror Lake, New Hampshire (R. Moeller, personal communication) down to rooting depths of 2 m in its clear water. Between 2 m and its lower depth limit of 2.3 m in Mirror Lake, the rosettes of L. dortmanna are flowerless (Moeller, 1980). This might seem irrelevant to zonation were it not for the observation that flowering controls the vegetative reproduction of this species, because such reproduction only occurs when more than one axillary meristem develops to succeed the inflorescence meristem @berg, 1943; Moeller, 1980). Perhaps, if vegetative spread is poor or absent at such depths, seed germination might provide a substitute. All that is presently known of this aspect is that seeds of L. dortmanna need light to germinate (Spence, unpublished data) and seedlings are sparse at the species’ depth limit in Mirror Lake (Moeller, 1980). So L. dortmanna may inhabit relatively shallow water because of high light requirements for initiation of its flowering stem and for seed germination.

For Charophyta there is evidence that photoperiod (Karling, 1924) and red light promote the germination of oospores or the differentiation of the resulting protonemata (Rethy, 1968; Takatori and Imahori, 1971). However, while Stross (1979) reports that Nitella jlexilis meadows, extending from 7 to 13 m in Lake George, New York, only produce oospores in the shallow half of the species’ range, he notes that plants will reproduce vegetatively in deeper water (cf. Starling et al., 1974).

100 D. H. N. SPENCE

The stems and leaves produced in shallow water by a range of submerged aquatic angiosperms are frequently red with anthocyanin, in contrast to the wholly green plants and leaves of these species when growing entirely in deep water; also, in shallow water the parastrophic (marginal) position of chloroplasts contrasts in, for example, Potarnogeton crispus with the diastrophic position assumed by chloroplasts of leaves in deep water (Spence, 1976a). Both anthocyanin production and the parastrophic position may be attributed to the metabolically active ( P f l ) form of phytochrome but their relevance to zonation of particular species is not known. That is, would a shallow-water species grown in high PAR and R i m exhibit these features more than a deep-water species grown in the same conditions?

Underwater shoots and internodes are typically short in shallow water, long in deep water in angiosperms (e.g. Bodkin, 1979 and Fig. 22, from Spence and Dale, 1978), bryophytes (Bodin and Nauwerk, 1968; Hutchinson, 1975) and Charophyta (Corillion, 1957; Forsberg, 1965; Stross, 1979). Again the short internode of shallow, relatively red-rich water is a typical phytochrome- mediated response and more or less capacity to vary internode length may help determine the zonation of particular species.

Radiant flux density ( 4 0 0 - 7 0 0 n m ) as o/o mean daily total in fulldaylight

Fig. 22. Rate of increase in mean internode length of shoots of transplants of Pota- mogeton richardsonii grown in full daylight (loo%), shade (12% daylight) and artificial light (4% daylight). (95% C.L.: 100% daylight & 0.13; 12% daylight 0.02 and 4% daylight f 0.12). From Spence and Dale (1978).


2. Specijic Leaf Area, Photosynthesis and Zonation

Direct links have been formed between plant zonation, leaf morphology and photosynthetic characteristics. A survey of about 100 Scottish lochs established the means and ranges in water depths occupied by a large number of species (Spence, 1964); data for five Potamogeton species are shown in Fig. 23. Plants of P. polygonifolius and P . obtusifolius, representing a shallow water and a deep water species with mutually exclusive depth ranges, were grown in a glasshouse; sun leaves were produced in full light with 16 h supplementary irradiation while shade leaves were grown under muslin and received about 6% PAR reaching the sun leaves (Spence and Chrystal, 1970b).

Ppowgonifohus I- - - - -- -t

Pnatans I - - - I

I? filiformis

Px zizii b - - - - , _- - Pgramineus +- - -+

Pobtusifolius I----I

Pprae/ongus l-----i

-i - -- --- b,-,- - - - - 4

I +

- - - - - - - - - - - - - - - - - - - - - - - - - - -

I 1 I I I 1

-40 0 40 00 120 160 200 240 200 320 Depthof water ( c m )

Fig. 23. The means, standard deviations (- ) and ranges (-----) of depth of water of Quadrats in which the named species occurred; from survey data of the macrophyiic vegetation of Scottish lochs. After Spence (1964), Spence-and Chrystal (1970a).

Flowering plants can, to varying degrees, adjust their leaf morphology to sun or shade conditions by altering their thickness and specific leaf area (SLA:

leaf area per unit leaf dry weight). For instance, specific leaf areas of various Potamogeton species increase with depth of water but the incremental increase is typical of the water body rather than the species (Spence et al., 1973). Sun leaves are thick with low SLA, shade leaves are thin with high SLA. Spence and Chrystal(1970b) showed that the sun and shade leaves of P. polygonifolius and P. obtusifolius grown in the glasshouse all had mutually exclusive specific leaf areas (Fig. 24).

In subsequent experiments, maximum rates of photosynthesis at the highest irradiance (80 pW m- ’) were found to decrease in the order: sun polygonifolius, shade polygonifolius, sun obtusifolius and shade obtusifolius, while light compensation points lay in the reverse order. These lower light compensation

I02 D. H. N. SPENCE

SLA cm' mfr leaf dry weight

0 1 5

Dark respiration 0, cm-' hr-'

IIL

t- I I

I I I I 1

Fig. 24. Specific leaf area, with standard error, of leaves of Potarnoyeron obrusffofius (obt.) and P. polygonfolius (poly.) grown in uniform sun or shade conditions in a glasshouse; together with their oxygen uptake, with standard error, in the dark in 2-3 h experiments using sun and shade leaf discs or detached leaves: in a Warburg apparatus with 0.1 M Warburg buffer no. 11 at 20°C. Data redrawn from Spence and Chrystal (1970b).

points follow directly from a decrease in dark respiration rates per unit leaf area (Fig. 24), while the photochemical capacity-gross photosynthesis per unit weight chlorophyll-remains relatively invariable. This decrease in dark respiration relates to a reduction in leaf weight per unit leaf area and, moreover, these rates of dark respiration are inversely proportional to SLA.

It follows therefore that, since magnitude of SLA is correlated with a physiological function, the development by two species of different intrinsic ranges in SLA has contributed to their occupying different depth zones.

In Lake Kalgaard the cylindrical-leaved species Littorellu unifioru and Zsoetes lacustris predominate, forming mutually exclusive and almost pure zones: L. unifroru from 0-2 m, 1. lacustris from 2.0-3.5 m (Sand-Jensen, 1978). After studying the seasonal variation in photosynthesis and dark respiration of both species, Sand-Jensen concluded that the lower dark respiration rate per unit leaf dry weight was the essential factor that enabled I . lacustris to penetrate deeper water than L. unifrora in this lake.

3. Photomorphogenesis, Photosynthesis at Lower Depth Limits

Where light rather than unsuitable sediment or low temperature determines the lower depth limits of a species in a lake, what are the physiological


controls? There is little hard fact at present. Reference has already been made to possible inhibition of flowering shoot production or of seed germination in Lobelia dortmanna. In the case of Hippuris oulgaris there is evidence that depth limits are primarily set by the light level below which carbohydrate requirements cannot be met (Bodkin, 1979). This contrasts with the situation reported by Stross (1979) for NitellaJIexilis in Lake George, New York. He notes particularly that the plants are still tall at this species’ depth limit and argues that a photomorphogenetic reaction alone may determine this limit- acting perhaps at the point of the life cycle when spores or some vegetative equivalent germinate, or when the protonema becomes a shoot. At the time of writing, this hypothesis has still to be tested.

The overall question of the mechanism of photomorphogenetic responses underwater, as distinct from the relevance of these responses to zonation, is examined by Spence (198 1) with particular reference to angiosperms.

4. Conclusions

The absence or poor development of underwater leaves may help restrict some emergents to relatively shallow water. One emergent species with submerged leaves reaches depths of 6 5 m and its heterophylly is photo-reversibly controlled. The light requirement for germination by two tropical Potamogeton species can be related to zonation while Lobelia dortmanna may occupy shallow water because of a high light requirement for flowering stem initiation and for seed germination. High anthocyanin production and the parastrophic position of chloroplasts in leaves, and short internodes, which are features of terrestrial species known to be influenced by high R/FR ratios, are found in various aquatic plants when growing in shallow water. Any significance to zonation is not known. Two species of Potamogeton have mutually exclusive ranges in water depth and this zonation relates to leaf morphology and physiology, because the shallow water species has an intrinsically low SLA

and high dark respiration per unit leaf area, the deep water species the converse.

C. Growth Forms, Plant Strategies and Interspecific Competition

The depth distribution of five growth forms in Scottish lochs is shown in Fig. 25. It is based mainly on a survey involving 382 quadrats which were grouped according to the growth forms of their predominant species and arranged in depth of water classes down to 3.2 m (Spence, 1964). This survey was largely carried out beyond wading depth by the use of a grab from a boat. Since then a number of lochs have been examined by diving with Scuba

104

40

D. H . N . SPENCE

Emergent

pc Floating - leaved

a Submerged broad-

leaved r-7 Rosette or lsoetid

-L /’

L I I I I I 1 I 0 1 2 3 4 5 6 ‘-5

Depth of water ( m )

Fig. 25. Growth forms of predominant species in relation to water depth and below 3.2 m as depth ranges only, where thick lines indicate predominance of broad leaved species or rosette (isoetid) species; below 6.5 m only Charophyta or Bryophyta occur. (Data to water depths of 3.2 m from Spence, (1964) and, below that. previously unpublished.)

(Spence, 1976a, and unpublished data) but data were not always recorded in quadrats so, beyond 3.2 m, only the predominance and overall depth range of each growth are shown. Broad-leaved submerged species are rarely rooted in sediments under water less than 1 m deep and, if so, even more rarely as dominants, indicating a largely adaptive connection between deep water and such plants in relation to shelter and shade. Down to its limits, however, the rosette or isoetid type appears to occur independently of depth. The submerged linear-leaved group includes Chara, Nitella and Fontinalis and accordingly extends furthest-to 15 m in Scotland (Loch Borralie).

Attention has already been drawn to the way in which growth habits of different perennial members of the Tracheophyta may determine their ability to survive burial by sediment and thus help determine succession in a changing environment. In addition to adaptations in leaf and shoot morphology discussed in the previous section, overall growth pattern, size and reproductive strategy will also help determine which succeeds in any competition for resources, principally light. Such patterns include disposition of dry matter between above- and below-ground parts; above ground, between leaves, fruit and (if present) stem turions and, below ground, between rhizomes, roots or other absorptive and anchoring organs, and root tubers. Specific differences in metabolic rates contributing for example to differences in light compensa-


tion points and in growth rates are also likely to be involved. However, in the almost total absence of suitable quantitative data, especially with reference to zonation, the comparisons which follow are largely qualitative.

Deep, clear granitic lakes of high altitude or latitude are dominated by bryophytes and the maximal biomass is small. In warmer lakes, bryophytes only dominate on rocks in shallow water or on sediments in deeper water than that occupied by angiosperms or Charophyta. In nutrient-poor north temperate lakes, typical species are Lobelia dortmanna, Pilularia globulifera, Myriophyllum tenellum, Eriocaulon septangulare and species of Elatine, Sub- ularia and Isoetes, together with submerged forms of Juncus species such as J . bulbosus or J . kochii. Sometimes J . bulbosus f.j?uitans can be more than 0.5 m long but otherwise all these species or their vicariads produce short plants or rosettes. Seddon (1965) suggested that I. lacustris is usually restricted to oligotrophic Welsh lakes by competition in more nutrient-rich lakes from large angiosperms. Although the species appeared to be likewise apparently confined in Scotland to waters of low alkalinity (Spence, 1964, 1967), it has recently been found, by diving, to form extensive stands at depths around 2 m, and to achieve leaf lengths up to 11 cm, in waters which are moderately nutrient-rich and frequently under a canopy of a large species like Potamo- geton natans (Spence and Allen, 1979; Spence et al., 1979b). Is the species only a “poor competitor” where sedimentation rates are high: often, that is, in the more nutrient-rich waters? By comparison, perhaps its ability to withstand sedimentation is a reason why the creeping, rosette species Littorella uniflora can dominate in both nutrient-poor and nutrient-rich lakes.

Clear, calcareous waters with nutrient-rich sediments and ze of 10 m or more can support the largest biomass, contributed by the largest Charophyta and submerged angiosperms, like Chara contraria, Potamogeton praelongus and P. amplifolius. By contrast, the linear-leaved P . jliformis is the predominant macrophyte in Loch Leven, an eutrophic lake with zC of 1 m. The only broad-leaved species is P. perfoliatus, the shallow-water form of which occurs occasionally (Jupp and Spence, 1977a). Sixty years ago I. lacustris, which had been present 40 years earlier, had gone but zc still extended over 5 m and P. praefongus was abundant between 3 and 5 m (West, 1910) as it is today in, for instance, Loch Borralie. This large plant never grows in less than 1.5 m depth of water, producing in all but the clearest lakes a dense leaf canopy just beneath the surface. Its absence points to a growth strategy inadequate for the stresses of an entirely wave-mixed macrophyte zone, which may include sediments too mobile for firm anchoring (Fig. 18).

Competition also may have been involved in the stages of lake enrichment before zc became too shallow. In some Madison, Wisconsin, lakes which have undergone similar eutrophication and reduced light penetration, two species of different growth form still co-exist (Titus and Adams, 1979): Vallisneria

106 D. H. N. SPENCE

americana, producing long-leaved rosettes, and Myriophyllum spicatum, a large canopy-former (which resembles P. praelongus in habit and habitat). V. americana, however, has been partly or wholly replaced by M. spicatum and these authors give photosynthetic evidence which suggests that, while native V. americana is favoured by midsummer conditions, the invasive M. spicatum is at an advantage at other times-hence its competitive “edge” in sites around 1 m deep which are, presumably, sheltered.

Since rosette and low-growing species are typical of nutrient-poor sites and are usually small, at least in water depths in which other angiosperms can attain considerable sizes because light is not limiting, they may have lower relative growth rates than all potentially larger species. This hypothesis is based on an analogy with the contrasted relative growth rates of species native to low or high-nutrient terrestrial sites (Grime and Hunt, 1979). Growth habits mentioned already, and low relative growth rates, would help explain the absence of most rosette and prostrate species from nutrient-rich sediments beneath both nutrient-rich and nutrient-poor (calcareous) water; also, their restriction in some of these nutrient-rich waters to the coarsest, shallow-water sediments. The lower light compensation points and other shade-adaptive features of many Bryophyta and Charophyta would in turn favour species of these groups in deeper water.

Another response which varies amongst different macrophytes (and microalgae) is the ability to utilize exogenous HCO; in photosynthesis (Steemann Nielsen, 1947; Raven, 1968; Allen and Spence, 1981, for example). Apart from calcareous lakes, low nutrient waters are accompanied by low bicarbonate concentrations so that the only direct carbon source for photosynthesis is C02; in mesotrophic, eutrophic and calcareous lakes, bicarbonate provides another potentially direct carbon source.

Allen and Spence (1981) studied the photosynthesis of 15 species of microalgae and macrophytes in bathing solutions of known alkalinity and carbon concentrations. The microalgae had much greater apparent affinities for HCO; and slightly greater apparent affinities for C02 than the macrophytes (including several previously established HCO; users); the macrophytes had larger apparent affinities for C02 than for HCO; and larger diffusive resistances to COZ. Rather than “users” and “non-users” of HCO; a gradation exists, use depending on HCO; as affected by alkalinity and pH of the bathing solution, and on the species’ HC0;-compensation point. From these experiments, and a knowledge of natural alkalinities, it is unlikely that most macrophytes assimilate a significant proportion of their carbon directly from HCO, until the pH of the water exceeds 9.0 and, then, their photosynthetic rate will only be about 10% of their potential rate at saturating C02 concentrations. Natural rates of photosynthesis of macrophytes and some microalgae are usually functions of exogenous concentration of C 0 2


while those of other microalgae are functions of the concentrations of COz and HCO;; this means that macrophytes vary in their potential and actual use of bicarbonate far less than microalgae and that the real competitive exclusion is likely to be achieved by microalgae acting on any macrophytes growing in water where microalgal carbon uptake has produced very high pH values in water of low alkalinity.

Besides the work ofTitus and Adams just referred to, one of the few attempts to discern ecological strategies of aquatic plants has been that of Raven et al. (1979) who have fitted the metabolic characteristics of giant-celled and small- celled macroalgae into the ecological types proposed by Dayton (1975) and Grime (1974, 1977). They show that the small-celled thalloid Enteromorpha intestinalis is metabolically a sun plant with a relatively high light compensation point because of a high rate of dark respiration per unit dry weight; strategically it is a fugitive or (Grime, 1979) a competitive species. Combined with a high RGR its abundance may be anticipated in sheltered shallow water of highly eutrophic lakes. On the other hand, Raven et al. demonstrate that the giant-celled Chara corallina is metabolically a shade plant, e.g. low light compensation point because of low dark respiration per unit dry weight (see their Table 1, p. 305), but they suggest its ability to behave as a stress- tolerant, perennial canopy former comes from its efficient long-distance transport mechanism (p. 89). Data of Van et al. (1978) shows how the angiosperm Hydrilla uerticillata in Florida seems to combine the metabolic features of a shade plant, such as low light compensation point, with rapid annual growth, formation of a canopy at the water surface and massive vegetative reproduction by turions, tubers and stem fragments-characteristics of competitive strategies.

While these observations indicate the complexities of metabolic and ecological interactions they do not encourage much meaningful comment on zonation. One approach to this aspect is provided by a recent comparison by Yen (1980) of the ecological strategies of Ludwigia peploides spp. monteui- densis, Myriophyllum brasiliense and Marsilea mutica, shallow water amphibious species in a lake in the Sydney region of New South Wales. Measurements were made in the field, and under conditions in which temperature, water depth and nutrient concentrations were controlled. Marsilea is native, the others introduced; the three species appear to co-exist because of niche differentiation via growth form, phenology and regeneration (viz., Grubb, 1977). For example, all have different optimal temperatures for dry matter production which show some relationship with their seasonal biomass data in the lake; only with shallow submergence does Marsilea have enough dry matter to allow sporocarp production-essential for surviving subsequent periods of drought; all species have high RGR’S when grown in a full nutrient medium but Marsilea responds least. This last finding

108 D. H. N. SPENCE

corroborates phenological data which suggest that Marsilea is stress-tolerant in Grime's (1979) terminology; the others, rather, being competitors. Judged by their growth rates, all three species have the same optimal depth or the same fundamental niche (Hutchinson, 1965). However, the floating leaves of Marsilea create shelter in which Ludwigia replaces that species and, in turn, Myriophyllum replaces Ludwigia so that only Myriophyllum occurs naturally at its optimal depth. In this important respect, the realized niche of Myriophyllum corresponds with its fundamental one but Ludwigia tends to occur to lakeward of that species, and Marsilea beyond Ludwigia or in gaps that may develop between either species.

VI. COMPETITION WITH MICROALGAE AND THE CONTROL OF MACROPHYTE ZONATION

BY SUBSTRATE OR BY LIGHT

A. Competition with Microalgae, and Extent of ze

A broad relationship has been established between zc and K,i,, with the obvious implication that light controls the depth penetration of macrophytes. In Section I1 the roles of suspended inorganic matter, yellow substance, phytoplankton and epiphytes in controlling underwater spectral intensity were discussed. In certain cases a strong influence is exerted by yellow substance as allochthonous peaty material and by sediment as a clay suspension but in general it is assumed that microalgae limit the underwater radiant energy reaching macrophytes. It has been argued elsewhere (Spence, 1976a) that a key to the depth penetration and to some extent the amount of submerged macrophytes in any lake is the degree of competition with phytoplankton for light and nutrients, particularly inorganic carbon; periphyton, as actively or passively attached epiphytes, may enhance any competitive effects of phytoplankton.

Specifically it was contended that zc in any lake is generally controlled by water chemistry in so far as water chemistry determines phytoplankton density and, therefore, the extent of competition with macrophytes. It was shown in the same paper that, for undisturbed catchments, those lakes studied where alkalinity was less than 0.4 m-equiv l-', and marl lakes, always had low phytoplankton densities and that zc was consequently predictable from a measurement of &,in. In the remaining lakes in the series with alkalinities over 0 4 m-equiv 1- ', phytoplankton densities had higher maxima and more variability in any one year, so zc was reduced but unpredictable from a random

THE ZONATION OF PLANTS IN FRESHWATER LAKES I09

reading of a highly variable Kmin. Increases in density and in unpredictability were considered to be consequences of seasonally varied surface water enrichment, bringing increased but fluctuating phytoplankton competition with macrophytes. Subsequently, Jubb and Spence (1977a) showed that over three summers in Loch Leven (alkalinity about 1 m-equiv I - ' ) the growth of Potamogeton jiliformis was indirectly controlled by high phytoplankton densities, especially when blooms of Anabaena species developed in late summer as a result of high levels of phosphorus.

Phillips et al. (1978) have proposed that the well-documented loss of submerged macrophytes from artificially fertilized lakes is the result of increased growth of, and shading by, epiphytes and filamentous algae associated with weed beds, and that phytoplankton development is subsequent rather than causative. These authors base their argument on an unproved allelopathic one: that substances excreted by submerged macrophytes suppress phytoplankton while epiphytes can tolerate them, so increased nutrient loading in a lake initially encourages macrophytes and then epiphytes, which suppress the macrophytes, whereupon phytoplankton in turn increases. Brammer (1978) has since shown that phytoplankton is suppressed in the vicinity of submerged Stratiotes aloides in parts of two shallow lakes (one in Sweden and one in Poland) and attributes this suppression to competition by Stratiotes for nutrients, together with changes in the ionic composition of the water, rather than to allelopathy. Allen and Spence (1981) produce strong presumptive evidence that photosynthesis by certain microalgae can, inter a h by raising solution pH, severely limit carbon supply for submerged macrophytes in enriched but poorly buffered waters.

There seems little doubt however that suppression of submerged angiosperms and Charophyta by epiphytes and filamentous algae does occur in enriched waters, whatever the mechanism. Like the abundance of Entero- morpha intestinalis and Cladophora glomerata, this may be commonest in small, relatively sheltered water bodies or in sheltered bays of larger lakes whereas suppression by phytoplankton may be a commoner feature of the more turbulent water of large lakes generally.

The causes of high microalgal crops form a subject in themselves and it is only stated here that the apparent relationship between phytoplankton density and alkalinity, alluded to in a previous paragraph, is probably a function of soluble phosphorus levels. From an unpublished study of the extensive data of Lohammar (1938) on Swedish lakes, it seems likely that an alkalinity around 0.4 m-equiv I - ' in Northern Europe represents an approximate level of catchment fertility above which agricultural improvement and therefore P additions have been economically worthwhile; these P additions would in turn influence phytoplankton density and thus the degree of competition with macrophytes. In climates with cool summers,

110 D. H. N . SPENCE

catchments with shallow soils around marl lakes may mean a preponderance of “unimproved” pasture leading, in conjunction with the high concentration of calcium, to low P levels in the lakes themselves (like those in Loch Borralie). On the other hand, in any lake with alkalinity below 0-4 m-equiv l-’, P additions will increase microalgal growth dramatically and, in this poorly buffered water, the photosynthesis of certain microalgae will eventually result in high pH and low carbon concentrations. Such phytoplankton/phosphorus relationships form the basis of predictive models (e.g. Dillon and Rigler, 1974).

B. The Macrophyte Biomass/Depth Curve: some Implications

The similar shapes of the curves of submerged biomass upon depth on the open shores in a number of lakes showed from a maximum at a given depth, a decline towards shallow water and a logarithmic decrease towards deeper water (Spence, 1976a, b), consistent with limitations by exposure and light respectively. This led to the hypothesis that the resultant of these opposing factors determines the depth at which maximal biomass occurs, measured preferably when the lake is producing its largest seasonal overall macrophyte biomass. Subsequent studies by Bodkin (1979) of growth and photosynthesis of Hippuris uulgaris along a depth gradient in one of these lakes (Loch Borralie) showed that short-term net photosynthesis of enclosed detached shoots declines logarithmically with PAR over the depth 1-4 m (Fig. 26); however, the aggregate shoot and root length of individual transplants along the species’ natural depth range in the lake, 2-6.5 m, was indeed limited in shallow water as well as at greater depths (Fig. 27), thus conforming to the hypothesis.

In spite of such support, however, the general hypothesis needs to be qualified. First, as well as stopping growth at the macrophyte depth limit, light is assumed to limit growth down the depth gradient, producing a log linear relationship between maximal seasonal biomass and depth. This assumption rests on another one, that maximal biomass accurately estimates annual net production, i.e. production/biomass (P/B) is a constant; indeed, it only slightly under-estimates it (Raspopov, 1972; Westlake, 1979, i.e. P/B - 1 . For some angiosperms in fertile lakes, however, the under-estimate can reach 707; (Adams and McCracken, 1974) while for a typical species of oligotrophic water such as Lobelia dortmanna the over-estimate exceeds 45% (Moeller, 1978). Clearly, the match between maximal seasonal biomass and water depth in a lake is only as close to that of net annual production and


In PAR

Fig. 26. Net photosynthesis in relation to the natural logarithm of PAR for shoots of Hippuris vulgaris incubated in Loch Borralie 15th September 1977 (A) and 18th March 1978 ( + ). Incubation depths are listed. After Bodkin (1979).

depth, as the ratio of net production to biomass is to unity. Second, seasonal variation may occur in the phenology of a dominant at different depths, as with Scirpus subterminalis in Lawrence Lake, Michigan (Rich et al., 1971). Finally, the extent may vary to which substrates are colonizable even in deep water.

None the less, in those cases where P/B is near unity it should be possible to distinguish between a maximal biomass that is small because of exposure and one that, in the absence of exposure, is small because of nutrient-poor sediment. Further, this concept that variation of biomass as water deepens, in a lake of given trophic status, is under the control of both wave action and light leads to a hypothesis which unites both factors.

112 D. H. N. SPENCE

I

1 I I I I I I J 0 1 2 3 4 5 6 7

Depth of water (ml

Fig. 27. Total shoot and rhizome length of Hippuris uulgaris plants placed in pots a t five depths of water in Loch Borralie in March 1977 and harvested in June 1977. After Bodkin (1979).

VII. CONCLUDING HYPOTHESIS WHEN SUBSTRATE OR LIGHT CONTROLS THE DISTRIBUTION OF MACROPHYTES IN LAKES

It is concluded that, in a given climate, the shape and size of the lake basin determines the overall depth of the wave-mixed zone (z,) while factors controlling the underwater light climate primarily determine the depth of the macrophyte zone (2,) which, barring unsuitable substrata at its base, is reasonably uniform in that lake.

It is postulated that the extent to which wave action-with-sediment, or light, determines zonation in a lake depends on the relative amount of its macrophyte lying within or below the wave-mixed zone, although the wave-mixed zone may vary in depth in the same lake because of differences in aspect of shores (Fig. 28).

Let us start by assuming that the macrophyte zone of a lake lies mainly in the wave-exposed zone. This means that a lesser portion lies in the purely depositional zone which occurs in deeper water or, on occasional sheltered stretches of shore, in shallow water. To vertical variation in wave action and sediment type down any shore will be added horizontal variation in these

THE ZONATION OF PLANTS IN FRESHWATER LAKES 1 I3

zc zw 4 = zw zc zw

Macrophyte zone ( zc) lies wholly or mainly in zw wave oction-with- sediment control macrophyte zonotion

zc >2zw

More than half the macrophyte zone of the lake lies below the wave-mixed zone,light exerts the prime control on zonation

z,> zw > 2 Z W

Macrophyte zone exceeds the depth of the wave-mixed zone.but less than twice the depth of the wovemixed zone Both waveaction- with-sediment, and light, determine zonation

Fig. 28. Diagram to illustrate situations where the macrophyte zone in a lake is controlled primarily by (1) wave action-with-sediment and (2) light; in (3), both wave action-with-sediment and light determine zonation. (For explanation, see text.)

factors between stretches of exposed and, less frequent, sheltered shore. Variation may also occur, in the vertical and horizontal planes, in the rate of sedimentation. In lakes of this type therefore the degree of wave action and the type of sediment, and locally its rate of deposition, exert prime control on the growth form and stature, distribution, zonation and biomass of all macrophytes. Species diversity decreases between sheltered and exposed shores, often as strikingly as it does with increasing water depth.

114 D. H. N. SPENCE

Let us next assume that the macrophyte zone lies mainly below the wave- mixed zone, in the purely depositional zone. Apart from some depositional areas among sheltered bays in shallow water, this means that most of the vegetation grows in a zone where at any depth around the lake the sediments are uniform and (pre-existing rock or boulder slopes excluded) vary only with depth. In these circumstances, evidence from biomass, physiological and morphological studies indicate that underwater light quality and quantity exert the prime control on zonation. Species diversity decreases as water deepens and may relate to increasing needs for shade adaptation.

In a lake where the macrophyte zone is not more than twice the depth of the wave-mixed zone, then both sediment type and light control zonation. To summarize, where zw > or = zc, wave action with sediment type determine zonation ofplants while, where zc > 2zw, light determines zonation and, where zc 3- 2zw, both wave action with sediment, and light, determine zonation.

As outlined in Smith (1979) the hydraulic conditions which delimit the wave-mixed zone of a shore of a lake can now be identified quantitatively so it should be possible to test this hypothesis which distinguishes between lakes having depth zones colonized by macrophytes lying wholly, and those lying partly, within the wave-mixed zone.

ACKNOWLEDGEMENTS

I should like to thank Dr P. C . Bodkin and Dr Shangtien Yen for permission to quote from their unpublished work, M r Ian Smith and Professor Jean Wooten for their comments on an early draft of this review, Dr David Ford for his helpful editorial assistance and Miss Anita Brien and Miss Sandra Sinclair for their efficient typing. The original field and laboratory work reported here has been carried out by research students and myself with support from the Natural Environment Research Council and the St Andrews University Scholarship Committee.


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NOTES

1. Phanerophytes-woody plants with perennating buds more than 25 cm above soil

2. Hydrophytes-water plants; with perennating buds below the water surface

3. Helophytes-marsh plants with perennating buds at or just above the soil surface. 4. Nomenclature of British angiosperms and vascular cryptogams follow Clapham

level.

(Spence, 1964; a broader definition than the original of Raunkiaer, 1937).

et al. (1962).

APPENDIX: LIST OF SYMBOLS

= phase velocity or windspeed = diameter of particle = Einstein, or mol of quanta = downwelling vector irradiance = upwelling vector irradiance = fetch, a t point of measurement downwind = far red light at 730 nm = wave height = light intensity a t subsurface ( z = 0). horizontal detector = light intensity a t depth z, horizontal detector = vertical diffuse attenuation coefficient, downwelling irradiance = vertical diffuse attenuation coefficient, upwelling irradiance = Kd, of light through broad band pass blue, green, red filters = least attenuated of K B , K G and K R = K d , integrated over 400-700 nm = Leaf Area Index, unit leaf area per unit ground area = length = mass transfer per unit area in unit time = eddy viscosity = form of phytochrome mainly induced at 660 nm


P ,

r R

R e Scuba

P A R

SLA

t T U tr u / d

VS

= form of phytochrome mainly induced at 730 nm = Photosynthetically active radiation (4W700 nm) = radius of orbital motion beneath waves = red light a t 660 nm = Reynold’s number, ratio of inertial to viscous forces in a fluid = self contained underwater breathing apparatus = Specific Leaf Area, unit leaf area per unit leaf dry wt = time = temperature = horizontal current velocity at any depth = mean horizontal current velocity = friction or shear velocity due to the drift current near the lake bed = settling velocity = depth of water: below lake surface (light readings, zmr ievr z , ) above

lake bed (velocity profiles, z , ) and between lake surface and lake bed ( Z C )

= depth of zone colonized by macrophytes = depth of mixed zone, epilimnion in a stratified lake or z - zo in an

= euphotic zone, having about 17, subsurface PAR

= depth of zero current velocity, equals “roughness” height above bed = depth of wave-mixed zone = thickness of laminar sub-layer = wavelength of electromagnetic radiation = coefficient of kinematic viscosity = density of water = flux of momentum per unit area, Reynold’s stress = stress on lake bed = frequency of electromagnetic radiation

unstratified lake

The Evolutionary Consequences of Interspecific Competition

WALLACE ARTHUR

I . Introduction . . . . . . . . . . . . . . . . I1 . Proposed Patterns of Competitively-induced Evolution . . . . .

A . Character Displacement . . . . . . . . . . . . B . Character Convergence . . . . . . . . . . . . C . Character Release . . . . . . . . . . . . . D . Evolution of Competitive Ability . . . . . . . . . . E . Genetic Feedback . . . . . . . . . . . . . F . Effects of Competition on Polymorphic Loci . . . . . . .

A . Introduction . . . . . . . . . . . . . . . B . The Models . . . . . . . . . . . . . . .

. . . . . . A . Criteria for Conclusive Demonstration of Character Displacement in

Natural Populations . . . . . . . . . . . . . B . Criteria for Conclusive Demonstration of the Evolution of Interspecific

V . The Evidence . . . . . . . . . . . . . . .

B . Changes in the Variance of Quantitative Characters . . . . . C . Changes in Heterozygosity and Gene-frequency . . . . . .

VI . Conclusions . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . .

I11 . Some Coevolutionary Models . . . . . . . . . . .

IV . Criteria for Demonstrating Competitive Selection

Competitive Ability in Experimental Populations

A . Changes in the Mean of Quantitative Characters

. . . . .

. . . . .

i27 129 129 131 131 132 133 134 136 136 137 145

145

149 150 150 173 174 181 182 182

I . INTRODUCTION

When populations of two different species compete with each other. both will suffer increased mortality and/or decreased natality . However. such effects are unlikely to be spread evenly across the various members of either population . If the two species concerned are cross-fertilizing plants or animals. then their populations will be genetically heterogeneous and indeed are likely to exhibit polymorphism at a large proportion of their genetic loci . (For a

128 WALLACE ARTHUR

review of the extent and nature of genetic variation in natural populations see Lewontin, 1974.) It is still not clear whether the majority of these polymorphisms affect fitness, but intensive studies on some loci have shown that in at least some polymorphisms, the different variants differ in their fitness under certain environmental conditions (see Clarke, 1975). It is likely that some of the polymorphisms affecting fitness influence the interspecific competitive ability. If this is so, then the competing populations may each evolve as a result of their competitive interaction. This will apply equally to chromosomal polymorphism and to heritable variation in quantitative characters, where these also affect competitive ability.

Early models of interspecific competition did not take into account the possibility that different genetic variants within each population might differ in their ability to compete (for example Volterra, 1926). Nevertheless, such variation in competitive ability has now been shown to exist in a number of cases (see Section V). More recent models of competition, such as that of Lawlor and Maynard Smith (1976), have included provision for genetic variation. Whether competitively-induced evolutionary change will actually be effective in natural populations depends partly on the competitive population dynamics. If one species is rapidly excluded by a superior competitor it will have little time in which to exhibit an evolutionary response. Given a state of stable coexistence, however, or a very slow trends towards competitive exclusion, a similar selective differential within one (or both) species will have a much longer time in which to take effect.

The main aim of this article is to assess the degree to which genetic changes in mixed species populations can be ascribed to natural selection resulting from interspecific competition. In order to achieve this aim, I will proceed through a number of steps. Firstly, the main postulated patterns of competitively-induced evolution will be outlined. Secondly, the relevant theoretical models will be briefly discussed. A series of criteria will then be developed which should be satisfied before an instance of variation in some character can be conclusively attributed to selection stemming from interspecific competition. Finally, experimental and observational case-studies on a wide range of species will be reviewed in the light of these criteria.

It is necessary at the outset to give the definition of interspecific competition which will be adopted, since several alternative definitions are available. The populations of two species are considered to be in competition here if each exerts an inhibitory effect on the growth-rate or equilibrium size of the other. This corresponds to the (-, -) population-interaction described by Odum (1971) and elaborated by Williamson (1972). The mutual inhibitory effect can be achieved in two rather different ways; directly, for example, by the secretion of substances which harm the other species, in which case we have interference competition; or indirectly, through depletion of a common

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION 129

limiting resource, which may be described as exploitative competition. It should be stressed that if only one population suffers in the interaction, while the other is unaffected, then this falls outside the definition of competition adopted, and this asymmetrical type of interaction is referred to as amensalism. For further discussion of the relationships between competition and other sorts of population-interaction, see Odum (1971; p. 21 1). For verbal economy I will often use the words competition, competitor and competitive in this review without a qualifying adjective. In all such cases the interspecific sense should be inferred. Finally, most of the discussion is centred on Competition between two species, since until this simplest case is understood it seems unlikely that discussion of the simultaneous coevolution of many competing species will be fruitful.

11. PROPOSED PATTERNS OF COMPETITIVELY-INDUCED EVOLUTION

Several different forms of evolutionary change, resulting from interspecific competition, have been proposed. These include character displacement (Brown and Wilson, 1956), character convergence (see Cody, 1973), alteration of the variance of morphological characters (Van Valen, 1965), evolution of competitive ability (Moore, 1952b) and genetic feedback (Pimentel et al., 1965). The aim of this section is to consider what is meant by such terms; and to discuss their relationships to, and differences from, each other. These discussions will serve two purposes. Firstly, they will reveal in some detail, and at an early stage, what the alternative possible modes of competitively- induced evolution are; and secondly, they will lead to the remainder of the review being left relatively free of controversy over terminology.

A. Character Displacement

It has long been held that a common evolutionary consequence ofcompetition between two species is divergence of the species, in some character, in areas of sympatry. The character concerned may be ecological, behavioural, morphological or physiological, though the last of these possibilities has received little attention. This sort of divergence was termed character displacement by Brown and Wilson (1956), a term which has gained general acceptance. These authors also distinguished between reproductive and competitive character displacement. The former is an evolutionary response to the selective disadvantage of producing interspecific hybrids and is thus

130 WALLACE ARTHUR

synonymous with the Wallace Effect (see V. Grant, 1966 and review by Murray, 1972). Competitive character displacement, on the other hand, is an evolutionary response to interspecific competition. In the present article, I will be concerned only with competitive character displacement.

Grant (1972), in a critical review of the subject, redefined character displacement, and some of his points deserve brief mention here. Firstly, in their original definition, Brown and Wilson (1 956) referred specifically to animals; Grant extended the definition to include plants. In this respect, Grant’s definition seems preferable. There is some evidence for reproductive character displacement in plants (see Levin, 1970) though as yet there appears to be no botanical evidence for competitive displacement of non-reproductive characters. (Levin has suggested, though, that plants may diverge in reproductive characters for competitive reasons-for example, floral structure of angiosperms may diverge in sympatry to avoid competition for a limited supply of pollinators.) Secondly, Grant (1972) has restricted the term character displacement to include only changes in morphological characters. This is desirable on two grounds: because most studies of character displacement have in fact been morphologically orientated; and because the problem of unknown, possibly low heritabilities (discussed at some length later in connection with morphological characters) is even more acute with non- morphological characters. Indeed it is likely, though by no means certain, that many ecological/behavioural changes associated with interspecific competition, such as Schoener’s (1975) “habitat shift”, may be non- evolutionary responses. The third of Grant’s (1972) modifications to the definition of character displacement will not be accepted here. Grant has argued that both convergence and divergence of a character in sympatry should be included under the overall heading of “character displacement”. Thus there would be convergent character displacement and divergent character displacement. This seems unnecessarily cumbersome and so I will treat convergence as a totally separate category from displacement. In a fourth modification, Grant (1972) distinguished between cases where allopatry preceded sympatry temporally and those where the reverse was true, considering only the former cases to be describable as character displacement. This distinction, which I will not make here, seems unhelpful since the time- sequence of allopatry and sympatry is usually unknown. Finally Grant (1972) has distinguished between unilateral and bilateral displacement depending on whether one or both species displace in sympatry. This seems a useful distinction and I will retain it here. Mayr (1963) uses the term character divergence in preference to character displacement, apparently on the basis that Darwin (1 859) devoted much discussion to “divergence of character”. However, Darwin (1 859) used his “divergence of character” in a different, and much broader sense than Brown and Wilson (1956) used their term of

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION 1 3 1

character displacement. Thus I will adhere to Brown and Wilson’s term. Throughout this article, then, competitive character displacement will refer

to: the process by which the mean values of a morphological character, in two competing species, displace away from each other in areas of sympatry, or converge towards each other in allopatry, because of the presence in sympatric populations, but not in allopatric ones, of a selective pressure stemming from interspecific competition.

B. Character Convergence

When two species become more similar in some character in sympatry, this may be termed character convergence-competitive character convergence where the selection producing the convergence emanates from competition. A theoretical argument suggesting that competition might lead to character convergence was put forward by MacArthur and Levins (1967), though this argument has been disputed by Lawlor and Maynard Smith (1976). Details of that dispute will be given in Section 111. The evidence for competitive convergence, as opposed to competitive displacement of characters is more restricted and is mostly related to interspecific territoriality in birds (see Cody, 1973). As with character displacement, the discussion of case-studies will be restricted to morphological characters, and only competitive convergence will be treated, though the difficulties of separating this from other sorts of sympatric convergence will form a major part of the discussion.

C. Character Release

Both of the processes described above represent alterations in the mean value of a character. However, it has also been proposed that, as a result of competition, a change in the variance of a character may occur. Basically, an expansion of the feeding habits or the numbers of microsites occupied is thought to take place when a population moves to a relatively competitor- free environment such as, for example, an island. This phenomenon has been termed ecological release (Wilson, 1961). Note that the related term competitive release has been used by Yeaton and Cody (1974) in the slightly different sense of an increase in population density in competitor-free areas. An increased variability in ecological habits may lead to an increased variance of morphological characters (Van Valen, 1965) and I will refer to this as character release, in order to stress its relation to ecological and competitive release. (It should be noted that this usage of the term character release differs from Grant’s (1972) usage.) The process concerned is an example of

132 WALLACE ARTHUR

disruptive selection if migration is from a species-rich to a species-poor area, or stabilizing selection if migration is in the reverse direction. Since disruptive/ stabilizing selection and directional selection may occur simultaneously on the same character, release of a morphological character is not necessarily an alternative to displacement/convergence of the same character; the two processes may occur together.

D. Evolution of Competitive Ability

Much of the evidence for and discussion of competitive character displacement, convergence and release has come from field-workers studying populations of vertebrates. However, considerable experimental work on interspecific competition has been conducted on laboratory populations of insects, notably Drosophila and Tribolium, as well as plants, and i t is largely from this work that the concept of the evolution of competitive ability has arisen.

A frequent observation in an experiment in which two species of insect are in competition for some food-medium, is that at some stage in the experiment the species-frequency trajectory in one cage suddenly alters from a gradual march towards competitive exclusion of one species to an increase in the frequency of that same species. In other words there is a reversal of competitive dominance, despite the environmental conditions being kept relatively constant. This sort of observation has been made on a number of occasions (for example, Ayala, 1966, 1969) and has often been interpreted as an evolutionary increase in the competitive ability of the species whose frequency has increased after first declining. Several points need to be made here.

If competitive ability is to be measured, the variable by which it is measured should be independent of the species-frequency (i.e. the number of individuals of one species as a fraction, or percentage, of the combined numbers). It is thus dubious, at least in comparing competitive abilities between cages with different species-frequencies, to use the change in species-frequency itself (i.e. the equivalent of the geneticist’s Aq) as a measure of competitive ability. In fact the differential in competitive abilities that will produce an increase in the frequency of species 1 (say) of 17% in one generation of competition starting with equal numbers of both species will only produce a 9% alteration in species-frequency in an experiment started at 80% of species 1 . Thus i t is desirable to have a different measure of competitive ability, and one which has no inherent relationship with the species-frequency. One possible measure is the cross-product-ratio or CPR (see Cook, 1971 and Arthur, 1980a, b) or its natural log, which has been used as a measure of fitness in studies of polymorphism (for example Muggleton, 1979). The CPR measuring the competitive ability of species 1 relative to species 2

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION 1 33

where N is the population size in the i th generation, subscripts refer to species, and N ‘ is the population size in the (i + l)Ih generation. In some situations, such as comparison of competitive abilities in cages started at the same species-frequency, or where the alteration in competitive ability is very marked (such as a “reversal”), the change in species-frequency itself may be a good enough estimator of competitive ability.

If competitive ability is seen to alter during the course of an experiment (with reversals of dominance being an extreme case), and if this change can be attributed to selection, then there are two possible selective explanations.

(1) The species which has increased in competitive ability has done so because it has become more efficient at inhibiting the other species or more efficient at obtaining or converting the resource it was already using.

(2) The relative patterns of resource-utilization may have altered; for example, the species which has increased in competitive ability may have evolved so that it can utilize a greater, and/or shifted range of resources than before.

The first of these explanations is often assumed to be correct because a single food-medium is generally used in the sort of experiment concerned. However, even a single food-medium may be chemically heterogeneous; some experiments in which competitive ability putatively evolved have provided more than one resource (for example, three in the experiments of Pimentel et al., 1965); and even a resource that is chemically homogeneous may require differing strategies to utilize different portions of it, for example, different layers within a resource-bottle. Thus the second explanation given above cannot be eliminated on a priori grounds alone, and so the relationship between character displacement (or its behavioural equivalent) and the evolution of competitive ability remains obscure. If explanation (1) is correct, the two processes are very different; if (2) is correct, they may not be.

E. Genetic Feedback

This concept was advanced in conjunction with the results of an experiment by Pimentel et al. (1965) and will be described in detail along with those experimental results in Section V.A. Briefly, the hypothesis of genetic feedback is an extension of the idea that competitive abilities may evolve, whereby: (a) selection for increased interspecific competitive ability is stronger on the rarer species which thus evolves faster and eventually becomes competitively superior; (b) the process is then reversed; and (c) a series of evolutionary and

134 WALLACE ARTHUR

dynamic oscillations thus results, leading eventually to the stable coexistence of the two species.

F. Effects of Competition on Polymorphic Loci

So far, I have discussed only the evolution of quantitative characters in response to competition between species. Although variation in such characters is contributed to by polymorphic variation at a large number of loci, the effects of most loci on their own are small. However, several studies have now been conducted in which the effect of selection on one polymorphic locus, or on a small group of such loci, has provided the focus of attention (Murphy (1976), Arthur (1978, 1980c), Powell and Wistrand (1978), Clark (1979) and Gosling (1980)). These studies will be described in Section V.C, but I will briefly state here the possible results of competitive selection at this level using, for illustrative purposes, the simplified situation of a biallelic locus, in each of two competing species (with alleles A1, A2 in species A ; B1, B2 in species B), which in some way affects competition. First of all, considering each of the species in turn, there are two possibilities:

(1) If one homozygote is a superior competitor to the other, and there is complete, partial or no dominance, then the favoured allele will eventually become fixed in the population.

(2) If the heterozygote is the most able interspecific competitor, the polymorphism will be balanced by competition, and will thus persist in the population with an equilibrium gene-frequency determined by the relative competitive abilities of the two homozygotes.

It should be noted that these two possibilities exist when any selective agent is operating; here, they have merely been stated in such a way as to refer specifically to the situation where the selection stems from competition. However, when competition is the selective agent, both species may evolve. Thus their coevolution needs to be considered. Several combinations of the results described above are possible, since selection will operate separately in the two species, and there is no necessity for the ranking of genotypes by competitive ability to be the same in both. I wish in particular to distinguish between three forms of coevolution, which are as follows:

(1) The selective differential within each species may depend on the gene- frequency in the other (an extension of the concept of frequency-dependent selection (Clarke and O’Donald, 1964) to a two-species situation) such that single-locus equivalents of displacement and convergence are possible. Thus the species might displace or converge in gene-frequency in sympatric regions.

(2) The selective differential within each species may be independent of the gene-frequency in the other. This would happen if one genotype, in each species, is simply a superior interspecific competitor to other genotypes. The


result of this situation would be a parallel change in sympatry (p(A 1 ) increases in species A and p(B1) increases in species B) or an antithetical change (p(Al) increases but p(B1) decreases). If the polymorphisms are not analogous, then of course it would not be possible to say whether the coevolutionary changes were parallel or antithetical, but it would still be possible to distinguish these two possibilities, taken together, from the situation described under (1).

(3) It is important to stress that, especially if species compete by interference rather than exploitation, the genetic bases of susceptibility and antagonistic ability may be separate. In such cases, limit cycles in gene-frequency may result. If, instead of one locus in each species we now consider two-an “attack” and a “defence” locus, then two limit cycles may be set up if one of species A’s “attack” genotypes is more effective on one of species B’s “defence” genotypes, and the same holds for species B “attacking” species A. This possibility has received little attention, though a simpler sort of limit-cycling behaviour in parasite-host coevolution has been dealt with by Clarke (1976).

To summarize, then, there are several possible patterns of competitively- induced evolutionary change. Some of these, such as character displacement and character convergence, are mutually exclusive. Others, such as character displacement and character release, are not. Also, some relationships such as that between character displacement and the evolution of competitive ability, are obscure. Thus for any pair of competing species in a natural community, many possibilities are open, ranging from a complete lack of coevolution because (for example) of rapid competitive exclusion of one species, to the simultaneous occurrence of two or more of the processes described in this section. It is now necessary to enquire:

(1) For which of these evolutionary patterns is there clear evidence from at least one species-pair?

(2) How taxonomically and geographically widespread are the various patterns described, both in absolute terms and relative to each other?

In order to answer these questions, it is necessary to consider the evidence from individual case-studies, and this will be done in Section V. First, though, some coevolutionary models which expand on some of the proposals of this section will be briefly discussed (Section III), and some criteria will be developed (Section IV) that case-studies should satisfy if they are to be regarded as providing conclusive evidence in favour of a particular coevolutionary pattern.

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111. SOME COEVOLUTIONARY MODELS

A. Introduction

Initially, the models of population genetics assumed fixed selective coefficients, suggesting an unrealistic insensitivity of selection to population density, frequency of different phenotypes within the population, and the relative frequencies of the species concerned and those with which i t interacted, such as competitors and parasites. Early ecological models, as already stressed, often assumed the equally unrealistic situation of genetically homogeneous populations. However, a substantial collection of models, treating both genetic and ecological factors as variables has now been built up; these are known as coevolutionary models, and have recently been reviewed by Slatkin and Maynard Smith (1979).

Two somewhat separate questions have been asked in relation to the coevolution of interacting species:

(1) What effects do the population dynamics of the interaction have on the extent and nature of evolutionary change in the interacting populations?

(2) What are the effects of the genetic structure and evolution of the populations concerned on the outcome of their numerical interactions?

These questions may be applied equally, of course, to predation and parasitism as well as interspecific competition. Also, with some rewording, they may be applied to a joint study of the evolution and dynamics of a single-species population. In the present article, I will be concerned only with a very restricted section of the field of coevolution. Firstly, only situations of interspecific competition will be considered. Secondly, since the article is concerned with “the evolutionary consequences of interspecific competition”, the emphasis will be on question (1) rather than question ( 2 ) . Finally, I will deal for the most part with two-species, as opposed to multi-species models, since the latter remain to be developed. Those readers wishing a more comprehensive review of coevolutionary models should consult Slatkin and Maynard Smith’s (1979) paper.

The theoretical approach to the coevolution of competing species was pioneered by MacArthur and Levins (1964, 1967), and subsequent models have been provided by Levin (1969a, 1971), Leon (1974), Bulmer (1974), Crozier (1 974), Lawlor and Maynard Smith ( 1 976), Roughgarden ( 1976), Fenchel and Christiansen (1977) and Slatkin (1980). These various models differ in some important ways and, as a result, arrive at sometimes different conclusions. The emphasis of the models at the outset may be different, some being predominantly concerned with directional evolutionary changes resulting from interspecific competition (for example Crozier, 1974), while


others (such as Llon, 1974) have been more preoccupied with the role of competition in maintaining genetic variability within the competing populations. Also, some models have dealt with continuously-variable characters, others with discrete variation. The models will now be briefly outlined, with emphasis on their assumptions and their predictions.

B. The Models

MacArthur and Levins (1967) developed a graphical analysis of evolutionary change in competitors, following on from their earlier (1964) largely ecological study. These authors considered the evolution of a continuously variable character of unspecified inheritance, namely “niche position” (not breadth). A situation was described in which two species were already present in a community and a third, immigrant species subsequently appeared. Given sufficient genetic variation, the immigrant will evolve to a point of minimum combined competitive inhibition from the two resident species (i.e. minimum

a

@

Fig. 1. Graphical illustration of evolutionary change in niche-location, 4) represents phenotype, defined as the midpoint of the niche along some environmental axis. a1 and a2 are the values of the competition coefficients of the two (resident) competing species: (a) niche-separation; (b) “niche-convergence”. See text for further details. From MacArthur and Levins (1967).

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a1 + a2). This results in a divergence of the immigrant away from either of the other two species to the point Q in cases where the two species are themselves sufficiently distant from each other that a1 + a2 is at a minimum between the separate modal a-values of species 1 and 2 (see Fig. la). However, when the a1 and a2 curves are closer (Fig. lb), there is no “intermediate minimum” and the immigrant converges, in niche-location, towards point P , which corresponds to the modal a-value of the less severe competitor. MacArthur and Levins point out that this convergence will only occur if “there is a large linear array of competing species”. This qualification is necessary since, if there is not such an array, the immigrant species may evolve past point P and hence ultimately diverge from both of the others. Lawlor and Maynard Smith (1976) dispute MacArthur and Levins’ second prediction, namely convergence, claiming that convergence would also occur in the absence of competition and so cannot be regarded as an evolutionary outcome of it. It is certainly clear from Fig. Ib that the convergence of the immigrant towards species 2 would occur in the absence of species 2 due simply to the immigrant’s divergence from species 1. (Whether the immigrant would move past point P in this case would depend on the amount of genetic variability present and on the presence or absence of further competitors.)

A more detailed model has been developed by Levin (1969a, 1971) and is based on the Lotka-Volterra equation:

(Ki - N,- ctNj ~ = riNi dNi dt

where N is the population size, r the intrinsic rate of increase, K the carrying capacity, a the competition coefficient; and i, j = 1, 2 for the simplified case of 2-species competition.

Levin introduced variation into the parameters r, K and r so that the model becomes:

where h refers to genotypes within species i (there are gi of them); k refers to genotypes within speciesj; and (i jhk is the inhibitory effect of an individual of genotype-k within speciesj on the growth of the genotype4 subgroup of species i.

Using various numerical values for the parameters, Levin ran simulations to determine the result of competition and to examine the evolutionary changes within the competing populations. Some of his main conclusions are as follows. Variation in r has little effect on the outcome of competition, as would be expected from the well-known conditions for coexistence of the


Lotka-Volterra model, which do not involve r. Selection on K leads simply to the maximization of K, and this can have implications for the population dynamics, as can selection on the competition coefficients. In particular, if selection leads to a situation where each species inhibits itself more than the alternative species, and this was not the case prior to selection, then selection results in stable coexistence of the two species. However, Levin points out that the possible results of selection on variable competition coefficients are too numerous to yield a simple conclusion. In the restricted situation where one genotype of each species has a minimum sensitivity to competitive inhibition from all genotypes in both species, then selection will favour this genotype.

One interpretation of this last result is that selection will favour genotypes within each species that are least similar to the alternative species. However, in addition to the fact that Levin only considered a restricted case, there are several assumptions built into his model. The model relates to a pair of asexual haploid species, each of which has an array of discrete genotypes. Time-lags (for example in competitive inhibition) are excluded from the model, as indeed they are in most similar ones. Also, for the most part, Levin considered selection on r, K and u separately. Thus the model’s predictions must be considered against this background.

Leon (1974) has provided a model that is complementary to the previous one in that it deals with a pair of diploid sexual species. In each species there is assumed to be a biallelic locus (with alleles A1, A Z in species A; B1, BZ in species B ) which affects competition in some way. It is further assumed that no other polymorphic loci are involved and that while genotypes (at the A, B loci) vary in their sensitivity to competition, they do not vary in their ability to inhibit their competitors. For this situation, Leon’s equations (in discrete-time form) for changes in population density and allele-frequency respectively are:

N A ( t + 1) = F ( t ) N A ( t )

N B ( t + 1) = V ( t ) N B ( t )

where N represents the population size, and pi the frequency of the i I h allele. Wi and Vi are estimates of the fitness of allele i in species A, B respectively, based on the genotypic adaptive values and gene-frequencies as follows:

1 40 WALLACE ARTHUR

wi(t) = C ~ 4 ( t ) wij(t)

vi(t) = C p ? ( t ) vij(t).

j

j

The genotypic adaptive values (Wij and Vij) are highest for those genotypes least affected by competition.

Using this model, Leon investigated the evolution of the two species, and concentrated on establishing the conditions under which both will remain stably polymorphic. These conditions turn out to be heterozygous advantage in K and/or competitive sensitivity. That is, heterozygotes must have either the highest K-value or the lowest sensitivity to competition or both.

Levin (1971) and Leon ( 1 974) gave special consideration to the possibility of genetic feedback (see Section V and Pimentel et al., 1965) and they reached a similar conclusion: evolutionarily-induced oscillations in numerical dominance of competing species can only occur if there is an inverse relationship between interspecific and intraspecific competitive abilities. Levin (1971) considered this unlikely to be a common occurrence, though he does point out that i t could occur if the different components of competitive ability were improved by different alleles at the same locus. Levin concludes that a genetic mechanism for reversals of competitive dominance is not likely to be common and that “such reversals are not important to either evolutionary or ecological theory”.

In contrast with Leon (1974), who was largely concerned with conditions for stable polymorphisms, Crozier (1974) investigated directional change in gene-frequency and phenotype-frequency in a similar system-two diploid species each with a biallelic locus affecting competition. Crozier considered a situation in which a resource-array, consisting of five discrete resources, was utilized by both species, with different genotypes within each species differing in their optimal resource, as shown below:

Resource subunit 1 2 3 4 5 Genotype of species A for which each resource is optimal

Genotype of species B for which each resource is optimal

] A A AU aa

BB Bb bb

The fitness of each genotype falls off to each side of its optimal resource and is given by:

where Fij is the fitness of genotype i on resource j ; Vi is the “utilization


phenotype” of genotype i (which is designated a value of optimal subunit +2); Vj is the optimal utilization phenotype for resourcej; and x is a constant (10 in the simulations performed by Crozier). A result of the above equation is that the fitness ofany genotype on its optimal resource is 1.0 and its fitness on any other resource is between 0 and 1. The survival ofeach genotype is given by the product ofits fitness (as defined above) and a crowding parameter.

The results of the model are in fact predictable, at least in direction, from the allocation of optimal resources given in the table above. In particular, it is apparent from this table that only one genotype in each species shares an optimal resource with any members of the other species-namely, aa and BB. Thus it would be expected that these genotypes, and the corresponding phenotypes, would decline in frequency in sympatric populations. This indeed occurred in Crozier’s (1974) simulations. Various simulations, each with a different distribution of quantities of resource between the five subunits, showed qualitatively similar (but quantitatively different) patterns. Inter- specific divergence in phenotype was universal but the exact pattern of divergence depended on the resource-distribution.

This model shows, more vividly than most, the dependence of a model’s predictions on the assumptions built into it-in particular on the relative patterns of resource-utilization that are assigned to different genotypes. If the table of resource allocation had been constructed differently in this case, a completely different pattern of coevolutionary change could have been produced. The problem lies in deciding exactly what genotype/utilization relationship is most realistic, and as yet there are few data on which to base this decision.

Bulmer (1974) approached the problem of competitively-induced evoiution in a different manner. He based his model on a continuously variable character, which affected competition, with individuals having similar values of this character competing more severely than those with different values. Unlike MacArthur and Levins (1967), Bulmer’s character had an explicit genetic basis, The character’s phenotypic value (y) was considered to be the result of the action of n loci, each with equal effect and without dominance, combined with an environmental component that was taken to be normally distributed. For each locus, then, we have:

Genotypes CICl ClC2 C2C2 With effects + a 0 - a on y.

Bulmer first extended the concept of density-dependent selection (see Clarke, 1972) to the case of metric characters, and then considered the effect of a second, competing species on the evolution of the character, y (in both species). He found that when, in addition to optimizing selection, of environmental origin, on y, there is also selection resulting from interspecific

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competition, divergence of the two species will occur, but to a very limited extent. In fact, divergence will stop when the difference between the mean y-values, in the two species,

( M i - M 2 ) = 1,850,

which will not yield a bimodal distribution of the character concerned, since the condition for bimodality is

( M 1 - M 2 ) > 20,

where the two curves have equal values of 0. The small degree of difference between the two species that would result under the model would be insufficient to account for most purported examples of character displacement (Bulmer, 1974). The model can only predict a higher degree of displacement if the optimizing selection on y is largely a result of the genetic, rather than the external, environment. In this case, as selection proceeds, the “target value” of the optimizing selection changes simultaneously.

A model by Lawlor and Maynard Smith (1976) has introduced, into the study of coevolving competitors, the concept of the evolutionarily stable strategy (or ESS). This is the strategy such that, when it is adopted, the population is resistant to invasion by mutant individuals with alternative strategies, (but subject to the same constraints as the other members of the population). The coevolutionary model of Lawlor and Maynard Smith is based on the following ecological model (from MacArthur, 1972; see also Stewart and Levin, 1973):

1 dX1 = ~ I I W I R I + a12w2R2 - T I -~

Xi dt

where X1.2 are the population sizes of consumer species I , 2; R1.z are the population sizes of resource species 1, 2; T1.2 are the threshold food requirements for the consumers to main-

ai, is the probability of capturing and consuming a unit of resource

w, is the value of a unit of resource j to the consumer.

tain themselves;

j per unit time (for an individual of species i);

(Equations for the rate of change of the resource populations are also given by Lawlor and Maynard Smith, 1976.)

The parameters chosen as the evolutionary variables were the aij’s.

Importantly, a constraint was built into the model such that, within either


species, phenotypes with improved ail suffered a decreased value of ai2 . This was expressed in the form of two constraint equations:

a12 = hl(al1) and a 2 2 = h2(a21)

where the (declining) functions h~ and h2 may or may not be equal. As stated in the discussion of Crozier’s (1974) work, this sort of assumption is crucial to the predictions a model makes. It is pertinent to ask if the above relations between ail and ai2 are realistic. If the two resources were very different (e.g. worms and snails) then it would seem reasonable that as ail increases, ui2 should fall. However, if the resources were very similar (e.g. two closely related species of worm) then it would seem more likely that as ail increases, ai2 will also increase, though of course there must be some limit to their increase.

The predictions of the model are that, although the ESSs for each species in the absence of competition would be generalist strategies, the coevolutionary ESSs are for the two species to evolve as specialists on different resources. In a coarse-grained environment, specialization will be complete, but in a fine-grained environment, specialization may only be partial. No cases of evolutionary convergence in patterns of resource-utilization were found. Lawlor and Maynard Smith (1976) state explicitly that no form of group selection is entailed in the coevolutionary process-the interspecific divergence towards complementary patterns of resource-utilization is achieved entirely by natural selection acting at the level of the individual in both species.

Roughgarden (1976), in addition to developing some general coevolutionary models, dealt specifically with cases of competition in two- species and three-species systems, where evolution of niche-location, but not niche-breadth, was permitted. The Lotka-Volterra equations (as described earlier in this section) formed the basis of the model, with Ks and as being genetically variable. The variation in both of these parameters, in Rough- garden’s model, derives from the variation in niche-location. Since niche- breadth is constant, the competition coefficients for two species are functions of the distance between their niche-locations. In addition, it is assumed that as niche-location moves along the spectrum of available resources, the resultant carrying capacity also varies.

In this model, interspecific displacement in niche-location evolves, though Roughgarden shows that selection does not result in the species adopting niche-locations that maximize their population sizes. Also, the degree of displacement between “consecutive” species is higher in the two-species than in the three-species system.

An interesting point made by Roughgarden (1976) is that natural selection will not necessarily favour increased ability, within one species, to competi-

1 44 WALLACE ARTHUR

tively inhibit the other species. This is despite the fact that if the more inhibitory type were fixed in a population, it would lead to a higher overall population size for that species. Indeed i t may often be the case, as Rough- garden suggests, that “interspecific nastiness is selectively neutral”. However, it should be noted that this will not always be so. In particular, selection might well favour “nasty” genotypes in sedentary populations where the individuals concerned, and possibly their offspring, will reap the benefits of a localized inhibition of competitors. This difference in the action of selection on such traits in mobile and sedentary species may explain the commonness of allelopathic inhibition in plants (see Muller, 1970) and its relative rarity in animals.

Like Roughgarden’s model, that of Fenchel and Christiansen (1977) involves systems of two and three species whose competitive interactions are described in terms of the Lotka-Volterra equations. Competition coefficients (a) are determined by the extent of overlap in patterns of utilization of a 1 -dimensional resource spectrum. Genetic variation is assumed to exist in only one species and takes the form of a biallelic locus, with the three genotypes differing in their competition coefficients.

In the simplest situation, where only two species compete, where the resource spectrum is considered to be infinite, and where intraspecific competition is ignored, an evolutionary decrease in competition coefficients occurs. If niche breadth is fixed and the genetic variants differ only in niche position, then the decrease in the value of the competition coefficients takes the form of ecological displacement. If a third species is added to the system such that the genetically variable species has a utilization function intermediate between the other two, then Fenchel and Christiansen (1977) show that the variable species will evolve towards the midpoint between the utilization functions of the other two species. They also show that where effects of intraspecific competition are included, the prediction of displacement still applies.

In a recent model put forward by Slatkin (1980), two species with discrete, non-overlapping generations compete for a limiting resource, with their competition being mediated by a continuously-variable character (designated z) which is normally distributed and under polygenic control. At any time t , we have a number Ni(t) of each species, whose mean character-value is .2i(t), with variance (ri2(t). Fitness values Wi(z) for individuals with each particular value of z are determined jointly by intra- and inter-specific competition. Slatkin (1980) used his model to explore the evolutionary consequences of competition in a number of different situations. The results are complex and suggest that displacement will occur under certain conditions but not under others. In particular, Slatkin shows that the existence of constraints on the genetic and phenotypic variance of the character, and the


nature of such constraints, has a considerable influence on the predictions. Constraints may arise due to pleiotropic effects of the genes contributing to the character (z) or because of selection on characters correlated with z. If, for some such reason, the variance in each species is constrained so that it is held below its single-species equilibrium value, displacement (divergence between 21 and 2 2 ) evolves rapidly. However, if the variance is held above its equilibrium, Z1 and Zz will converge towards each other. If there are no constraints on the variance, then permanent displacement will only occur if the two species have different patterns of resource-utilization in the absence of interspecific competition. The evolution of displacement in this case is essentially an equivalent, for quantitative characters, of the evolution of displacement at a single locus described by Crozier (1974) where cor- respondence between genotypes and resource-subunits differed between the two species.

IV. CRITERIA FOR DEMONSTRATING COMPETITIVE SELECTION

Before considering the evidence from particular case-studies for evolutionary change in competing populations, it is desirable to consider what criteria a study should satisfy in order to provide an unambiguous conclusion. I will deal in particular with two sorts of study: first, studies of natural populations where variation in the mean value of a morphological character is attributed to character displacement; and second, experimental studies where a demonstration of the evolution of interspecific competitive ability is attempted. These have been chosen since they are the commonest sorts of study attempted in this field. However, many of the comments made are of general relevance.

A. Criteria for Conclusive Demonstration of Character Displacement in Natural Populations

Studies falling under this heading typically involve the monitoring of a character along a transect which crosses from an allopatric to a sympatric region. If the mean values of the character, in the two species, diverge (either unilaterally or bilaterally) at the border between allopatry and sympatry, then it is often proposed that character displacement is the process responsible for this shift. However, a number of problems may arise in attempting to draw this conclusion. These will now be discussed in some detail, along with possible ways of avoiding them.

I46 WALLACE ARTHUR

1. The alteration in the mean value of the character at the allopatrylsympatry border should not be predictable from variation within either of these areas

This point has been stressed by Grant (1972) and so requires less explanation than the others. Briefly, the argument is that, along a transect over a number of sampling sites, many characters will exhibit clinal variation. If the “displacement” of a character (in either species) could be merely an extension of a cline which started somewhere within (say) the allopatric region, then it is unnecessary to invoke a special explanation for the simple continuation of the cline. If, on the other hand, there is an abrupt change in the character’s mean value at the border between allopatry and sympatry, considerably steeper than any clinal gradient elsewhere on the transect, there may be a need for a special explanation. To distinguish which of the above two situations pertains, it is clearly necessary to take sufficient samples to get a good idea of the nature of variation within allopatry and within sympatry. A further complication here is that stepwise changes in genetically-based characters can occur even in the absence of stepwise environmental changes (see Clarke, 1966).

2. Sampling should be conducted along several geographically separate transects from allopatry to sympatry, each preferably located in an area whose habitat differs from that of the others

The existence of an abrupt change in the mean value of a character, as described above, may, if it only occurs on a single transect, have a specific local explanation. However, if displacement occurs on many or all of a number of transects then some general explanation is required. Of course, it is very difficult to rule out the possibility that some environmental factor always associated with (and perhaps giving rise to) the border between allopatry and sympatry is itself the selective agent causing displacement. Indeed, it might be expected that allopatry/sympatry borders would occur at the position of steps in one or more environmental variables. However, this sort of explanation can at least be rendered less likely by taking transects (from allopatry to sympatry) in different places with different habitats.

3. Heritability must be estimated because if the character- difference under study has a low or unknown heritability then an evolutionary explanation such as character displacement is suspect

Heritability has not received nearly enough attention in studies of character displacement. By heritability, I mean the ratio of additive genetic variance


in a character to its total phenotypic variance, as described by Falconer (1960-quivalent to the “narrow heritability” of Mather and Jinks (1977). There are, however, several problems involved in the estimation and interpretation of this parameter. Firstly, the heritability of variation within and between populations may differ. Secondly, either of these two types of heritability may vary from place to place. Thirdly, there are complications in estimating heritability caused by interactions between genotype and environment (see Falconer, 1960). Finally, breeding experiments and rearing of the F1 generation in the laboratory may artificially reduce the environmental component of the variance and hence lead to an overestimate of the heritability. Despite these problems, estimates of heritability have been obtained in species which were the subject of evolutionary investigations other than character displacement, even some whose generation-time is fairly long (for example, shell size in land-snails with a 2-3 year generation time: Cook, 1965, 1967). There is no reason why similar studies should not be undertaken in species which have been the subject of investigations of character displacement, and their continued rarity in this field (with some notable exceptions such as the study by Boag and Grant, 1978) is unfor- tunate.

If the heritability of a character is low or unknown then not only is there a serious gap in the argument for character displacement, but there is indeed a possible non-evolutionary explanation for frequent divergence in character between two species in sympatry, which is as follows. A commonly observed effect of crowding in single-species cultures is a decrease in the size of individuals. This has been noted in a wide range of organisms including Drosophila melanogaster (Bakker, 196 l), the land-snail Cepaea nemoralis (Williamson et al., 1976), the seaweed fly Coelopa frigida (Collins, 1978) and the pond snail Lymnaea palustris (Forbes and Crampton, 1942). When populations of two competing species meet, a frequent result is an increase in the total density with a concomitant decrease in the densities of both individual species. In such situations, the effect of the different components of density on the size of individuals in each species has not been thoroughly studied. One possible outcome, however, is that the larger competitor will respond mainly to its own density, while the smaller species will respond to the overall density (see Wilson (1975) for a possible reason for this). Thus in sympatry the larger species would become larger, the smaller one smaller. Taking any morphological character that is positively correlated with size-and most are-then this too will exhibit sympatric divergence unless it is expressed as a fraction of total body size. Here, then, we have a possible non-genetic “mimic” of character displacement. In species where there is no clear distinction between juveniles and adults, there is the added problem that changes in age structure will affect the mean value of a character, assuming

148 WALLACE ARTHUR

that all individuals, or those above some arbitrary cut-off point are measured. This problem is discussed further in Section V.

4. selection resulting from interspeciJic competition is proposed, then it is desirable that there should be evidence that the species are indeed competing, and that the character investigated has some bearing on the competitive process

The number of cases in which experimental evidence for interspecific competition is available is limited, and where such evidence exists it is incomplete (see Williamson, 1972 and Pianka, 1976). This is no doubt due in part to the practical difficulties involved in conducting the required “reciprocal explant” experiment, with sufficient replicates, in the field. Evidence for competition may also be difficult to obtain since, if character displacement has indeed occurred in a particular case, then the amount of competition still taking place may be considerably reduced. Circumstantial evidence for competition is more widely available but is of much more variable quality. If, in a particular case-study, there is little or no evidence that interspecific competition is occurring, then the case for competition being the selective agent, as in character displacement, is weak.

If competition is occurring, a character would only be expected to exhibit displacement if it is involved in obtaining the limiting resource, whether i t be food or space, and if the relationship between the patterns of resource- utilization of the two species is such that selection will favour those members of each species least like the other. (Correlated characters would also be expected to show some degree of displacement.) To maximize the likelihood of this being the case most studies of character displacement have monitored the size or shape of feeding apparatus (such as beak dimensions in birds); but the exact relationship between character-variation and the obtaining of resources has rarely been determined in studies of character displacement, a notable exception being the study of Fenchel(1975a, b), described in Section V.

The conclusiveness of a particular study of character displacement will depend on the degree to which the above four criteria are satisfied for the populations studied. Individual case studies will be discussed in Section V.A. Also, it should be noted that while the preceding discussion was couched in terms of character displacement, much of what has been said is relevant also to studies of character convergence and character release.


B. Criteria for Conclusive Demonstration of the Evolution of Interspecific Competitive Ability in Experimental Populations

The results of competition experiments are often presented as graphs of the species-frequency (i.e. the numbers of one species as a fraction of the total numbers) against time. The species-frequency trajectories sometimes show a steady change towards an equilibrium, whether trivial or non-trivial: see Arthur (1980a) for examples of the former. However, on other occasions (for example, Ayala, 1966) one or more cages show a more or less sudden change in the direction of the trajectory at some stage during the experiment. One interpretation of this occurrence is that one of the competing populations has evolved an increased interspecific competitive ability. In fact, there are at least three possible explanations for this sort of observation, which are described in Sections 1, 2 and 3 below. An outline of an experiment to distinguish between the different explanations is given in Section 3.

1 . Changes in Environmental Conditions

It is clear from the work of Park (1948, 1954) and others that the relative competitive abilities of two species can be markedly altered by environmental conditions such as temperature and humidity. It is equally clear that such variables can only be controlled within certain limits in a typical laboratory incubator or culture-room. It is common, in experiments with Drosophila for example, to keep the temperature at 25 & 1°C. However, even a 2°C shift in temperature can have a dramatic effect on the outcome of interspecific competition (see Ayala, 1971). It is therefore highly desirable that continuous records of temperature and indeed of as many other variables as possible be kept throughout all experiments. Screening for parasites is also desirable since parasitic infection can cause a change in relative competitive abilities. An example of this is given by Park (1948) for infection of Tribolium cultures with the parasite Adelina.

2. In traspecijic Competitive Selection

If many environmental variables have been monitored, and none exhibit any marked change when a reversal of competitive superiority occurs, then it is likely that one of the species has evolved an increased interspecific competitive ability. However, such an evolutionary change need not have arisen through selection resulting from interspecific competition. It may, rather, have occurred as an evolutionary response to extremely high density-in which case it might also have occurred in single-species culture. In other words, though the effects of the selection may include increased interspecific

I50 WALLACE ARTHUR

competitive ability, the cause of the selection need not have been interspecific competition. It may be, of course, that a particular investigator is only concerned to show that an evolutionary change has occurred, in which case it is not necessary to distinguish this explanation from the next one (3). However, if a distinction between these two is required, as indeed it is in the context of this review, then it should be possible to contrast the effects of single- and mixed-species cultures as described in the next section.

3. Interspecijic Competitive Selection

The proposal that a change in competitive ability is a direct result of selection originating from interspecific competition can be tested as follows. A sample of the population, in which a change in competitive ability has been observed, along with a sample from its parent population which has not undergone interspecific competition, and a third sample which has undergone intense intraspecific competition, should be transferred to new containers and cultured in standardized conditions. Their offspring should then be allowed to compete for one generation with a standard stock of species 2. This sort of test of course needs to be replicated many times, as single-generation experiments on competition are subject to considerable heterogeneity between replicates. If the CPR-values (or equivalent) measuring the competitive ability of the stock which had previously undergone interspecific competition are significantly higher than those for the other stocks of the same species, then it is clear that selection stemming from interspecific competition has modified the competitive ability. It is still desirable to have continuous recordings of environmental conditions, though, so that it can be seen whether the evolutionary change is likely to have been wholly, or only partially responsible for the observed alteration in competitive ability.

V. THE EVIDENCE

A. Changes in the Mean of Quantitative Characters

The majority of case-studies on the evolutionary consequences of interspecific competition fall into this category, including purported cases of character displacement, character convergence and the evolution of competitive ability. The inclusion of the last of these three categories in this section is somewhat arbitrary though, since the underlying character may have changed in mean and/or variance. It is important to stress that competitive ability, as measured by change in species-frequency or preferably, the CPR or some equivalent, is a result, and what is causing this result usually remains obscure. An increase


in the mean efficiency of resource-conversion could cause an increase in competitive ability, but so also could an increase in the variance of resources utilized.

I . Character Displacement

Since the concept of character displacement was put forward by Brown and Wilson (1956), a large number of surveys has been conducted on field populations in an attempt to obtain evidence for displacement in sympatry. These studies have dealt with a wide range of taxonomic groups, and have usually taken the form of a comparison of a morphological character in allopatric and sympatric samples of two closely-related species. The earlier studies have been critically reviewed by Grant (1972), and there is thus little point in discussing them in detail here. Grant’s conclusion, with which I fully agree, was that “the evidence for the ecological aspect (i.e. competitive as opposed to reproductive) of morphological character displacement is weak”. Thus after a brief consideration of two of the case-studies covered by Grant, on which there have been developments since 1972, I will move on to the more recent evidence for character displacement.

These two species of rock nuthatch provide what has become known as the classical case of character displacement (see Grant, 1975). This case stemmed originally from studies by Vaurie (1951), was used by Brown and Wilson (1956) to provide an example ofcharacter displacement, and was subsequently reviewed (Grant, 1972) and exhaustively re-analysed (Grant, 1975) by Grant. Two main areas of uncertainty in this study, which are of general relevance, have been partially clarified by Grant (1972, 1975). Firstly, to what extent would character-values in sympatry have been predicted from the pattern of variation in allopatry? Grant has shown that for the characters most likely to be directly related to competition for food-beak dimensions-clinal variation in allopatry “predicts” the variation in sympatry in S. tephronota. (The data on variation of S. neumayer in allopatry were insufficient to perform a similar analysis.) Thus there is no necessity to invoke competitive character displacement in beak-size. Secondly, to what extent is variation in individual characters simply a result of changes in body-size, and the correlation of these characters with size? Grant (1975) did find some evidence for sympatric displacement in eye-stripes, which relate to mate-recognition, but argued that this was partially a result of variation in body-size-though the data on the latter were too limited to warrant a firm conclusion. Thus although there is some evidence for displacement in a reproductive character in Sitta, there is no clear evidence for competitive character displacement. In addition, there was only one transect from allopatry to sympatry; heritability estimates for

(a) Sitta neumayer and Sitta tephronota

152 WALLACE ARTHUR

the relevant characters were not made; and there was no firm evidence of competition. Thus none of points 1 to 4 (see Section 1V.A) are fully satisfied by this study.

Among the many evolutionary inferences that have been drawn from data on Darwin’s finches (see Lack, 1947) is that of character displacement in beak-depth between the medium and small ground-finch. These two species are found together on most of the Galapagos Islands. However, each is found allopatrically on small islets. On Daphne, where the larger species G . fortis occurs alone, its beak-depth is considerably smaller (and thus closer to values of the same character in G.fuliginosa) than the beak-depth of the G . fortis individuals coexisting with G.fuliginosa. Similarly, when G . fuliginosa is found alone (on the Crossman islets), its beak-depth is considerably larger than when this species is found sympatrically with G . fortis. Data on beak-depths in these two species are shown in Fig. 2.

The interpretation of these data made by Lack (1947) was, although he did not use the phrase, character displacement. Both Lack (1947) and Grant (1972) have pointed out that migration was probably from the larger to the smaller islands and thus the allopatric populations on Daphne and Crossman are probably derived from sympatric populations on the main islands. This led Grant (1972), because of his definition of character displacement, to exclude Geospiza as an example of it. However, under the definition adopted here, the time-sequence of allopatry and sympatry does not occupy a central role, and so the Geospiza example cannot be excluded as an example of character displacement for this reason.

I t is clear from Fig. 2 that the allopatric/sympatric difference in beak-depth is very marked in both species. While it would clearly be desirable to have measurements on several additional allopatric populations, the number of these is of course strictly limited since the species concerned are entirely restricted to the Galapagos, and because this example concerns island populations, it is not open to the transect approach described in point 2 of Section 1V.A. As regards heritability, estimates have recently been made (Boag and Grant, 1978) for a number of morphological characters in G . fortis (but not G . fuliginosa), and all characters studied showed a high heritability. These included beak-depth (0.82), beak-width (0.95) and beak-length (0.62). The figures given here are those derived from midparent-offspring regression, with other estimating techniques giving slightly higher values for all three characters. I t should be stressed, though, that all the above figures relate to variation of G . fortis within Daphne and their relevance to inter-island variation is thus questionable. While bearing this problem in mind, as well as others concerned with the estimation of heritability, it seems likely that the observed variation in beak-depth in Geospiza is largely genetic in origin. The evidence

(b) Geospiza fortis and Geospiza fuliginosa


5 0

'/o 30- 10-

50

'/o 30-

10

40

'/o 3 0 10

fortis magnirostris

ABINGDON, BINDLOE, JAMES, JERVIS

- - fortis magnirostris

ALBEMARLE ,INDEFATIGABLE -

Da rw I n's mognirostris CHARLES

A - fuliginoso fortis

CHARLES, CHATHAM

-

I DAPHNE

o/o 20 fuliginosa CROSSMAN

I l l r l l l l r l l r l l l l l l l r l l l l l l l l l l l l l l l r 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23

Fig. 2. Distributions of beak-depth in G. fortis and G. fuliginosa on islands where these species occur together and apart. (Data on G. magnirostris are also given.) From Lack (1947).

for competition is less satisfactory in that it is based largely on observed dietary overlaps (Snodgrass, 1902; Lack, 1947) but if competition for food does occur, then clearly beak-depth is a potentially relevant character. Lack (1947) suggests, though not from quantitative data, that there is a correlation between the size of food eaten and the size of the beak in Galapagos ground- finches. Abbott et al. (1977) have shown that in the genus Geospiza in general, the overlap in diet between two sympatric species decreases markedly as the ratio of beak-depth in the larger to beak-depth in the smaller species increases. Relating the Geospiza study, then, to the discussion of Section IV, it can be seen that criteria 1 and 3 are largely satisfied, while 2 and 4 are not.

154 WALLACE ARTHUR

(c) Typhlosaurus gariepensis and Typhlosaurus lineatus A case of possible competitive character displacement in these two species of legless subterranean lizards has been reported by Huey and Pianka (1974; see also Huey et al., 1974). This investigation was one of unilateral displacement as there were insufficient allopatric sites of T. gariepensis to examine whether or not this species reacted to the presence of the larger species, T. lineatus. An allopatric/sympatric comparison was possible for the latter species, with eight sympatric samples and a much larger number of allopatric ones. Several morphological characters were measured including snout-vent- length (SVL) and the length and width of the head. In these three characters, individuals of T. lineatus showed significantly higher values in samples sympatric with T. gariepensis than in allopatric samples. Huey and Pianka (1974) state that, for SVL, the shift from allopatric to sympatric values is “step-wise”. However, the pattern of variation in allopatry is not presented clearly and there is considerable lumping of data from geographically separate samples in order to calculate means, which is clearly unsatisfactory. Also, while the variation in males is fairly sharp, at the allopatry/sympatry border, that in females is much less so. Little is known of the heritability of morphological characters in Typhlosaurus, and non-genetic variation in size thus remains a possibility (see Lister and McMurtie, 1976). However, there is some information on the possible relevance of size-variation to competition for food: the larger, sympatric T. lineatus eat significantly larger prey (P < 0.001) than the smaller, allopatric individuals (Huey and Pianka, 1974). In this example, it is apparent that points 1 and 4 are to some extent satisfied, whilst 2 and 3 are not.

Several purported cases of character displacement in fossils have been discussed by Eldredge (1974) who cites these two species of benthic trilobites as presenting “perhaps the most compelling case of character displacement in the paleontological literature”. Yet this must be a comment on the general difficulties of working with fossils rather than the completeness of this example. Only one sympatric sample was available, and as Eldredge himself points out, only one individual of P. iowensis within this single sample was measurable. Thus while P. iowensis is seen to diverge morphologically from P . rana in sympatry, this “divergence” cannot be taken very seriously, as only one trilobite specimen is “diverging”. More data are available for P . rana, but the results are far from simple: in one character this species diverges from P . iowensis, in others it converges towards the later species, and in still others there is no marked convergence or divergence. This example does not-apart from some circumstantial evidence of competition-satisfy any of the criteria put forward in Section IV.A, and no firm conclusion

( d ) Phacops iowensis and Phacops rana


as to whether or not character displacement has occurred in Phacops is possible.

Another case in which morphological variation in closely-related fossil species -this time two radiolarians-is ascribed to character displacement, is presented by Kellogg (1975). The older species, E. calvertense, is thought to have given rise, possibly by evolutionary divergence of a peripheral population, to the more recent E. matuyamai, which subsequently re-contacted its ancestral species in a phase of “neosympatry” which persisted for about one million years. During this period, the larger species (E. matuyamai) increased greatly in size and E. calvertense became smaller. The character measured was the width, in microns, of the fourth segment. There are, however, several problems in attributing this divergence in size to character displacement. Firstly, since E. calvertense pre-dated and post-dated its congener in the area where the populations were for a time sympatric, only unilateral character displacement of E. calvertense from E. matuyamai can be investigated. Secondly, although the sympatric period saw a steepening of the reduction in size of E. calvertense, this was not sufficiently abrupt to make it clear that the presence of E. matuyamai was responsible. Added to these difficulties is the impossibility of making heritability estimates, though it might be argued that the particular pattern of variation described by Kellogg is unlikely to be of a non-genetic nature.

A point noted by both Eldredge (1974) and Kellogg (1975) is that, despite other problems, fossil studies can at least answer the question of whether allopatry preceded sympatry in a particular region. This question must often go unanswered in studies of contemporary species.

The most detailed case of character displacement is provided by Fenchel’s (1975a, b) study of populations of mud-snails from Northern Jutland. The main study-area comprised 57 sampling sites; in all, about 13 0oO animals were collected; the lengths of approximately 100 snails were measured, to the nearest 0.25 mm, in each population. In addition to H. ulvae and H. ventrosa, two further species of mud-snail were collected: H. neglecta and Potamopyrgusjenkinsi. However, the latter was not considered to be in strong competition with any of the Hydrobia species, while the data for H. neglecta were patchy and, according to Fenchel, difficult to interpret. The data on H. ulvae and H. ventrosa showed consistent divergence between these two species in sympatry: see Fig. 3. Histograms illustrating the variation within typical allopatric and sympatric samples are shown in Fig. 4. The numbers in both of these figures refer to sampling sites. It can be seen from Fig. 3 that the variations between samples within sympatry and within allopatry

(e ) Eucyrtidium calvertense and Eucyrtidium matuyamai

(f) Hydrobia ulvae and Hydrobia ventrosa

156 WALLACE A R T H U R

‘1 7 6 12 23A 9 10 10A 19 1 U lU IF Y GW 700

5758636965 23 2 3766 7 0 A 7OE GI

‘I 1

Fig. 3. Average lengths of H . uluae (open circles) and H . ventrow (closed circles) from localities where the two species coexist (a) and where they occur alone (b). Vertical bars indicate one standard deviation. From Fenchel (1975b).

is slight, for both species, compared with the clear difference between allopatric and sympatric samples of each. Furthermore, sympatric samples from different localities show similar divergences.

Having established that H. ulvae and H . ventrosa did indeed exhibit consistent sympatric divergence, Fenchel (1975b) proceeded to determine what effect shell-size had on the size of particles ingested. (These snails ingest particles of substrate and assimilate attached micro-organisms and detritus.) A positive association was found between the mean diameter of ingested particles and the shell-size (see Fig. 5); though for any particular size of shell, Potarnopyrgus snails ingested larger particles than did Hydrobia. Considering the ingestion-patterns of typical allopatric and sympatric samples of H. ulvae and H . ventrosa, then, it can be seen (Fig. 6) that divergence in size leads to

"i 20

6

H venfrosa

I 0 L 0

H ulwe

10

0 2 3 4 5 6 m m

43 010 I

i i 4 4 i m m

Fig. 4. Length-frequency distributions of the shells of H . uluae and H. uentrosa from a locality where they coexist (above) and from two localities where they occur allopatrically (below). From Fenchel (1975b).

I I I I I 1 1 1 1 2 3 4 5 678910

Shel l length (mm)

Fig. 5. Relationship between size of shell and size of food particles in Hydrobia and Potamopyrgus. From Fenchel(1975b).

158 WALLACE ARTHUR

6 O/O

60 - -

40 - -

20 - -

0 - - 2

-

-

6 0

40 -

-

43

20 -

0 -

40 -

20

4 8 16 32 64lhBi56k12 Diameter ( p m )

Fig. 6. Distributions of the size of food-particles (expressed as volume %) for populations of H . uluae (open circles) and H . uentrosa (closed circles) from sympatric (top) and allopatric localities. From Fenchel (1975b).

divergence in the size of particles ingested, in other words, partial partitioning of resources.

When this case-study is considered in relation to the criteria put forward in Section IV.A, it can be seen that points 1, 2 and 4 are reasonably well satisfied. The divergence on moving into sympatry is sharp and would not be predicted from a knowledge of the variation between samples within allopatry; many geographically separate comparisons show similar divergence; there is some circumstantial evidence for competition in Hydrobia (Fenchel, 1975a); and the importance of shell-size to the selection of food- particles has been experimentally demonstrated. The only serious gap in the evidence provided by this study is the lack of information on the heritability of the observed differences in size. It is particularly important that this information should be obtained, not only because the rest of the data are so clear, but also because coexistence has an effect on the timing of reproduction (Fenchel, 1975b), and hence on the age-distribution of the population,


which will no doubt affect the distribution of shell-size. The effect of coexistence on age-distribution varies from place to place but in general there appears to be a shortening of the reproductive period in sympatric areas. Thus point 3 is not yet satisfied for this case-study, but despite this Hydrobia provides probably the clearest evidence yet obtained for character displacement.

A study of several morphological characters in these two species of skates has been carried out by McEachran and Martin (1977). In one area, the Gulf of St Lawrence, R. ocellata occurs allopatrically, while other populations of this species are sympatric with R. erinacea. The possibility of unilateral displacement (of R. ocellata) was investigated here.

While some characters were very similar in allopatric and sympatric samples of R. ocellata, one showed significant divergence in sympatry and one significant convergence. The former character was the number of tooth- rows in the upper jaw, and the latter was the number of pre-caudal vertebrae. There was also considerable sympatric divergence in total body-length. How- ever, only three samples were measured in all-one of R. erinacea and two (one allopatric plus one sympatric) of R. ocellata. No data on heritability for any of the characters studied are given by the authors. Some information on feeding habits is given, but evidence for competition is lacking. Thus none of criteria 1 to 4 are fully satisfied in this study, and it is difficult to draw any firm conclusion.

Schindel and Gould (1977) measured five morphological characters in these fossil landsnails, and derived two further characters (ratios relating to shell- shape). They then considered the overall (multivariate) pattern of variation between habitats, which were determined by the substrate from which the fossils were removed, and between allopatry and sympatry. The effect of a congener was found to be greater than the effect of habitat, and was in such a direction that the species were more different in sympatry than in allopatry. The displacement was greater in P. discrepans than in P. circumjirmatus. The characters contributing most to the overall displacement were spire-height and shell-shape, the latter measured as the ratio of width to height.

There is a problem as regards the choice of individuals to measure in Poecilozonites because neither species exhibits a recognizable adult stage (Schindel and Gould, 1977). These authors state that they measured “between ten and thirty of the larger specimens of each species for each locality”. This is obviously less satisfactory than the measurement of a clearly-defined adult group, where such exists. Also, there is the problem of unmeasurable heritability. The allopatric/sympatric difference is repeatable in different places and is not likely to be a result of habitat since, as has already been

(9) Raja erinacea and Raja ocellata

(h) Poecilozonites circumjirrnatus and Poecilozonites discrepans

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noted, habitats were separated out in this study and had less effect on morphology than the presence or absence of a congener. Whether the two species competed, and what relation the size and shape of the shells had to any competition remains obscure. Thus criteria 1 and 2 are satisfied while 3 and 4 are not.

The study by Dunham et al. (1979) on these two species of freshwater fish (and some other congeners) stands out from most other studies of character displacement in its attempt to dissociate competitive effects on morphological variation from effects due to other environmental factors. Dunham et al. (1979) studied two morphological characters-the number of gill rakers in the anterior row on the first anterior gill arch, and the number of vertebrae. The first of these characters relates to the sieving of food particles to be ingested and so has an obvious potential relation to competition for food; the second character is unlikely to be of direct relevance to competition.

A stepwise multiple regression technique was used to separate the effects of a number of environmental factors on the two dependent variables. These environmental factors were elevation, mean and minimum water discharge rates, latitude, longitude and gradient. In addition, two variables were constructed in an attempt to quantify the degree of interspecific competition. Firstly, as regards competition between C . discobolus and C . platyrhynchus, the intensity of interspecific competition experienced by each of these was estimated by the species-frequency of the other + 1 for sympatric areas (which were thus on a scale from 1 to 2), with allopatric areas being allocated a value of 0. Secondly, the degree of intersubgeneric competition was estimated as the relative frequency of the alternative subgenus (i.e. alternative to the subgenus Pantosteus in which the above two species are placed) + I , with areas where the alternative subgenus was absent being allocated a value of 0. Multiple regression was then used to calculate the partial correlation coefficients representing the effects of the different environmental variables on the number of gill rakers and number of vertebrae. This analysis showed that both of the competitive indices (and many of the other environmental variables) had significant effects on morphological variation. C . discobolus and C . platyrhynchus showed significant displacement in the numbers of both gill rakers and vertebrae. The species with higher values of these characters (C. discobolus) showed increases in both with increased intensity of competition from C . platyrhynchus, and the latter species showed significant declines in both morphological variables with increased frequency of C . discobolus. (Competition from the other subgenus also had significant effects on both species.)

The main problem with this study, as with Fenchel’s (1975a, b) study of Hydrobia, is the lack of information on heritability, but otherwise it satisfies

( i ) Catostomus discobolus and Catostomus platyrhynchus


the criteria of Section 1V.A fairly well. One cautionary comment should perhaps be added though-the results of a multiple regression analysis are very sensitive to exactly which independent variables are included in it.

In addition to case-studies on particular pairs or groups of related species, many general studies which are of relevance to character displacement have been undertaken. I will not attempt to review these, since many studies are relevant to character displacement in one way or another, but one article in particular deserves mention.

Wilson (1975) questioned whether selection would indeed favour smaller individuals of the already-smaller species, and consequently whether a pattern of displacement in sympatry was realistic. His argument was based on a considerable amount of data on the relationship between the size of predators and the size of their prey, which suggested that larger predators might have a greater variance in prey-size as well as a larger mean prey-size. Thus the prey of smaller individuals would be included in the distribution of prey eaten by larger individuals and so there would be what Wilson called a competitive gradient, rather than resource-partitioning. The data from one experiment are shown in Fig. 7. This pattern gives a rather different impression from the patterns of ingestion of particles in relation to size in Hydrobia (Figs 5 and 6) though the difference may be partly due to different presenta- tions of the data. The relative commonness of different relationships between

55 c a - 45

.- a-

U

25

5u 45 55 65 75 85 95 105

Animal length (rnrn)

Fig. 7. Prey size as a function of predator size. Data from an experiment where different stages of the copepod Acartia tonsa were fed with plastic beads. The data points are the maximum and minimum 5% ingested. From Wilson (1975).

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the size of a consumer and its choice of food clearly needs to be established. In summary, it is by no means clear at this stage whether the lack of

conclusive evidence for character displacement means that the process is rare, or that it is simply a difficult phenomenon to demonstrate, or both.

2. Character Convergence

The possibility that evolution might favour convergence of competitors in their patterns of resource-utilization was put forward by MacArthur and Levins (1967). However, this suggestion has been criticized by Lawlor and Maynard Smith (1976) on the basis that the evolutionary shift described as a convergence would also have occurred in the absence of the competitor which was converged towards (see Section 1II.B and Fig. 1). Nevertheless, cases exist in which apparent convergence in sympatry has been attributed to natural selection resulting from interspecific competition, and these cases have been reviewed by Grant (1972) and Cody (1973). These two reviewers reached markedly different conclusions: Grant (1972), as we have seen, concluded that the evidence for competitive “character displacement” was weak, and it should be recalled that Grant defined displacement so as to include convergence. Cody (1973) on the other hand considered that the evidence for character displacement and character convergence was strong. Indeed, Cody stated that character displacement was widely accepted “not with- standing recent doubts of the purity of commonly cited examples” (a reference to Grant’s review). However, the validity of a general theory ultimately relies on the purity of the individual examples on which it is based, so gaps in the evidence provided by particular case-studies cannot be so easily dismissed. This point has already been stressed in relation to character displacement.

It is even more important to have a watertight case when postulating competitive character convergence, because there are several highly plausible reasons why two species might converge in sympatry. Firstly, if the species hybridize to any appreciable extent they may exhibit sympatric convergence. Secondly, if there is a conventional mimetic relationship (either Batesian or Mullerian-see Sheppard, 1967) then they might be expected to resemble each other more closely in sympatry than in allopatry. Thirdly, there may be “social mimicry” (Cody, 1973) where increased similarity facilitates gregariousness in mixed-species flocks (but see also Barnard, 1979). Fourthly, there may be other non-competitive selective pressures acting in a convergent manner in sympatry, such as selection for crypsis against a common background. Finally, where behavioural patterns or morphological characters are concerned, non-genetic forces may have considerable influence. As well as there being a variety of possible causes of sympatric convergence, the evidence for competitive convergence is more taxonomically restricted than that for


displacement, and stems mostly from studies on birds, though some possible instances in other groups are discussed by Cody (1973).

The term character convergence is restricted by Cody (1973) to situations where selection favours similar individuals in two or more species so that interspecific territories may be established. Examples of interspecific territoriality are known, for example in wrens (P. R. Grant, 1966). However, in this particular case there is no evidence for character convergence (Grant, 1972). In other cases, such as the meadowlarks Sturnella magna and S. neglecta, interspecific territoriality has been observed (Lanyon, 1956) and characters associated with display have converged in sympatry (Rohwer, 1973). However, it has not been possible to demonstrate that selection acts through competition and associated interspecific territoriality rather than through some other route, or indeed that the variation observed is a result of selection at all, though the nature of some of the characters (pigmentation patterns) suggest that a non-genetic explanation is unlikely.

A case of very marked similarity in floral structure and colour of nine species of hummingbird-pollinated plants has been reported by Brown and Kodric- Brown (1979). Since the nine species represent seven different families, the similarities are presumably due to convergence; and the nature of the common phenotype suggests that it is an evolutionary response to facilitate pollination by hummingbirds. Cases such as this, while demonstrating very marked evolutionary convergence in several characters, leave open the question of whether the agent giving rise to the selection is limiting, in other words whether the convergence is truly a competitively-induced one.

There appears to be no single study where there is consistent convergence in sympatry of a heritable character which is clearly not attributable to any of the non-competitive mechanisms listed earlier. Taking this fact together with criticism (Lawlor and Maynard Smith, 1976) of the theory of competitive convergence, it can be seen that the case for this supposed evolutionary process is very weak.

3. The Evolution of Competitive Ability

Included in this section are cases where, usually in experimental populations of insects, it appears that one or both of a pair of competing species has undergone an evolutionary increase in its interspecific competitive ability. Although I will not be concerned here with the evolution of intraspecific competitive ability, the relationship between the genetic basis of this, and of interspecific competitive ability is of considerable interest, as has already been pointed out (see also Levin, 1969a, b, 1971).

One of the earliest studies in which an experimental population appeared to evolve an increased interspecific competitive ability was that of Moore (1952a, b) using the sibling species Drosophila melanogaster and D. simulans.

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Out of 20 cages in which these two species competed (Moore, 1952a) D. simulans fared markedly better in one than in the other 19. Moore (1952b) then took a sample of D . simulans from this cage and allowed it to compete with further stocks of D. melanogaster in new containers. This process was repeated three times giving, eventually, an experiment where the D. melanogaster had not experienced competition with D . simulans previously, but the D. simulans had been in competition with D. melanogaster for 500 days. The results of this experiment are shown in Fig. 8. These results were interpreted as a demonstration that interspecific competition gave rise to selection for increased competitive ability. While this interpretation may well be correct, there are a number of points which have not been noted in relation to Moore’s (1952b) experiment. Firstly, it is not clear to what extent the higher competitive ability of the selected D. simulans was due to selection during the experiment as opposed to genetic differences between the original stocks. Secondly, the results of all experiments are presented as graphs of species-frequency over time, and competitive ability inferred from changes in species-frequency. Yet in some experiments (see Fig. 8) controls and experimentals were started at very different species-frequencies and so the results, as presented, are not directly comparable. Thirdly, it is not clear whether the selection, if it occurred, was caused by high density in general or the presence of a second species in particular. Finally, competition involving the selected stock of D. simulans showed a markedly increased heterogeneity of outcome between different generations compared with competition involving unselected D. simulans (Fig. 8) , a phenomenon that remains to be explained.

Further studies of changes in competitive ability in Drosophila have been

0. --*-- Cage 24 --o-- Cage 25 ” . I

1 I I I I I I 0 100 200 300

Time in days

Fig. 8. Results of competition between D. melanogaster and D. simulans. Cages 24 and 25 contain “stock” samples of both species. Cages 26 and 27 contain stock D . melanogaster and “pre-competed” D . simulans. From Moore (1952b).


conducted by Ayala (1966, 1969), Barker (1973), Futuyma (1970), Hedrick (1972), Hoenigsberg (1968) and Tantawy et al. (1970). Some general comments on the subject have been made by Gill (1974) and Sammeta and Levins (1970). The studies of Hoenigsberg (1968) and Tantawy et al. (1970) were field surveys and it is not clear whether evolutionary changes need be invoked. Futuyma’s (1970) study yielded complex results which, according to the author, required an explanation involving qualitatively different changes in different populations.

In Ayala’s (1966) experiments, three populations of D. serrata (competing against different species) increased in frequency after first declining; these effects were interpreted as evolutionary changes in interspecific competitive ability. However, none of the three possible causes of the apparent changes in competitive ability, as discussed in Section IV.B, were excluded, and hence a firm conclusion cannot be drawn. In a later study (Ayala, 1969) D. serrata competed with D. nebulosa and the results of competition in two replicate populations are shown in Fig. 9. Ayala pointed to the increase in the frequency of D. serrata in population I starting around week 22 and devised an experiment to test whether this was a result of evolutionary increase in competitive ability in D. serrata. However, it must be pointed out that D. serrata in population I appeared to fare better, from the start of the experiment, than did their counterparts in population 11. Also, there was considerable heterogeneity in the species-frequency between generations in the earlier period of the experi-

1OOC

1 I I I I I I I I I

Weeks 0 3 6 9 12 15 18 21 24 27 30

Fig. 9. Per cent D. serrata in two experimental populations (in competition with D. nebulosa). From Ayala (1969).

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ment for which an evolutionary explanation seems unlikely; so some degree of caution is necessary in interpreting the later results as a consequence of evolutionary change.

Ayala (1969) performed a second experiment to test whether the competitive ability of D. serrata had indeed evolved. F1 offspring of samples of this species from populations I and I1 and from the original stocks were made to compete with a standard stock of D. nebulosa. If the competitive ability of D. serrata had evolved in population I then this should of course be reflected in the results of this second experiment. The results do suggest this (Fig. 10) but they are by no means clear and they are fraught with several problems. The difference in the results between the different treatments (i.e. different origins of D. serrata) differed over time. There was considerable heterogeneity between replicates of the same treatment. In addition, the increase in the average performance of D. serrata from population I was roughly equal to the decrease in the average performance of D. serrata from population 11, as compared

Weeks

Fig. 10. Results of competition between D. serrata and stock D. nebulosa. The D. serrata originated from population I (solid line), population 11 (dashed line) and a stock cage (dot/dash line). Each line represents the average of the replicates whose identifying numbers are given. From Ayala (1969).


to the performance of the original stock (see Fig. 10). Yet it seems very unlikely that a population can show an evolutionary decrease in competitive ability during a competition experiment. The only situation in which interspecific competitive ability might indeed decline during a competition experiment would be where it is negatively correlated with intraspecific competitive ability, and selection resulting from intraspecific competition is stronger than that resulting from interspecific competition (see Levin, 1969b). For these various reasons, the results of Ayala’s (1969) experiment are difficult to interpret in a conclusive manner.

Hedrick (1972) has shown a clear case of a population of D. melanogaster that had a much higher competitive ability than other populations with ultimately the same origin. The contrast was very marked, though it was present from the start of the competition experiment in which it was observed, and so it would appear not to be a result of selection through interspecific competition (at least in the laboratory) even though the resultant stock is of considerably increased competitive ability.

A somewhat complex series of experiments was conducted by Barker (1973) in an attempt to determine whether D. melanogaster and/or D. simulans evolved in relation to interspecific competition. However, the interpretation of the results is impeded due to a number of interruptions of the standardized experimental conditions. In generation 10, the entire experiment was shipped from America to Australia and slightly different medium and containers were employed subsequently. At generation 14 the heating systems failed and “developmental rate was markedly reduced. From generation 55 a different grade of agar was used. Further, although Barker tested for evolutionary change in both species, the stock of D. melanogaster used was a yellow, white strain which had been kept in the laboratory for an unspecified length of time in vials. Thus it is likely that its genetic variation would have been severely depleted prior to its involvement in the competition experiments. The lack of evidence for evolution of competitive ability in this stock is thus hardly surprising. In three of the four D. simulans populations which were subjected to competition with D. melanogaster there was also no evidence for evolution of competitive ability. In the remaining population there was what Barker (1973) calls “presumptive evidence” for selection leading to ecological divergence but there is little basis for this statement in the data. Although much work was clearly put into this experiment, no clear conclusion on the evolutionary effects of competition can be drawn from it.

The role of genetic factors in competition between the flour beetles Tri- bolium castaneum and T. confusum has received considerable attention since Park’s (1948, 1954) classic experiments on these species. It was shown at an early stage that different strains differed in competitive ability (Lerner and

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Ho, 1961), a fact well known also in Drosophila. Park et al. (1964) showed that different strains of T . castaneum differed more in competitive ability than those of T. confusum. However, Park and Lloyd (1955) considered that natural selection resulting from competition played little part in determining the (dynamic) outcome of competition. This suggestion was supported by negative results of an experiment by Dawson (1973). Recent work by Dawson (1979), however, has demonstrated that evolutionary changes in feeding behaviour can occur in T . castaneum, apparently as a result of exposure to T . confusum. The situation is complex in that T. confusum and T . castaneum compete by eating each other’s eggs, as well as their own. Dawson (1979) showed that the progeny of T. castaneum originating from cultures differing in the relative proportions of T. castaneum and T . confusum differed in their species-preference of eggs eaten in a choice experiment, despite their having had no contact with the cultures from which their parents came. In other words, an inherited preference appears to have evolved. If this result can be confirmed as a general one, it has important implications for the theories of apostatic selection (Clarke, 1962) and predator-switching (Murdoch, 1969) as well as being of relevance to competition.

The genetics and evolution of competitive ability in plants has been the subject ofconsiderable study, for example Sakai (1955,1961), Sakai and Gotoh (1955), Turkington (1975) and review by Harper (1977; Chapter 24). Much of this work has centred on intraspecific competitive ability, but some of the results deserve mention nevertheless. In particular, Sakai’s (1961) study led him to the conclusions that intraspecific competitive ability, although i t included a genetic component, was of low heritability and was usually un- associated with gross morphological characteristics. The lack of clear evidence for character displacement or rapid evolution of interspecific competitive ability in animals suggests that Sakai’s conclusions may not be restricted to within-species competition or to plants.

One study of a plant population which was directly relevant to evolution in mixed-species assemblages was that of Turkington (1975). In this study, samples of the clover species Trifolium repens were removed from vegetation patches dominated by one of four species of grass-Lolium perenne, Agrostis tenuis, Holcus lanatus and Cynosurus cristatus. The clover samples were then cloned and the cloning-products used in an experiment to test their relative performances when each was grown in combination with each of the four species of grass. With one exception, the clover population which had originated from a patch dominated by a particular species of grass fared better against that species than did other populations of clover.

A field experiment carried out by Hairston (1980), using two species of salamander, Plethodon jordani and Plethodon glutinosus, has yielded results which are difficult to interpret. Two sites were studied-one in the Great


Smoky Mountains where the two species show altitudinal segregation with a narrow overlap zone; the other in the Balsam Mountains where the zone of overlap is much wider. Both study-sites were within the zones of overlap. Each site was divided into plots, some of which remained unaltered as controls, the other, experimental, plots having their resident P . jordani replaced with those from the alternative site. If the different widths of overlap zone in the two mountain ranges are a result of evolutionary differences in competitive abilities or patterns of resource utilization between the two areas, then the population sizes of P. glutinosus in the control plots and experimental plots should differ, and moreover the directions of the experimental/control difference should be opposite when the two sorts of transplant are compared. However, while the P. glutinosus in the Smokies showed a significant increase in population size after replacement of the congeners, the P. gfurinosus populations in the Balsams showed no detectable difference between experimentals and controls. Unfortunately Hairston (1980) lumped his data from different plots and presented only mean population sizes. Thus it is not possible to assess the situation further by examining the fate of the populations in individual plots.

It seems likely from the various experiments described above that it is sometimes possible for the competitive ability of a population to increase through selection resulting from the competitive process itself-though there are pit- falls in attempting to demonstrate this and few cases of putative evolution of competitive ability can be regarded as conclusive. Two further questions may be asked of those situations in which competitive ability does evolve:

(1) Is the rate of such evolution (in either species) dependent on the species- frequency?

(2) What effect does the evolutionary change have on the dynamics of the mixed-species population?

Pimentel et al. (1965) put forward a hypothesis, relating to these questions, known as “genetic feedback”, and proceeded to test it using experimental populations of the housefly, Musca domestica and the blowfly, Phaenicia sericata. I will first outline their general hypothesis, and then review their experimental results in some detail.

Pimentel et al. (1965) proposed that: (1) During an experiment in which two species are made to compete, the

species that is rarer, at any particular time, will be undergoing more intense selection for improvement of its interspecific competitive ability than the commoner species.

(2) The competitive ability of the rarer species will thus increase more quickly than that of its competitor, and will eventually surpass it.

(3) The result of this will be a “reversal” in the population dynamics, with the species which was initially rare becoming more common.

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(4) The differential in selective pressures is now reversed and thus, eventually, the competitive abilities return to their original ranking.

(5) The oscillations in species-frequency resulting from “genetic feedback” will be damped and the system will converge towards a state of stable coexistence.

To test this scheme, several different experiments were devised. In nine cages, houseflies and blowflies competed in simple, one-cell containers. In a single experiment, the two species competed in a more complex, 16-cell cage, the different cells being connected in a 4 x 4 arrangement by a series of plastic tubes. Finally, as a test of the evolution of competitive ability in the 16-cell experiment, 15 more single-cell cages were set up in which experimental blowflies (sampled from the 16-cell cage after 38 weeks of competition) competed with wild-caught houseflies (5 cages); experimental houseflies competed with wild-caught blowflies (5 cages); and experimentally-derived samples of both houseflies and blowflies competed with each other (5 cages).

The results of these experiments varied considerably. Some showed fairly straightforward elimination of one species (see Fig. 11). Some showed a single reversal of competitive dominance, followed by extinction of one species (the 16-cell cage: see Fig. 12). Others showed several reversals of dominance (Fig. 13). In all experiments, one species-though not always the same one- was eliminated.

The interpretation of these diverse results is far from easy. It is perhaps simplest to start by stating what the results do not show. They certainly do not show damped oscillations leading to an eventual equilibrium in species-

Weeks

Fig. 11. Results of competition between houseflies and blowflies in one of the single- cell cages. (Solid line-housefly; broken line-blowfly). From Pimentel et d. ( 1 965).

Weeks

Fig. 12. Results of competition in the 16-cell cage. (Solid line-housefly; broken line -blowfly). From Pimentel et a/. (1965).

Weeks

Fig. 13. Results of competition between houseflies (-) and blowflies (---) in one of the single-cell cages showing more than one reversal of competitive dominance. From Pimentel et al. (1965).

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frequency. If anything, the oscillations in species-frequency were divergent, and in all cases led to elimination of one species by the other. This was true of the complex 16-cell environment as well as the single containers, and indeed the period of coexistence in some of the latter was longer than in the former (compare Figs 12 and 13). Thus step 5 of the general scheme proposed by Pimentel et al. was rejected, at least in the prevailing experimental conditions. Step 4 of the scheme did not materialize in the 16-cell experiment, since there was only one reversal before extinction of the housefly population; however, a minority of the single-celled cages showed several reversals, which would be compatible with step 4 (but which might equally be produced by other mechanisms-such as variation in uncontrolled environmental factors).

The clearest evidence for the operation of steps 1, 2 and 3 of the scheme appears to derive from the very marked reversal of competitive superiority approximately one year after the start of the 16-cell experiment. This is backed up by an apparently increased competitive ability of the blowflies removed from this experiment after 38 weeks (they won 5 /5 contests with wild houseflies, whereas wild blowflies won in only 3/9 similar contests). However, on closer examination, the method of maintenance of the 16-cell cage reveals an alternative reason for this increase in blowfly competitive ability. Samples of wild-caught blowflies (and houseflies) were added to the cage at irregular intervals during the course of the experiment “to prevent any possible significant loss of genes due to inbreeding”. Of the origin of these flies we are told only that the “housefly and blowfly used were collected in the Ithaca area”. Such additions were made, amongst other times, in weeks 15, 22, 23 and 25 of the experiment. If some of these flies originated from a different panmictic unit than the original experimental flies, then the high competitive ability at week 38 may have been due, not to selection operating within the original population, but to a selective differential between different blowfly populations within the experimental cage-a point the authors themselves mentioned.

I t is apparent, then, that while some of the experimental results give some support to parts of the general hypothesis put forward, none of the proposed steps are confirmed by all the experiments, and the scheme in its entirety is supported by none. Also, there are some remaining problems in the interpretation of the results. It is not clear, for example, why very short-term fluctuations in the numbers of both species occurred. In addition, the cages contained three resources-an agar-based medium, portions of liver and sugar-lumps; yet the possible role of heterogeneous resources in any evolutionary change of competitive ability was not investigated.

No subsequent experiments have conclusively demonstrated the “genetic feedback” model of Pimentel et al. (1965) for any competitive system, nor even clearly shown that selection for increased competitive ability is depen-


dent on the species-frequency; though a related phenomenon has been described by Dawson (1979) as discussed earlier. Thus these must for the moment remain as intriguing possibilities.

B. Changes in the Variance of Quantitative Characters

It has sometimes been proposed that, where a population exists in the absence of interspecific competitors, the members of that population are found in a wider range of habitats, or utilize a greater variety of resources than do other populations (of the same species) which exist alongside competitors. This phenomenon has been given a number of names, and which of these has been used in particular cases has depended partly on the time-sequence of allopatry and sympatry. Where the former is thought to have arisen by migration of one species out of a sympatric area, the phenomenon has been referred to as ecological release (Wilson, 1961) and niche-expansion (for example, Lister, 1976a, b). Where sympatric colonies are thought to follow allopatric ones (temporally), the phenomenon has been referred to as ecological compression, and the idea that compression of habitats, but not resources, occurs in sympatry has been termed the “compression hypothesis” (see MacArthur and Levins, 1967; Schoener et al., 1979).

All such changes in the variance of ecological characteristics in a population may be due to within-phenotype and/or between-phenotype effects, as described by Roughgarden (1972). In either case, the change in the variance of the population may be an evolutionary change, or merely an uninherited behavioural response to the absence of competitors. As Schoener el al. (1979) have pointed out, changes in the variance of ecological characters associated with sympatry have often been considered to be non-evolutionary, behavioural processes, though these authors have begun to explore an explicitly evolutionary model.

Van Valen (1965) centred his discussion on morphological characters, which are likely to have a higher heritability than behavioural ones, and has proposed an evolutionary hypothesis (sometimes referred to as the “niche- variation hypothesis”). Basically, Van Valen argued that increased intraspecific morphological variation was found in allopatric island populations; and that this was due to an increased between-phenotype component of the niche, with different phenotypes filling slightly different ecological roles. Selander (1966) made a similar proposal, but a more specific one in that the phenotypes thought to adopt different ecological roles were the two sexes. Van Valen (1965) based his argument on bill measurements of six species of birds. Of the six, five showed a greater variability in bill-size on islands than on the mainland, the difference being statistically significant, for at least one sex, in four out of these five. In the sixth species, populations on the

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Azores were significantly more variable than mainland populations, but populations from the Canaries were less variable-though not significantly so. Thus the evidence from these six species suggests strongly that birds are more morphologically variable on islands than on the mainland.

Further studies on morphological variability in birds were undertaken by Soule and Stewart (1970). These authors compared the variability of three species of relatively generalist feeders with three relative specialists, and found no evidence that the former group were consistently more variable than the latter. On the basis of this finding and several other arguments Soule and Stewart rejected Van Valen’s (1965) hypothesis. While the use of a comparison of different species to comment on a hypothesis of intraspecific variation is questionable (Van Valen and Grant, 1970), some of the other points made by Soule and Stewart (1970) reveal some serious difficulties in accepting Van Valen’s interpretation of his data. Their most important criticism is that there are various possible explanations for Van Valen’s (1965) data, none of which has been ruled out as the cause of the increased variance on islands. These possible explanations (in addition to Van Valen’s) are: firstly, immigration to an island from a number of genetically different mainland populations; secondly, directional selection in a new environment temporarily exposing genetic variation already present; and thirdly, sampling from more than one panmictic unit on islands. In addition to these points, it is necessary to stress once again that, although morphological characters usually have higher heritabilities than behavioural ones, it is nevertheless quite possible that the increased variation in bill measurements on islands, as observed by Van Valen, reflects a non-evolutionary response to a reduction in the degree of interspecific competition or to some other feature of the island environment. Further work by Rothstein (l973), which supports Van Valen’s (1965) hypothesis, is subject to the same difficulties. However, Grant et al. (1976) have also provided evidence for Van Valen’s hypothesis from studies of Darwin’s finches, and there is now (Boag and Grant, 1978) evidence that the characters concerned, such as beak dimensions, have high heritabilities (as discussed in Section V.A) which favours an evolutionary explanation.

A detailed discussion of the ecology of landbirds on islands, which is relevant to the issue ofcharacter release, has been provided recently by Abbott (1980).

C. Changes in Heterozygosity and Gene-frequency

There are both advantages and disadvantages of working with gene-frequency or phenotype-frequency at a single locus (or a group of loci) rather than with the mean or variance of a quantitative character. The main advantage is that,


at least for those polymorphisms whose genetics have been established, there is no problem of unknown heritability-and indeed many cases of polymorphic variation are completely genetic in nature, a situation probably never found with continuous variation. (Note that, with a “new” enzyme polymorphism, where the electromorphs have not yet been analysed genetically, the problem of heritability remains.) The greatest disadvantage is that the link between the variation under study and the mechanism of competition is often more obscure. It is fairly obvious, at least in general terms, that the size and shape of feeding apparatus may affect competition for food. It is much less obvious how (or whether) the frequency of the “fast” allele at a particular enzyme locus will affect competition. It may be, of course, that the locus concerned is one of the polygenes which contribute to the size and shape of the mouthparts: here we approach the general problem of the relationship between enzymic and quantitative variation, a problem which requires further investigation and is beyond the scope of the present article. If it is not clear how a particular locus might affect competitive ability, then of course selection may be acting not on the locus under study, but on a closely-linked locus. This problem has been discussed by Clarke (1975).

As yet there have been few studies on the effects of interspecific competition on polymorphisms, and so far they have not been reviewed as a group. I will deal fairly intensively with these, treating experimental studies first and following with a discussion of studies on natural populations.

I . Experimental Populations

Powell and Wistrand (1978) examined the effect of a competitor (D. persirnilis) on the heterozygosity, with respect to nine polymorphic loci, of D. pseudoobscura. This was part of a more general investigation on the effects of environmental variability on heterozygosity in the latter species. Two types of comparison were made which are of relevance to competitive selection. Firstly, single populations of D. pseudoobscura kept at 25°C on a single medium-type were compared, for heterozygosity, with populations competing against D. persirnilis but under otherwise identical conditions. Secondly, D. pseudoobscura from single and mixed populations, both of which experienced two media and a variable temperature, were compared in the same way. Comparisons, in both of the above cases, were made after 12, 18 and 24 months. (D. persirnilis, the weaker competitor, was continually replenished throughout the experiment.)

In the first type of comparison, the presence of D. persirnilis significantly increased the heterozygosity of D. pseudoobscura after 24 months of competition. In the second comparison, however, the competitor had no statistically- detectable effect on heterozygosity in D. pseudoobscura. These results are

(a) Drosophila pseudoobscura and Drosophila persirnilis

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difficult to interpret, both in the inconsistency between different comparisons, and in the direction of the competitive effect when it did occur. Powell and Wistrand (1978) argued that D . persimilis might have increased the genetic variability in its congener by adding excreta and other substances to the environment and so making it more complex. However, as the authors point out, it might equally have been predicted that genetic variability would decline in D. pseudoobscura in the mixed population due to some form of resource-partitioning. If D. persimilis did add something to the environment, the unknown substance presumably must have been already present in the second medium-type in the “variable” populations if the lack of competitive selection in the second comparison is to be explained. An alternative explanation could be that competition favours heterozygotes and that there is less competition in heterogeneous environments than in homogeneous ones. Finally, the question of whether and how selection was acting on the particular loci studied remains unanswered, though at least the loci concerned were shown not to be involved in chromosomal inversions.

(b) Drosophila melanogaster and Drosophilu simulans A second study of the effects of interspecific competition on polymorphic variation in Drosophila was carried out by Clark (1979). A stock of D. melanoyaster with a somewhat artificial fourth-chromosome polymorphism was produced. The stock was obtained by crossing a homozygous sparkling poliert spap’’ strain with a balanced lethal strain (ciD/1(4)29). The resultant stock contained only heterozygotes and sparkling homozygotes, because of the lethality of 1(4)29 homozygotes. Due to the superior fitness of heterozygotes over sparkling homozygotes, the polymorphism was maintained in all treatments. The question asked was whether competition with D. simulans altered the equilibrium frequency or the rate of attainment of the equilibrium. To answer this question, four replicates of three treatments were set up. In treatment A, D. melanoyaster populations were cultured in the absence of D. simulans; in treatment B, the species-frequency was maintained at 0.67 D. melanoyaster, and in C, at 0.33 D. melanoyaster. Species-frequencies were held constant in B and C by addition, when necessary, of extra D. simulans (the weaker competitor). In fact, all individuals of D. simulans were periodically replaced with new flies to prevent this species from evolving in response to interspecific competition.

The differences between treatments A, B and C in the frequency of the fourth-chromosome lethal allele were then observed, and are shown in Fig. 14. I t can be seen that populations of D. melanogaster subject to competition from D. simulans reached a significantly different allele-frequency to the single culture, and they appeared to reach that equilibrium more quickly. An additional experiment confirmed that the different results between treatments were not simply due to different densities of D. melanoyaster. There was little


Generation

Fig. 14. Frequencies of the 1(4)29 lethal allele in D. melnnogaster. A-single-species population. B, C-populations mixed with D. simulans. Each curve is based on mean of four replicates. Bars represent f 2 standard errors. From Clark (1979).

or no difference between allele-frequencies in treatments B and C, indicating that the intensity of interspecific competition, given that it occurred, had no effect (or at least no detectable effect) on the polymorphism.

This study shows rather clearly that interspecific competition can affect a polymorphism, but the relevance of the sort of polymorphism involved to the more subtle forms of variation usually found in natural populations is questionable.

2. Natural Populations

There appear to have been only three studies explicitly dealing with the selective effects of interspecific competition on individual polymorphic loci in natural populations. These studies, by Murphy (1976), Arthur (1978,1980~) and Gosling (1980) were all conducted on populations of molluscs, but all reached different conclusions. Murphy (1976) concluded that, in the genus Acmaea, selection produced interspecific divergence in allele-frequency. Arthur (1978, 1980c) concluded that interspecific competition gave rise to selection favouring a particular phenotype, in each of two species of Cepaea, regardless of the gene-frequency in the other. Gosling (1 980) concluded that convergent changes in allele-frequency in sympatry in Cerastoderma were not

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Alleles

Fig. 15. Cumulative frequency diagrams of Lap alleles of unispecific (-) and coexisting (---) populations of limpets. A, A . pelta; 0, A digitalis; H, A . scabra. a and b, Pigeon Point. c, Pacific Grove. N, number of animals. From Murphy (1976).

due to interspecific competition at all. I will now consider these studies in more detail.

(a) Acmaea. Murphy (1976) studied three species of this genus of intertidal limpets, namely A. pelta, A . digitalis and A. scabra. He examined populations from two areas of Californian coastline-Pigeon Point, where all three species were sampled, and Pacific Grove, where only the first two were studied. The locus examined was the Lap locus, coding for leucine aminopeptidase. The results are given in Fig. 15. All three allopatric/sympatric comparisons show apparent unilateral divergence in allele-frequency in sympatric populations.


However, there are two main problems in interpreting this as competitive selection on allele-frequency.

(i) Only one allopatric and one sympatric sample was taken of each species in each area (except for A. digitalis at Pigeon Point which was used to compare with A. pelta and A. scabra separately). Thus there is no information on variation of these species within allopatry or within sympatry.

(ii) This study was in fact based on electromorphs, and alleles were “inferred” rather than known. Thus, in common with most studies on morphological characters (see Section V.A), there is uncertainty as to whether the variation observed is genetic. (The possibility of non-genetic “polymorphism” must be kept in mind due to the known occurrence, in many species, of post-translational modification of proteins.) As a result of these problems, it is not possible to draw a firm conclusion from this study of electrophoretic variation in Acmaea.

(b) Cepaea. Arthur (1978, 198Oc) studied allopatric and sympatric populations of the helicid landsnails C. nemoralis and C. hortensis from a number of geographically separate areas in Britain and Europe. The locus examined was that determining the presence or absence of bands on the shell. This locus is known to have two alleles, with unbanded being dominant to banded in both species (see Cain and Sheppard (1957) and Murray (1963)). A summary of the results in all areas studied (Arthur, 198Oc) showed that in many though by no means all areas, sympatric populations exhibited a significantly higher frequency of bandeds than allopatric populations. This was true of both species, and in some cases the significance levels were extremely high. The results for the area in which this effect of sympatry was greatest are shown in Fig. 16. It is important to note that although this individual area appears to represent a displacement of C. nemoralis away from C . hortensis in sympatry, other areas showed sympatric convergence. However, although the results were not consistent from place to place in terms of displacement/ convergence, they were consistent in that all areas showing a significant effect of sympatry exhibited a decline in the frequency of unbandeds. Thus the change in frequency in one species was not dependent on the value of the equivalent phenotype-frequency in the other co-existing species. The evolutionary changes in the two species are thus in parallel, as described in Section I1.F.

The easiest interpretation of these results is that unbanded snails, of either species, are weaker interspecific competitors than bandeds. Certainly, the variation associated with sympatric areas cannot be nongenetic. Nor could the pattern of variation observed be caused by interspecific hybridization or by any of the non-competitive selective forces known in Cepaea, acting alone (Arthur, 198Oc). However, there are still two important weaknesses in this case-study.

180

II

100

40

20

0

WALLACE ARTHUR

Sympatry I I I I I I I I I I I I I I I I

! I I

1 I I I 2 4 6

Distance(m x 100)

I 14

Fig. 16. The change in the frequency of unbandeds (XB') in C. nemoralis (0) on entering an area of sympatry with its congener, C. korrensis. (The frequency of unbandeds in the latter species is designated W.) Bars indicate 957" confidence limits. Distance is measured north from the southernmost sample. From Arthur (1978).

(i) Significant changes in morph-frequency between allopatry and sympatry are not observed in all geographical areas. This might not be expected, since the habitats differ and not all mixed-species colonies need entail interspecific competition. Also, the most marked shift in morph-frequency occurred in the very habitat (dunes) where competition is thought to be most severe in Cepaea (see Oldham, 1929; Boycott, 1934). Nevertheless, the lack of shifts in morph-frequency at allopatry/sympatry borders in some areas does render the interpretation of this case-study more difficult.

(ii) Although the hypothesis that unbanded snails of either species are weaker interspecific competitors would explain all the results, i t is not yet clear why-i.e. by what physiological or behavioural mechanism-unbandeds should indeed be less able to compete. Until this is established, a combination of other selective agents cannot be ruled out as a possible explanation for the changes in morph-frequency observed.

( c ) Cerastoderma. Gosling (1980) studied variation at the phosphogluco- mutase locus (Pgm) in two species of marine cockle, Cerastoderma rdule and C. gluucum, with particular reference to the effect of sympatry on allele- frequencies. Although allopatric samples showed little variation from place to place, there was highly significant convergence in sympatry, this being of a unilateral kind, entirely due to a shift in allele-frequency in C. gluucum.


Gosling (1980) argues that this convergence is the result of selection for common characteristics in a common environment, and two lines of evidence support this assertion. Firstly, the habitat of all the mixed populations and the single C. edule populations was an intertidal one whereas C. glaucum normally occurs allopatrically in stagnant saline pools. Thus the species which shows a change in gene-frequency is the one which encounters a marked change in habitat. Secondly, in one of the “mixed” populations, the two species were in fact separated by a distance of 0.5 km yet the convergence still occurred. It should also be noted that interspecific hybridization is known to be possible between C. edule and C . glaucum (Kingston, 1973) and this is clearly another potential cause of sympatric convergence, although the pattern of electrophoretic variation observed in Gosling’s study indicated that hybridization was not occurring in the populations sampled. In conclusion, there appears to be no need to invoke competitive selection in this particular example.

VI. CONCLUSIONS

Several possible evolutionary consequences of competition between species have been proposed, and some of these have been developed in detail by theorists. Many experimental and observational case-studies have now been conducted in which evolutionary aspects of interspecific competition have been examined. Yet in very few instances have such studies been able to conclusively demonstrate that variation observed in a character was a direct consequence of selection resulting from the competitive process.

On the present evidence, it seems unlikely that character convergence as a direct result of interspecific competition is a common event, and indeed it is questionable whether truly competitive convergence occurs at all. Also, there is considerable doubt as to whether the elaborate genetic feedback hypothesis is correct. However, despite a number of problems besetting many individual case-studies, there is increasing evidence that, in at least some situations, competition may result in character displacement, or in the evolution of increased competitive ability, in one or both competing species. There is also a reasonable case (though perhaps a less convincing one) for the view that competition reduces genetic variability in morphological characters or, conversely, that the lack of competition acts to increase such variability. However, as regards the relative commonness of character displacement, character release and the evolution of competitive ability, and indeed the extent to which these processes occur separately to each other, almost nothing is known. From the few studies that have been conducted on the evolutionary effects of interspecific competition at the level of the

182 WALLACE ARTHUR

individual locus, there is some evidence that competitive selection does operate at this level. However, again, the relative commonness of different coevolutionary patterns is uncertain.

In order that these gaps in evolutionary knowledge be reduced, future studies ought to become more preoccupied with the heritability of characters, more analytic as regards the meaning of competitive ability, and more determined in their attempts to distinguish interspecific competition from other selective agents, than the majority of studies conducted to date.

ACKNOWLEDGEMENTS

I would like to thank Paul Greenwood and Gordon Robertson for reading and criticizing the manuscript; and Jan Laverick for doing the typing. I am grateful to the Universities of Newcastle upon Tyne and Durham for the use of their libraries; and to the authors and publishers concerned for their permission to reproduce the Figures shown in the text.

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Landscape Ecology as an Emerging Branch of Human Ecosystem Science

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I. Introduction. . . . . . . . . . . . . . . . 189 . . . 190

A. Some Definitions of Landscape and Landscape Ecology . . . . 190 B. Some Relevant Conceptual and Methodological Contributions . . 193 C. Towards a General Biosystems Theory . . . . . . . . 197 D. The Role of Landscape Ecology as a Human Ecosystem Science . . 204

111. Practical Contributions of Landscape Ecology . . . . . . . 210 A. Major Contributions in Central Europe . . . . . . . . 210 B. Landscape Ecological Studies in Israel . . . . . . . . 222

IV. Landscape Ecology and Environmental Education . . . . . . 228 V. Summary and Conclusions . . . . . . . . . . . . 229

Acknowledgements . . . . . . . . . . . . . . . 230 References . . . . . . . . . . . . . . . . . 230

11. The Conceptual and Theoretical Basis of Landscape Ecology

I. INTRODUCTION

In Central and Eastern Europe, landscape ecology has gained general recognition as a branch of modern ecology, dealing as it does with the interrelations between man and his open and built-up landscapes. There are chairs of landscape ecology in several universities in West Germany and a Federal Institute for Nature Conservation and Landscape Ecology in Bad Godesberg. In 1968, a symposium on landscape ecology was held (Tuxen, 1968) and many papers are devoted to this subject at meetings of the German Society for Ecology.

The English-speaking world, and especially the United States, is almost totally unaware of these developments. In a recent critical review of human ecology (Young, 1974), landscape ecology was not mentioned at all, in spite of long discussions on related subjects, such as landscape architecture, land planning, nature conservation and applied ecology in general. Although more than 400 references were cited, there was not a single, relevant non-English one among them.

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The object of this paper is to bridge this gap by reviewing some of the recent developments in landscape ecology in Europe and Israel and, at the same time, to make a first attempt at outlining the unifying principles and concepts of landscape ecology as an emerging human ecosystem science.

11. THE CONCEPTUAL AND THEORETICAL BASIS OF LANDSCAPE ECOLOGY

A. Some Definitions of Landscape and Landscape Ecology Probably the earliest literary reference to landscape was in the Book of Psalms, 48:2, where the beautiful view over Jerusalem from Mount Zion is mentioned.

The meaning of the term ‘’landscape’’ has undergone great changes (Whyte, 1976), but the original visual-perceptual and aesthetic connotation from the Bible is still used in literature and art and by most landscape architects and designers (Young, 1974). In recent years, highly sophisticated statistical methods and advanced psychological theories have been used to evaluate landscapes, but an ecological perception has been lacking (see Arthur et al., 1977; Zube et al., 1975 for reviews).

In the Germanic languages, Landschaft-landscape, derived from “land” and sometimes identical to it, can also mean a certain geographical-political area. It has been adopted by geographers as a synonym for geomorphological landforms and has become a scientific term.

Russian geographers were the first to broaden the narrow geomorphological definition of landscape. They included both inorganic and organic phenomena of the earth’s crust and called the study of its totality “landscape geography” (Troll, 197 1). The Russian term “biogeocenose” (Sukachew, 1960) has a broader geographical-regional meaning than the English “ecosystem” as introduced by Tansley (1935). Russian ecologists also emphasize the active and very often positive role of modern man in shaping the landscape, and use for this the term “culture-biogeocenose”. In marked contrast, in the Western world, under the dominating influence of Clementsian climax theories, man is still viewed solely as an external, destructive agent.

The semantic polarity between natural-unspoiled-wilderness+limax, on the one hand, and man-made-spoiled-artificial, on the other, is so deeply ingrained in Western ecological ideology, that a holistic landscape concept is not easily accepted. This in spite of the fact that one of the outstanding North American ecologists, Dansereau (1957), introduced it in an English textbook. In the introductory chapter to his pioneering Biogeography, an ecological perspective, he stressed that the crux of ecological thinking is “the

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holocenotic point of view”, in which the ecologist views the environment as a whole. He considered the landscape to be the object of study at the highest integrative level of environmental processes and relationships, namely the industrial level. The science covering this is human ecology, which has affinities with anthropology, agriculture, forestry, human geography, soci- ology and history and studies the influence of man on the landscape as he uses the land and its resources. He devoted the last chapter of this book to the subject of man’s impact on the landscape and described six successional phases of use, in which man gained increasing control: gathering, hunting, herding, agriculture, industry and urbanization. Man achieved this by upsetting natural balances and creating completely new ecosystems on the one hand, and by deliberately moulding the evolutionary forces in living organisms (including himself), on the other. In Dansereau’s opinion, through this new and highest level of landscape modification, man has inaugurated a new geological epoch in the exploitation of environmental resources: the “noosphere”. This term was first suggested by Vernadsky (1945) and re-evaluated by Teilhard de Chardin (1966) as a major evolutionary advance of mankind and his “co- reflexive self-evolution”.

More recently, Dansereau (1966) added atmospheric control and extra- orbital travel to the six successive phases of human interference in the landscape. He was not aware of the science of landscape ecology in Europe, but, in discussing the new technological methods of inquiry into conservation and multiple land use, he stated that we are now entering the engineering phase, which acknowledges the fact that virtually all landscapes in the world are under some kind of management. This must be a rationally scientific, ecological landscape management and “not merely applied ecology, any more than medicine can be reduced to applied biology”.

German biogeographers, especially Troll and Schmithusen, further developed the Russian geographers’ holistic interpretations of the landscape. Schmithusen (1936) defined it as “the whole Gestalt of any part of the geosphere of relevant order of size which can be perceived according to its total character as a unit”. He distinguished between the pristine Urlundschuf, the natural Naturlundschuft and the cultural Kulturlandschuft. According to Schmithusen (1 96 I ) , more extensive Nuturlundschuften can be found where the nature of the land precludes man’s permanent habitation, such as ice and sand deserts, high alpine mountains and certain parts of the tropical rain- and mountain-forests, and the boreal forests and tundra. The Kulturlundschuft is dominated by the naturally-conditioned spatial order only to a limited extent. Here, different principles of order, determined by human requirements, are operating and the question of what part the vegetation plays in the landscape from an ecological, functional and spatial point of view, should be considered separately.

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According to Buchwald (1963), we are living in a Kulturlandschaji which has been shaped by man over centuries. A state of equilibrium has been established between Kulturlundschaft, population density, landscape potential and requirements of society for living space; these factors find their external expression in the spatial order of this living space, its life system and its scenery. Buchwald views the landscape as the total living space and as a multi-layered Wirkungsgefuge: an interacting structure of both the geosphere and the biosphere. He designated to landscape ecology the important task of overcoming the tensions between modern society and its landscapes. Tensions which result, in his opinion, from the discrepancy between the rapidly increasing demands of the industrial society and the natural potentials of the land.

The term landscape ecology was introduced by Troll (1939), who realized the great potential of aerial photography to obtain an overall view of the landscape. He proposed to combine the “horizontal” approach of the geo- grapher, who examines the spatial interplay of natural phenomena, with the “vertical” approach of the ecologist, who studies the functional interplay at a given site-“ecotope”-as an ecological system. Later Troll (1 968) defined landscape ecology as “the study of the main complex of causal relationships between living communities and their environment in a given section of landscape. These relationships are expressed regionally in a definite distribution pattern and landscape mosaic and in a natural regionalization of various orders of magnitude”.

An important, first attempt at system-theoretical and cybernetic interpretation of landscape ecology was made by Langer (1970). He defined landscape ecology as “a scientific discipline, dealing with the internal functions, spatial organization and mutual relations of landscape-relevant systems”. Like Dansereau, he considered the landscape-ecological system as the highest integrative level, above the autecological “monocene” system and the syneco- logical “holocene” system. This regional-ecological system integrates ecotopes as the smallest landscape elements. The term ecotopes has been proposed by Troll (1950) as a complex of biotopes and has both spatial-geographical and ecological dimensions.

Langer stated that the problems arising in the Kulturlandschuft are related not only to the natural sciences, but also to the social and cultural sciences, and he stressed the importance of the study of human influences through utilization and other anthropogenic impacts. In his opinion, landscape ecology can provide an overall view only in natural landscapes; in cultural landscapes it can merely define natural potentials of the anthropogenically influenced Wirkungsgefuge.

Langer (1973) also distinguished between bio-ecology and human ecology from a system-theoretical point of view, claiming that the man-environment system presents a special field of ecological observation: the “geo-social


environment”, which is also relevant in planning processes. This has much in common with the techno-ecosystems referred to below, but lacks integration with a higher level of organization (see Section 1I.C).

In his 1970 paper, Langer cited Focker-Hanke (1959) who stated that “in the Kulturlandschaf, anthropogenic elements do not just join natural ones, but form units at a higher level: a true integration”. Langer, however, did not attempt to classify Natur and Kulturlandschaften from a system- theoretical point of view and this will be done in Section 1I.D.

B. Some Relevant Conceptual and Methodological Contributions

2. The Broadening of Phytosociology

In its formative stage, landscape ecology was conceived largely as a bio- geographical discipline. However, plant ecologists’(and in Central Europe this means phytosociologists and geobotanists), because of their field-oriented outlook and their concern with the open landscape and its natural and man- modified vegetation, quickly took a leading position in this field. They were joined by applied ecologists, foresters, agronomists and gardeners, as well as landscape architects and planners with an ecological outlook.

Without doubt, one of the central features in the theory of landscape ecology was the recognition of the dynamic role of man in the landscape and the quest for systematic and unbiased study of its ecological implications. For this purpose it was essential to eliminate preconceived Clementsian climax-succession dogmas from any methodological and practical considerations. These dominated not only American ecology, but were accepted almost without criticism by the Braun-Blanquet school of phytosociology. It was also important to broaden the scope of this methodology itself, from its sole reliance on floristic species composition, to include causal ecological relations between vegetation and environment, based on ecophysiological studies and insight. This has been achieved, to a large extent, through the contributions of some outstanding German ecologists, who educated a new generation of plant ecologists and others in related fields, who now occupy leading positions in landscape ecology.

A first, important step in this direction was the replacement of the term “climax” by the more meaningful “potential natural vegetation”. This was suggested by Tuxen (1956) and adopted by Schmithusen as the “potential Naturlandschaft”. It refers to the composition of the vegetation which would become established if man suddenly disappeared. It is based on current knowledge of actual existing vegetation potential, its developmental tendencies and site relationships.

Ellenberg (1963, 1978) has shown that the vegetation of Central Europe

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is the result of thousands of years of human history and its impact of hunting, gathering, burning, cutting, coppicing, trading etc. “which did not leave a single spot in its original state”. It should, therefore, be considered as an old Kulturlandschaft and, because of the far-reaching changes in habitat conditions, it is impossible to reconstruct the pristine Urlandschaft. At most a reconstruction of the potential Naturlandschaft, sensu Tuxen, can be attempted, with the help of ecological, historical and geographical data, but even so, information is missing for many densely populated areas.

In Germany maps showing potential vegetation have been drawn, using phytosociological methods of the Zurich-Montpellier school (Trautmann, 1966). They have yielded important information for landscape planning and management and their interpretation had benefited much from the pioneering work of Ellenberg (1950) on man-modified pastoral and weed associations and the introduction of “ecological species groups” as criteria for plant community classification. It was found that these could be used as indicators of climatic and edaphic conditions and thus the basis was laid for a successful synthesis with other classification and ordination methods which have become important in integrated landscape-ecological surveys. Ellenberg’s (1 956) summary of his methods has been revised and enlarged in an attempt to produce an integrated synthesis of European and Anglo-American approaches (Muller-Dombois and Ellenberg, 1974). In recent years, Ellenberg has devoted himself to broadening the scope of ecology in Central Europe by initiating integrated ecosystem studies, especially the Solling project (Ellen- berg, 1971), which has become one of the most comprehensive multidisciplinary forest and grassland ecosystem studies within the International Biological Program.

Ellenberg (1972) proposed the following definitions of the environmental burdens on ecosystems:

Landscapes, in general, are composed of mosaics of ecosystems which form a more or less closely integrated whole through their mutual relations. These can then be considered as ecosystems of a higher order. Burden (6): impact of factors, such as air pollution by SOz, or complex of factors, which do not belong to the normal natural system and are mostly man-induced. Liability to burden (D): liability of a certain ecosystem to be harmed by burdens on the landscape, e.g. a steep slope is more susceptible to water erosion than a less inclined one. Liability to temporary burden (L): extent and rate of changes in the equilibrium of the constituents, caused by burden in a certain ecosystem and/or in their abiotic conditions. It is the reciprocal value of the resilience or buffering against disturbance of the equilibrium by burden.


Susceptibility to temporary burden (a: product of liability and temporary burden lability, S = D x L. If D and L are rated on a scale of 10, then S,,, = 100. Regeneration capacity and temporary load (R): the extent and rate of regeneration of an ecosystem which has been distorted by burden. Burden carrying capacity (B): A measure of the susceptibility of ecosystems to burden and their regeneration capacity expressed as B = kR( 100 - E), with k = 0.1 or 0.01, and R rated on a scale of 10. The kind of burden can be expressed by indices, such as bS02, D s o ~ , S S O ~ , Bso,, Snoiso etc.

As an example of this quantitative rating system, Ellenberg (1972) estimated for the first time the relative impact of SO2 in different ecosystems.

2. The Introduction of Ecophysiology and Dynamic Ecology One of the greatest influences in modifying the scholastic Clementsian and Braun-Blanquet dogmas, was H. Walter, who introduced eco-physiological methods into geobotany. In his Standortlehre, an analytical-ecological geobotany with a holistic treatment of ecological factors, including the anthropogenic one, Walter ( 1960) prepared the ground for integrated ecosystem studies. In his monumental Die Vegetation der Erde in oeko-physiologischer Betrachtung (Walter, 1964, 1970), he provided a world-wide view of landscapes, as covered by intricate patterns of dynamic vegetation types, formations and ecosystems, determined not only in floristic composition but also in structure, stability, diversity and productivity by regional climate, local site conditions, biotic interactions and human modification. In his introduction he refuted the theories of climax and primary succession and stated that even the “zonal vegetation”, typical of distinct climatic zones, corresponds to the climax concept only in a very limited way:

All attempts to save the climax concept by establishing a poli-climax term or by introducing climax groups or clusters are not satisfactory, because they still include the concept of primary succession. A certain dynamic view of the vegetation is indeed justified. It should, however, not leave the ground of reality and lose itself in speculations. In this book, neither climax and succession stages, nor hierarchical plant

community classifications were mentioned, but the importance of burning, grazing and human intervention in shaping and maintaining these vegetation types was stressed, as was the need for continuous management as an ecological means of conservation, e.g. in the case of the Caluna and Erica heather formations.

3. The “Dutch School” of Landscape Ecology In the Netherlands a sound theoretical framework for landscape ecology and its practical, large-scale application has been provided by work conducted in

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the Botanical Institute of the University of Nijmegen and the RIN State Institute for Nature Conservation at Leersum. Those involved in landscape ecology have been inspired by the work on nature conservation and landscape management and planning of Westhoff (1969, 1970, 1971), Moerzer Bruyns (1967) and Benthem (1952). Landscape ecology is firmly established in the extensive research carried out in the field of vegetation science. As in Germany, this has been based on the phytosociological methodology of the Zurich-Montpellier school, but original and highly advanced quantitative methods have been developed (Van der Maarel, 1969; Westhoff and Van der Maarel, 1978), and close links maintained with the applied fields of forestry, agriculture, hydrology, regional and town planning and land reclamation, as well as with geography and pedology. Dutch landscape ecologists with their good knowledge of English and German, have been able to incorporate into their methodology the most valuable concepts and techniques, not only from European, but also from Anglo-American sources and from modern ecology as a whole.

A central feature in Dutch landscape ecology is the recognition of the dynamic role which man has played over many centuries in creating diversity and stability. Van Leeuwen (1966, 1973) interpreted this role in a cybernetic way and formulated the “general relation theory” of pattern (changes in space) and processes (changes in time), and established the inverse relation between spatial and temporal variety. Westhoff (1971) and Van der Maarel(l971) have illustrated this theory with many examples. They distinguished two contrasting types of environmental boundary: the limes convergens or ecocline, characterized by (1) sharp boundaries between contrasting, adjacent sites, which fluctuate in time, (2) coarse-grained vegetation patterns, and (3) low alpha diversity (sensu Whittaker, 1972); and the limes divergens or ecotone, characterized by (1) gradual changes from one site type to another, (2) a fine- grained pattern and (3) high alpha diversity. The ecotone is maintained chiefly by small-scale, spatial changes in the environment, causing numerous small, stable boundaries, and was favoured by the former agricultural and mining systems. Ecoclines are currently being created through abrupt changes in management: cessation of grazing or mowing, burning and change of owner- ship, and are therefore highly undesirable for nature conservation when defined as the conservation of the highest potential landscape diversity.

In combining the ecological classification of landscapes according to naturalness (Westhoff, 1971) with a scale of the human influences on man- modified landscapes and ecosystems in Germany (Sukopp, 1972), Van der Maarel(l975) distinguished seven stages from “natural” to “cultural” in which both flora and fauna, vegetation and soil structure were controlled by man. Superimposing on this the stages of successional development from pioneer to mature, he arrived at an interesting three-dimensional ordination, which


could be helpful in appraising landscapes for conservation and management purposes.

Van der Maarel(l975) claimed that over the previous 25 years European vegetation science had helped to show that a subtle balance existed between natural and cultural demands which enriches man’s biotic environment. He distinguished on the one hand “man-made natural ecosystems”, sharing properties of the mature, resistant ecosystems, called by him “internally stable” and, on the other hand dynamic, elastic systems, called by him “externally stable”. He based practical suggestions for landscape management on this.

Van der Maarel made a plea to face the challenge of the very complex, interrelated patterns of man and his natural ecosystems at the landscape level. He referred to landscape ecology as the relevant science to deal with this challenge and complained of the little attention paid to it during the first INTECOL congress where he delivered his paper.

4. Conclusions

Landscape ecology views the landscape not just as an aesthetic asset and as part of the physical environment but as the total spatial and functional component of man’s living space, integrating geosphere with biosphere and noospheric, man-made artefacts. Landscape ecology thus extends beyond the purely natural realm of classical, biophysical and bio-ecological science and enters the realm of man-centred fields of knowledge, such as the socio- psychological, techno-economical, cultural and historical aspects involved in modern land uses. The question arises whether it thereby also approaches the definition of an interdisciplinary, human, ecological science with all the philosophical-epistomological and methodological implications, pointed out by Young (1974) in such a comprehensive way.

This can be comprehended only within the framework of a unified, ecological theory. Moreover, since Young’s (1974) review, several important developments have taken place in general systems theory, biocybernetics and eco-systemology which may contribute much towards advancing such a unified ecological theory and the role which landscape ecology could play in it.

C. Towards a General Biosystems Theory

1. New Insights into the Holistic Axiom

The relations between ecology and general systems theory have been discussed from the point of view of natural resources management by Schultz (1967) and from the point of view of human ecology by Young (1974). For landscape

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ecology both approaches are equally important and therefore should be amalgamated and used as a joint basis for future studies.

At the First International Meeting of Human Ecology in Vienna in 1975, organized by the Society for Human Ecology (Knotig, 1975), two sessions were devoted to the theoretical background of human ecology and its relations to ecology and other sciences. Although the terms systems, ecosystems and human ecosystems were mentioned in several papers and attempts were made to define their role in a theory of human ecology, the only contribution approaching the problem from a truly system-oriented point of view was that by Bierter (1975).

The philosophical basis of a general systems theory is the holistic approach to a hierarchical organization of nature as open systems with increasing complexity through the evolution of emergent qualities at each higher level of organization (Von Bertalanffy, 1968; Weiss, 1971). Egler (1942) was the first ecologist to recognize this approach, which is now generally accepted in ecology, as a central feature in vegetation science (Rowe, 1961; Dansereau, 1975; Buchner, 1971). Koestler (1969) introduced the term holon to charac- terize the unique nature of the systems at each integrative level of the hierarchical order: they are intermediary entities, functioning as self-contained wholes relative to their subordinates, but at the same time depending on entities at the next higher hierarchical level of integration. As Bierter (1975) pointed out, the term holon is most valuable to describe the complementary aspects of being-part-of and wholeness, of differentiation and integration in ecological systems and it will be used in our further discussion.

The holistic axiom that the whole is more than its parts, has been restated in quantitative terms by Mesarovic et al. (1970). Using a quantitative description, Weiss (1969) has shown that because of the constraints on the degrees of freedom of component parts as a result of system behaviour, the variance of the total system V, is less than the sum of the variances of its elements (V,,, vb, V,, . . . V,,): V, < V,, + Vb + V, . . . V,,. Thus, coordination and control become the emergent qualities of the new holon.

An example of this holistic axiom has been cited by Lorenz (1973). He referred to the work of Hassenstein (1970) which showed, by means of a simple electronic model, how the coupling of two independent electric circuits cause the sudden, flash-like emergence of a new system with its own qualities and behaviour. Lorenzcalled the sudden birth ofa system with new properties, which cannot be expected or predicted from the properties of each holon, fulguration (jiulguratio = lightning flash), and attached great importance to its occurrence in evolution. He stated that “cybernetics and system theory have freed this sudden creation of a system with new properties and new function from the odium of a miracle”.


2. Living Systems and Ecological Systems- “Biosystems ”

In recent years, general systems theory has been expanded into general living systems theory. Miller (1975a, b) has distinguished between abstract, conceptual systems and concrete systems, as real entities which have definable space and time relations. He identified seven levels of living systems, with the cell as the lowest and the supranational system as the highest, whilst Rowe (1961) pointed out that ecosystems integrate these living systems and their physical environment, and should be considered as a higher level of integration.

As open systems, ecological systems as well as living systems exchange energy, matter and information with their environment which enables them to renew their components and to maintain their structure in a state of dynamic flow-equilibrium. But as a result of the fulguration process, whereby a system with new properties evolves as a result of system interaction, new isomorphs arise from the integration of these living systems and their environment. These are the main subjects of ecological research. It would be most revealing to identify, on a similar basis to that used by Miller, the isomorphs of the most critical subsystem of both natural and human ecosystems. If this were achieved, it would prepare the ground for a truly integrated theory of living and ecological systems or biosystems.

3. Reductionistic Tendencies and Cybernetic Approaches

Young (1974), in discussing the relationship between general systems theory and human ecology, warned that “a general system approach could return us to a discarded mechanistic focus, ignoring the reality of man”. He also doubted whether the methods of definition and measurement utilized in biological ecology were acceptable to human ecology and whether such techniques as the mathematical analyses of ecosystems might not be directly applicable to human systems. Egler (1970) expressed a further serious warning that “the scientific and ecological concepts may wither and only the dry technology of system analyses be left”. He claimed that the advent of the computer had often “encouraged the trivialization of scholarship and the belief that the things that count are those that can be counted”.

There are real dangers in this. There is a reductionistic tendency which depicts energy exchange as the only basic process, not only in natural ecosystems, but also in human systems. However, energy flow diagrams and models (Odum, 197 1) provide only simplistic “ecological” explanations of human systems which could be interpreted as a new kind of neo-materialistic “energy marxism”. As Ellenberg (1973) rightly remarked, this would be harmful both to ethics and to ecosystem research. In order to avoid this

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danger, it should be emphasized that the quantitative and functional energetic aspects, measured by energy and matter flow in ecosystems, must be complemented by a qualitative description of the structural aspects of regulation, as measured by information exchange.

Cybernetics, the scientific discipline dealing with regulation of ecological systems, was developed by Wiener (1948) for system engineering and communication and extended to biology by Ashby (1963). It is now also widely used in the rapidly growing field of mathematical ecology and in system analysis (e.g. Dale, 1970 Patten, 1971; Caswell et al., 1972). Its scope has been considerably broadened in Germany, as is demonstrated by the excellent Worterbuch der Kybernetic (Klaus, 1969) and, with a “marxist-dialectic’’ interpretation, it has also become an important scientific discipline in Eastern Europe.

Important contributions on the application of cybernetics to human biology, ecology and environmental education have been made by Schaefer (1972,1977) and to the theory of landscape ecology by Langer (1970) and Van Leeuwen (1966). Cybernetic-mathematical models have been suggested in landscape ecological studies by Bauer et al. (1973), but of greater significance is the biocybernetic approach to human ecology and environmental planning by Vester ( 1 976).

Lorenz (1973) approached the problems of energy, information and evolution from a cybernetic point of view. He stressed that the gain and storage of information relevant for survival of the species in evolution is as vital a process as that of gain and storage of energy and that these two processes are coupled by positive feedback loops. This coupling within a cybernetic cycle results in a synergistic effect. It is the prerequisite for life, provides an explanation of how “life is able to hold its ground facing the superior force of the merciless inorganic world”. It also helps to provide a solution to the riddle of speed and direction of evolution. Life can be regarded as gain of information, that is a cognitive process together with an economical one.

According to Lorenz, the high organization of social cooperation in primates was the prerequisite for the creation of human society, a “fulguration”, which resulted in the integration of conceptual thinking, syntactical language and a cumulative tradition in cognitive performance. The concrete realization of such a supra-individual system is called a culture. However, Lorenz emphasized that although there is the same positive feedback coupling information and energy gain, in the formation of a culture as in the survival of a non-social organism, the transfer of acquired knowledge is done by a different mechanism. Man is the only living creature who mobilizes energy, apart from solar energy which enters the living cycle through photosynthesis. Our planet now faces the results of this positive coupling of gain of information and energy by homo industrialis. We shall refer to it below in discussing

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our man-made and driven techno-ecosystems as lacking negative feedback coupling, and therefore also lacking in homeostatic regulation.

4. Prigogine’s Theory of Selforganization and Human Systems

A major breakthrough has occurred recently in the field of non-equilibrium thermodynamics with the discovery of the principle of “order through fluctuation” (Prigogine and Nicolis, 197 1; Prigogine, 1975; Prigogine et al., 1972; Nicolis and Prigogine, 1977). This principle may cast some doubts on the validity of the Second Law of Thermodynamics as interpreted by Boltzman’s ordering principles and perhaps resolve the apparent contradiction between the general trend of increase in entropy and dissipation of structure and the increase of neg-entropy towards higher levels of organization of life and creation of structure in the evolutionary process. Contemporary reductionistic biologists, like Monod (1970), have tried in vain to explain this by the process of random fluctuations, which would result in the random formation of macromolecules and in the process of evolution. However, according to Prigogine’s theory of “order through fluctuation”, systems which are partly open to the inflow ofenergy, matter and information, are in a non-equilibrium state. They tend to move through a sequence of transitions to new regimes which in each case generate the conditions of renewal of high entropy production within a new and higher regime of organization and thus open up possibilities for the continuation of metabolizing activity for life. The recognition of behaviour of such “dissipative structures” has opened the way for a new theory of self-organization of physical systems. As Prigogine (1976) and Nicolis and Prigogine (1977) have shown this theory is valid not only in the physical domain but also in the biological and ecological domain, and according to Jantsch (1975) also in the social and spiritual realm of man. He pointed out that “order through fluctuation” seems to be a basic mechanism, penetrating all hierarchical levels of human systems, organizations, insti- tutions and cultures, as well as the overall dynamic regimes of mankind as a whole, which evolved from hunting and fruit collecting to primitive agriculture and hence to our global systems of cooperation. In his opinion, social sciences had recognized only external, “Darwinian” factors and he tried, successfully, to shed some light on internal factors in the evolution of human systems which have great relevance to this discussion.

Jantsch distinguished three basic types of internal self-organizing behaviour:

(1) Mechanistic systems, which do not change their internal organization. (2) Adaptive (or organismic) systems, which adapt to changes in the environment through changes in their internal structure in accordance with pre- programmed information (e.g. engineered or genetic templates); to these

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belong all non-human bio-systems and we shall refer later to this type of information as “biophysical information”. (3) Inventive or human action systems, which change their structure through internal generation of information (invention) in accordance with their intentions to change the environment. Such information is generated within the system and in feedback interactions with the environment. The evolutionary time scale for adaptive systems in the biological domain corresponds to what Teilhard de Chardin called the “unfolding of biogenesis”, whereas for inventive systems in the human domain it would correspond to noogenesis (referred to as “cultural information”).

In relation to planning, this implies, according to Jantsch, our integral participation as regulators in the system to be regulated.

5. Bio-cybernetic Regulation and the Total Human Ecosystem Concept

Vester (1976) has stressed the high technological efficiency characteristic of the use of energy/matter and cybernetic information in biosystems, in contrast to the low efficiency of human technology and has described both in terms of certain basic biocybernetic rules which all viable biosystems obey. Amongst these are negative feedback coupling, to ensure that the system settles down to a stable equilibrium, recycling, re-use of everything produced, and the highly efficient and economical utilization of energy, particularly where sources other than direct solar energy are involved, e.g. energy in cascades, chains and coupling; the principle whereby force is not combatted with a counterforce, but is merely diverted and controlled cybernetically and is thus utilized for the purpose of the receiver, e.g. as in jiu-jitsu. These laws also include symbiosis and the principle of multiple use. The final rule, also to be applied in human systems, is the basic biological design, bringing organizational cybernetics together with creative “bionics”. This is the exploitation of the information gained from biological systems for technological purposes (Vester, 1974) so that every product, function and organization should be compatible with the biology of man and nature.

Vester made the suggestion that these rules are the internal rules of all viable biosystems from the cell up to the largest ecosystem, the biosphere, and that they should also apply to the system of human civilizations, which according to his definition, is one subsystem of the biosphere. He argued that they should provide a far better guarantee for survival and further evolutionary development than, for instance, “such a stupid premise as a single-tracked compulsion towards economic growth”.

This evolutionary strategy implies the ability of biosystems to alter their


behaviour and “jump to a higher organizational level, when reaching critical stages of density”. In Vester’s view these stages have been reached now:

Humanity and its man-made artificial systems (roads, towns, factories, mines, agriculture, etc.) were for a long time located relatively far apart on earth. However, due to the increasing population density, these systems have been crammed together so closely that a multitude of chemical, physical, energetic and social interactions have emerged between these, man and the biosphere. Inter- actions which have led to a new subordinate system: that of human civilization on this planet!

This system is not necessarily stable and viable. It may destroy itself and be eliminated from the biosphere, if it does not obey the above-mentioned fundamental roles.

The main reasons for the ecological, sociological, economic and political problems, such as man has never known before, are a lack of knowledge of these laws or failure to observe them. As long as our changed situation is not comprehended and the interlaced network is not realized-and even when these changes are realized, they are described in such a complicated way that they cannot be understood-we will continue to suffer ever greater setbacks and be forced to redouble our efforts in order to carry on just a little longer in the old way, all the time increasing our energy and raw material consumption. To put it briefly, what we need are new decision-making aids.

These should also be used in integrated land use planning and as an educational illustration of this, Vester used an environmental simulation game in which a simple but ingenious cybernetic sensitivity matrix of environmental interactions at the landscape level is applied.

As already mentioned, Egler (1942) was one of the first to realize the holistic nature of ecology and he criticized the conceptual and methodological weak- ness of contemporary plant ecology in failing to take account of this. More than 20 years later, Egler (1964) used the example of the failure to cope with the pesticide problem through scientific, ecological information to demonstrate the urgent need for holistic human-ecosystem ecology as the highest “ninth” level of integration, above the biocommunity and ecosystem level. In this “man-plus-his-total-environment form a single whole in nature that can be, should be and will be studied in its totality”. Egler (1970) called this the total human ecosystem and stated:

The chief goal of human ecosystem science is a knowledge of, and man-oriented technology towards, a permanent balance between man and his total environment, both operating as part of a single whole, that will afford a life of the highest quality.

As a highly qualified plant ecologist, Egler has devoted much of his energy in the past 30 years to the development of “vegetation management”. He summarized his experience in this field in what could be considered one of the

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first human ecosystem science books (Egler, 1975). He thereby became one of the first human-ecosystem/landscape ecologists in the United States.

D. The Role of Landscape Ecology as a Human Ecosystem Science

I . The Ecosystem Classification of Ellenberg

In the foregoing section, attention has been focused on certain conceptual developments which have occurred almost simultaneously and which have contributed much, in my opinion, to the consolidation of a general biosystems theory, and serve as a basis for a unified ecological theory and for the interdisciplinary concepts of human ecology.

This is a holistic, scientific theory of hierarchic order of open, living and ecological systems as holons with biocybernetic self-regulation and feedback control, and with the total human ecosystem as its highest level of integration.

That such an integration is conceivable is clearly indicated by the thermo- dynamic findings of Prigogine on “order through fluctuation of dissipative structures”, as a “fulguration” envisaged by Lorenz in a cognitive process in human cultural evolution, in Jantsch’s socio-ecological terms as noogenesis in “inventory human systems”, or, in Vester’s biocybernetic language, as a “jump to a higher system level of organization”. That this should be the chief aim of human-ecosystem ecology has been stated clearly by Egler.

After having outlined the broad framework of such a biocybernetic system- theoretical and ecological philosophy, or human ecosystemology, there is need for elucidating the role of landscape ecology and this can be accomplished only after a more concise definition than has been attempted to date, has been given of the semantic relations between natural and human ecosystems and of natural and cultural landscapes within a classification or ordination system. In this respect the recent ecosystem classification, proposed by Ellen- berg (1973) is of great value and can be used as a starting point for our considerations.

According to his definitions, “ecosystems are Wirkungsgefuge, interacting structures, formed by living organisms and their abiotic surroundings, which are to a large extent self-regulatory”. As functional units, ecosystems cannot be typified and ordinated in the same way as some of their components and therefore existing classifications of communities, climatic and edaphic types etc. can only assist, but not determine this classification. Because of our very limited knowledge of the diverse, smaller ecosystems, Ellenberg proposed an inductive, hierarchical classification, starting from the most extensive and complex ecosystems. His first grouping relates to their similarity in main


functional criteria, e.g. dominant life media (air, water, soil), primary pro- ducers and their limiting factors for production, material gains and losses, relative role of micro- and macroconsumers and the role of man in creating a particular ecosystem and its energy and raw material cycling, especially with regard to additional energy sources. The term “ecosystem” has no rank and can be used in the abstract, according to the classification hierarchy and nomenclature e.g. “limnic ecosystem”, and in the concrete, sensu Miller, e.g. “Lake of Galilee limnic ecosystem”.

Contrary to the widely held misconception, the biosphere should not be regarded, according to Ellenberg, as a higher level of integration on its own, but as the most extensive and diverse concrete global ecosystem. It has been subdivided by Ellenberg into two major groups, namely natural ecosystems, which more or less depend on solar energy, and urban-industrial ecosystems, which depend on fossil energy (and increasingly on nuclear energy). In this classification, Ellenberg has dealt only with subdivisions of the first group, according to size and function.

2. Bio-ecosystems and Techno-ecosystems as Holons of the Total Human Ecosystem

When we clarify the fundamental functional differences between the two groups of ecosystems, we must conclude that the biosphere can be regarded only as the largest natural or, more precisely, biological ecosystem, in short bio-ecosystem. On the other hand, the urban-industrial or technological ecosystems, techno-ecosystems, in lacking the biological function of photosynthetic conversion of solar energy, cannot be regarded as part of the biosphere. Thus, in accordance with the definition that ecosystems have no rank, the latter form the largest global techno-ecosystem or the technosphere. Consequentially, the largest entity embracing both biosphere and technosphere, together with relevant parts of the geosphere, is the ecosphere. In the technosphere, man with his technological skills, has overstepped the ecological and spatial limits set to life in the biosphere and thus, the ecosphere of “homo industrialis” includes all those parts of the geosphere, the atmosphere, lithosphere and hydrosphere, which are directly or indirectly influenced by him. He has also overstepped the limits of the geosphere in the stratosphere, with far-reaching ecological consequences for life on earth.

All natural or man-modified ecosystems should thus be regarded as bio- ecosystems in which autotrophic organisms are the primary basis for productivity. These are maintained by inputs of solar energy, natural biotic and abiotic material resources and are regulated chiefly by bio-physical information. On the other hand, techno-ecosystems are designed, made, maintained and controlled by man through inputs of fossil energy, man-made or con-

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verted material from the geosphere and biosphere and are regulated by cultural noospheric (scientific, political, spiritual, technological etc.) information, processed by human industrial civilizations.

As mentioned in the previous section, biocybernetic feedback control has evolved as one of the structural features of higher complexity during the long evolution of natural bio-ecosystems, ensuring their viability. Techno- ecosystems, on the other hand, are the very recent creation of man’s civilization and as such they are fed on positive feedback loops of energy/ matter and cultural information, but lack the biocybernetic feedback control, inherent in “adaptive biological systems”, sensu Jantsch.

Since the second industrial revolution they have grown rapidly into progressively larger urban-industrial complexes, showing not only symptoms of what Vester (1976) called the “urban crisis” syndrome, but threatening at the same time the bio-ecosystems with direct replacement, environmental pollution and what Naveh (1973a) called the “syndromes of neo-technological landscape degradation”.

However, man as a biological creature is dependent for his existence on the viability of natural and agricultural bio-ecosystems. His techno-ecosystems cannot survive without the biosphere, and their exponential growth may endanger not only the biosphere but also the technosphere itself.

Modern man occupies a dual position, serving as a receiver of vital inputs from the biosphere and geosphere but, through the outputs of the technosphere, concurrently modifying the biosphere and the geosphere. He is thus

Fig. 1. Modern man-the affector and the affected.


affecting and being affected by these modifications (Fig. 1). This dichotomy in man’s position, of dependence and independence, has probably been the major cause of the vague semantic and conceptual differentiation between human and biological ecosystems. It is a result of his closely interwoven biological and cultural evolution, his biogenesis and noogenesis. For millions of years, primeval man was an integral part of natural bio-ecosystems, until his cultural evolution added unique psycho-sociological and techno-economical dimensions to his biophysical nature. This lead in very general terms to the creation of both an abstract system, the noosphere (or if the sociosphere is regarded as a separate entity, of two abstract systems), and a concrete, spatial and physical system, the technosphere, in addition to the existing biosphere and geosphere.

More detailed discussions of the complex, cybernetic nature of human systems are given by Lazlo (1972) and Jantsch (1975). The latter sketched these basic systemic dimensions in relation to a hierarchy of natural systems (physical, biological, social and spiritual, named by Lazlo “cognitive”) and stressed their dynamic and simultaneous interplay.

From the ecological point of view this dichotomy of man’s position in nature can be resolved only by recognizing the holon properties of man, biosphere and technosphere as autonomous wholes towards their subordinates, but at the same time as dependent parts of a higher controlling whole, integrating man and his total environment, the biosphere, technosphere and geosphere, i.e. the ecosphere, into the total human ecosystem, as termed by Egler (Fig. 2).

3. Re-dejinition of Landscape and Landscape Ecology

The visual and spatial integration of biosphere, technosphere and geosphere already exists in the landscape. But now we can redefine it as the concrete, space/time entities of the total human ecosystem, with the ecotope as the smallest and the ecosphere as the largest, global landscape unit.

In Fig. 3 an attempt has been made to present a model of the relationships between different, major ecosystems holons and their concrete landscape units. These are distinguished as different types of open, cultural and built-up landscapes according to the kind and size of energy, material and information inputs from these holons and the increasing dominance of man-made artifacts. They can be viewed as a continuum of increasing modification, conversion and replacement of natural bio-ecosystems. At the present rate of exponential urban-industrial expansion, there is an alarming tendency towards the lower left corner of this ordination and towards the creation of more and more monotonous cultural landscapes. It is now obvious that this “neo- technological landscape degradation” is characterized by an increasing input

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Ecosphere

Natural and Semi- Natural Bio-Ecosystem

Agricultural and Seml- Agricultural

Bio-Ecosystem

Geosphere

0 u

Geosphere

Ecnsohere

Urban Industrial Techno - Ecosystem

Rural Techno

Ecosystem

Fig. 2. The ecosphere and its holons as concrete systems of the total human ecosystem. To the left of the Geosphere is the Biosphere, and to its right is the Technosphere.

of cultural information, fossil energy and man-made waste material from urban-industrial techno-ecosystems, together with the loss of natural and spontaneously occurring organisms and the natural negative feedback loops which ensure environmental stability and resilience (Holling, 1973). These are substituted by agro-technical, chemical and engineering feedbacks which are not a subordinate part of the hierarchy of homeostatic feedback controls of the biosphere and cause “side effects” of environmental pollution. At the same time, the vital role of the natural vegetation canopy in this homeostatic control which acts as a “living sponge” and ensures the closed loops of bio- geochemical cycles, is diminished more and more.

It has recently become apparent (Woodwell, 1978) that the large-scale reduction and harvesting of dense forests or their replacement by agricultural crops may have disastrous long-term effects on global stability by disturbing the carbon cycle. The contribution to the steady increase in atmospheric CO2 made by the reduction in forest cover is even greater than that made by industrial fuel burning.

We come to the conclusion that to ensure our survival and that of our techno-ecosystems, their visual and spatial integration in the landscape with biosphere and geosphere must be complemented by a functional and structural integration through change towards a new dynamic regime at a higher state of complexity. As Prigogine has shown for dissipative structures such as


I

( Semi-agricultural

\ landscape

\

- - Rural \ landscape

I I \

Urban-industrial landscape L - - - - - -L - -landscape Bio- where Techno- sphere

Built \ \ I landscape

Cultural 1

Modification-Conversion-Replacement of natural bio-ecosystems A Bio-physical information and control ACultural information and control 0 Natural organisms *Man- made artifacts G.olar energy NFOSSII fuel energy

Fig. 3. Ordination model of major landscape units as concrete systems of total human-ecosystem holons.

open ecological systems, this new dynamic flow equilibrium should not be considered as a stationary state but as a flow process. For its preservation in epigenesis and evolution Waddington (1970) has coined the term homeo- rhesis and Jantsch (1975) suggested its use also for the evolution of human systems, instead of the term “homeostasis” which may lead to the mistake of assuming that a stationary equilibrium of our “world model” can be reached.

By supplying regulative feedback in the decision-making process landscape ecology could play an important role by furthering the functional and structural integration of the concrete spatial entities of the human ecosystem holons at their most critical interphase with man, namely land use. Indeed, this should be the chief goal of landscape ecology as a human ecosystem science.

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111. PRACTICAL CONTRIBUTIONS OF LANDSCAPE ECOLOGY

A. Major Contributions in Central Europe

1. Landscape Ecology as Part of Landscape Care and Management

According to the Handbuch f i r Landschaftspfege und Naturschutz (Buchwald and Englehart, 1968), landscape ecology provides on the one hand, if protection of the organic world of plants and animals takes precedence, the scientific basis for nature conservation and, on the other hand, if the function of the landscape as a living space for man is to take precedence, the scientific basis for landscape care. Landscape care is considered together with nature conservation and arrangement of green areas as part of land care (Table 1).

The following definitions have been given (Woebse, 1975): Landespjlege, land care: to protect, care for and develop all the natural

life supports of man in residential, industrial, agricultural and recreational areas. It aims at a balance between the natural potential of the land and the demands of society.

Landschaftspjlege, landscape care: to protect, care for and develop landscapes for optimal sustained productivity by man. Management with this objective aims to prevent damage to nature’s system and landscape scenery and to repair damage already done. It requires that the historical, biological, ecological, social and economic factors which cause changes in the landscape, be investigated. Such investigations involve landscape analysis and diagnosis and an understanding of landscape construction and use with care (pfegliche Nutzung), of the natural resources in the open landscape.

Grinordnung, green arrangement: to safeguard the spatial and functional arrangement and coordination of all green areas and green plantings within the urban development which are essential for man’s spiritual and physical well-being. It is done on the basis of social, biological-ecological and economic considerations. It includes analysis and diagnosis of the contribution of green areas and their maintenance at city boundaries integrated with landscape care.

Nature conservation is carried out both in open and settled landscapes. It aims to safeguard landscapes and landscape units which are worthwhile for cultural, scientific, social and economic reasons and includes care for endangered animal and plant species and their habitats. It can be achieved through general landscape protection as well as through the establishment of protected areas.

Table 1 Land care and management (LandespJege).

Land care

Arrangement and planning of green Landscape care: land protection, areas planning and design; ecological landscape units and conservation

engineering (bio-engineering) Management

Nature conservation: protection of

Designing Maintenance

Built-up landscape Open landscape

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2. Ecological Design and Planning Woebse (1975) has made some important statements on ecological design which clearly illustrate the differences between the European landscape- ecological approach and the purely architectural aesthetic approach prevalent amongst landscape architects in the English-speaking world.

Amongst Europeans the following criteria are used for the evaluation of landscape quality:

( 1 ) The maintenance of natural functions, structure and ecological equilibrium. To do this the designer must be well-versed in natural sciences, understand ecological principles, the natural potentials of the landscape and the changes in the equilibrium which are induced by economic use.

(2) Site factors of climate and soil. (3) Geology and geomorphology. (4) The present shape of the land with vegetation and cultural artifacts.

Evolution must take into consideration dynamic changes occurring in the landscape and these contrast with the static endproduct of architectural design.

In recent years it has become increasingly apparent that the problems of landscape care and landscape planning and thereby also of landscape ecology, are closely interwoven with other inter-disciplinary aspects of regional and urban planning. In Germany, this has led to a broadening of the basic concepts.

The study group TRENT (1973) reviewed some hundred landscape plans carried out between 1967 and 1972 in West Germany. They stressed the need for revision of the foregoing criteria to ensure that landscape planning becomes closely integrated with regional planning:

Landscape planning must define in a more specific way its status between spatial planning (Raumordnung), and the contact-professional branches of planning, such as leisure-time planning, agricultural planning etc. It must abandon its defensive position in order to fulfil the requirements of dynamic development plans and to provide the foundation for the decision-making process in land use, to improve its methodology.

It was proposed to change the term Landschaftspflege into Landschafts- plannung, landscape planning, and to abandon the distinction between open landscapes and built-up green planning. One of the most far-reaching decisions was to regard ecological planning as the central tool of landscape planning. As such it should not be concerned directly with the “use with care of natural resources” (see above, because this is the aim of the specific professional disciplines, such as forestry, agronomy, water engineering etc., but it should judge the impact on “the natural foundation” (impact analysis). However, an optimal design cannot be achieved if impact analysis is limited


exclusively to material loadings. The scenic appearance (Erscheinungsbild) of the geofactors and their protection must be included in the analysis. In this way landscape design and nature and landscape protection are objectives of the overall plan.

3. Landscape Ecology, Planning and Management

In the past many landscape ecology studies have been carried out as integral parts of landscape planning projects, some on a large scale as for example in the Netherlands, Switzerland, Belgium, West Germany, Sweden and in various East European countries. These have been ordered by federal, regional or local authorities and carried out by special government agencies, universities or private landscape planners. A survey of these studies was published in the Proceedings of a German Society for Ecology meeting at Erlangen, in 1974.

Langer (1970) discussed the relationship between landscape care and landscape ecology and regarded the planning-oriented landscape ecology as both a scientific and practical part of landscape care and management which was involved in three problem areas: (1) to determine the functional aspects of the loading which anthropogenic influences place on the landscape and to define the need for special care of landscape components and ecosystems; (2) to determine the spatial aspects of landscape ecology assessment in regional planning requirements, and (3) to examine the methodological aspects of land-use planning and management in relation to landscape ecology. The Federal Institute for Nature Conservation and Landscape Ecology at Bad Godesberg, Bonn, has played a leading role in the introduction and formulation of landscape ecology principles and methods and their practical application in regional planning and development (Olshowy, 1972).

Olshowy (1975) has described in some detail the contribution of landscape planning related landscape ecology through inventories (analysis) and evaluations (diagnosis) of landscapes. Such inventories are carried out both on large scale maps, 1 : 200,000, and on more detailed, regional maps, 1 : 25,000, and include maps of natural vegetation and the distribution of wild flora and fauna, current agricultural, forestry and other land uses, protection areas, areas with extensive damage by soil erosion and local climate. The landscape diagnosis is intended for nature conservation, recreation, agriculture, forestry as well as for settlement, traffic and other land uses (Bauer, 1973; Dahmen, 1973; Olshowy, 1973).

One of the most relevant contributions is the preparation of maps of the potential natural vegetation of West Germany, which covered some 4000 km2 by 1970. They serve as valuable guides for regional and local planning for landscape development, agriculture, reforestation and revegetation, planning

214 ZEV NAVEH

of highways and waterways, mining operations etc. and are used to guide the selection of trees and shrubs (Trautmann, 1973; Olshowy, 1973).

At the same time, actual vegetation maps are widely used and, with other aids (e.g. remote sensing), have been applied in Scandinavia for multiple-use planning (Schiirholz et al., 1972). The interpretation of vegetation types through aerial photography has, as predicted by Troll (1939) offered a wide scope for an ecologically based land appraisal (e.g. Schneider, 1973). The use of aerial photography interpretation methods in landscape ecology studies and elsewhere has been discussed by Zonneveld (1972) (see also Whyte, 1976).

An important abstracting service in landscape ecology and related subjects is provided by the Federal Institute for Nature Conservation and Landscape Ecology through its Dokumentationen fur Umweltschutz und Land- schaftspjege. Established in 1950, i t had reviewed 13000 studies by 1972.

An important contribution to the development of landscape ecology as a scientific and practical discipline has been the establishment of special chairs of landscape ecology in universities. At the Technical University of Aachen the department is closely connected with the Faculty of Architecture. Its main achievements are in the field of landscape planning and design and in the education of regional planners. Amongst the many research and planning projects (reviewed by Pflug, 1973), one of special interest is the study of the city of Aachen and its natural supplying and compensatory regions. For this study, a system-analytical model was prepared which described the specific needs for natural resources of this industrial town of 160000 inhabitants, the flow of goods from and to the built-up area and the network of interdependence and influences of all natural factors in the surroundings.

The Institute for Landscape Ecology at the Technical University of Miinchen at Freising Weihenstephan, has closer links with agriculture and forestry and in addition to academic teaching, research and planning activities, much effort is devoted to formulate and apply multiple-use politics (Haber, 1971). This institute produced an outstanding example of a landscape ecology study in using hydrophytic plants and communities as bio-indicators of eutrophication and pollution of the Mosach river system. This served as a basis for practical recommendations for control and landscape reclamation measures (Haber and Kohler, 1972).

At the University of Miinster on the other hand, the chair for landscape ecology and “geo-ecology” is attached to the Institute of Geography, so keeping alive the tradition of the late G. Troll. In a memorial lecture Schreiber (1977a) stated: “The basic concept of the science, named landscape ecology by G. Troll, has remained the same, despite the present pre-occupation with environmental conservation. It consists in the exploration, within a given landscape, of the total environmental interaction patterns of all inter- dependent factors, including man”.


In this lecture, Schreiber stressed the “open plan” character of the landscape and the functional interconnection of different, sometimes widely distant ecosystems. He also suggested that the concepts underlying the techniques for the assessment and presentation of ecological structures are still in the early stages of development. He applied a geographical approach to defining ecological- spatial units in a landscape classification designed for use in planning (Table 2). Identification of the smallest workable units is determined by criteria of homogeneity within and between units. In general, ecological field methods used to map forests and agricultural resources, yield small ecological regions or ecotopes. These are sometimes confusing for the planner and Schreiber proposed to combine these into larger regions according to contiguity and similarity of the landscape. He did this (Schreiber et a!., 1976) in the ecological delineation of agricultural potentials within the framework of comprehensive agricultural planning for Baden-Wiirttenberg. However, he remarked that for hydrological purposes the catchment area and its watersheds “cut right across ecological unit patterns and landscapes, conceived in the geographical sense, and at times can connect parts of different landscapes with each other. In this context, the patterns of water flow have dictated a functional consideration instead of any other spatial linkage”.

At present, landscape planning is used chiefly as a tool for making decisions about the impact at landscape level of different land uses and the conflicts arising from these. In Schreiber’s opinion it should take into consideration the flow of resources, connecting individual areas and regions. However, even the most sophisticated, computerized methods of landscape analysis cannot overcome the main problem in landscape ecology, namely the lack of basic ecological data on the functional and structural features of bio-ecosystems and whole landscapes. This shortage of data exists for both the energy production aspects of ecology and the regulatory, compensatory “life support” and environmental-protection aspects. This information should be collected, stored, computed and modelled in such a way that it could provide more reliable answers on the most pressing questions about the present burdens on the landscape and predict its behaviour under future ones. Although many studies are carried out which use modelling and simulation methods to arrive at such predictions, especially on water quality, they lack this comprehensive landscape ecology approach and their translation into practical planning and decision making terms is very difficult. A striking example of the kind of basic information on flow of resources is the watershed ecosystem concept study by Bormann and Likens (1968) of the Hubbard Brook Experi- mental Forest in New Hampshire.

Schreiber (1977b) used the annual phenological development of the plant cover as a measure for the thermal scales and demarcations of climatic regions in Switzerland and was thereby able to delineate topoclimatic problem areas

Table 2 Order of work, results and aims of a classical ecological landscape classification (I, 11) and present utilization (111). As an aid in deciding on the utilization alternatives and to help resolve the conflict of aims within the framework of a complete ecological landscape plan (IV), there must be an evaluation of the ecological consequences of a particular use and also a spatial demarcation

of use (Schreiber, 1977).

I I1 I11 IV Classification of Demarcation of natural Evaluation of natural Evaluation of the ecoloeical

Order the natural of conditions work Landscape

ecological analysis

conditions

Landscape ecological synthesis

Y

potential utilization

Ecological re-modelling Problem-oriented ecological-

consequences of a particular form of utilization

effect analysis

Soil Water budget

Contents Vegetation and Micro-climate results Topography

etc.

Aims

Prognostication variable For: In relation to: Agricultural cultivation The ecological spatial unit

Hydrology (Hydrotop) eco- Forestry Related or inter-connected Vegetation (Phytotop) logical Melioration spatial units

Morphology (Morphotop) units Infrastructures demands etc. Storage of waste

Soils (Pedotop)

Climate (Klimntop)

etc. (Ecotop, Habitat, etc., with nearly Recreation identical conditions and identical etc. ecological potential.)

spatial Building Other uses or utilization

1

1 Association with ecological units Inclusion in specialized planning, Formation of functional spatial (Ecotop pattern) e.g.: units classified according to inter- Demarcation of natural spatial Utilization plan for agri- connection through the flow of units classified by internal cultural areas matter (catchments, smoke locational interaction, natural Utilization plan for forestry emissions, etc., including the spatial units and land- Regional agricultural planning extent of the effects)

character. etc. scapes of a certain (focal points of cultivation) 1

Inclusion in ecological landscape + planning


of which particular account must be taken in planning considerations. He also stressed the importance of biological indicators with integral characters to which quantitative expression can be given. He adopted a dynamic approach both to nature conservation, demanding active interference in order to conserve what seems most worthwhile from the ecological point of view (Schreiber, 1977c) and to the controversial problem of soziul Bruche, thousands of acres of derelict agricultural land lying fallow because to cultivate it is no longer profitable. More basic knowledge is required before deciding whether to leave this land until it reaches a final “climax” stage, to preserve it by simulation of previous agricultural and pastoral practices, as for example, in the Netherlands and the UK with certain types of grassland and heather, or to transform it by extensive afforestation or other means into a new recreational landscape. Therefore a series of long-term secondary succession studies is being carried out (Schreiber, 1976) in which the effect on vegetation and soil of all types of management practices, such as burning, grazing, killing weeds, mulching, cutting, etc. are carefully investigated.

Schreiber (1977a) summarized the most relevant contributions of landscape ecology to the field of planning and environmental protection as follows:

(1) Establishment of a new concept of a functionally oriented ecological landscape classification.

(2) Cooperation in experimental investigations into different aspects of ecosystem research, in order to obtain the basis for an ecological landscape classification, particularly for problem oriented ecological impact analyses of certain types of landscape uses.

(3) Cooperation in the development and application of simple and quick methods for the characterization of important parameters of landscape structure.

4. Ecological Methods for Landscape Evaluation

Kiemstedt’s (1967) method which provides a quantified measurement of the recreational suitability of landscape units, was a first and important step in replacing general and sometimes vague statements. In this method the close interconnection between the natural parameters and the human perceptual and cultural content of landscape values are realized. In the choice of parameters he took into consideration the following factors:

(1) With respect to man’s recreation: (a) their effectiveness as indicators of sensual and visual experience; (b) feasibility of utilization; (c) whether or not they might have a direct influence on man (e.g.

climatic effects). (2) With respect to practical application:

218 ZEV NAVEH

(a) how widespread the factors were; (b) how effectively they could be quantified so permitting simple

He combined all “recreationally effective” landscape factors and elements

(1) Forest border lines (in m km -2).

(2) Shorelines of lakes and rivers (in m km-*). (3) Relative differences between the highest and lowest point in the area as

(4) Types of land use in bordering areas such as fields, green areas, forests,

( 5 ) Bioclimatic regions. Multiplying each factor by a coefficient according to its relative importance,

he arrived at V the diversity value (Vielfiiltigkeit):

forest ecotone + water ecotone + relief + utilization 100 x climatic factor

statistical calculations.

into a formula based on the following scaling factors:

“relief energy” (in m).

bogs, heaths etc. (in percentages).

V =

This method has proved efficient and is now widely used. In a more recent large scale application in Sauerland, Kiemstedt (1975) modified the evaluation procedure:

(1) The manifold single criteria were grouped and presented in such a way that they could still be recognized in each step of the evaluation and checked.

(a) the larger areas of general suitability of the landscape; (b) the water ecotones; (c) the typification of each location.

(2) Three main evaluation areas were distinguished:

Kiemstedt (1971) has made a second important contribution to broadening the bio-ecological scope of ecological planning and so reducing the polarity between Naturplan and Kulturplan in the planning process. He introduced the concept of an evaluation matrix between the spatial demands of the user and a series of influencing natural factors. This was based on the assumption that the user will find the location best suited to his needs where it is least restricted by the constraints of natural factors and where it will cause least interference to other users. In this way, a differentiation can be made between those that cause the restricting effects on nature and those that are affected and this goes far beyond the term “landscape damage” which is laden with ideological misconceptions.

More recently, a “second generation” of this method has been applied by Bachfischer et al. (1977) as a quantified, ecological risk analysis in regional planning in Southern Germany. The method was developed to appraise the alternative effects of different land uses and to plan feasibility studies. In this


particular study, different conflict areas between the basic natural factors and the way in which the landscape was used were tested: soil/water, climate/air, biotopes/recreation. The intensity of potential restrictions were weighed against the different demands, using indicators. All single indicators were aggregated to show “intensity of potential restriction” versus “sensitivity to the restriction” and combined into a value expressing the risk connected with each specific restriction. As a detailed example and because of its decisive ecological importance, the conflict areas of groundwater were presented. Five degrees of risk intensity were used for mapping and on the basis of these three alternative regional development options in the urban conglomeration of Nurnberg were discussed.

Bechmann (1977) has reviewed these and other methods developed for combined landscape evaluation and land use approaches. In many respects they resemble the methodology of the “environmental impact” studies carried out in the USA and elsewhere (Welch, 1976). However, in contrast to most of the latter, the former were not initiated as particular responses to particular proposals for land or industrial development, but existed as important parts of the general planning and decision making machinery on federal, regional and local levels.

Krymanski (1971) discussed the “utilitarian” and integrated ecological, social, economic and cultural approach towards the open landscape and its implementation for planning and land management. He made comparisons between attitudes and approaches towards the landscape and methods for its planning in Germany and the English-speaking world.

5. Landscape Ecology Studies in the Netherlands

Van der Maarel and Stumpel (1974) presented an impressive picture of the wide application of an integrated ecological approach to planning in the Netherlands, where five out of the eleven provinces and many other official agencies require landscape ecological inventories in the making of which inter-disciplinary teams of biologists, geographers and pedologists were employed. By 1974, 60 different projects had been undertaken. In 1971 a working group for landscape ecology, the WLO, was founded with about 100 members to organize scientific meetings and issue a special bulletin.

The ecotope is used as the basic unit for soil and vegetation mapping and several ecotopes are combined into landscape units or geotopes. As in Germany, the basis for this work is formed by phytosociological surveys of natural, semi-natural and other vegetation types (see Section 1I.B). Zoological data are based on larger units. All phytosociological, pedological, geomorphological and landscape historical data are graded according to evaluation criteria or parameters and interpreted as to their final overall diversity value,

220 ZEV NAVEH

as in Kiemstedt’s system. The biotic parameters include criteria for variety and rarity of plant communities and ecotopes and for maturity or irreplace- bility. Relationships between diversity and stability are also considered. At the top of the scale of ecological components is the most natural region and at the bottom is the least natural region of the country. The recommendations for land use planning are based on interpretation of these values: land with the highest value, 5, is highly recommended for complete protection and optimal nature management. That with the lowest value, 1, is rarely considered as valuable for conservation and few restrictions are placed on it for utilization. In addition, special recommendations are given on specific land uses, such as for the building of roads and towns, agriculture etc. Indicator plants and communities are used for the evaluation of these changes. Recom- mendations for the development of highly modified systems towards semi- natural and close-to-natural systems are based on the ecological theory of Van Leeuwen (1966, 1973). Advanced integrated evaluation methods are also applied in the Netherlands for outdoor recreation planning, especially in forests close to urban areas (Bijkerk, 1975).

Amongst the many projects carried out, the integrated Kromme Rijn project (Tjallingli, 1974), which was initiated by student groups from the University of Utrecht and the Department of Geography is particularly worthy of mention. It is an outstanding example of using landscape ecology both for actual regional planning and for multidisciplinary environmental education, to which I refer in more detail in the following section.

6. Landscape Ecology and Landscape Reclamation

The term landscape care implies active development and management; landscape ecology provides the scientific basis for landscape care. Ecological management, development and reclamation are directly concerned not only with a specific economic use of natural resources, although this may be one of the final reclamation aims, but also with those open, disturbed or destroyed landscapes which should be managed and/or reconstructed for maximum overall ecological benefit.

In addition to the ecological management of existing vegetation in nature reserves and parks, this includes the management and reconstitution of rights- of-way and highway embankments, shorelines of lakes, rivers and other waterways, quarries and mines, protective plantings against wind and water erosion and avalanches, and against environmental pollution. The major technology developed by landscape ecologists such as trained foresters, garden-architects, agronomists and engineers, is living construction (Lebens- bau or Lebendverbau), or green construction (Grunverbau) and “engineering biology” or “vegetation engineering”.


These achievements have been surveyed by Woebse (1975) and reviewed by Bittman (1968) and Schluter (1971). The techniques particularly applicable for coal mining reclamations have been reviewed by Darmer (1972) and those for protection measures in the landscape by Schiechtl (1973). The latter, working in the Austrian alpine region, demonstrated the potentials of combining biological-ecological principles and biotechniques with advanced highway engineering methods in the protective and scenic “regreening” of the Brenner Pass highway. He applied his patented Schiechtl mixtures of seed and mulching material by hydroseeding methods. The development of these methods, widely used in landscape reconstruction projects and promoted by the German Federal Institute for Highway Construction, has been reviewed by Strunk (1972). In contrast to similar methods used in the US with agronomic pasture and turfgrass mixtures, as well as with ornamental plantings along highways, the landscape construction and reclamation work in Central Europe is mainly concerned with the reconstruction of the actual and potential natural vegetation and with ecological and not purely archi- tectual and functional landscape design. This applies not only to natural parks and reserves, but also to cultural landscapes. Thus, when travelling on the major German highways from east to west and north to south one can study a transect through the major forest formations by observing the verges on either side.

Darmer (1974) broadened the bio-ecological aims of landscape reclamation from phytosociological considerations to the reconstruction of a diversified biotope. In this, the re-establishment of plants creates sheltered habitats and refuge sites for animals. Pioneer plants for recultivation are chosen according to their “degree of biocenotic efficiency” and bearing in mind the ultimate use of the reclaimed site: either for nature conservation, recreation or multiple functions. The chief aim, however, is to ensure the highest biotic diversity.

To illustrate this, Darmer used the reclamation of coal spoil heaps in the Rhine-Ruhr region, one of the largest and most successful landscape reclamation projects carried out since 1951 within the framework of the regional planning project of the Ruhr (Olshowy, 1973). The same principles were applied to the reclamation of the close-to-natural biotopes on the re- alignment of the Elbe Canal near Berlin and the artificial lake created there (Jacob, 1972).

A further impressive example of large scale ecological and scenic integration and of a successful compromise between the demands of landscape and of technology, has been the reclamation carried out following the re-alignment of the river Mosel, as part of the Rhine-Rh6ne Canal, to make it navigable to bigger ships. Dams were built and the narrow, winding riverbed was broadened. The Mosel is considered the most scenic river in Germany and great care was taken in construction, reclamation and earthwork to cause

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as little damage as possible. This was achieved with the help of comprehensive landscape development plans (Pflug and Bittman, personal communication) which contained detailed instructions for engineering constructions and build- ings, for the biological reclamation of disturbed slopes, the disposal of earthwork and for the protection of the shoreline from the heavier waves by planting the more resilient hydrophytic Carex species.

In Germany, as described by Mathe (1973), much attention has been paid to protective plantings along roads and in urban-industrial regions and to their protective beneficial functions in the reduction of noise, dust and air pollution. His own work is concerned with the role of trees in this respect. He emphasized the importance of the use of bio-indicators, either as sensitive plants or as accumulators of dust, fluoride or heavy metals. Probably the most significant contribution to the development of quantitative, biological monitoring systems, which supplement chemical-physical measurements made in the Rhine-Ruhr region, has been made by the Landesanstaltfir Immissionschutz des Landes Nordrhein- Westfalen in Essen (Scholl and Schon- beck, 1973; Schonbeck and Von Haut, 1973; Prinz and Scholl, 1975).

In recent years, foresters have also emphasized that forests have a role to play in protecting the environment in densely populated regions, as well as to produce timber (Briinig, 1972). The findings of Knabe (1973), that a forested strip, 2 to 3 km wide, could reduce the average SO2 concentration in the industrial Rhine-Ruhr region from 0-2&0*11 mg m-3, are of special interest.

Important work is also carried out in landscape ecology, planning and development and in what Vanicek (1 977) has called “eco-engineering” in Czechoslovakia. This has been extensively reviewed by Vanicek and Hrabel (1974).

B. Landscape Ecological Studies in Israel

1. Arthur Glickson, the “Father” of Landscape Ecology in Israel

Glickson was a farsighted and ecology-minded architect, whose vision of ecological planning and design was one in which “the landscape should be useful and beautiful at the same time; a resource of life and its renewal”. He was most influential in formulating principles of comprehensive ecological and regional landscape planning (Glickson, 1964, 1966) and his views on comprehensive multiple-use recreational planning were expressed as early as 1956 (Thomas, 1956). He was the first to use “environmental quality” in defining objectives in land use planning and management and was the first to state the need for ecological integration of the open and built-up landscapes and their ecosystems. This he considered was the greatest challenge for the regional planner: “There is no place for a separate ecology of the rural


or urban environment. No viable urban development can take place if not on the basis of its surrounding, regional life-sustaining landscapes”. He considered that a similar integration was needed in the reconstruction of the landscape, for which he used the term “geotechnics”, first conceived in Scot- land by Patrick Geddes.

In the reconstruction of landscape, cooperation between town and country and among professions would recreate a fertile and habitable environment. It would be the greatest enterprise of planned environmental change since neolithic times and the best act of social creation we can imagine. With the help of science, man reconstructs nature in its own image, which is at the same time his own best image (Glickson, 1956).

2. The Degradation of Mediterranean Landscapes

The process of man-induced desiccation of the Meditteranean landscape in Israel has been described by Naveh and Dan (1973) as seven degradation and aggradation cycles of anthropogenic biofunctions. These correspond to seven main phrases of landscape modification and land use. They commence with the use of fire by Pleistocene hunters and gatherers and continue with increasing intensity at the present time. As in Europe, but for a much longer period and with much greater intensity, the primeval landscape, its forests, woodlands and semi-arid steppe grasslands have been converted into a semi-natural landscape, with a dynamic, multi-layered and rich vegetation, containing mosaics of regeneration and degeneration phases, as described by Walter (1968) for the Mediterranean Basin as a whole.

One of the main conclusions to be drawn from the study of the mountainous region of Israel is that during the long phase of agricultural decay and population decline, a new equilibrium has been established in the non- cultivated upland ecosystems which are neither overgrazed nor heavily coppiced, nor yet completely protected. This man-maintained equilibrium between trees, shrubs, herbs, grasses and flowering geophytes has contributed much to the biological diversity, stability and attractiveness of the Mediter- ranean landscape. It is without doubt a most important asset for recreation and tourism. However, it is now endangered not only by the population explosion and increasing intensity of traditional land use, but also by the accelerated speed of urban sprawl and neo-technological despoilation, pollution and erosion.

If the recent trends of landscape degradation proceed unhindered and with their present speed and intensity, the few open unspoiled landscapes that are left will be turned into overcrowded recreational slums. This condition has already been reached on the shores of the Mediterranean Sea and inland waters, areas which rank highest in outdoor-recreation demand.

A special challenge faces landscape ecologists in developing countries,

224 ZEV NAVEH

including Israel and others in the Mediterranean Basis (Naveh, 1978a). In such regions most efforts are directed towards the development of the most productive agricultural areas, where the ratio between investment in research and resources and expected economic benefits seems most favourable. On the other hand, the less fertile and marginal lands, which comprise more than 50% of the total land surface of most countries in the Mediterranean, are not developed. They are used mainly for grazing and are encroached upon by uncontrolled urban and recreational developments.

Landscape ecologists should focus their attention on this marginal and untillable land and find practical ways of reconciling the need for conservation and reconstitution of the open landscape, its biotic resources, the socio-economic needs of its inhabitants and the national economy. Trans- formation of the intangible, ecological, scenic and recreational “non-economic riches” into workable quantitative parameters, based on integrated ecological studies is no less urgent in these regions than in the developed, industrial countries.

3. Ecological Management of Untillable Uplands

Investigations have been made along a climatic and anthropogenic gradient in the maquis belt of the problems of conservation and management of nature reserves and parks and the effect of anthropogenic interference (fire, cutting, grazing) on biotic diversity (Naveh, 1971; Naveh et al., 1976; Naveh, 1977a). In a more recent study these results have been compared with other Mediterranean landscapes in which similar trends are apparent (Naveh and Whittaker, 1979). Figure 4 shows that high structural, floristic and animal diversity can only be maintained by ensuring the specific defoliation pressure, through burning, grazing, coppicing, cutting etc. under which the communities evolved. The process of structural, floristic and faunistic impoverishment which leads to stagnation, high inflammability and therefore instability, runs contrary to classical climax-succession theories according to which “the well- developed maquis is removed by human intervention from its final successional and relatively stable climax stage” (Zohary, 1962). It was concluded that rather than just passive protection, active scientific ecological management was required to simulate these optimum defoliation pressures and so conserve abundance in plant and animal species and structural richness.

For the management and improvement of degraded Mediterranean uplands, outside of nature reserves, a closely interwoven network of multiple land uses was suggested (Naveh, 1974; 1978b). This was based on dynamic vegetation management by manipulation of the soil-plant-animal complex (Naveh and Ron, 1966) and on the results of multi-purpose environmental landscaping and afforestation trials in typical, degraded and rocky, untillable

N

ME MU FO

Annual Farbs Annual Legumes

Annual Grasses

Perennial Herbs

Woody Vegetation

N SlCExpH

00

Closed Moqui Semi-open Maqui

G I BT

Shrub Grassland Open Woodland

Fig. 4. Structural and floristic diversity of mediterranean shrub and woodland as affected by protection, as opposed to disturbance and grazing (Naveh, 1977a). Note that protected ME and MU has chiefly woody vegetation, but lowest diversity; disturbed FO and BO has also chiefly woody vegetation but much higher diversity; disturbed GI with shrub-grass has high diversity, but heavily disturbed BT low diversity; moderately grazed AL and AA with chiefly herbaceous vegetation have the highest diversity.

226 ZEV NAVEH

0

6 0 -,

0 0

5 Very high 4 High 3 Medium 2 LOW

I Very low

land-uses environ- mentol functions

I Environmental woler- shed protectim

2 Fire hozord resis10nCe

3 Biotic diversity

4 Recreol\on amenity 5 Llveslo€h production 6 Forestry protection 7 Water yields

from oquifer

wild life

I Monogement types]

4 Protection Misuse

Multipurpose euxystern + monogement 4 Multipurpose envimnmentol

offorestotion -C+ Pine offorestotion

Fig. 5. Management flow diagram of Mediterranean upland ecosystems (Naveh, 1978b).

hill land in Northern Israel. Intensive treatment is essential for revegetation of denuded slopes and for fire protection and buffer zones.

Alternative management strategies (Fig. 5 ) would convert the presently misused, low value uplands (a), into existing alternatives of protected, im- penetrable and monotonous maquis and forest reserves (b), into dense, chiefly mono-culture pine forests (c), into the new options mentioned above, as recreation forests and woodlands (dl), multiple use forests, woodlands and shrublands (d2) or fodder shrublands, woodlands and grasslands (d3), or into semi-natural, multi-layered forests, parks and woodlands with suitable indigenous and exotic drought and limestone tolerant trees and shrubs, used chiefly for recreation (e,) for pasture (e3) or as flexible multi-purpose systems


Fig. 6. A cybernetic interaction model of land use factors (Naveh, 1978b). A Environ- mental and watershed protection. B Fire hazard resistance. C Biotic diversity and wildlife. D Recreation amenity. E Livestock production. F Forestry production. G. Water yields from aquifer. AS Active sum. PS Passive sum. Q Quotient AS : PS. 0 No influence. 1 Slight influence. 2 Medium influence. 3 Strong influence. Active element: Highest Q : F (F). Passive element: Lowest Q : G (D).

(ez). The highest overall multiple benefits can be expected from the latter. They include environmental and watershed protection, resistance to fire hazard, biotic diversity, recreation amenity and plant and animal production. As a tool for evaluating the degree to which all factors influence each other, a cybernetic interaction matrix can be constructed (Fig. 6) (Vester, 1976). This permits a more accurate determination of the most active and critical variables that have the greatest effect on all other variables, in this example forest and to a lesser degree livestock production and recreation, and the most passive variables, which change greatly under the slightest influence of all other variables, in this case water yields. At our present stage of knowledge, management strategies aiming at multi-purpose options dz and ez are preferable. However, these results should be considered as a first approximation and a major task is to express these relative values by actual quantitative data, which would permit optimization in planning and actual implementation of multiple-use strategies. For this purpose, combined research and demonstration teams of foresters, livestock and wildlife specialists and landscape ecologists and planners would be most desirable.

228 ZEV NAVEH

Special attention has been devoted to the role of fire in Mediterranean landscapes, both from the ecological (Naveh, 1973b; 1975b; 1977c) and from the planning and landscape management points of view (Derman and Naveh, 1977).

The model for multi-purpose land use in the dry maquis described above has considerable benefits for fire protection. There is a very real conflict between the pastoralists, burning shrub and woodland to increase the sparse pasture understorey and the foresters who try, in vain, to protect nearby, highly inflammable and valuable pine forests. Its representation to Mediter- ranean foresters (Naveh, 1977b) contributed to the formulation of new, multiple use strategies in which fire and fuel management are combined with grazing and thinning of maquis for recreation.

4. Landscape Ecology Studies in Intensively Used Landscapes

The ecological restoration of cultural Mediterranean landscapes degraded or destroyed by neo-technology has been attempted with the help of drought resistant and low-maintenance plants (Naveh, 1975a). Both local and exotic hardy herbaceous and woody species were selected for the reclamation and revegetation of slopes, highway embankments and limestone quarries. These are established as mixtures of fast-growing and soil-protecting, low cover “pioneer” plants, and slower growing, but taller and more persistent, soil ameliorating shrubs and trees. A condensed successional process is achieved by “vegetation engineering”, hydroseeding and afforestation methods. Pro- mising results of these studies and reclamation projects point to the great scope of woody plants from local origin, as well as from the Western Mediterranean, Australia, South Africa, South America and California for biological, scenic and economic enrichment of degraded Mediterranean landscapes.

IV. LANDSCAPE ECOLOGY AND ENVIRONMENTAL EDUCATION

As an holistic, task-solving oriented science, landscape ecology is especially suitable for fulfilling an important educational function. With its trans- disciplinary and multidimensional outlook it can help to break down the thick walls surrounding the ivory towers of three cultures in which plant and animal ecologist-biologist, the environmental engineer-technologist and the socio- logist and economist-humanist are still functioning. The intention is not only to teach landscape ecology as an academic discipline in universities, but as a major content in environmental and conservation education of middle and


higher school education. Promising beginnings in this direction have been made in Israel (Shachak et al., 1975) and were reported in more detail in a special symposium on environmental education at the Second International Congress of Ecology held in Jerusalem, 1978 (Bakshi and Naveh, 1980).

V. SUMMARY AND CONCLUSIONS

This paper, firstly, reviews the development of landscape ecology in Central Europe, secondly offers a revision of its principles and concepts in the light of recent insights in general systems theory and human ecology, and thirdly presents some of its contributions as an emerging, inter-disciplinary ecosystem science.

Landscape ecology has its roots in Central and Eastern Europe, where biogeographers have viewed the landscape not just as an aesthetic asset or as part of the physical environment, but as the total spatial and visual entity of human living space, integrating the geosphere with the biosphere and the noospheric man-made artifacts.

This holistic viewpoint of the landscape has been adopted by ecologists well versed in vegetation science, or trained originally as agronomists, foresters, gardeners or planners who abandoned the sometimes narrow restrictions of their respective professions outlooks for a modified phytosociological methodology of integrated field surveys and ecosystem studies.

The development of landscape ecology in the Netherlands, where it has had its greatest influence on actual large-scale regional planning, was inspired by achievements in nature conservation management, landscape planning and reclamation on the one hand and by cybernetic theories of pattern and process in vegetation on the other. By bridging the communication gap between the English and German languages, Dutch vegetation ecologists have broadened both the scope of quantitative phytosociology and landscape ecology.

Currently, landscape ecology in Europe is viewed as the scientific basis of land and landscape planning, management, conservation, development and reclamation, and as such it has overstepped the realm of classical bio- ecological sciences and entered the realm of man-centred fields of knowledge, the socio-psychological, economic, geographical and cultural sciences in as far as they are connected with modern land uses.

This is reflected in the broad range of landscape ecology and landscape planning oriented studies of the complex interrelationships between modern man and his open, cultural and built-up landscapes. These aim at a compromise between conflicting natural, cultural and socio-economic demands and, at the same time, at an enrichment of man’s biotic environment.

230 ZEV NAVEH

An attempt has been made to outline the major principles of a general biosystems theory. A central feature is the recognition of the total human ecosystem as the highest level of integration, with the ecosphere as the largest, concrete, global landscape entity and the ecotope as the smallest. The visual and spatial integration of the bio-, techno- and geospheres must be complemented by their functional and structural integration through the creation of a new equilibrium at a higher level of organization and complexity.

Landscape ecology is contributing to this goal by supplying scientific, ecological and educational information. Its foremost future tasks are three- fold:

(1) To increase the number of integrated, multidisciplinary, long-term ecosystem studies of man’s land uses and their impacts.

(2) To replace degraded and destroyed natural bio-ecosystems by new semi- natural, attractive, diverse and stable bio-ecosystems.

(3) To achieve recognition of the important role of landscape ecology in the process of cultural evolution and noogenesis, as a basis for interdisciplinary, task-oriented, environmental education.

ACKNOWLEDGEMENTS

I acknowledge with gratitude the efforts spent on critically reviewing and editing this article by the editors and Mrs M. Cannell.

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Author Index

A Abbott, I., 153, 174, 182, 184 Abbott, L. K., 182, 184 Aberg, B., 99, 114 Adams, M. S., 105, 107, 110, 114, 123 Alizai, S. A. K., 90, 114 Allen, E. D., 47,54,74,75,76,83,87,105,

Altman, E., 234 Anderson, E. R., 59, 115 Aplin, R. T., 2, 6, 7, 34 Arber, A., 72, 90, 11 5 Arisz, W. H., 87, 115 Arthur, L. M., 190, 230 Arthur, W., 132, 134, 149, 177, 179, 180,

Ashby, W. R., 200, 230 Auglig, G., 230 Ayala, F. J., 132, 149, 165, 166, 167, 182

B

106, 109, 114, 122

182

Babloyantz, A,, 234 Bachfischer, R., 218, 230 Bakker, K., 147, 182 Bakshi, 229 Balon, E. K., 55 , 115 Baranowski, A., 86, 119 Barclay, A. M., 122 Barker, J. S. F., 165, 167, 182 Barnard, C. J., 162, 183 Barsdale, R. J., 87, 119 Bauer, G., 213, 230 Bauer, H. J., 200, 230 Bechmann, A., 219, 230 Benn, M. H., 34 Benthem, R. J., 196, 230 Berger, F., 52, 115 Bernatowicz, S., 80, 84, 115 Bertalanffy, L. von, 198, 231 Best, M. D., 87, 88, 89, 115 Bharucha, F. R., 40, 92, 117

Bierter, W., 198, 231 Bijkerk, C., 220, 231 Bindloss, M., 55, 115 Bisset, G. W., 7, 34 Bittman, E., 221, 222, 231 Black, 64 Boag, P. T., 147, 152, 174, 183 Boatman, D. J., 90, 117 Bodin, K., 46, 100, 115 Bodkin, P. C., 53, 54, 57, 77, 79, 98, 100,

Bormann, F. H., 215, 231 Bornemissza, G. F., 4, 5, 8, 9, 10, 1 1, 13,

14, 18, 34 Boster, R. S., 230 Bourne, W. S., 86, 115 Bowes, G., 123 Boycott, A. E., 180, 183 Boye-Petersen, J., 41, 47, 115, 121 Boylen, C. W., 46, 75, 77, 121 Brammer, E. S., 115 Brand, F., 46, 115 Bretschneider, C. L., 64, 69, 115 Bristowe, J. M., 87, 115 Britton, R. H., 118 Brown, C. L., 40, 118 Brown, J. H., 163, 183 Brown, J. M. A., 115, 122 Brown, W. L., 129, 130, 131, 151, 183 Browse, J. A., 65, 115 Brunig, E. F., 222, 231 Brush, R. O., 237 Bucher, G. E., 14, 34 Buchner, H. K., 198, 231 Buchwald, K., 192, 210, 231 Bulmer, M. G., 136, 141, 142, 183 Burmil, S., 234 Buttery, B. R., 116

103, 109, 111, 112, 115, 122

C Cain, A. J., 179, 183

240 AUTHOR INDEX

Cairns, D., 5 , 6, 36 Cameron, E., 4, 5 , 11, 13, 14, 34 Cameron, R. A. D., 187 Campbell, B. J. , 3,8, 10, 18, 19,20,28,36 Campbell, R. M., 87, 116, 122 Carignan, R., 87, 89, 116 Carter, M. A., 187 Caswell, H. W., 200, 231 Chambers, P., 52 Chapman, V. J . , 122 Chardin, P. Teilhard de, 191, 202, 231 Christiansen, F. B., 136, 144, 184 Christmann, R. F., 51, 116 Chrystal, J., 101, 102, 122 Clapham, C. T., 98, 99, 116 Clark, A,, 176, 177, 183 Clarke, B.. 128, 134, 135, 141, 146, 168,

175, 183, 184 Clowes, F. A. L., 87, 116 Cockbill, G. F., 36 Cody,M. L., 129, 131, 162, 163, 183, 187 Collins, P. M., 147, 183 Cook, L. M., 132, 183 Coons, L. W., 184 Cordone, A. J., 46, 117 Corillion, R., 100, 116 Crampton, H. E., 147, 184 Crawford, R. M. M.. 72, 116, 118 Crowder, A. A., 88, 116 Crozier, R. H., 136, 140, 141, 143, 145,

Currie, G. A., 10, 34 Curtis, J . T., 38, 116

183

D Dahmen, F. W., 213, 231 Dale, H. M., 60, 65, 84, 95, 100, 116, 122 Dale, M. B., 200, 231 Dan, J., 223, 234 Daniel, T. C., 230 Dansereau, P., 190, 191, 192, 198, 231 Darmer, G., 221, 231 Darwin, C., 130, 183 Daviault, L., 11, 34 David, J., 230 Dawson, P. S., 168, 173. 183 Dayton, P. K., 107, 116 De Marte, J . A., 87, 116 Dempster, J . P., 2, 3, 4, 5 , 6, 7, 8, 9. 10,

11, 13, 14, 15, 16, 17, 21, 22, 23, 24,

25, 27, 29, 30, 31, 32, 33, 34, 35, Denny, P., 42, 86, 87, 116. 123 Derman, A., 228, 231 Dillon, P. J . , 110, 116 Dokulil, M., 50, 5 5 , 58. 116 Downes, J. A,, 36 Drew, E. A., 76, 116 Dromgoole, F. I., 115 Dunham, A. E., 160, 183 Dykyjova, D., 71, 116

E Edmonson, W. T., 95, 116 Egan, M. E., 184 Eggeling, W. J.. 38, 40, 117 Egler, F. E., 198, 199, 203, 204, 207, 231 Einevoli, O., 235 Eldredge, N., 154, 155, 183 Ellenberg, H., 193, 194, 195, 199, 204.

205, 231, 232, 233 Eminson, D.. 120 Englehart, W., 210, 231

F Fabos, J . G., 237 Falconer, D. S . , 147, 184 Fassett, N. C., 46, 11 7 Fegers, R., 200, 230 Feinberg, E. H., 186 Fenchel, T., 136. 144, 148. 155, 156, 157,

Ferling, E., 77, 117 Focker-Hanke, G., 193. 232 Forbes, G. S.. 147, 184 Forbes, J. C., 5, 34 Forsberg, C., 98, 100. 117 Frantz, T. C., 46, 117 Fraser. J., 122 Frazer, J. F. D., 7, 34, 35 Frick, K. E., 4, 35 Fuchsig, H.. 46, 117 Futuyma, D. J. . 165, 184 Fyfe, R. V., 10, 34

158. 160, 184

G Geddes, P.. 223 Gessner, F., 38, 76. 77, 87. 117 Ghassemi, M., 51, 116 Ghent, A. W., 35 Gibbs, M. E., 36

AUTHOR INDEX 24 I

Gil, C. J., 40, 117 Gill, D. E., 165, 184 Gillespie, J. J., 60, 65, 116 Glickson, A,, 222, 223, 232 Glidewell, S. M., 120 Goche. A. G., 55, I15 Godfrey, R. K., 38, 72, 117 Godwin, H., 40, 92, 117 Golubic, S., 46, 77, I17 Gosling, E., 134, 177, 180, 18 1, 184 Gotch, K., 168, 186 Could. S. J.. 159, 186 Goulder, R., 90, 117 Gradwell, G. R., 25, 36 Grant, B. R., 184 Grant, P. R., 130, 131, 146, 147, 151. 152,

Grant, V., 130, 184 Green, C., I19 Green, W. Q., 20, 35 Grime, J. P., 106, 107, 108, 117 Grubb, P. J.. 107, 117

162, 163, 174, 182. 183, 184, 187

H Haber, W., 214, 232 Hairston, N. G., 168, 169, 184 Hall, K. J., 51. 117 Haller. W. T., 123 Harper, J. L.. 4, 5, 35, 168, 184 Harris, P., 6, 9, 1 I , 14, 30, 33, 34, 35, 36 Hartman, R. T., 87, 116 Haslarn. S. M., 71, 96, 97, 98, 117 Hasler. A. D., 46, 118 Hassenstein, B., 198, 232 Haut. H. von, 222, 235 Hawkes, R. B., 4, 9, 1 1 , 14, 35 Hayes, J. T., 186 Heath, 0. V. S., 1 1 8 Hedrick, P. W., 165, 167, 184 Hejny, S., 38, 118 Hemmings, C. C., 51, 118 Hesjedal, O., 235 Heywood. R. B., 46, 119 Ho, F. K., 168, 185 Hoenigsberg, H. F., 165. 184 Holling, C. S., 208, 232 Holloway, J. K., 4, 35 Hood, D. D., 72, I18 Hook, D. D., 38, 40, 118 Hope, A. B., 87, I18

Hrabel, A,, 222, 236 Huey, R. B., 154, 184, 186 Hunt, R., 106, 117 Husak, s., 38, 118 Hutchinson, G. E., 38, 39, 51, 60,61, 77,

100, 108, 118 Hutchinson, J. N., 119

I Irnahori, K., 99, 122 Isaacson. D. L., 5, 9, 1 I , 30, 31, 35, 36

J Jacob, H., 221, 232 Jantsch, E., 201, 202, 204, 206, 207, 209,

Jennings, J. N., 119 Jerlov, N. G., 50, 51, 118 Jeschke, W. D., 87, I18 Jinks, J. L., 147, 185 Jones, J. S., 184 Juday, C., 46, 118 Juniper, B. E., 87, 116 Jupp, B. P., 47, 76, 84, 85, 88, 95, 105,

109, 116, 1 I8

K Kahn, T. M., 234 Kalff, J., 87, 89, 116 Kalle, K., 51, 118 Karling, J. S., 99, 118 Kaukal, A,, 87, 11 7 Keeney, D. R., 87, 89, 119 Kellogg, D. E., 155, 184 Kiemstedt. H., 217, 218, 220, 230, 232 King, M. R., 116 Kingston, P., 181, 184 Kirk, J. T. 0.. 51, 52, 57, 118 Klaus, G., 200, 232 Knabe, W., 222, 232 Knotig, H., 198, 232 Kodric-Brown, A., 163, 183 Koestler, A., 198, 232 Kohler, A., 214, 232 Koning, H. E., 231 Krymanski, R., 219, 232 Kvit, J., 71, 116

L Lack, D., 152, 153, 184 Laing, H. E., 72, 119

232

242 AUTHOR INDEX

Lakhani, K. H., 5 ,6 ,9 , 13, 15, 24, 25, 27,

Lambert, J. M., 71, 116, 119 Langer, H., 192, 193, 200, 213, 232 Lanyon, W. E., 163, 184 Larsson, J., 235 Lawlor, R., 128, 131, 136, 138, 142, 143,

Lazlo, E., 207, 232 Lee, G. E., 51, 117 Leeuwen, G. G. van, 196, 200, 220, 233 Leon, J. A,, 136, 137, 139, 140, 185 Leonard, N. J., 6, 35 Lerner, I. M., 167, 185 Leslie, P. H., 186 Levin, B. R., 136, 138, 139, 140, 142. 163,

167, 185, 187 Levin, D. A,, 130, 185 Levins, R., 131, 136, 137, 138, 141, 142,

Lewontin, R. C., 128, 185 Light, J. J., 46, 119 Likens, G., 215, 231 Lind, E. H., 38, 40, 119 Lister, B. C., 154, 173, 185 Lloyd, M., 18, 35, 168, 186 Lohammar, G., 109, 119 Lorenz, K., 198, 200, 204, 233 Lund, J. W. G., 46, 47

30, 31, 34, 35

162, 163, 185

162, 165, 173, 185, 186

M Maarel, E. vande, 196,197,219,233,236 Macan, T. T., 43, 119 MacArthur, R. H., 131, 136, 137, 138,

Mackereth, F. J. H., 95, 119 Macko, D., 233 Mann, A., 234 Mantai, K. E., 86, 87, 89, 115 Maristo, L., 78, 119 Marsh, G. A., 14, 36 Martin, C. O., 159, 185 Masry, A. M., 187 Mathe, P., 222, 233 Mather, K., 147, 185 Maynard Smith, J., 128, 131, 136, 138,

Mayr, E., 130, 185 McCracken, M. D., 110, 114 McEachran, J. D.. 159, 185

141, 142, 162, 173, 185

142, 143, 162, 163, 185, 186

McManus, J., 90, I14 McMurtie, R. E., 154, 185 McRoy, C. P., 87. 119 Meijden, E. van der, 2, 3, 4, 5, 9, 10, 15,

Mertz, D. B., 186 Mesarovic, M. D., 198, 233 Milburn, T. R., 122 Miller, D., 8, 11, 35 Miller, G. E., 95, 116 Miller, J. G., 199, 233 Misra, R. D., 86, 119 Moeller, R. E., 75, 99, 110, 119 Moerzer Bruyns M. F., 196, 233 Monkemeyer, W., 46, 119 Monod, J.. 201, 233 Monteith, J. L., 61, 119 Moore, J . A,, 129, 163, 164, 185 Morista, M., 19, 35 Morrison, M. E. S., 38, 40, 119 Mortimer, C. H., 65, 119 Moss, B., 120 Mourad, A. M., 187 Moyle, J. B., 86, 119 Mueller-Dombois, D., 194, 233 Muggleton, J., 132, 185 Muller, C. H.. 144, 185 Mulligan, H. F., 86, 119 Muntz, W. R. A,, 51, 119 Murdoch, W. W., 168, 185 Murphy, P. G., 134. 177, 178, 185 Murray, J. J., 75, 119. 130, 179, 185, 186 Myers, J. H.,3,8,10. 18, 19,20,28,29,31,

17, 18, 20, 21, 23, 32, 35

36

N Nauwerck, A., 46, 100, 1 1 5 Naveh, Z., 206, 223, 224, 228, 229. 231,

Ndawula-Ssenyimba, M., 122 Neary, M. E., 35, 36 Nichols, D. S., 87, 89, 119 Nicolis, G., 201, 234

0

233, 234

O’Donald, P., 134, 183 Odum, E. P., 128, 129, 186 Odum, H. T., 199, 234 Oldham, C., 180, 186 Olshowy, G., 213, 214, 221, 234

AUTHOR INDEX 243

P Park, T., 149, 167, 168, 186 Patten, B. C., 200, 234 Pearsall, W. H., 42,43, 44,47, 73,90, 91,

Peltier, W. H., 86, 120 Pennington, W., 95, 120 Pflug, W., 214, 222, 234 Philips, G. L., 95, 109, 120 Philogene, B. J. R., 4, 36 Pianka, E. R., 148, 154, 184, 186 Pickard, W. F., 89, 120 Pigott, C. D., 94, 120 Pimentel,D., 129, 133, 140, 169, 170, 171,

Pond, R. H., 86, 120 Poole, A. L., 5 , 6, 36 Powell, J . R., 134, 175, 176, 186 Prigogine, I., 201, 204, 208, 234 Prinz, B., 222, 234 Pullar, L., 75, 119

Quennerstedt, N., 39, 121

Rackham, O., 65, 120 Rash, J. A., 231 Raspopov, 1. M., 110, 120 Raunkiaer. C., 120 Raven, J. A., 87, 89, 106, 107, 120 Rees, T. ap, 72, 121 Rethy, R., 99, 120 Rich, P. H., 98, 110, 120 Richards, L. J., 29, 36 Rigler, F. H., 110, 116 Roberts, E., 122 Rohwer, S. A., 163, 186 Roll, H., 86, 120 Ron, B., 224, 234 Rose, S. D., 2, 3, 15, 21, 36 Rosenfels, R. S., 87, 120 Ross, Q. E., 231 Rothschild, M., 2, 6, 7, 8, 34, 35, 36 Rothstein, S. I., 174, 186 Roughgarden, J., 136, 143, 144, 173, 186 Round, F. E., 95, 120 Rowe, J. S., 198, 199, 234

S Sakai, K.-I., 168, 186

94, 120

172, 186

Q

R

Sammeta, K. P. V., 165, 186 Sand-Jensen, K., 58, 102, 120 Sauberer, F., 58, 121 Sayre, G., 91, 121 Schachter, M., 34 Schaefer, G., 200, 234 Schiechtl, H. M., 221, 235 Schindel, D. E., 159, 186 Schluter, U., 221, 235 Schmid, W. D., 46, 121 Schmidl, L., 4, 5 , 8, 36 Schmithusen, J., 191, 193, 235 Schneider, S., 214, 235 Schoener, T. W., 130, 173, 186 Scholl, G., 222, 234, 235 Scholtens, J. R., 38, 118 Schonbeck, H., 222, 235 Schoof-Van Pelt, M. M., 121 Schreiber, K. F., 214, 215, 216, 217, 235 Schultz, A. M., 197, 235 Schiirholz, G., 214, 235 Sculthorpe, C. D., 38, 72, 121 Seddon, B., 105, 121 Seidelin-Raunkaier, F., 47, 121 Selander, R. K., 173, 186 Shackak, M., 229, 234 Sheldon, R. B., 46, 75, 77, 121 Sheppard, P. M., 162, 179, 183, 186 Sifton, H. B., 97, 121 Sinker, C., 118 Slatkin, M., 136, 144, 186 Smith, A. M., 72, 121 Smith, F. A., 120 Smith, G. R., 183 Smith, I., 61,62,63,64,65,66,67,69,70,

114, 121 Smith, J. N., 119, 184 Smith, R. C., 50, 55, 56, 121, 123 Sneil, K., 86, 121 Snodgrass, R. E., 153, 186 Soule, M., 174, 187 Spence, D. H. N., 39, 40, 41,42, 43, 46,

47, 48, 51, 53, 54, 55, 57, 58, 59, 70, 71, 72, 73, 74, 75, 76, 78, 80, 81, 82, 83, 84, 85, 87, 88, 89, 91, 93, 94, 97, 98, 99, 100, 101, 102, 103, 104, 105, 106, 108, 109, 110, 114, 118, 121

Spooner, D. L., 122 Stilberg, N., 46, 122 Starling, M. B., 99, 122

244 AUTHOR INDEX

Steeman Nielsen. E., 106, 122 Steinhaus, E. A., 14, 36 Stewart, B. R., 174, 187 Stewart, F. M.. 142, 187 Stimac, J. L., 5 , 30, 31. 33, 36 Stross, R. G., 99, 100, 103, 122 Strunk, W., 221, 235 Stumpel, A. H. P., 219. 233 Sukocher, V. N., 190, 235 Sukopp, H., 196, 235 Sundborg, A,, 65, 122

T Takahara, Y., 233 Takatori, S., 99, 122 Talling, J. T., 54, 5 5 , 56, 57, 122 Tansley, A. G., 38, 39, 91, 94, 122, 190,

Tantawy, A. 0.. 165, 187 Taylor, J. N., 183 Thomas, W. L., 222, 235 Thompson, L. S., 35, 36 Thunmark, S., 83, 91, 123 Thuy, N., van, 120 Titus, J. E., 105, 107, 123 Tjallingli. S. P., 220, 235 Toetz, D. W., 87, 123 Trautmann, W., 194, 214, 235 Trent Forschunggruppe, 2 12, 235 Trippel, R., 200, 230 Troll, C.. 190, 191, 192, 214, 235, 236 Turkington, R. A,, 168, 187 Tutin, T. G., 46, 116, 123 Tiixen, R., 189, 193, 194, 236 Tyler, J. E., 50, 55, 56, 121, 123

V Van, T. K., 107, 123 Valen, L. van, 129, 131, 173, 174, 187 Vanderkloet, S., 1 16 Vanicek. V., 222, 236 Varley, G. C., 25, 36 Vaurie. C., 151, 187 Vernadsky, W. I., 191, 236 Vester, F., 200, 202, 203, 204, 206, 227,

Volterra, V., 128, 187 Vouk, V., 89, 123

235

236

W Waals-kooi, R. E. van der. 4, 5 , 35

Waddington, L. H., 209, 236 Walker, D., 38. 87, 95, 123 Walker, N. A,, 118 Walter, H.. 195, 223, 236 Warburg, E. F., I16 Warren, F. L., 6, 36 Webster, A,, 90, 123 Weeks, D. C.. 87, 115, 116 Weiss, P. A,, 198, 236 Welch, E. B., 86, 87, 120 Welch, W. H., 219. 236 Welsh, R. P. H.. 123 West, G., 46, 93, 94, 105, 123 Westhoff. V., 196, 236 Westlake, D. F., 50, 51, 52. 53, 110. 123 Wetzel, R. G.. 53, 61. 69, 120, 123 Whitcombe, M., 87, 115 Whittaker, R. H.. 196, 224, 236 Whyte, R. O., 190, 214, 236 Wiener, N., 200, 236 Wilkinson, A. T. S.. 6, 1 I , 30, 35, 36 Williams, C. B., 2, 36 Williams, R. S., 46, 123 Williams, W. T., I16 Williamson, M. H., 128, 148, 187 Williamson, P., 147, 187 Wilson, D. S., 147, 161, 187 Wilson, E. O., 129. 130, 131. 151, 161,

173, 183, 187 Wilson, J. F., 120 Wilson, L. R., 47, 94, 123 Windecker, W., 7, 36 Winter. H., 87, 124 Wistrand, H., 134, 175, 176, 186 Woebse, H. H., 210. 212, 221, 236 Wolsey. P.. 118 Wood, P. W., 186 Wood, W. A,, 4. 5. 35 Woodwell, G. M.. 208. 236 Wooten, J. W., 38, 72, I17

Yeaton, R. I., 131, 187 Yen, S., 107. 124 Young, G. L., 189, 190, 197. 199, 236

Z Zachwieja, J., 80, 84, I15 Zohary, M., 224, 237 Zonneveld, I. S., 214, 237 Zube, E. H., 190. 237

Y

Subject Index

A

Acari, predatory, 9 Acmaea, 177, 178 Acrocladium, see Calligeron Adaptations of lake plants, 95 ff. Aerenchyma, 72 Agrostis, 168 Algae

filamentous, 38 micro, 106, 108, 109 thalloid, 38 unicellular, 38

Alisma, 93 AInus glutinosa, 39,94 Anabaena, 109 Anaerobiosis in freshwater plants, 72 Anchoring strength of plants, 96 Angelica, 41 Anthocoris nemorum, 9 Anthocyanins, 100, 103 Ants, see Formica, Lasius, Camponotus,

Apanteles popularis, 1 1,24, 33 Araneae, 9, 1 1 Armadillidium vulgare, 9 Avifauna, island, 174 Azolla, 38

B

Beauveria bassiana, 14 Beer’s law, 49 Beetles, see Carabidae, Cantharidae Bembidion lampros, 9 Betula, 39, 48,94 Bicarbonate, 106 Biogeocenose, 190 Biogeography, 191 Bioindicators, 222 Biomass/depth ratio and aquatic plants,

110

Biosystems, 199 general theory, 197

Braconidae, I 1 Broads, East Anglian, 7 1 Bryophyta, 39,44, 73,90, 105, 106 Burden, environmental, 194

C

Cacomantis pyrrhophanus, 8 Calathus f i c ipes , 1 1 Calliergon cuspidatum, 41,42, 93 Calluna, 40 Camponotus, 10 Cantharidae, 10 Carabidae, 9, 1 1 Carbon dioxide

atmospheric, 208 ff. diffusion in lakes, 64

Carex, 222 elata, 94 lasiocarpa, 40,41,48, 49 nigra, 41, 7 1 paniculata, 41 rostrata, 40, 42, 48, 93, 94, 95

Carr, 40,48, 7 1 Catostomus, 160 Cepaea, 147, 177, 179 Cerastoderma, 180 Ceratophyllum demerswn, 38,87,90 Cerosomyia casta, 1 1 Chara, 39, 43 ff., 68, 73 ff., 84, 87 ff., 99,

104, 106, 107 Characeae, see Chara Chaerocoris paganus, 9 Character

convergence, 130 ff., 150 ff., 162 displacement, 129 ff., 145 ff., 150 ff.

Chloroplasts, marginal, 100 Chrysococcyx lucidus, 8 Cinnabar moth, see Tyria jacobaeae Cladium, 92

246 SUBJECT INDEX

Cladophora, 38,43, 89. 109 Clovers, competition, see Trifolium Co-evolution, 32, 136 ff. Competition,

evolutionary effects. 127 ff. exploitative, 129 ff., 135 for food, 151 ff. interference, 128 ff., 135 interspecific in aquatic plants, 103

Competitive ability, in evolution, 132 ff.,

Convergence, see Character convergence Crowding, Lloyd’s index of, 18 Cuckoo, see Cuculus canorus

150 ff., 163 ff.

fan-tailed, see Cacomantis pyrrhophanus

Cuculus canorus, 8 Cuticle thickness in aquatic plants, 87 Cybernetics, 200, 206, 229 Cynosurus, 168

D

Dark respiration, 102, 103 Decision making, 203 Degradation of landscape, 207 ff. Density dependent selection, 141 Density gradients in lakes, 48, 60 ff. Dispersion, Morisita’s index of, 19 Dispersal, 2 Displacement, see Character displace-

ment Divergence, 130 ff. Diversity

and disturbance. 224 and stability, 196

Drepanocladus sandteri, 45, 78 Drosophila, 149, 163 ff., 175 ff. Dryopteris dilatata, 39

E

Earwig, see Forjculu uuriculuriu Echthromorpha intricaroria, 1 1 Ecocline, 196 Ecological release, 173 Ecological species groups, 194 Ecophysiology, 195 Ecosystem. 190,204,205

bio-, 205

techno-, 205 Ecotone, 196 Ecotope, 192,230 Edaphic factors in lakes, 72,91 Education, environmental, 228 Eichornia, 38 Elatine hexandra, 99 Eleocharis palustris, 42, 84,90,94 ff.

multicaulis, 97 Elodea canadensis, 48, 77,91.96,97 Emergent qualities, 198 Emergent vegetation, 86 Energy flow, 199 En!eromorpha, 38, 107, 109 Entropy, 201 Epiphytes, 58, 89 EquisetumJuviatile, 4 I , 42, 84, 95,97 Erica terralix, 48 Eriocaulon, 105 Erosion in lakes, 65 ff.

susceptibility, 96 tolerance, 96

Ervrhraeus phalangoides, 9. 24 Eucyrtidium, 155 Euphotic zone, 39 Evaluation of landscapes, 2 17 Evolutionarily stable strategy (E.S.S.),

Exposure tolerance, 96 I42 ff.

F

Feedback, see Cybernetics

Fen, 48, 71.92 Feronia (Pterostichus) melanaria, 1 1 Fetch, 68 Filipendulu, 4 1 Fire, environmental factor, 228 Fitness, 128 ff. Flies, see Musca, Phaenicia, Drosophila Flow of water in lakes, 95 Fluctuation, order through, 20 I Fontinalis untipyretica, 40, 44, 46, 74, 78,

Forficula auricularia, 9 Formica polyctena, 10 Frungula alnus, 93 Fraxinus pennsylvanica, 40, 94 Fulguration, 198

genetic, 133, 169

91,94, 104

SUBJECT lNDEX 247

G K

Galium palustre, 4 I , 42 Gelbstoff, 51 Geospiza, 152 ff., 174 Germination of aquatic plants, 98, 103 Glyceria maxima, 41 Grasses, see Lolium. Agrostis, Cynosurus Grazing of lake plants by farm stock, 45,

Ground beetles, see Carabidae Groundsel, 2 Group selection, 141 Growth forms, 103

71, 83,94

H

Harpobittacus nigriceps, 10 Helophytes, 39 Heritability, 146, 152 Heterophylly, 98 Heterozygosi ty and gene frequency, 174 Hippuris vulgaris, 42, 45, 73. 77, 79, 98,

Holon, 198,204,205,208 Hydraulic resistance, 96 Hydrilla verticillator, 107 Hydrobia, 155 ff., 160 Hydrophytes, 39 Hydroseeding, 22 1 Hydrosere, 92 Hyperparasitoids, 12

I

103, 110 ff.

Ichneumonidae, I 1 Ichneumon perscrutator, 13 Impact, environmental, 219 Integrative levels, 198, 204 Internode length of aquatic plants, 1

Iris, 41 Irradiance, 49 ff. Island avifaunas, I74 Isoetes, 76, 81, 84, 90, 91, 94, 102 Israel, landscape studies, 222 ff.

103

J

Juncus, 41, 42, 71, 81, 82, 91,93,98

00,

K-factor analysis, 25 Kromme Rijn project, 220 Kulturlandschaft, 19 1, 194

L

Landscape classification, 21 7 damage, 2 18 evaluation, 21 7 mediterranean, 223 ff. reclamation, 221

Landscape ecology, 189 ff. Dutch school, 195 ordination model, 209 surveys, 194

Landschaftspjege, 20 1 Lasius alienus, 10 Leaf area, 101 Lebensbau, 220 Lemna, 38 Life form, 39 Light climate in lakes, 48 ff., 59, 76

absorption, 51 ff. attenuation, 51 ff. colour, 48 ff. scattering, 48 ff. spectral intensity, 56

Limes convergensldivergens, 196 Littorella, 42, 43, 48, 68, 76, 81 ff., 90,

Liverworts, see Bryophyta Lobelia, 43, 48, 81, 83, 84, 98, 99, 103,

Lolium, 168 Lotka-Volterra equations, 138, 143 Ludwigia peploides, 107

94,98, 102, 105

105, 110

M

Management landscape, 210 ff. vegetation, 203

Maquis, 224 Marsilea mutica, 107 Marsupella, 45 Melanchra persicariae, 7 Menyanthes, 40,42 Mesochorus facialis, 33

248 SUBJECT INDEX

Microalgae, see Algae, micro competition from. 108 ff.

Mites, see Acuri Mole, see Tulpu europeu Molecular motion in lakes, 61 ff. Moliniu, 92 Mossses, see Bryophyta Muscu, 169 Myricu. 40,4 1,48 Mvriophvllum, 45, 48. 74, 76. 81. 82, 84,

96. 105 ff.

N

Nubis rugosus, 9 Nuturlundschuft, 191 ff.

potential, 193 Negative binomial distribution, 19 Neodiprion, 2 1 Niche expansion, 173

Nitella. 45, 68. 74, 76, 78. 83. 91, 99, 103, 104

Noosphere, 191, 197,230 Nosemu. I4 Nuphur (urea. 96, 97 Nuthatch, see Situ spp. Nutrients in lakes. 86 ff., 95 Nyussu uquuticu, 40 N.vmphueu, 40. 42, 72

location. 137

0

Organic matter in lake sediments, 91 Orvcolugus cuniculus, 9

P

Passer domesticus, 8 Peat removal, 45 Pentatomidae, 9 Periphyton, 108

Phueniciu, 169 ff. Phalangida as predators, 9 Phu1uri.s. 93 Phanerophytes. 39 Photomorphogenesis, 97, 103 Photosynthesis, 97. 101 ff., 106

Phuecops, I54

Phrugmites, 41, 42, 71, 72. 84, 90, 93, 95 ff.

Phytolittoral, 84 Phytosociology, 193 Piluluriu, 105 Pistiu, 38 Planning, ecological, 193, 212 ff. Pluntugo aquuticu. 93 Pleiotropic effects, 145 Plethodon, 168 Poecilozonites, 1 59 Pollution, 214 Polygenes, 173 Polygonum umphibium, 84, 95, 96 Polymorphism, I27 ff.

balanced, 134 effects of competition on, 134

Populus deltoides, 40 Potumogeton alpinus, 48

umpl~folius, 42, 105 crispus, 100 j l fo rmis , 82,85,87, 101, 105, 109 grumineus, 101 lucens, 42. 98 nutuns, 40, 42, 48, 72, 73. 96, 97, 101,

pectinutus. 45. 96 perfoliutus, 72, 82, 83,9 I , 105 polvgonifolius. 42. 10 1

106

pruelongus, 45, 48, 68, 76. 82. 83. 87. 101. 105

pusillus, 74, 82, 83 obtusijolius, 96,97, 10 1 richurdii, 98 richurdsonii. 72, 76, 83, I00 rostrutu. 48 schweinjurthii, 98 x zizii, 48, 83, 101

Pressure in lakes, 48, 60 ff., 76 Prigogine’s theory, 20 I Production/biomass (P/B) ratio, I 10 Psammo-littoral. 84 Psychophugus omnivorus, I3

Q Quercus robur, 40.94

R

R/FR ratio. 98. 103

SUBJECT INDEX 249

Rabbit, see Oryctolagus cuniculus Ranunculus aquatilis, 96,97 Ragwort, see Senecio jacobaea Rainfall, effect on Senecio and Tyria, 27 Raja, 159 Recreational use of landscape, 2 17 ff. Reductionism, 199 Reed swamp, 41,48,71,80,84,93 Reforestation, 213 Regulation in ecosystems, 201 Release, character-release, 13 1 Remote sensing, 214 Revegetation, 226 Reynold’s number, 63 Rhagonycha, 10 Rhamnus catharticus, 92 Rhizoclonium, 38

S

Salix, 39,92,94 Salt uptake in lake plants, 87 Salvinia, 38 Schoenoplectus lacustris, 40 ff., 72,76,93,

95 ff. Scirpus subterminalis, I 10 Scorpion fly, 10 SCUBA diving, 44 Sediments

interstitial water in, 88 organic matter in, 91 suitability for plant growth, 75, 82,90,

trapping of, 90

density dependent, 141 disruptive, 132 stabilizing, 132

alkaloids, 6 biological control, 4, 33 biomass, 16 co-evolution with Tyria, 32 defoliation, 6

response to, 17 frost mortality, 32 germination, 4 rainfall, effects of, 6 regeneration, 5 root buds, 6

104

Selection competitive, 145 ff.

Senecio jacobaea, 1 ff.

seed production, 5 seedling survival, 5 size, 5 toxicity, 6

Senecio vulgaris. 2 Serological test for predators, 9, 24 Settling velocity, 65 ff. Shelter for lake plants, 86,92 Sita, 15 I Sorting of particles, 67 Spargsnium amersum, 42,96 Sparrow, see Passer domesticus Sphagnum, 4 1.45 Spicaria gracilis. 14 Spiders, see Araneae Spodoptera littoralis, 7 Starling, see Sturnus vulgaris Stoneworts, see Chara Stratiodes aloides, 109 Sturnella, 163 Sturnus vulgaris, 8 Sublittoral, 84 Substrate, lake, 95 ff. Subularia aquatica, 43,99 Succession in lake vegetation, 92 ff. Sulphur dioxide, environmental effects,

Swamp forest, 39 Symbiosis, 202 Systems theory, general, 197 ff.

222

T

Tachinidae, 1 1 Talpu europaeu as predator of Tbv-ia, 7,

8 , 24 Technosphere, 205 Telenomus, 1 1 Temperature gradients in lakes, 48,60 ff. Terracing of lake bottoms, 68 Thamnium, 45 Tracheophyta, 39,73,87 Tribolium. 149, 167 ff. Trifolium, competition with grasses, 168 Turbulence in lakes, 48, 60, 82, 92, 96 Typha latijolia, 97 Typhlosaurus, 154 Tyriajacobaeae, 1 ff.

adult predators, 1 1 alkaloids in. 7

250 SUBJECT INDEX

Tyria jacobaeae-cont. aposematism, 7 carrying capacity, 3 1 co-evolution with Senecio jacobaea, 32 defensive secretions, 7 density dependent factors, 3 I development, 3 diapause, 2 ff. disease organisms, 13 dispersal, 18 ff., 32 dispersion, 18 ff. distastefulness, 7 egg clusters, 19 ff.

density, 18 and survival, 21

and density, 27 and female longevity, 17 and female size, 17 and food supply, 25

flicking movements, 8 food, 3

nitrogen content, 15 quality, 14 ff. quantity, 16 ff. shortage. 12 plant density, extinction, 23, 32

fecundity, 3

geographical variation, 30 larvae, 3 ff., 10 ff.

cannibalism, 24 competition, 21 dispersal, 27 emigration, density dependent, 24 gregariousness, 2 I migration, 23 starvation, 25

life tables, 24 mating, 2 microsporidia in, 13 mortality, 24 parasitoids, 11 population model, 27 ff. population stability and egg size, 28 predators, 7 ff., 33

pupa, 3 predators of, 8 size and larval food, 29

predators, vegetation and density, 9 and larval density, 21

quality of individual. 29 soil moisture, 4 stress, 14 viruses, 10. I3 ff. water balance, 4 Weeting Heath model, 27 ff.

U

Underwater leaves, 98 Uplands, management of, 224 ff. Urlandschufr, 19 I , 194 Utricularia purpurea, 38. 75. 79, 93 Valisneria umericana, 105 Variance of qualitative characters, 173 ff. Vielfaltigkeit, 2 18 Wallace effect, 130 Water table, 39 Watershed ecosystems, 2 I5 Waves, 62

Wave-mixed zone, 1 12 Wetland types, 38 Wirkungsgefliige, 204 W.L.O. (workshop group), 219 Woodland management, 228 Woodlice, see Armadillidium vulgare.

Philoscia muscorurn

depth, 70

x Xisticus cristatus, 11

Z

Z,, 39, 43, 55, 78, 108 ff.

Zonal vegetation, 195 Zonation of plants in lakes, 37 ff, Zosteru marina, 58

z,,, 39, 55

Advances in Ecological 1-1 1 ..

Research, Volumes

Cumulative List of Titles

Aerial heavy metal pollution and terrestrial ecosystems, 11, 21 8 Analysis of processes involved in the natural control of insects, 2, 1 The distribution and abundance of lake-dwelling Triclads-towards a hypothesis, 3, 1 The dynamics of aquatic ecosystems, 6, 1 The dynamics of a field population of the pine looper, Bupulus piniurius L. (Lep.,

Ecological aspects of fishery research, 7, 115 Ecological conditions affecting the production of wild herbivorous mammals on

Ecological implications of dividing plants into groups with distinct photosynthetic

Ecological studies at Lough Ine, 4, 198 Ecology, evolution and energetics: a study in metabolic adaptation, 10, 1 Ecology of fire in grasslands, 5, 209 The ecology of serpentine soils, 9, 255 Ecology, systematics and evolution of Australian frogs, 5, 37 The effects of modern agriculture, nest predation and game management on the

Energetics, terrestrial field studies and animal productivity, 3, 73 Energy in animal ecology, 1, 69 Forty years of genecology, 2, 159 The general biology and thermal balance of penguins, 4, 131 Heavy metal tolerance in plants, 7, 2 Human ecology as an interdisciplinary concepts: a critical inquiry, 8, 2 Industrial melanism and the urban environment, 11, 373 Integration, identity and stability in the plant association, 6, 84 Litter production in forests of the world, 2, 101 Mathematical model building with an application to determine the distribution of

The method of successive approximation in descriptive ecology, 1, 35 Pattern and process in competition, 4, 1 Population cycles in small mammals, 8, 268 Predation and population stability, 9, 1 The pressure chamber as an instrument for ecological research, 9, 165 The production of marine plankton, 3, 1 17 Quantitative ecology and the woodland ecosystem concept, 1, 103

Geom.), 3, 207

grasslands, 6, 137

production capacities, 7, 87

population ecology of partridges (Perdix perdix and Alectoris rufu), 11, 2

Dunban@ insecticide added to a simulated ecosystem, 9, 133

252 CUMULATIVE LIST OF TITLES

Realistic models in population ecology, 8, 200 Rodent long distance orientation (“homing”), 10, 63 Secondary production in inland waters, 10, 91 A simulation model of animal movement patterns, 6, 185 Studies on the cereal ecosystem, 8, 108 Studies on grassland leafhoppers (Auchenorrhyncha, Homoptera) and their natural

Studies on the insect fauna on Scotch Broom Sarothamnus scoparius (L.) Wimmer,

Soil arthropod sampling, 1, 1 A synopsis of the pesticide problem, 4, 75 Theories dealing with the ecology of landbirds on islands, 11, 329 Towards understanding ecosystems, 5, 1 The use of statistics in phytosociology, 2, 59 Vegetational distribution, tree growth and crop success in relation to recent climate

enemies, 11, 82

5, 88

change, 7. 177

advances in ecological research, volume 12

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