Oecologia (Berl.) 36, 93-102 (1978) Oecologia �9 by Springer-Verlag 1978

Artificial Oases in a Lacustrine Desert

C.F. Mason

Department of Biology, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, England

Summary. 1. Aspects of colonization by freshwater invertebrates on artificial substrata (macrophyte models) placed in the benthos of a eutrophic lake were studied.

2. Colonization was rapid, with equilibrium occuring at about 35 days. The colonization rate curve decreased with time but extinction rate remained constant.

3. Predators formed 22-32% of the fauna at equilibrium. 4. Area and distance accounted for 92% of the variation in species

richness; 69% of the variation was due to area alone. 5. The faunal coefficients z were higher than expected and may be due

to competitive interactions in simple habitats.

1. Introduction

MacArthur and Wilson (1963, 1967) described the number of species on islands as being a dynamic equilibrium determined by the rates of immigration and extinction. The number of species which an island can support depends on the size of the island and its distance from sources of propagules.

Evidence in support of the equilibrium theory has been presented from observations made on the faunas of archipelagos (e.g. Diamond, 1969, 1971), from the experimental manipulation of small islands (e.g. Crowell, 1973; Simber- loft, 1969; Simberloff and Wilson, 1969; Wilson and Simberloff, 1969), from a study of habitat islands (e.g. Brown and Brown, 1977; Seifert, 1975) and from the use of artificial islands in aquatic habitats (e.g. Cairns et al., 1969; Patrick, 1967; Schoener, 1974 a, b). Simberloff (1974) has emphasized that any model should be relevent to small scale and local systems as well as larger ones.

The work presented here examines aspects of the colonization by inverte- brates of simple artificial habitats (aquatic macrophyte models) submerged in a lake from which aquatic macrophytes disappeared a decade ago due to hyper- eutrophication.

0029-8549/78/0036/0093/$02.00

94 C.F. Mason

2. Site

A l d e r f e n B r o a d , N o r f o l k ( N a t i o n a l G r i d R e f e r e n c e T G 354196) is a smal l ,

s h a l l o w l ake ( a r e a 4 .7 ha , a v e r a g e d e p t h 0.8 m) , fu l ly d e s c r i b e d in M a s o n (1977).

T h e si te f o r m e r l y c o n t a i n e d a r i ch m a c r o p h y t e f lo ra , d o m i n a t e d b y Ceratophyl- lure demersum L. T h e m a c r o p h y t e s d i s a p p e a r e d d u r i n g the p e r i o d 1 9 6 8 - 7 0 d u e

to excess ive e u t r o p h i c a t i o n ( M a s o n a n d B r y a n t , 1975) a n d o n l y C. demersum h a s s ince b e e n r e c o r d e d , in s m a l l a m o u n t s o n l y a n d p r o b a b l y i n t r o d u c e d acci-

d e n t a l l y d u r i n g r e s e a r c h ac t iv i t ies .

D u r i n g m o n t h l y s a m p l i n g b e t w e e n N o v e m b e r 1971 a n d J u n e 1975 22 i n v e r t e -

b r a t e t a x a we re r e c o r d e d in t he s e d i m e n t s o f t he b r o a d a n d o n l y s e v e n o f t h e s e

c o u l d b e d e s c r i b e d as o f r e g u l a r o c c u r r e n c e ( M a s o n , 1977). T h i s u n s t r u c t u r e d a n d

m o b i l e s e d i m e n t h a b i t a t w i t h l ow b i o t i c d i v e r s i t y c a n be l i k e n e d to a dese r t .

I n c o n t r a s t , w i t h i n t he 1.6 h a o f r e e d s w a m p a l o n g t h e e a s t e r n edge o f t he

lake , s a m p l e s t a k e n in Ju ly 1971 r e v e a l e d 114 t axa , o f w h i c h 62 t a x a were

p r e s e n t a t t he i n t e r f a c e b e t w e e n s w a m p a n d o p e n w a t e r ( M a s o n a n d B r y a n t ,

1974). T h i s i n t e r f a c e is s h a r p a n d t he f a u n a 1 m o u t f r o m t h e r e e d s w a m p

is i d e n t i c a l to t h e b e n t h i c f a u n a o f t he l ake ( M a s o n , 1971).

3. Methods

The standard unit for colonization experiments consisted of a l0 x 10 cm square of wire-mesh netting (1.5 cm aperture) onto which 12 strands of 20 cm long, three-stranded, polypropylene rope (diameter 0.7 cm) were sealed using a bunsen flame. Thus the total strand length per unit was 240 cm and the total surface area of the strands was 528 cm 2. One hundred units were made.

On 7 April, 1977, the units were sited in the open water of the lake, 4 m out from the reedbed and approximately 8 m apart. Each unit lay flush with the surface of the mud and was secured with an individually numbered bamboo cane (diameter 1.5 cm), the polypropylene strands floating upwards in the water.

On each of eight sampling occasions ten randomly selected units were recovered. Twenty units were lost or vandalized during this period. Each unit was carefully lifted from the mud and a pond-net placed beneath. The unit was then removed from the bamboo cane and transferred to a polythene bag, together with any dislodged material in the net. The bamboo cane was examined carefully and any animals were transferred to the polythene bag.

In the laboratory the contents of the bag were washed into a 250 gm aperture sieve to remove silt and then sorted in a white tray under a bright light. Arthropods were preserved for subsequent identification, anneiids, turbellaria and molluscs were identified immediately.

To examine the effect of island area and distance from sources of propagules on the number of species, three wire-mesh units were made of each of four sizes, 10 • 10 cm, 20 x 20 cm, 30 x 30 cm and 40 • 40 cm (i.e. areas of 100 cm 2, 400 cm 2, 900 cm 2 and 1600 c m 2 respectively). Polypropylene strands of the same length (20 cm) and density (12 strand/100 cm 2) as the first experiment were attached. On 13 June, 1977 one unit of each size was placed respectively at 12 m, 30 m and 50 m from the reedbed and about 30 m apart. The larger units required anchoring with two bamboo canes. All units were recovered on 15 August, 1977 (after 63 days exposure) and treated as in the first experiment.

4. Results

N o t all t a x a c o u l d be i d e n t i f i e d to t he spec ies level. U n i d e n t i f i e d species we re

a s s i g n e d n u m b e r s . A t o t a l o f 51 t a x a w e r e r e c o r d e d o n t h e u n i t s d u r i n g expe r i -

m e n t s a n d t h e s e a re l i s t ed in A p p e n d i x 1.

Artificial Oases in a Lacustrine Desert 95

30

20

I0

10 20 30 40 50 60 70 80 90 100 110 doys

Fig. 1. The mean number of taxa (o)_+2SE and the total number of taxa (o) recorded on I00 cm 2 units placed 4 m out f rom the reedbed and exposed for varying lengths of time (days) f rom 7 April 1977

300-

200'

_• 100-

n:s

50

10 ~._ 10 20 30 40 50 60 70 80 90 100

days

I:i~. 2. The mean number of individuals recorded on 100 cm 2 units placed 4 m out f rom the reedbed toc vary ing lengths of t ime f rom 7 April 1977

During the colonisation experiments on the 10 cm x 10 cm units a total o f 45 taxa was recorded. The most abundant colonizers were the chironomids Polypedilurn sp. 1, Polypedilurn sp, 2 and Cricotopus sp. 1, the caddis Cyrnus flavidus and the leech Helobdella stagnalis.

The colonization curve is shown in Figure 1. Equilibrium was reached at about 35 days after a rapid build-up. Individual units reached equilibrium with about ten species, the equilibrium level for the sampling occasion of ten units was with about 24 species. An examination of the curve for the total invertebrate population per unit (Fig. 2) shows that an equilibrium of individuals was only

96

60 50.

40

~30- ,

~20-

C.F. Mason

z6 46 6o ~o ~60 days

Fig. 3. The percentage of taxa (e) and individuals (o) of the total fauna that are predators, collected on 100 cm 2 units exposed for varying lengths of time from 7Apri l 1977, 4 m out from the reedbed

3

2

1-

7 3

&0.5

C12

o

io ~'o 6'o 8o loo days

Fig. 4. The rates of colonization (o, upper line) and decolonization (o, lower line) on 100 cm 2 units exposed for varying lengths of time from 7 April 1977 at a distance of 4 m from the reedbed

reached towards the end of the experiment (80-100 days) due to continuous immigration of individuals and to reproduction on the units. Densities of animals at equilibrium averaged 10,400 m- 2 bottom.

The proportion of taxa and individuals that were predators is shown in Figure 3. Predator species formed 50% of the initial colonizers, but fell quickly to 22-32%. Numbers of predator individuals showed a peak of 27% of the total population after 28 days, but then declined to a level of 8-12%.

Colonization rate curves (calculated from the number of new species since the last sampling occasion divided by the number of days between samples) and decolonization rate curves (the number of species eliminated since the last sampling occasion divided by the number of days between samples), follow- ing Cairns et al. (1969), are shown in Figure 4. The rate of colonization decreases

Artificiai Oases in a Lacustrine Desert 97

30,

j 1 2 m 20.

/ . ~" 30m

10.

~5

lo0 ' ' (0o' 'iobo iooo 5 area cm 2 6

20

10.

x ~ c~

ii .... 10 50 100

distance m

Fig. 5. The number of taxa recorded on units of four sizes placed at distances of 12 m (o), 30 m (o) and 50m (m) from the reedbed

Fig. 6. The number of taxa recorded on units of 100 cm 2 (e), 400 cmz (m) 900 cm 2 (a) and 1600 cm 2 (o) placed at three distances from the reedbed

with time, as predicted by the MacArthur-Wilson model. The fitted regression relating colonization (number of new species per day) with time is:

log y = 0.2641 - 0.0089)(.

The gradient is significantly different from zero (P<0.05). However, the extinc- tion rate also decreases with time, the regression equation being:

log y =0.0128 - 0.0066X.

The gradient is not significantly different from zero (P > 0.05). The turnover rate of the equilibrium community can be predicted from

the equation 1.15 xS/to.90 (MacArthur and Wilson, 1971), where ~ is the mean number of species present at equilibrium and to.90 is the time taken to reach 90% of the equilibrium species number. S, calculated from the last four sampling occasions, is 24.5 and to.90 is 23 days, giving a turnover rate of 1.23 species per day.

The turnover rate can also be calculated from the equilibrium position. For the final three sampling periods (i.e. at equilibrium) the mean of the daily colonization rate was divided by the mean of the daily extinction rate, giving a turnover rate of 1.83 species per day.

The units in the second experiment were exposed for 63 days. The effects of size of unit on the number of species present at the three distances is shown in Figure 5. At the three distances from the reedbed the number of species recorded increases steadily with the area of the unit. The regressions of number

98 C.F. Mason

of species (5) against area (A) at the three distances (d) are:

l o g S = - 0 . 3 5 + 0 . 5 2 logA (r=0.90) d = 1 2 m l o g S = - 1 . 0 2 + 0 . 6 8 logA (r=0.99) d = 3 0 m log S = - 1 . 8 0 + 0 . 8 9 log A (r=0.99) d=50 m

All regressions were significantly different from zero (P < 0.05). The effects of distance on the number of species present on islands of four

sizes are shown in Figure 6. In all cases the numbers of species present declined with distance. The regression equations are:

log S = 1.64 log S = 2.47 log S = 1.73 log S = 1.56

-0 .95 log d (r=0.99) A = 100 cm 2 -1 .16 log d (r=0.99) A=400 cm 2 -0 .48 log d (r =0.99) A=900 cm z -0 .31 log d (r=0.99) A = 1600 cm 2

All slopes are significantly different from zero (P < 0.05). A multiple regression with area and distance as independent variables gave

the equation :

log S = -0 .03 +0.70 log A - 0 . 7 2 log d.

Ninety-two per cent of the variation in S can be explained by area and distance. Sixty-nine per cent of the variation can be explained by area alone.

5. Discussion

The artificial units used in these experiments model in a simple way the aquatic macrophytes which no longer occur in Alderfen Broad. They resemble true islands in that the terrain between the source area (the reedbed) and the units is essentially hostile. While invertebrates may be able to feed to some extent in the shifting muds of the benthos there is nowhere suitable for oviposition. Furthermore predation on invertebrates by the large fish population is likely to be intense in an unstructured benthic habitat offering no shelter.

The units present a very simple habitat for colonization, with a wire-netting base and attached strands of nylon floating freely in the water, the whole secured in place on the surface of the mud by a bamboo cane. There may, of course, be a more subtle environmental heterogeneity. Algae, a food source to many invertebrates will colonize (Patrick, 1967) and the algal community will change with time. Wortley (1974) has shown that artificial substrata covered with periphyton are colonized by significantly more invertebrates than substrata free of periphyton.

Forty-five taxa were recorded during the colonization experiments with 10 x 10 cm units. The colonizers can be compared with the species recorded in 1971 for the source area of the reedbed/water interface (Mason and Bryant, 1974). Species of chironomids and hydracarines have been combined as they were not identified in 1971. Of 36 taxa recorded on the island units, 27 (75%)

Artificial Oases in a Lacustrine Desert 99

were present in the reedbed in 1971. Six further island taxa, not recorded in the reedbed in 1971, have since been found there regularly (unpublished observations). Conversely, 58% of the taxa recorded at the reed/water interface in 1971 occured on the island units in 1977. All of the seven regular benthic species were recorded on the units, but always in low numbers.

Colonization of the units was rapid, with equilibrium being reached in about 35 days. Similar rapid invasion rates have been recorded for invertebrates invad- ing implanted substrata in Swedish streams (Ulfstrand et al., 1974) and in a marine lagoon (Schoener, 1974b). MacArthur and Wilson (1963) suggested that invasion rates are likely to be high in new habitats.

The equilibrium model of MacArthur and Wilson (1963, 1967) requires that colonization rates decline and extinction rates increase until they eventually become equal. Colonization and extinction rate curves have been examined by Cairns et al. (1969), Dickson and Cairns (1972) and Schoener (1974b). The rate of colonization on the units in Alderfen Broad does decrease with time but there is no significant increase in extinction rate. Equilibrium would therefore appear to be reached when the colonization rate has declined to equal a constant extinction rate. The increasing extinction rates with time suggested by Cairns et al. (1969) and Schoener (1974b) are also unconvincing.

Heatwole and Levins (1972), re-analyzing the data of Simberloff and Wilson (1969, 1970), showed that the trophic structure of defaunated mangrove islands eventually closely resembled that before defaunation even though the faunistic composition was different. Species of predators made up 22% of the mangrove community. On the units in Alderfen Broad, predator species initially formed 50% of the fauna, but the proportion fell rapidly to make up 22-27% of the community in the final 50 days of the experiment. In terms of numbers of predator individuals the proportion reached a peak of 27% of the total community after 30 days exposure and then fell to 8-12%; no explanation can be offered for the peak.

If extinction occurs commonly, its frequency should increase as population sizes decrease. Area may therefore affect species number independently of habitat diversity (Simberloff, 1974). Lack (1975), however, concerned with the avifaunas of natural, undisturbed islands, emphasized a major role in habitat diversity determining species richness; smaller islands have less habitat diversity than large ones.

In the second experiment in Alderfen Broad, larger units differed from small units only in terms of area. One unit of each size was placed at three distances from the reedbed. The units were exposed for 63 days, 30 days longer than the 100 cm 2 units in the first experiment. It can be argued that, as coloniza- tion was not followed, there is no evidence that equilibrium had been attained. However, if the regression line for the effect of distance on species richness of 100 cm 2 units (Fig. 6) is traced back it predicts that, at 4 m, the equilibrium community would be 12 species. The equilibrium population on 100 cm 2 units at 4 m in the first experiment was 10_+2 species. It would, therefore, appear that equilibrium was approached in the second experiment.

The number of species was influenced by both area and distance, which combined accounted for 92% of the variation. Sixty-nine per cent of the variation could be explained by area alone. Experiments by Simberloff (1976) with man-

100 C.F. Mason

grove islands have also shown that species richness increases with area alone, independently of habitat diversity.

The faunal coefficient z, expressed as the slope of the regression of log S on log A, is considered to have values between 0.20 and 0.35 for true islands (MacArthur and Wilson, 1963, 1967; May, 1975). On the artificial units in Alderfen Broad, z was much higher, with values of 0.52 at 12m, 0.68 at 30 m and 0.99 at 50 m from the source of propagules. Other high values recorded are of 0.406 for insects inhabiting clumps of Heliconia wagneriana (Seifert, 1975) and 0.428 for mammals inhabiting mountain tops (Brown, 1971). Opler (1974) considered that highly interactive (e.g. competitive or symbiotic) commu- nities may show higher z values than those in the range considered by MacArthur and Wilson (1967). This has also been shown by Strong (1974) for the phytopha- gous insect fauna of trees. The very simple structure of the experimental units on Alderfen Broad probably ensured that the herbivorous species present were exploiting the same periphytic algal resource. With little habitat structure for concealment, the herbivores may be open to attack by a wider range of predator species present, which may hence also be in competition.

The dispersive habit of the invertebrates presumably evolved when the chance of successful colonization was very high i.e. lakes such as Alderfen Broad have a seasonal emergence of a diverse aquatic macrophyte flora, growing densely and presenting a wide range of micro-habitats, initially free of invertebrates. This seasonal emergence of plants no longer takes place in Alderfen Broad, due to the effects of eutrophication, and the termination was sudden, in about 1969. The macrophyte models of these experiments present oases to dispersing animals which would otherwise almost certainly perish, by star- vation, by being eaten or being unable to reproduce in the structureless, shifting muds of the benthic desert. However, the simplicity of the models does not allow for the niche separation which would occur in the mixed species sward of real macrophytes, so that competition initially is likely to be intense.

Appendix 1

The Taxa Recorded on Art i f ic ial Substrata in Alderfen Broad

Spongilla Iacustris (L.) Polycelis tenuis (Ijima) Valoata piscinatis (Muller) Potamopyrgus jenkinsi (Smith) Bithynia tentaculata (L.) Lymnaea peregra (Muller) Planorbis albus (Muller) Acroloxus lacustris (L.) Anodonta cygnaea (L.) Sphaerium eorneum (L.) Dero digitata (Muller) Stylaria lacustris (L.) Potarnothrix hammoniensis (Michaelson) Enchytraeidae sp. 1.

Asellus aquaticus (L.) Aaellus meridianus Racovitza Caenis robusta Eaton Caenis horaria (L,) Ischnura elegans (Linden) Erythromma najas (Hansemann) Cymatia bonsdorffi (Sahlberg) Sigara falleni (Fieber) Dytiscus sp. 1, Sialis lutaria (L.) Cyrnus Jlavidus (McLachlan) Phryganea grandis L. Limnephilus sp. 1. Mystacides longieornis (L.)

Artificial Oases in a Lacustrine Desert 101

Hemiclepsis ma~'ginata (MuIler) Glossiphonia heteroclita (L.) Glossiphonia complanata (L.) Helobdella stagnalis (L.) Erpobdella octoculata L.) Hydracarina sp. 1. Hydracarina sp. 2. Hydracarina sp. 3. Eurycercus lamellatus (Muller) Cyprididae sp. I. Argulus foliaeeus (L.)

Culicoides sp. 1. Bezzia nobilis (Winnertz) Procladius sp. 1. Cricotopus sp. 1. Cricotopus sp. 2. Metriocnemus sp. 1. Camptochironomus tentans Fabr. Chironomus plumosus (L.) Polypedilum sp. 1. Polypedilum sp. 2. Polypedilum sp. 3. Micropsectra sp. 1.

Acknowledgements. The Norfolk Naturalists Trust kindly allowed access to their reserve at Alderfen Broad. Mr. J. Fosker assisted with experiments and Mr. A. Hussey with computing. Mrs. E.A. Dunn kindly typed the manuscript.

References

Brown, J.H. : Mammals on mountaintops: non-equilibrium insular biogeography. Am. Nat. 105, 467-478 (1971)

Brown, J.H., Kodric-Brown, A.: Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58, 445-449 (1977)

Cairns, J., Dahlberg, M.L., Dickson, K.L., Smith, N., Waller, W.T. : The relationship of fresh-water protozoan communities to the MacArthur-Wilson equilibrium model. Am. Nat. 103, 439-454 (1969)

Crowell, K.L.: Experime:ntal zoogeography: Introductions of mice to small islands. Am. Nat. 107, 535-558 (1973)

Diamond, J.M. : Avifaunal equilibrium and species turnover rates on the Channel Islands of Califor- nia. Proc. Nat. Acad. Sci. (Wash.) 64, 57 63 (1969)

Diamond, J.M.: Comparison of faunal equilibrium turnover rates on a tropical and a temperate island. Proc. Nat. Acad. Sci. (Wash.) 68, 2742-2745 (1971)

Di~kson, K.L., Cairns, J. : The relationship of fresh-water macro-invertebrate communities collected by floating artificial substrates to the MacArthur-Wilson equilibrium model. Am. Midl. Nat. 88, 68 75 (1972)

Heatwole, H., Levins, R.: Trophic structure stability and faunal change during recolonization. Ecology 53, 531 534 (1972)

Lack, D. : Island Birds. Oxford: Blackwells i976 MacArthur, R.H., Wilson, E.O.: An equilibrium theory of insular zoogeography. Evolution 17,

373-387 (1963) MaeArthur, R.H., Wilson, E.O.: The theory of island biogeography. Princeton, N.J.: Princeton

Univ. Press 1967 Mason, C.F.: Populations and production of benthic animals in two contrasting shallow lakes

in Norfolk. J. Anim. Ecol. 46, 147-172 (1977) Mason, C.F., Bryant, R.J. : The structure and diversity of the animal communities in a broadland

reedswamp. J. Zool. (Lond.) 172, 289-302 (1974) Mason, C.F., Bryant, R.J.: Changes in the ecology of the Norfolk Broads. Freshwat. Biol. 5,

257-270 (1975) May, R.M. : Patterns of species abundance and diversity. In : Ecology and evolution of communities

M.L. Cody, J.M. Diamond (eds.), pp. 81 120. Cambr i dge -London : Harvard University Press 1975

Opler, P.A. : Oaks as evolutionary islands for leaf-mining insects. Am. Sci. 62, 67-73 (1974) Patrick, R.: The effect of invasion rate, species pool, and size of area on the structure of the

diatom community. Proc. Nat. Acad. Sci. (Wash.) 58, 1335 1342 (1967) Schoener, A. : Colonization curves for planar marine islands. Ecotogy 55, 818-827 (1974a)

102 C.F. Mason

Schoener, A.: Experimental zoogeography: colonization of marine miniislands. Am. Nat. 108, 715~38 (1974b)

Seifert, R.P.: Clumps of Heliconia inflorescences as ecological islands. Ecology 56, 1416-1422 (1975)

Simberloff, D.S. : Experimental zoogeography of islands. A model for insular colonization. Ecology 50, 296-314 (1969)

Simberloff, D.S.: Equilibrium theory of island biogeography and ecology. An. Rev. Ecol. Syst. 5, 161 182 (1974)

Simberloff, D.S. : Experimental zoogeography of islands: effects of island size. Ecology 57, 629-648 (1976)

Simberloff, D.S., Wilson, E.O. : Experimental zoogeography of islands: The colonization of empty islands. Ecology 50, 278 296 (1969)

Simberloff, D.S., Wilson, E.O.: Experimental zoogeography of islands: A two year record of colonization. Ecology 51, 934-937 (1970)

Strong, D.R.: Nonasymptotic species richness models and the insects of British trees. Proc. Nat. Acad. Sci. (Wash.) 71, 2766-2769 (1974)

Ulfstrand, S., Nilsson, L.M., Stergar, A. : Composition and diversity of benthic species collectives colonizing implanted substrates in a south Swedish stream. Ent. Scand. 5, 115-122 (1974)

Wilson, E.O., Simberloff, D.S. : Experimental zoogeography of islands: Defaunation and monitoring techniques. Ecology 50, 267-278 (1969)

Wortley, J.S.: The role of macrophytes in the ecology of gastropods and other invertebrates in the Norfolk Broads. Unpublished Ph.D. thesis, University of East Anglia (1974)

Received May 2, 1978