[Advances in Marine Biology] Advances in Marine Biology Volume 10 Volume 10 || Habitat Selection by Aquatic Invertebrates
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Adv. mar. Biot., Vol. 10, 1972, pp. 271-382
HABITAT SELECTION BY AQUATIC INVERTEBRATES
P. S. MEADOWS AND J. I. CAMPBELL Department of Zoology, University of Blasgow, Scotland
Introduction . . . . . . .. .. .. .. .. .. The Physical and Chemical Environment . . .. .. .. ..
A. Intertidal Animals . . . . .. .. .. .. .. B. Marine Animals . . .. .. .. .. .. .. C. Freshwater Animals . . .. . . . . .. .. .. D. Interstitial Animals . . .. .. . . . . .. ..
Commensal and Parasitic Associations . . .. .. .. .. The Biological Environment . . .. .. .. .. .. ..
A. Settlement Behaviour . . . . .. .. .. .. .. B. Gregariousness . . .. .. .. .. .. .. .. C. Spacing Out and Aggression . . . . . . .. .. .. D. Associations with Plants . . . . . . . . .. .. E. Larval Chemoreception at Settlement . . .. . . . . F. Habitat Selection and Micro-organisms . . . . .. .. G. Food Selection . . .. .. .. .. .. .. .. H. Homing .. .. .. .. .. . . .. .. .. I. Oviposition Preferences . . .. . . .. .. ..
Physiology and Viability . . .. .. .. .. .. .. Mechanisms of Habitat Selection . . .. .. .. .. . . Learning, Environmental History, and Physiological State . . .. Individual Variation, the Colonization of New Habitats, and the Origin
of New species . . .. .. .. .. .. . I * . Conclusion . . .. .. . . . . .. .. . . . . summary.. . . . . .. .. .. .. .. . . . . Acknowledgments . . . . . . .. .. .. .. .. References . . . . .. . . . . . . . . . . . .
27 1 273 273 280 286 294 297 302 302 304 311 314 318 319 324 328 329 330 334 340
346 355 366 360 361
I. INTRODUCTION These
habitats are dispersed in differing patterns and at different densities over a species geographical range. The present review attempts to explain why animals are found in certain habitats and not in others, and is restricted to a consideration of habitat selection by marine and freshwater invertebrates as revealed by experimental analysis. There is, of course, strong circumstantial evidence for habitat selection from field studies on the distribution of invertebrates in relation to their habitats, but we do not intend to review this as the literature is extensive and not strictly pertinent to our viewpoint.
Most species are found in easily recognizable habitats.
272 P. 5. MEADOWS AND J. I. CAMPBELL
The restriction of a species to localized habitats within its geo- graphical range might be due to one of two reasons; animals might die if they wandered outside the limits of their habitat, or alternativeIy, be able to recognize their habitat and to return to it or other similar ones after having made excursions into less suitable habitats. Almost all the experimental evidence we shall present supports the latter hypothesis. Animals find, return to, or stay in their usual habitat by a process of choice, in which they are continuously assessing and responding to information received from the environment. Habitat selection, therefore, is essentially the relationship between behaviour and environment, and we consider that i t largely determines the local distribution of animal species. On the larger scale of geographical distribution it is as yet uncertain how important habitat selection is although it almost certainly plays a significant role. Occasionally, of course, animal distribution even at the local level will be directly con- trolled by environmental rather than by behavioural factors. Past flowing water in rivers, wind-induced water currents in fresh water and the sea, as well as tides, waves and ocean currents, will carry many smaller planktonic organisms from place to place in spite of any behavioural responses they might show. However, these instances only serve to emphasize the validity of our general thesis that the distribution of animals is determined by their behaviour, and this will become evident from the examples we quote.
For the purposes of the present review we shall consider the ways in which animals react to various parts of their environment. Firstly we discuss the reactions of invertebrates to their physical and chemical environment and consider intertidal, marine, freshwater and interstitial invertebrates, in that order (Verwey, 1949). Then, after commenting on some problems presented by commensal and parasitic associations, we outline the response of aquatic invertebrates to their biological environmentgregariousness and spacing out, larval behaviour and settlement, reactions to plants and to micro-organisms, and feeding and oviposition preferences. In the final sections on the general processes of habitat selection, we outline what is known of physiology and viability in relation to habitat selection, point out the variability that can occur between individuals of a species, consider the influence of learning and previous experience, and lastly discuss the ways that new environments are colonized and how habitat selection may play a part in speciation.
We have not discussed the assorted migrations undertaken by many aquatic invertebrates (e.g. annual, diurnal, vertical) unless they are relevant to the subject under consideration, as there are a number
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of reviews covering these subjects already (Allen, 1966; Cloudsley- Thompson, 1962; Knight-Jones and Morgan, 1966; Korringa, 1957); neither have we referred to the original literature on the responses of marine larvae to their physical environment at settlement since the subject is adequately covered by Williams (1964, 1952).
11. THE PHYSIOAL AND CHEMICAL ENVIRONMENT
A . Intertidal animals Animals on intertidal shores are exposed to a wide range of environ-
mental variables. On a hot summers day tide pool temperatures are likely, even in temperate climates, to reach 3O-4OoC, while during cold winter spells temperatures may fall below 0C. Fresh water flowing over a beach will expose animals in its path to salinity fluctuations of 0-33%, during a single tidal cycle, and the beach itself is exposed to air twice a day as the tide rises and falls. Animals living on the shore must, therefore, be able to respond to fluctuations in their environment, particularly of temperature, salinity and humidity, if they are to maintain themselves in one position.
Little is known of local fluctuations in temperature on the shore or of the temperature preferences of animals that live there. Temperatures in tide pools (Pyefinch, 1943; Ganning, 1967) and sediments (Johnson, 1965) change from hour to hour, and presumably animals must react to them. Two tide pool copepods studied by Ganning and Wulff (1966) and Ganning (1967) showed temperature preferences which accorded with their distribution.
Salinity can fluctuate widely on beaches, and there is some evidence that intertidal Crustacea are capable of selecting specific salinities in which to live. Ligia baudiniana Milne-Edwards survives longer in air over damp sand, than in sea water, and longer in sea water than in distilled water (Barnes, 1932). However, if offered a choice, it prefers filter paper moistened with 1O-25% sea water, rather than 100% sea water or distilled water (Barnes, 1938). Its behaviour and survival will, therefore, tend to limit it to the upper shore in areas where damp sand flanks freshwater rivulets. Other crustaceans also show salinity preferences (Gross, 1955, 1957; Teal, 1958; Lagerspetz and Mattila,l961; Ganning, 1967; McLusky, 1970), but nothing is known of intertidal organisms from other phyla.
As the tide recedes across intertidal beaches, the humidity in and around heaps of stones and at the surface of and within sandy sediments will fall from 100% R.H. to lower values, only to move back again as the tide rises. Isopod and amphipod Crustacea (Lagerspetz, 1963 ;
274 P. 9. MEADOWS AND J. I. CAMPBELL
Lagerspetz and Lehtonen, 1961 ; Perttunen, 1961 ; Williamson, 1951a) and the intertidal sand beetle Thinopinus pictus Leconte (Craig, 1970) preferred more humid habitats in choice experiments.
It is a common observation that clean and also fairly coarse sands on intertidal sand banks can drain and become appreciably dry as the tide recedes. There are passing references to Nereis, Arenicola and amphipods finding dificulty in burrowing under these conditions (Maxwell, 1897, p. 277; Chapman and Newell, 1947, p. 448; Chapman, 1949, p. 136; Croker, 1967, p. 187), but no detailed studies.
Most intertidal animals live under stones, in crevices or within sedi- ments. They may either live there all the time or retire there as the tide falls. Onemight expect, therefore, that if their distribution is determined by their light responses, the former would be photonegative both
FIQ. 1. The light reactions of Littorina neritoides in sea water. Animals move away from light except when upside down. Thin arrows indicate direction of movement. (From Fraenkel, 1927.)
in and out of water, and the latter photonegative when exposed but indifferent or even photopositive when immersed. Few workers have considered these points. Chitons, littorinids and isopods are photo- negative in air (Mitsukuri 1901; Evans 1951; Perttunen, 1961; Croker, 1967) but their responses were not recorded under water, while gammarids, isopods and polychaetes are photonegative under water but their responses were not tested when out of water (Herter, 1926; Wolsky and Huxley, 1932; Clark, 1956; Jansson and Kallander, 1968).
There are a number of fairly detailed studies on the light reactions of intertidal animals. Littorim neritoides (L.) is photonegative under water, except when upside down when it moves towards light (Fig. 1) while if exposed it is consistently photonegative (Fraenkel, 1927). These observations help to explain why L. neritoides is found in crevices towards high water. It moves into and then out of crevices under
HABITAT SELEOTION BY AQUATIO INVERTEBRATES 275
water, and, since it is geonegative, also moves upwards. As it emerges, or as the tide falls, it will be trapped by its photonegative responses in the fist crevice that it encounters. Similar observations for three other species of Littorina have been recorded by Gowanloch and Hayes (1 927). The amphipod Talitrus saltator (Montagu) lives during the day in burrows at about high tide mark. At night it moves out over the sands surface as the tide falls, sometimes to below mid-tide level (c.f. Holmes, 1901). From his observations on its behaviour Williamson (1961b) felt that form vision of sand dunes or hillocks might account for the species movements, and in subsequent experiments he demon- strated how Talitrus moved towards the angle formed by a dark object on a flat surface. He suggested that other intertidal amphipods might react in the same way. A related amphipod, Orchestia agilis S . I. Smith, has equally well defined light responses (Holmes, 1901). During daylight when the tide is down i t hides under seaweed. If removed it is at first photonegative, but soon becomes photopositive; under water it is strongly photonegative. These responses can be repeated under laboratory conditions. The interpretation of Holmes results is, however, difficult. Perhaps animals disturbed from their seaweed hide are at first photonegative in an attempt to return there, but if after a certain length of time they are unsuccessful they become photopositive, and so, since the sea is brighter than the land, move towards the waters edge. Once in water, being strongly photonegative, they will swim to the bottom. Corophiunz volutator (Pallas), a burrowing amphi- pod, also has distinctive light responses. It is photopositive when swimming, photonegative when walking over a surfaae out of water, and burrows more readily in the light than in darkness (Meadows and Reid, 1966; Meadows, 1967; Barnes et al., 1969). These responses ensure that animals will move towards the water line both down the shore, and up from the sublittoral zone, and will burrow in the brighter light of shallower waters. Finally, it should be noted that light appears to play a significant part in setting the cyclical rhythms of swimming behaviour that enable certain Crustacea to maintain their position on the shore (Enright, 1963; Fincham, 1970; Jones and Naylor, 1970).
The particle size of sediments on the shore varies from gravel to fine mud, often doing so within a few metres, and it is obvious even from a passing glance that the distribution of a number of species on the shore is influenced by these substrates. What evidence there is suggests that this is caused by animals preferring sediments of certain particle sizes (Wieser, 1956; Teal, 1968; Meadows, 1 9 6 4 ~ ; Croker, 1967; Sameoto, 1969; Jones, 1970; Phillips, 1971). Only Wieser has attempted to explain particle size preferences in terms of their relevance to the
276 P. s. MEADOWS AND J. r. CAMPBELL
animals biology. The cumacean Cumella vulgaris Hart prefers two size ranges : (a) under 150 pm (unsieved) in which it feeds as a deposit feeder on fine organic debris; and (b) 150-300 pm in which it feeds as an epistrate feeder scraping material from the surface of individual sand grains. There are no published investigations of animals from other phyla, although unpublished experiments by Meadows, Tevendale and Thompson show that the polychaete Nereis prefers finer sands as it moves through sediments.
Lagoon sands, and this presumably applies to intertidal sands as well, vary in volume of capillary water they take up (Webb, 1958b). The h e r the sand, the more water it holds until at below 200 pm quick- sands form; furthermore, mixtures of different particle sizes have a lower porosity than either size separately. In a later paper Webb (1969) directed his attention to the different ways in which sand grains can pack together. During compression from loose packing to close packing, the geometry of the lattice that the particles form moves through three phases, changing abruptly from one to the next. Webb (1969) has begun to analyse how animals that live in sand respond to these characteristics and the results are promising. More recently, Morgan (1970), although he does not refer to Webbs papers, has attempted to analyse how similar parameters affect the particle size preferences of the amphipod Pectenogammarw planicrurus Reid. He argues convincingly that the particular grade of sand preferred by Pectenogammarus is determined by the size of the throats connecting the voids between sand particles; in smaller grain sizes the throats are also smaller and the animals cannot enter or move through these. In fact it would appear that the maximum diameters of the animals compare closely with the calculated diameters of the throats of the samples they select.
There are a number of other intertidal variables that are less obvious but nevertheless may prove significant to animals as they select habitats on beaches.
The depth of sand over rock, mud, or gr...