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The structure of helminth communities
THE STRUCTURE
OF HELMINTH JOHN
COMMUNITIES
C. HOLMES
Department of Zoology University of Alberta Edmonton, Alberta T6G 2E9 Canada INTRODUCTION Two of the major questions of interest to community ecologists are 1) Do communities show predictable structure, i.e., patterns of species occurrence, relative abundances, and resource use? and, if SO 2) What processes produce the structure? Extensive debate on these two questions over the past decade led to the realization that communities vary greatly in the extent to which they are structured, and that this diversity is due to the differential importance of several distinct, but interacting, processes, necessitating a pluralistic view of community structure (Diamond & Case, 1986). Iti parasitology, debate has focussed on whether parasites regularly interact (or have interacted in the past) to produce a predictable community structure (Holmes, 1973) or, alternatively, whether structure is a fortuitous result of a random combination of independently-evolved species (Rohde, 1979; Price, 1980). As is so often the case in polarized debates, each side is correct for some of the communities. Holmes & Price (1986) recognized that both “interactive communities” (the first type) and “isolationist communities” (the second type) exist in nature, showed that each of these two types of community is predicted by a variety of concepts of community organization, and suggested that parasitologists should turn their attention to elucidating the conditions which lead to each of the two types of communities of parasites, and the conditions under which each of the concepts is applicable. They recognized that interactions should be important only when species regularly co-occur at substantial population densities. Those concepts which regard interactions as unimportant all assume features which prevent such co-occurrence (represented by the effective screens in Fig. IA), so that hosts are rarely exposed to parasites, and parasites are specialized so that few of them are able to establish. Concepts which regard interactions as important assume that these screens are relatively ineffective, as in Fig. 1B. A second development in community ecology is the recognition that structure may be more readily discerned by focussing on restricted groups of species. One way of restricting the species stems from the hypothesis that in any community there is a group of dominant species (“core species”) which determine the structure of that community (Hanski, 1982). A second way is to focus on guilds, groups of species that use the same set of resources in the same way (Root, 1967). In’either case, structure apparent within the restricted group may be less apparent in the community as a whole. A third development in community ecology is the recognition that ecological processes operate on different scales, that observations and analyses need to be made at the proper scale, and that processes operating on larger scales may determine what can happen on smaller scales (Dayton & Tegner, 1984). The habitats of parasites are inherently patchy, and at several different scales. The most fundamental scale is that of the host individual, with its singular genetic makeup and homeostatic control. Data are collected at this level, and all direct interactions between parasites (or between parasites and the host) take place at this level. Therefore, data should be analyzed for direct interactions at this level. However, the parasites available for possible interactions depend upon processes acting at scales at the level of the host population, and at the level of the host community. The next section will I) examine the structure of helminth communities at the level of the host individual (or infracommunities), using as an example data (from Bush & Holmes, 1986a, b) on infracommunities in lesser scaup, Aythya afiinis, 2) examine core-satellite and guild approaches, and 3) focus on evidences of interaction. The following section will examine how processes at the level of the host population and host community affect structure at the infracommunity level. The final section is a plea for greater communication with community ecologists. 203
J.C. Hulmes
204
INFRACOMMUNITIES
OF HELMINTHS
Animals belonging to the same host species provide the most similar replicates of habitat that a field ecologist is likely to encounter. Similarly, the helminths within those animals provide replicated infracommunities, allowing statistical examination of patterns. Evidence on interactions is generally sought by examining presence/absence data (for evidence of exclusion); data on intensity, growth, maturation, or fecundity (for effects on fitness); and location (for evidence of niche restriction or niche shifts). Which species should be examined for such evidence? Hanski (1982) suggested that species which occupy patchily-distributed habitats tend to be bimodal in frequency, with core species found, generally at high population densities, in a high proportion of the patches, and satellite species found, generally in low densities, in very few. Under those circumstances, interactions important to the community are likely to be limited to those between core species (although interactions with core species may be what restricts the frequency and density of the satellite species). The major difficulty in applying the core-satellite concept to communities of parasites appears to be in determining which are the core species. When the frequency distribution of species is strongly bimodal, selection of core species is unequivocal. However, many surveys contain species of intermediate frequency, making selection of core species arbitrary. An alternative method of selecting the important species in the community is the recurrent group analysis (Fager & McGowan, 1963), which identifies groups of species which regularly co-occur. In our experience, the recurrent group analysis usually selects a larger group of species than the core species analysis.
A
B
POOL OF POTENTIAL PARASITES
--- --i
li
REALIZED PARASITE COMMUNITY
POOL OF POTENTIAL PARASITES
INTERACTIONS
-
I
IX
IX
REALiZED PARASITE COMMUNITY
Fig. 1.
The relative influence of three types of screens on realized communities of parasites. A. Isolationist community: screens blocking exposure or establishment are effective; interactions are unimportant. B. Interactive community: screens blocking exposure and establishment
are ineffective; interactions are important.
Core (or recurrent group) species frequently show positive associations in presence/absence or intensity data. These positive associations can arise in a number of ways. First, they may be a function of similar exposure to parasites, as could occur through common seasonal or zoogeographic factors, or use of the same food chain. In scaup, one group (guild) of positively associated species used the amphipod ~~~lel~~ azteca as an intermediate host; a second group used another amphipod, Ganvnarus lacustris. Second, in scaup the numbers of almost all frequent species, including members of each guild, plus others, were positively correlated, suggesting that all of the species may be responding to some aspect of host quality (see also Barger, 1984). Third, positive associations may be due to mutuahstic interactions (e.g., Ewing, Ewing, Keener & Mulholland. 1982). These three possibiIities can be distinguished only with a thorough knowledge of the system. A second way of searching for interactions is to analyze data on measures of fitness (growth, maturation or fecundity), rarely used in community-level studies, but commonly used in population-level studies. Because of their potential to distinguish the type of competition (discussed below), those measures deserve more attention. A third way of searching for interactions is to analyze data on the location of helminths. Two types of
Community Structure
205
patterns have been looked for: dispersion within the available habitat (including the availability of “empty niches”), and shifts in location in the presence of other species. In scaup, core species were spread out along the length of the intestine, and a comparison with the broken-stick model of Bush & Holmes (1983) showed that this dispersion was significantly more uniform than expected. The degree of uniformity was significantly reduced when the satellite species were included in the analysis. The absorbers (cestodes and acanthocephalans) among the core and secondary species (those of intermediate frequency) in scaup could be divided into guilds consisting of small species (usually intimately associated with the mucosa) and the large species (which protruded into the central lumen). Each group of absorbers showed a significantly uniform distribution along the intestine. Although the existence of “empty niches” has been taken as evidence of isolationist communities (Holmes & Price, 1986; Price, this volume), interactions can still occur in low-diversity systems. If two species have similar optimal positions along the small intestine, they may compete for that position, regardless of the availability of other, unused positions. In such cases, niche shifts are likely to occur (see below). Empty niches were present even in the rich communities in scaup; most scaup lacked a small (or large) absorber in a part of the intestine. Given the other evidence for interactions in these communities, it is obvious that the presence of “empty niches” cannot be taken’as proof that interactions are unimportant. A marked change in the distribution of a parasite in the presence of a second species, as in the H. diminuta-M. dubius example (Holmes, 1961), can provide a second type of evidence of interaction between species. There are some examples of niche shifts from field systems (e.g., Riley & Owen, 1975; Hobbs, 1980), but in other systems, no such marked changes have been reported (e.g., Rohde, 1979). Unfortunately, most workers have followed the example of Holmes (1961) by looking for niche shifts in data summed across many infracommunites, rather than within infracommunities. In our experience, analysis of summed data can reveal only gross changes in distribution. In scaup there were no marked shifts, and the summed distributions of almost all species overlapped broadly. However, within birds, relatively minor distributional shifts led to relatively low average overlap values between adjacent species. Although there were significant correlations between species in density and each species showed significantly expanded distributions in high-density infrapopulations, adjacent species showed no significant increases in overlap values with increases in joint population sizes. Once again, patterns were clearer within guilds; overlap values for adjacent species within the two absorber guilds were considerably less than values for adjacent species between guilds. Whether competition leads to exclusion or to niche shifts may well depend on what the species are competing for, and the type of competition they use. Branch (1984) showed that, for marine organisms, competition for space, usually by interference, frequently resulted in exclusion, whereas competition for food, usually by exploitation, usually resulted in coexistence, sometimes with niche diversification. Branch emphasized that space is an absolute requirement, cannot be shared, and is renewed only slowly, if at all; in contrast, food is a relative requirement, can be shared, and is often renewed fairly quickly. It may be difficult to determine whether intestinal helminths, for which the kinds and amounts of food available are strongly correlated with location along the intestine, are competing for food or space. In addition, such helminths may well be using both types of competition simultaneously. For example, laboratory studies have shown that both H. diminuta and M. dubius compete for sugars by exploitation (Read, 1959; Crompton, Keymer, Singhvi & Nesheim, 1983; Keymer, Crompton & Singhvi, 1983). However, Roberts and co-workers (Zavras & Roberts, 1985 and references therein) have demonstrated that under crowded conditions, H. diminuta releases compounds that interfere with DNA synthesis in worms from uncrowded conditions, and have suggested that this interference plays a significant part in the crowding phenomenon. (Whether or not such interference mechanisms play any role in interspecific interactions has not been investigated, but the possibilities are obvious.) Other interference mechanisms, which have been shown to operate interspecifically, are modification of the environment in ways that interfere with other parasites (e.g., Fried & Gainsburg 1980), or stimulation of an immune response which interferes with another parasite (e.g., LeJambre, 1983). If Branch’s concepts apply to parasites, these kinds of interference may be more likely to result in exclusion, either completely, from the host individual, or partially, from a particular location in the host. Competition by the exploitation of renewable food sources may be likely to result in diversification of niches either spatially or along the food dimension. Parasitologists could benefit greatly from investigating these kinds of interactions in natural systems. Cooperative research along these lines with physiologists or immunologists would be rewarding. Interactions between parasites are not all competitive. The presence of one species of parasite may facilitate, rather than inhibit, a second species (e.g., Ewing ef al. 1982), either by altering the environment, or by modulating the host’s immune response in a favorable way (e.g., Jenkins & Behnke, 1977). Studies on community structure should consider the possibility of such interactions.
J.C. Holmes
206
LARGER
SCALE COMMUNITIES
The parasite communities in individual hosts are non-random samples of the parasites available in the environment they occupy, having been filtered by the screens in Fig. 1. What parasites are available depend on two larger-scale communities of parasites: the parasites in a host population, and the parasites in a host community. The basic relationships among these three levels of parasite communities are indicated in Fig. 2A. The community in the host population is dominated by the core species. In a complex parasite community, the full complement of core species is likely to occupy most, but not all, of the ecological niches available. For example, in scaup, although the usual distributions of the small absorbers occupied the entire length of the small intestine, those of the large absorbers occupied less than half of the length of the intestine. Most parasite species are successful in relatively few host species, and are often concentrated in only one of those few (Kontrimavichus & Atrashkevich, 1982; Freeland, 1983). Consequently, most of the core species are likely to be host specialists, possibly coevolved. In scaup, 6 of 8 core species were specialists; the core small absorbers all belonged to the guild using Hyalella as an intermediate host and all have specialized egg capsules adapted for transmission to that amphipod, suggesting that they have coevolved. The specialist large absorbers all belong to the guild using Gammarus as an intermediate host, and may also be coevolved. As is shown in Fig. 2A, an individual animal is likely to be exposed preferentially to these core specialists, so that most, if not all, are likely to be present. However, chance factors, individual diet specialization, or other factors may result in the absence (or low population levels) of one or more of the core species. These empty niches (and those not occupied by core species) may be filled by generalist parasites, or by other species normally part of the parasite communities in other host species, to which the individual becomes exposed. These become the satellite species.
Fig. 2. Contributions of parasite communities in the host population and in the host community to parasite infracommunities. A. The basic system. B. Dominant host species (or depauperate host community). C. Rare host species (or one with few or no core species).
This basic pattern may be modified if the food habits, habitat selection, or general behavior of the host are such as to act as screens (as in Fig. 1) which restrict the kinds of parasites to which it may be exposed, or those which can become established. Under such circumstances, the number of core specialists would be low, and so would the number to which individual hosts would be exposed (as in Fig. 2C). For example, Kennedy (1981) and Price & Clancy (1983) have suggested that there are fundamental differences between parasite communities in fish and those in birds, with the former relatively depauperate, with interactions relatively uncommon and unimportant, and the latter richer, with interactions more common and more important. Kennedy, Bush & Aho (1986) have identified four factors that they believe lead to systematic differences between communities in freshwater fish and those in birds or mammals in diversity, average
Community SIructure
207
numbers of parasites, and interactions. Three of those factors, host vagility, the breadth of the diet, and the energy demands of homeothermy, lead to systematic differences in exposure. The fourth, the greater complexity of the avian gut, leads to possible differences in niche diversification. The contribution of parasites from the host community may be limited (as in Fig. 2B) if that community is poor in species, or has few parasites (through screens acting on the other host species). Both appear to be the case for several of the freshwater fish hosts analyzed by Kennedy et al. (1986). The basic pattern in Fig. 2A may also be modified if the populations of the host and those of its ecological associates are disparate (Fig. 2B, C). Individuals of the abundant host species are likely to be extensively exposed to their own core parasites, leaving few empty niches, so that satellite species may be limited to isolated individuals (Fig. 2B). lndividuals of the rare host species are likely to be sparsely exposed to their own core parasites, but more frequently exposed to the core parasites of the abundant host (Fig. 2C). Parasite communities in the rare host species may thereby become impoverished, and dominated by the parasites of the abundant host species, as, for example, in the freshwater fishes in Cold Lake. Alberta (Leong & Holmes, 1981). A more graphic example is that of the parasites of avocets (Recurvirostra americana); in the sloughs of Manitoba, they have a characteristic parasite fauna of their own, whereas at Cowoki Lake, Alberta (which has a very large population of scaup), their parasite fauna is essentially that of scaup (A.O. Bush, pers. comm.). The last example is evidence of the dynamic nature of parasite communities and of how ecological factors may be able to override evolutionary factors such as host specialization. A PLEA FOR COMMUNICATION The study of communities of parasites has much to offer to community ecology in general, for reasons ably stated by Price (1980). That fact is beginning to be recognized by general ecologists, as is evident from the inclusion of chapters on parasites in most of the recent books on community ecology (Futuyma & Slatkin, 1983; Price, Slobodchikoff & Gaud, 1984; Strong, Simberlof, Abele & Thistle, 1984; Anderson & Kikkawa, 1986; and Diamond & Case, 1986). However, most of these chapters have been written by persons trained as ecologists, many of whom have little experience with the organisms usually dealt with by parasitologists. Perhaps as a result, almost all of these chapters contain generalizations that many parasitologists cannot agree with. It is our duty to try to get our ideas, and our disagreements with the ideas of others, into the ecological literature. We can only do so if we speak the same language as ecologists, are familiar with the same concepts, and use methods, particularly analytic methods, which are familiar and well understood. In return, the concepts and methods used by community ecologists studying other kinds of organisms are relevant to communities of parasites (as I have tried to show in this paper), and parasitologists interested in the ecology of the animals they study should be aware of developments in general ecology. SUMMARY The existence of both interactive and isolationist communities of helminths, each of which may be produced by any one of several processes, necessitates a pluralistic view of helminth community structure. A scheme involving three hierarchical scales of communities of helminths is proposed. Interactions between species occur in infracommunities, and should be looked for there. Interactions are often clearer in smaller groups of species, either among core species or within guilds. Infracommunities are samples of helminth communities at two larger scales: the helminth community in the host population provides core species, largely specialists, and that in the host community provides the generalists and the satellite species. The richness of each of the two large-scale communities is affected by various ecological, historical and evolutionary factors. The different concepts which have been applied to parasite communities are based on these factors. Acknowledgements-I thank numerous colleagues, especially John Addicott, Al Bush, Clive Kennedy, Peter Price, Bill Samuel and Mike Stock, for the discussions which have led to these ideas. I thank John Addicott and Mike Stock for comments on earlier drafts, Mike Stock for making the figures, and Al Bush for permission to use his unpublished results. Supported by N.S.E.R.C. Canada grant A1464.
J.C. Holmes
208
REFERENCES ANDERSON D.J. & KIKKAWA J. (Editors) 1986. Community Ecology: Pattern and Process. Blackwell Scientific Publications, Oxford. In press. BARGERI.A. 1984. Correlations between numbers of enteric nematode parasites in grazing lambs. International Journal for Parasitology 14: 587-589.
BRANCHG.M. 1984. Competition between marine organisms: ecological and evolutionary implications. Oceanography and Marine Biology, Annual Review 22: 429-593.
BUSH A.O. & HOLMES J.C. 1983. Niche separation and the broken-stick American
model: use with multiple assemblages.
Tile
Naturalist 122: 849-855.
BUSH A.O. & HOLMES J.C. 1986a. Intestinal helminths of lesser scaup ducks: patterns of association. Canadian Journal of Zoology. In press. BUSH A.O. & HOLMESJ.C. 1986b. Intestinal helminths of lesser scaup ducks: an interactive community. Canadian Journal of Zoology. In press. CROMPTOND.W.T.. KEYMER A.E.. SINGHVI A. & NESHEIM M.C. 1983. Rat dietarv fructose and the intestinal distribution and growth of Moniliformis (Acanthocephala). Parasitology 86: 57-71. DAYTON P.K. & TEGNER M.J. 1954. The importance of scale in community ecology: a kelp forest example with terrestrial analogs. In: A New Ecology: Novel Approaches to Interactive Systems pp 457481 (Edited by Price P. W., Slobodchikoff C.N. & Gaud W.S.) John Wiley & Sons, New York. DIAMONDJ. & CASE T.J. (Editors) 1986. Community Ecology. Harper & Row, New York. EWING M.S., EWING S.A., KEENER M.S. & MULHOLLANDR.J. 1982. Mutualism among parasitic nematodes: a population model. Ecological Modelling 15: 353-366. FAGER E.W. & MCGOWANJ.A. 1963. Zooplankton species groups in the North Pacific. Science 140: 453-460. FREELANDW.J. 1983. Parasites and the coexistence of host animal species. The American Naturalist 121: 223-288. FRIED B. & GAINSBURGD.M. 1980. Concurrent infections of cecal trematodes, Zygocotyle Iunata and Norocotylus sp., in the domestic chick and observations on host-parasite relationships of Notocotylus sp. Journal of Parasitology 66: 502-505.
FUTUYMAD.J. & SLATKINM. (Editors) 1983. Coevolution. Sinauer Associates, Sunderland, Massachusetts. HANSKI I. 1982. Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38: 210-221, HOBBS R.P. 1980. Interspecific interactions among gastrointestinal helminths in pikas of North America. American Midland Naturalist 103: 15-25.
HOLMES J.C. 1961. Effects of concurrent infections on Hymenopepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). I. General effects and comparison with crowding. Journal of Parasitology 47: 209-216. HOLMESJ.C. 1973. Site selection by parasitic helminths: interspecific interactions, site segregation, and their importance to the development of helminth communities. Canadian Journal of Zoology 51: 333-347. HOLMESJ.C. & PRICE P.W. 1986. Communities of parasites. In: Community Ecology: Pattern and Process. (Edited by Anderson D.J. and Kikkawa J.) Blackwell Scientific Publications, Oxford. In press. JENKINS S.N. & BEHNKEJ.M. 1977. Impairment of primary expulsion of Trichuris muris in mice concurrently infected with Nematospiroides dubius. Parasitology 75: 71-78. KENNEDYC.R. 1981. Parasitocoenoses dynamics in freshwater ecosystems in Britain. Trudy Zoologicheskogo lnsfituta Akademia Nauk USSR 108: 9-22. (in Russian) KENNEDY C.R., BUSH A.O. & AHO J.M. 1986. Patterns in helminth communities: why are birds and fish different? Parasitology. In press. KEYMER A.E., CROMPTOND.W.T. SINGHVI A. 1983. Mannose and the “crowding effect” of Hymenolepis in rats. International Journal for Parasitology 13: 561-570.
KONTRIMAVICHUSV.L. & ATRASHKEVICHG.I. 1982. Parasitic systems and their role in the population biology of helminths. Parazytologica 16: 177-187. (in Russian) LEJAMBREL.F. 1983. Pre-mating barriers to species hybridization in Haemonchus. International Journal for Parasitology 13: 365-370.
LEONG T.S. & HOLMES J.C. 1981. Communities of metazoan parasites in open water fishes of Cold Lake, Alberta. Journal of Fish Biology 18: 693-713. PRICE P.W. 1980. Evolutionary Biology of Parasites.Princeton University Press, Princeton, New Jersey. PRICE P.W. & CLANCY K.M. 1983. Patterns in number of helminth parasite species in freshwater fishes. Journal of Parasitology 69: 449454.
PRICE P.W.. SLOBODCHIKOFFC.N. & GAUD W.S. (Editors) 1984. A New Ecology: Novel Approaches to Interactive Systems. Wiley, New York. READ C.P. 19.59. The role of carbohydrates in the biology of cestodes. VIII. Some conclusions and hypotheses. Experimental
RILEY J. &
Parasitology 8: 365-382.
OWEN
R.W. 1975. Competition between two closely related Tetrabothrius cestodes of the fulmar (Fulmaris
glacialis L.). Zeitschrift fur Parasitenkunde
46: 221-228.
ROHDE K. 1979. A critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. The American
Naturalist 114: 648-671.
blue-green gnatcatcher. Ecological Monographs 37: 317-350. & THISTLE A.B. (Editors) 1984. Ecological Communities: Conceptual Issues and the Evidence. Princeton University Press, Princeton. ZAVRAS E.T. & ROBERTSL.S. 1985. Developmental physiology of cestodes: cyclic nucleotides and the identity of putative crowding factors in Hymenolepis diminuta. Journal of Parasitology 71: 96-105.
ROOT R.B. 1967. The niche exploitation of the STRONG D.R., SIMBERLOFFD., ABELE L.C.
OF HELMINTH JOHN
COMMUNITIES
C. HOLMES
Department of Zoology University of Alberta Edmonton, Alberta T6G 2E9 Canada INTRODUCTION Two of the major questions of interest to community ecologists are 1) Do communities show predictable structure, i.e., patterns of species occurrence, relative abundances, and resource use? and, if SO 2) What processes produce the structure? Extensive debate on these two questions over the past decade led to the realization that communities vary greatly in the extent to which they are structured, and that this diversity is due to the differential importance of several distinct, but interacting, processes, necessitating a pluralistic view of community structure (Diamond & Case, 1986). Iti parasitology, debate has focussed on whether parasites regularly interact (or have interacted in the past) to produce a predictable community structure (Holmes, 1973) or, alternatively, whether structure is a fortuitous result of a random combination of independently-evolved species (Rohde, 1979; Price, 1980). As is so often the case in polarized debates, each side is correct for some of the communities. Holmes & Price (1986) recognized that both “interactive communities” (the first type) and “isolationist communities” (the second type) exist in nature, showed that each of these two types of community is predicted by a variety of concepts of community organization, and suggested that parasitologists should turn their attention to elucidating the conditions which lead to each of the two types of communities of parasites, and the conditions under which each of the concepts is applicable. They recognized that interactions should be important only when species regularly co-occur at substantial population densities. Those concepts which regard interactions as unimportant all assume features which prevent such co-occurrence (represented by the effective screens in Fig. IA), so that hosts are rarely exposed to parasites, and parasites are specialized so that few of them are able to establish. Concepts which regard interactions as important assume that these screens are relatively ineffective, as in Fig. 1B. A second development in community ecology is the recognition that structure may be more readily discerned by focussing on restricted groups of species. One way of restricting the species stems from the hypothesis that in any community there is a group of dominant species (“core species”) which determine the structure of that community (Hanski, 1982). A second way is to focus on guilds, groups of species that use the same set of resources in the same way (Root, 1967). In’either case, structure apparent within the restricted group may be less apparent in the community as a whole. A third development in community ecology is the recognition that ecological processes operate on different scales, that observations and analyses need to be made at the proper scale, and that processes operating on larger scales may determine what can happen on smaller scales (Dayton & Tegner, 1984). The habitats of parasites are inherently patchy, and at several different scales. The most fundamental scale is that of the host individual, with its singular genetic makeup and homeostatic control. Data are collected at this level, and all direct interactions between parasites (or between parasites and the host) take place at this level. Therefore, data should be analyzed for direct interactions at this level. However, the parasites available for possible interactions depend upon processes acting at scales at the level of the host population, and at the level of the host community. The next section will I) examine the structure of helminth communities at the level of the host individual (or infracommunities), using as an example data (from Bush & Holmes, 1986a, b) on infracommunities in lesser scaup, Aythya afiinis, 2) examine core-satellite and guild approaches, and 3) focus on evidences of interaction. The following section will examine how processes at the level of the host population and host community affect structure at the infracommunity level. The final section is a plea for greater communication with community ecologists. 203
J.C. Hulmes
204
INFRACOMMUNITIES
OF HELMINTHS
Animals belonging to the same host species provide the most similar replicates of habitat that a field ecologist is likely to encounter. Similarly, the helminths within those animals provide replicated infracommunities, allowing statistical examination of patterns. Evidence on interactions is generally sought by examining presence/absence data (for evidence of exclusion); data on intensity, growth, maturation, or fecundity (for effects on fitness); and location (for evidence of niche restriction or niche shifts). Which species should be examined for such evidence? Hanski (1982) suggested that species which occupy patchily-distributed habitats tend to be bimodal in frequency, with core species found, generally at high population densities, in a high proportion of the patches, and satellite species found, generally in low densities, in very few. Under those circumstances, interactions important to the community are likely to be limited to those between core species (although interactions with core species may be what restricts the frequency and density of the satellite species). The major difficulty in applying the core-satellite concept to communities of parasites appears to be in determining which are the core species. When the frequency distribution of species is strongly bimodal, selection of core species is unequivocal. However, many surveys contain species of intermediate frequency, making selection of core species arbitrary. An alternative method of selecting the important species in the community is the recurrent group analysis (Fager & McGowan, 1963), which identifies groups of species which regularly co-occur. In our experience, the recurrent group analysis usually selects a larger group of species than the core species analysis.
A
B
POOL OF POTENTIAL PARASITES
--- --i
li
REALIZED PARASITE COMMUNITY
POOL OF POTENTIAL PARASITES
INTERACTIONS
-
I
IX
IX
REALiZED PARASITE COMMUNITY
Fig. 1.
The relative influence of three types of screens on realized communities of parasites. A. Isolationist community: screens blocking exposure or establishment are effective; interactions are unimportant. B. Interactive community: screens blocking exposure and establishment
are ineffective; interactions are important.
Core (or recurrent group) species frequently show positive associations in presence/absence or intensity data. These positive associations can arise in a number of ways. First, they may be a function of similar exposure to parasites, as could occur through common seasonal or zoogeographic factors, or use of the same food chain. In scaup, one group (guild) of positively associated species used the amphipod ~~~lel~~ azteca as an intermediate host; a second group used another amphipod, Ganvnarus lacustris. Second, in scaup the numbers of almost all frequent species, including members of each guild, plus others, were positively correlated, suggesting that all of the species may be responding to some aspect of host quality (see also Barger, 1984). Third, positive associations may be due to mutuahstic interactions (e.g., Ewing, Ewing, Keener & Mulholland. 1982). These three possibiIities can be distinguished only with a thorough knowledge of the system. A second way of searching for interactions is to analyze data on measures of fitness (growth, maturation or fecundity), rarely used in community-level studies, but commonly used in population-level studies. Because of their potential to distinguish the type of competition (discussed below), those measures deserve more attention. A third way of searching for interactions is to analyze data on the location of helminths. Two types of
Community Structure
205
patterns have been looked for: dispersion within the available habitat (including the availability of “empty niches”), and shifts in location in the presence of other species. In scaup, core species were spread out along the length of the intestine, and a comparison with the broken-stick model of Bush & Holmes (1983) showed that this dispersion was significantly more uniform than expected. The degree of uniformity was significantly reduced when the satellite species were included in the analysis. The absorbers (cestodes and acanthocephalans) among the core and secondary species (those of intermediate frequency) in scaup could be divided into guilds consisting of small species (usually intimately associated with the mucosa) and the large species (which protruded into the central lumen). Each group of absorbers showed a significantly uniform distribution along the intestine. Although the existence of “empty niches” has been taken as evidence of isolationist communities (Holmes & Price, 1986; Price, this volume), interactions can still occur in low-diversity systems. If two species have similar optimal positions along the small intestine, they may compete for that position, regardless of the availability of other, unused positions. In such cases, niche shifts are likely to occur (see below). Empty niches were present even in the rich communities in scaup; most scaup lacked a small (or large) absorber in a part of the intestine. Given the other evidence for interactions in these communities, it is obvious that the presence of “empty niches” cannot be taken’as proof that interactions are unimportant. A marked change in the distribution of a parasite in the presence of a second species, as in the H. diminuta-M. dubius example (Holmes, 1961), can provide a second type of evidence of interaction between species. There are some examples of niche shifts from field systems (e.g., Riley & Owen, 1975; Hobbs, 1980), but in other systems, no such marked changes have been reported (e.g., Rohde, 1979). Unfortunately, most workers have followed the example of Holmes (1961) by looking for niche shifts in data summed across many infracommunites, rather than within infracommunities. In our experience, analysis of summed data can reveal only gross changes in distribution. In scaup there were no marked shifts, and the summed distributions of almost all species overlapped broadly. However, within birds, relatively minor distributional shifts led to relatively low average overlap values between adjacent species. Although there were significant correlations between species in density and each species showed significantly expanded distributions in high-density infrapopulations, adjacent species showed no significant increases in overlap values with increases in joint population sizes. Once again, patterns were clearer within guilds; overlap values for adjacent species within the two absorber guilds were considerably less than values for adjacent species between guilds. Whether competition leads to exclusion or to niche shifts may well depend on what the species are competing for, and the type of competition they use. Branch (1984) showed that, for marine organisms, competition for space, usually by interference, frequently resulted in exclusion, whereas competition for food, usually by exploitation, usually resulted in coexistence, sometimes with niche diversification. Branch emphasized that space is an absolute requirement, cannot be shared, and is renewed only slowly, if at all; in contrast, food is a relative requirement, can be shared, and is often renewed fairly quickly. It may be difficult to determine whether intestinal helminths, for which the kinds and amounts of food available are strongly correlated with location along the intestine, are competing for food or space. In addition, such helminths may well be using both types of competition simultaneously. For example, laboratory studies have shown that both H. diminuta and M. dubius compete for sugars by exploitation (Read, 1959; Crompton, Keymer, Singhvi & Nesheim, 1983; Keymer, Crompton & Singhvi, 1983). However, Roberts and co-workers (Zavras & Roberts, 1985 and references therein) have demonstrated that under crowded conditions, H. diminuta releases compounds that interfere with DNA synthesis in worms from uncrowded conditions, and have suggested that this interference plays a significant part in the crowding phenomenon. (Whether or not such interference mechanisms play any role in interspecific interactions has not been investigated, but the possibilities are obvious.) Other interference mechanisms, which have been shown to operate interspecifically, are modification of the environment in ways that interfere with other parasites (e.g., Fried & Gainsburg 1980), or stimulation of an immune response which interferes with another parasite (e.g., LeJambre, 1983). If Branch’s concepts apply to parasites, these kinds of interference may be more likely to result in exclusion, either completely, from the host individual, or partially, from a particular location in the host. Competition by the exploitation of renewable food sources may be likely to result in diversification of niches either spatially or along the food dimension. Parasitologists could benefit greatly from investigating these kinds of interactions in natural systems. Cooperative research along these lines with physiologists or immunologists would be rewarding. Interactions between parasites are not all competitive. The presence of one species of parasite may facilitate, rather than inhibit, a second species (e.g., Ewing ef al. 1982), either by altering the environment, or by modulating the host’s immune response in a favorable way (e.g., Jenkins & Behnke, 1977). Studies on community structure should consider the possibility of such interactions.
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LARGER
SCALE COMMUNITIES
The parasite communities in individual hosts are non-random samples of the parasites available in the environment they occupy, having been filtered by the screens in Fig. 1. What parasites are available depend on two larger-scale communities of parasites: the parasites in a host population, and the parasites in a host community. The basic relationships among these three levels of parasite communities are indicated in Fig. 2A. The community in the host population is dominated by the core species. In a complex parasite community, the full complement of core species is likely to occupy most, but not all, of the ecological niches available. For example, in scaup, although the usual distributions of the small absorbers occupied the entire length of the small intestine, those of the large absorbers occupied less than half of the length of the intestine. Most parasite species are successful in relatively few host species, and are often concentrated in only one of those few (Kontrimavichus & Atrashkevich, 1982; Freeland, 1983). Consequently, most of the core species are likely to be host specialists, possibly coevolved. In scaup, 6 of 8 core species were specialists; the core small absorbers all belonged to the guild using Hyalella as an intermediate host and all have specialized egg capsules adapted for transmission to that amphipod, suggesting that they have coevolved. The specialist large absorbers all belong to the guild using Gammarus as an intermediate host, and may also be coevolved. As is shown in Fig. 2A, an individual animal is likely to be exposed preferentially to these core specialists, so that most, if not all, are likely to be present. However, chance factors, individual diet specialization, or other factors may result in the absence (or low population levels) of one or more of the core species. These empty niches (and those not occupied by core species) may be filled by generalist parasites, or by other species normally part of the parasite communities in other host species, to which the individual becomes exposed. These become the satellite species.
Fig. 2. Contributions of parasite communities in the host population and in the host community to parasite infracommunities. A. The basic system. B. Dominant host species (or depauperate host community). C. Rare host species (or one with few or no core species).
This basic pattern may be modified if the food habits, habitat selection, or general behavior of the host are such as to act as screens (as in Fig. 1) which restrict the kinds of parasites to which it may be exposed, or those which can become established. Under such circumstances, the number of core specialists would be low, and so would the number to which individual hosts would be exposed (as in Fig. 2C). For example, Kennedy (1981) and Price & Clancy (1983) have suggested that there are fundamental differences between parasite communities in fish and those in birds, with the former relatively depauperate, with interactions relatively uncommon and unimportant, and the latter richer, with interactions more common and more important. Kennedy, Bush & Aho (1986) have identified four factors that they believe lead to systematic differences between communities in freshwater fish and those in birds or mammals in diversity, average
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numbers of parasites, and interactions. Three of those factors, host vagility, the breadth of the diet, and the energy demands of homeothermy, lead to systematic differences in exposure. The fourth, the greater complexity of the avian gut, leads to possible differences in niche diversification. The contribution of parasites from the host community may be limited (as in Fig. 2B) if that community is poor in species, or has few parasites (through screens acting on the other host species). Both appear to be the case for several of the freshwater fish hosts analyzed by Kennedy et al. (1986). The basic pattern in Fig. 2A may also be modified if the populations of the host and those of its ecological associates are disparate (Fig. 2B, C). Individuals of the abundant host species are likely to be extensively exposed to their own core parasites, leaving few empty niches, so that satellite species may be limited to isolated individuals (Fig. 2B). lndividuals of the rare host species are likely to be sparsely exposed to their own core parasites, but more frequently exposed to the core parasites of the abundant host (Fig. 2C). Parasite communities in the rare host species may thereby become impoverished, and dominated by the parasites of the abundant host species, as, for example, in the freshwater fishes in Cold Lake. Alberta (Leong & Holmes, 1981). A more graphic example is that of the parasites of avocets (Recurvirostra americana); in the sloughs of Manitoba, they have a characteristic parasite fauna of their own, whereas at Cowoki Lake, Alberta (which has a very large population of scaup), their parasite fauna is essentially that of scaup (A.O. Bush, pers. comm.). The last example is evidence of the dynamic nature of parasite communities and of how ecological factors may be able to override evolutionary factors such as host specialization. A PLEA FOR COMMUNICATION The study of communities of parasites has much to offer to community ecology in general, for reasons ably stated by Price (1980). That fact is beginning to be recognized by general ecologists, as is evident from the inclusion of chapters on parasites in most of the recent books on community ecology (Futuyma & Slatkin, 1983; Price, Slobodchikoff & Gaud, 1984; Strong, Simberlof, Abele & Thistle, 1984; Anderson & Kikkawa, 1986; and Diamond & Case, 1986). However, most of these chapters have been written by persons trained as ecologists, many of whom have little experience with the organisms usually dealt with by parasitologists. Perhaps as a result, almost all of these chapters contain generalizations that many parasitologists cannot agree with. It is our duty to try to get our ideas, and our disagreements with the ideas of others, into the ecological literature. We can only do so if we speak the same language as ecologists, are familiar with the same concepts, and use methods, particularly analytic methods, which are familiar and well understood. In return, the concepts and methods used by community ecologists studying other kinds of organisms are relevant to communities of parasites (as I have tried to show in this paper), and parasitologists interested in the ecology of the animals they study should be aware of developments in general ecology. SUMMARY The existence of both interactive and isolationist communities of helminths, each of which may be produced by any one of several processes, necessitates a pluralistic view of helminth community structure. A scheme involving three hierarchical scales of communities of helminths is proposed. Interactions between species occur in infracommunities, and should be looked for there. Interactions are often clearer in smaller groups of species, either among core species or within guilds. Infracommunities are samples of helminth communities at two larger scales: the helminth community in the host population provides core species, largely specialists, and that in the host community provides the generalists and the satellite species. The richness of each of the two large-scale communities is affected by various ecological, historical and evolutionary factors. The different concepts which have been applied to parasite communities are based on these factors. Acknowledgements-I thank numerous colleagues, especially John Addicott, Al Bush, Clive Kennedy, Peter Price, Bill Samuel and Mike Stock, for the discussions which have led to these ideas. I thank John Addicott and Mike Stock for comments on earlier drafts, Mike Stock for making the figures, and Al Bush for permission to use his unpublished results. Supported by N.S.E.R.C. Canada grant A1464.
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