[advances in marine biology] advances in marine biology volume 10 volume 10 || habitat selection by...

Adv. mar. Biot., Vol. 10, 1972, pp. 271-382

I. 11.

III. IV.

V. VI.

VII. VIII.

IX. X.

XI. XII.

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.

271

272 P. 5. MEADOWS AND J. I. CAMPBELL

The restriction of a species to localized habitats within its geographical 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 controlled 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

HABITAT SELECTION BY AQUATIU INVERTEBRATES 273

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 summer’s day tide pool temperatures are likely, even in temperate climates, to reach 3O-4OoC, while during cold winter spells temperatures may fall below 0°C. 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 ;


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 sediments. 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

n r

‘6 Light

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 photonegative 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 sand’s 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 demonstrated 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 water’s edge. Once in water, being strongly photonegative, they will swim to the bottom. Corophiunz volutator (Pallas), a burrowing amphipod, 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

animal’s 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 Webb’s 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 gravel varies on different parts of a shore, and Chapman and Newell (1949) concluded from an ecological survey that this was the main factor governing the distribution of Arenicola marina (L.) on a muddy shore at Whitstable. That this might be so had, however, been shown experimentally long before by Reid (1929). In the laboratory Arenicota would not burrow into sand containing 2% ferric oxide; if the sand containing ferric oxide was covered by ordinary sand, animals burrowed down to the ferric oxide layer and then burrowed horizontally. Similar results were obtained by using CaCO,, MgCO,, Kaolin, clay or kieselguhr. Reid‘s general conclusion was that sub-surface layers of sand whiah were

IIABITAT SELEUTXON BY AQUATIU INVERTEBRATES 277

in any way unpleasant to Arenicola stopped it from burrowing deeper. Experiments designed to test whether other animals can select particular sediment depths are in principle fairly straightforward, but apart from Reid’s work have only been attempted by Meadows (1964b). Corophium volutator does not occur on muddy beaches if the mud is shallower than about 1 cm, and in multi-choice experiments it avoids sediments that are as shallow as this. It does not, however, distinguish between 2, 5 and 9 cm deep muds and this agrees with its field distribution. Meadows calculated that Corophium probably avoids shallow sediments because it finds difficulty in constructing or maintaining its U-shaped burrow in them.

Thixotropic sands become liquid on agitation and firm again on standing, while dilatant sands firm on pressure-noticeable as a light area around one’s footpr intand soften again once the pressure is removed. Both occur on intertidal beaches (Chapman, 1949). The changes in thixotropy and dilatancy associated with differing grades of sediment (Webb, 1958b) are likely to affect habitat selection (Craig, 1970), particularly in view of Chapman and Newell’s (1947) observation that Arenicola utilized the thixotropic properties of the sediment as it was burrowing. The sand crab Emerita analoqa (Stimpson) responds to changes in sand fluidity of this sort (Cubit, 1969). The lower and upper edges of the tide’s wash zone are bounded by bands of sand made fluid by water movement. Emerita is retained between these two bands because it burrows out of fluid sands and into f%m sand, and so moves up and down the beach held by the edges of the advancing and receding tide. Similar behavioural adaptations may account for the tidal migration of some species of bivalves (Mori, 1938; Ansell and Trevallion, 1969) and for the intertidal distribution of the isopod Eurydice pulchra Leach (Jones and Naylor, 1970).

Since beaches slope towards the sea, a gravity sense should enable animals to locate themselves on the shore. Those species that have been studied show gravity responses of this sort (Fraenkel, 1927; Gowanloch and Hayes, 1927; Barnes, 1932; Carriker, 1957; Newell, 1958b), and it is probably a widespread attribute of intertidal animals. The changes in response to gravity that occur as animals become immersed, or move from wet to dry sand, will also help in the maintenance of position in the intertidal zone. Nassarius obsoletus (Say) is geonegative under water but geopositive in air (Crisp, 1969), Lepihchitona cinerea (L.) is indifferent to gravity in water but geopositive in air (Evans, 1951), and the isopod Tylos punctatus is geonegative on wet sand and geopositive on dry sand (Hamner et al., 1968)”.

The pressure around an intertidal animal living towards low water

* See note added in proof on page 493.


will fluctuate between atmospheric as the advancing tide covers it, up to about 0.4 atm above atmospheric in a 4 m high tide. Animals that swim when covered by the tide must therefore swim downwards as the tide advances and upwards as the tide recedes if they are to maintain their position, and these changes in swimming behaviour as the tide rises and falls appear to be, in part at least, dependent on pressure responses. Corophium volutator has a tidal rhythm of swimming activity which persists in the laboratory for three days, and the rhythm can be experimentally entrained by cyclical pressure changes of tidal amplitude and frequency. Animals swim most actively at the beginning of the ebb tide, and this agrees with their increased swimming activity following pressure decrease in the laboratory (Morgan, 1965). The pycnogonid Nymphon gracile Leach, which lives under stones near low water, responds in a similar way by swimming more actively if the pressure is reduced, and, if exposed to cyclical pressure changes of approximately tidal range, swims most actively during late ebb and low water (Morgan et al., 1964). These authors’ approach could well be extended to other species; we wonder, for instance, how animals that live at the top of the intertidal zone might respond when compared to Corophiurn which lives over a wide range of shore levels and to Nymphon which lives at low water. Other investigations on intertidal animals include those of Enright (1962) on various intertidal Crustacea, of Rice (1964), on Nymphon and Capella, and of Fincham (1972) on Marinogammarw, although these authors did not expose their animals to artificial pressure cycles and their approach is rather more physiological. The general phenomenon of the rhythmic activity shown by a number of intertidal Crustacsa, aswell as by fish, which willundoubtedly affect the localized distribution of these species, has been discussed by Rodriguez and Naylor (1972), and their paper should be referred to for further details.

As the tide falls and rises over mud flats and sand banks, horizontal water currents are generated, the speed of which depends on the local topography and slope of the beach, and on the tidal range. In order to remain in the same position in these circumstances, animals which make excursions into the overlying water, besides detecting changes in pressure (see above), should be capable of detecting current flow. Marinogammarus marinus (Leach) (Fincham, 1972) and Corophium volutator (Meadows, unpublished observations) show responses of this sort being rheopositive, while Chiton tuberculatus L. an the other hand is rheonegative (Arey and Crozier, 1919).

Anaerobic conditions often exist under large stones or rocks on a gravel shore and also a little way below the surface of muddy sediments.

HABITAT SELECTION BY AQUATIC INVERTEBRATES 279

It is clear that few animals would choose this sort of environment unless they made some attempt to ameliorate it. Many animals that live in anaerobic mud bring oxygenated water down to them from the surface -bivalves use their siphons for instance and others such as Arenicola marina and Corophium volutator ventilate their burrows with water. These examples can hardly be regarded as habitat selection, for the animals are locally modifying their environment to suit their needs. There appears to be only one instance of a species actually preferring a deoxygenated habitat under experimental conditions. Corophiurn votutator prefers both deoxygenated sediments (Meadows, 1964a) and deoxygenated water (Gamble, 1971), and its respiratory physiology would clearly be of interest. In other species, animals always prefer the more oxygenated habitat offered (Corophium arenarium Crawford (Meadows, 1964a ; Gamble, 1971) ; Gammarus oceanicus Segerstrsle (Cook and Boyd, 1965); D q h n i a magna, (Ganning and Wulff, 1966) ; Gammarus pulex (Costa, 1967)). Cook and Boyd’s experiments, however, should be treated with some caution because they were conducted with only five male animals, and also because under natural conditions on the shore the species is found in the anaerobic conditions that it avoids in the laboratory.

Many intertidal animals must have behaviour patterns that can be classified as thigmotactic but we know little of them (Russell-Hunter, 1949), and the same is true of responses to the micro-topography of rock surfaces, mud surfaces and so on, except that the latter are important to homing limpets (see section on homing, p. 329).

An animal is almost certainly assessing information from a number of environmental variables as it selects a suitable habitat on the shore, and occasionally workers have taken account of this (Evans, 1951; Crisp, 1969). Perhaps the most complete picture for any species com es from studies on the intertidal amphipod Corophium volutator by Gamble, McLusky, Meadow8 and Morgan. Corophium lives in U-shaped tubes on intertidal mud flats often in or at the mouths of estuaries. It is found in salinities above 2%,, breeds at above 7 ~ 5 % ~ (McLusky, 1968) and will survive in the laboratory at above 2%, (McLusky, 1967). In preference experiments it chooses 10-30%, sea water (McLusky, 1970). McLusky (1968) suggests that where the salinity is above about 6%,, abundance and distribution are controlled by the nature of the substrate, and his suggestion is confirmed by the results of laboratory experiments. C. volutator prefers fine to coarse grained sands and lives slightly longer in them (Meadows, 1964c; Meadows, 1967); it avoids very shallow sediments (Meadows, 1964b), is influenced by the nature of the microbial fauna in the sediment (Meadows, 1964a), prefers deoxygenated sediments and sea water (Meadows, 1964c; Gamble, 1971) and is photo-

280 P. S. MEADOWS AND J. I. CAMI'BELL

positive in water and photonegative and geopositive in air (Meadows and Reid, 1966; Barnes et al., 1969). Small animals differ from large ones when selecting substrates ; they burrow more readily and are less likely to leave their burrows (Meadows and Reid, 1966; Meadows, 1967). Corophium is also gregarious (Meadows, 1964b and unpublished observations) and is sensitive to pressure changes. Animals sometimes leave their burrows when covered by the rising tide (Vader, 1964), although they are most likely to do so after high tide, as the tide and pressure begin to fall (Morgan, 1965). We see from this, that although it is usually necessary to study one variable at a time in experiments, if we are to understand how a species' behaviour determines its distribution, many variables must be tested in turn. Having undertaken a series of experiments of this sort, one should then consider how the variables interact with each other to alter behaviour; are swimming Corophium, for instance, always photopositive at all salinities? We know very little of these interactions, although they could be investigated by suitably designed factorial experiments (c.f. LaRow, 1970 ; Gale, 1971).

The intertidal environment, therefore, is a fluctuating one, where animals have to react to a number of variables that alter quickly. What work there is suggests that intertidal species utilize information from many of these variables. Perhaps the most important area for future study is in a detailed approach to other intertidal species similar to that adopted by Gamble, McLusky, Meadows and Morgan. More information about the way intertidal animals respond to fluctuations of, say, pressure or humidity or immersion and emersion would also be useful, because it would help in understanding the way in which many species stay at one level on the shore as the environment fluctuates around them.

B. Marine animals The marine environment is very large in comparison to the inter-

tidal zone, and is usually a great deal more uniform at least over horizontal distances of a mile or so. However with increasing depth, light intensity and pressure change rapidly (Nicol, 1967, p. 19, 22). We shall therefore consider firstly light and pressure responses, and then outline what little is known of the detection of salinity differences, of gravity, and of sediment depth and particle size.

There are many detailed studies on the light responses of marine invertebrates (c.f. Mast, 1911). In his comprehensive review of the light responses of larvae of 141 species of benthic marine invertebrates, Thorson (1964) states that 82% are photopositive, 12% indifferent and 6% photonegative during early larval life. As the larvae approach


settlement they become photonegative, except for the larvae of intertidal species which remain photopositive until they stop swimming. This latter observation would in itself account for the intertidal settlement of many species. Strong light intensities, increased temperature and reduced salinity induce some photopositive larvae to change their response to a photonegative one, which would explain why few pelagic larvae are found in brackish waters and why larvae are often not quite a t the water surface (Thorson, 1964). The literature on invertebrates that are planktonic during the whole of their life is less massive, presumably because they are more difficult to catch and keep (Lewis, 1959). Russell (1927, 1936), Spooner (1933) and Cushing (1951) have reviewed the light responses of planktonic organisms and it seems that light is a major determinant of vertical migration. In comparison, not a great deal is known of the light responses of benthic marine invertebrates (Jennings, 1907; Bauer, 1913; Allee, 1927; Oviatt, 1969; Salazar, 1970).

Benthic and, to a lesser extent, intertidal invertebrates are now known to undertake horizontal migrations of various magnitudes (Allen, 1966). The behavioural mechanisms governing these migrations are not understood, although the persistent rhythmic activity of the shore crab Carcinus maenas (L.) may well be related to its tidal migrations (Naylor, 1958, 1962). Experimental analysis of these horizontal migrations is likely to show that they are largely controlled by light, pressure and temperature, in the same way as light and pressure govern the vertical migrations of planktonic invertebrates.

Evidence shows that planktonic invertebrates are likely to migrate vertically and maintain their position in the water column using pressure as well as light as an environmental clue (Russell, 1927, 1936; Knight-Jones and Morgan, 1966). Forty-three out of 53 species of a wide range of adult and larval planktonic invertebrates investigated by Rice (1964) responded to pressure changes of 1000 millibars or less. Increased pressure stimulated them to increase their activity and to move upwards, while decreased pressure had converse effects; the responses will obviously limit those species that show them to well defined depths. It is probable that the larvae of many bottom-dwelling invertebrates, on the approach of settlement may alter their behaviour to pressure in the same way as they do to light; older larvae of Mytilus edulis L., for example, are less likely to swim upwards on increased pressure until at the pediveliger stage (settling stage) they are unaffected (Bayne, 1963); there appear to be no comparative studies on other larvae. Little attention has been paid to the way in which pressure might interact with other environmental variables to influence habitat

282 P. 9. MEADOWS AND J. I. UAMPBELL

selection. Bohn (1912), for instance, observed how lobster larvae, which were normally photonegative, became photopositive when the pressure was increased and how, as they aged, the effect waned. Knight-Jones and Morgan (1966, p. 268) quote other examples. In general, they visualize the response of planktonic animals to pressure and its relation to depth regulationand vertical migration “ as involving accommodation to gradual changes of limited range, until the pressure builds up sufficiently to evoke a long-sustained compensatory swimming. This would provide an oscillatory feedback mechanism which probably helps, not only in setting bounds to the vertical migrations of planktonic animals, but also in maintaining their cyclical activity’’ (loc. cit. p. 278). As they point out, pressure is unlikely to be the only variable involved, since cyclic behaviour continues in shallow laboratory tanks (Harris, 1963), and we have already drawn attention to the probable interactions between pressure and light. We are not aware of any investigations of the influence of pressure on benthic marine invertebrates although intertidal invertebrates are known to respond to pressure.

We have seen that planktonic larvae of benthic animals respond to light and pressure so as to maintain themselves well above the bottom, and in this way they are dispersed from place to place by water currents. Their responses to gravity effect the same end, as during most of their planktonic life they are geonegative as well as photopositive (Loeb, 1893; Bayne, 1964) or geonegative only if they have no light receptors (Lyon, 1906 ; Grave, 1926). As settlement approaches their light and gravity responses reverse and they become geopositive and photonegative (Bayne, 1964). Amongst adult planktonic invertebrates, the copepod Centropages typicus K r ~ y e r is geonegative as well as being photopositive (Johnson and Raymont, 1939). We are not aware of other studies on adult planktonic invertebrates. The few benthic invertebrates investigated appear to be geonegative (a nudibranch, Crozier and Arey, 1919; various starfish, Crozier, 1935 for references) but only Crozier and Arey have attempted to link the behaviour with the species’ distribntion.

Various species of planktonic animals and larvae stop swimming upwards (Lance, 1962 ; Lyster, 1965) or become photonegative (Loeb, 1893; Rose, 1925, p. 465) when they meet layers of less saline water and the adaptive advantage of this at the mouths of estuaries is obvious. There are no comparative studies on bottom-dwelling animals although simple methods have been described (Jansson, 1962 ; McLusky, 1970) which offer animals a horizontal rather than a vertical salinity gradient, and these could be modified to accommodate animals of differing sizes and to allow animals contact with a suitable substrate as they made their choice. An interesting variant of the vertical salinity gradient


has been adapted by Harder (1968) to study the behaviour of marine plankton towards density discontinuities. After testing a range of species he concluded that almost all of them aggregated at the interface between waters of Werent densities, and cites instances of this occurring in the sea. More recently, localized discontinuities in the microstructure of temperature, salinity, and velocity profiles in the sea and of temperature profiles in fresh waters have been described (Simp- son and Woods (1970), Woods (1971), for references) and may influence planktonic animals in the same way.

As far as we are aware little is known of the temperature preferences or current responses of marine planktonic or benthic invertebrates, apart from studies on the relation of temperature to light preferences in three species of planktonic copepod (Lewis, 1959), on the relation of temperature to the burrowing activity of two Penaeus species (Aldrich et al., 1968; p. 345 below), and on the rheotropic responses of a shallow water nudibranch (Chromodoris zebra Heilprin) (Crozier and Arey, 19 19).

Except under unusual conditions such as the aftermath of a plankton bloom, anaerobic conditions are rare in the sea, and there is no record of planktonic animals responding to them. On the other hand they must be common in sublittoral sediments although there are no studies of their possible significance to benthic invertebrates. Many benthic invertebrates must also respond positively to touching or being surrounded by solid objects, but again little appears to be known of this behaviour or of any responses to the microtopography or roughness of surfaces (Diebschlag, 1938).

Many mobile bottom-dwelling invertebrates, such as brittle stars, octopods, crabs, and lobsters, seek shelter on the approach of predators, or live semi-permanently in crevices or dens. This behaviour, which is well known to divers, has only been experimentally analysed in two species of crayfish. Nonaka (1966) and Cobb (1971) have shown that the number and size of shelters, and their relative dimensions, are likely to influence the local distribution of Panulirus jarponicus von Siebold and Homarus arnericunus Milne Edwards respectively.

It is well known that benthic marine invertebrates in mud and sand burrow to different depths-the various burrowing bivalves are good examples-but there are no experimental studies that attempt to link possible depth preferences with distribution.

Pravdi6 (1970) has recently described a new parameter by which sediments may be classified. He has designed an apparatus to measure the electrical charge at the surface of sediments, and has investigated the changes in charge as salinity varies. All sediments were negatively charged in sea water while most of them were positively charged in fresh water. Charge reversal occurred between 2 and 6%, salinity. It would be


interesting to know whether small invertebrates that burrow into sediments, particularly those living in estuaries, respond to these changes.

Sediments in the sea differ from place to place, sometimes over as short distances as in the intertidal zone (Fleming and Stride, 1967; Krumbein, 1971) and are of great importance in animal distribution (Holme, 1950). The finest and coarsest sediments tend to contain the greatest proportion of specialized forms, while the finest sediments are richest both in numbers of species and number of animals (Davis, 1923, 1925). Surprisingly, in contrast to the intertidal environment the results of ecological surveys have not often been followed by experimental work on habitat preferences. Williams (1958) has offered three species of burrowing prawns a choice of beach sand, shell sand, muddy sand, sandy mud and loose peat in a long tank. There were interspecific differences, for Penaeus duorarum Burkenroad preferred the shell sand, while P. aztecus Ives and P. setiferus (L.) were found most frequently in the muddy sand, sandy mud and loose peat. Williams states that his results agree well with the species sublittoral distribution obtained from trawling. The gastropods, Aporrhais pes-pelecuni (L.) and A . serresiana (Noh.), are specialized for burrowing respectively into muddy gravel at shallow, and into soft mud at greater, depths. When the former is placed on soft mud it flounders and becomes clogged; the latter was unable to " shoulder " its way through muddy gravel (Yonge, 1937). The hairy snail, Trichotropis cancellata Hinds, on the other hand, demands a firm substratum for locomotion and clear water for ciliary feeding; even on mixed shell gravel and mud movement was found to be greatly hampered (Yonge, 1962).

The most detailed study to date is on Branchiostoma nigeriense Webb from Lagos Lagoon, Nigeria (Webb, 1958a; Webb and Hill, 1958). In a series of experiments Webb and Hill linked the ecological distribution of the species with its survival in Werent grades of sediment, and these in turn with its substrate preferences. The sand from the natural habitat of Branchiostorna has a wide grain size range with a maximum in the 300-200 pm band and contains less than 25% very fine grains (under 200 pm) and less than 16% silt. The results of 24-h survival experiments are as follows : in 2 000-600 pm sand animals were active and swam strongly when touched ; in the 600-300 pm and 300-200 pm ranges animals sometimes burrowed so that the oral end projected above the surface; in the 200-180 pm and the 180-100 pm ranges animals did not respond readily to touch and little attempt was made to burrow, in addition to which in the 180-100 pm range the animals were moribund and their oral apertures became blocked with small sand grains and mucus. In choice experiments the 300-200 pm range was preferred to others and this agrees with the main particle


size group of their natural sand. Animals avoid the coarse sands and the survival experiments show that they will rapidly swim away from these; they avoid the finest sand and silt, and the survival experiments show how they will die if they remain on or in them. Other experiments illustrate that animals in the most suitable sand may well remain in the same position for days. The detrimental effect of very fine sands is borne out by experiments in which either the fraction under 200 pm or the silt fraction was removed from natural sand whereupon it became considerably more attractive than before. By adding more fine sand or silt the natural sand became concomitantly less attractive. Webb and Hill (1958) conclude that Branchiostoma is found in its typical sand because (a) it finds it easier to burrow in 200-300 pm sand as opposed to coarse sand, (b) the sand is the correct size for the functioning of the branchiae, and (c) animals that attempt to burrow in finer sands do not do so completely and so are easily disturbed by any tactile stimulation. As with the intertidal environment, we know very little about the influence on habitat selection of the changing porosity and packing that occur as particle size changes (Webb, 1958b, 1969).

To summarize, there is in general less evidence for habitat selection by marine invertebrates than there is for intertidal forms. The reasons for this must partly be ones of manpower, although the difficulties of collecting and maintaining planktonic and benthic marine animals may dissuade many workers. We saw how there were many well documented instances of the light and pressure responses of larval planktonic invertebrates and some evidence for adult planktonic invertebrates. But when we turned to other variables, such as sediment characteristics, currents, salinity and gravity, to which animals must respond as they select habitats, we found the evidence scattered, often fragmentary, and for benthic animals almost non-existent. Further investigation would also be profitable on the responses of planktonic species to discontinuities of density and temperature (Harder, 1968) and on the responses of benthic species to the surface charge of sediments (Pravdid, 1970). When considering the intertidal environment we commented on the very few attempts to integrate the various factors that govern habitat selection in any one species ; there are none for sublittoral invertebrates. Clearly the sublittoral marine environment offers considerable potential, particularly for those who can combine experimental studies in the laboratory with observations and experiments on the behaviour of animals under natural conditions in the sea. Since the results are likely to be of direct application to the management of commercial fisheries, to pollution

286 P. 9. MEADOWS AND J. I. ULLMPBELL

and to fish farming, perhaps these are research fields that might interest applied institutions such as fisheries laboratories.

C. Preshwater animals Fresh waters may range from temporary ponds of under a metre in

depth that dry out in hot weather, to deep and stable oligotrophic and eutrophic lakes, and from steep fast mountain streams to flat slow rivers. The water may be saturated with oxygen, as in a stream, or may be anaerobic in the hypolimnion of a rich eutrophic lake during summer. Temperatures may vary widely especially in fairly stagnant waters, and here marked annual and diurnal fluctuations are well known. Once the thermocline is established in eutrophic lakes during the spring, temperatures may change 10°C or more within a few metres vertically. Wide variations also occur in the nature of the bottom: boulders and gravel in fast-moving streams, sand and mud banks in slower rivers, peat bottoms in acid bog pools, and rich muds with decaying organic matter, algae, and higher plants in lakes and ponds. The concentrations of inorganic ions and of organic materials vary with the type of water ; they are low in the soft waters of some glacial lakes and high in the richer eutrophic ones ; their relative concentrations also differ from place to place and throughout the year (Mortimer, 1942).

Conditions in fresh waters therefore vary widely, and so it follows that invertebrates living in fresh waters will have to respond to many of these variations in order to find and remain in their preferred habitat. It is likely that animals will use information from water movements, anaerobic conditions, salt and organic concentrations and so on, as well as variables that fresh water shares with the sea, such as temperature, pressure, light, and the nature of the bottom. Let us consider these.

Many animals that live at the bottom of streams and rivers move into the current-are rheopositive-and have clear preferences for particular current velocities when tested experimentally. The isopod Asellus communis Say is common in small streams with rapids and is also found less frequently in larger streams and in lakes (Allee, 1912, 1914) ; in all these environments it must have abundant places to cling to (Allee, 1912). In laboratory tests it swims into the current at low to medium current speeds ; however as current speed is increased it clings to the substrate a t a speed less than the speed common in the parts of the river where the species is normally found. From these observations Allee (1914) concludes that the distribution of Asellus communis in streams cannot be accounted for by its rheotactic response alone,

HABITAT SELECTION BY AQUATIa INVERTEBRATES 287

but by interacting positive rheotaxis and positive thigmotaxis (clinging). The current responses of various insect nymphs and larvae have been investigated by Edington (1968), Madsen (1969) and in great detail by Ambuhl (1959). Edington placed baffles into a small stream which locally reduced the current flow ; this induced the larvae of the caddis fly Hydropsyche instabilis (Curtis) to move to where the current was faster. Ecological experiments of a similar nature are simple and are likely to be very informative, so it is surprising that they have not been undertaken more frequently. The wide range of insect nymphs and larvae tested by Ambiihl fell into three groups, those that avoided a strong current, those that preferred it, and those that behaved indifferently. With Allee (1914) he felt that the results of his experiments did not strictly accord with the ecology of the species although they did illustrate the importance of a single factor. We know less of the current responses of other invertebrates. The leech Dina microstoma Moore is strongly rheopositive (Gee, 1913) but little attempt was made to link this to its normal environment (c.f. Herter, 1928). Allen (1923) and Bovbjerg (1962a) suggested that natural aggregations of stream-dwelling bivalves and a snail, respectively, might be related to current responses and Bovbjerg presented evidence in support of this. How do the current responses of stream-dwelling forms differ from those of forms that live in lakes and ponds? Stream forms show abnormal behaviour in still water (Madsen, 1969), but there is more detailed evidence than this. Firstly, Allee (1912) compared the current responses of AseZZu communis collected from streams with those collected from ponds, and found that a higher proportion of the former were rheopositive. In passing, it would be interesting to know whether these results could be repeated with animals from the same field population that had been kept in the laboratory either in still water or in a suitable current for some while previously. Secondly, in a comparison of the responses of two crayfishes, Bovbjergh (1962b) showed how the stream-dwelling species Orconectes propinquus (Girard) maintained its position in currents more successfully than did the pond-dwelling form Cambarus fodiens (Cottle). In an analogous study by Edington (1968), the net-spinning larvae of the caddis fly Hydropsyche instabilis which are found in exposed sites in rapids, built their nets more easily at high current speeds than did the larvae of Plectrocnemia conspersa (Curtis), a species that is characteristic of more sheltered sites. The current responses of stream-dwelling forms, therefore, are well adapted to their own environment and seem to play an important role in habitat selection.

Anaerobic conditions appear to inhence habitat selection in one of

288 P. S, MEADOWS AND J. I. OAMPBELL

two ways. Animals may react to them indirectly, by a change in a pattern of behaviour, or may respond more directly by an avoidance reaction. As an example of the former, consider the behaviour of a photonegative planktonic animal moving down during the day from the surface waters of a rich eutrophic lake. If it continues to swim downwards, in the summer at least, it will eventually encounter unfavourable anaerobic conditions. It can avoid these however by becoming photopositive as soon as it meets them; the animal will then immediately move upwards again. There is evidence from laboratory investigations that switches in behaviour of this sort can occur. Carbon dioxide induces normally photonegative Gammurus, Daphnia and Cyclops, and mayfly nymphs to move towards a light source (Loeb, 1904, 1906a, b ; Wodsedalek, 191 l), although these animals may be responding to lowered pH since acids produced similar effects. Allee (1912) noted a change in the behaviour of Asellus in lowered oxygen or increased carbon dioxide concentrations ; stream forms became less rheopositive, and also preferred water of high oxygen content if they had previously lived in this. Other freshwater crustaceans react directly to anaerobic conditions, showing marked preferences for water containing low carbon dioxide concentrations : the sensitivity of four Cambarus species studied by Powers (1914) mirrored their ecological distribution, the stream species being more sensitive than the pond or mud dwelling ones. However these preferences might well be for pH rather than anaerobic conditions as the crayfish showed similar behaviour in response to acetic and hydrochloric acids. Analogous behaviour has also been noted by Allee and Stein (1918) for mayfly nymphs. These problems clearly need reinvestigation in which the effects of anaerobiosis, pH, and inorganic ions are distinguished (Costa, 1967a, b). In a well designed factorial experiment, LaRow (1970) has studied the influence of reduced oxygen tension, of temperature changes and also of the presence or absence of food on the vertical migration of Chaoborus punctipennis Say larvae (Diptera : Culicidae). These larvae emerge from sediments shortly after sunset, migrate into the upper water strata, then descend and burrow again before sunrise. Under experimental conditions the larvae only migrate upwards in low oxygen concentrations, although the degree of migration is influenced quantitatively by temperature and food.

Temperature, light and pressure are environmental variables that fresh waters and the sea share in common, and many animals in fresh water are known to respond to them.

Temperature, like anaerobic conditions, might affect habitat selection indirectly as well as directly through temperature preferences,


and so we can argue, in the same way as when considering anaerobic conditions, that it might be advantageous for planktonic animals which shun the very bright surface layers to become photopositive if they pass across the thermocline. There is no clear evidence of this however ; in fact the hemipteran Ranatra fusca P.B., although hardly planktonic, shows exactly the opposite response (Holmes, 1905), but so do Volvox and Pandorina colonies and they are planktonic (Mast, 1919). The only investigations on preferred temperatures we know of are by McGinnis (191 1) on Branchipus (= Eubranchipus) serratus Forbes, by Ackefors and Rosen (1970) on Podon polyphemoides Leuckart (Cladocera) by Costa ( 1966b) on Caridina pristis Roux and C. simoni Bouvier (Atyidae, Decapoda), and by Gebczyhski (1965) who demonstrated species differences in the preferences of the snails Planorbis corneus rubra L. (17-19 "C) and Limnea stagnalis L. (12-13 "C) which agreed with their usual habitats.

Many planktonic Crustacea (Yerkes, 1899, 1900; Towle, 1900; Loeb, 1906a, b; Dice, 1914) and some other planktonic animals (Mast, 1919 ; Pause, 1919) are photopositive. Hutchinson (1967, chapter 25) reviews these responses in detail. Siebeck (1968), in a comprehensive paper, presents evidence that planktonic Crustacea avoid the shore by a horizontal migration because the shore looks dark. Migration is particularly noticeable when the horizon is hilly or has a high elevation. His elegant apparatus could easily be adapted for marine use. The light responses of planktonic animals in fresh water are therefore likely to play a large part in maintaining them at the water surface and away from the shore line. In the sea, many planktonic larvae are photopositive during their early life and then photonegative as settlement and metamorphosis approaches, and in this way species are dispersed. The only example of a similar behaviour in fresh water is of Chironomus gregarius (= C . thummi Kieffer) larvae (Pause, 1919). It would be worth while examining the planktonic larvae of the bivalve mollusc Dreissena polymorpha (Pallas).

As one might expect, animals that live on the bottom of lakes and rivers are usually photonegative. The following groups have been studied : planarians (Loeb, 1894; Hesse, 1897 ; Parker and Burnett, 1900; Ullyott, 1936a, b), gastropods (Walter, 1906), bivalves (Allen, 1923), leeches (Gee, 1913), amphipods (Holmes, 1901; Loeb, 1904; Wolsky and Huxley, 1932), isopods (Banta, 1910; Janzer and Ludwig, 1952), mayfly and dragonfly nymphs (Wodsedalek, 1911; Curtis Riley, 1912; Allee and Stein, 1918; Hughes, 1966), chironomid larvea (McLach- Ian, 1969), caddis fly larvae (Lehmann, 1972). On the other hand, species that are found on lighter parts of the bottom, on a sunlit gravel

290 P. 8. MEADOWS AND J. I. OAMPBELL

bed for instance, are photopositive (Holmes, 1905; Allee and Stein, 1918; Hughes, 1966), although this relationship is not always as clear as one might hope, presumably because of confusion by other environmental variables. Some bottom living animals are also influenced by the shade or colour of their background (Brown, 1939; Popham, 1941) while

TABLE Ia. Selection of a substrate by its colour. The freshwater hemipteran Arctocorba dbtincta ranges in colour from light brown to dark brown, as do the bottoms of the ponds in which it lives. Animals tend to match the background of their pond. In an attempt to explain this, Popham (1941) noted the number of alightments under experimental conditions on substrates whose colours ranged from light brown to dark brown. He matched the coloura to an Ostwald colour chart (a series of graded greys containing different percentages of black). Animals alighted more often on substrates that matched their own colour.

Number of al@htrnents made by inseots whose colour wm I

colour of eubetrate dark ligh8

dark medium light

62 30 20 26 18 46

TABLE Ib. Substrate colour and its influence on the development of cuticle colour in Arctooorha dbtinota. Popham (1941) collected nymphs in their ultimate or penultimate instar, and maintained them over dark or light substrates during their moults to adulthood. At the beginning of the experiment all the nymphs were the same colour, whereas at the end of the experiment the adults matched the background over which they had moulted.

COfOUT Of &8~att?

over which the nymph Colour of adults

were maintained dark: medium leht

dark light

21 16 0 0 6 24

others take no account of it (Hughes, 1966; McLachlan, 1969). The hemipteran Arctocorisa distincta (Fieber) varies in colour from light to dark brown, and is normally found in ponds whose bottom sediments are the same colour as itself (Popham, 1941). In the laboratoryit prefers shades of background similar to its own (Table Ia), and is very restless and attempts to fly away if it does not match its background. Adults maintained for seven weeks over different coloured backgrounds retained their original colour, but nymphs from eggs laid over two different coloured backgrounds matched their respective backgrounds;

kL4l3ITAT SELEOTION BY AQUATIO INVERTEBRATES 291

furthermore penultimate and ultimate instar nymphs maintained over two different backgrounds moulted to adults that were the same colour as the background (Table Ib). A study of the shed skins and killed adults from the latter two experiments made it clear to Popham that the lighter backgrounds had in some way inhibited the process of pigmentation. There is one similar example. In the species Asellus aquaticus L., dark animals are mostly photopositive, medium coloured animals are usually photonegative, and light animals are always photonegative (Janzer and Ludwig, 1952). Popham’s and also Janzer and Ludwig’s experiments are of great importance particularly if they can be substantiated with other species. They also imply that the previous experience and previous environment of an animal population, and morphological or physiological differences between animals, can affect habitat selection. But these topics will be discussed more fully in Sections VII and VIII.

As in the sea, planktonic invertebrates are likely to maintain their position and migrate vertically in the water column using light and pressure as environmental clues. There is evidence that planktonic Crustacea respond t o gravity (McGinnis, 1911; Dice, 1914; Clarke, 1930,1932) but there appears to be no information on their pressure responses. The possible interrelationships of light, gravity and pressure responses in regulating vertical migration in fresh waters is considered in great detail by Cushing (1951) and Hutchinson (1967) and it is not proposed to discuss the matter further. One should consider, however, whether it is really possible to distinguish an animal’s response to gravity from its response to pressure in water, particularly since the latter varies very sharply with depth. There are few investigations of the gravity responses of benthic freshwater invertebrates (Walter, 1906 and Kanda, 1916b for references).

Bottom living animals in fresh waters may well prefer contact with solid objects (thigmotaxis) as well as preferring certain types of bottom such aa gravel and sand, and we will now examine these hypotheses, Mayfly and dragonfly nymphs are thigmotactic and cling to stones or plants depending on their normal habitat (Curtis Riley, 1912 ; Lyman, 1945; Wautier and PattBe, 1955), while caddis fly larvae respond in the same way to their tubes. Asellus aquaticus is strongly thigmotactic and will aggregate under a clear sheet of glass in the light part of a dish even though i t is usually photonegative (Janzer and Ludwig, 1952). These examples show that thigmotactic behaviour is likely to occur widely amongst animals living on the bottom of lakes and rivers and to be an important factor in their choice of habitat.

Freshwater invertebrates that burrow or build their tubes in sea-


ments, or that live at the sediment surface, have preferences which in general agree with their distribution. The larvae of the mayfly Hexa- genia can only burrow easily in mud-their normal environment (Lyman, 1943), while larvae of the chironomid Nilodorurn brevibucca Freeman prefer the same type of sediment to sand (McLachlan, 1969), and larvae of Chironomus riparius Meigen prefer algae to a gravellsand mixture (Edgar and Meadows, 1969). The Nilodorum larvae were much more likely to migrate from unfavourable than from favourable sediments, which is also true of the behaviour of the hemipteran Arctocorisa (Popham, 1941) and of larval chironomids (Edgar and Meadows, 1969). The preferences of mayfly (Ephemeroptera and stonefly (Plecoptera) nymphs living at the sediment surface have also been investigated, and they mirror the species usual habitats (Madsen, 1968, 1969). Analogous species differences that agree with their natural distributions have been described for two crayfish (Bovbjerg, 1952b). Finally, caddis fly larvae (Trichoptera) are very particular as to how and with what they make their cases (Hanna, 1961; Hansell, 1968), although these are perhaps rather special instances of habitat selection. In all these instances, laboratory preferences agree in general with field distribution, however this is not always true (Cummins and Lauff, 1969, 10 species of insect larvae and nymphs and a snail; Bovbjerg, 1970, two crayfish species Orconectes; Gale, 1971, a bivalve, Sphaerium; see Section VI). As in the sea, we know almost nothing of the way animals may respond to changes in thixotropy and packing of sediments (Webb, 195813, 1969) except for an interesting study by Wallace (1958) on the movement of nematodes in wet sand (see section on interstitial animals, p. 296).

The depth of sediments is likely to vary as much in fresh waters as it does in the sea, and the distribution of burrowing animals will be influenced by these variations if they avoid very shallow sediments or prefer a particular level within a deeper one. Preferences of this nature have been demonstrated experimentally. The depth to which mayfly nymphs will burrow is limited by a layer of sand below mud-their preferred sediment (Lyman, 1943), while the larvae of Chaoborus punctipennis prefer the top 3-5 cm of sediments (LaRow, 1969). LaRow’s study is interesting because it seems to be the only one in which vertical migration within a sediment has been experimentally investigated. Under continuous light Chaoborus larvae are dispersed between depths of 0-6cm during the day but also migrate slowly upwards, so that at sunset they are within 1 cm of the sediment surface. If the light is left on after this time they move slowly down again but if it is turned off, many of them become planktonic. Particu- larly noteworthy is LaRow’s conclusion that the larvae rise to the surface


at sunset and assess the light intensity before swimming upwards or burrowing deeper into the sediment again.

Freshwater animals are likely to meet more saline water if they move into a river’s tidal reaches, and as well as their positive response to water currents, an avoidance of salty water would be advantageous (Costa, 1966a). [In Finland, Lagerspetz and Lehtonen (1961) and Lagerspetz and Mattila (1961) record Asellus aquaticus from fresh waters and from the Pucus vesiculosus L. zone on the shores of the Baltic, where salinity can rise to 8%,. Individuals collected from fresh or brackish waters could not distinguish between tap water and brackish water from the Baltic (54-6*0%,), and Lagerspetz and Mattila (1961) conclude from this that localized variations in salinity caused by, say, melting ice are not likely to influence the species distribution. However, they obtained rather different results using sodium chloride. Individuals from fresh water distinguished between tap water and lo/,,,, NaC1, whereas, although those from brackish water could not make this distinction, they did prefer S%, NaCl to tap water. The problem needs further investigation on this and other species that are likely to encounter brackish waters. Lagerspetz and Lehtonen (1961) also offered Asellus from fresh water and brackish water different humidities, and individuals from both environments preferred the wetter of the two sides of a choice dish. Other freshwater animals living at the edges of rivers and lakes would be expected to avoid low humidities but there are no studies.

Occasionally authors have attempted to assess the relative importance of a range of environmental variables and their results illustrate how successful the approach can be (Bovbjerg, 1952b; Hughes, 1966; McLachlan, 1969; LaRow, 1970). Bovbjerg’s work is the most elegant of these studies He firstly considered the ecology of two crayfish species and then showed how much of their local distribution could be accounted for by their behaviour and by viability limits. Cambarus fodiens lives in small muddy ponds that are often temporary. In summer the ponds stagnate, are hot, and often dry out ; they have a low oxygen content in both summer and winter, and a low CaCO, content. Orconectes propinquw lives in clear, rock bottomed streams and in lakes. Its environment is much more stable : temperature, depth and oxygen content remain fairly constant over the year, there is no summer stagnation, and there is a high CaCO, content. In reciprocal field transplant experiments, both species survived in the other’s environment. Bovbjerg also studied their burrowing abilities. Both species were placed on mud in the field at the time of the summer drying and in the laboratory on mud without a covering of water ; in both types of experiments Cambarw fodiens burrowed immediately and

A.Y.B.--IO 11

294 P. 9. MEADOWS AND J. I. UAM2BELL

all were alive after three days, but Orconectea propinqum were not able to burrow and half of them died within the three days. Viability experiments showed similar effects; C. fodiens survived longer on desiccation and at increased temperatures than did 0. propinquus. The two species were also differentiated by their current responses- C. fodiens is able to maintain its position more successfully in fast currents, and by their substrate preferences-C. fodiens prefers mud while 0. propinquw prefers gravel. Even this excellent study, however, is not complete. We hope that Bovbjerg will eventually study the two species' temperature and humidity preferences and their responses to calcium ions.

It is clear from this survey that animals living in fresh waters use information from many physical and chemical variables when choosing their habitats. Responses to contact with solid objects (thigmotaxis), to current speed, to the nature of the bottom, and to light, are known for a number of species, but more comparative studies are needed. On the other hand very little is known of pressure responses, temperature preferences, reaction to anaerobic conditions and their relation to pH, humidity and salinity preferences, and for burrowing animals, preferences for certain depths of sediment. Finally, we would stress the lack of knowledge of the role of inorganic and organic ions in solution and of the porosity and thixotropic properties of sandy sediments, and point out the need for investigations into the way variables interact with each other to determine the most suitable habitat of a given species.

D. Interstitial animals The peculiar nature of the habit and habitat of animals that live

between sand grains in marine and freshwater sands has only recently received anything but passing comment. It is a rich new world for the taxonomist as well as for the experimental ecologist. Swedmark (1964) considers that the space between the sand grains is the most important factor determining the types and numbers of animals present. Almost as important, he feels, are the granulometric characteristics of the sands, and the continuous rearrangement that the surface layers of intertidal and inshore sands must receive from wind, wave and currents. Temperature, salinity and oxygen availability since they vary significantly from place to place will also be important (Swedmark, 1964; Enckell, 1968), as will solid/liquid interfacesb ecause animals often meet them (Faur6-Fremiet, 1950). The animals in this environment are an odd assortment representing most invertebrate phyla; they share the common Characteristics of small size, bizarre form and ability to

HABITAT SELEUTION BY AQUATIC INVERTEBRATES 295

move by one means or another in the sand interstices. Most of them are confined to the topmost 5 cm of lake beaches and the topmost 12 cm of marine beaches, while variations in their population densities in time and space are more pronounced on freshwater than on marine beaches (Pennak, 1951). FaurB-Fremiet (1950) divides the marine interstitial ciliates into the mesoporal fauna-those that live in coarse sand and which are not limited to the interstitial environment, and into the microporal fauna-those that are only found in the interstices between sand grains and are highly specialized. The distinction might profitably be applied to the invertebrate interstitial fauna.

Our knowledge of the way these organisms respond to their environment is scant, and depends almost entirely on the researches of Boaden, Gray and Jansson. What evidence there is indicates that interstitial animals use environmental clues to select their habitats in the same way as do larger aquatic invertebrates.

Boaden (1962) observed the rate at which sands of differing particle size were recolonized on an intertidal shore and concluded that the rate of recolonization depended on particle size. The study could well be extended to other interstitial habitats. In a later paper Boaden (1963) concentrated on one species, the archiannelid Trilobodrilus heideri Remane which lives near high water in moist sand and shell gravel of about 350-650 pm particle size. It is strongly photonegative, and is rheopositive in full strength sea water but unresponsive below about lo%,. The latter behaviour will keep it away from fresh waters and the former from the surface layers of sand where dry air might desiccate it. Trilobodrilus is gregarious, and periods of aggregation occur twice in each tidal cycle, a t about low and high tide. Exactly how this behaviour affects their distribution is not clear, although Boaden (1963, p. 249) has some suggestions. Gray (1965; 1966a, b, c, d) has studied various aspects of the habitat selection of another archiannelid Proto- drilus symbioticus (Giard) that also lives intertidally. It prefers 15°C in a temperature gradient of 6OG25"C but shows no salinity preference, which is surprising, and onIy a slight reaction to current. It will occur near the surface of sands as it prefers high oxygen concentrations, but not at the surface because it avoids high light intensities and high temperatures. Protodrilw symbioticus, in common with two other interstitial species, reacts to the numbers and types of micro- organisms on sand grains (Gray, 1966d, 1967, 1968), but we shall return to this subject later (p. 321).

Jansson (1962, 1967) has adopted a more comparative approach, and in a comprehensive paper has attempted to link salinity preferences with mortality limits (Jansson, 1968). Most of the species


he worked with were collected on intertidal beaches from the Baltic coast where the water is brackish. He describes (Jansson, 1967) a vertical core of sand whose sand grains had an overall mean diameter of 500 pm, but in which the means of sub-samples varied between 100 pm and 800 pm, and deduces from this that the selection of certain grades of sand by interstitial animals is likely to influence markedly their local distribution. But he then points out that a species of turbellarian which moves by ciliary creeping, and a species of oligochaete which burrows by peristaltic movement, have no significant preference for graded sand fractions over the range 74 to 1000 pm-a paradox indeed. However, he suggests that this might be due to the two species’ methods of locomotion, and quotes as evidence the clear grain size preferences of two other interstitial forms, a species of oligochaete and a species of copepod, each of which moves with a sliding type of locomotion. Further comparison with other species would be worthwhile.

Pore size and permeability in different types of sand are almost certainly of great importance to interstitial animals, and there are now available some details of the way in which they can vary (Webb, 1958b; 1969). It certainly seems that the movement of interstitial terrestrial nematodes at least is controlled by some similar factors. Wallace (1958) after detailing the physics of water movement through a sandy loam, considers how nematodes move through sand fractions of differing size and moisture content. A much greater proportion of the larvae of the beet eel worm Heterodera schuchtii Schmidt migrate through 150-500 pm sands than through 20-150 pm sands, and through sand the interstices of which are half full of water rather than through sand where the interstices are full or empty. While studying the movement of larvae in single layers of grains, he was able to show that in 75-150 pm sand many of the interstices were too small for the larvae, that in 150-250 pm sand the interstices were wide enough for the larvae to travel in straight lines, but that in 250-500 pm sand the interstices were so large that the larvae slowed down. Wallace also watched larvae moving in water films on glass and on alginate jelly. They moved fastest when the film was 2-5 pm thick, and progressively slower as the film thickness was increased to 50 pm, while they did not move at all if the film was less than 1 pm thick. The details of these latter experiments however should be treated with a little caution, as Wallace’s methods of obtaining films were approximate.

It is evident, therefore, that a great deal more work is needed before we can define the distribution of interstitial animals in terms of their behaviour. While there are many thousands of species in the interstitial environment, only one has been studied in any detail, Proto-

HABITAT SELEOTION BY AQUATIC INVERTEBRATES 297

drilus s ~ ~ b i o t i c u s , by Gray. The results published to date suggest that temperature, light, salinity, oxygen content, sand permeability, and pore size and particle size, are significant to many species, and perhaps further research should be concentrated in these areas.

111. COMMENSAL AND PARASITIC ASSOCIATIONS There are many well known examples of commensal and parasitic

associations in marine and fresh waters (Caullery, 1952) ; we shall limit ourselves to experimental studies that attempt to discover those behavioural mechanisms which promote and maintain such associations. Our examples are mostly of commensal associations, because there are few parasitic associations that have been analysed experimentally.

It seems almost stating the obvious to say that at some stage of their life history commensals and parasites will have a repertoire of responses to stimuli from the physical and chemical environment which parallels those of free-living animals. However, these responses often receive only passing reference or an aside to make clear that the author is aware of their existence. Are they only generalized environmental responses, or do they play a specific role in leading an animal to its host? Too little is known to make a generalization from facts that are available. Temperature preferences, responses to light, and reactions to current, contact and gravity, usually appear to be nothing more than one might expect of free-living species (Fasten, 1913; Davenport and Hickok, 1951; Davenport et al., 1960; Morton, 1962; Ronald, 1960). On the other hand, it is possible on occasion for preferences of this sort to aid an animal in localizing its host (freshwater leeches, Herter, 1928, 1929; marine bivalves, Gage 196613). The burrowing bivalve Montacuta substriata (Montagu) is geonegative so will stay near the sand surface where its host Spatangus purpureus 0. F. Muller lives; its close relative Montacuta ferriginosa (Montagu) is geopositive and so is likely to burrow further into sediments where it will encounter its deeper living host, Echinocardium cordatum (Pennant) (Gage, 196613). The changing light responses of the larvae of the trematode, Discocotyle sagittata Leuckart, might constitute another example (Paling, 1969).

Specific stimuli from a host to its parasite or commensal, are probably the most frequent method by which these relationships are established and maintained, and their study has occupied a number of workers. The specific stimulus from a host may take a number of forms, some of which may act in unison. There appear to be no investigations of visual recognition of a host in sea or fresh water, although no doubt instances exist. Hermit crabs are not exactly commensal


with the shells they inhabit although their selection of shells may play a part in determining their local distribution (Orians and King, 1964, p. 305); however they do provide two examples of “hos t” recognition by the physical attributes of weight and volume that might be applicable to other true commensal relationships (Reese, 1962 ; Vdker, 1968). Gilpin-Brown (1969) has described the unusual way in which Nereis fucuta (Savigny) finds its host hermit crab. He has shown that it recognizes its host’s approach by vibrations on the substrate, and then by contact with the surface of the shell (c.f. Herter, 1929, pp. 280-6). Hermit crabs utilize tactile stimuli in choosing their shells, for Clibanarius misanthropus Risso prefers shells such as Cerithium (its usual shell) and Murex that are fairly bumpy, to smoothed Cerithium shells or to BuZZa and Gibbula shells (Hertz, 1933).

By far the most popular group of specific responses to study have been those to chemicals produced by the host and this probably reflects a genuine prevalence in aquatic environments. It is clear from the literature that some commensals respond to chemicals at a distance from the host and therefore might be able to home in (Davenport, 1955), while others detect chemicals on contact so must encounter their host at random or else home by some other means. The significance and reason for these differences have not been analysed experimentally, but will serve as an empirical basis for discussion.

Specific host chemicals that act at a distance from the host are usually offered in one side of a Y tube choice apparatus (Davenport, 1950). During studies of this sort Davenport and Hickok (1961) and Johnson (1952) noticed a number of commensals that were not attracted to water that had flowed over their hosts. Evidence from later work by Davenport (1953a, b), Davenport et al. (1961) and Ross and Sutton (1961a, 1963, 1967) suggests these might be instances of responses to species specific chemicals on contact, rather than at a distance, and might be analogous to the contact chemical response of barnaele cyprids that Crisp and Meadows (1963) recorded.

Many commensals and also some parasites respond at a distance to chemicals emitted by their hosts. One of the earliest records and most elegant analyses is that of Fasten (1913). The freshwater parasitic copepod, Lernaeopoda edwardsii Olsson, is found on the gills of brook trout but not on those of the rainbow or German brown trout. I n the presence of isolated gills of the brook trout its larvae become very active. On the other hand, even though the larvae come into contact with them, they show no response to the gills of the other two species. A specific chemical must be diffusing out from the brook trout gills. I n order to test the ecological meaning of these experiments, Fasten


immersed the three trout species in a hatching tank known to contain copepod larvae. After two days the brook trout but not the rainbow or German brown trout were infected. Faust and Meleney (1924), Herter (1928, 1929), Welsh (1930, 1931), Carton (1968a, b) and Wieser (1955) have shown similar responses in other parasites, and many commensals behave in the same way (Davenport, 1950; Davenport and Hickok, 1951; Johnson, 1952; Gage, 1966b; Morton, 1962). Speci- fic chemical responses clearly play a major role in directing parasites and commensals towards their hosts. In contrast, no one has yet identified any of the chemicals involved although a number of authors have conducted preliminary experiments (Carton, 1968b; Davenport, 1963a; Davenport et al., 1961; Ross and Sutton, 1963).

Species specific chemicals either lead an animal towards its host or “ capture ” the animal once it has encountered its host. However, there are other ways in which a chemical might act. It might, for instance, change a behaviour pattern to such an extent that an otherwise unsuccessful animal would be able to find its host. Welsh (1930, 1931) has studied just such an example. The freshwater mite, Unioni- cola ypsilophorus var. haldemani (Piers) is a parasite in the mantle cavity of the bivalve, Anodonta cataracta Say. If it is removed from the clam and washed it is photopositive, but it quickly becomes photonegative if exposed to mantle cavity water or to gill extract from its host, Gill extracts of other freshwater bivalves are not effective. According to Welsh, the reversal in light response enables Unionicola to find its host’s mantle cavity-one presumes by seeing the bivalve’s gape as a dark hole. It would be interesting to know of other relationships that depend on the same sort of mechanism.

Many commensals and parasites in the sea are restricted to one species of host. Where it has been investigated, the restriction usually depends on a positive response to the host’s chemicals, but only a slight one or none at all to chemicals from other species (Welsh, 1931; Daven- port, 1950, 1953b; Ross and Sutton, 1961a; Kearn, 1967; Carton, 1968a). Davenport (1953a) has tested the species specificity of the response of Acholoe to its starfish host and to related species (Table 11). Activity is restricted to Acholoe’s normal host and to one other species in the order Phanerozonia; species in other orders of the class Asteroidea have a low activity (c.f. Kearn on Trematode parasites of fish, 1967, p. 693).

On occasion, a commensal may live with one of a number of host species. Gage (1966a) describes how the bivalves Xontacuta substriata and M . ferruginosa may each be found with four different echinoid hosts. Although they are most commonly found with only one of the

300 P. 9. MEADOWS AND J. I. CAMTBELL

four, the associatiom are not permanent, and the bivalves can re- associate with another individual or even remain free living in the substratum. The evidence is conflicting as to whether these associations can be explained by different individuals having different preferences, or by all individuals within a species being indiscriminate as long as they have one of the four host species. Gage (1966b, p. 84), although he does not give details of his results, states that the bivalves

TAB^ PI. Species specificity in commensalism. The polynoid Acholoe astericola is found in the ambulacral groove of most of the starfish Astropecten irregulark collected near Plymouth, England. On contact with its host, or isolated tube feet from its host, A . astericola becomes active and then clings. The species Specificity of the response was tested by touching A . astericola with the tube feet of species from three genera of starfish. An immediate positive response is scored as 2, a delayed response as 1, and no response aa 0. Six Acholoe were each tested once with the tube feet of the 10 starfish hosts. (From Davenport, 1963a, Table la and b.)

Speciea of Asteroidea whose tube fee t were teated against Acholoe

Summed scores of six Acholo6

Class Asteroidea Order Phanerozonia

Astropecten irregularis (normal host) Luidia cilia& Porania &villus

Order Spinulosa Asterina gibbosa Henricia sanguinolentu Palmipa rnembranuceua Solaster pappocrue

Order Forcipulata Aster& rubens Marthasterim glacialis Stichastrella rosea

12 10 4

2 1 0

he worked with behaved similarly towards each of their four host species. Hickok and Davenport (1967) however, were able to demonstrate some sort of specificity, but the Commensals were specific to separate host species in different parts of their geographical range, not in the same geographical area as were Gage’s commensals. The commensal polychaete Podarke pugettensie Johnson is commensal with the starfish Luidiafoliolata Grube in Puget Sound, and with the starfish


Patiria miniata (Brandt) in southern California. Podarke from Puget Sound responded similarly to a number of non-host animals, i.e. the response was not specific, while Podarke from southern California showed a specific response to their normal host there, Patiria miniata. Hickok and Davenport (1957) also undertook some preliminary experiments with another commensal polychaete, Arctonoe fragilis (Baird), which is recorded from a number of host species of asteroid in the same geographical area. Here, when commensals from three separate host species were tested, each preferred its own host. The problem is obviously complex and needs further investigation.

Commensals that have a number of hosts are not common. How- ever, their host relationships pose interesting questions since once they have met their host, individuals might remain there for the rest of their life or from time to time move to new hosts of the same (Simon, 1968a), or of a different, species. It is also possible that if they do this they may spend some time as free-living individuals (Caullery, 1952, p. 10; Gage, 1966a). Hickok and Davenport (1957) have compared the host preferences of Podarke pugettensis that are commensal with the starfish Luidia foliolata with those of free-living members of the species where both types of animal came from the same geographical area. The commensal individuals easily found their host in a large container of sea water while the free-living ones did not. Investigation of problems similar to this will undoubtedly lead to a fuller appreciation of how commensal relationships arise.

If a commensal can live with more than one species of host (Hickok and Davenport, 1957; Gage, 1966a;) one should consider whether its relationships are equally successful with each host species. Un- fortunately, nothing is known of this problem in commensal relationships, but Carton (1964, 1967) has considered the same problem in his investigation of parasitic copepods. Stellicola clausi (Rosoll) is an external parasite of the starfishes, Marthasterias glacialis (L.) and Asterina gibbosa (Pennant). Its morphology is slightly different when on each host, but not enough to justify species status. Carton (1964) removed females from their respective hosts and then replaced them either on to their own or the other host species. Females from both host species lived longer on their natural host. In a later paper Carton (1967) transplanted the parasitic copepod, Sabelliphilus sarsi Claparkde from its normal host Spirographis spallanmni Viviani to two other sabellids on which it never occurs, Sabella pavonina Savigny and Spirographis spallanzani var. brevispinu Quatrefages. The parasite is eventually rejected after a series of tissue reactions that culminates in the formation of tt scab around it. Kearn

302 P. 9. XEADOWS AND J. I. CABU'BEI&

(1967) has adopted a similar approach by transplanting adult Entobdella soleae (Trematoda) onto abnormal host species of fish. In this instance, however, the abnormal host exhibited no rejection reaction but even so, the parasites only survived for a short while. Kearn also attempted to infect an abnormal host with the species, oncomiracidia larvae, which subsequently grew but did not reach sexual maturity. We consider these are most important papers, not only in their own right, but also in their relation to habitat selection and the development of commensal and parasitic associations in general.

Host finding and habitat selection by commensals and parasites, therefore, offer a wide range of research opportunities. Apart from the examples already referred to, little is known of how young or larval commensals and parasites find their hosts (Hazlett and Provenzano, 1965; Kearn, 1967; Carton, 19680; Paling, 1969). Perhaps the greatest gap in our knowledge, however, concerns the behavioural mechanisms by which commensal and parasitic associations are set up and maintained amongst freshwater invertebrates (Fasten, 1913; Herter, 1928, 1929; Welsh,l930, 1931).

IV. THE BIOLOGICAL ENVIRONMENT The reactions of animals to their biological environment and the

part these play in habitat selection are very varied, and have been considered from a number of points of view by different authors. We will consider firstly the behaviour of larvae as they settle, and then discuss gregarious behaviour, spacing out, and aggressiveness. As well as recognizing members of their own and related species, many animals obtain important environmental clues from plants and micro-organisms, so these are also discussed. Finally, we refer to studies on feeding preferences, homing, and egg-laying which show that these also may at certain times affect the distribution of animals.

A . Settlement behaviour The larvae of a diverse range of marine invertebrates behave very

similarly as settlement approaches (Nelson, 1924 ; Visscher, 1928 ; Wilson, 1928 ; Prytherch, 1934 ; Cole and Knight-Jones, 1939 ; Knight- Jones, 1961 ; Isham and Tierney, 1963 ; F0yn and Gjlaen, 1964 ; Sildn, 1964; Crisp, 1961; Crisp and Meadows, 1962; Gee and Knight-Jones, 1962). From leading an essentially planktonic life they move towards the bottom, and begin to alight periodically on different surfaces, the alightments becoming more frequent as time goes on. At each alightment they explore the surface, crawling over it and stopping from time to time, as well as frequently changing direction. The

HABITAT SELEOTION BY AQUATIC INVERTEBRATES 303

larvae may then swim off or stay to continue their investigations over a more limited area of the bottom (a few mm). Here they re-cross their tracks a number of times as if making quite sure that the area chosen is just right for metamorphosis ; having done this they attach themselves permanently to the surface and enter metamorphosis (Fig. 2). Clearly not all animals show this sequence, errant polychaetes, for instance, do not attach to a surface, but the account is general enough to be useful. There is one unusual exception to the behaviour we have described. Wisely (1958a) noted that settling larvae of the serpulid Hydroides norvegica (Gunnerus) sometimes attach to surfaces com- paratively early in their free-swimming life, and never show any

F"3 ..:!:.;,e .. ...... I I

(bl

FIG. 2. Final movements at settlement of (a) a cyprid of Balanw balanoidea (after Crisp, 1061) and of (b) a l m a of Spirorbia borealis (after Wisely, 1960). The barnacle oyprid comes into contact with its own adults, and the &~?iro~bia larva approaches close to an adult, before metamorphosing nearby. The two black dots represent the point at which the larva metamorphoses. The stippled areas represent the position of adults. Black bars = 1111111.

searching behaviour at settlement. Information concerning other instances of this type of behaviour would be welcome.

Little is known of any analogous patterns of searching behaviour amongst freshwater larvae, except for a passing observation by Weerekoon (1956) on the larvae of a caddis species and for an ecological study on culicid larvae (Diptera) in an Ontario Lake by Wood (1956) ; this ia clearly a field for further research.

We do not intend to review the reactions of marine larvae to their physical environment at settlement, since Williams (1964, p. 258 ; 1965, p. 397) has considered these in detail. Larvae react to light, gravity, ourrent velocity, surface texture, surface contour, angle of surfaces, colour and light reflectance of the surface, and to particle size. Reference


should be made to Williams’ papers and to more recent ones by Hubschman (1970) and Straughan (1972).

B. Gregariousness Many animals appear to recognize other individuals of their own

species by moving towards or staying near them. Gregarious behaviour, as here defined, will lead to aggregations of a species both in uniform and non-uniform local environments but will be more obvious in the former. A great deal is known of the gregarious behaviour of marine invertebrates, and we will summarize this fist before considering freshwater animals. Field and laboratory experiments show that the larvae of a wide range of sedentary marine species settle preferentially near adults of their own species. Data are available for the following species : (a) Coelenterates, Tubularia larynx Ellis and Solander (Pyefinch and Downing, 1949). (b) Polyzoa, Watersipora cucullata (Busk) (Wisely, 1958b). (c) Polychaetes, Mercierella enigmatica Fauvel (Straughan, 1972), Polydora ligni Webster (Blake, 1969)) Subellaria alveolata (L.) (Wilson, 1968), 8. spinulosa Leuckart (Wilson, 1970b), Spirorbis borealis Daudin, S. pagenstecheri Quatrefages (Knight- Jones, 1951,1953a). (d) Gastropodmolluscs, Rissoa splendida Eichwald, Bittium reticulatum (da Costa) (Kiseleva, 1967a). (e) Bivalve molluscs, Ostrea edulis L. (Cole and Knight-Jones, 1949; Knight-Jones 1949; Bayne, 1969). (f) Cirripedes, Balanw amphitrite Darwin (Daniel, 1955), B. balanoides (L.), B. crenutus BrugiAre (Knight-Jones, 1953b), Elminius modestus Darwin (Knight-Jones, 1953b; Knight-Jones and Stephenson, 1950).

Although there may be the occasional exception (Straughan, 1972), a large body of evidence makes it clear that most larvae settle gregar- iously in response to chemicals present in, or perhaps in some cases released by, larvae or metamorphosed adults. The larvae of the ascidian Styela partita Stimpson, for example, metamorphose sooner in water that has been occupied by other larvae; the larvae metamorphose sooner the more larvae originally present in the water, to the point at which they do not metamorphose at all, but die (Grave, 1944). Because of this last observation, the results should be treated with a little caution. On the other hand the larval life of other ascidians is shortened in a similar way by larval or adult tissue extracts (Grave, 1936, 1941 ; Grave and Nicoll, 1940). Grave’s experiments are the only ones suggesting that larvae produce an external metabolite which induces something akin to a gregarious response.

The chemical basis of the gregarious behaviour of barnacle cyprids has been studied in some detail by Crisp and Meadows (1962, 1963). They developed a technique used by Crisp and Williams (1960) to test


the eEcacy of chemicals on surfaces for inducing settlement. Cypris larvae of barnacles settled in Iarge numbers on pitted slate panels previously soaked in an extract of adult barnacles but not on control untreated surfaces. Using the technique as a bioassay, Cri;sp and Meadows established that the chemical to which cyprids respond is probably the cuticular protein, or family of proteins, arthropodin, while Crisp (1965) in a subsequent paper proved that cyprids responded to arthropodin even when it was present as a layer of a few molecules thick. A similar approach has been adopted by Crisp (1967) to study the chemical basis of gregarious settlement by Crassostrea virginica (Gmelin) larvae and by Bayne (1969) to investigate the chemical nature of the substance responsible for the gregarious behaviour of oyster larvae (Ostrea edulis). The settlement inducing activity of adult tissue extracts demonstrated by Bayne could be fractionally precipitated by ammonium sulphate and was destroyed by the enzyme pronase, thus establishing the protein nature of the active substance. Wilson (1968) after seven years of detailed experiments on the settlement behaviour of larvae of the polychaete Sabellaria alveolata has confirmed in this species also that gregarious behaviour depends on larvae recognizing a chemical, which in this case is the cement secreted by adult Sabellaria to stick together the sand grains of their tubes. A long term biochemical programme will be needed to identify in more detail the chemicals recognized by larvae of different species as they settle. It is however fully justified on applied criteria alone, since with this information a direct attack can be made on the problems of the fouling of ships’ bottoms and man-made structures in ports and estuaries.

If larvae settle near adults of their own species in response to chemicals, and if gregariousness is to have a biological meaning, both the response and the chemicals producing it are likely to be species specific, and this proves to be so. Larvae of several species can recognize adults of their own species from those of closely related ones. In reciprocal settlement experiments, more Spirorbis borealis larvae settled on stones bearing 8. borealis than on stones bearing S. pagenstecheri, while larvae of S. pagenstecheri settled preferentially on the stones bearing 8. pagenstecheri rather than on the stones bearing S. borealis (Table 111) (Knight-Jones, 1951). Cypris larvae of Balanus balanoides, B. crenatus and Elminius modestus recognize their own species in a similar way (Knight-Jones, 1953b). Species specific recognition may occur even at a subspecific level (Daniel, 1955), but sometimes breaks down at an interspecific level (Wilson, 1968, 1970a and b). Wilson describes the odd case of two closely related Sabellaria


species where the larvae of one, S. spinulosa, always prefers the sand tubes of its own species to those of S. alveolata, but where larvae of the other, S. alveolata, show the same preference, that is, prefer S. spinulosa tubes to those of their own species as long as the tubes have been constructed in the laboratory (Wilson, 1970a, p. 28-30). In a letter to the authors, Wilson (1972) states “ I think it would be as well to point out that the preference shown by alveolata larvae for spinulosa tubes is only for tubes built in laboratory tanks. When natural spinulosa tubes from the sea are offered with natural alveolata tubes, both together in the same dish, the former are nothing like as attractive to the larvae as are the latter, though the former will induce metamorphosis when

TABLE III. SPECIES RECOGNITION DURINQ GREGARIOUS SETTLEMENT. Larvae of Spirorbis borealis and Spirorbis pagenstecheri were put together into a dish containing a number of slate panels. Each slate either bore previously settled S. borealis or previously settled S. pagensteoheri (Knight-Jones, 1951, Table 5. Summary of experiments 1-10).

No. of No. of

Choke hmae larvae settling settling

on slatea on slates

S. borealis 8. pagenstecheri

Slates bearing previously settled S. borealis 217 97

Slates bearing previously settled S. pagemtecheri 86 204

present alone.” Neither Wilson nor we can account for these laboratory findings. Since no colonies are recorded containing the two species together in the field, one must suppose that other as yet unrecognized aspects of the behaviour of S. alveolata larvae prevent them from joining S. spinulosa colonies or that the laboratory tubes of spinulosa are peculiar in some way.

The species specific response of larvae to intact adults are paralleled by specificity at a chemical level. Metamorphosis of the larvae of the ascidian Phallusia nigra Savigny is rapidly and consistently induced by extracts of adult P. nigra but not by extracts of adult Polyandrocarpa tincta, and thereverse is true of the metamorphosis of P. tincta larvae (Grave, 1936). The cypris larvae of Balanus balanoides and of Elminius modestus distinguish clearly between extracts of their own adults and extracts of adults of the other species in

TABLE IV. Activity of extracts from organisms of different phyla. Balanw balanoides cyprids were offered a choice of slate panels previously soaked in an extract or culture of the appropriate organism, slate panels previously soaked in an extract of adult Balanzls balanoides and clean slate panels. (From Table 8, Crisp

and Meadom, 1962.)

The chemical basis of gregariousness in barnacles.

Extracts wed to treat experimeatal panels

No. of cyprids settling on panels treated with

(6) ( b )

Balanus experimental untreated balanoides

extract controls extract

( a )

Unicellular algae Phaeodactylzlm tricornutum (culture) 2 121 1 Navicula salinicola (culture) 9 133 1

Chlorophyceae Ulva lactwa 4 50 1 Phaeophyceae F u c w serratue 0 8 1 Rhodophyceae Cora.?lina oficinalis 12 50 1 Porifera Ophlitaspongia seriata 72 119 6 Coelenterata Metridium senile 2 25 1 Annelids Arenicola marina 4 93 3 Arthropoda-Crustacea

Branchio poda Artemia salina 13 19 0 Cirripedia Lepas hilli 62 84 1

Chthamalua stellatus 72 109 0 Balanus balanus 101 104 2

Blaberus sp. 50 85 0 Mollusca m e l l a iap i i iu~ 9 37 0 Echinodermata Asteriaa rubena 3 93 3 Pisces Blennius pholis 269 354 8 Mammalia Bos taurus 13 116 7

-1nsecta

W s

308 P. 9. MEADOWS AND J. I. CllMPBELL

experiments where extracts of both species are serially diluted; furthermore, although extracts of other arthropods tested are fairly active (the cuticle of all arthropods contains arthropodin-like proteins), extracts of representatives from other phyla in general lack activity (Crisp and Meadows, 1962, Fig. 3, Tables 8 and 15) (Table IV). The larvae of Ostrea edulis also recognize chemical differences between their own and other species (Bayne, 1969).

The chemical basis and chemical specificity of gregarious settlement by larvae of marine sedentary organisms is therefore well established. On the other hand, it is not known how the gregarious tendency of larvae varies from species to species, nor is there any indication of how gregarious behaviour might interact with other larval responses to produce the patterns of distribution occurring in nature. Variation between species could be measured by comparing the degree of aggregation of different species of settling larvae under uniform experimental conditions using nearest neighbour methods (cf. Edgar and Meadows, 1969; Campbell and Meadows, 1972), and the interaction of gregarious responses with other aspects of larval behaviour should not be difficult to investigate.

The large body of information on the gregarious behaviour of larvae at settlement contrasts markedly with the little that is known of gregariousness in adult animals. There is no reason why mobile adult animals such as the adults of many molluscs, echinoderms and crustaceans should not be gregarious, but they have not as yet attracted much attention. Similarly, little is known of any gregarious tendencies amongst the young of such groups as the free-living nematodes, viviparous echinoderms, or amphipod and isopod Crustacea, in which there is no larval stage and therefore no metamorphosis, and in which the young bear a strong resemblance to the adult (Sheader and Chia, 1970). Let us now, therefore, consider the evidence for gregarious behaviour by adult animals.

The only records of gregarious behaviour in adult planktonic animals are those of Bainbridge (1952) on Calanus and of Clutter (1969) on mysids. Both authors describe swarms in the sea ranging in size from about 12 individuals (Calanus) to more than 1000 individuals (mysids). Clutter concludes from his experiments that mysid swarms are maintained by visual clues during the day and perhaps by body contact and swimming currents in darkness.

Little is known of gregarious behaviour by adult sublittoral animals living in or on sediments, although the observations of divers imply it may be fairly general. The spider crab Maia s q u i d 0 (Herbst) forms heaps or pods of about 1 m diameter and 0.6 m high in which there may

HABITAT SELECTION BY AQUATIC INVERTEHRATES 309

be 60 individuals (Carlisle, 1957). The pod observed by Carlisle remained m the same position for over 10 weeks, and was joined by a further twenty individuals during the first four weeks of this. Soft newly moulted Haia were always found in the centre, which may therefore protect them from predation. These, however, were preliminary observations, and too much weight should not be attached to them. StevZiO (1971) studied aggregations (heaps) of the same species under laboratory conditions in which 5 groups of 20 individually marked animals were observed over 3 weeks, and established a relationship between dominance rank and individual position within the heaps. Higher ranked animals, which were usually larger males, occurred predominantly away from heaps and were rarely found inside them. Prom these results, 8tevEi6 suggested that the aggregations may have a protective function, but pointed out that they were rare in his area (the Adriatic Sea) and evidently not obligatory (loc. cit. p. 25). It is still not clear, therefore, exactly what function these aggregations might have. Similar aggregations are known to occur in field populations of two species of spiny lobster and in the king crab, Paralithodes ; in these instances the size of the aggregation depends on the age of the animals (Lindberg, 1955 ; Fielder, 1965 ; Powell and Nickerson, 1965).

Boaden (1963) and Crisp (1969) have analysed gregariousness in an adult interstitial annelid and an adult intertidal gastropod respectively. Boaden’s work has already been referred to (see Interstitial Animals). M. Crisp (1969) attempted to assess what aspects of the behaviour of the gastropod, Nassarius obsoletus (Say), led to the formation of its very characteristic aggregations. These latter, she concluded, were in part due to the species’ responses to its physical and chemical environment, but also related to a chemical or chemicals given off by the animals themselves.

Apart from direct gregariousness, that is when animals recognize and move towards animals of their own species, some animals in similar circumstances change their behaviour, the change in its turn leading to an aggregation. Unpublished work on Corophium volutator provides an example. In this species, animals in groups are more likely to burrow and also more likely to prefer fine to coarse sand, and these two behaviour changes will undoubtedly lead to aggregations in the field. We might call this an indirect gregarious response. The change in behaviour to light when individuals of the polychaete Nephthsy cirrosa Ehlers are grouped together (Clark, 1956), and the lowered activity amongst groups of the prawn Palaemon elegans Rathke (Rodriguez and Naylor, 1972), might be other examples, but it is not so apparent in these cases whether the changes in behaviour would increase the chances of aggregate formation.

310 P. 9. MEADOWS AND J. I. CAMPBEU

Very little is known of gregarious responses in freshwater invertebrates although they must surely be common. Aggregations of the marine bivalve Mytilw edulis are for instance paralleled by similar aggregations in the structurally similar but unrelated freshwater zebra mussel Dreissena polymorpha (Yonge and Campbell, 1968, p. 30) while the larvae of the caddis fly Potamophylax catipennis Curtis form very distinctive aggregations on the undersurface of stones (Campbell and Meadows, 1972). Several authors have noted sponta- neous aggregations of freshwater invertebrates in the laboratory that might be caused by gregariousness (Curtis Riley (dragonfly nymphs) 1912 ; Gee (leeches) 1913 ; Holmes (water beetles) 1905), and these are common observations to anyone working on freshwater animals. However, the only detailed studies are on planarian aggregations, and gregariousness and parental care in leeches. Planarians form two types of aggregations ; in one, animals maintain a distance equivalent to their own breadth from their neighbours, while in the other, animals overlap and are orientated randomly (Pearl, 1903). Pearl was able to distinguish sluggish animals from very active ones. Active animals moved right through an aggregation and appeared to take no notice of it while the sluggish ones turned towards an aggregation when a short distance away. From these observations Pearl felt that the planarians were react- ing to a chemical produced by themselves but gave no experimental evidence. Planarian aggregations caused by gregarious behaviour may be species specific, for Reynierse (1967) noted that two species if mixed together formed aggregations solely with their own species. More recently, Reynierse et d. (1969), after a series of long and involved experiments, have suggested that aggregate formation is the result of the joint effects of chemotaxis, photokinesis and of distinctive species morphology. However, we have found it difficult to follow their reasoning. The young of some species of leech stay attached to their parents for a week or two after hatching, which can be regarded as a form of gregariousness and Hatto (1968) has studied their parental preferences. Young a108S@0& heteroclita (L.) cannot distinguish between their own parent and other adults, but will not attach to adults of a Werent species. It is interesting to note that the newly liberated young of the intertidal amphipod Marinogarnmum obtwatw (Dahl) behave similarly, and are able to distinguish between females of their own and another species (Sheader and Chia, 1970). Of course, for these experiments to have any ecological meaning the young would have to leave their parents from time to time or run a reasonable risk of being dislodged.

Thus gregarious behaviour occurs among a large number of settling

HABITAT SELECTION BY AQUATIC INVERTEBRATES 31 1

larvae of marine sedentary invertebrates, and further studies are likely to show that it is equally common amongst mobile adult invertebrates both in the sea and in fresh water. A widespread occurrence of gregarious behaviour would suggest that it has a high selective advantage. Gregarious behaviour is almost certainly of advantage to both sedentary and mobile species, particularly in large areas of environmental uni- formity, because it will assist breeding, and evidence for this is provided by the demonstration of female sexual attractants (pheromones) in Portunus sanguinolentus (Herbst) (Ryan, 1966) and in Cammarus duebeni Lilljeborg (Dahl, Emanuelsson and von Mecklenburg, 1970). It may also be important in protecting populations from predation and in the selection of a suitable habitat ; the authors, however, are aware of flaws in these latter two arguments. The first circumscribes the behaviour of a predator more than is warranted by the available experimental evidence. The second assumes there would be an advantage per se in recognizing a suitable habitat by the presence of other individuals of the same species rather than by recognizing it by its own attributes (e.g. temperature, light, shelter, food) ; it also assumes that the first colonizers are making the right decision. On present experimental evidence these assumptions are not justified.

C. Spacing out and aggression Gregarious behaviour brings animals of a species close enough to

one another for them to breed, but if they are too close they will compete unnecessarily for food and living space. Probably for these reasons many animals have a means of limiting their gregarious tendencies that expresses itself either as spacing out, caused by what Crisp (1961) terms territorial behaviour, or by aggressiveness, and of course similar considerations apply to animals on land. Spacing out behaviour in sedentary marine invertebrates takes place as the larvae settle and is in fact superimposed on the gregarious behaviour already described. As a result, gregarious larvae both in the sea and in the laboratory are more likely to settle on surfaces lightly colonized by their own species than on heavily colonized surfaces (Knight-Jones, 1951 ; Meadows, 1969). Wisely (1960) and Crisp (1961) have described the behaviour of the larvae of Spirorbis borealis (Annelida) and Balanus balanoides (Cirripedia) as they recognize and avoid newly-settled individuals (Fig. 2)) while Knight-Jones and Moyse (1961) feel that barnacle cyprids space out more readily to their own rather than to other species. On the other hand, not all larvae space out, for the larvae of Sabellaria alveolata settle on top of or very close to one another (Wilson, 1968, p. 428 and personal communication) and oyster spat


maintain no individual distance from their neighbours (Bagne, 1969) ; it would be interesting to know of other examples. Crisp’s (1961) work makes it clear that although barnacle cyprids prefer to have a space of at least their own body length around them, they settle more closely together, albeit still spaced out, as density increases. Presumably the density of settled individuals must eventually reach a level at which cyprids alighting cannot lind room to settle and so swim off to find more suitable, and less crowded, surfaces. The complex ecological effects of this have been discussed by Meadows (1969) for barnacles, and by Edgar and Meadows (1969) and McLachlan (1969) who analysed spacing out behaviour in chironomid (Diptera) larvae in fresh water. Future work might be directed towards describing the presence or absence of spacing out behaviour in other marine and freshwater larvae, towards determining its species specificity, and towards assessing its relation to gregarious behaviour.

Mobile adult invertebrates appear to space out in the same way as do the larvae of sedentary marine invertebrates (Pearl, 1903; Bovbjerg, 1960; Connell, 1963). Bovbjerg (1953, 1964) using simple but elegant experiments, has for some while been concerned with the analysis of aggressiveness and its relation to spacing out and dispersal in adult aquatic invertebrates. He contrasts species that show aggressive behaviour to their own species and disperse more quickly as the population density increases, with species showing no aggressiveness which disperse at a rate independent of density. Examples of the former are the intertidal crab Pachygrapsus crassipes Randall (Bovbjerg, 1960) and the freshwater crayfish Cumburus alleni Faxon (Bovbjerg, 1959), while examples of the latter are the freshwater snail Campelomu decisum Say (Bovbjerg, 1962a) and the freshwater amphipod Gammarus pseudolimruzeus Bonsfield (Clampitt, unpublished results in Bovbjerg, 1964). However, before these generalizations can be fully accepted more work is needed, and Bovbjerg (1964) himself realizes this.

Aggressive behaviour, which will of course tend to lead to a spaced out distribution, has been studied in a number of other adult invertebrates, but usually from a purely ethological point of view rather than by trying to correlate the ecological distribution of a species with its behaviour (Reese, 1964). Characteristic encounters occur when various Crustacea (Douglis, 1946; Crane, 1958; Fielder, 1965; Cameron, 1966; Hazlett, 1966; Dingle and Caldwell, 1969) meet each other, and also when burrowing worms (Nereis: Clark, 1959) and Crustacea (Erichthonius: Connell, 1963; Mictyris: Cameron, 1966; Corophium: Meadows and Reid, 1966; Gonoduetylus: Dingle and Caldwell, 1969)

EABITAT SELEUTION BY AQUATIC INVERTEBRATES 313

attempt to enter burrows that are already occupied. Hazlett’s (1966) detailed study on the hermit crab Calcinus tibicen (Herbst) involved testing a variety of factors in the species’ immediate and past environment that might influence aggressiveness. The aggressive behaviour of Calcinw was usually limited to exchanges of stereotyped display movements using the chelipeds and ambulatory legs. In most cases the presence and movements of one individual caused the other to retreat. In others, dominance was affected by the following factors: crabs elevated on a ledge were dominant to a lower crab, and turquoise green coloured animals dominated the more frequent reddish brown animals, but there was no sexual dominance. Its past environment manifested itself as follows : starved animals were dominant to well-fed animals, and animals that had lost fights for 50 h continued to lose fights. Finally, isolated animals were more aggressive but not more dominant than non-isolated ones.

Aggressive behaviour between individuals in which stereotyped behavioural displays develop after visual or physical contact are evidently one way of ensuring that crowding in a population does not reach too high a level. But there are other alternatives which will produce a spaced out distribution, and one of these is by the secretion of repellent chemicals which act to ward off other members of the same species, thus producing a sphere of repulsion around each individual. The behaviour of the carnivorous marine gastropod, Fasciolaria tulipa, investigated by Snyder and Snyder (1971) falls into this category. The behaviour of Fasciolaria, however, is more compli- cated than might be expected, for the same chemical seems to induce not only avoidance reactions but also copulatory responses and feeding behaviour depending on its concentration and on the respective sizes and sex of the individuals involved in the encounter.

Behaviour which leads to a spaced out distribution has obvious advantages when predators are common, when a minimum living space is required, or when food is at a premium, and yet these considerations have rarely been submitted to experimental analysis. Recently, however, convincing evidence has been provided by Stimson (1970) that the territorial behaviour displayed by the large owl limpet, Lottia gigantea Sowerby, is directly responsible for the maintenance of an uninterrupted suppIy of its food. Individual Lottia occupy a territory of about 1OOOcm2 on rock surfaces in the intertidal zone on the Californian and North Mexican coast. Their territories are character- ized by a thick algal mat (their food) which is not present on adjacent areas of rock, and by the absence of other species of mobile and sedentary invertebrates. Stimson’s field experiments, which included transplants

314 P. 9. MEADOWS AND J. I. UAMPBELTA

of Lottia to other areas, prove conclusively that the algal mat actually develops more fully within the species’ territory than on adjacent areas, because individuals actively push off not only intruders of their own species, but also those of other species.

Behaviour leading to spaced out patterns of distribution is therefore well documented for the adults of a number of marine and freshwater invertebrates as well as for the settling larvae of several marine species. The complexity of this behaviour has been emphasized by the studies of Hazlett (1966) on the importance of the past and present environment, of Snyder and Snyder (1971) on the significance of intra-specific repellent chemicals, and of Stimson (1970) on the function of territorial behaviour in maintaining food supplies. For the future, an experimental dehition of the relationship between gregariousness and spacing out is likely to be rewarding, and to lead to a better understanding of the role these factors play in determining localized patterns of distribution.

D. Associations with plants Seaweeds cover many rock surfaces on the shore and in the sea, and

their species are zoned vertically. Certain sedentary and mobile invertebrates are found exclusively on one or a few of these species, which has led many research workers to suggest that their localized distribution is the result of habitat selection. Almost all of the experimental work published to date has been concerned with the settlement of the larvae of sedentary invertebrates whose adults are normally found attached to a particular seaweed. Little attention has been paid to the possible preferences of mobile animals that live on seaweeds except for some researches on the food preferences of molluscs which will be considered below (Food Selection).

As with gregarious behaviour, settlement on seaweeds has been approached either from an ecological point of view, in which larvae are offered a range of seaweed species for settlement, or from a biochemical point of view, when inert surfaces are treated with seaweed extracts and these then offered to larvae.

In the 6rst category, much attention has been paid to the preferences of Spirorbis spp. (Polychaeta). Spirorbis borealis, the most commonly studied species, usually occurs on Fucus serratus L., but sometimes on other fucoids. In laboratory experiments its larvae settle on Fucus species in preference to other seaweeds and related Spirorbis spp. behave similarly (Garbarini, 1936; Gross and Knight-Jones, 1967; Gee and Knight-Jones, 1962; de Silva, 1962; Gee, 1965). Hydroids and

HABITAT SELECTION ny AQUATIC INVERTEBRATES 315

Polyzoa are also common on seaweeds and the larval preferences of a few species have been documented. The larvae of two Japanese hydroids studied by Nishihira (1967a, 1968a) settled on the species of seaweed to which they were normally attached in nature. It is interesting to note that the larvae of one of the species, Sertularella miurensis Stechow, although not planktonic and not likely to swim, still showed distinct preferences (Nishihira, 1967b) ; this is reminiscent of the larval behaviour of Spirorbis rupestris (Gee and Knight-Jones, (1962) and it would be interesting to know of other examples. Ryland (1959) studied the settlement preferences of four polyzoan species and showed preferences which, as in the case of the hydroids and the Spirorbis spp., resembled their natural distribution.

Williams (1964) and Gee (1965) have conclusively demonstrated that the specific stimulus Spirorbis larvae receive from fucoids is chemical and they have made some attempt to categorize the biochemical nature of the substances involved. Experiments on polyzoan and hydroid larvae (Crisp and Williams, 1960; Nishihira, 1968b) and on the settlement of gastropod and bivalve larvae on the seaweed Cystoseira, closely related to dargmsum (Kiseleva, 1966b, 1967a), indicate the existence of chemical stimuli in these instances too.

Detailed comparison between these results is difficult because of different experimental and biochemical procedures. However some seaweed extracts appear to have inhibitory effects. Extracts of Cystoseira tested by Kiseleva (1966a, 1967a) did not stimulate aettle- ment, but the larvae tested belonged to species having a wide distribution over a range of habitats (Mytilus galloprovincialis Lamarck, Nereis zonata Malmgren and Platynereis dumerili (Audouin and M. Edwards)) and so the results do not have much ecological meaning. On the other hand, Visscher (1928) obtained experimental verification for the rare occurrence of barnacles on seaweeds from his observations on the unsuitability of extract treated surfaces for the settlement of barnacle cyprids, and Nishihira (1968b) showed that larvae of the hydroid Coryne uchidai Stechow were killed by extracts of a species of seaweed on which they were not normally found in the sea. Indeed, it is possible that settlement sometimes occurs not because a surface is attractive, but because it is not unattractive, although this might be a, semantic point.

In contrast to the marine environment, very little is known of habitat selection by freshwater invertebrates living on plants apart from their plant food preferences which will be considered below. The unusual aquatic larvae of Bellura melanopyga Grote (Lepidoptera) burrow into and feed on the leaves of a yellow water lily, Nymphea


americana, found in protected fresh waters and sphagnum bogs in America (Welch, 1914). They construct elaborate tunnel systems, eventually burrowing lengthwise down the petiole. They then often leave the leaf and swim on the water surface until they meet ano er leaf by chance. At this point the larvae must be able to disting r ish between the leaves of Nymphaea and those of other plants in the same environment, and laboratory experiments confirm this, for the larvae will only burrow into the leaves of the white water lily Castalia odorata = Nymphaea ohrata Aiton if Nymphaea is not available, and consistently refuse Potamgeton and Sagittaria spp. There are a few more recent studies, but most of them are less comprehensive. The nymphs of the mayfly Heptagenia juewgrisea (Retz) live associated with the freshwater plant Batrachium but not with CaZZitriche which is also common in the same environment. When offered a choice they prefer Batrachium to CaZEitriche, stones, gravel or sand (Madsen, 1968). Egglishaw (1 964) has conducted some interesting preliminary experiments on the colonization of trays containing different amounts of plant detritus in a stream riffle. The greatest number of animals colonized trays containing the most detritus.

The possible complexity of the sequence of behaviour patterns elicited by plant chemicals can be appreciated if one turns for the sake of comparison to the terrestrial environment, and to the recent work on the way in which bark beetles find the particular species of tree into which they burrow. The situation is analogous to the settlement of larvae on one particular seaweed, animals aggregating in response to chemicals produced by their host plant. The only differences are that in this instance the chemicals act at a distance (the beetles smell their way to the tree) that both the plant and the beetles produce chemicals, and that if we are to believe a recent hypothesis (Renwick and VitB, 1969), a series of chemicals act in sequence, at first to attract the beetles and then to regulate their sex ratio and population density (Fig. 3).

We may therefore summarize the associations between invertebrates and plants and their relation to habitat selection as follows. Associa- tions between sedentary invertebrates and seaweeds appear to be largely dependent on chemical clues received by larvae as they settle, although the exact nature of the chemicals involved in these associations is not known and there is no indication of the relative importance of chemical and other less specific stimuli at settlement. There is evidence of inhibitory chemicals in seaweeds, and chemicals of this sort may be more widespread in aquatic environments than is appreciated ; it is possible, for example, that they might occur in animals as well as plants, and be

HABITAT SELECTION BY AQUATIC INVERTEBRATES

(c) inhibition of later arrivals: termination of attack

317

:*6 $ } - - - - - - + verbenone

.:$ e ...

’;$:: .:: .: .:$;

. . :..I ::..::

... :.. * ..... . ....

(a) Initial attack by females

.. .. . 3 .. ..i

:.:::,; _ _ _ _ _ _ _ + f u m - v e r b e n ~

frontalin

:.. .. .. . .. : . . ... . ... . : :..: .:....: ...... : : I : . >.. . * r.....

.. . ... . . *..

..... ._.. --.--------> a-pinene . . ..

(b) Regulation sex ratio

of Verbenone

7ions-verbml frontalin E

. a-pinene

FIQ. 3. Chemical attractants from plants. The bark beetle Dendroctonpla frontalis Zimm. (Coleoptera) burrows into pine trees. Initially, females colonize a tree. As soon as they alight they release the pheromones trans-verbenol and frontalin, while the host tree volatile a-pinene diffuses from the resins released by their subsequent burrowings. (a) The pheromones and a-pinene attract many males and a few females. (b) The males release the pheromone verbenone, which with trans- verbenol, frontalin, and a-pinene attracts equal numbers of males and females. (c) The males give off large quantities of verbenone which eventually inhibits further colonization. (Modified from a hypothesis of Renwick and Vit6, 1969.)

the basis of some instances of spacing out behaviour and interspecific competition (Goodbody, 1961 ; Snyder and Snyder, 1971). Finally, we have cited the few experimental analyses of freshwater invertebrates living in or on plants ; since many freshwater invertebrates associate with plants in one way or another, they offer a large number of research opportunities at the ecological and possibly also at the biochemical level.

318 P. 9. MEADOWS AND J. I. OILI\IPBELL

E. Larva$ ehemoreceptim at settlement

We may now consider how larvae detect the chemicals stimulating them to settle near adults of their own species or on a particular species of seaweed. It is possible for larvae to detect specific chemicals at a distance and swim up a concentration gradient, or to respond only after contact with the surface from which the chemical is diffusing or to which the chemical is adsorbed. Certainly, larger animals such as some polynoid commensals are apparently capable of detecting and of moving up concentration gradients of host substances in solution (see section on commensalism and parasitism). Crisp and Meadows (1962, p. 615) however, have pointed out the theoretical inaccuracies involved in scaling this situation down to the size of many larvae (1-2 mm in length). “ Firstly, the distance separating its (the larva’s) sense organs would be so small in comparison with the scale of chemical gradients in the fluid that concentration differences are not likely to be detectable. Secondly, a chemical diffusing from a small surface area into a moving fluid (sea water) gives rise to a sharp gradient of concentration near the boundary layer where the movement of fluid is restricted by the solid surface (Crisp, 1966), but outside this boundary layer the concentration and its gradient are small. This boundary layer is unlikely to reach a thickness exceeding the dimensions of the larva. Thus for a very small animal situated at a distance greater than its own dimensions from a source of diffusing material both the above factors operate, so that the chemical gradient could not be detected and a directional response would be impossible.” Perhaps this last statement is a little dogmatic, but they were able to prove in a later paper (Crisp and Meadows, 1963) that cyprids recognize the settling factor responsible for their gregariousness only when it is adsorbed to a surface. They started from the observation that even when extract treated surfaces were placed very close to untreated ones there was no spread of settlement from one to the other, and they then offered cyprids a choice of extract treated and untreated panels in duplicate dishes. In one dish the cyprids were resuspended in sea water, and in the other they were resuspended in the same extract that had previously been used to treat the extract treated panels (this particular extract had been made up in sea water and the cyprids behaved entirely normally in it). The cyprids distinguished equally well between the extract treated and the untreated panels both in sea water and in extract. The only way that cyprids could have responded in the latter instance was to the settling factor as an adsorbed layer on the surface of the panels, since they were surrounded by exactly the same concentration and there would be therefore no


chemical gradient. It also means that even if the settling factor becomes adsorbed to the cyprid's antennules from solution and the cyprid then alights on an untreated surface, no settlement follows ; the chemical must be adsorbed to the surface on which the cyprid alights. The extrapolation of these results to field conditions is not as yet possible, except to say that cyprids will only settle after having come into contact with a chemically suitable surface. Although no other critical experiments have been conducted, larvae of other sedentary invertebrates probably react in the same way because a number of authors think that larvae only respond to chemicals after contact with treated surfaces (Kampf et al., 1959; Williams, 1964; Wilson, 1953a, 1968).

F. Habitat selection and micro-organisms 1. The microbial fauna of sediments

A large body of work proves that the larvae of benthic marine invertebrates settle and metamorphose most readily in the presence of sand or mud from their normal habitat (Mortensen, 1921 ; Wilson, 1932, 1948,1951; Day and Wilson, 1934; Nyholm, 1950; Smidt, 1951; Si lh , 1954; Scheltema, 1956, 1961). In a similar manner the adults of mobile invertebrates prefer their usual sediments, although few species have been studied (Meadows, 1964a; Gray, 1966~). We have already seen how particle size might account for part of this specificity, but sediments differ in two other important ways: their non-living organic content, and also the numbers and species of micro-organisms in or on them, will vary from place to place (Lloyd, 1931 ; McCoy and Henrici, 1937 ; Zobell, 1938a ; Zobell and Rittenberg, 1938 ; Pearse et al., 1942; Westeide, 1968; Anderson and Meadows, 1969). These considerations have led to experiments in which sandy sediments, treated in ways that alter or remove living micro-organisms and non-living organic material, are offered to larvae for settlement. In general, settling larvae find the treated sands far less suitable for metamorphosis than natural untreated ones (Wilson, 1953a, 1955 ; Scheltema, 1961). In a similar manner, adults of mobile benthic and interstitial invertebrates avoid treated sands (Wieser, 1956 ;Meadows, 1964a ; Gray, 1966d ; Marzolf, 1966 ; Sameoto, 1969). The treatments used to render sands unattractive have included drying, soaking in distilled water or acids, heating to lOO"C, autoclaving, rtshing and treatment with fixatives and detergents. None of these treatments, however, distinguishes between killing micro-organisms, removing all or part of the non-living organia material, and possible etching of the surfaces of sand grains.

Sands rendered unattractive can have their attractiveness restored


by soaking in natural sea water (Wilson, 1954, 1955) or fresh water (Marzolf, 19661, or in sea water that has previously been in contact with a suitable sediment (Wilson, 1953b ; Scheltema, 1961), although the method is not always successful (Meadows, 1964a) and does not distinguish between non-living organic material and living micro-organisms.

It is clear from other experiments that micro-organisms are largely responsible for the attractiveness of natural sediments. Flagellates (but not ciliates) render sands more suitable for the settlement of the polychaete Ophelia bicornis Savigny (Wilson, 1954), while irradiation of sediments with ultraviolet light, which would kill micro-organisms,

TABLE V. Bacteria and habitat selection by interstitial marine invertebrates. (a) Protodrilus qmbioticus, Archiannelida; (b) Protodrilw hypoleucw, Arohianne- lida; (c) Leptastucw comtrictw, Copepoda (modified from Gray, 1966d, 1967, 1968 and personal communication). The dashes represent choices that were not offered.

Choices offeved

Natural sand Autoclaved sand inoculated with:

bacteria isolated from natural sand soil bacteria Paeudomonm sp. N.C.M.B. 129 Flavobacterium sp. N.C.M.B. 246 Flavobacterium sp. N.C.M.B. 411 Serratia marinombra N.C.M.B. 4 Corynebacterium erythrogenes N.C.M.B. 5

No bacteriwontrol

27

23 18 14

6 6 6 2

-

62 - -

4 1 2

31 0

34

1?

9 28 14 3

-

-

reduces their attractiveness for the settlement of gastropod larvae (Scheltema, 1961 ; Kiseleva, 1967b). More detailed evidence of the importance of micro-organisms has been provided by Gray’s (1966d, 1967, 1968) study on habitat selection by three interstitial organisms (Table V). Gray inoculated unattractive sands with different species of bacteria obtained from a culture collection, but more significantly isolated naturally occurring bacteria from sands and inoculated unattractive sands with these also. The species from the culture collection varied in their attractiveness, while the natural sand bacteria were always very attractive. In a later paper, Gray and Johnson (1970) demonstrated different levels of attractiveness associated with different species of naturally occurring sand bacteria. We consider these latter


two fin dings particularly important since it is the first time that micro- organisms from an animal’s naturaI environment have proved to be a major determinant of habitat selection. The work should be extended to the settlement of the larvae of benthic invertebrates.

Gray’s work emphasizes the importance of bacteria in the selection of suitable sediments, but the microbial fauna of freshwater and marine sand grains includes many other forms whose presence has not been

Bacteria

FIG. 4. Microbial fauna on the surfaoe of a sand grain from an intertidal beach. Note the colonies of bacteria, of diatoms, and of the blue-green alga Merimopedia, as well as the organic staining material in hollows and the flat surfaces that are bare. Bar = 100 pm. (From Meadows end Anderson, 1968.)

fully appreciated until recently (Meadows and Anderson, 1966, 1968). Diatoms and blue-green and green algae may be as abundant as bacteria on the surfaces of sand grains and are all arranged in micro-colonies of up to about 100 cells, interspersed with organic material in hollows and depressions on the sand grain surface, while the more open areas of the grain’s surface are entirely bare (Fig. 4). There are great difficulties in designing experiments which would assess the significance of the different parts of this microbial fauna as well as of the organic material ;

322 P. 5. MEADOWS AND J. I. ClLMPBELL

presumably a first step would be the isolation and description of the microbial species and of the organic material involved, followed by culturing and inoculation of sterile sand in an attempt to restore its attractiveness. An almost identical suggestion has been made by Wilson (1958), and so it may be many years before we understand what aspects of this extremely complex micro-habitat are important. Finally, to add confusion to complexity, sands with an experimentally modified microbial fauna exhibit changed physical properties (Webb, 1969).

2. The microbial fauna on f i t surfaces Like sediments, the flat surfaces of rock, stones, and seaweeds as

well as those of man-made structures, such as concrete, ships’ bottoms and glass slides, collect a recognizable spectrum of micro-organisms in the sea and in fresh water. On these flat surfaces the micro-organisms form a film that covers the whole surface; there are no bare surfaces comparable to those on the surfaces of sand grains. The film formed by micro-organisms on surfaces has often been called the primary or microbial film although the concept has had a chequered career. The following quotations represent the earliest references to it that could be found : “ The organisms develop upon the slide in a fairly uniform film ” (Henrici, 1933) ; “ Bacteria and, to a lesser extent, other micro- organisms are the primary film formers on submerged glass slides ” (Zobell and Allen, 1935); “Bacteria and closely related micro- organisms, together with varying quantities of adsorbed organic matter are the primary film formers ” (Zobell, 1938b). Following the formation of a primary film the larvae of sedentary marine invertebrates that settle on flat surfaces do so in progressively greater numbers (Zobell and Allen, 1935; Scheer, 1945; Wood, 1950). Meadows (1964a) citing earlier references felt that the primary film probably forms by three processes: the attachment of micro-organisms, the production by these micro-organisms of extra-cellular metabolites and slimes which then become adsorbed to the surface, and the adsorption from sea water of organic materials. This hypothesis could be tested by experiment.

Settling larvae of sedentary marine invertebrates react to the primary film in a number of ways. The film’s presence either stimulates (Miller et al., 1948; Cole and Knight-Jones, 1949; Wisely, 1958b; Crisp and Ryland, 1960; Meadows and Williams, 1963; Straughan 1972) or inhibits (Harris, 1946; Pyefhch and Downing, 1949 ; Crisp and Ryland, 1960) settlement, has contrary effects when observed by different workers (Visscher, 1928 and Harris, 1946, on cirripedes), or no effect at all (Wilson, 1968), depending on the species investigated. There have only

HABITAT SELEOTION BY AQUATIU MVERTEBRATES 323

been two attempts to analyse which constituents of the primary film cause it to stimulate or inhibit settlement. Knight-Jones (1951) and Meadows and Williams (1963), working on Spirorbis borealis larvae, coated clean surfaces with micro-organisms by soaking them in the appropriate culture.. The larvae preferred to settle on films of the green algae Chlamydomonas and Prasinocladus, the diatom Navicula, and the blue-green alga Synechococcus, but avoided a film of the green alga Dunaliella. Meadows and Williams also showed that membrane filtered sea water did not render surfaces attractive, while if the precipi- tate from the membrane-filtration was resuspended in the filtered sea water, surfaces soaked in it became attractive again, a strong indication that naturally occurring micro-organisms produce an attractive film.

An unusual example of the importance of micro-organisms for the settlement of marine larvae is the influence of fungi on the settlement of larval shipworms (genus Teredo). Shipworm larvae are responsive both to surface roughness and to chemicals present in wood (Harington, 1921 ; Isham and Tierney, 1953), but they are also markedly influenced by the state and type of fungal decay undergone by the wood. Kampf et al. (1959) offered the larvae of Teredopedicellata Quatrefages a choice of woods either treated artificially or decomposed by fungi. Few larvae settled on wood with a layer of agar over it or on wood previously treated with sodium hydroxide or sulphuric acid, all of which treatments were said to simulate the softness associated with fungal decay. However wood decomposed by the basidiomycete fungus Lentinus lepideus F.R. was fairly attractive, while wood previously soaked in sea water for four months and hence heavily infested with naturally occurring fungi was extremely attractive. These observations might lead to a method for the prevention of woodworm attack under natural conditions ; field trials with wood treated before immersion with fungistatic or fungicidal agents might be worth while to determine whether larvae are deterred from settling. It would also be interesting to know whether other animals that burrow into wood, such as the crustaceans Limnoria lignorum Rathke and Chelura terebrans Phillipi, prefer to do so if the wood is decomposed by fungi. One species, Limnoria tripunctata Menzies, has a lower mortality when fed live mycelium of the fungus Peritrichophora integra then when fed sterile wood (Schafer and Lane, 1967) ; however, the animals were not offered a choice. Schafer and Lane's conclusions are a little difficult to follow. They do not give enough details of their quantitative results, they imply that the temperature rdgime of their experiments fluctuated and they do not appear to have aerated the tubes in which the animals were maintained (p. 294, loc. cit.).

324 P. S. MEADOWS AND J. I. O.UPBELL

Apart from the rather special example of the Teredo larvae, nothing is known of exactly how or why larvae settle on certain kinds of primary films, of the relative importance of the different film constituents, or of the way in which the film is formed. We have no idea whether mobile adult invertebrates in the sea respnnd to the film, and what is really most surprising, no evidence at all, apart from somewhat circumstantial evidence presented by Marzolf (1966), of any freshwater invertebrate responding to primary films on flat surfaces or detecting the microbial fauna of muds and sands.

a. Food selection It goes without saying that almost all animals select the food they

eat, and for an animal that moves around this means searching for food which will in turn lead animals to aggregate where suitable food is abundant.

Firstly we will consider the food preferences of marine and freshwater planktonic invertebrates. A number of marine calanoid copepods and larvae show clear preferences for particular species of diatom (Harvey, 1937), feed preferentially on larger as opposed to smaller phyto- and zoo-plankton (Mullin, 1963) or on zoo- rather than phytoplankton (Haq, 1967), or avoid eating their own young (Mullin and Brooks, 1967). The veliger larvae of the marine gastropod Nassarius obsoletus, when presented with a mixture of two species of diatoms and one green alga (Cyclotella, Phaeiductylum and Dunaliella) usually prefer Cyclotella and always avoid eating Dumliella (Paulson and Scheltema, 1968). These authors say their " experiments do not reveal how the larvae select their choice of food, whether it be by size, concentration, or chemotactic sense ". The gymnosomatous pteropod molluscs Clione limacina (Phipps) and Pneumodermopsis paucidens (Boas), both carnivorous species, are highly selective in the food they eat, and will only accept certain species of thecosomatous pteropods when offered a choice (Sentz-Braconnot, 1965; Lalli, 1970). Their feeding responses are elicited solely after direct contact with their prey, and so do not depend on a distance chemical sense. Any gymnosome aggregations resulting from feeding must therefore be caused not by movement towards areas where there are thecosomes, but by gymnosomes h d i n g thecosomes by chance and then remaining in that area. The experimental evidence for food selection by freshwater planktonic animals is more sparse. Burns (1969) fed two species of Daphnia with a suspension of different sized spherical plastic beads mixed with a yeast; the size distribution of beads the animals ingested differed significantly from the size distribution of those in suspension, but since the yeast was


somewhat smaller than the beads and its concentration in the animals’ guts was not measured, the ecological significance of Burns’ results is not clear.

Seaweeds growing in the intertidal and immediately sublittoral environment are clearly zoned. A number of herbivorous benthic invertebrates feed on them and may show feeding preferences that accord with their observed distribution in the field. Van Dongen (1956) and Bakker (1959) both offered Littorina obtusata (L.) (= L. littoralis) a range of common algae but have disagreed in the interpretation of their results. Van Dongen felt that Littorina chose algae which did not agree with its distribution on the shore, while Bakker concluded that the vertical distribution of Littorina was mainly determined by its algal preferences. Other papers of a similar nature are those by Den Hartog (1959) whose results on nudibranchs are preliminary, by Frings and Frings (1965) on the chemosensory basis of food-finding and feeding by the nudibranch Aplysia juliana Pease, and by Sakai (1962) and Carefoot (1967, 1970) to whose works we will refer in another section (see section on Physiology and Viability). Leighton (1966) in a comprehensive paper on the food preferences of eleven species of herbivorous marine invertebrates, measured the weights of a number of seaweed species consumed in 24 hours as an indication of preference ; amongst other observations he noted that the deepest living herbivore studied, Lytechinus anamesus H. L. Clark (Echinodermata), preferred the red alga Gigartina armuta, and pointed out the agreement between this and the supplantation of brown by red algae at greater depths.

There is very little evidence on the plant food preferences of freshwater benthic invertebrates although they no doubt could be demonstrated using suitable techniques. Bovbjerg (1965, 1968) observed four species of lymnaeid snails feeding for most of the time on algae or higher plants but occasionally on dead animals. In Y tube experiments, the snails orientated strongly to chopped crayfish but not to chopped pond weed, although they stopped moving on contact with the weed and so in this way could aggregate on it. Bovbjerg (1968) suggested that animal foods are detected at a distance and plant food after contact ; but this is not general, for in the marine environment Littorina and Aplysia can sense fucoids and Ulva respectively at some distance (Van Dongen, 1956 ; Frings and Frings, 1965).

Carnivores, because they often hunt or forage, are likely to be well equipped to detect their prey from a distance and to aggregate around moving or stationary animals. A number of experiments with freshwater and marine invertebrates prove that this is so. The freshwater leech Clossiphonia heteroclita (L.) eats Lymnaea stagnalis in preference

A.M.B.-lO 13


to enchytraeid worms but does not normally attack undamaged Lymnaea (Hatto, 1968), which might be an inconvenience in the field as there may not be many damaged Lymnaea available. Their preference for damaged Lymnaea was confirmed by Y tube experiments. The North American water bug, Notoneeta un&ulata Say, is an important predator of mosquito larvae and pupae and Ellis and Borden (1970) have shown that it has a well-defined preference for these over other prey organisms.

Amongst other invertebrates certain nudibranchs are known to feed on sea anemones and they also respond in a Y tube to water that has passed over their natural food (Braams and Geelen, 1953 ; Stehouwer, 1964; Van Haaften and Verwey, 1959). Using similar techniques, Castilla and Crisp (1970) have reinvestigated the chemical basis of feeding and predator avoidance of Asterias rubens L. The oyster drill Urosalpinx cinerea (Say) responds to substances released into sea water by its prey Crmsostrea virginim and Modiolus demissus Dillwyn and its response is greater to individuals having a higher respiratory rate (Blake, 1960). Blake goes on to suggest that Urosalpinx may be able to select a particular individual from within a group because that individual has a higher respiratory rate and hence is producing more of some hypothetical metabolic product. It would seem more reasonable to suggest that the Urosalpinx could be attracted to the oyster around which the level of attractant (metabolic product) is highest because of the higher respiratory rate. It is di6cult to see how this can operate in field conditions and of what advantage it is to the Urosalpinx t o be able to detect perhaps small differences in levels of concentration of attractant in an area which may contain many oysters.*

Other studies on feeding by carnivorous marine invertebrates are those of Lindberg (1955), which is an essentially descriptive account of foraging behaviour by the spiny lobster Panulirzls interrqtus (Randall), of Matthews (1955), which briefly proves that the sand crab Hippa pacifica Dana detects its preferred food, the Portuguese man-of-war (Physalia utriculus = P . physalis L.) by a chemical sense, of Shelton and Mackie (1971) which is concerned with the chemical basis of feeding in Carcinus maenas (L.), of Brun (1972) on the feeding habits of Luidia ciliaris (Philippi), and of Landenberger (1966, 1967, 1968), which is an experimental analysis of the feeding of the Pacific starfish Pisaster.

Landenberger's detailed studies serve as a model for future research in this field, and some of his results will be summarized here. Pisaster giganteus (Stimpson) feeds on a wide variety of animals, but mainly on molluscs. In one particular area it is very abundant under and on the *See note added in proof on page 493.

E4BITAT SELEUTION BY AQUATI0 INVERTEBRATES 327

pilings of a pier which extends half a mile out from the shoreline near Santa Barbara, California. Mytilus, on which it feeds, grows intertidally in clusters on the pilings, and from time to time clusters of Mytilus fall beneath the pier helped by predation of the Pisaster on the pilings. Most of the Pisaster however are found under the pier and here Mytilw are very patchily distributed. Landenberger, because he was able to train Pisaster to move down the side of a tank to food with a light stimulus, suggested that the starfish were kept in the general area of the pier by learning to associate food with the region of reduced light intensity under the pier. Perhaps the connection between these observations is a little tenuous, but the idea is an interesting one. Under the pier, large aggregations of Pisaster form around the clumps of Mytilus, only to disperse again when the clump is eaten. Landenberger (1967) induced the formation of new aggregations by placing clumps of Mytilus on parts of the bottom where there were few Mytilus and therefore few Pisaster. Pisaster migrated in from areas nearby but unexpectedly stayed there for some two or three months after the food had been eaten, so they may have learned to associate the particular area of the bottom with food, the association taking some time to wane. Landenberger (1968) also described in detail the food preferences of Pisaster. Seven species of intertidal molluscs were offered in pairs, and Pisaster showed a clear hierarchy of preferences with Mytilus edulis and M . calij’ornianus Conrad being the most suitable.

If we accept Landenberger’s reasoning about the relationship between the shade under the pier and training Pisaster to light, his work demonstrates clearly how the starfish remain in the general area of their food (the shaded area under the pier) and then within this area detect and aggregate around clumps of Mytilw-their preferred food. Landenberger’s detailed analysis shows how a complex example of habitat selection can be understood by suitable experimentation, and is likely to lead to further research.

The examples we have quoted illustrate how marine and freshwater carnivorous invertebrates seek out and aggregate around their prey ; however, some prey organisms take avoiding action to escape their predators and this can be considered a form of habitat selection since their behaviour will influence their distribution. The escape responses of intertidal gastropods to predatory gastropods and to starfish, of the sea anemone Stomphia coccinea (Miiller) to starfish, and of bivalves, gastropods and brittle stars to starfish are examples, and appear to be based on chemicals detected at a distance from or on contact with the predator (Bauer, 1913; Weber, 1924; Bullock, 1953; Clark, 1958; Ross, 1965; Gore, 1966; Kohn and Waters, 1966; Mackie, 1970). Mackie loc.

328 P. S. MEADOWS AND J. I. CAMPBELL

cit. and Kohn (1961) refer to other apposite papers and consider the biochemistry of these responses. Unfortunately, in no case has the prey's response to the predator and the predator's response to the prey been studied in the same pair of species. The comparison would be worthwhile.

H . Homing

Some intertidal invertebrates migrate from and return to a recognizable site on the shore, and these movements are usually termed homing behaviour in contrast to the larger scale horizontal

.;.d '% <, a .:::. :.::::. _,:, . .:.:. .................... .......... .:.:.:.:.:.:. ........... ;:;::;;;:::.. ............. .:.

G"' L b (a1 pL(b) ( C )

. 5cm

FIG. 6. The homing movements of intertidal limpets (Patella spp., Gastropoda) on rock surfaces. A, the tracks of an individual as i t returned to its scar six times over a 10 day period. B, the return of an individual continues after it has been displaced from (1) to (2). The return took 2 hours. C, the track of an individual that had to circumnavigate a plaster obstacle in order to reach its scar. The return took 1 hour. The large black dots represent the limpets' scars. Arrows indicate direction of movement. L = length of limpet. (Modified from Cook et al., 1969.)

The returns took between 1 and 4 hours.

migrations that some intertidal and marine invertebrates exhibit (see section on Marine Animals). The most clearly defined instances of homing behaviour are shown by the intertidal pulmonate Onchidium and by limpets. Onchidium J'loridanum Dall is a deep blue naked pulmonate very common around Bermuda. When the tide is up it lives in communities in holes in the rock which are less than " the size of man's head ') and which usually contain more than twelve individuals (Arey and Crozier, 1918, 1921). When the tide falls, individuals come out through a small opening and wander in various directions to feed on the felt covering of algae on the rocks. They return to their own community even when individuals from different holes mix on the shore, and do so not by following their previous wandering tracks home,


but by moving in straight lines. Animals removed to any point within 30-100 cm are able to return to their own hole. They will also home after having been kept in the laboratory for 24 hours. Animals whose oral lappets are removed cannot home. The oral lappets are constantly in touch with the algal carpet which therefore may give Onchidium some chemical clues of its whereabouts. There are other air-breathing invertebrates in the intertidal zone (e.g. Petrobius maritimus (Leach), Thysanura), and much of the crevice fauna on the shore is essentially terrestrial. If these animals emerge from their holes or crevices for food or to explore when the tide is out, they may also home, and must at any rate behave in a way that will return them to some shelter as the tide rises (Cameron, 1966; Craig, 1970). The homing of limpets on to their own rock scars is we11 known (Wells, 1917; PiBron, 1919; Thorpe, 1956, pp. 186-191). Cook et al. (1969) have recently attempted to determine its mechanism, but experienced difficulty in finding conditions that would inhibit it (Fig. 5). The problem appears to be difficult, but would be worth further detailed study under more stringent laboratory conditions. It would be interesting to know, for instance, whether limpets could be taught to recognize an artificial scar on a flat surface of say wood or brick.

I . Oviposition preferences Aquatic invertebrates that lay their eggs on particular surfaces or

in particular sediments must presumably choose a site for oviposition, and their choice will obviously define the distribution of their young. Examples are caddis flies (Trichoptera), dragonflies (Odonata), mayflies (Ephemeroptera) and notonectids (Hemiptera) in fresh water and cephalopods, some gastropods, and some polychaetes in the sea, and there are many others. Little is known of the oviposition preferences of any of those animals in contrast to the many studies on terrestrial insects. Craig (1970) refers, in passing, to the intertidal beetle Thino- pinus pictus preferring wetter sand for oviposition. Hudson (1956) who has studied the oviposition of mosquitoes, offered Culex pipiens molestus ForskU and Aedes aegypti (L.) salt solutions of different concentrations and counted the numbers of rafts of eggs and also the numbers of individual eggs laid. Solutions of greater than 0.085 M were avoided. The behaviour of the two species will obviously prevent them from laying eggs on the surface of brackish waters. In a more recent paper Hudson and McLintock (1967) showed how Culex tarsalis Coquillet preferred to oviposit on water containing pupae, exuviae, or emerging adults of their own species, rather than water containing other related species, a nice analogy to the chemical basis of gregarious-

330 P. 8. MEADOWS AND J. I. (IAMPBELL

ness in marine invertebrates. The subject is discussed in further detail by Macan (1963, Oh. 6).

V. PHYSIOLOGY AND V I A B ~ Y Elton (1927, p. 40) has suggested that “ the ultimate limits of

environment are set by an animal’s physiological make-up ; if these limits are reached an animal will die. It is therefore undesirable that the animal should run the risk of meeting such dangerous conditions and it has various psychological (i.e. behavioural) reactions which enable it to choose, to a large extent, the optimum conditions for life. The animal is not usually occupying the extreme range of conditions in which it could survive”. There is good evidence for this, and in most cases species choose to live well within their lethal limits.

The relationship between preferences and lethal limits has been investigated for the following variables and species. (a) salinity: Ligia baudiniana (Barnes, 1934, 1938) ; 8 species of interstitial animals (Jansson, 1962, 1968) ; Phyllodoce muculata larvae (Lyster, 1965) ; 3 species of fiddler crab (Teal, 1958) ; Corophium volutator (McLusky, 1967, 1970) ; Branchiostoma nigeriense (Webb and Hill, 1968). (b) humidity: Ligia italicu Fabr. (Perttunen, 1961); 3 species of talitrid amphipod (Williamson, 1951a). (c) particle size : Corophium volutator (Meadows, 1964c, 1967) ; Branchiostoma nigeriense (Webb and Hill, 1958). (d) dissolved carbon dioxide : Cambarus species (Powers, 1914). (e) temperature : Protodrilus symbioticus (Gray, 1965). (f) phytoplank- tonic food: Neomysis vulgaris (= N . integer (Leach)) (Lucas, 1936). At first sight this seems a large body of work, but some of it is preliminary, and in much of it the results of preference and viability experiments are not related to each other. Exact correlation is also intrinsically di5icult because most preference experiments are conducted over an hour or so, while viability experiments may last several days. There are other difficulties. A species may prefer, say 25%, sea water while being capable of living in 0 to PO%, sea water. And yet, the result as such might have very little meaning, since some other variable might impose limits that in any case restrict the species to 20 to 30%, sea water. Elton (1927, p. 41) realizes this: ‘‘ animals are not completely hemmed in by their environment in any simple sense, but are nearly always prevented from occupying neighbouring habitats by one or two limiting factors only ”. With these provisos, some of the work is detailed enough to lead to meaningful conclusions.

It would seem most probable a priori that the preferred level of a paxticular variable should be equidistant from the upper and the lower lethal limits of the same variable, and this is so of the preferred tempera-

EABFI'AT SELEOTION BY AQUAmC INVERTEBRATES 331

ture of the interstitial archiannelid Protodrilus symbioticus which lies almost exactly midway (f15'C) between its upper (+34-3'C) and its lower (-3.7OC) lethal limits (Gray, 1965) (Fig. 6a). On the other hand there are records of animals whose preferred level of a particular variable is very close to the lower or upper lethal limit imposed by that

hizwera baliico Nitocha fohciosa Schizopera baliico

T 1 1 5 10 15 20 25 30 5 10 15

Saliniiy (%d

FIG. 6. Lethal limits and preferred range. (A) The preferred temperature of the intertidal interstitial archiamelid Protodrilua syrnbioticw lies almost exactly midway between the species' upper and lower lethal limits. (Modified from Gray, 1965.) (B) The preferred salinities of two brackish water interstitial harpaoticoid copepods, Nitochra fallacioaa and Schizopera baZtica, lie at their lower lethal limits. (Modified from Janason, 1968.) - - - - = lethal limits: 0-0 = preferred range.

same variable, or even, which seems entirely paradoxical, at or outside the lethal limits. The preferred salinity of various interstitial organisms studied by Jansson (1968) are just such a case in point, and lie very close to or beyond the lower lethal limits (Fig. 6b), and Jansson (loc. cit. p. 61) found it difficult to explain his results. Similarly, Lyster (1965) gave the larvae of PhyZZodoce maculata (L.), an intertidal poly-

332 P. S. MEADOWS AND J. I. CaMPBELL

chaete, a choice of salinities in a vertical column and found larvae collecting at a salinity of 12%, which would have killed them in a few hours.

It would appear, then, that some animals choose habitats which will eventually kill them. If this conclusion is not based on experimental artifact, these seem to be instances of habitats selecting animals rather than animals selecting their habitat. Turning to the terrestrial environment, there are clear cut cases amongst insect parasites of the parasite’s habitat-its hostselecting the parasite, in other words killing it. A number of ovipositing insects cannot distinguish between insect hosts in which their progeny will develop successfully and hosts in which their progeny will die (Balfour-Browne, 1922 ; Cendaiia, 1937 ; Ishii, 1952) and this is apparently most marked in the parasitic Diptera (Salt, 1938). It would be extremely interesting to know if any aquatic parasites show similar lack of discrimination to their hosts. The only vaguely related work we know of is by Carton (1967), who transplanted the parasitic marine copepod Sabelliphilus sarsi from its normal polychaete host Spirographis spallanzani to two closely related species. In both transplants the copepod was eventually rejected after a series of tissue reactions followed by scab formation. However the work is not strictly comparable because in nature the copepod is not found on the two species to which it was transplanted.

Animals are continuously assessing the suitability of their environment and moving from place to place so that they can take best advantage of the range of conditions available to them. Little is known of how their physiology alters as they do so or as they remain for a while in an unsuitable environment. Oxygen consumption has been used as an index of the metabolic activity of mayfly nymphs in sediments of different particle size (Eriksen, 1963; Wautier and PattBe, 1955) and of Corophium in different salinities (McLusky, 1969). The mayfly nymphs were less active and their oxygen consumption was lowest in the preferred sediments, whereas the oxygen consumption of Corophium, although very variable, did not vary consistently between salinities even though some of the latter were avoided in choice experiments (McLusky, 1970). Further work would be worthwhile particularly since some early experiments by Allee (1927) indicate a similar lowering of oxygen consumption in starfish after they have aggregated into clumps.

Sakai (1962) has studied the relation between growth, maturity and food preferences in the marine gastropod Haliotis discus hannai Ino. Haliotis will eat a number of species of brown, green, and red seaweeds, but shows distinct preferences if offered a choice (Table VI). Its rate of feeding, efficiency of food conversion, increase in weight and develop-

TABLE VI. Habitat selection, growth and sexual maturity. The Japanese marine gastropod Haliotis discus hlannai will eat a number of species of brown, green and red algae, but shows distinct preferences if offered a choice. Sakai (1962) offered Haliotis choices of three different seaweeds in preference experiments. He also maintained Haliotis on one or other of three

seaweed species for one month, and noted feeding rates, efficiency of food conversion

yo increase in body weight, and the development of sexual maturity.

x loo), : food ingested (g) increase in body wt (g) 5

u F M

rp The results of the month’s experiment conformed exactly with the species’ food preferences. (Modified from Sakai, 1962, Tables 2, 3 and 7. )

n 3 & W ic L- R)

Food consumption, growth and development of sexual muturity at the end of one month feeding on the three algal species

r A \

Seaweed eaten in 1 month Sexual maturity h A Preferences for , \ I -I 9

2 Undaria 4

PinnatiJida (a brown alga) 66 6-17 5.07 32.1 90 10 z !i 5 pertusa (a green alga) 25 3.76 2-29 E.5 55 44

Carpopeltis E afinis (a red alga) 9 2.15 1.50 3.6 44 55

the three species Eficiency of yo increase Fairly mature Indistinct Species of seaweed of seaweed (%) glday food conversion (yo) in weight to mature to immature 0

t4 Ulva

W W W

334 P. 8. MEADOWS AND J. I. OA?dPBELL

ment of sexual maturity were all highest on the preferred seaweed species Unduria pinnatim Sur. More recently, Carefoot (1967, 1970) has analysed the relationships between algal food preferences, growth, and maturity in various species of the nudibranch Aplysia, while Bovbjerg (1968) has studied a similar problem in the feeding of the freshwater gastropod Limnaea stugnalis Say. Limnaea eats both animal and plant material but can live on either. However it grows fastest and shows its characteristic reproductive behaviour when given a mixture of the two rather than either separately. Investigation of the feeding habits and associated growth in other aquatic invertebrates would be profitable, and a great deal could be learnt from comparisons with the terrestrial environment. The feeding habits and physiology of aphids feeding on plants for instance, have been studied in great depth (Mittler and Dadd, 1966).

It is evident, therefore, that there are many studies in which both preferences and lethal limits have been investigated but only a few in which the two types of experiment have been conducted in enough detail to allow of a direct comparison. It is to be expected that most preferences will fall well within lethal limits ; however there are instances where this is not so, and these we have discussed a t some length. We have also seen that little is known of the physiological changes that might occur as animals select their habitats and so in this respect the careful work of Sakai (1962) on the food preferences and growth of Haliotis discus hannai and of Carefoot (1967, 1970) on Aplysia represent an important advance and suggest how similar problems might be approached experimentally.

VI. MECHANISMS OF HABITAT SELECTION The behavioural mechanisms by which animals select their habitats,

light reactions, gravity responses, gregariousness and so on, have been covered already. However there are a number of additional topics which might be considered most conveniently at this point. They include behaviour in choice experiments, coarse and h e selection, indirect clues to habitats, noise in choice experiments, hierarchies of preferences, and the slope of a preference, amongst others.

Fraenkel and Gunn (1940) have categorized the behaviour of animals in two dimensional environments, and the behaviour of invertebrates on flat surfaces in water and on land can usually be accommo- dated to their scheme. But many invertebrates in aquatic environments move in three dimensions; planktonic animals are obvious examples, while some benthic invertebrates move about on the surface of sediments, burrow into sediments, and swim in the body of the

HABITAT SELECTION BY AQUA!CIC INVERTEBRATES 336

water. No descriptive scheme has yet been evolved to fit this three dimensional movement (which incidentally is also shown by flying animals) although Douwes (1968) has attempted to do so after studying the flight pattern of the geometrid moth Cidaria a Z ~ Z a ~ a L., and Keegan and Meadows (unpublished observations) have in a similar way attempted to document the three dimensional behaviour of Corophium as it alternately swims and alights on sediments.

Little attention has been paid to the way animals find their habitats. They may, for example, be led to the right habitat by aseries of different stimuli that bring them closer by stages. We might envisage smell, sight and hearing as leading animals to the general area of a suitable habitat (coarse selection), and then touch, taste and contact chemical senses being used to define the exact habitat (fine selection). On the other hand, stimuli from the physical and chemical environment (light, heat, salinity) might act as coarse indicators, and biotic stimuli (gregariousness, detection of plants as food) as fine indicators. Not a great deal is known of these sequences although there is no doubt that they take place. The larvae of benthic marine invertebrates approaching metamorphosis, for example, change from being photopositive to photonegative and this will lead them to the general area of the bottom, after which the more localized stimuli of gregariousness and algal preferences can take over. Even after contact with the correct environment, sequential stimuli may play a part, and Hansel1 (1968) has demonstrated the way in which a series of ordered assessments of particles are used by caddis fly larvae before they incorporate sand grains into their cases.

It is possible that certain species may utilize indirect clues during the selection of a preferred habitat (Lack, 1949, p. 299-300; Moynihan, 1968). Consider, for example, a benthic invertebrate living in and preferring a sediment of a certain particle size; it might select the sediment by particle size, but find it suitable to live in not because of its particle size per se but because its food-a certain species of micro- organism-is found only on sand grains of that size. This hypothetical example may suggest how similar problems could be approached experimentally, and might lead to a re-examination of already published work where the results have presented some unexpected and perhaps contradictory conclusions (cf. Meadows, 1964a, p. 508).

The appreciation of chemicals at a distance from their source enables various aquatic invertebrates to locate their habitats, and the distinction between this and contact chemical senses has already been made when considering larval settlement. The contrast could also be regarded as one between coarse and h e selection-contact chemical


stimuli falling into the latter category, but there is little evidence for this at present. Chemicals emanating from food, hosts, predators or individuals of the same species in aquatic environments are usually detected at a distance (Copland, 1918 ; Welsh, 1930 ; Davenport, 1950 ; Stehouwer, 1954; Lindberg, 1955 ; van Dongen, 1956; Davenport et al., 1960 ; Frings and Frings, 1965 ; Gore, 1966 ; Bovbjerg, 1968 ; Castilla and Crisp, 1970; Dahl, Emanuelsson and von Mecklenburg, 1970; Snyder and Snyder, 1971). On the other hand there are a few well documented instances of adult invertebrates responding to chemicals only after contact : certain freshwater snails detect their plant food onIy on contact (Bovbjerg, 1965, 1968), the marine commensal poly- noids Acholoe and Gattyana recognize their respective hosts only after they have encountered them (Davenport, 1953a), and the swimming sea anemone Stomphia coccinea has to touch the starfishes to which it responds before it will swim (Sund, 1958). These examples do not appear to fall into any set pattern, and there is as yet no clear indication as to why, under field conditions, some of the chemicals should be detected at a distance and others only after contact.

Hierarchical relations, peck orders and so on, form an accepted part of current behavioural thinking, and this has led to similar systems being proposed for habitat selection. Consider a number of alternatives, A, B, C, D, where A is preferred to B, B to C, and C t o D. The alternatives can be offered in pairs or as a group together, and may differ qualitatively or quantitatively. Few authors have considered these relationships in detail (Meadows and Campbell, 1972), although Dawkins (1969a, b) has proposed theoretical models. Dawkins’ reasoning is a little difficult to follow in parts, and we are not entirely convinced of the ecological significance of his hypotheses although they were not of course intended as such; however they may well serve as a basis for experimentation,

The distinction between qualitative and quantitative differences of preference is a very real one. The mechanisms used by animals to distinguish between A and B, and B and C, when A, B, and C are qualitatively different, may well be entirely different, while if A, B, and C differ only quantitatively the mechanisms are likely to be the same. An example of qualitatively different alternatives would be the Kariba weed (Salvinia auriculata Aubl.), line sand, and organic matter, preferred in that order by larvae of the chironomid Nilodorum brevibucca Freeman when these choices were offered in pairs (McLachlan, 1969). Unfortunately the mechanisms by which the larvae distinguish between the choices are not known. An example of quantitatively different alternatives would be the series of grades of sand obtained


from sieving the typical sediment of Corophium volutator (Meadows, 1964~) . When offered paired choices Corophium always preferred the finer of the two sediments, although again the mechanism by which the animals distinguish between the sand grades is not known.

Landenberger (1968) has considered the changes in apparent preference when qualitatively different choices, three species of mussel, three species of gastropod and a chiton, are offered, firstly in pairs, and then in a multi-choice experiment as food to the starfish Pisaster. In all but one pair of choices Pisaster showed a significant preference for one alternative, and the order, or hierarchy of preferences, was well defined and consistent among replicates. When the seven prey species were presented together in a multichoice experiment, the preferences were in the same order but were in general weaker-that is-not so clear cut as those when the prey were presented in pairs. Similar studies of preferences for quantitatively different items would be well worthwhile. Landenberger’s results can be extrapolated to natural conditions as follows. Consider an environment in which habitats A and B are randomly distributed at the same population density in a uniform environment : then remove habitats A and B and replace them by habitats A, B, C, and D, these to be distributed randomly, but each at the same density, among the positions originally occupied by A and B. If an animal encounters this environment and prefers A to B to C to D, then the animal will aggregate in larger numbers on A when only A and B are present than when A, B, C, and D are present (Meadows and Campbell, 1972).

The difference between successive levels of a variable, where A, B, C, and D represent the different levels, may be so small as to escape detection, in which case an animal will not distinguish between A and B, B and C or C and D, but might distinguish greater differences such as those between A and C, B and D or A and D. We can regard this as the slope of the variable (Harder, 1968, p. 159), and Amos (1969) and Amos and Waterhouse (1 969) have demonstrated its ecological significance in the terrestrial environment during a study of the behaviour of beetles along humidity gradients of different slopes. The concept could be profitably applied to such variables as salinity, light and temperature in aquatic environments, as indicated in Meadows and Campbell (1972).

So called “ noise ’’ or interference from other aspects of the environment might also obscure preferences (Landenberger, 1968). One might, for example, class as noise the overriding of the preference for rough over smooth surfaces by the preference for filmed over unfilmed surfaces shown by larvae of Spirorbis rupestris (Gee, 1965) and also the influence of other animals on habitat selection described by Clark (1956) and


Naylor (1959). Reports of conflict between laboratory experiments and field distribution might represent other examples. Amongst 10 freshwater species of insect larvae and nymphs and one gastropod investigated by Cummins and Lauff (1969), the substrate preferences of 6 appear to disagree with their field distribution. Presumably other variables take precedence in the field. Bovbjerg (1970) recorded a discrepancy between the results of laboratory experiments and field distribution in two species of crayfish which was clearly the result of interspecific competition (see Section VIII), and finally, the freshwater bivalve Sphaerium transversum (Say) , although preferring mud in choice experiments is equally common in sand, sandy mud or mud sediments (Gale, 1971). Gale could not account for his findings but suggested that other factors in the environment overrode the species substrate preferences.

It is obviously advantageous for an animal to be able to choose B or C or D until A again is encountered or reappears in the environment. Several species behave in this way. In the freshwater environment, the aquatic larvae of the moth Bellura will eat and thrive on white waterlily leaves if their preferred food of yellow waterlily leaves is not available (Welch, 1914), and caddis fly larvae will use for case building less preferred materials if deprived of more suitable ones (Gorter, 1929 ; Fankhauser and Reik, 1935; Hanna, 1961). The intertidal crustaceans Uca pugi- lator (Bosc) and Corophium volutator and the sublittoral species Calli- anassa islagrande Schmitt burrow in unfavourable sediments when presented with these or with even less suitable sediments (Teal, 1958; Meadows, 1964c; Phillips, 1971), the hermit crab Pagurus hirsutiusculu8 will accept less suitable gastropod shells if its preferred shell is not available (Orians and King, 1964), and the settling larvae of the marine polyzoan Bugula neritina L. will settle on slime-free surfaces although they normally avoid these if offered a choice (Miller, Rapean and Whedon, 1948). Radwin and Wells (1968, p. 81), after studying the prey preferences of seven species of muricid gastropods for the three species of bivalve, made an interesting distinction between three of the muricid species which were highly selective and fed on only one of the bivalve species, and two of the muricid species which although preferring one bivalve species would on occasion eat the other two. Concerning the latter species of muricids, Murex fulvescens Sowerby and Urosalpinx tampaensis, they state that ‘‘ when the supply of preferred prey was exhausted, these snails attacked the remaining bivalve prey with little selectivity, and when the bivalves were consumed, they attacked and consumed one another ”. Without further study it is difficult to weigh the disadvantages of not being willing to eat other

What happens if the preferred habitat A is not available?

HABITAT SELEOTION BY AQUA'I'ICJ INVERTEBRATES 339

food if one's preferred food is not available (the first group of muricids) against the disadvantages of being likely to eat members of one's own species (the second group of muricids). The concept could however, be extended to other aspects of habitat selection with certain modi- fications.

It would be naive to expect animals to differentiate between every variable they encounter in their environment, and yet few animals are known to show lack of preferences. The larvae of three polychaetes (Platynereis, Nereis and Polydora) settle equally well on a range of sediments (Kiseleva, 1967a, b), the larvae of the bivalve Chione cancellata L. metamorphose with or without contact with sediment although slightly earlier when sediment is present (D'Asaro, 1967), and the gregarious larvae of Sabellaria alveolata do not distinguish between tubes of their own species and those of 8. spinulosa (Wilson, 1968). The oncomiracidia larvae of the trematode Discocotyle sagittata do not appear to recognize their normal host, the brown trout (Paling, 1969), while adults of the gastropods Murex firifer and Urosalpinx perragatus Conrad fed equally readily on three species of bivalve they were offered as food, without apparent preference (Radwin and Wells, 1968). Pabricia sabella (Ehrenberg) (Polychaeta) do not distinguish between different particle sizes (Lewis, 1908), Heterocypris salinus cannot distinguish between waters of different oxygen content (Gaming, 1967) and Pontoporeia affinis Lindstr6m (Amphipoda) show no humidity preferences (Lagerspetz, 1963). Pontoporeia is a sublittoral amphipod and so may have no need of humidity preferences ; on the other hand it may be limited to the sublittoral region because it cannot detect dry air-animals stranded in the intertidal zone would in this case be killed by dehydration. As a final example, the beach amphipod Orchestoidea corniculata Stout does not detect the shore line of the beach by lunar orientation (Craig, 1970) in contrast to Talitrus maltator (Papi and Pardi, 1963), in fact, the animals are very quiescent at full moon (loc. cit. Table 2) and Craig argues that lunar orientation in this instance would have little biological value. The reasons for the other examples are obscure, but must have some ecological significance.

It can be seen, therefore, that a range of unexpected mechanisms may play a part in habitat selection. We have discussed the possible importance of coarse and fine selection, of indirect clues, and of the slope of a preference, and have considered what might happen if a suitable habitat were not available and also the result of an animal showing a lack of preference for a particular variable. All these offer new ways of investigating the mechanisms of habitat selection. How- ever the description of the three dimensional behaviour shown by many aquatic animals is likely to be a more difficult problem. The only topic which has received any detailed attention is that of the

340 P. S. MEADOWS AND J. I. CAMPBELL

hierarchical relationship between different choices investigated by Landenberger (1968) and we have attempted to show how this might influence the distribution of animals under natural conditions. Finally we have drawn a distinction between those habitats that differ only quantitatively and those that differ in qualitative characters.

VII. L E ~ N X N O , ENVIRONMENTAL HISTORY, AND

PHYSIOLO~ICAL STATE Habitat preferences may remain fixed throughout the life span of an

animal, or they may alter depending upon its physiological state, its age, its previous experience and learning, or its past and present environment (Lindroth, 1953). The evidence in favour of these possibilities will now be examined.

There are scattered references to changes in the habitat preferences of animals as they age (Crozier and Arey, 1918; Arey and Crozier, 1919), and of course a good example of this is the progressive change in general behaviour and responses to environmental stimuli of marine and freshwater larvae as they approach metamorphosis (Thorson 1964; Lehmann, 1972; above, p. 302). Amongst freshwater animals, newly liberated Asellus communis do not react to water currents (Allee, 1912), the young of Daphniapulex (De Geer) are more strongly photopositive and geonegative than are older individuals (Dice, 1914), and young Gammarus pulex (L.) are more sensitive to pH changes (Costa, 1967) while ecological studies in the marine environment show a change from gregarious to solitary behaviour amongst older individuals of the lobsters Jasus lalandei (H. Milne-Edwards) and Panulirus interruptus (Randall), and of the king crab Parulithodes camtschtica Tilesius (Fielder, 1965; Lindberg, 1955; Powell and Nickerson, 1965). Behav- ioural changes of this sort can often be related to the changing distribution of animals under natural conditions. The young of freshwater and marine planktonic species, for instance, usually occur higher in the water column than do older individuals (Welch, 1935, p. 225; Moore, 1958, p. 238), which can in part be explained by their stronger photo-positive responses (Dice, 1914; Clarke, 1932; Lucas, 1936).

Changes in habitat selection related to physiological state have occasionally been recorded and may not be unusual. Allee (1913a, b) publishing the same data twice, observed a single male Asellus communis change its behaviour to currents as it approached and passed through a moult : between moults it was usually rheopositive, while it became less so over the period of the moult. But this is really no more than one might expect for during the moult muscles must be released from the old cuticle and become functional only when the new


one has hardened. It is surprising therefore that similar behaviour has not been recorded for other Crustacea. Prehaps less expected are the changes in behaviour shown by starved invertebrates. A number of terrestrial invertebrates alter their habitat preferences as they are starved, but the only records of similar behaviour in aquatic invertebrates are those of Gee (1913) and Herter (1929) on freshwater leeches, of Hazlett (1966) on the marine hermit crab Calcinus tibicelz, of Jones and Naylor (1970) on the light responses of the intertidal isopod Eurydice pulchra Leach, and of Brun (1972) on the feeding of Luidia ciliaris. Although difficult to interpret ecologically, Crozier and Libby’s (1925) study on the physiology of feeding and starvation in the terrestrial slug Limax maximus L. may be relevant to future investigations on aquatic invertebrates. Limax maximus is usually photonegative, but after a meal of cooked potato becomes indifferent to light. The effect is mimicked by injection of M/10 sucrose into the body fluids or into the stomach via the mouth. Other foods including raw potato have no influence. Crozier and Libby inferred that the injected sugar was acting in the same way as the sugar released from the digestion of cooked starch.

A number of marine invertebrates show clearly defined learning abilities which may influence habitat selection (Thorpe, 1956 ; Wells, 1965). The brittle star Ophiothrix fragilis (Abildgaard) can be taught to turn back on encountering a smooth/rough substrate boundary or a wavy/smooth glass boundary (Diebschlag, 1938) and the starfish Pisaster giganteus can learn to associate a light stimulus with food (Landenberger, 1966). The spiny lobster Panulirus argus (Latreille) learns with a light stimulus to walk down a ramp to an aquarium containing sea water (Schtine, 1961) and individuals of a related species Palinurus vulgaris Latreille learn to eat the hermit crab Eupaguruus bernhardus (L.)-a food they never usually eat-when other food is scarce (Wilson, 1949). The recognition and association of certain types of substrate with, say, predators (Ophiothrix), the searching for food in shady areas of the bottom where food has previously been encountered (Pisaster), and the ability to learn new sources of food (Palinurus), will clearly be advantageous to these species in the sea and will influence their selection of habitats. Hazlett and Provenzano (1965) have analysed the role played by learning in the development of intraspecific aggression and ahell selection by young hermit crabs. They concluded that although individuals execute the appropriate movements (or behavioural units) the first time they meet another individual or attempt to enter a gastropod shell they need a number of encounters before learning to integrate these units into a coordinated


and successful behavioural sequence. It follows that young crabs are likely to be at a selective disadvantage compared to older ones and so it is interesting to find that the young of the spiny lobster Jasus Zalandei may experience a similar disadvantage (Fielder, 1965). In- vertebrates living in fresh water are likely to show similar abilities although there is very little evidence. Further investigations should be concentrated on the relationship between learning in laboratory experiments and habitat selection in the field. It would be interesting to know for example what ranges of shape, size, colour and so on a species can learn to recognize, and whether these do in fact occur in the species’ natural environment. Even at the present time it might be possible to make ecologically s igdcant deductions about the distribution of octopi from the detailed work already published on their learning abilities (Wells, 1962).

We should now turn to consider how an animals’ previous experience or previous environmental history affects its behaviour (Brown, 1939; Popham, 1941; above, pp. 290-291). The light reactions of several species of aquatic invertebrate are largely dependent on the conditions of illumination to which the animals have been previously exposed. The freshwater isopod AseZZzts communiis (Banta, 1910) and the intertidal gastropod Littorim littorea (L.) (Newell, 1958) are both photopositive when dark adapted but photonegative in the light; Newell, however, encountered a lot of variation amongst his animals and his paper should be consulted for further details. The physiological basis of the response has been investigated on the intertidal amphipod Cammarus annulatus S. I. Smith (Smith, 1905). Smith transferred dark adapted animals into the light and measured their responses to light and the migration of their eye pigment. During the &st 10 minutes they were indifferent to light, slightly photonegative, or slightly photopositive, and then subsequently became strongly photopositive; this latter change was associated with the time at which their eye pigment migrated from its dark adapted to its light adapted position. In a similar way an animal’s previous environmental history can influence its temperature preferences, its food preferences, and its aggressiveness. The temperature preferences of the freshwater gastropods Planorbis cornew rubra L. and Lirnnea stagnalis L. are related to their previous temperature rbgime (%bczyliski, 1966), Pacific starfish of the genus Pisaster show an increased preference for snails if they are fed on these for three months previously (Landenberger, 1968), and the aggressive tendencies of the hermit crab Calcinus tibicen are dependent on its previous experience (Hazlett, 1966) (see section on spacing out). Where past experience or past environmental history


does influence an animal’s behaviour, there are many ways in which it might interact with habitat selection to produce an observed pattern of distribution in the field. Very little is known of these interactions.

There are, however, some species whose preferences are clearly not affected by their previous experience. The intertidal snail Littorina obtwata prefers to eat Bucus spiralis L. and B. vesiculosus rather than F. serratus L. or Pelvetia canaliculata (L.) Dene et Thur. even when they are fed for 10 days beforehand on the latter two species of seaweed (Bakker, 1959). There are other examples. The particle size preferences of Corophium volutator are not affected by the particle size of the sediment they have previously lived in (Meadows, 1967), the microbial food preferences of the marine copepod Calanus heligolandicus Claus and of the larvae of the gastropod Nassarius obsoletus are not influenced by their previous diet (Mullin, 1963; Paulson and Scheltema, 1968), and the temperature preference of Podon polyphemoides Leuckart (Cladocera) does not appear to be influenced by their previous temperature regime (Ackefors and Rosen, 1970). It is quite reasonable to suggest that these results might have been different if the time during which the animals were conditioned before the experiments had been longer, but putting aside this criticism one may ask whether there are any factors common to those preferences that are influenced by previous experience as compared to those that are not. A detailed reading of the papers so far published has convinced us that there are no such factors.

There are a number of studies on terrestrial invertebrates in particular on insects that give an important insight into the way in which previous experience can influence habitat selection. These will almost certainly be relevant to future studies on aquatic invertebrates and so are considered here. Thorpe and Jones (1937) persuaded females of the endoparasitic hymenopteran Nemeritis canescens Gravenhorst, whose usual host is the moth Ephestia kuhniella Zeller, to oviposit in an unnatural host, the moth Meliphora grisella Fabricius. The resultant larvae developed normally, suffered no great mortality, and gave rise to adults whose morphology and colour was normal, and so Thorpe and Jones felt able to test the adults’ host preferences in a Y tube olfactometer. The preferences of adults reared in M. grisella were significantly different from normal adults. Although still preferring the smell of E . kuhniella to the smell of M . grisella they did so to a less marked degree, and in separate experiments preferred the smell of M . grisella to clean air-a distinction that normal adults could not make. The authors went on to rear N . canescens on the abnormal host M . grisella over a number of generations but failed

344 P. 5. MEADOWS AND J. 1. OAMPBELL

to show any progressive increase in its response to the abnormal host. In this sense, then, preimaginal olfactory conditioning is a phenotypic effect. More recently, Jermy, Hanson and Dethier (1968) have conducted analogous experiments. Both these examples are of experiments concerned essentially with biological conditions-an unusual host or food plant-but one can obtain the same effect using highly artificial factors such as the odour of peppermint (Thorpe, 1939; Crombie, 1942) and cedarwood oil (Thorpe, 1938), and so, to paraphrase Thorpe (1939) a new stimulus (odour) need not be related to any particular act such as feeding, oviposition or settlement, in order to produce a preference for itself. Research on this and related topics in aquatic environments would be very welcome, and must surely have relevance to the artificial culture of fish, molluscs and other commercial species. It might be possible, for instance, to induce plaice larvae to accept species A as food when they normally eat species B, so that they could be transplanted to sheltered inshore waters where environmental factors were propitious for their survival but where species A but not B were abundant. At a more academic level, Wecker's (1963) investigations into the role of early experience in habitat selection by the prairie deer mouse Peromyscus maniculatus Bairdi suggest another approach. Amphipods or other invertebrates having no larval stage could be hatched in the laboratory, reared in isolation from their natural environment, and then offered choices that field caught animals are known to respond to in a predictable way. Similar experiments could be undertaken with invertebrates having a larval phase although there might be practical difCiculties in rearing.

The responses of invertebrates to some environmental stimuli may alter either in direction or in intensity as a result of changes in other variables in their immediate environment (Russell, 1927, p. 248-251). The most labile of these are responses to light, and although we have already referred to some examples we will recapitulate in order to present a complete account. Acartia tonsa Dana, Parmalanus parvus (Claus) and Calanopia americana Dahl, three species of planktonic marine copepod studied by Lewis (1959), are indifferent to light between 16°C and 32°C-the annual range in their natural habitat-but are photonegative a t temperatures above 32°C and photopositive at temperatures below 16 "C. Two species of planktonic marine Crustacea studied by Lucas (1936) are increasingly photonegative in higher concentrations of the diatom Nitzchia closterium Ehrenberg-one of their usual foods. The water scorpion Ranatra fusca (Hemiptera) (Holmes, 1905) and the semi-terrestrial isopod Ligia italica (Perttunen, 1961) become increasingly photopositive at higher temperatures, while the reverse is true of Daphnia magna (Clarke, 19321, of the copepod


Temora longicornis (0. F. Muller) and also of the larvae of the archiannelid Polygordius (Loeb, 1893). The latter two animals, and the larvae of Palaernonetes (Loeb, 1906b), become photonegative if salinity falls, and will therefore be led away from low salinity river water that flows out over the more dense sea water in estuaries. Various species living in fresh water become photopositive as the concentration of CO, increases (Loeb, 1904; 1906a, b; Wodsedalek, 1911), the larvae of Palaemonetes behave in the same way to increases in pressure (Bohn, 1912). The responses of stream dwelling animals are also influenced by their immediate environment. Under experimental conditions Cam- marus pulex (L.) are less likely to move upstream at high current speeds or when food is available but not when more shelter is provided (Hughes, 1970), and Asellus species become less rheopositive as the oxygen concentration decreases and the carbon dioxide concentration increases (Allee, 1912) (c.f. Walker, 1906, pp. 26-7). It is interesting to note in passing that Allee describes a marked decrease on the percentage of positive responses to current by Asellus communis during the breeding season (c.f. Crozier and h e y , 1919, pp. 277-8), which is during the spring when currents are at their fastest; by this seasonal change of behaviour, therefore, Asellus cornmunis may be barred from fast flowing streams that it would otherwise have colonized. Finally, three species of intertidal gastropod of the genus Littorinu investigated by Gowanloch and Hayes (1 927) and Hayes (1 927) become less geonegative when desiccated which would lead them away from the upper and drier regions of the shore. The ecological significance of these switches in behaviour are usually obvious, but perhaps the clearest example of behaviour changing with environmental conditions is that of the burrowing activities of the marine shrimps Penaew axtecus and Penueus setiferus (Aldrich et al., 1968). In the laboratory, the postlarvae of P. aztecus burrow into substrates when the temperature is experimentally lowered from 25°C to 12-17°C and emerge again when the temperature is raised to 18-21-5"C, whereas, under the same conditions, the postlarvae of P. setiferw do not. The difference in their behaviour agrees closely with their distribution in the sea. Both species spawn at sea and their larvae develop there. In the Gulf of Mexico the postlarvae then move inshore to estuarine areas such as Galveston Bay, Texas, where they grow rapidly to subadult size before migrating offshore again to attain maturity and spawn. There is a marked difference, however, in the season at which postlarvae of the two species arrive in Galveston Bay. The postlarvae of P. setiferus arrive during summer when water temperatures are consistently warm (25-32OC) whereas most P. aztecus arrive during March and April when the bay is not only cool (15-25°C) but subject to drastic


temperature reductions (often to 12OC) caused by atmospheric cold fronts. Thus the postlarvae of P. uztecus are exposed to considerably lower and more changeable estuarine temperatures than those encountered by P . setiferus. Aldrich et al. suggest that burrowing by P . azteczcs postlarvae could extenuate the influence upon them of the temperature changes to which they are exposed and could also protect them from predators when their escape responses are slowed by the fall in temperature. They go on to consider circumstantial evidence which suggests that the postlarvae of P . uztecus may also burrow offshore during part of the winter, before entering shallower water.

Many intertidal animals behave differently in and out of water and will therefore show alterations in behaviour as they are continually covered and then uncovered by the tide. The molluscs Nussurius Ob8OletUS and Lepidochitonu cinerea are geonegative under water and geopositive out of water (Evans, 1951 ; Crisp, 1969), and Corophiurn volutator is geopositive and photonegative when crawling over surfaces out of water and photopositive when swimming in water (Barnes et ul., 1969; Meadows and Reid, 1966). Analogous behaviour changes have been noted for the amphipod Hawtoriw arenarim (Slabber) which is photopositive while swimming and photonegative when burrowing (Dennell, 1933) and for Littorina neritoides which, when under water, crawls towards light on the under surface of a rock but away from light on the upper surface (Fraenkel, 1927). These are all animals living in the sea or on the shore and it would be interesting to know of instances from the freshwater environment. Furthermore, the whole concept of invertebrates being able to switch their behaviour in contrasting situations is one that has not received the attention it deserves.

We have presented in this section clear evidence that aquatic invertebrates can learn, and have suggested how this might influence their selection of suitable habitats. Habitat selection is also influenced by the age, physiological state, previous experience, and the past and present environment of an animal although in some cases so little is known of aquatic invertebrates that one can only quote terrestrial parallels. As yet it is not possible to state how important or common these factors might be in the general processes of habitat selection in fresh waters and the sea ; however their listing should at least draw them to the attention of those planning or executing experiments.

VIII. INDIVIDUAL VARUTION, THE COLOMZATION OF

NEW HABITATS, AND THE ORIGYX OF NEW SPECIES The previous section emphasizes how variable many aspects of

habitat selection are, and how previous experience, learning, and the

HABITAT SELEUTION BY AQUATIU INVERTEBRATES 347

present environment of an animal can often determine to a large degree the behaviour of a species as it selects suitable habitats. In this h a 1 section we will consider the marked variation in behaviour shown by individuals of some species, and then go on to relate this and other topics to the possible ways in which animals may colonize new habitats and to the part habitat selection might play in the origin of new species.

Provided the surrounding environment is stable and the physiological state of the animals themselves is constant, then one generally assumes that within fairly broad limits the behaviour of any individual is much the same as any other individual of the same species. However in some cases this is not so, and i t will pay to examine these. It is possible to classify the recorded instances of individual variation in behaviour into three categories. In the hst , individuals of a species can show a range of behaviour rather analogous to a cline (Carter, 1951) where each individual has a repeatable and characteristic response to a particular stimulus but where different individuals show different degrees of response. Records of this type of behaviour amongst invertebrates living in aquatic environments are rare, although Walter (1907) measured the rate of movement of 10 Planaria under different light intensities and found their rates of movement different enough to allow each one to be identified.

In the second category one or two individuals in a population show responses which are atypical of the population as a whole, but which are very characteristic of that particular animal. As an example, the marine polynoid Acholoe astericola D. Ch. in general shows a strongly positive response by becoming very active and attempting to attach when presented with the tube feet of its host the starfish Astropecten irregularie (Pennant) but only responds slightly when presented with tube feet of other members of the order Phanerozonia (Davenport, 1953a). One animal however (animal no. 3 in Table la, loc. cit.) gave positive responses to all the starfish species tested. Several papers refer to occasional odd behaviour in populations of freshwater animals. One is on Asellus communis (Allee, 1913a) in which one or two individuals were as often rheonegative as rheopositive while most of the population were consistently rheopositive, and Walter (1 906) (Lymnaeus) and Kanda (1916b) (Physa) record other instances. Staropolska and Dembowski (1950) attempted to analyse the variability of the case building behaviour of the larvae of Molanna angustata Curtis by push- ing larvae out of their cases and observing how they reconstructed them. The successive cases of one particular larva were different from those of the others, being always constructed of smaller than normal sand grains. Furthermore, when the larvae were offered different sized

348 P. 9. MEADOWS AXD J. I. UAMPBEU

but similar shaped grains, or different shaped but similar sized grains, a few larvae were more discriminating than their fellows.

The third category consists of species in which animals are of two types present in approximately equal numbers. We will consider two examples of marine invertebrates and two of freshwater invertebrates, before discussing the pertinence of Wellington’s (1957, 1964) extremely interesting work on the western tent caterpillar Malacosoma pluviale (Dyar) for aquatic environments. Individuals of the marine planktonic copepod Centropages typicus are either persistently attracted to a light source, or after continuous exposure become indifferent to light (Johnson and Raymont, 1939). The other marine example comes from a commensal relationship. The Mediterranean hermit crab Dardanus arroaor often actively assists the sea anemone Calliactis parasitica (Couch) to transfer from another surface to its own molluscan shell. Ross and Sutton (1961b) distinguished between non- performing hermit crabs-which do not assist the sea anemone, and performing crabs that do. The former were usually male and the latter female. The first freshwater example is from an early paper by Pearl (1903) on Planaria. Individuals of the species he studied appeared to be either very active or rather sluggish, but they differed in more than this, for the active ones moved right through aggregations on encountering them and took no notice, while the sluggish ones turned towards aggregates when a short distance away, and joined them. The second example comes from a detailed study by Clarke (1930) on the light and gravity responses of Daphnia magm. Most individuals were photonegative and geopositive while a small number were consistently photopositive and geonegative (p. 126, loc. cit.).

One of the most detailed investigations on behavioural differences between individuals has been undertaken by Wellington (1957,1964) on the western tent caterpillar Malacosoma pluviale. Larvae emerging from egg sacs are of two types. Type I individuals are active, move in straight lines, and are capable of independent directed movements towards a light source. Type I1 individuals are sluggish larvae and move very little. The latter tend to sway about and turn frequently, exhibit no directed movement, and if placed in a beam of light huddle together. On the other hand, if one type I larva is added to a type I1 larval aggregation, it leads all the type I1 larvae along with it as it moves from place to place, until if the type I larva is taken away, the type I1 larvae huddle together again-illustrating a quite remarkable sequence of behavioural reactions. Type I larvae reach distant food in the laboratory more readily, and in the field disperse more rapidly than do type I1 larvae ; they also move more over the leaves they are eating,


and so leave a more ragged leaf than those left by the type I1 larvae. The comparative behaviour of colonies of the two types in the field is also noteworthy. Type I colonies construct several tents in a short time, and they space these and their feeding sites over distances of several metres, while type I1 colonies construct one tent and remain feeding on one leaf sometimes for more than 10 days. Following metamorphosis the type I larvae give rise to active adults, whereas adults from type I1 larvae are sluggish. Wellington’s detailed study is interesting in its own right, but quite clearly has broader implications for the study of behavioural differences between individuals of species living in the sea and fresh water, a field that has received very little attention.

Putting aside the possibility of observer or experimental error, it is at f i s t sight difficult to understand what function these behavioural differentiations might have, and we are not even certain whether our classification has any meaning apart from bringing order to scattered observations. Neither is it clear whether most of the recorded instances of individual variation are phenotypic or genotypic. However we do feel that some unusual behaviour patterns may be the means whereby in certain circumstances new environments are colonized, and thus may also play a part in speciation. These points will be discussed in detail below.

Although the behaviour of individuals within a species may vary in rather unexpected ways, in general species have recognizable behaviour patterns that they use to select their habitats. We should now turn to consider how these recognizable behaviour patterns differ between taxonomically closely related species occupying the same or different habitats. Reference will only be made to papers in which species within the same genus have been investigated. The studies of Powers (1914) on four species of freshwater crayfish (Cambarus), of Gowanloch and Hayes (1927) on three intertidal species of Littorina, of Meadows ( 1 9 6 4 ~ ) and Gamble (1971) on two Corophium species, of Williams (1958) and Aldrich et al. (1968) on three marine shrimps (Penaeius), of Jones (1970) on two species of intertidal isopod (Eurydice), and of Phillips (1971) on two species of Callianassa, demonstrate species differences in preferences mirroring the species’ ecological distribution, and in the same way there are differences in substrate preferences between the settling larvae of various Spirorbis species (Garbarini, 1936; de Silva, 1962), differences in the reaction to current of the settling larvae of Balanus species (Smith, 1946), and in fresh water, differences in the habitat preferences of the nymphs of two closely related mayfly species (Heptagenia) which are often found in the same part of a stream (Madsen, 1968). Other examples come from commensal relationships such as the


two Montacuta species studied by Gage (1966b) and the polynoid commensals belonging to the genus Arctonoe (Davenport, 1950; Davenport and Hickok, 1951). There is therefore clear evidence for closely related species having different habitat preferences which will separate them spatially in the field. Where these species are obviously sympatric, as are the two Heptagenia, the three Littorim species, the two Eurydice species, and some of the Spirorbis species, the differences may well be important in mitigating interspecific competition, and also have been important in the past, in preventing inter-breeding as the species diverged from each other.

However the behaviour of some sympatric species is not so widely different that it accounts for their spatial separation into different microhabitats. Larvae of the polyzoans Alcyonidium hirsutum (Fleming) and A . polyoum (RassaIl), for instance, both settle in largest numbers on Pucus serratus (Ryland, 1959). Spatial separation here might be maintained by the preferences of the larvae for slightly different convexities or for slightly different parts of the Fuczcs frond (Ryland, 1959, Tables 7 and 9). On the other hand spatial separation could be achieved by interspecific competition itself, although this does not appear to be common, and may therefore have less selective advantage than direct behavioural recognition of an appropriate habitat. Interspecific competition between closely related sympatric species has been observed in the laboratory between two species of the intertidal crab Uca and between two species of the freshwater crayfish Orwnectes (Teal, 1958; Bovbjerg 1964, 1970 respectively), and also in the field between two species of the barnacle BaZanus (Meadows 1969). Orconectes virilis (Hagen) and Orconectes immunis (Hagen) (Bovbjerg loo. cit.) are two North American species of crayfish having similar geographical ranges but different habitats-0. virilis inhabits rock or gravel in streams and lake margins, and 0. immunis inhabits mud in ponds and slow moving streams. In the middle stretches of the Little Sioux River (Minnesota and Iowa) where the two species are sympatric, each is restricted to its own habitat. Bovbjerg’s experiments prove that this is the result of interspecific competition. If each species is separately offered a choice of rock, gravel, and mud, they both prefer the rock, whereas if the two species are mixed and then offered the same choice 0. virilis prefers the rock as before but drives most of the 0. immunia onto the mud.

Having considered differences between sympatric species, it may now be asked whether sympatric subspecies show differences in their selection of habitats. We have only been able to find one instance. The two subspecies of Littorim obtusata, L. 0. olivacea and L. 0. citrina, live


on fucoids on rocky shores, olivacea in general living in the upper half and citrina in the lower half of the tidal zone, and both subspecies feed on the fucoids on which they are found. Van Dongen (1956) offered the two subspecies four species of Fucus that were zoned down the shore in the hope that the snails would choose species of Fwcus in keeping with their observed distribution. Unfortunately this was not the case, but in the present context the results are interesting for the two subspecies did show slightly Merent preferences. Studies on other subspecies such as those in the I o t e a group (Isopoda) and those in the cfarnmarzcs group (Amphipoda) would be worth while.

Differences in habitat preferences, then, can occur between closely related species living in the same environment, can extend to a subspecific level, and can sometimes be demonstrated between individuals within one population of a species. Two related topics now merit attention before we consider how habitat selection might be involved in speciation. These are the mechanisms by which populations of a species living in contrasting habitats select their appropriate habitat, and the mechanisms by which new environments are colonized.

Most species live in one easily recognizable habitat but on occasion a species is encountered living in two habitats that contrast strongly. Of course one explanation might be our inability to appreciate h e distinctions between two species (cf. Simon, 1968b), but putting this aside the problem is an interesting one. Perttunen (1961) discovered an isolated population of the intertidal isopod Ligia italica living in brackish water. Individuals from the brackish water population died when immersed in sea water while animals collected from the shore survived for many hours. Although the difference is physiological rather than behavioural, it does illustrate a contrast between animals from the two habitats. Corophium volutator commonly occurs on muddy intertidal shores, and in the laboratory has a rhythm of swimming activity with maxima during the early ebb tide. Morgan (1966) was able to coIIect a population from a non-tidal brackish pool environment which showed no such rhythm. The remaining examples are of larval behaviour, of a commensal relationship, and one of the behaviour of the freshwater isopod Asellus. The larvae of the marine polychaete Cirriformia tentaculata Montagu are usually accepted as being planktonic, but George (1 963) discovered a localized population in Southampton Water, England, whose larvae were all demersal, while larvae from a nearby population at Drakes Island were pelagic. These interesting observations prompted him to survey other areas in the neighbourhood to disoover how general the phenomenon was

352 P. 9. MEADOWS AND J. I. UAXPBELL

(George, 1967). Populations from other areas produced free swimming and demersal larvae from one and the same egg batch, and while the proportion of the two types was constant in different samples from a single brood it varied between broods. George was unable to separate the larvae morphologically but recorded a biochemical difference in the esterase pattern of the adults which might prove relevant. He suggested (loc. cit. 1967) that the population in Southampton Water which produced only demersal larvae might be genetically isolated from other populations and might have arisen from an initial colonization by a few demersal larvae from one brood. Unfortunately there are no genetic experiments on any freshwater or marine species on which to base this reasoning. The work of Bartel and Davenport (1956) and of Hickok and Davenport (1957) on different populations of the hesionid polychaete Podarke pugettensis living either free or commensal with the starfishes Patiria miniata or Luidia foliata has been referred to already in the section on commensalism and will not be discussed further here. The final example is of the isopod Asellus communis which lives in ponds among herbage and vegetation and also in streams and rivers. Animals collected from streams are consistently more rheopositive than animals from ponds (Allee, 1912).

We consider this particular field of habitat selection very important, and the few references we have been able to find suggest that populations of a species that live in contrasting habitats do show preferences in accordance with these contrasts. It is not known how the populations might have become initially separated. The separation might have been a result of the development of a geographical barrier, or might have been caused by mutant behavioural changes in the population or by the colonization of different habitats by a few aberrant individuals. Some of these processes at least are likely to be taking place as populations sporadically split off from a parent stock and move into new habitats. Indication of the way the initial separation may have arisen might come from a study of intertidal animals which have an extended vertical distribution on the shore and which, therefore, may be considered as living in different habitats when at either extreme of their range. The behaviour of individuals of three species of Littorina collected from extremes of their ranges accords with their habitats (Gowanloch and Hayes, 1927 ; Hayes, 1927) ; for example, those collected from higher levels of the shore were more photopositive and geonegative than those from lower levels.

The successful colonization of habitats that are new to a species cannot be very common, otherwise a large proportion of the range of habitats within a particular environment would eventually be colonized


by each and every species present. New habitats may suddenly become available to a species by changes induced by man-new wharfs, buoys, lighthouses, or by natural changes such as the shifting of a sand bank, the gradual silting up of an estuary, or the appearance of new sources of food. The ecological consequences of changes of this sort in aquatic environments have been followed by Kitching (1937), Pyefinch (1943), Holme (1949), Boaden (1962) and Landenberger (1967) but have not been analysed experimentally. What really amounts to a recolonization of old habitats can also occur after short periods of environmental catastrophe, such as the 1962163 cold winter in Britain, and again the consequences have been described (Bradley and Cooke, 1958 ; Webb, 1968a ; Crisp, 1964). Members of a species are sometimes forced to move out to new habitats by population pressure and the phenomenon is well known in the terrestrial environment, but has not been systematically investigated in the sea or fresh water except by Bovbjerg (1964). New habitats may also be colonized in aquatic environments by a process akin to olfactory conditioning in insects (see above) : a group of animals might not for one reason or another be able to find their normal habitat or host, and might then make do with something less suitable. Once in the less suitable habitat the animals might then become conditioned to it in preference to their original habitat, and so remain (Meadows and Campbell, 1972). Obviously this sequence of events is a matter of some speculation, but enough is known of conditioning in insects to make the speculation feasible.

Spontaneously occurring mutations changing a pattern of behaviour will almost certainly influence the responses of a species to its environment, and probably to a great enough extent to allow colonization of new habitats that might then become the permanent home of the mutant. There is enough evidence from the terrestrial environment at least, to support this hypothesis. A number of Drosophila mutants respond differently to light intensity and wavelength (McEwen, 1918; Brown and Hall, 1936; Volpe et al., 1967) and also to a combination of light and humidity (Waddington et al., 1954). The only aquatic example is of the behaviour of mutant Gammarus chevreuxi Sexton towards light (Wolsky and Huxley, 1932). These are all responses to the physical environment ; however there are also instances where mutation appears to change the behaviour of an animal to its biological environment. We consider that the changed activity and mating behaviour of Drosophila mutants (Bastock, 1956), and of the mutants of the moth Panaxia dominula (L.) (Sheppard, 1952) fall into this category. Studies on behavioural mutants of aquatic invertebrates would be rewarding. It would be very interesting, for instance, to find


mutants of sedentary marine invertebrates whose larvae displayed unusual gregarious or territorial patterns of behaviour.

If a species colonizes a new type of habitat by a process not dependent on genetic change, for example by new habitats suddenly becoming available or because of population pressure, one may ask whether over a number of generations the new habitat can change the preferences of the species to such an extent that it prefers the new to the old habitat and can survive more successfully in it.

There are no studies relating to this topic on aquatic invertebrates. However, several investigations on terrestrial animals have been designed to answer these questions and can now be considered. They fall into two categories. In the first, a species is reared for a number of generations in or on a particular habitat and then offered a choice of this habitat with another. Sladden and Hewer (1938) have demonstrated an alteration in the food preferences of the stick insect Carausius (Dixippus) mrosus (Br.) for privet and ivy leaves in this way and four other examples are quoted by Dethier (1954, p. 43). On the other hand Morimoto (1939) and Wood (1963) in analogous experiments on other insects were unable to show any changes in preferences. In the second category, animals are bred for a number of generations and at each generation are given a choice of two habitats, A and B, the subsequent generation always being bred from only those animals that chose A. At the end of the experiment the population is given a choice of A and B on the assumption that it will prefer A to a greater extent than would an unselected population. If two populations are run in parallel, then one is selected for the A choice and the other for the B choice; at the end of the experiment both populations are offered the choice of A and B in the hope that the population selected for A will prefer A to B and the population selected for B will prefer B to A. There are furfher permutations of this type of experiment, but these need not concern us here. Successful experiments falling into this category have been performed by Eloff (1936), Wilkes (1942), Dob- zhansky and Spassky (1962), Connelly (1966) and Ogden (1970), on the preferences of insects for water, temperature, gravity, and on activity respectively. In at least one instance the changed preferences selected for over a number of generations have been correlated with genetic changes in the population (Dobzhansky and Spassky, 1962, 1967; Ehrman et ab., 1965; Dobzhansky et al., 1969), and it is genetic changes of this sort which may in some cases prelude the origin of new species.

Any part that habitat selection might play in the initial steps of speciation can clearly occur only during sympatric speciation, that is,

HABITAT SELECTION BY AQTJATIU INVERTEBBATES 355

when two incipient species are separating in the same environment (Hinde, 1959) and so, allopatric origin of new species, where separation takes place by the development of geographic barriers over long periods of time, need not concern us.

Perhaps the most probable way habitat selection may initiate or assist sympatric speciation is by leading animals to new local habitats which might then result in the formation of new breeding populations (Meadows and Campbell, 1972). However the individuals in the new colony must be prevented from periodically returning to the parent population if they are to have a reasonable chance of evolving into a new species. Now this could conceivably take place by an alteration in the local environment such as the isolation of a sand bank by shifting sediments in an estuary, but environmental change of this sort when it occurs may not be permanent. The effective isolation of a colony would of course be straightforward if the colony had originated from a mutant line whose behaviour and habitat selection had thus been genetically altered, and we have given examples of mutants that fall into this category. If the new colony came from some of the aberrant individuals known to occur in populations of certain species, effective isolation would be more difficult, although once set in motion the process could be reinforced by something analogous to olfactory conditioning in insects. But more than this is likely to be needed since there would still be very little to prevent individuals from the new colony returning to the parent population. A genetic change in behaviour would on the other hand prevent the return, and this is exactly what has been described by Dobzhansky and his co-workers as occurring in populations of Drosophila selected for particular behaviour traits over a number of generations.

IX. CONCLUSION The evidence we have presented in this review shows that the local

distribution of most aquatic invertebrates is determined by their behavioural reactions to their environment. Animals respond to a wide range of physical and chemical variables such as temperature, light and salinity as well as to their biological environment which includes encounters with their own and other species, with plants and micro-organisms, with their food, and with predators or prey. Upon this background of the interplay between behaviour and environment is superimposed variation caused by age , previous experience, physiology, individual variation, and so on. Animals therefore test and select their habitats according to a complex set of rules. An explanation of animal distribution in terms of animal behaviour


must therefore await a detailed understanding of these rules and of their interactions. The authors have speculated that this might also come from a predictive mathematics which would correlate behaviour with distribution by matching the classical concepts of probability and statistics, perhaps expressed pictorially by a series of response surfaces (Box and Wilson, 1951 ; Box, 1954), with the advanced cybernetics and computer technology at present available. Although concerned with the modelling of field distributions themselves rather than with models which interpret field distribution in terms of habitat selection, the works of Skellam (1951), Watt (1968), Siniff and Jessen (1969) and Kitching (1971) illustrate both the benefits and the limitations of the approach.

One of the functions of the present review has been to outline areas where more research is needed. It is really quite surprising, for instance, that there are so few comprehensive studies on any one species, that so little is known of habitat selection by sublittoral benthic invertebrates in the sea, that we know nothing of the reactions of freshwater invertebrates to the microbial fauna of sediments, and that conditioning, the genetics of habitat selection, and the colonization of new habitats in aquatic environments have received so little attention.

In the long term, studies on habitat selection, in other words on the behaviour which results in animals being found in particular places a t particular times, are bound to be of great economic importance. Before fish can be farmed efficiently or molluscs and crustaceans cultured successfully, their choice of habitats, their preferred foods, their avoidance of predators and their gregariousness must be understood in detail.

x. SUMMARY

1. The present review attempts to explain the field distribution of marine and freshwater invertebrates in terms of their behaviour and habitat selection.

2. Habitat selection is considered firstly in relation to the non- biological, or chemical and physical, environment.

(a) Intertidal invertebrates react to a wide range of environmental variables which will tend to restrict them to localized areas of the shore. Their responses to light, to gravity and pressure, and to the particle size of sediments are fairly well documented, but less is known of their salinity, temperature, or humidity preferences, or of their responses to anaerobic conditions. The depth of sediments, their packing characteristics, and their degree of dryness appear to be important to the few burrowing invertebrates that


have been investigated. Some intertidal invertebrates maintain themselves in one position on the shore as the tide moves over them, while others move up and down with the advancing or receding water’s edge ; in most cases the patterns of behaviour determining these distributions are not understood.

( b ) There is in general less experimental evidence for habitat selection by sublittoral marine invertebrates. The light and pressure responses of planktonic species are well known ; however, the responses of benthic invertebrates to temperature, salinity, currents, gravity, density discontinuities and to the characteristics of sediments (packing, depth, surface charge, particle size), have rarely been recorded.

(c) Many freshwater invertebrates choose their habitats by responding to current speed, to light, to the nature ofthe bottom, and to contact with solid objects. Less is known of their temperature, humidity, or salinity preferences, or of their reactions to anaerobic conditions and pH changes, or of the preferences of burrowing animals for varying depths of sediment. Responses to ions and organic molecules in solution and to the packing characteristics of sediments have not been studied.

(d) Interstitial animals (invertebrates and Protozoa) live in the spaces between grains in freshwater, intertidal, and marine sandy sediments. Their behaviour suggests that temperature, light, salinity, oxygen content, sand permeability, pore size and particle size, play a significant part in their selection of habitats.

3. The maintenance of parasitic and in particular of commensal associations in the marine environment has received much attention, but little is known of freshwater associations, or of the way any of these associations are initiated. The responses of commensals to their non- biological environment appear to be similar to free living animals, and most associations depend on specific chemical stimuli detected at a distance from or on contact with the host. The nature of the chemicals is not known. A few commensals can live with more than one host species ; their specificity to and success on the different hosts is not clearly understood.

4. Aquatic invertebrates respond to information from a number of sources in their biological environment.

(a) The behaviour of the larvae of marine benthic invertebrates at settlement is very similar and is described. The responses of

A . M . B . - ~ ~ 13

358 P. 5. MEADOWS AND J. I. CAIWBELL

larvae to their physical environment have not been considered as they are listed by Williams (1964, 1966). Many larvae are gregarious, and settle near adults of their own species in response to species specific chemicals present on or possibly emanating from the adults. The chemical nature of the substances has been studied. The mobile adults of some species of marine and freshwater invertebrates are gregarious. One or two species change their behaviour when near other members of their own species ; these changes increase the probability of aggregations forming ; we have therefore termed the phenomenon indirect gregariousness.

(b) The larvae and adults of some species of aquatic invertebrates, most of which are also gregarious, maintain a minimum distance from each other (space out), while the adults of others show well d e h e d aggressive behaviour. Spacing out behaviour may be related to the secretion of repellent chemicals. The interaction of gregarious and spacing out behaviour has not been investigated.

(c) The larvae of marine invertebrates that occur on seaweeds can recognize their preferred seaweed by species specific chemicals. Some species of seaweed appear to contain inhibitory chemicals. Many freshwater invertebrates live on or in plants, but few of these associations have been analysed.

(d ) Marine larvae that settle under experimental conditions in response to chemicals which are specific either to their own adults or to a particular species of seaweed, seem in most instances to detect the chemicals only after contact with the solid surfaces to which the chemicals are adsorbed.

(e) The larvae of adults of burrowing intertidal and marine invertebrates recognize their characteristic sediments in part by the nature of the associated microbial fauna; this fauna can be extremely complex but has only been studied in detail on sand grains.

(f) Micro-organisms form a film on flat surfaces in fresh waters and in the sea. The larvae of sedentary marine invertebrates have a confusing array of responses to this a m .

(9) Nothing is known of the responses of freshwater invertebrates to the microbial fauna of sediments or to the microbial film on flat surfaces.

(A) The food preferences of mobile herbivorous and carnivorous species, and the responses of prey species to their predators,


have been discussed. It is clear that these preferences and responses will affect the distribution of animals under natural conditions. In no case has the response of a predator species to its prey, and of a prey species to its predator, been investigated for the same pair of species.

(i) Some intertidal invertebrates migrate from and return to a recognizable site on the shore. The basis of these homing migrations is not fully understood.

(j) There are very few studies on the oviposition preferences of aquatic invertebrates.

5. Although there is in total a large body of work on the habitat selection of aquatic invertebrates in relation to their non-biological and to their biological environment, there are very few comprehensive studies which present a complete picture of the habitat preferences of a species, and few investigations in which laboratory experiments have been correlated both with field distribution and with experiments conducted under field conditions.

6. Most aquatic invertebrates choose habitats that are well within their lethal limits. The exceptions, where species appear to prefer habitats that will eventually kill them, are not easy to explain.

7. Very little is known of any changes in physiology associated with animals living in favourable as compared to less favourable habitats. The gastropod mollusc Haliotis discus hunnui, one of the few speci.es studied in any detail, grows fastest and is more likely to reach sexual maturity when fed on its preferred species of seaweed food.

8. A number of unexpected factors may play a part in habitat selection and can be listed as follows: indirect clues, slope of a preference, lack of preference, lack of suitable habitat, coarse and fine selection, three dimensional behaviour, qualitative and quantitative differences between choices, and hierarchies of choice.

9. The habitat that an animal selects may depend on its age, its physiological state, its learning and previous experience, and its past and present environment.

10. The behaviour of some species shows a great deaI of individual variation. This may take the following forms: (a) each individual may have a characteristic response to a particular stimulus but Werent individuals may show Werent levels of response; ( b ) one or two individuals in a population may behave atypically ; (c) individuals may belong to two or more behavioural types present in the population in approximately equal proportions. It is not clear whether these variations have a genetic basis.

360 P. 9. MEADOWS AND J. I. CAMX'BELL

11. The habitat preferences of closely related species living in different habitats correspond to their habitat. When the species a10 sympatric, that is, are living in the same locality, their different preferences will be important in mitigating interspecific competition. Interspecific competition will be more important where there is no difference in preferences. Differences in habitat preferences can extend down to a subspecific level.

12. A species occasionally lives in two contrasting habitats. Individuals from the contrasting habitats have contrasting habitat preferences.

13. Habitat selection by behavioural mutants is discussed. 14. New habitats may be colonized by individuals whose behaviour

is atypical of the species, by mutant individuals, or by animals becoming conditioned to an initially unfavourable habitat (cf. olfactory conditioning in insects).

16. The role of habitat selection in the sympatric origin of new species is considered.

XI. ACKNOWLEDGMENTS

We would like to thank Dr J. G. Amos, Dr A. D. Boney, Dr R. A. Crowson, Dr W. D. Edgar, Dr A. F. G. Dixon, Dr J . S. Gray, Dr A. R. Hill, Mr J. B. C. Jackson, Dr T. A. Norton, Dr A. Manning, Dr J. S. Ryland, Dr D. P. Wilson, Dr J. D. Woodley, for their comments and criticism, and Sir Frederick Russell and Sir Maurice Yonge for their advice during preparation of the manuscript. We would also like to thank Mrs A. Bird for invaluable help in the literature survey, Miss E. Macartney for translating many German papers, and Mrs P. F. Rowan, Miss C. Swarm and, in the latter stages, Miss M. T. Emerson, for their help in the preparation of the article.

The final preparations of parts of this paper were undertaken by correspondence between J.I.C. and P.S.M. while one of us (P.S.M.) was on a sabbatical year's leave of absence from the University of Glasgow (1970/71). He is grateful to the Nuffield Foundation for financial support in the form of a Travelling Fellowship in Tropical Marine Biology which enabled him to visit the West Indies, and also to Professor Ivan Goodbody, of the Department of Zoology, University of the West Indies, Jamaica, for his unstinting help in many directions. The authors gratefully acknowledge a grant from the Royal Society to purchase an underwater camera and diving equipment which enabled many animals to be observed in their natural habitats.


XII. REFERENCES Ackefors, H. and RosBn, C.-G. (1970). Temperature preference experiments

with Podon polyphemoides Leuckart in a new type of alternative chamber. J . exp. mar. Biol. Ecol. 4, 221-228.

Aldrich, D. V., Wood, C. E. and Baxter, K. N. (1968). An ecological interpretation of low temperature responses in Penaeus aztecua and P. seiiiferwr post larvae. Bull. mar. Sci. 18, 61-71.

Allee, W. C. (1912). An experimental analysis of the relation between physiological states and rheotaxis in Isopoda. J . exp. 2001. 13, 269-344.

Allee, W. C. (1913a). Further studies on physiological states and rheotaxis in Isopoda. J . exp. 2001. 15, 257-295.

Allee, W. C. (1913b). The effect of moulting on rheotaxis in Isopods. Science,

Allee, W. C. (1914). The ecological importance of the rheotactic reaction of stream Isopods. Biol. Bull. mar. biol. Lab., Woods Hole, 27, 52-66.

Allee, W. C. (1927). Studies in animal aggregations: some physiological effects of aggregation on the brittle starfish, Ophioderma breviapina. J . exp. Zool. 48, 475-495.

Allee, W. C. and Stein, E. R. (1918). Light reactions and metabolism in mayfly nymphs. I. Reversals of phototaxis and the resistance to potassium cyanide. 11. Reversals of phototaxis and carbon dioxide production. J . exp. 2001. 26, 423-458.

Allen, J. A. (1966). The rhythms and population dynamics of decapod Crustacea. Oceanogr. Mar. Biol. Ann. Rev. 4, 247-265.

Allen, W. R. (1923). Studies of the biology of freshwater mussels. 11. The nature and degree of response to certain physical and chemical stimuli. Ohio J . Sci.

Ambiihl, H. (1959). Die bedeutung der Stromung als okologischer Faktor. Schweiz. Z . Hydrol. 21, 133-264.

Amos, T. G. (1969). Reactions of Carpophiha spp. (Coleoptera, Nitidulidae) to humidity with reference to gradient steepness. Anim. Behav. 17, 9-13.

Amos, T. G. and Waterhouse, F. L. (1969). The distribution and biology of Tribolium castaneum (Coleoptera, Tenebrionidae) on temperature gradients varying in steepness. Entomologia exp. appl. 12, 44-52.

Anderson, J. G. and Meadows, I?. S. (1969). Bacteria on intertidal sand grains. Hydrobiologia, 33, 33-46.

Ansell, A. D. and Trevallion, A. (1969). Behavioural adaptations of intertidal molluscs from a tropical sandy beach. J . exp. mar. Biol. Ecol. 4, 9-35.

h e y , L. B. and Crozier, W. J. (1918). The " homing habits " of the pulmonate mollusk Onchidium. Proc. natn. Acad. Sci., U.S.A. 4, 319-321.

Amy, L. B. and Crozier, W. J. (1919). The sensory response of Chiton. J . exp.

Amy, L. B. and Crozier, W. J. (1921). On the natural history of Onchidium. J . exp. 2001. 32, 443-502.

Bainbridge, R. (1952). Underwater observations on the swimming of marine zooplankton. J . mar. biol. Ass. U.K. 31, 107-112.

Bakker, K. (1959). Feeding habits and zonation in some intertidal snails. A r c h n8erl. 2001. 13, 230-257.

Balfour-Browne, F. (1922). On the life-history of Melittobia acmta, Walker; a Chalcid parmite of bees and wasps. Parasitology, 14, 349-370.

N . Y . 37, 882-883.

23, 57-82.

2001. 29, 157-260.

362 P. 9. MEADOWS AND J. I. Cl-BELL

Banta, A. M. (1910). A comparison of the reactions of a species of surface isopod with those of a subterranean species. Part I. Experiments with light. J . exp. 2001. 8, 243-310.

Barnes, T. C. (1932). Salt requirements and space orientation of the littoral isopod Zgia in Bermuda. BWE. Bull. mar. biol. Lab., Woods Hole, 63, 496-504.

Barnes, T. C. (1934). Further observations on the salt requirements of Ligia in Bermuda. Biol. Bull. mar. biol. Lab., Woods Hole, 36, 124-132.

Barnes, T. C. (1938). Experiments on &iCG in Bermuda. V. Further effects of salts and of heavy sea water. Biol. Bull. mar. biol. Lab., Woo& Hole, 74,

Barnes, W. J. P., Burn, J., Meadows, P. S. and McLusky, D. S. (1969). Corophium volutator-an intertidal crustacean useful for teaching in schools and universities. J . biol. Eduo. 3, 283-298.

Bartel, A. H. and Davenport, D. (1966). A technique for the investigation of chemical responses in aquatic animals. Br. J. Anim. Behuv. 4, 117-119.

Bastock, M. (1966). A gene mutation which changes a behaviour pattern. Evolution, 10, 421-439.

Bauer, V. (1913). Zur Kenntnis der Lebensweise von Pectenjacobmus L. Zool. Jb.

Bayne, B. L. (1963). Responses of MytiZua edulis larvae to increases in hydro-

Bayne, B. L. (1964). The response of the larvae of Mytilua edulis (L.) to light and

Bayne, B. L. (1969). The gregarious behaviour of the larvae of Ostrea edulis L.

Blake, J. A. (1969). Reproduction and larval development of Polydora from

Blake, J. W. (1960). Oxygen consumption of bivalve prey and their attractive-

Boaden, P. J. S. (1962). Colonization of graded sand by an interstitial fauna.

Boaden, P. J. S. (1963). Behaviour and distribution of the archiannelid

Bohn, M. G. (1912). La sensibilit6 des animaux aux variations de pression.

Bovbjerg, R. V. (19628). Ecological aspects of dispersal of the snail Campeloma

Bovbjerg, R. V. (1962b). Comparative ecology and physiology of the crayfish Orconectecr propinquua and C a m b m fodiens. Phyeiol. Zool. 25, 34-66.

Bovbjerg, R. V. (1963). Dominance order in the crayfish Orconectes wirilis (Hagen). Physiol. Zool. 26, 173-178.

Bovbjerg, R. V. (1959). Density and dispersal in laboratory crayfkh populations. Ecology, 40, 504-606.

Bovbjerg, R. V. (1960). Behavioural ecology of the crab, Pachygrapm craesipes. Ecology, 41, 786-790.

Bovbjerg, R. V. (1964). Dispersal of aquatic animals relative to density. Verh. int. Verein. theor. angen. Limnol. 15, 879-884.

Bovbjerg, R. V. (1966). Feeding and dispersal in the snail Stagnicola reflexa (Basommatophora : Lymnaeidae). Malacologia, 2, 199-207.

Bovbjerg, R. V. (1968). Responses to food in Lymnaeid snails. Physiol. Cool. 41, 412423.

108-1 16.

33, 127-149.

static pressure. Nature, Lond. 198, 406-407.

gravity. Oikos, 15, 162-174.

at settlement. J . mar. biol. Ass. U .K . 49, 327-366.

Northern New England (Polychaeta : Spionidae). Ophelia, 7, 1-63.

ness to the gastropod Urosalpinx cinerea. Limnol. Oceanogr. 5, 273-280.

Cah. Biol. mar. 3, 246-248.

Trilobodrilua heideri. J . mar. biol. Ass. U.K. 43, 239-260.

C.r. hebd. S&m. A d . Soi., Paris, 154, 240-242.

d m k m . Ecology, 33, 169-176.

HABITAT SELEOTION BY AQUATI0 INVERTEBRATES 363

Bovbjerg, R. V. (1970). Ecological isolation and competitive exclusion in two crayfish (Orconectea virilk and Orconectea immunk). Ecology, 51, 226-236.

Box, G. E. P. (1964). The exploration and exploitation of response surfaces : some general considerations and examples. Bimetrice, 10, 16-60.

Box, G. E. P. and Wilson, K. B. (1961). On the experimental attainment of optimum conditions. Jl R. statist. SOC. 13, 1-46.

Braams, W. G. and Geelen, H. F. M. (1963). The preference of some nudibrancha for certain coelenterates. Arch. nderl. 2001. 10, 241-262.

Bradley, W. H. and Cooke, P. (1968). Living and ancient populations of the clam (Oemma gemma) in a Maine coast tidal flat. Fiah. Bull. 137, 306-334.

Brown, F. A. (1939). Background selection in crayfishes. Ecology, 20, 607-616. Brown, F. A. and Hall, B. V. (1936). The directive influence of light upon

Drosophila rnelanogaater Meig and some of its eye mutants. J . exp. Zool. 74, 206-220.

Brun, E. (1972). Food and feeding habits of Luidia ciliark Echinodermata: Asteroidea. J . mar. bwl. Ass. U.K. 52, 226-236.

Bullock, T. H. (1963). Predator recognition and escape responses of some intertidal gastropods in presence of stari%h. Behccviour, 5 , 130-140.

Burns, C. W. (1969). Particle size and sedimentation in the feeding behaviour of two species of Daphnia. Limnol. Oceanogr. 14, 392-402.

Cameron, A. M. (1966). Some aspects of the behaviour of the soldier crab Mictyria longicarpus. Pwq. Sci. 20, 224-236.

Campbell, J. I. and Meadows, P. 8. (1972). An analysis of aggregations formed by the caddis fly larva Potamophylax Icctipennis in its natural habitat. J. ZooZ., Lond. in press.

Carefoot, T. H. (1967). Growth and nutrition of Aplysia punctata feeding on B

variety of marine algae. J . mar. biol. Ass. U.K. 47, 666-689. Carefoot, T. H. (1970). A comparison of absorption and utilisation of food

energy in two species of tropical Aplysia. J . exp, mar. Biol. Ecol. 5 , 47-62. Carliele, D. B. (1957). On the hormonal inhibition of moulting in decapod

Crustacea. 11. The terminal aneodysis in crabs. J. mar. biol. Ass. U.K. 36,

Carriker, M. R. (1967). Preliminary study of behaviour of newIy hatched oyster

Carter, G. S. (1961). “Animal Evolution”. Sidgwick and Jackson, London. Carton, Y . (1964). SpBcXcitB relative a l’int6rieur de l’espbce Stellicola olausi

(Rosoll), copBpode cyclopoide parasite des deux stellBrides Marthateria ghialk (L.) et Asterha gibbosa (Perm.). Arohs 2001. ezp. gdn. 103, Notes et Revue 1, 13-19.

Sp6cXcit6 parasitaire de Sabelliphilw aarsi, parasite de Spirographia spallanzani. 11. RBactions histopathologiques des hbtes lorn des contaminations experimentales. A r c h Zool. exp. gdn. 108, 387-411.

Specificit6 parasitaire de Sabelliphilw sarsi, parasite de Spirographia spallanzani. 111. Mise en Bvidence d’une attraction biochimique du copBpode par l’ann6lide. A r c h 2001. exp. gdn. 109, 123-144.

Carton, Y. (1968b). Sp6cificit6 parasitaire de Sabelliphilw sarsi, parasite de Spirographia spallanzani. N. gtude biochimique des hbtes et de leurs 86cr6tions. A r c h 2001. exp. 9th. 109, 269-286.

Carton, Y . (19680). Gtude exp6rimentale de l’infestation d’Arnphipholi8 8qWmUtU Delle Chiaje (Ophiuride) par Cancerilh ttdndata Dalyell (Copdpode Cyclopoide). Cah. Biol. mar. 9, 269-284.

291-307.

drills, Urosalpinx cinerea (Say). J . El&ha Mitchell scient. Soc. 73, 328-351.

Carton, Y . (1967).

Carton, Y. (1968a).

364 P. 9. MEADOWS AND J. I. CAMl’BELL

Castilla, J. C. and Crisp, D. J. (1970). Responses of Asteriaa rubem to olfactory

Caullery, M. (1952). Parasitism and Symbiosis. Sidgwick and Jrtckson, London. Cendaiia, S. M. (1937). Studies on the biology of Coccophagua (Hymenoptera),

a genus parasitic on nondiaspidine Coccidae. Univ. Calif. Publs Ent. 6, 337-399.

Chapman, G. (1949). The thixotropy and dilatancy of a marine soil. J . mar. biol.

Chapman, G. and Newell, G. E. (1947). The r81e of the body fluid in relation to movement in soft-bodied invertebrates. 1. The burrowing of Arenicola. Proc. R. Soo. B. 134, 431-465.

Chapman, G. and Newell, G. E. (1949). The distribution of lugworms (Arenicola marina L.) over the flats at Whitstable. J . mar. biol. Ass. U.K. 28, 627-634.

Clarke, G. L. (1930). Change of phototropic and geotropic signs in Daphnia induced by changes in light intensity. J . exp. Biol. 7, 109-131.

Clarke, G. L. (1932). Quantitative aspects of the change of phototropic sign in DqhnicC. J . exp. Biol. 9, 180-211.

Clark, R. B. (1956). The eyes and the photonegative Lehaviour of Nephtys (Annelida, Polychaeta). J . exp. Biol. 33, 461-477.

Clark, R. B. (1959). The tubicolous habit and the fighting reactions of the polychmte Nereia pelagica. Anim. Behav. 7 , 85-90.

Clark, W. C. (1968). Escape responses of herbivorous gastropods when stimulated by carnivorous gastropods. Nature, Lond. 181, 137-138.

Cloudsley-Thomson, J. L. (1962). “Rhythmic activity in animal physiology and behaviour”. Academic Press, London.

Clutter, R. I. (1969). The microdistribution and social behavior of some pelagic mysid shrimps. J . exp. mar. Biol. Ecol. 3, 126-165.

Cobb, J. S. (1971). Theshelter-relatedbehavior ofthelobster, Homarwamericanua.

Cole, H. A. and Knight-Jones, E. W. (1939). Some observations and experiments on the setting behaviour of larvae of Ostrea edulis. J . Cona. Perm. int. Explor. Mer, 14, 86-105.

Cole, H. A. and Knight-Jones, E. W. (1949). The setting behaviour of larvae of the European flat oyster Ostrea edulis L., and its influence on methods of cultivation and spat collection. Fishery Invest. Lond. (Ser. 2) 17, no. 3, 1-39,

Connell, J. H. (1963). Territorial behavior and dispersion in some marine invertebrates. Researches Popul. Ecol. Kyoto Univ. 5, 87-101.

connolly, K. (1966). Locomotor activity in Drosophila. 11. Selection for active and inactive strains. Anim. Behav. 14, 44P449.

Cook, A,, Barnford, 0. S., Freeman, J. D. B. and Teideman, D. J. (1969). A study of the homing habit of the limpet. Anim. Behccv. 17, 330-339.

Cook, R. H. and Boyd, C. M. (1966). The avoidance by Gammarua oceanicua SegerstrAle (Amphipoda, Crustacea) of anoxic regions. Can. J . 2001. 43,

The olfactory reactions and organs of the marine snails Alectrion obsoleta (Say) and Busycon canaliculatum (Linn.). J . exp. 2001. 25,

Costa, H. H. (196613). Salinity responses of two species of Ceylon freshwater atyid shrimps. Ceylon J . Sci. biol. Sci. 6 , 33-36.

Costa, H. H. (196613). Thermal sensitivity and response in two species of freshwater Caridina. Hydrobwlogia, 28, 583-588.

Costa, H. H. (19674. Responses of Gammarw pulex (L.) to modified environment. 11. Reactions to abnormal hydrogenion concentrations. Crwtaceana, 13,l-10.

stimuli. J . mar. bid. A88. U.K. 50, 829-847.

Ass. U.K. 28, 123-140.

Ecology, 52, 108-116.

971-976. Copland, M. (1918).

177-227.


Costa, If. H. (1967b). Responses of Gammarwpulex (L.) to modified environment. 111. Reaction to low oxygen tensions. Crwtaceana, 13, 176189.

Craig, P. C. (1970). The behaviour and distribution of the intertidal sand beetle Thinopinus pictzcs (Coleoptera : Staphylinidae). Ecology, 51, 1012-1017.

Crane, J. (1958). Aspects of social behavior in fiddler crabs, with special reference to Uca maracoani (Latreille). Zoologica, N . Y . 43, 113-130.

Crisp, D. J. (1955). The behaviour of barnacle cyprids in relation to water movement over a surface. J . exp. Bwl. 32, 569-590.

Crisp, D. J. (1961). Territorial behaviour in barnacle settlement. J . exp. Biol. 38,

Crisp, D. J. (ed.) (1964). The effects of the severe winter of 1962-63 on marine life in Britain. J . Anim. Ecol. 33, 165-210.

Crisp, D. J. (1965). Surface chemistry, a factor in the settlement of marine invertebrate larvae. Proc. 5th Mar. Biol. Symp. Botanica Gothoburgemia,

Crisp, D. J. (1967). Chemical factors inducing settlement in Crwaoatrea virginica (Gmelin). J . Anim. Ecol. 36, 329-335.

Crisp, D. J. and Meadows, P. S. (1962). The chemical basis of gregariousness in cirripedes. Proc. R. SOC. B. 156, 500-520.

Crisp, D. J. and Meadows, P. S. (1963). Adsorbed layers: the stimulus to settlement in barnacles. Proc. R. SOC. B. 158, 364-387.

Crisp, D. J. and Ryland, J. S. (1960). Influence of filming and of surface texture on the settlement of marine organisms. Nature, Lond. 185, 119.

Crisp, D. J. and Williams, G. B. (1960). Effect of extracts from fucoids in promoting settlement of epiphytic Polyzoa. Nature, Lo&. 188, 1206-1207.

Crisp, M. (1969). Studies on the behaviour of Nasaariw obeoletw (Say). Biol. Bull. mar. biol. Lab., Wooda Hole, 136, 355-373.

Croker, R. A. (1967). Niche diversity in five sympatric species of intertidal amphipods (Crustacea : Haustoriidae). Ecol. Monogr. 37, 173-200.

Crombie, A. C. (1942). On oviposition, olfactory conditioning and host selection in Rhizopertha dominica Fab. (Insecta, Coleoptera). J . exp. Biol. 18, 62-79.

Crozier, W. J. (1935). Geotropic response in Asterina. J . gen. Phyeiol. 18, 729-37. Crozier, W. J. and Arey, L. B. (1918). On the significance of the reaction to

shading in Chiton. Am. J . Phyaiol. 46, 487-492. Crozier, W. J. and Arey, L. B. (1919). Sensory reactions of Chromodoria zebra.

J . ezp. 2001. 29, 261-310. Crozier, W. J. and Libby, R. L. (1925). Temporary abolition of phototropism in

Limax after feeding. J . gen. Phyaiol. 7 , 421-427. Cubit, J. (1969). Behawour and physical factors causing migration and aggrega-

tion of the sand crab Emerita analoga (Stimpson). Ecology, 50, 118-123. Cummin~, K. W. and Lauff, G. H. (1969). The iduence of substrate particle on

the microdistribution of stream macrobenthos. Hydrobiologia, 34, 145-181. Cushing, D. H. (1951). The vertical migration of planktonic crustacea. Biol.

Rev. 26, 158-192. Dahl, E., Emanuelsson, H. and von Mecklenburg, C. (1970). Pheromone reception

in the males of the amphipod Gammarw duebeni Lilljeborg. Oikoa, 21.42-47. Daniel, A. (1955). Gregarious attraction as a factor influencing the settlement

of barnacle cyprids. J . Madma Univ. B . 25, 97-107. D’Asaro, C. N. (1967). The morphology of larval and post larval Chione cancellata

Limit5 (Eulamellibranchia : Veneridae) reared in the laboratory. Bull. mar.

1. The polynoid genus Arctonot?. Bwl. Bull. mar. biol. Lab., Wooda Hole, 90, 81-93.

429-446.

3, 51-66.

S C ~ . 17, 949-972. Davenport, D. (1950). Studies in the physiology of commensalism.

366 P. 9. MEADOWS AND J. I. U A M P B m

Davenport, D. (1963a). Studies in the physiology of commensalism. 111. The polynoid genera AoholoS, Qattyam and Lepidasthonia. J . mar. bwl . Ass. U.K.

Davenport, D. (1963b). Studies in the physiology of commensalism. IV. The polynoid genera PolynoS, Lepidmthenia, and Harmothoe. J . mar. biol. Ass. U.K. 32, 273-288.

Davenport, D. (1966). Specificity and behaviour in symbioses. &. Rev. Biol. 30,

Davenport, D., Camougis, G. and Hickok, J. F. (1960). Analyses of the behaviour of commensals in host factor. 1. A hesionid polychaete and a pinnotherid crab. Anim. Behuv. 8, 209-218.

Davenport, D. and Hickok, J. F. (1951). Studies in the physiology of commensalism. 2. The polynoid genera Arctonoe and Halosydna. Biol. Bull. mar. biol. Lab., Woods Hole, 100, 71-83.

Davenport, D., Ross, D. M. and Sutton, L. (1961). The remote control of nema- tocyst-discharge in the attachment of Calliactis pmaeitica to shells of hermit crabs. Vie Milieu, 12, 197-209.

Davis, F. M. (1923). Quantitative studies on the fauna of the Dogger Bank. Fishery Invest., Lond. (Ser. 11) 6, no. 2.

Davis, F. M. (1926). Quantitative studies on the fauna of the southern North Sea. Fishery Invest., Lond. (Ser. 11) 8, no. 4.

Dawkina, R. (196%). A threshold model of choice behaviour. Anim. Behav. 17,

Dawkins, R. (196933). The attention threshold model. Anim. Behuv. 17,134-141. Day, J . H. and Wilson, D. P. (1934). On the relation of the substratum to the

metamorphosis of Scolecolepis fuliginosa (ClaparBde). J . mm. biol. Ass. U.K. 19, 665-662.

Dennell, R. (1933). The habits and feeding mechanism of the amphipod Haustorim arenarim Slabber. J . Linn. Soc., 2001. 38, 365-388.

Dethier, V. G. (1964). Evolution of feeding preferences in phytophagous insects. Evolution, 8, 33-64.

Dice, L. R. (1914). The factors determining the vertical movements of Daphnia. J . Anim. Behv. 4, 229-266.

Diebschlag, E. (1938). Ganzheitliches Verhalten und Lernen bei Echinodermen. 2. vergl. Physiol. 25, 612-664.

Dingle, H. and Caldwell, R. L. (1969). The aggressive and territorial behaviour of the mantis shrimp Gonodactylus bredini Manning (Crustacea : Stomatopoda). Behavimr, 33, 115-136.

Dobzhansky, T. and Spaasky, B. (1962). Selection for geotaxis in monomorphic and polymorphic populations of Droeophila pseudoobscura. Proc. natn. Acad. Sci. U.S.A. 48, 1704-1712.

Dobzhansky, T. and Spassky, B. (1967). Effects of selection and migration on geotactic and phototactic behaviour of Drosophila I. Proc. R. SOC. B. 168,

Effects of selection and migration on geotactic and phototactic behaviour of Droeophila 11. Proo.

Dough, M. B. (1946). Some evidences of a dominance-subordinance relationship

Douwes, P. (1968). Host selection and host finding in the egg-laying female

32, 161-173.

29-46.

120-133.

27-47. Dobzhansky, T., Spassky, B. and Sved, J. (1969).

R. SOC. B. 173, 191-207.

among lobsters, Homarm americanus. Anat. Rec. 96, 663.

Cidaria albulccta (Lep. Geometridae). Opuac. ent. 33, 16-279.

HABlTAT SELECTZON BY AQUATIC INVERTEBRATES 367

Edgar, W. D. and Meadows, P. S. (1969). Case construction, movement, spatial distribution and substrate selection in the larva of Chironomw riparius Meigen. J . exp. Biol. 50, 247-263.

Edington, J. M. (1968). Habitat preferences in net-spinning caddis larvae with special reference to the influence of water velocity. J . Anim. Ecol. 37, 676- 692.

Egglishaw, H. J. (1964). The distributional relationship between the bottom fauna and plant detritus in streams. J . Anim. Ecol. 33, 463-476.

Ehrman, L., Spassky, B. and Dobzhansky, T. (1966). Sexual selection, geotaxis and chromosomal polymorphism in experimental populations of Droeophila pseudoobscura. Evolution, 19, 337-346.

Predation by Notoneota undulata (Heteroptera : Notonectidae) on larvae of the yellow fever mosquito. Ann. ent. Soc. Am. 63, 963-973.

Eloff, G. (1936). Behaviour of local Droeophila melamgaeter during late larval stage. Nature, Lond. 138, 402-403.

Elton, G. E. (1927). “Animal Ecology”. Sidgwick and Jackson, London. Enckell, P. H. (1968). Oxygen availability and microdistribution of interstitial

mesofauna in Swedish freshwater sandy beaches. Oilcos, 19, 271-291. Enright, J. T. (1962). Responses of an amphipod to pressure changes. Comp.

Bwchem. Phyaiol. 7, 131-146. Enright, J. T. (1963). The tidal rhythm of activity of a sand beach amphipod.

2. vergl. PhyGl. 46, 276-313. Eriksen, D. H. (1963). The relation of oxygen consumption to substrate particle

size in two burrowing mayflies. J. exp. Biol. 40, 447-463. Evans, F. G. C. (1961). An analysis of the behaviour of Lepidochitona cinerew

in response to certain physical features of the environment. J . Anim. Ecol. 20, 1-10.

Fankhauser, G. and Reik, L. E. (1936). Experiments on the case-building of the caddis-fly larva, Neuron& postica Walker. Physiol. Zool. 8, 337-369.

Fasten, N. (1913). The behaviour of a parasitic copepod, Lemeopoda edwardaii Olsson. J . Anim. Behv. 3, 36-60.

Faur6-Fremiet, E. (1950). Ecologie des cilids psammophiles littoraux. Bull. biol. Fr. Belg. 84, 35-76.

Faust, E. C. and Meleney, H. E. (1924). Studies on Schtktosomiastk japonica. MonographSer. Am. J . Hyg. 3, 1-339.

Fielder, D. R. (1966). A dominance order for shelter in the spiny lobster Jmw lalandei (H. Milne-Edwards). Behaviour, 24, 236-246.

Fincham, A. A. (1970). Rhythmic behaviour of the intertidal amphipod Bathy- poreia pelagica. J . mar. biol. Ass. U.K. 50, 1067-1068.

Fincham, A. A. (1972). Rhythmic swimming and rheotropism in the amphipod Marinogammarua marinua (Leach). J . exp. mar. Biol. Ecol. 8, 19-26.

Fleming, N. C. and Stride, A. H. (1967). Basal sand and gravel patches with separate indications of tidal current and storm-wave paths, near Plymouth. J . mm. biol. Ass. U.K. 47, 433-444.

F0yn, B. and Gjaen, I. (1964). Studies on the serpulid Pomatoceros triqueter L. 1. Observations on the life history. aytt . 24%~. Zool. 2, 73-81.

Fraenkel, G. (1927). Beitriige zur Geotaxis und Phototaxis von Littorim. 2.

Fraenkel, G . S. and Gunn, D. L. (1940). “The Orientation of Animals”. Oxford

Ellis, R. A. and Borden, J. H. (1970).

vergl. Phyawl. 5. 686-697.

University Press.

368 P. 5. MEADOWS AND J. I. UANPBELL

Frings, H. and Frings, C. (1965). Chemosensory bases of food-finding and feeding in Aplysia juliana (Mollusca, Opisthobranchia). Biol. Bull. mar. biol. Lab., Woods Hole, 128, 211-217.

Observations on the bivalves Montacuta substriata and M . ferruginosa, “commensals” with spatangoids. J . mar. biol. Ass. U .K . 46,49-70.

Experiments with the behaviour of the bivalves Montacuta substriata and M . ferruginosa, ‘‘ commensals ” with spatangoids. J . mar.

Gale, W. F. (1971). An experiment to determine substrate preference of the fingernail clam Sphaerium traneversum (Say), Ecology, 52, 367-370,

Gamble, J. C. (1971). The responses of the marine amphipods Corophium arenarium and C. volutator to gradients and to choices of different oxygen concentrations. J . exp. Biol. 54, 275-290.

Ganning, B. (1967). Laboratory experiments in the ecological work on rockpool animals with special notes on the ostracod Heterocypis salinua. Helgolander wias. Meeresunters. 15, 27-40.

Ganning, B. and Wulff, F. (1966). A chamber for offering alternative conditions to small motile aquatic animals. Ophelia, 3, 151-160.

Garbarini, P. (1936). Le choix du support pour les larves de Spirorbia borealia Daudin. C.T. Sdanc. SOC. Biol. 122, 158-160.

Ggbczyriski, M. (1965). Preferendum termiczne Blimltkow slodkowodnychzatoczka rogowego (Planwbia corneua rubra L.) i blotniarki stawowej (Limnea stagnalb L.). Zeaz. nauk. Univ. jagiellonak. 9, 87-96.

Gee, J. M. (1965). Chemical stimulation of settlement in larvae of Spirorbia rupeatris (Serpulidae). Anim. Behav. 181, 1-86.

Gee, J. M. and Knight-Jones, E. W. (1962). The morphology and larval behaviour of a new species of Spirorbia (Serpulidae). J . mar. biol. Ass. U.K.

Gee, W. (1913). The behaviour of leeches with especial reference to its modifiability. A. The general reactions of the leeches Dina microstoma Moore and Clossiphonia stagnalb Linnaeus. B. Modifiability in the behaviour of the leech Dina microstoma Moore.

Behavioural differences between the larval stages of Cirrqormia tentaculata (Montagu) from Drake’s Island (Plymouth Sound) and from Southampton Water. Nature, Lond. 199, 195.

George, J. D. (1967). Cryptic polymorphism in the cirratulid polychaete Cirrqormia tentaculata. J . mar. biol. AM. U.K. 47, 75-79.

Gilpin-Brown, J. B. (1969). Host-adoption in the commensal polychaete Nereia fucata. J . mar. biol. Ass. U.K. 49, 121-127.

Goodbody, I. (1961). Inhibition of the development of a marine sessile community. Nature, Lond. 190, 282-283.

Gore, R. H. (1966). Observations on the escape response in Naasariua vibex Say, (Mollusca : Gmtropoda). Bull mar. Sci. 16, 423-434.

Gorter, F. J. (1929). Experiments on the case-building of a caddis-worm (Linanophilua jlavicornia Fabr.). Tijdschr. ned. dierk. Vereen. 1, 90-93.

Gowanloch, J. N. and Hayes, F. R. (1927). Contributions to the study of marine Gastropods. 1. The physical factors, behaviour and intertidal life of Littorina. Contr. Can. Biol. Pbh. 3, 133-165.

Grave, C. (1926). Molgula citrina (Alder and Hancock). Activities and structure of the free-swimming larva. J . Morph. 42, 453-471.

Grave, C. (1936). Metamorphosis of escidian larvae. Pap. Tortugas Lab. 29,

Gage, J. (1966a).

Gage, J. (1966b).

bid. ASS. U.K. 46, 71-88.

42, 641-654.

Univ. Calif. Publs Zool. 11, 197-305. George, J. D. (1963).

209-292.


Grave, C. (1941). Further studies of metamorphosis of ascidian larvae. Biol. Bull. mar. biol. Lab., Woods Hole, 81, 286287.

Grave, C. (1944). The larva of Styela (Cynthia) partita, structure, activities and duration of life. J . Morph. 75, 173-191.

Grave, C. and Nicoll, P. A. (1940). Studies of larval life and metamorphosis in Ascidia nigra, and species of Polyandrocarpa. Pap. Tortugas Lab. 32, 1-46.

Gray, J. S. (1965). The behaviour of Protodrilua symbioticua (Giard) in temperature gradients. J . Anim. Ecol. 34, 455-461.

Gray, J. S. (1966a). The response of Protodrilua symbioticua (Giard) (hchianne- lida) to light. J . Anim. Ecol. 35, 55-64.

Gray, J. S. (1966b). Factors controlling the localizations of populations of Protodrilua symbioticua Giard. J . Anim. Ecol. 35, 435-442.

Gray, J. S. (1966~). Selection of sands by Protodrilua symbioticus Giard. Verofl. Inat. Meeresforsch. Bremerh. 2, 105-1 16.

Gray, J. S. (1966d). The attractive factor of intertidal sands to Protodrilue symbioticua. J . mar. bwl. Ass. U.K. 46, 627-645.

Gray, J. S. (1967). Substrate selection by the archiannelid Protodrilue hypo- leucua Armenante. J . exp. mar. Bwl . Ecol. 1, 47-54.

Gray, J. S. (1968). An experimental approach to the ecology of the harpacticid Leptaatacua constrictua Lang. J . exp. mar. Biol. Ecol. 2, 278-292.

Gray, J. S. and Johnson, R. M. (1970). Bacteria of a sandy beach as an ecological factor affecting the interstitial gastrotrich Turbanella hyalina Schultze. J . exp. mar. Biol. Ecol. 4, 119-133.

Gross, J. and Knight-Jones, E. W. (1957). The settlement of Spirorbis borealis on dgaa. Proc. Challenger SOC. 3, no. 9.

Gross, W. J. (1955). Aspects of osmotic regulation in crabs showing the terrestrial habit. Am. Nat. 89, 205-222.

Gross, W. J. (1957). A behavioural mechanism for osmotic regulation in a semi- terrestrial crab. Biol. Bull. mar. biol. Lab., Wood Hole, 113, 268-274.

Hamner, W. M., Smyth, M. and Mulford, E. D. (1968). Orientation of the sand- beach isopod Tylo8 punctatw. Anim. Behav. 16, 405-409.

Hanna, H. M. (1961). Selection of materials for case-building by larvae of caddis flies (Trichoptera). Proc. R. ent. SOC. Lond. A. 36, 37-47.

Hansell, M. H. (1968). The home building behaviour of the caddis-fly larva Silo pallipes Fabricius: 11. Desoription and analysis of the selection of small particles. Anim. Behav. 16, 562-577.

Haq, S. M. (1967). Nutritional physiology of Metridia Zucena and M. longa from the Gulf of Maine. Limnol. Oceanogr. 12, 40-51.

Harder, W. (1968). Reactions of p l d t o n i c organisms to water stratification. Limnol. Oceanogr. 13, 156-168.

Harington, C. R. (1921). A note on the physiology of the shipworm Teredo norvegica. Biochem. J . 15, 736-741.

Harris, J. E. (1946). Report on anti-fouling research 1942-44. J . Iron Steel Inat.

Harris, J. E. (1963). The role of endogenous rhythms in vertical migration.

Hartog, C. Den (1959). Distribution and ecology of the slugs Alderia modesta

Harvey, H . W . (1937). Note on selective feeding by Calanus. J . mar. biol. A8s.

Hatto, J . (1968). Observations on the biology of Glossiphonia heteroclita (L.).

2, 297-334.

J . mar. biol. Ass. U.K. 43, 153-166.

and Limapontia depreesa in the Netherlands. Beaufortia, 7, 16-36.

U . K . 22, 97-100.

Hydrobiologia, 31, 363-384.

370 P. 5. NEADOWS AND J. I. CAMPBELL

Hayes, F. R. (1927). The negative geotropism of the periwinkle : a study in littoral ecology. proc. Trans. Nova Scotian Imt. Sci. 16, 155-173.

Hazlett, B. A. (1966). Factors affecting the aggressive behaviour of the hermit crab Calcinue tibicen. 2. tierpsychol. 23, 655-671.

Hazlett, B. A. and Provenzano, A. J. (1966). Development of behaviour in laboratory reared hermit crabs. Bull. mar. Sci. 15, 616-633.

Henrici, A. T. (1933). Studies of freshwater bacteria. 1. A direct microscope technique. J . Bact. 25, 277-286.

Herter, K. (1926). Versuche uber die Phototaxis von Nereis diversicolor 0. F. Miiller. 2. vergl. Physiol. 4, 103-141.

Herter, K. (1928). Reizphysiologie und Wirtsfindung des Fischegels Hemiclepsis margimta 0. F. Miill. 2. vergl. Physwl. 8, 391-444.

Herter, K. (1929). Reizphysiologisches Verhalten und Parasitismus des Enten- egels ProtoclepeiS tesselata 0. F. Miill. 2. vergl. Physiol. 10, 272-308.

Hertz, M. (1933). tfber daa Verhalten des Einsiedlerkrebses Clibanariw misanthropw gegeniiber verschiedenen Gehauseformen. 2. vergl. Physiol.

Hesse, R. (1897). Untersuchungen iiber die Organe der Lichtempfhdung bei niederen Thieren. 11. Die Augen der Plathelminthen, insonderheit der tricladen Turbellarien. 2. wk.9. 2001. 52, 527-582.

Hickok, J. F. and Davenport, D. (1957). Further studies in the behaviour of commensal polychaetes. Biol. Bull. mar.bw1. Lab., Woods Hole, 113,397-406.

Hinde, R. A. (1959). Behaviour and speciation in birds and lower vertebrates. Biol. Rev. 34, 85-128.

Holme, N. A. (1949). The fauna of sand and mud banks near the mouth of the Exe estuary. J . mar. biol. Ass. U.K. 28, 189-238.

Holme, N. A. (1950). The bottom fauna of Great West Bay. J . mar. biol. Ass.

Holmes, S . J. (1901). Phototaxis in the Amphipoda. Am. J . Physwl. 5, 211-234. Holmes, S. J. (1905). The reactions of Ranatra to light. J . comp. Neurol. 15,

Hubschman, J. H. (1970). Substrate discrimination in Pectinatella magnifica Leidy (Bryozoa). J . exp. Biol. 52, 603-607.

Hudson, B. N. A. (1956). The behaviour of the female mosquito in selecting water for oviposition. J . exp. Biol. 33, 478-492.

Hudson, A. and McLintock, J. (1967). A chemical factor that stimulates oviposition by Culex tarsal& Coquillet (Diptera, Culicidae). Anim. Behav. 15,

The role of responses to light in the selection and maintenance of microhabitat by the nymphs of two species of mayfly. Anim. Behav. 14, 17-33.

Hughes, D. A. (1970). Some factors affecting drift and upstream movements of Gamrnarua pulex. Ecology, 51, 301-305.

Hutchinson, G. E. (1967). Introduction to lake biology and limnoplankton. In ‘‘ A Treatise on Limnology ”. Vol. 2. Wiley, London.

Isham, L. B. and Tierney, 3. Q. (1963). Some aapects of the larval development and metamorphosis of Teredo (Lyrodue) pedicellata de Quatrefages. Bull. mar. Sci. Gulf Caribb. 2, 574589.

Ishii, S. (1952). Studies on the host preference of the cowpea weevil (Callosobruchus chinemis L.). Bull. mtn. Inst. agric. Sci., Tokyo, 1, 185-256.

Jansson, B.-0. (1962). Salinity resistance and salinity preference of two oligochaetes Aktedrilus monospermatecue Knoller and Marionina pre-

18, 597-621.

U.K. 29, 163-183.

305-349.

336-341. Hughes, D. A. (1966).

HABITAT SELEOTION BY AQUATIO INVERTEBRATES 371

Clitellochaeta n.sp. from the interstitial fauna of marine sandy beaches.

Jansson, B.-0. (1967). The si@cance of grain size and pore water content for the interstitial fauna of sandy beaches. Oikos, 18, 311-322.

Jansson, B.-0. (1968). Quantitative and experimental studies of the interstitial fauna in four Swedish sandy beaches. Ophelia, 5 , 1-71.

Jansson, B.-0. and Kallander, C. (1968). On the diurnal activity of some littoral peracarid crustaceans in the Baltic Sea. J . exp. mar. Biol. Eool. 2, 24-36.

Janzer, W. and Ludwig, W. (1962). Versuche zur Evolutorischen Entstehung der Htihlentiermerhle. 2. indukt. Abatamm. -u. Vererb Lehre, 84, 462-479.

Jennings, H. S. (1907). Behavior of the star&h, Asterias forreri de Loriol. Univ. Calq. Publa 2001. 4, 63-186.

Jermy, T., Hanson, F. E. and Dethier, V. G. (1968). Induction of specific food preference in lepidopterous larvae. Entomologia exp. appl. 11, 211-230.

Johnson, I. S. (1962). The demonstration of a “ host-factor ” in commensal crabs. Tram. K a m . Acad. Sci. 55, 468-464.

Johnson, R. G. (1965). Temperature variation in the infaunal environment of a sand h t . Limnol. Oceanogr. 10, 114-120.

Johnson, W. H. and Raymont, J. E. G. (1939). The reactions of the planktonic copepod Centropccgea typicua, to light and gravity. Biol. Bull. mar. biol. Lab., Woods Hole, 77, 200-216.

Jones, D. A. (1970). Factors affecting the distribution of the intertidal isopods Eurydice pulchra Leach and 1. af$nia H m e n in Britain. J. Anim. Ecol.

Jones, D. A. and Naylor, E. (1970). The swimming rhythm of the sand beach isopod Eurydice pukhra. J . exp. mar. Biol. Ecol. 4, 188-199.

Kampf, W.-D., Becker, G. and Kohlmeyer, J. (1969). Versuche uber das AufEnden und den Befall van Holz durch L m e n der Bohrmuschel Teredo pedicellccta Qutrf. 2. angew 2001. 46, 257-283.

Kanda, S. (1916a). Studies on the geotropism of the masine snail Lithmka littorea. Biol. Bull. mar. biol. Lab., Wood8 Hole, 30, 67-84.

Kanda, 8. (1916b). The geotropism of freshwater snails. Biol. Bull. mar. biol. Lab. wood8 Hole, 30, 86-97.

Kearn, G. C. (1967). Experiments on host-finding and host-specificity in the monogenean skin paraite Entobdella; 8 0 k m . Parasitology, 57, 685-606.

Kiseleva, G. A. (19681%). Some aspects of the ecology of the l w a e of Black Sea Mussels. I n “The Distribution of Benthio Fauna and the Biology of Benthic Animal Life in Southern Waters ‘I. Symposium published by the Ukranian Acad. of Sciences, Kiev, 16-20.

Kiseleva, G. A. (1966b). Factors stimulating larval metamorphosis of the lamellibranch, Braohyodontee lineatwr (Gmelin). 2001. Zh. 45,1671-1673.

Kiseleva, G. A. (1967a). Influence of substratum on settlement and metamorphosis of larvae of benthic fauna. I n “ Benthic Biocenosis and the Biology of Benthonic Organisms from the Black Sea ”. Published by Ukranian Acad. of Sciences, Kiev, 1, 71-84.

Settlement of Polydora Oiliata (Johnston) larvae on different substrates. I n “ Benthio Biocenosis and the Biology of Benthonio Organisms from the Black Sea ”. Published by Ukranian Acad. of Sciences, Kiev, 1, 86-90.

Kitching, J. A. (1937). Studies in sublittoral ecology. 11. Recolonization at the upper margin of the sublittoral region; with a note on the denudation of Laminaria forest by storms. J. Anim. Ecol. 25, 482-495.

Oikos, 13, 293-305.

39, 455-472.

Kiseleva, G. A. (196713).

372 P. 9. MEADOWS AND J. I. OAMFBELL

Kitching, R. (1971). A simple simulation model of dispersal of animals among units of discrete habitats. Oecologia, 7, 95-116.

Knight-Jones, E. W. (1949). Aspects of the setting behaviour of larvae of Ostrea edulis on Essex oyster beds. Rapp. PA. Reun. Cow. perm. int. Explor. Mer, 128, 30-34.

Knight-Jones, E. W. (1951). Gregariousness and some other aspects of the setting behaviour of Spirorbis. J . mar. biol. Ass. U.K. 30, 201-222.

Knight-Jones, E. W. (19534. Decreased discrimination during setting after prolonged planktonic life in larvae of Spirorbis borealis (Serpulidae). J . mar. biol. Ass. U.K. 32, 337-345.

Knight-Jones, E. W. (1953b). Laboratory experiments on gregariousness during setting in Balanus balanoidea and other barnacles. J . exp. Biol. 30, 684-698.

Knight-Jones, E. W. and Morgan, E. (1966). Responses of marine animals to changes in hydrostatic pressure. Oceanogr. Mar. Bwl. Ann. Rev. 4, 267-299.

Knight-Jones, E. W. and Moyse, J. (1961). Intraspecific competition in sedentary marine animals. Symp. Boo. exp. Biol. 15, 72-95.

Knight-Jones, E. W. and Stevenson, J. P. (1950). Gregariousness during settlement in the barnacle Elminius modestua Darwin. J . mar. biol. Ass. U .K .

Kohn, A. J. (1961). Chemoreception in gastropod molluscs. Am. Zool.1,291-308. Kohn, A. J. and Waters, V. (1966). Escape responses of three herbivorous

gastropods to the predatory gastropod Conus textile. Anim. Behuv. 14,340-45. Korringa, P. (1957). Lunar periodicity : chapter 27.In"Treatise on Marine Ecology

and Paleoecology", Vol. 1, Ecology. (J. W. Hedgpeth, ed.) Mem. Ueol. SOC. America, 27, 917-934.

Krumbein, W. E. (1971). Sediment microbiology and grain-size distribution, as related to tidal movement during the first mission of the West German Underwater Laboratory " Helgoland ". Mar. Biol. 10, 101-112.

Lack, D. (1949). The significance of ecological isolation. In "Genetics, Paleont- ology and Evolution". (Jepson, Mayr and Simpson, ed.) Princeton University Press, Princeton, New Jersey.

Lagerspetz, K. (1963). Humidity reactions of three aquatic amphipods, Gammarus duebeni, G . oceanicus and PontoporeicG a@nk in the air. J . exp. Biol. 40, 106-110.

Lagerspetz, K. and Lehtonen, A. (1961). Humidity reactions of some aquatic isopoda in the air. Biol. Bull. mar. biol. Lab., Woo& Hole, 120, 38-43.

Lagerspetz, K. and Mattila, M. (1961). Salinity reactions of some fresh- and brackish-water crustaceans. Biol. Bull. mar. biol. Lab., Wood8 Hole, 120, 44-53.

Structure and function of the buccal apparatus of Clione limacina (Phipps) with a review of feeding in gymnosomatous pteropods. J . exp. mar. Bwl. Ecol. 4, 101-118.

Lance, J. (1962). Effects of water of reduced salinity on the vertical migration of zooplankton. J . mar. biol. Ass. U.K. 42, 131-164.

Landenberger, D. E. (1966). Learning in the Pacific s tamh, PiSmter giganteus. Anim. Behav. 14, 414-418.

Landenberger, D. E. (1967). A study of predation and predatory behaviour in the Pacific starfish Pismter. Ph.D. Thesis Univ. Calif., Santa Barbara.

Landenberger, D. E. (1968). Studies on selective feeding in the Pacific stafish Piswter in Southern California. Ecology, 49, 1062-1075.

LaRow, E. J. (1969). A persistent diurnal rhythm in Chaobom larvae. 11. Ecological Sigtllficance. Limnol. Ocmnogr. 14, 213-218.

29, 281-297.

Lalli, C. M. (1970).


LaRow, E. J. (1970). The effect of oxygen tension on the vertical migration of Cluzobom larvae. Limnol. Oceanogr. 15, 357-362.

Lehmann, U. (1972). Tagesperiodisches Verhalten und Habitatwechsel der Larven von Potamophylax luctuoew, (Trichoptera). Oecologia, 9, 265-278.

Leighton, D. L. (1966). Studies of food preference in algivorous invertebrates of Southern California kelp beds. Pacif. Sci. 22, 104-113.

Lewis, A. G. (1959). The vertical distribution of some inshore copepods in relation to experimentally produced conditions of light and temperature. Bull. mar. Sci. Gulf. Caribb. 9, 69-78.

Lewis, D. B. (1968). Some aspects of the ecology of Fabricia sabella (Ehr) (Annelida, Polychaeta). J . Linn. SOC. 47, 515-626.

Lindberg, R. G. (1955). Growth, population dynamics and field behaviour in the spiny lobster Panulirus interruptus (Randall). Univ. Calq. Publa 2001. 59,

Lindroth, C. H. (1953). Some attempts toward experimental zoogeography.

Lloyd, B. (1931). Muds of the Clyde Sea Area. 11. Bacterial content. J . mar.

Loeb, J. (1893). f h e r Kiinstliche Umwandlung positiv heliotropischer Thiere in negativ heliotropische und umgekehrt. Pjliigers Arch. ges. Physwl. 54,

Loeb, J. (1894). BeitrBge zur Gehirnphysiologie der Wiirmer. PjZiigers Arch. sea.

Loeb, J. (1904). The control of heliotropic reactions in freshwater crustaceans by chemicals.

Loeb, J. (1906a). Columbia University Press, New York.

Loeb, J. (1906b). Uber die Erregung von positivem Heliotropismus durch Saiire, insbesondere Kohlensaiire, und von negativem Heliotropismus durch ultraviolette Strahlen. Pjliigers Arch. ges. Physiol. 115, 564-581.

Lucas, C. E. (1936). On certain inter-relations between phytoplankton and zooplankton under experimental conditions. J . Cona. perm. int. Explor. Mer, 11,

Lyman, F. E. (1943). Swimming and burrowing activities of mayfly nymphs of the genus Hexagenh. Ann. ent. SOC. Am. 36, 250-256.

Lyman, F. E. (1945). Reactions of certain nymphs of Stenonema (Ephemer- optera) to light as related to habitat preference. Ann. ent. Soo. Am. 38,

Lyon, E. P. (1906). Note on the geotropism of Arbach larvae. Biol. Bull. mar.

Lyster, I. H. J. (1965). The salinity tolerance of polychaete larvae. J . Anim.

Macan, T. T. (1963). “Freshwater Ecology”. Longmans, London. McCoy, E. and Henrici, A. T. (1937). The distribution of heterotrophic bacteria

in bottom deposits of lakes. J . Bact. 33, 84-85. McEwen, R. S. (1918). The reactions t o light and to gravity in Drosophila and its

mutants. J . exp. 2001. 25, 49-105. McGinnis, M. 0. (1911). Reactions of Branchipus serratus to light, heat and

gravity. J . exp. 2001. 10, 227-240. Mackie, A. M. (1970). Avoidance reactions of marine invertebrates to either

steroid glycosides of starfish or synthetic surface-active agents. J. exp. mar. Biol. Ecol. 5, 63-69.

157-248.

Ecology, 34, 657-666.

bid. ASS. U .K . 17, 751-766.

81-107.

Ph?/siol. 56, 247-269.

Univ. Calq. Publa Physiol. 2 , 1-3. “ The Dynamics of Living Matter ”.

343-362.

234-236.

biol. Lab., Woods Hole, 12, 21-22.

E d . 34, 517-527.


McLachlan, A. J. (1969). Substrate preferences and invasion behaviour exhibited by larvae of Nilodorum bre&bueca Freeman (Chironomidae) under experimental conditions. Hydrobiologkz, 33, 237-249.

McLusky, D. 5. (1967). Some effects of salinity on the survival, moulting and growth of Corophium volututor (Amphipoda). J . mar. biol. Aaa. U.K. 47,

McLusky, D. 8. (1968). Some effects of salinity on the distribution and abundance of Corophium volutator in the Ythan estuary. J . mar. biol. Ass. U.K. 48, 443-454.

McLusky, D. S. (1969). The oxygen consumption of Corophium volutator in relation to salinity. Comp. Biochem. Physiol. 29, 743-753.

McLueky, D. S. (1970). Salinity preference in Corophium volututor. J . ma^. biol. Aaa. U.K. 50, 747-752.

Madsen, B. L. (1968). A comparative ecological investigation of two related mayfly nymphs. Hydrobiologh, 31, 337-349.

Madsen, B. L. (1969). Reactions of Brachypteru hi (Morton) (Plecoptera) nymphs to water current. Oikoa, 20, 95-100.

Marzolf, G. R. (1966). The trophic position of bacteria and their relation to the distribution of invertebrates. I n “Organism-substrate relationships in streams.’’ (Cummins, K. W., Tryon, C. A. and Hartman, R. T., eds.) pp. 131-136. Special Publication no. 4, Pymatuning Laboratory of Ecology, Univ. Pittsburg.

Mast, S. 0. (1911). Light and the Behaviour of Organism. Wiley, London. Mast, S. 0. (1919).

607-618.

Reversion in the sense of orientation to light in the colonial forms, Volvox globator and Pandorina morum. J . exp. 2001. 27,

Matthews, D. C. (1965). Feeding habits of the sand crab Hippa pacifica (Dana). P m q . Sci. 9, 382-386.

Maxwell, S. S. (1897). Beitriige zur Gehirnphysiologie der Anneliden. Pjliigera Arch. gee. Phyaiol. 61, 263-297.

Meadows, P. S. (19648). Experiments on substrate selection by Corophium species: GLms and bacteria on sand particles. J . exp. Bwl. 41, 499-611.

Meadows, P. S. (1964b). Experiments on substrate selection by Corophium volutator (Pallas) : depth selection and population density. J . exp. Biol. 41,

Meadows, P. 5. (1964~). Substrate selection by Corophiwm species: the particle size of substrates. J . Anim. EGO^. 33, 387-394.

Meadows, P. S. (1967). Discrimination, previous experience and substrate selection by the amphipod corophium. J . exp. Bwl. 47, 553-559.

Meadows, P. 5. (1969). Settlement, growth and competition in sublittoral populations of barnacles. Hydrobiologb 33, 66-92.

Meadows, P. S. and Anderson, J. G. (1966). Micro-organism attached to marine and freshwater sand grains. Nature, Lond. 212, 1069-1060.

Meadows, P. S. and Anderson, J. G. (1968). Micro-organisms attached to marine Band grains. J . mar. biol. As8. U.K. 48, 161-176.

Meadows, P. 8. and Campell, J. I. (1972). Habitat selection and animal distribution in the sea: the evolution of a concept. 2nd Int. Congr. Hist. Oceanogr. Proc. R. Soo. Edinb. B in press.

The behaviour of Uorophium volututor

367-390.

677-687.

Meadows, P. 8. and Reid, A. (1966). (Cmtacea: Amphipoda). J. 2001. LO&. 150, 387-399.


Meadows, P. S. and Williams, G. B. (1963). Settlement of Spirorbb borealis (Daudin) larvae on surfaces bearing films of micro-organisms, Nature, Lond.

Miller, M. A,, Rapean, J. C . and Whedon, W. F. (1 948). The role of slime film in the attachment of fouling organisms. Bwl. Bull. mar. biol. Lab., Woods HoZe,

Mitsukuri, K. (1901). Negative phototaxis and other properties of Littorina in determining its habitat. Annotnes zool. jap. 4, 1-19.

Mittler, T. E. and Dadd, R. H. (1965). Differences in the probing responses of Myzus persicae (Sulzer) elicited by different feeding solutions behind a para- film membrane. Entomologia exp. appl. 8, 107-122.

198, 610-611.

94, 143-157.

Moore, H. B. (1958). Marine Ecology, Chapman Hall, London. Morgan, E. (1965). The activity rhythm of the amphipod Corophium wolututor

(Pallas) and its possible relationship to changes in hydrostatic pressure associated with the tides. J . Anim. Ecol. 34, 731-746.

Morgan, E. (1970). The effect of environmental factors on the distribution of the amphipod Pectenogammarus planicrurus with particular reference to grain size. J . mar. biol. Ass. U.K. 50, 769-785.

Morgan, E., Nelson-Smith, A. and Knight-Jones, E. W. (1964). Responses of Nymphon gracile (Pycnogonida) to pressure cycles of tidal frequency. J . exp. Biol. 41, 825-836.

Characteristic tidal rhythmic migration of a mussel, Donax 8emignosus Dunker, and the experimental analysis of its behaviour at the flood tide. 2001. Mag., Tokyo, 50, 1-12.

Morimoto, S. (1939). The host selection of Callosobruchus chinen.& L. Rev. appl. Ent. 27A, 361.

Mortensen, T. (1921). Studies of the Development and Larval Forms of Echinoderms. G.E.C. Gad : Copenhagen.

Mortimer, C . H. (1942). The exchange of dissolved substances between mud and water in lakes. J . Ecol. 30, 147-201.

Morton, J. E. (1962). Habit and orientation in the small commensal bivalve mollusc Montacuta ferruginosa. Anim. Behaw. 10, 126-133.

Moynihan. M. (1968). The “ Coerebini ” : a group of marginal areas, habitats, and habits. Am. Nat. 102, 573-681.

Mullin, M. M. (1963). Some factors affecting the feeding of marine copepods of the genus Cabnus. Limnol. Oceanogr. 8, 239-250.

Mullin, M. M. and Brooks, E. R. (1967). Laboratory culture, growth rate, and feeding behavior of a planktonic marine copepod. Limnol. Oceanogr. 12,

Naylor, A. F. (1959). An experimental analysis of dispersal in the flour beetle Tribolium confumm. Ecology, 40, 453-465.

Naylor, E. (1958). Tidal and diurnal rhythms of locomotory activity in Carcinus maenaa (L.). J . exp. Biol. 35, 602-610.

Naylor, E. (1962). Seasonal changes in a population of Carcinus maenaa (L.) in the littoral zone. J . Anim. Ecol. 31, 601-609.

Nelson, T. C. (1924). The attachment of oyster larvae. Biol Bull. mar. biol. Lab., Wood8 Hole, 46, 143-151.

Newell, G. E. (1958). An experimental analysis of the behaviour of Littorina littorea (L.) under natural conditions and in the laboratory. J . mar. biol.

Nicol, J. A. C. (1967). “The Biology of Marine Animals”. (2nd Ed.) Pitman,

Mori, S. (1938).

657-666.

ASS. U.K. 37, 241-266.

London.


Nishihira, M. (1967a). Observations on the selection of algal substrata by hydrozoan larvae, Sertularella miureneis in nature. Bull. biol. Stn Asamushi, 13, 35-48.

Nishihira, M. (1967b). Dispersal of the larvae of a hydroid, Sertularella miureneis. Bull. biol. Stn Asamushi, 13, 49-56.

Nishihira, M. (1968a). Experiments on the algal selection by the larvae of Coryne uchidai Stechow (Hydrozoa). Bull. biol. Stn Asamushi, 13, 83-89.

Nishihira, M. (196813). Brief experiments on the effect of algal extracts in promoting the settlement of the larvae of Coryne uchidai Stechow (Hydrozoa). Bull. biol. Stn Asamushi, 13, 91-101.

Nonaka, M. (1966). Experiments on the habitat selection of the Japanese spiny lobster. Bull. Jap. SOC. Scient. Fish. 38, 630-638.

Nyholm, K. (1950). Contributions to the life history of the Ampharelid, Melinna cristata. 2001. Bidr. Uppa. 29, 79-91.

Ogden, J. C. (1970). Artificial selection for dispersal in flour beetles (Tenebrioni- dae: Tribolium). Ecology, 51, 130-133.

Orians, G. H. and King, C. E. (1964). Shell selection and invasion rates of some Pacific hermit crabs. Pacif. Sci. 18, 297-306.

Ottaway, J. R. and Thomas, I. M. (1971). Movement and zonation of the intertidal anemone Actinia tenebrosa Farqu. (Cnidaria: Anthozoa) under experimental conditions. Aust. J . mar. Freahwat. Rea. 22, 63-78.

Oviatt, C. A. (1969). Light influenced movement of the starfish Aeterhforbeei (Desor). Behaviour, 33, 52-57.

Paling, J. E. (1969). The manner of infection of trout gills by the monogenean parasite Discocotyle sagittata. J . 2001. Lond. 159, 293-309.

Papi, F. and Pardi, L. (1963). On the lunar orientation of sand hoppers (Amphi- poda: Talitridae). Biol. Bull. mar. biol. Lab., Woods Hole, 124, 97-105.

Parker, G. H. and Burnett, F. L. (1900). The reactions of planarians, with and without eyes, to light. Am. J . Physiol. 4, 373-385.

Paulson, T. C. and Scheltema, R. S. (1968). Selective feeding on algal cells by the veliger larvae of Naasariw obaoletw (Gastropoda, Prosobranchia). Biol. Bull. mar. biol. Lab., Woods Hole, 134, 481-489.

Pause, J. (1919). Beitriige zur Biologie und Physiologie der Larve von Chironomw gregariw. 2001. Jb. 36, 339-452.

Pearl, R. (1903). The movements and reactions of freshwater planarians : a study in animal behaviour. Q . Jl microac. Sci. 46, 509-714.

Pearse, A. S., Humm, H. J. and Wharton, G. W. (1942). Ecology of sand beaches a t Beaufort N.C. Ecol. Monogr. 12, 135-190.

Pennak, R. W. (1961). Comparative ecology of the interstitial fauna of freshwater and marine beaches. Annde biol. 27, 449480.

Perttunen, V. (1961). RBactions de W i a italica F. zd la lumibre et zd l’humiditd de l’air. Vie Milieu, 12, 219-259.

Phillips, P. J. (1971). Observations on the biology of mudshrimps of the genus Callianassa (Anomura: Thalassinidea) in Mississippi Sound. Gulf Bee. Rep. 3, 165-196.

PiBron, H. (1919). De l’importance respective des divers facteurs sensoriels dans le sen8 du retour de la Patelle. 0. r. Shnc. SOC. Biol. 82, 1227-1230.

Popham, E. J. (1941). The variation in the colour of certain species of Arctocorisa (Hemiptera, Corixidae) and its significance. Proc. 2001. SOC. Lond. 111,

Powell, G. C. and Nickerson, R. B. (1965). Aggregations among juvenile king crabs (Paralithodea camtschatica Tilesius) Kodiak, Alaska. Anim. Behaw. 13, 374-380.

135-172.


Powers, E. B. (1914). The reactions of crayfishes to gradients of dissolved carbon dioxide and acetic and hydrochloric acids. Biol. Bull. mar. biol. Lab., Woods Hole, 27, 177-200.

Pravdib, V. (1970). Surface charge characterization of sea sediments. Limnol. Oceanogr. 15, 230-233.

Prytherch, H. F. (1934). The role of copper in the setting, metamorphosis, and distribution of the American oyster Ostrea virginica. Ecol. Monogr. 4,

Pyefinch, K. A. (1943). The intertidal ecology of Bardsey Island, North Wales, with special reference to the recolonization of rock surfaces, and the rock pool environment. J . Anim. Ecol. 12, 82-108.

Pyefinch, K. A. and Downing, F. S. (1949). Notes on the general biology of Tubularia larym Ellis & Solander. J . mar. biol. Ass. U.K. 28, 21-43.

Radwin, G. E. and Wells, H. W. (1968). Comparative radular morphology and feeding habits of muricid gastropods from the Gulf of Mexico. Bull mar.

Reese, E. S . (1962). Shell selection behaviour of hermit crabs. Anim. Behav.

Reese, E. S . (1964). Ethology and Marine Zoology. Oceanogr. Mar. Biol. Ann. Rev. 2, 455-488.

Reid, D. M. (1929). On some factors limiting the habitat of Arenicola marina. J . mar. biol. Ass. U.K. 16, 109-116.

Renwick, J. A. A. and Vit6, J. P. (1969). Bark beetle attractants: mechanisms of colonization by Dendroctonwr frontalie. Nature, Lo&. 224, 1222-1223.

Reynierse, J. H. (1967). Aggregation formation in Planaria : Phagocata gracilk and Cura foremani : species differentiation. Anirn. Behav. 15, 270-272.

Reynierae, J. H., Gleason, K. K. and Ottemann, R. (1969). Mechanisms producing aggregations in Planaria. Anim. Behav. 17, 47-63.

Rice, A. L. (1964). Observations on the effects of changes of hydrostatic pressure on the behaviour of some marine animals. J . mar. biol. Ass. U.K. 44,

Riley, C. F. C. (1912). Observations on the ecology of dragonfly nymphs: reactions to light and contact. Ann. ent. SOC. Am. 5, 273-292.

Rodriguez, G. and Naylor, E. (1972). Behaviour rhythms in littoral prawns. J . mar. biol. Ass. U.K. 52, 81-95.

Ronald, K. (1960). The effects of physical stimuli on the larval stage of Terranova decipiens (Krabbe, 1878), (Nematoda : Anisakidae). I. Tempera- ture. Can. J . Res. 38, 623-642.

Rose, M. (1925). Contribution a l’etude de la biologie du plankton ; le probleme de migration verticales journalieres. Archs 2001. exp. gen. 64, 387-542.

Ross, D. M. (1965). Preferential settling of the sea anemone Stomphia coccinea on the mussel Modiolw modiolw. Science, N . Y . 148, 527-528.

Ross, D. M. and Sutton, L. (1961a). The response of the sea anemone CaZliactk paraaitica to shells of the hermit crab Pagurms bernhardwr. Proc. R. SOC.,

Ross, D. M. and Sutton, L. (1961b). The association between the hermit crab Dardanw arrosor (Herbst) and the sea anemone Calliactia paraeitica (Couch). Proc. R . SOC., B, 155, 282-291.

Ross, D. M. and Sutton, L. (1963). A sea anemone, a hermit crab and a shell- an ecological triangle. PTOC. 16th Int. Congr. 2001. 1, 62.

Ross, D. M. and Sutton, L. (1967). The response to molluscan shells of the swimming sea anemones Stomphia coccinea and Actinostola new species. Can. J . 2001. 45, 895-906.

47-107.

S C ~ . 18, 72-85.

10, 347-360.

163-175.

B, 155, 266-281.

378 P. 9. MEADOWS AND J. I. OAIKPBELI,

Russell, F. S. (1927). The vertical distribution of plankton in the sea. Bbl Rev. 2, 213-262.

Russell, F. S. (1936). Submarine illumination in relation to animal life. Rapp. PA. R4un. Comrn. int. Explor. Mer, 101, 3-8.

Russell-Hunter, W. (1949). The structure and behaviour of Hiatella gallimm (Lamarck) and H.arctioa (L.), with special reference to the boring habit. Proc. R. SOC. Edinb. B 63, 271-289.

Ryan, E. P. (1966). Pheromone: evidence in a decapod crustacean. Science, N . Y . 151, 340-341.

Ryland, J. S. (1969). Experiments on the selection of algal substrates by Polyzoan larvae. J. mp. Biol. 36, 613-631.

Sakai, S. (1962). Ecological studies on the Abalone, Haliotta dtacw h a n d Ino-1. Experimental studies on the food habit. Bull. Jap. SOC. Scient. Fbh. 28, 766-779.

Salazar, M. H. (1970). Phototaxis in the deep-sea urchin Albcentrotus fragilk (Jackson). J . exp. mar. Biol. Ecol. 5, 254-264.

Salt, G. (1938). Experimental studies in insect parasitism. VI. Host suitability. Bull. ent. Res. 29, 223-246.

Simeoto, D. D. (1969). Physiological tolerances and behaviour response of five species of Haustoriidae (Amphipoda : C'rustacea) to five environmental factors. J . Piah. Res. Bd Can. 26, 2283-2298.

Schafer, R. D. and Lane, C. E. (1967). Some preliminary observations bearing on the nutrition of LimnoriQ. BulE. mar. Sci. Gulf. Cad&. 7, 289-296.

Scheer, B. T. (1946). The development of marine fouling communities. BwZ. Bull. mar. biol. Lab., Woods Hole, 89, 103-121.

Scheltema, R. S. (1966). The effect of substrate on the length of planktonic existence in Naaea~us obeoletus. Biol. Bull. mar. biol. Lab., Woods Hole, 111, 312.

Metamorphosis of the veliger larvae of Naa8wius obsoletuis (Gaatropoda) in response to bottom sediment. Bwl. Bull. mar. bwl. Lab., Wood8 Hole, 120, 92-109.

Schbne, H. (1961). Learning in the spiny lobster P a n d i m argue. Bwl. Bull. mar. bwl . Lab., Woods Hole, 121, 364-366.

Eentz-Braconnot, E. (1965). Sur la capture des proies par le ptbropode gymnosome Pneumoderrnopaia pauoidene (Boas). Cah. Bwl. mar. 6, 191-194.

Sheader, M. and Chia, F.8. (1970). Development, fecundity and brooding behaviour of the amphipod Marinogarnmarua obtueatus. J. mar. bid. A88.

Shelton, R. G. J. and Mackie, A. M. (1971). Studies on the chemical preferences of the shore crab Carcinua rnaenm (L.). J . exp. mar. Bwl. Ecol. 7 , 41-49.

Sheppard, P. M. (1962). A note on non-random mating in the moth Panaxk dominulcc (L.). Heredity, 6, 239-241.

Siebeck, V. 0. (1968). Uferflucht und optische Orientierung pelagischer Crusta- ceen. Arch Hydrobwl. Suppl. 35, 1-118.

Silbn, L. (1964). Developmental biology of Phoronidea of the Gullmar Fiord area (west coast of Sweden). A c e 2001. 35, 216-268.

Silva, P. H. D. H. de (1962). Experiments on choice of substrate by Spirorbh larvae. J . exp. Bwl. 39, 483-490.

Simon, J. L. (1968a). Incidence and behaviour of Hhtriobdella homari (Annelids, Polychaeta), a commensal of the American Lobster. Bioscience, 18, 36-36.

Simon, J. L. (1968b). Occurrence of pelagic larvae in Spw setosa Verrill, 1873 (Polychaeta: Spionidae). Bwl. Bull. mar. bwl. Lab., Woods Bole, 134, 603-616.

Scheltema, R. S. (1961).

U.K. 50, 1079-1099.


Simpson, J. H. and Woods, J. D. (1970). Temperature microstructure in a

Siniff, D. B. and Jessen, C. R. (1969). A simulation model of animal movement

Skellam, J. G. (1951). Random dispersal in theoreticd populations. Biometrika,

Sladden, D. E. and Hewer, H. R. (1938). Transference of induced food-habit from parent to offspring. 111. Carausius dizippm-the stick insect. Proc. R. SOC. B 126, 30-45.

Smidt, E. L. B. (1951). Animal production in the Danish Waddensea. Meddr Danm. Fkk.-og Hawnders. 11, 1-146.

Smith, F. G. W. (1946). Effect of water currents upon the attachment and growth of barnacles. Bio2. Bull. mar. biol. Lab., Woods Hole, 90, 51-70.

Smith, G. (1905). The effect of pigment migration on the phototropism of Gammamur annulatw S. I. Smith. Am. J. Physiol. 13, 205-216.

Snyder, N. F. R. and Snyder, H. A. (1971). Pheromone-mediated behaviour of Faaciolaria tulipa. Anim. Behav. 19, 257-268.

Spooner, G. M. (1933). Observations on the reactions of marine plankton to light. J. mar. biol. Ass. U.K. 19, 385-438.

Staropolska, S. and Dembowski, J. (1950). An attempt of analysing the variability in the behaviour of the caddis-fly larva Molanna angustata. Acta Bwl. ezp., Vars. 15, 37-55.

Stehouwer, H. (1954). The preference of the slug Aeolidia papillosa (L.) for the sea anemone Metridium senile (L.). Arch8 n$ed 2001. 10, 161-170.

StevEiO, 2. (1971). Laboratory observations on the aggregations of the spiny spider crab (Maja s q u i d 0 Herbst). Anim. Behav. 19, 18-25.

Stimson, J. (1970). Territorial behaviour of the owl limpet Lottia gigantea.

Straughan, D. (1972). Ecological studies of Mercierella enigmatica Fauvel (Annelida: Polychaeta) in the Brisbane river. J. Anim. Ecol. 41, 93-136.

Sund, P. N. (1958). A study of the muscular anatomy and swimming behaviour of the sea anemone Stomphia coccinea. &. J1 microsc. Sci. 99, 401-420.

Swedmark, B. (1964). The interstitial fauna of marine sand. Biol. Rev. 39, 1-42. Teal, J. M. (1958). Distribution of fiddler crabs in Georgia salt marshes. Ecology,

39, 186-193. Thorpe, W. H. (1938). Further experiments on olfactory conditioning in a para-

sitic insect. The nature of the conditioning process. Proc. R. SOC. B 126, 370-397.

Thorpe, W. H. (1939). Further studies on pre-imaginal olfactory conditioning in insects. Proc. R. SOC. B. 127, 424-433.

Thorpe, W. H. (1956). “Learning and Instinct in Animals”. Methuen, London. Thorpe, W. H. and Jones, F. G. W. (1937). Olfactory conditioning in a parasitic

insect and its relation to the problem of host selection. Proc. R. SOC. B. 124, 56-81.

Thorson, G. (1964). Light aa an ecological factor in the dispersal and settlement of larvae of marine bottom invertebrates. Ophelia, 1, 167-208.

Towle, E. W. (1900). A study in the heliotropism of Cypriclopsk. Am. J. Phyaiol. 3, 345-365.

Ullyott, P. (1936a). The behaviour of Dendrocoelum lacteum. I. Responses at light-and-dark boundaries. J . ezp. Biol. 13, 253-264.

Ullyott, P. (1936b). The behaviour of Dendrocoelum laoteum. 11. Responses in non-directional gradients. J. exp. Bwl. 13, 265-278.

freshwater thermodine. Nature, Lond. 226, 832-835.

p8tt~lllE. Adv. Eco~. Rm. 6, 185-219.

38, 196-218.

ECOJOgy, 51, 113-118.


Vader, W. J. M. (1964). A preliminary investigation into the reactions of the fauna of the tidal flats t o tidal fluctuations in water level. Neth. J . Sea Rea.

Van Dongen, A. (1956). The preference of Littorina obtuaata for Fucaceae.

Van Haaften, J. L. and Verwey, J. (1959). The role of water currents in the

Verwey, J. (1949). Habitat selection in marine animals. Folia Biotheor. 4, 1-22. Visscher, J. P. (1928). Nature and extent of fouling of ships’ bottoms. Bull.

Bur. F’ish., Wash. Doc. no. 1031, 193-252. Volker, L. (1968). The shell of the land hermit crab Coenobita ecaevola ForskAl

from the Red Sea. J . exp. mar. Bwl. Ecol. 1, 168-190. Volpe, P., Carfagna, M. and Di Lorenzo, M. (1967). Extra-retinal pigmentation

and colour discrimination. 1. Choice of colour of substrate during oviposition in Drosophila melanogaater. J . exp. Biol. 47, 297-305.

Waddington, C. H., Woolf, €3. and Perry, M. M. (1954). Environment selection by Drosophila mutants. Evolution, 8, 89-96.

Wallace, H. R. (1958). Movement of eelwonns. 1. The influence of pore size and moisture content of the soil on the migration of larvae of the beet eelwonn, Heterodera schmhtii Schmidt. Ann. appl. Biol. 46, 74-85.

Walne, P. R. and Dean, G. J. (1972). Experiments on predation by the shore crab, Carcinus maenua L., on Mytilua and Mercenaria. J . cons. int. Explor. Mer. 34, 190-199.

Walter, H. E. (1906). The behavior of the pond snail Lynanaeua elodes Say. Cold Spring Harbor Monogr. 6 , 1-35.

Walter, H. E. (1907). The reaction of planarians to light. J . exp. 2001. 5,35-162. Watt, K. E. F. (1968). Ecology and Resource Management. McGraw-Hill,

London. Wautier, J. and Patthe, E. (1955). Experience physiologique et experience

ecologique. L’iduence du substrat sur la consommation d’oxygene chez lea Iarves d’ephemeropteres. Bull mens. SOC. linn. Lyon, 7, 178-183.

Webb, J. E. (1958s). The ecology of Lagos Lagoon. 111. The life history of Branchioetoma nigeriense Webb. Phil. Trans. R. SOC. B. 241, 335-353.

Webb, J. E. (1958b). The ecology of Lagos Lagoon. V. Some physical properties of lagoon deposits. Phil. Trans. R. Soc. B. 241, 393-419.

Webb, J. E. (1969). Biologically significant properties of submerged marine sands. Proc. R. SOC. B. 174, 355-402.

Webb, J. E. and Hill, M. B. (1958). The ecology of Lagos Lagoon. IV. On the reactions of Branchiostoma nigeriense Webb to its environment, Phil. Trans. R. SOC. B. 241, 355-391.

Weber, H. (1924). Ein Umdreh- und ein Fluchtreflex bei Nassa mutabilia. 2001. Anz. 60, 261-269.

Wecker, 5. C. (1963). The role of early experience in habitat selection by the Prairie deer mouse, Peromyacua manioulatua Bairdi. Ecol. Monogr. 33,

Weerekoon, A. C. J. (1956). Studies on the biology of Loch Lomond. 2. The repopulation of McDougall Bank. Ceylon J . Sci. 7 no. 2, vol. 1 (N.S.), 95-133.

Welch, P. S. (1914). Habits of the larva of Bellura melanopyga Grote (Lepidop- tera). Biol. Bull. mar. biol. Lab., Woo& Hole, 27, 97-114.

Welch, P. 5. (1935). Limnology. McGraw-Hill, London. Wellington, W. G. (1957).

dynamics : the development of a problem. Can. J . 2001. 35, 293-323.

2, 189-222.

Arch nderl. 2001. 11, 373-386.

orientation of marine animals. Archa nderl. 2001. 13, 493-499.

307-325.

Individual differences as a factor in population


Wellington, W. G. (1964). Qualitative changes in populations in unstable

Wells, M. J. (1962). “Brain and Behaviour in Cephalopods”. Heinemam, London. Wells, M. J. (1965). Learning by marine invertebrates. Adv. mar. Biol. 3, 1-62. Wells, M. M. (1917). The behaviour of limpets with particular reference to the

homing instinct. J . Anim. Behav. 7, 387-395. Welsh, J. H. (1930). Reversal of phototropism in a parasitic water mite. BWZ.

Bull. mar. biol. Lab., Woods Hole, 59, 165-169. Welsh, J. H. (1931). Specific influence of the host on the light responses of

parasitic water mites. Biol. Bull. mar. biol. Lab., Woods Hole, 61, 497-499. Westeide, W. (1968). Zur quantitativen Verteilung von Bakterien und Hefen in

einem Gezeitenstrand der Nordseekiiete. Mar. Biol. 1, 336-347. Wieser, W. (1955). The attractiveness of plants to larvae of root-knot nematodes.

1. The effect of tomato seedlings and excised roots on Meloidogyne hapla Chitwood. Proc. helminth. SOC. Wash. 22, 106-112.

Wieser, W. (1956). Factors influencing the choice of substratum in Cumella vulgark Hart (Crustacea, Cumacea). Limnol. Oceanogr. 1, 274-285.

Wilkes, A. (1942). The influence of selection on the preferendum of a Chalcid (Microplectron fuocipennie Zett.) and its significance in the biological control of an insect pest. Proc. R. SOC. B. 130, 400-415.

Williams, A. B. (1958). Substrates as a factor in shrimp distribution. Limnol. Oceanogr. 3, 283-290.

Williams, G. B. (1964). The effect of extracts of Fuouo serratus in promoting the settlement of larvae of Spirorbk borealis (Polychaeta). J . mar. biol. Ass.

Williams, G. B. (1965). Observations on the behaviour of the planula larvae of Cluva squamata. J . mar. biol. Ass. U .K . 45, 257-273.

Williamson, D. I. (1961a). Studies in the biology of Talitridae (Crustacea, Amphipoda): effects of atmospheric humidity. J . mar. biol. Ass. U.K. 30,

Studies in the biology of Talitridae (Crustacea, Amphipoda) : visual orientation in Talitrus saltator. J . mar. biol. Ass. U.K.

Wilson, D. P. (1928). The larvae of Polydora ciliata Johnston and Polydora hoplura ClaparBde. J . mar. biol. Ass. U.K. 15, 667-602.

Wilson, D. P. (1932). On the mitraria larva of Owenia fusiformk Delle Chiaje. Phil. Trans. R . SOC. B. 221, 231-334.

Wilson, D. P. (1948). The relation of the substratum to the metamorphosis of Ophelia larvae. J . mar. biol. Ass. U.K. 27, 723-760.

Wilson, D. P. (1949). Notes from the Plymouth aquarium. J . mar. biol. Ass.

Wilson, D. P. (1951). Larval metamorphosis and the substratum. Annke biol. 27,

Wilson, D. P. (1953a). The settlement of Ophelia bicornk Savigny larvae. The 1951 experiments. J . mar. biol. Ass. U .K . 31, 413-438.

Wilson, D. P. (1953b). The settlement of Ophelia bicornk Savigny larvae. The 1952 experiments. J . mar. biol. Ass. U.K. 32, 209-233.

Wilson, D. P. (1954). The attractive factor in the settlement of Ophelia bicornis Savigny. J . mar. biol. Ass. U .K . 33, 361-380.

Wilson, D. P. (1955). The role of micro-organisms in the settlement of Ophelia bicornie Savigny. J. mar. 6iol. Ass. U.K. 34, 631-543.

environments. Can. Ent. 96, 436-451.

U.K. 44, 397-414.

73-90. Williamson, D. I. (195lb).

30, 91-99.

U.K. 28, 346-351.

491-501.


Wilson, D. P. (1968). Some problems in larval ecology related to the localized distribution of bottom animals. In " Perspectives in Marine Biology". (Buzzati-Traverso, ed.) University of California Press, Berkeley and Los Angeles.

Wilson, D. P. (1968). The settlement behaviour of the larvae of S a b e l W alveolata (L.). J . mar. bwl. Ass. U.K. 48, 387436.

Wilson, D. P. (1970a). Additional observations on larval growth and settlement of Sabellaria alveolata. J. mar. bwl. Ass. U.K. 50, 1-31.

Wilson, D. P. (1970b). The larvae of SabeZlaria spinulosa and their settlement behaviour. J. mar. bwl. Ass. U.K. 50, 33-62.

Wisely, B. (1968a). The development and settling of a serpulid worm, Hydroides norvegica Gunnerus (Polychaeta). Auat. J. m r . Freehwat. Ree. 9, 361-361.

Wisely, B. (1968b). The settling and some experimental reactions of a Bryozoan larva Watersipora c d l a t a (Busk). Auat. J. mar. Freehwat. Ree. 9, 362-371.

Wisely, B. (1960). Observations on the settling behaviour of larvae of the tube- worm Spirorbis borealis Daudin (Polychaeta). Auat. J. 111~. Freehwat. Rea. 11, 66-72.

Wodsedalek, J. E. (1911). Phototactic reactions and their reversal in the may-fly nymphs Heptagenia interpundata (Say). Bwl. Bull, mar. bwl. Lab., Wooda Hole, 21, 266-271.

Wolsky, A. and Huxley, J. S. (1932). The reactions of normal and mutant types of Gammama chevreuxi to light. J . exp. Bwl. 9, 427-440.

Wood, D. L. (1963). Studies on host selection by Ips Gonfwrue (Leconte) (Coleoptera : Scolytidae) with special reference to Hopkins' host selection principle. Univ. Calif. Puble Ent. 27, 241-282.

Wood, E. J. F. (1950). Investigations on underwater fouling. 1. The role of bacteria in the early stages of fouling. Aust. J. mar. Freehd . Ree. 1,

Wood, K. G. (1966). Ecology of Chborwr (Diptera: Culicidae) in an Ontario Lake. Ecology, 37, 639-643.

Woods, J. D. (1971). Micro-oceanography. In " Underwater Science, an introduction to experiments by divers ". Woods, J. D. and Lythgoe, J. N. eds. pp. 291-317, Oxford University Press, London.

Yerkes, R. M. (1899). Reactions of Entomostraca to stimulation by light. Am.

Yerkes, R. M. (1900). Reaction of Entomostraca to stimulation by light. II. Reactions of Daphnia and Cyprie. Am. J. Physiol. 4, 40-22.

Yonge, C. M. (1937). The biology of Aporrhaie pee-pelecani (L.) and A . serreSiana: (Mich.). J . mar. biol. Ass. U.K. 21, 687-704.

Yonge, C. M. (1962). On the biology of the mesogastropod Trichotropis cancellata Hinds, a benthic indicator species. Biol. Bull. mar. biol. Lab., Wood8 Hole. 122, 160-181.

Yonge, C. M. and Campbell, J. I. (1968). On the heteromyarian condition in the bivalvia with species reference to Dreissem polymwpha and certain Mytilacea. Tram. R. SOC. Edinb. 68, 21-42.

Zobell, C. E. (1938a). Studies on the bacterial flora of marine bottom sediments. J. sedim. Petrol. 8, 10-18.

Zobell, C. E. (193813). The sequence of events in the fouling of submerged surfaces. Official Digest Fed. Paint and Varnish Prod. C1. Sept., 1-8.

Zobell, C. E. and Allen, E. C. (1936). The significance of marine bacteria in the fouling of submerged surfaces. J. Bwt. 29, 231-261.

Zobell, C. E. and Rittenberg, S. C. (1938). The occurrence and characteristics of chitinoclastic bacteria in the sea. J. Bact. 35, 276-287.

86-91.

J . Phy&l. 3, 167-182.

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