* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Download Enemy free space and the structure of ecological
Survey
Document related concepts
Restoration ecology wikipedia , lookup
Introduced species wikipedia , lookup
Occupancy–abundance relationship wikipedia , lookup
Molecular ecology wikipedia , lookup
Island restoration wikipedia , lookup
Biodiversity action plan wikipedia , lookup
Storage effect wikipedia , lookup
Latitudinal gradients in species diversity wikipedia , lookup
Habitat conservation wikipedia , lookup
Lake ecosystem wikipedia , lookup
Coevolution wikipedia , lookup
Ecological fitting wikipedia , lookup
Transcript
Biologiral Journal of the Linncan Socity (1984), 23: 269-286. With 1 figure Enemy free space and the structure of ecological communities M. J. JEFFRIES AND J. H. LAWTON Department of Biology, University of York, Heslington, York YO1 5DD Acccptcd for publication May I983 We define ‘enemy free space’ as ways of living that reduce or eliminate a species’ vulnerability to one or more species of natural enemies. Many aspects of species’ niches, in ecological and evolutionary time have apparently been moulded by interactions with natural enemies for enemy free space. We review a large number of examples. Yet many ecologists continue to think and write as though classical resource based competition for food or space is the primary determinant of species’ niches. Often it is not. The recognition that the struggle for enemy free space is an important component of many species’ ecologies may have important consequences for studies of community convergence, limits to species packing, and the ratio of predator species to prey species in natural communities. KEY WORDS:-Natural structure. enemies - interspecific competition - niche - escape space - community C0N TEN TS Introduction . . . . . . . . . . . . . . . Historical perspective . . . . . . . . . . . . . Theoretical arguments: a brief summary . . . . . . . . Examples . . . . . . . . . . . . . . . . . Species exclusion by natural enemies: community composition effects Fixed and flexible responses . . . . . . . . . . Evolution and enemy free space . . . . . . . . . Taxonomic range . . . . . . . . . . . . . Consequences . . . . . . . . . . . . . . . Caveats and conclusions . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269 271 273 274 274 279 279 280 28 I 282 283 283 INTRODUCTION Ecological theory relies heavily on the notion that species’ niches are moulded primarily by interspecific competition for limited resources, particularly food (e.g. Hutchinson, 1957; MacArthur & Levins, 1967; MacArthur, 1970, 1972; May & MacArthur, 1972; May, 1974). In ecology texts, niche theory and interspecific competition for limited resources are often discussed together (e.g. Krebs, 1978; Pianka, 1978; May, 1981). Predation, if it is discussed at all in this context, is usually regarded as something which modifies the primary role of interspecific competition, for example by promoting co-existence of potential 0024-4066/84/120269+ 18 $03.00/0 13 269 01984 The Linnean Society of London 270 M. J. JEFFRIES AND J. H. LAWTON competitors. Only in marine (e.g. Paine, 1966) and freshwater systems (Zaret, 1980) has predator-structuring of ecological communities been coherently and extensively studied. This paper reviews the role of natural enemies in moulding ecological niches. Our aim is to show how many numerous aspects of the ecology of animal species that are traditionally reviewed as components of their niche, (body size, feeding stations, feeding methods, etc.), have been influenced, not by competitors, but by natural enemies. Although all ecologists recognize that this must be so, many continue to act and write as though classical resource-based competition, especially for food, is the primary constraint operating on species’ niches, and to interpret community structure in this light. Hence, we have assembled a wide range of examples illustrating the extent to which natural enemies influence species niches. ‘Niche’ can be defined in several ways (Elton, 1927; Hutchinson, 1957, 1978; Whittaker et ul., 1973; Maguire, 1973). For present purposes, differences between these definitions are unimportant. Ecologists use the niche concept in its broadest sense to discuss a number of questions. Are there limits to the number of co-existing species in communities, i.e. are there limits to niche-space and niche-overlap? How and why do species differ in their use of resources, i.e. what is the significance of differences between species? These are some of the questions that we address in this paper. Species’ niches are influenced by many variables, including the physical environment, the nature and rate of supply of food resources, interspecific competition for limiting resources such as food or space and natural enemies. Because natural enemies have so often been ignored, we wish to focus on their effects, This does not mean we believe that other forces moulding species’ niches are unimportant. The idea of predator moulded niches is not a new one. Connell (1975) and Zaret (1980) cover many examples; Salt (1967) suggests the inter-relatedness of prey and predator niches, and our tables show the repeated, independent discovery of these same ideas. This review draws the disparate examples together. Twenty-five years ago. Williamson (1957) argued cogently that the consequences for two species sharing a natural enemy are, in general terms, iden tical to more conventional forms of interspecific competition for limiting resources. Indeed, Lotka (1925: 94) makes much the same point. These theoretical arguments were elaborated by Holt (1977) (see below), who coined the term “apparent competition” for cases where two or more victim species interact via a shared enemy, or enemies. Lotka, Williamson and Holt show that the abundance of species may be reduced, or species eliminated entirely from a community by populations of polyphagous enemies sustained by alternative prey species. Hence there may be competition between victim species for “enemy free space”. By enemy free space we mean ways of living that reduce or eliminate a species’ vulnerability to one or more species of natural enemies. Absolute enemy free space is extremely rare in nature. Life styles that reduce or eliminate attacks by one group of enemies will usually expose victim species to alternative modes of attack. Species co-existing and surviving in a community have by definition found sufficient enemy free niche space to sustain their populations. Inter aliu, species may be eliminated from a community because they are critically vulnerable to one or more species of resident natural enemy; ENEMY FREE SPACE 271 and in the long run species may evolve to reduce this vulnerability (Vermeij, 1982). Hence a study of enemy free space has two components, contemporary interactions taking place in ‘ecological time’ and much longer responses in ‘evolutionary time’. Our aim in this review is not to show how predators control species diversity, except in passing. Such data have already been summarized by Connell (1975) and Zaret (1980) amongst others. Rather our objectives are: (1) to show how species niches are influenced by the presence or absence of natural enemies, in ecological and evolutionary time; (2) to summarize examples of species competing via shared natural enemies, and to clarify the nature of enemy free space; (3) to consider the sorts of communities where competition for enemy free space may be paramount in determining community structure; (4) to consider the implications of enemy free space arguments for such phenomena as community convergence, limits to species packing and the ratios of number of predator species to number of prey species in ecological communities. By ‘enemy’ we mean any consumer that eats living victims; these need not be only conventional predators, they may also be insect parasitoids hunting for hosts (Askew, 1971; Hassell, 1978), or even internal parasites (Freeland, 1983). Our own expertise and knowledge of the literature is unevenly distributed across these three types of enemy, being strongest in the first two. We have, for good measure, included some plant (victim)-herbivore (enemy) examples, although our main emphasis is on animals and their enemies. For convenience, we have used ‘predation’ to include attack by all these enemies. We have made no attempt to provide an exhaustive review, but have assembled examples that are familiar to us. We believe they are sufficient to sustain our case. HISTORICAL PERSPECTIVE The notion that species may compete for enemy free space has a long history. T o our knowledge the idea has been explicitly formulated by at least 15 authors, or implicitly developed or hinted at by several others (Table I ) , but for some reason it has never received full attention, nor do workers in independent fields always appreciate that much the same mechanism is a t work in many types of ecological system. All the papers in Table 1 explicitly argue that major aspects of species’ lifestyles (i.e. niche) are moulded by the impact of natural enemies. Charles Darwin was the first to argue this when he wrote (quoted in Hutchinson, 1978: 153) “one is sometimes tempted to conclude, falsely as I believe, that nature has worked for mere variety. Thus when we h e a r . . . that M r Bates collected within a days journey, in a quite uniform part of the valley of the Amazons, 600 different species of butterflies one may at first doubt whether each is adapted to its own peculiar and different line of life; but from what we know of our own British Lepidoptera we may confidently believe that most of the 600 caterpillars would have different habits, or be exposed to different dangers from birds and hymenopterous insects”: In other words, many of these species characteristics are important for avoiding natural enemies. After this paper was accepted for publication, Dr R. D. Holt kindly drew our attention to a further important historical example. Grinnell (1917) in his M. J. JEFFRIES AND J. H. LAWTON 272 Table 1. Papers developing the concept of enemy free space, in date order, by author. Numbers refer to these examples in the text. Source I Darwin 2 Brower (1958) 3 Askew (1961) 4 Moment (1962) 5 Huffaker (1971) 6 Root (1973) 7 Hebert cf al. (1974) 8 Gilbert (1975) 9 Ricklefs & ORourke (1975) 10 Zwoelfer (1975) 11 Charnov cf al. (1976) 12 Orians & Solbrig (1977) 13 Otte & Joern (1977) 14 Schultz cf al. (1977) 15 Lawton (1978), Lawton & Strong (1981) 16 Price cf al. (1980) 1 7 Zaret (1980) 18 Atsatt (1981) 19 Kitchell cf al. (1981) 20 Freeland (1983) System Amazonian Lepidoptera Phytophagous insects Role of enemy free space See text Pressure to diversify to avoid predation Oak gall wasps and parasites Evolution of vaned gall shapes to minimize attacks by others’ parasi toids Many Phyla Notes individual variation; suggests this aids predator avoidance. “Reflexive evolution” Many systems Suggest role of predator pressure in diversification Insect communities Role of enemy free space hinted at for system structuring Canadian moths Most abundant species had fewest close relatives, suggesting shared predation upon similar species may reduce numbers of each Hcliconius and PasnjYora species Plant diversity dictated by number of leaf shape options to avoid other species’ caterpillar attackers Tropical and temperate moths Moth aspect diversity shows consistent limits. Siggests limit.to enemy free space Insects Explicitly discusses insect speciation and role of enemy free space in niche differentiation Many systems Complementarity of predator avoidance and system structuring Number and variety of ‘hiding places’ Insects on desert bushes profoundly influences community structure Grasshoppers System diversity related to “Escape space” Insects on Creosote bush, Number and variety of ‘hiding places’ profoundly influences community L.uwca sp. structure Phytophagous insects Pressure to avoid other species’ predators; enemy free space may mould community form Role of plant/herbivore interaction in Phytophagous insects avoiding predation. Use term “Escape Space” Freshwater zooplankton Role of enemy free space identified in communities detail Lycaenid butterflies Lycaenid radiation and patterns of host use linked to use of ant-associated enemy free space Fossil gastropods Predation produces competition among prey species to reduce attractiveness towards predators Explicitly identifies parasites as being Animal hosts of major importance in determining niche differences between host-species ENEMY FREE SPACE 273 famous paper on the niche of the California thrasher concluded that cover for escaping predation is an essential component, and that ‘it is not any peculiarity of food-source, or way of getting at it’, that alone limits the thrasher’s niche ( p 432). As Dr Holt pointed out to us, it is ironic that one of the very first instances of the use of the word ‘niche’ in ecology emphasized predation rather than competition as a constraint. THEORETICAL ARGUMENTS: A BRIEF SUMMARY Consider the simplest possible case of whether or not a species can invade and maintain itself in an established community. As Holt (1977) shows the conditions for invasion are identical to those needed for the invader to have a positive equilibrium density in the community, namely that its rate of increase must be higher than the rate at which established polyphagous natural enemies find and destroy it. Formally, for invasion and establishment: ?> ujp (1) Where ?=instantaneous rate of increase of invading victim species j ; uj= attack rate (or area of discovery-see Varley et uf., 1973; Hassell, 1978) of an established natural enemy population on species j ; p = density of established polyphagous enemies. Characteristics of species j that reduce uj, for instance their size, colour or feeding place, will favour the establishment o f j in the community. Clearly, the more speciesj differs from victim populations already in the community the less likely enemies are to recognize it as food, or the less likely they are to be able to deal with it successfully (i.e. the lower f j ) and the more likely speciesj is to invade. Likewise small densities of established enemies (p small) brought about by a shortage of alternative victim populations will also favour the establishment of j . In general terms such effects are identical to those seen in more conventional cases of competition, promoting co-existence of species with different ecologies, invasion in the absence of similar species and exclusion in their presence. Species may, of course, fortuitously possess characteristics that allow them to invade an established community. In a n ideal world such preadaptions (or exaptations”, Gould & Vrba, 1982) should be distinguished from character evolution as a direct result of predation (e.g. Vermeij, 1982). Unfortunately in the examples that follow we are often unable to do this. O u r inability to distinguish evolved adaptations from exaptations makes little difference to arguments about the importance of enemy free space as a force structuring communities, but it makes a big difference to understanding the evolution of enemy free space. Figure 1 formulates the notion of enemy free space diagrammatically. I n this hypothetical example three characteristics define species’ vulnerability to a set of existing predators, body size, rate of movement and toxicity. Clearly n such axes could exist, and the analogy with Hutchinson’s ‘hypervolume’ is very close. (Hutchinson, 1957). In the example there are five co-existing victim species with characteristics as indicated, subject to attack by established enemies. Invasion of two further species is not possible, because for both equation (1) is not satisfied. 6‘ M. J. JEFFRIES AND J. H. LAWTON 274 Increasing speed o f movement 4 Increasing body size Increasing toxity Figure 1 . Hypothetical example of species’ characteristics that determine their vulnerability to natural enemies. Five species (solid dots) are established in the community, with characteristics of speed of movement, size and toxicity as indicated. Two further species ( A and B) are excluded by the established natural enemies of species 1-5 because they possess characteristics that make them particularly vulnerable to predation. (See text for further discussion.) In one case (B, Fig. 1) we might imagine that the potential invader is too similar to one set of established species; the other potential invader (A, Fig. 1) is very slow, non-toxic and hence very vulnerable. A moment’s thought makes plain that enemy free space is unlikely to be fixed. In any habitat, it will depend upon the nature of established victims and enemies, as well as on the size and age of the potential invader. We return to these problems later. They do not make the concept of enemy free space impossible to work with. They do mean that critically testing the idea in real communities requires care and thought. EXAMPLES Despite such complication, examples of enemy free space and predator moulded niches abound in the literature. I t is to these that we now turn. Table 2 summarizes a wide range of examples of enemy free space in ecological communities, grouped by habitat and by taxa within habitat. Each example has been given a number as have the examples in Table 1. The phenomena gathered together in Tables 1 and 2 are many and varied, but each illustrates one or more aspects of the broad problem of enemy free space as follows. Species exclusion by natural enemies: community comfiosition efects Experimental manipulation of predators in communities often reveals victim species that are unable to survive in the presence of particular enemy species. 275 ENEMY FREE SPACE Table 2. Examples of enemy free space in a wide variety of ecological systems, grouped by taxa and habitat and thereafter in date order. Numbers refer to examples in the text. Source Freshwater systems 21 Porter (1973) 22 Briand & McCauley (1979) Victim Enemy Nature of enemy free space Phytoplankton Zooplankton S, M and other (toxins) Phytoplankton Zooplankton S. Sized based differential predation M. Spined morphs in e.f.s. Rotifers Invertebrate predators S, M. Size morph based differential predation 23 Gilbert (1967) 24 Kerfoot (1977) Rotifers Zooplankton 25 Hebert & Loaring ( 1980) Zooplankton 26 Hrbacek (1959) Zooplankton 27 Brooks & Dodson ( 1965) Zooplankton Fish 28 Rief and Tappa (1966) Zooplankton Fish 29 Galbraith (1967) Zooplankton Fish 30 Green (1967) Zooplankton Fish 31 Zooplankton Fish 32 Zaret (1969) Zooplankton Fish 33 Zaret (1972) Zooplankton Fish 34 Allen (1974) Zooplankton Fish 35 Stich & Lampert (1981)Zooplankton Fish Brooks (1968) 36 Sprules (1972) 37 Giguere (1979) Zooplankton Zooplankton 38 Lynch (1979) 39 Stein & Magnuson (1976) Zooplankton 40 Johnson & Crowley ( 1980a) 41 Johnson & Crowley (1980b) 42 James (1967) 43 Bay (1974) 44 Hulbert el al. (1972) Invertebrate predators S, M. Size morph based differential predation S, M. Size morph based Fish differential predation Salamander Salamander and Chaoborus Salamander S, P. Differential predation of sizes and littoral/pelagic morphs S. Differential predation of sizes S. Differential predation of sizes M. Differential predation of morphs S. M. Differential predation of sizes and morphs M. Differential morph predation M. Differential morph predation S. Size based differential predation in a model system P. Differential predation based on position in water column S. Differential size predation S. Differential size predation S. Differential size predation S, M, P. All criteria alter e.f.s.; crayfish may change many aspects of behaviour in presence of a predator P. Differential predation Fish Odonata larvae based on microhabitat available P. Differential predation Fish Odonata larvae based on microhabitat available Invertr 'ate pre tors P. Differential predation Mosquito larvae based on position in pond Invertebrate predators P. Differential predation Mosquito larvae based on position in pond Most prey not in enemy Many invertebrate taxa Fish free space. Differential predation of some due to position Crayfish Fish M. J. JEFFRIES AND J. H.LAWTON 276 Table 2. 45 Source Victim Kerfoot (1982) Many invertebrate taxa Various 46 McPhail (1969) 47 Moodie (1972) Enemy Sticklebacks Fiah Sticklebacks Fish 48 Fraser & Ccm (1982) Minnows Fish 49 Morin (1981) Tadpoles Salamander 50 Sih (1981, 1982) Freshwater systems Coastal and shallow marine systems 51 Randall (1965) Sea grass Fish 52 Paine (1969) Gastropods Starfish 53 Vermeij (1974) Gastropods Fish and crabs 54 Dayton (1971) Barnacles Limpet 55 Coen ct al. (1981) Shrimps Fish 56 Birkeland (1974) Sea pen Starfish 57 Menge (1976) Rocky shore system as a whole 58 Vance (1979) Rocky shore system as a whole 59 Campbell & Denno (1978) Salt marsh pool invertebrates 60 Evans (1979) Benthic and burrowing Shore-birds invertebrates Terrestrial invertebrates 61 Coeden & Louda (1976) Fish Biological control agents Predators and (phytophagous insects) parasitoids 62 Heinrich (1979) Caterpillars Various 63 Polis (1980) Scorpions Scorpions 64 Thornhill (1980) Scorpion flies Various 65 Opler (1981) Mantispidi Various Nature of enemy free space Other. Distaste and a m m a t i c coloration M. Morph bared differential predation M. Morph bared differential predation P. Change in distribution in presence of predator Differential predation of species. Precise form of e.f.s. not identified Predator avoidance has a major effect on species’ feeding ecology P. Differential predation based on distance from reef that harbours fish. Reef in e.Es. for the fish themselves P. Position on shore determines e.f.s. S, M. Shells give e.Es. Global and local scale S, M. Differential resistance to limpet grazing size and morph based P. e.f.s. based on microhabitat Other. Specific defences against certain species of starfish P. Barnacle dominance on upper shore due to absence of predation high up shore Most species of plant lost due to urchins. No e.Es. A few have morphological e.Es. Others. Toxic corixids in e.ts. Other species removed by fish P. Position in mud changes vulnerability Some introduced biological control agents arc not successfid because they are attacked by local predators. Not in e.Es. P. Foraging position gives efs. P. Position of feeding sites and activity patterns affect e.Es. P. E.Es. gained from position in vegetation M. Role of e.Es. and mimicry d i s c u d ENEMY FREE SPACE 277 Table 2. Source Terrestrial vertebrates 66 Janzen (1976) Victim Enemy Reptiles (African) Various 67 Carlquist (1965) Endemic bird species, often flightless 68 Barnard (1979) House sparrow 69 Howe (1979) Frugivorous birds 70 Nilsson (1979) Passerines 71 Grubb & Greenwald ( 1982) 72 Karr (1982) Sparrows 73 Patterson & Pascual ( 1968) S American fossil 74 Barbehenn (1969) Small mammals 75 Grant (1972) Snowshoe and Arctic hares 76 Leuthold (1977) African ungulates Terrestrial vegetation 77 Janzen (1966) Ground feeding birds marsupials Suggests paucity of reptile species due to low e.f.s.largely positional Various, e.g. cats, rats, Many examples of extinctions on islands are man due to lack of e.f.s. against new predators P. Feeding sites selected to Sparrowhawks reduce predation P. Feeding sites selected to Various reduce predation P. Feeding sites selected to Sparrowhawks reduce predation P. Feeding sites selected to Various reduce predation Extinctions caused by lack Snakes, coatis of e.f.s. N American mammal Extinction of marsupial herbivores may be due to predators lack of e.f.s. from invading predators. Prey actually duplicate predators’ previous prey type due to convergence, but lack coevolved defences P. Community defined by Parasites resistance to parasites. Cannot invade areas containing parasites of other species to which own species is not immune P. Arctic hare’s reduction Lynx due to alternative prey increasing lynx numbers Mammalian predators P. Differ in drinking sites due to predation Thorn acacia Phytophagous insects 78 Harper (1969) Plants Herbivores 79 Gilbert (1971) Passijlora spp. Heliconiid butterflies Microbial systems 80 Mitchell (1971) 81 Levin el a f . (1977) Microbial communities Escherichia coli Nature of enemv free space T. phage Other. Acacias derive protection from ant association Several instances of role of e.f.s. given e.g. Hypericum perfliatum in shade M. Trichome defence in some species Immigrant species do not flourish, have no e.f.s. to resident pathogens M. Differential morph resistance to 7. phage attack The nature of enemy free space (e.f.s.) classifies the means of avoiding or reducing the impact of natural enemies under three broad headings: M, morphology, e.g. possession of a shell, or defensive exoskeleton; S, size, i.e. the species is too small or too large to be attacked by resident enemies; P, position occupied in the habitat reduces or eliminates predation. Other mechanisms embrace a ragbag of alternatives, including toxicity, speed of movement etc. 278 M.J. JEFFRIES AND J. H.LAWTON For these victims of predation, enemy free space in the community in question is absent or too scarce a resource to ensure survival. At least one species, often more, falls into this category in many of the examples in Table 2. There is then a continuum of examples from total vulnerability to complete indifference to the presence or absence of particular predators. Examples of species immune to attacks of specific predators within a system can be found in several references (Table 2). Hence, predators may have profound effects in determining which, and how many species co-exist in ecological communities. This point has been made by Connell (1975), Zaret (1980) and other workers. The control of species numbers is, however, only one part of the problem. There are a whole set of important, but largely ignored questions about the characteristics distinguishing vulnerable species from non-vulnerable species, and how the non-vulnerable species escape enemies. Species may avoid predation in many ways (see Zaret, 1980 for detailed comments on freshwater systems), but we can classify these into three broad groups, listed in Table 2 as size (S), morphology (M) and position (P), together with a ragbag of mechanisms (‘other’) that do not conveniently fall into any category. The effects of size, position and morphology may be evaluated intraor interspecifically. No one species of predator has infinitely flexible hunting behaviour; so what constitutes enemy free space against one species, or guild, of predators may make a victim hopelessly vulnerable to others. T h e species that co-exist in one habitat do so because they are not fatally vulnerable to any of the enemies in that habitat. Usually we have no idea how this is achieved for all the enemies that a species may be exposed to, but we do know, or can guess, how it is achieved for particular enemies and potential victims (summarized in Table 2). Enemy free space may be achieved for some species by virtue of their size; they are either too large or too small to be killed by the predator(s) (e.g. Table 1: 17; Table 2: 22, 24, 25, 26, 27, 28, 29, 31, 34, 35, 36, 37, 38, 54). Similarly they may have morphologies that markedly reduce or eliminate predation (Table 1: 3, 8; Table 2: 21, 23, 25, 26, 30, 31, 32, 33, 46, 47, 54, 79, 81) or they may occupy parts or places in the habitat where they are not vulnerable (e.g. Table 2: 40, 41,42, 43, 44, 51, 52, 55, 57, 60, 74, 78). These three characteristics of size, morphology and position in the habitat are the very same criteria often given as ‘separating’ species in classical competition theory. Body size and position in the habitat, particularly feeding sites, are often cited as niche characteristics moulded by ‘conventional’ forms of competition for limiting food or space. Table 2 makes it obvious that the need to avoid enemies had identical effects. Morphological defences and many of the miscellaneous ways of avoiding or reducing predation (e.g. Table 2: 21, 56, 59, 65), are not usually cited as being directly influenced by interspecific competition for limiting resources. However, if species have evolved particular ways of avoiding predation, this may automatically impose constraints on many aspects of their ecology. Hence, many other aspects of a species’ niche may be a secondary, but inevitable, consequence of selection pressures imposed by predators, not competitors; or a compromise between the need to minimize the risk of predation, and the effects of competition. ENEMY FREE SPACE 279 Fixed andjexible responses Some species minimize or avoid the effects of certain predators because of genetically fixed features of their ecology; their size, shape or feeding site (e.g. Table 2: 27, 39, 42, 43, 46, 47, 65, 79). Some species display genetically flexible responses over several generations in the face of selection by predators (e.g. Table 2: 23). Still others change their short term behaviour, adopting one feeding mode or site in the absence of a predator and another in its presence (Table 2: 39, 48, 50, 68, 70, 71). This process has previously been called ‘depression’ by Charnov et al. (1976). Prey availability is lowered under predation, without necessarily any harvesting. There may be a brief, local behavioural change in prey availability or a longer term change. Several workers on optimal foraging theory have recently discussed risk avoidance by victims (e.g. Hassell & Southwood, 1978). This is exactly the problem of predators inducing short-term changes in a species’ feeding niche. I n the absence of a predator individuals may prefer to forage in one particular part of their habitat. In the presence of a predator behaviour changes markedly, foraging in the preferred site is abandoned or much reduced, and foraging concentrated in safer places (Table 2: 39, 48, 50, 68, 69, 70, 71). Such ‘niche shifts’ by the same species in different places are often attributed to changes in competitors (e.g. Diamond, 1975). They may equally well be due to the presence or absence of particular enemies. Sometimes vulnerability to enemies is altered by whether or not a second enemy involved. Parasites may modify host niches to enhance their host’s vulnerability and so ensure their being eaten by the next host in the parasite’s life-history (Holmes & Bethel, 1972). Alternatively insect parasitoids may alter host behaviour to lessen predation by normal host enemies. Fritz (1982) cites examples involving movement reduction, microhabitat shifts and morphological changes in parasitized hosts. In all such cases the parasitelparasitoids are manipulating host enemy free space to increase their own survival. Enemy free space considerations may impinge widely upon other behaviours, not strictly of ecological interest. We include two examples for completeness. Strong (1973) demonstrates that predation is a powerful modifier of amplexus in amphipods. Those in amplexus are more conspicuous and slower (reduced enemy free space). The time spent in amplexus correlated negatively with degree of predation, even in populations only a short distance apart. Similarly, mating calls in tropical frogs may be impaired by the presence of predatory bats (Tuttle & Ryan, 1981). Evolution and enemy free space The universal distribution of means of defence against enemies of one form or another, of mimicry, camouflage, aposematic coloration, spines, toxins, armour and so forth attests to the enormous selection pressures imposed by enemies upon their victims (see Vermeij, 1982 for recent discussion). What is not clear is how many of the examples of enemy free space summarized in Tables 1 and 2 are genuine cases of evolution or even of coevolution of sets of victim species with one or more enemies, and how many are fortuitously evolved characteristics selected for in other circumstances and/or by 280 M. J. JEFFRIES AND J. H. LAWTON other enemies in other habitats that now permit species to co-exist with little or no evolutionary history-exaptations in the sense of Gould & Vrba (1982). Distinguishing exaptations from evolved adaptations from co-evolution is a major challenge for future research. However, it would be bizarre if many predators have not played some part in the evolution of defences of prey that they feed upon at the present time. In other words, many of the niche characteristics influenced by predation, summarized in Table 2. are evolved responses to contemporary enemies. Others have undoubtedly been evolved in response to enemies long gone. Co-evolution, the reciprocal long-term evolutionary interaction of a n enemy and its victims is a more difficult problem. For example, Vermeij (1982) has recently retracted his earlier views (e.g. Vermeij & Covich, 1968) that enemy and victim are locked into an evolutionary ‘arms race’. The conditions under which co-evolution is to be expected are much more restricted than commonly supposed (Thompson, 1982). Problems of co-evolution aside, it does not seem to be widely appreciated how rather small differences between individual victims may radically alter predation pressures and hence selection pressures. Consider the case where predators forage optimally (see Krebs & Davies, 1978). Now, quite small changes in prey body size or in the form and strength of protective cases may sufficiently alter the predator’s ratio of food gain to effort as to make a previously desirable victim species no longer profitable, and vice versa. A former victim may simply be dropped from the optimum diet set if the predator’s ratio of energy gain to handling time with that victim falls below a critical level. Livdahl ( 1979) reports interesting differences in predator handling times with the same species of mosquito larvae collected from areas with and without predators; handling times were longer and hence prey profitability was less in mosquitoes from areas exposed to predation. The evolutionary implication of small changes in prey profitability are easy to envisage. Community effects are less clear. They suggest that enemy free space may depend critically on the relative profitabilities and abundances of other species in the habitat, making it difficult to discover why a species is able to invade one habitat, but not another area supporting the same, or similar, enemies, but different victims. Taxonomic range The effect of enemy free space is very clear and well documented in freshwater planktonic systems and is apparently the major factor determining species composition, with ‘classical’ interspecific competition only secondarily affecting the details of community structure (Zaret, 1980). Phytophagous insect communities also appear to provide some clear examples (Lawton & Strong, 1981; Strong, Lawton & Southwood, 1984). However, all taxa and habitats are represented to some extent in Tables 1 and 2, although major differences in the importance and mode of action of enemy free space are to be expected. Most important, Table 2 is not a random sample of the world’s biota and the distribution of examples across habitats and taxa are determined to a considerable extent by our own grasp of the literature, and a predisposition of workers on particular taxa or habitats to ignore or be interested in enemy free ENEMY FREE SPACE 28 1 space. The distribution of examined material certainly does not reflect the importance of enemy free space in nature. Bird populations, for example, have traditionally been regarded as food limited (Lack, 1966) and sets of bird species are widely assumed to be structured by interspecific competition for food (e.g. Cody, 1974; Diamond, 1975), but even here the role of natural enemies in determining the presence of absence of species, their distribution and feeding niches cannot be ignored (e.g. Table 2: 68, 69, 71, 72). In passing it is worth noting an important difference between ‘enemy effects’ and ‘competitive effects’. Interspecific competition for food by definition implies density dependent resource limitation. Niche differences and community structure determined by conventional competition are extremely unlikely without density dependent resource limitation (see Strong et al., 1984; Lawton, 1984 for further discussion). But we do not think it is necessary for species to be controlled by predation (in a direct or delayed density dependent fashion) for competition for enemy free space to be a significant ecological and evolutionary force. Predation may kill species in a density independent manner or inverse density dependent manner and selection will still favour not being killed. Hence one cannot deduce the likely importance of enemy free space in structuring a community or moulding niches from the nature of the density dependent controlling mechanisms (or lack of them) operating on species in a community. CONSEQUENCES The examples summarized in Tables 1 and 2 point logically to two conclusions, and lead us to speculate about two interesting theoretical possibilities. First, niche differences between similar species sharing a habitat, ‘co-existing species’, might often just as easily be explained by the effects of natural enemies as by more conventional competitive effects. Wherever populations of polyphagous natural enemies are sustained by more than one species of prey, selection may favour divergence in the characteristics of one or more of those prey species to minimize the impact of the natural enemy. Of course other scenarios are possible. Species may converge on the same solution, enhancing species’ similarities. Other ‘differences between species’ and the niche characteristics of particular species may be imposed by selection from strictly monophagous enemies, and so on. Our aim is not to become embroiled in such possibilities at this stage, but merely to remind ecologists of the profound effect that predators have upon species’ niches, and by so doing divert attention away from the widely held, and in our opinion, mistaken, view that niche differences between species are usually due to the historical effects of ‘classical’ resource based competition. The effects of competition for enemy free space deserve much more serious study. Second, numerous examples of niche shifts now exist in the literature, when a particular species behaves in one way in one community or place, but behaves differently somewhere else. Such niche shifts are almost invariably attributed to, or correlated with, the presence or absence of competition. Table 2 gives several examples where niche shifts appear to be due to the presence or absence of particular natural enemies. These changes in feeding behaviour, feeding site and 282 M. J. JEFFRIES AND J. H. LAWTON so on may be facultative and flexible or apparently genetically fixed in different populations. We do not argue that all niche shifts are enemy induced. We do argue that ecologists rarely consider enemies, and too often consider competitors, as the explanation for niche shifts when they find them. From the empirical base established in Tables 1 and 2 speculation is easy. We restrict ourselves to two possibilities, namely problems of convergence in community structure and the ratio of predators to prey in food webs. The theoretical arguments of Williamson (1957) and Holt (1977) (loc. cit.), show that competition for enemy free space has many of the consequences of more traditional forms of competition: limits to the number of co-existing species in a community, niche differences between species and so forth. But, whereas standard competition for limiting resources may, at least in theory, lead to convergence in community structure under similar climatic conditions (for discussion see Orians & Solbrig, 1977; Cody & Mooney, 1978), communities constrained by natural enemies will not converge unless the enemies are the same, or have similar properties, in the same environments. Zaret (1980) discusses this problem at length for the effects of fish predation on the structure of freshwater communities. This problem is worthy of more theoretical and empirical attention. We see no reason why convergence in community structure should necessarily be expected, even under similar climatic conditions, if communities of predators and prey start off, by chance, from different initial conditions, as often they must. Enemy free space depends on the nature of the predators, which often depend upon the nature of the prey, and simultaneously upon selection pressures being imposed by what everybody else is doing. We see no reason why this lottery should have only one unique configuration of niche space as its end point. But, given that only a limited number of prey types are able to co-exist with a particular type of predator, competition for enemy free space does lead to one interesting general feature of communities: namely, a broadly constant ratio of prey (victims) to predators (enemies) in food webs (e.g. Arnold, 1972; Cameron, 1972; Cohen, 1977, 1978; Moran & Southwood, 1982). The data on which such a generalization is based is nothing like as reliable as we should wish and our interpretation may simply be wrong (see for example Evans & Murdoch, 1968 versus Cole, 1980), in which case, speculation is idle. But if the data are even crudely correct, then a constant ratio of prey to predators in food webs may find its underlying theoretical explanation in competition for enemy free space among victim species and limits to the number of species able to co-exist with different species of predators (seeJeffries & Lawton, 1984 for further discussion). CAVEATS AND CONCLUSIONS Niche differences between species driven by competition for enemy free space, indeed the whole notion of enemy free space, is only a hypothesis. Tables 1 and 2 do not test the hypothesis, or any of its corollaries in detail. They merely gather evidence that is broadly in agreement with these ideas. It will require great efforts to distinguish the relative roles of predation and competition in moulding species’ niches and community structure in particular systems. Zaret’s (1980) work on freshwater communities is a pioneering example. Our main purpose in this paper has been to gather comparable examples ENEMY FREE SPACE 283 from a large number of different systems, illustrating the independent discovery of the same basic idea many times over. These examples are now so many that we do not understand why so many ecologists continue to write and think about niches and community structure as though they were almost always moulded by classical interspecific competition for limiting resources such as food. Enemy free space deserves more critical attention. ACKNOWLEDGEMENTS Professor Mark Williamson, Doctors Phillip Crowley and Malcolm MacGarvin, Philip Heads, and Simon Fowler read and made very helpful comments on earlier drafts of this paper. Dr R. D. Holt drew our attention to several early examples, particularly those by Lotka and Grinnell. M. J. Jeffries is supported by an NERC studentship. REFERENCES ALLAN, D. J., 1974. Balancing predation and competition in cladocerans. Ecology, 55: 622-629. ARNOLD, S. J., 1972. Species densities of predators and their prey. American Nafurulist, 106: 220-236. ASKEW, R. R., 1961. On the biology of the inhabitants of oak galls of Cynipidae (Hymenoptera) in Britain. Transactions of the Sociely for British Entomology, 14: 237-268. ASKEW, R. R., 1971. Parasitic Insects. London: Heinemann. ATSATT, P. R., 1981. Lycaenid butterflies and ants. Selection for enemy free space. American Naturalist, 118: 638-654. BARBEHENN, K. R., 1969. Host-parasite relationships and species diversity in mammals-a hypothesis. Biotropica, I : 29-35. BARNARD, C. J., 1979. Interactions between house sparrows and sparrowhawks. British Birds, 72: 569-573. BAY, E. C., 1974. Predator-prey relationships among aquatic insects. Annual Review of Entomology, 19: 441-453. BIRKELAND, C., 1974. Interaction between a sea pen and seven of its predators. Ecological Monographs, 44: 21 1-232. BRIAND, F. & McCAULEY, E., 1979. Zooplankton grazing and phytoplankton species richness: field tests of the predation hypothesis. Limnology and Oceanography, 24: 243-252. BROOKS, J. L., 1968. The effects ofsize selection by lake planktivores. Sysfemafic .(oology, 17: 273-291. BROOKS, J. L. & DODSON, S. I., 1965. Predation, body size and composition of plankton. Science, 150: 28-35. BROWER, L. P., 1958. Bird predation and food plant similarity in closely related procryptic insects. American Naturalist, 92: 183- 187. CAMERON, G. N., 1972. Analysis of insect trophic diversity in two salt marsh communities. Ecology, 53: 58-73. CAMPBELL, B. C. & DENNO, R. F., 1978. The structure of the aquatic community associated with intertidal pools in a New Jersey salt marsh. Ecological Entomology, 3: 181-187. CARLQUIST, S., 1965. Island Life. New York: Natural History Press. CHARNOV, E. L., ORIANS, G. H. & HYATT, K., 1976. Ecological implications of resource depression. American Naturalist, 110: 247-259. CODY, M. L., 1974. Compefition and the Structure of Bird Communities. Princeton, New Jersey: Princeton University Press. CODY, M. L. & MOONEY, H. A,, 1978. Convergence versus noncovergence in Mediterranean-climate ecosystems. Annual Review of Ecology and Systematics, 9: 265-32 I . COEN, L. D., HECK, K. L. & ABELE, L. G., 1981. Experiments on competition and predation among shrimps of sea grass meadows. Ecology, 62: 1484-1493. COHEN, J. E., 1977. Ratio of prey to predators in community food webs. Nature, London, 270: 165-167. COHEN, J. E., 1978. Food Webs and Niche Space. Princeton, New Jersey: Princeton University Press. COLE, B. J., 1980. Trophic structure of a grassland community. Nufure, London, 286': 76-77. CONNELL, J. H., 1975. Some mechanisms producing structure in natural communities; a model and evidence from field experiments. In M. L. Cody & J. M. Diamond (Eds), Ecology and Evolufion of Communities: 460-491. Cambridge, Mass.: Belknap Press. DAYTON, P. K., 197 I . Competition disturbance and community organisation; the provision and subsequent utilisation of space on a rocky inter-tidal community. Ecological Monographs, 41: 351-389. DIAMOND, J. M., 1975. Assembly of species communities. In M. L. Cody & J. M. Diamond (Eds), Ecology and Evolufion of Communities: 342444. Cambridge, Mass.: Belknap Press. ELTON, C. S., 1927. Animal Ecology. Londo-x Sidgwick and Jackson. M. J. JEFFRIES AND J. H. LAWTON 284 EVANS, F. C. & MURDOCH, W. W., 1968. Taxonomic composition, trophic structure and seasonal occurrence in a grassland insect community. Journal of Animal Ecology, 37: 259-273. EVANS, P. R., 1979. Adaptations shown by foraging shore birds to cyclical variations in the activity and availability of their intertidal prey. In E. Naylor & R. G. Hartnoll (Eds), Cyclic Phenomm in Marine Plants and Animals: 357-366. Oxford: Pergamon Press. FRASER, D. F. & CERRI, R. D., 1982. Experimental evaluation of predator-prey relationships in a patchy environment: consequences for habitat use patterns in minnows. Ecology, 63: 307-313. FREELAND, W. J., 1983. Parasites and the coexistence of host animal species. A m ' c u n Naturalist, 121: 223-236. FRITZ, R. S., 1982. Selection for host modification by insect parasitoids. Evolution, 36: 283-288. GALBRAITH,, M. G., 1967. Size selective predation on daphnia by rainbow trout and yellow perch. Transuctions of the Amnican Fisheries Society, 98: I - 10. GIGUERE, L., 1979. An experimental test of Dodson's hypothesis that Ambystoma (a salamander) and Chaoborur (a phantom midge) have complementary feeding niches. Canadian Journal of <oology, 57: 1091- 1097. GILBERT, J. J., 1967. Asplanchu and posterolateral spine production in Brachimw calycilorur. Archiv fun Hydrobiologic, 64: 1-62. GILBERT, L. E., 1971. Butterfly-plant coevolution: has PusniJora adenopoda won the selection race with Heliconiine butterflies? Science, 172: 585-586. GILBERT, L. E., 1975. Ecological consequences of a coevolved mutualism between butterflies and plants. In L. E. Gilbert & P. R. Raven (Eds), Coevolution of Animals and Plants: 210-240. Austin, Texas: University of Texas Press. GOEDEN, R. D. & LOUDA, S. M., 1976. Biotic interference with insects imported for weed control. Annual Review of Entomology, 21: 325-342. GOULD, S. J. & VRBA, E. S., 1982. Exaptation-a missing term in the science ofform. Paleobiology, 8: 4-15. GRANT, R. R., 1972. Interspecific competition among rodents. Annual Review of Ecology and Systematics, 3: 79- 106 GREEN, J., 1967. The distribution and variation of D . lumholzi (Crustacea, Cladocera) in relation to fish predation in Lake Albert, East Africa. Journal of <oology, 151: 181-197. GRINNELL, J., 1917. The niche-relationships of the California thrasher. Auk, 34: 427-433. GRUBB, T. C., Jr & GREENWALD, L., 1982. Sparrows and a brushpile: foraging responses to different combinations of predation risk and energy cost. Animal Behuviour, 3:637-640. HARPER, J. L., 1969. The role of predation in vegetation diversity. Brookhaven Symposia in Biology, 22: 48-61. HASSELL, M. P., 1978. 7 h e Dynamics of Arthropod Predator-prcy Systems. Princeton, New Jerscy: Princeton University Press. HASSELL, M. P. & SOUTHWOOD, T . R. E., 1978. Foraging strategies of insects. Annual Review of Ecology and Systematics, 9: 75-98. HEBERT, P. D. N. & LOARING, J. M., 1980. Selective predation and the species composition of arctic ponds. Canadian Journal of<oology, 58: 422-426. HEBERT, P. D. N., WARD, P. S. & HARMSON, R., 1974. Diffuse competition in Lepidoptera. Nature, London, 252: 389-391. HEINRICH, B., 1979. Foraging strategies of caterpillars. Oecologica, 42: 325-337. HOLMES, J. C. & BETHEL, W. M., 1972. Modification of intermediate host behaviour by parasites. In E. U. Canning & C. A. Wright (Eds), BehaVioural Aspects OJParasite Transmission. <oological journal of the Linnean Society, 51: 123- 149. HOLT, R. D., 1977. Predation, apparent competition and the structure of prey communities. Theoretical Population Biology, 12: 197-229. HOWE, H. F., 1979. Fear and frugivory. American Naturalist, 114: 925-931. HRBACEK, J., 1959. Density of the fish population as a factor influencing distribution and speciation in the genus Daphnia. Proceedings of XV Intmational Congress of <oologv. Section 10, Ecology: 794-795. (Brooks & Dodson, 1965 op. cit.). HUFFAKER, C. B., 1971. The phenomena of predation and its role in nature. in P. J. den Boer & G. R. Gradwell (Eds), Dynamics of Populations. Proceedings of the Advanced Studies Institute on the dynamics of numbers in populations, Wageningen. HULBERT, S. H., ZEDLER, J. & FAIRBANKS, D., 1972. Ecosystem alteration by mosquito fish (Gambusia ojinis) by predation. Science, 175: 639-641. HUTCHINSON, G . E., 1957. Concluding remarks. Cold Spring Harbour Symposia of Quontitatiuc Biology, 22: 415427. HUTCHINSON, G. E., 1978. An Introduction to Population Ecology. New Haven: Yale University Press. JAMES, H. G., 1967. Seasonal activity of mosquito predators in woodland pools in Ontaria. Mosquito News, 27: 453457. JANZEN, D. H., 1966. Coevolution of mutualism between ants and Acacias in Central America. Evolution, 20: 249-275. JANZEN, D. H., 1976. The depression of reptile biomass by large herbivores. Amrican Naturalist, 110: 371-400. JEFFRIES, M. J. & LAWTON, J. H., 1984. Predator-prey ratios in communities of freshwater invertebrates: the role of enemy free space. Freshwater Biology, 15: in press. ENEMY FREE SPACE 285 JOHNSON, D. M. & CROWLEY, P. H., 1980a. Odonate ‘hide and seek’: Habitat-specific rules? In W. C. Kerfoot (Ed.), American Society of Limnology and Oceanography. Evolution and Ecofogy of ,@plankton Communities. Special symposium, 3: 569-579. JOHNSON, D. M. & CROWLEY, P. H., 1980b. Habitat and seasonal segregation among coexisting d o n a t e larvae. Odonatologica, 9: 297-308. KARR, J. R., 1982. Avian extinctions on Barro Colorado Island, Panama: a reassessment. A m ‘ c a n Naturalist, 119: 220-239. KERFOOT, W. C., 1977. Competition cladoceran communities. The cost of evolving against copepod predation. Ecology, 58: 303-313. KERFOOT, W. C., 1982. A question of taste: crypsis and warning coloration in freshwater zooplankton communities. Ecology, 63: 538-554. KITCHELL, J. A,, BOGGS, C. H., KITCHELL, J. F. & RICE, J. A,, 1981. Prey selection by naticid gastropods: experimental tests and application to the fossil record. Paleobiology, 7: 533-552. KREBS, C. J., 1978. Ecology. The Expnimental Analysis of Distribution and Abundance. New York Harper and Row. KREBS, J. R. & DAVIES, N. B., (Eds), (1978). Behavioural Ecology. An Evolutionary Approach. Oxford: Blackwell Scientific. LACK, D., 1966. Population Studies of Birdr. Oxford: Clarendon Press. LAWTON, J. H., 1978. Host plant influences on insect diversity; the effects of space and time. In L. A. Mound & N. Waloff (Eds), Symposia of the Royal Entomological Society of London, 9: 105-125. LAWTON, J. H., 1984. Herbivore community organisation: general models and specific tests with phytophagous insects. In P. W. Price, C. N. Slobodchikoff & W. S. Gaud (Eds), A New Ecology: Novel Approaches to Interactive Systcmr: 329-352. New York: John Wiley & Sons. LAWTON, J. H. & STRONG, D. R., Jr, 1981. Community patterns and competition in folivorous insects. American Naturalist, 118: 3 17-338. LEUTHOLD, W., 1977. African Ungulates, a Comparative Review of their Ethology and Behamoural Ecology. Berlin: Springer-Verlag. LEVIN, B. R., CHAO, L. & STEWARDS, F. M., 1977. A complex community in a simple habitat; an experimental study with bacteria and phage. Ecology, 58: 369-378. LIVDAHL, T. P., 1979. Evolution of handling time. The functional response of a predator to the density of sympatric and allopatric strains of prey. Evolution, 33: 765-768. LOTKA, A. J., 1925. Elements of Physical Biology. Baltimore: Williams and Wilkins. LYNCH, M., 1979. Predation, competition and zooplankton community structure. An experimental study. Limnology and Oceanography, 24: 253-272. MACARTHUR, R. H., 1970. Species packing and competitive equilibrium for many species. Theoretical Population Biology, I : 1-11. MACARTHUR, R. H., 1972. Geographical Ecology. Patterns in the Distribution of Species. New York: Harper and Row. MACARTHUR, R. H. & LEVINS, R., 1967. The limiting similarity, convergence and divergence of coexisting species. American Naturalist, 101: 377-385. MAGUIRE, B., Jr, 1973. Niche response structure and the analytical potentials of its relationship to the habitat. American Naturalist, 107: 213-246. MAY, R. M., 1974. On the theory of niche overlap. Theoretical Populafion Biology, 5: 297-332. MAY, R. M., 1981. Theoretical Ecology; Principles and Applications. Oxford: Blackwell Scientific. MAY, R. M. & MACARTHUR, R. H., 1972. Niche overlap as a function of environmental variability. Proceedings of the National Academy of Sciences of the United States of America, 69: 1 109-1 113. McPHAIL, J. D., 1969. Predation and the evolution of a stickleback. Journal of the Fisheries Research Board of Canada, 26: 3183-3208. MENGE, B. A,, 1976. Organisation of the New England rocky intertidal community: role of predation, competition and environmental heterogenicity. Ecological Monograph, 45: 355-393. MITCHELL, R., 1971. Role of predators in the reversal of imbalance in microbial ecosystems. Nature, London, 230: 257-258. MOMENT, G. B., 1962. Reflexive selection; a possible answer to an old puzzle. Science, 136: 262-263. MOODIE, G. E. E., 1972. Predation, natural selection and adaptation in an unusual three spine stickleback. HerediQ, 28: 157-167. MORAN, J. C. & SOUTHWOOD, T. R. E., 1982. The guild composition of arthropod communities in trees. Journal of Animal Ecology, 51: 289-306. MORIN, P. J., 1981. Predatory salamanders reverse the outcome of competition among three species of anuran tadpoles. Science, 212: 1284-1286. NILSSON, S. G., 1979. Seed density, cover, predation and the distribution of birds in a beech wood in southern Sweden. Ibis, 121: 177-185. OPLER, P. A., 1981. Polymorphic mimicry of polistine wasps by a neotropical neuropteran. Biotropica, 13: 165-176. ORIANS, G . H. & SOLBRIG, 0. T. (Eds), 1977. Convergent Evolution in Warm Deserts. An Examination of Strategies and Pattents in Deserts of Argentina and the United States. London: Academic Press. OTTE, D. & JOERN, A., 1977. On feeding patterns in desert grasshoppers. The evolution of specialised diets. Proceedings of the Academy of Natural Sciences of Philadelphia, 128: 89-126. M. J. JEFFRIES AND J. H. LAWTON 286 PAINE, R. T., 1966. Food web complexity and species diversity. American Natura~ist,100: 65-75. ~a Prey patches, predator food preference and intertidal PAINE, R. T., 1969. The ~ i s a s l n - ~ e g u interaction; community structure. Ecology, 50: 950-961. PATTERSON, B. & PASCUAL, R., 1968. Evolution of mammals on Southern continents, 5. The fossil mammal fauna of South America. Quarterly Reuiew of Biology, 43: 409-451. PIANKA, E. R., 1978. Evolutionary Ecology. New York: Harper and Row. POLIS, G. A., 1980. Seasonal patterns and age-specific variation in the surface activity of a population of desert scorpions in relation to environmental factors. Journal of Animal Ecology, 49: 1-18. PORTER, K. G., 1973. Selective grazing and differential digestion of algae by zooplankton. Nature, London, 244: 179-180. PRICE, W. P., BOUTON, C. E., GROSS, P., McPHERON, B. A,, THOMPSON, J. N. & & WEIS, A. E., 1980. Interactions among three trophic levels. Influence of plants on interactions between herbivores. Annual Revicw of Ecologv and Systematics, 11: 41-65. RANDALL, J. E., 1965. Grazing effect on sea grass by herbivorous reef fishes in the West Indies. Ecology, 46: 255-260. RIEF, C. & TAPPA, D. W., 1966. Selective predation: Smelt and cladocerans in Harvey’s Lake. Limnology and Oceanography, 11: 437-438. RICKLEFS, R. E., & O R O U R K E , K., 1975. Aspect diversity on moths: A temperate-tropical comparison Evolution, 29: 3 13-324. ROOT, R. B., 1973. Organisation of a plant arthropod association in simple and diverse habitats; the fauna of Collards (Brassica oleracca). Ecological Monographs, 43: 95-1 24. SALT, G. W., 1967. Predation in an experimental protozoan population ( Woodru@a-Paramen’um). Ecological Monographs, 37: 113-144. SCHULTZ, J. C., OTTE, D. & ENDERS, F., 1977. Larrea as a habitat component for desert arthropods. In T . J. Mabry, J. H. Hunzickcr & D. R. Difeo (Eds), Creosote Bush: Biology and Chemistry of Larrea in New World Deserts: 176-208. Stroudsburg, Penn.: Dowden, Hutchinson and Ross. SIH, A,, 1981. Stability, prey density and age dependent interference in an aquatic insect predator, Notonecta hoffmni. j’ournd of Animal Ecology, 50: 625-636. SIH, A., 1982. Foraging strategies and the avoidance of predation by an aquatic insect, Notonecta hoffmni. ECO~OQ, 63: 786-796. SPRULES, W. G., 1972. Effects of size selective predations and food composition on high altitude zooplankton communities. Ecology, 53: 375-386. STEIN, R. A. & MAGNUSON, J. J., 1976. Behavioural response of crayfish to a fish predator. Ecology, 57: 751-761. STICH, H. B. & LAMPERT, W., 1981. Predator evasion as an explanation ofdiurnal vertical migration by zooplankton. Nature, London, 293: 396-398. STRONG, D. R., 1973. Amphipod amplexus. The significance of ecotypic variation. Ecology, 54: 1383-1388. STRONG, D. R., LAWTON, J. H. & SOUTHWOOD, T. R. E., 1984. Imectr on Plants. Cornmunip pattern and Mechanisms. Oxford: Blackwell Scientific. THOMPSON. 1. N.. 1982. Intnuction and Coevolution. New York: Wilev. THORNHILL, R., 1980. Competition and coexistence among Panorpa scorpionflies. Ecological Monographs, 50: 179-197. TUTTLE, M. P. & RYAN, M. J., 1981. Bat predation and the evolution of frog vocalisation in the Neotropics. Science, 214: 677-678. VANCE, R. R., 1979. Effects of grazing by the sea urchin Cmtrostephanus coronalus on prey community composition. Ecology, 60: 537-546. VARLEY, G. C., GRADWELL, G. R. & HASSELL, M. P., 1973. Insect Population Ecology. An Analytical Approach. Oxford: Blackwell Scientific. VERMEIJ, G. J., 1974. Marine fauna dominance and molluscan shell form. Evolution, 28: 656-664. VERMEIJ, G. J., 1982. Unsuccessful predation and evolution. American Naturalist, 120: 701-720. VERMEIJ, G. J. & COVICH, A. P., 1978. Coevolution of freshwater gastropods and their predators. American Naturalist, 112: 833-843. WHITTAKER, R. H., LEVIN, S. A. & ROOT, R. B., 1973. Niche, habitat and ecotype. American Naturalist, 107: 321-338. WILLIAMSON, M. H., 1957. An elementary theory of interspecific competition. NUtUre, London, 180: 422-425. ZARET, T. M., 1969. Predation-balanced polymorphism of Cniodaphnin cornuta Sars. Limnologv and Oceanography, 14: 301-302. ZARET, T . M., 1972. Predators, invisible prey and the nature of polymorphism in the Cladocera. Limnology and Oceunography, 17: 171-184. ZARET, T. M.,1980. Prcdcrlioion and Freshwater Communities. New Haven, London: Yale University Press. ZWOELFER, H., 1975. Speciation and niche diversification in phytophagous insects. Verhandlungm der Dcutschm zoologischm Gesellschaft, 67: 394401. I.,