Revista Chilena de Historia Natural 60: 159-179, 1987 Some roles of parasitic helminths in trophic interactions. A view from North America

Algunos papeles de los hehnintos panisitos en interacciones tr6ficas. Una vision desde Norteamerica

JANICE MOORE

Department of Zoology, Colorado State University, Fort Collins, Colorado 80523, USA

ABSTRACT

Parasites are seen as organisms that share physiological mechanisms with other species on a dynamic continuum of interactions with hosts, from detrimental to beneficial, that are not easily specified. Trophic and trophically mediated interactions between parasites and between parasites and their hosts are emphasized, especially recent North Amer- ican literature dealing with helminths. Parasite-host interactions include the following: 1) behavioral alterations of parasitized hosts - some examples, and evolutionary and ecological considerations; 2) effects on host distribution and abundance - via reproductive effects or the mediation of interactions with other free-living species; 3) environmental influences - biotic and abiotic - on parasites; 4) parasitic castration; 5) population effects - host and parasite pop­ ulation regulation, transmission and host diet, hosts as selective influences on parasites; and 6) coevolution - sexual selection, the evolution of pathogenicity, and phylogenetic studies of host-parasite evolution. Consideration of para- site-parasite interactions at the infrapopulation level includes the study of density-dependent effects, mate location and physiochemical influences. At the level of parasite communities within a host species, a variety of hypotheses that may account for structure are reviewed. Key words: Helminths, host-parasite interactions, parasite-parasite interactions, North America.

RESUMEN

Se considera a los panisitos como organismos que comparten mecanismos fisiol6gicos con otras especies en un con- tinuo dimimico de interacciones con huespedes, desde perjudicial a beneficiosas, las cuales son diffciles de especificar. Se enfatizan las interacciones tr6ficas, o mediadas tr6ficamente, entre parasitos y entre parasitos y sus huespedes; en particular aquellas interacciones documentadas sobre helmintos en Ia literatura reciente. Se examinan las siguientes interacciones panisito-huesped: 1) Alteraciones conductuales de los huespedes parasitados; con algunos ejemplos y consideraciones evolutivas y ecol6gicas. 2) Efectos sobre Ia distribuci6n y abundancia de los huespedes; vfa efectos reproductivos o mediaci6n de interacciones con otros organismos de vida libre. 3) Influencias ambientales, bi6ticas y abi6ticas, sobre los parasitos. 4) Castraci6n parasitaria. 5) Efectos poblaciones; regulaci6n poblacional de parasitos y huespedes, transmisi6n y dieta del huesped, huespedes como influencias selectivas sobre los parasitos. 6) Coevoluci6n; selecci6n sexual, evoluci6n de Ia patogenicidad y estudios filogenéticos de Ia evoluci6n parasito-huesped. Se consideran las interacciones parasito-parasito al nivel infrapoblacional, incluyendo efectos denso-dependientes, localizaci6n de pareja e influencias fisicoqufmicas. AI nivel de las comunidades de parasitos dentro de especies huespedes, se revisa una variedad de hip6tesis que pueden explicar su estructura. Palabras claves: Helmintos, interacciones huesped-parasito, interacciones parasito-parasito, Norteamerica.

INTRODUCTION Ecologists (e.g., Odum 1971, Ander- son & May 1978) usually view parasites as Parasites are generally thought to be detrimental to their hosts. Some of the organisms that live in close association organisms discussed in this paper have yet with larger hosts, frequently exhibiting to reveal their detrimental effects to a metabolic dependency on that host. inquiring scientists, however. The nature Occasionally, arguments have surfaced of their associations with hosts may change about how close the association must during host ontogeny. Even "harmful" be to be considered , or how parasites may have beneficial influences broadly the dependency can be charac- on their hosts. The definitions are not that terized. But the definition is basically realistic, and Van Beneden ( 18 7 6: 1) knew satisfying; it allows us to think we know this when he wrote, " ... the precise limit what a parasite is. at which commensalism begins is not (Received 25 October 1986. Accepted 1 July 1987) 160 MOORE

always easily to be ascertained". (See important, although I include some other also Price et al. 1986). Read (1970:3) areas of parasite ecology that are currently argued for a study of symbiology, i.e., developing in North America. I focus on , which he defined as " ... the the recent (6-8 yr) literature, especially sharing of physiological mechanisms by that pertaining to helminths. Other different species, without specifying the literature is included in a more eclectic relative benefits derived or outcome of fashion. Although the two areas can hardly the association". He argued that many be separated, I approach the material associations that we classify as "parasitism" first from the perspective of parasite-host or "mutualism" do not readily fit these interactions, and then from that of parasite definitions, and the extent to which community interactions. In the former they do may depend on circumstances. instance, I review literature pertaining to Finally, he (Read 1970:8) observed that behavioral alterations involved in parasite "Many of them [symbiotes] produce little transmission, parasite effects on host or no disease; but as will become apparent, distribution, reproduction, and population, the status quo is an illusory concept in coevolution, and environmental influences symbiosis." on parasites. Under parasite community The notion of symbiology has yet to interactions, I consider factors influencing catch on in the undergraduate curricula parasites at the infrapopulation (individuals of most North American universities. The of one parasite species within a single organisms I will discuss here are some host; Esch et al. 1975), infracommunity of the subjects of parasitology courses, (populations of all parasite species within and are commonly called parasites. Please a single host; Holmes & Price 1986) and remember that in some cases, such des- component community (all infracom- ignation is more a matter of convenience munities in a population of hosts; Holmes & than an accurate description of the asso- Price 1986) levels. [See Holmes & Price ciation. They are all, however, symbiotes. (1986) for discussion of compound com- Parasites are relevant to trophic inter- munities - all parasite populations in an actions in a variety of ways. They them- ecosystem.] selves have long been considered a trophic This is an admittedly broad view that, level, but as such, they are surprisingly it might be argued, goes beyond the topic disparate, ranging from facultative predators of trophic interactions. I maintain that on other parasites (Lie et al. 1965, Lie to the extent parasites influence the con- 1966), to "absorbers" (Bush & Holmes tours of host distribution and abundance, 1986b ). Many of them are transmitted sometimes being transmitted by those through food chains, sometimes by in- same hosts, their ecology in its broadest creasing a predator's encounters with prey, sense directly affects trophic interactions at and they are also known to affect the a variety of levels. feeding behavior of their hosts. Their ubiquity is equalled by their inconspic- PARASITE-HOST INTERACTIONS uousness in many instances, and we do not know how many reports of gastropod Behavioral Alterations biomass are really largely reports of the trematode biomass they may contain The emphasis of this workshop is on trophic (Duszynski, pers. comm.). interactions, and perhaps the most unusual The ecology of symbiotes has been way that parasites influence trophic inter- the subject of a fascinating book (Price actions is by affecting the availability of 1980), and I approach the topic from a their prey-item/intermediate hosts (hosts more restricted perspective. As indicated that harbor a juvenile parasite that must by the subject material of this conference, be eaten in order to reach adulthood in I have limited most of the review to the predator/final host). In so doing, they research activity by North Americans. may enhance their own probability of The excellent work being conducted on transmission to the final (definitive) host. other continents is largely accessible Holmes&Bethel (1972) delineated four ways through the bibliographies of the literature in which parasites might take advantage I cite herein. I emphasize areas in which of definitive host foraging behavior and trophic or trophically mediated inter- thus enhance transmission: they may alter actions of either parasites or hosts are host stamina, increase host conspicuousness NORTH AMERICAN ECOLOGICAL HELMINTHOLOGY 161

by changes in appearance, disorient the in the supraesophageal ganglion of car- host as a result of neurological damage, penter . These ants behave in a sluggish, and alter responses to environmental highly visible manner and may be more stimuli. More recently, Radabaugh (1980a) easily preyed upon by birds (Carney has shown that social (schooling) behavior 1969). Unlike B. mosquensis, which is in minnows is affected by a trematode, transmitted when the containing it Ornithodip/ostomum ptychochei/us, that is eaten, Plasmodium gallinaceum is trans- encysts in the brain (Radabaugh 1980b). mitted when its mosquito host (Aedes Infected minnows may form less compact aegypti) feeds. This malarial parasite schools and may be more vulnerable to affects the quality of the vector's saliva, piscivorous birds. necessitating increased probing activity When responses to environmental stimuli (Rossignol eta/. 1984). are altered, distributions of hosts may be In the case of vertebrate hosts, Rau & affected, with infected moving Caron (1979) showed that Echinococcus into areas of increased predator-prey hydatids may increase the likelihood of encounter (Holmes & Bethell972). Acantho- a moose being shot by a hunter (see also cephalans are especially notable in this Mech 1966). Rau (1983a, b, 1984a) regard, altering such behaviors as activity, discovered that mice infected with Tri- phototaxis, predator avoidance, exposure, chinella spira/is are less active and more substrate color choice and vertical dis- likely to exhibit subordinate behavior tribution. In some parasite-host associations, that could lead to predation and parasite these alterations have been shown to transmission. He did not find this with affect predation intensity in a laboratory T. pseudospira/is (Rau 1984b). Different setting (see Moore 1984a, b for reviews). predators may be involved in this parasite's Moore (1983) showed that an acantho- life cycle. Stibbs (1984) showed that rats cephalan, Plagiorhynchus cylindraceus, was infected with Trypanosoma brucei gam- also implicated in increased starling pre- biense had levels of serotonin, dopamine dation on the terrestrial isopod inter- and 5 - hydroxyindoleacetic acid that mediate host (Armadillidium vulgare) under differed from those of uninfected controls. field conditions. What this says to ecologists Activity levels in the two groups also in general is that parasites can affect the differed. distribution of animals in nature, and The cestode plerocercoid of Schisto- do so in a way that alters trophic inter- cephalus affects the respiration of its actions. Thus, two communities that stickleback intermediate host. These exhibit similar isopod relative abundances, require more oxygen, move to shallower but vary in the prevalence (""' infected water, and may be easier prey for pisciv- hosts; Margolis et a/. 1982) of P. cylin- orous birds (Lester 1971 ). The swimming draceus, could yield different rates of avian abilities of some intermediate hosts are predation on these isopods. impaired by the trematode, Nanophyetus Acanthocephalans are not alone in this sa/mineola, with a similar possible result respect, and a wide range of parasites (Butler & Millemann 1971 ). Changes are not have been shown to use a variety of means always specific, however, and Brassard in altering host behavior and thereby et al. (1982) found that Diplostomum possibly affecting transmission probabili- increased guppy susceptibility to brook ties. Moore & Lasswell (1986) showed that trout, which are not suitable hosts for the when infected with an immature nematode parasite. They speculated that such a risk (Dispharynx nasuta), the isopod A. vulgare may be part of the cost of lowering guppy exhibited altered behaviors other than activity levels and thus possibly enhancing those accompanying acanthocephalan in- general predation, including that from fection. They tentatively concluded that birds. in at least one of these host-parasite asso- The examples I have reviewed here ciations (acanthocephalan or nematode), have covered a wide range of behavioral the changed behavior was peculiar to the alterations - altered responses to environ- association and not a generalized isopod mental stimuli, neurological damage, and response to infection. Other examples debilitation. Conspicuous intermediate host of parasites that alter invertebrate host appearance is another way that predation behavior include the larva of the trematode, risk may be increased (Holmes & Bethel Brachylecithum mosquensis, which encysts 1972). Oetinger & Nickol (1982) have shown 162 MOORE

that there are differences in ommochrome fication in response to risk of parasite fractions between uninfected Asellus inter- acquisition. medius and A. intermedius infected with Evidence for behavioral changes that Acanthocephalus dirus. These differences are important in parasite transmission support the idea that the acanthocephalan is abundant, especially among cases where may compete with the isopod for com- predator-prey interactions are necessary pounds used in ommochrome synthesis, for parasite life cycle completion. Less thus resulting in pigment dystrophy. well known is the fact that changes in host Brattey (1983) has recently reported behavior may also alter the role of the that Asellus aquaticus exhibits darkened host as a consumer in community trophic respiratory opercula when infected with interactions. Curtis (1985) showed that Acanthocephalus lucii. In his laboratory after the breeding season the carrion studies, perch ate a disproportionately response of the snail, Jlyanassa obsoleta, large number of infected A. aquaticus. was affected by a variety of trematode The evolutionary history of behavioral larvae. This was not thought to be related changes associated with parasitism is to transmission efficiency, as the snails unclear. Holmes & Bethel ( 1972) considered were first intermediate hosts for the alteration of host behavior to be a parasite parasites, which will actively leave the strategy. Smith Trail (1980) hypothesized snails in search of the next host. Compared that under some conditions, behavioral to uninfected conspecifics, Helisoma tri- changes could be a kin-selected host volvis infected withEchinostoma revolutum adaptation. Through suicidal behavior, is less attracted to food (Boland & Fried the host individual could eliminate the 1984), and exhibits reduced radular activ- parasite from the host population. Parasite ity (Moore, unpubl.). Female grasshoppers transmission might later be favored by such infected with Nosema locustae, a pro- suicide. Moore (1984a) argued that this tozoan, consume less food than conspecifics was unlikely in the case of acanthoceph- (Oma & Hewitt 1984). For general reviews alans. She noted that in at least one case, of the physiological aspects of such host- (Polymorphus paradoxus in Gammarus parasite interactions, see Vinson and lacustris; Bethel & Holmes 1974) the behav- Iwantsch (1980), Thompson (1983), and ioral switch does not occur until the Beckage (1985). acanthocephalan is infective for the final host, a trait that clearly benefits the Host Distribution parasite. In addition, many intermediate hosts that suffer altered behavior when Parasites can affect the distribution of their infected with acanthocephalans are not hosts on a variety of scales, both locally and thought to occur near their kin, and some globally, and not all of these involve of them are reproductively functional, parasite transmission probabilities or host thus increasing the cost of suicide consid- foraging. Curtis & Hurd ( 1983) showed that erably (see also Wilson 1977). Studying trematode parasites were an important non-helminth parasites, Stamp (1981) component of the local spatial hetero- found the behavior of gregarious caterpillars geneity exhibited by the snail, Ilyanassa containing to be inconsistent obsoleta. Because oflarge spatial differences with the host suicide hypothesis. Horton in prevalence of trematodes, there were (ms. in prep.) has explored the possibility spatial differences in llyanassa reproductive of individual host defense mechanisms output. "Heavily infected snails are little playing a role in the evolution and main- more than 'sacks' of parasites with espe- tenance of altered behaviors found in a wide cially gonads, and sometimes digestive range of host-parasite associations. glands, virtually absent" (Curtis & Hurd The likelihood of parasite transmission 1983:823). Curtis & Hurd asked if such may also affect social behavior. Freeland parasites can be keystone species in the (1976) has suggested that primate social sense of Paine (1969). behavior, including aspects such as xeno- Parasites can clearly affect the distri- phobia, group size, infant handling, and bution of their hosts on a global scale. sexual fidelity, may have been influenced The meningeal worm, Parelaphostrongylus by correlates of pathogen transmission. tenuis, is benign in whitetail deer, but Current news sources speculate that human pathogenic for some other cervids (Karns social behavior may be undergoing modi- 1967, Anderson 1972). Range expansion NORTH AMERICAN ECOLOGICAL HELMINTHOLOGY 163 of whitetail deer has resulted in decreases parasitized. Most helminths have trans- in other cervid species. Barbehenn ( 1969) mission stages that must survive and in hypothesized that parasites may give a some cases, develop outside a host. Clearly, host a competitive advantage against other ambient conditions would be of great animals for which the parasite is more importance to these life history stages. pathogenic (see also Cornell 1974). Freeland Sankurathri & Holmes (1976) reported that (1983) expanded upon this idea at the high temperatures associated with thermal community level and suggested that the effluents had a negative effect on two notable phylogenetic, morphological and subspecies of Chaetogaster limnaei, an ecological differences among coexisting oligochaete associated with the gastropod animals that are often attributed to com- Physa gyrina. These were observed petition might result from the influence to eat larval stages of the trematodeEchino- of parasites. Such differences could act as paryphium recurvatum, and a decrease barriers to parasite transmission and thus in annelids coincided with an increase in allow coexistence. E. recurvatum infection. There is certainly evidence that parasites Temperatures external to the host can can modify the effects of host species on affect both the state of the parasite and one another (reviewed by Holmes 1979, its effect on the host, even where homeo- 1982, Holmes & Price 1986), and Park's thermic hosts are concerned. Novak (1979) ( 1948) classic work on Tribolium castaneum showed that the cestode Mesocestoides and T. confusum showed clearly that corti in mice exhibited greater biomass at parasites can reverse the outcome of colder temperatures. Also in mice, the competition between two species. Price cestode microstoma was et al. (1986) have recently reviewed the heavier, produced more eggs, and reached literature concerning ecological interactions patency (egg production) sooner at colder that are mediated by parasites (broadly temperatures (Evans & Novak 1983). This defined). They observed that the results tapeworm also influenced the weight of of such "germ warfare" were unlike those the liver (as did temperature and, to some of more direct interaction, in that the degree, host sex) and the weight of the effects of parasites could be far greater bile duct (Evans et al. 1985; see also Novak than their cost to the original host and et al. 1986 for effects of temperature and could be observed over large distances. infection on mouse They maintained that parasite-mediated small intestine). In a field study of habitat ecological interactions are quite common, variables and parasitism, Pence & Windberg and cited numerous examples of such (1984) found extrinsic factors such as phenomena as endosymbiosis, asymmetrical seasonality to be influential in populations effects on hosts (e.g. P. tenuis), protection of coyote parasites. against other parasites, diet selection that Holmes ( 1979) examined the effects includes parasiticidal elements, and me- that biotic influences on hosts might have diation of predator-prey interactions (e.g. on their parasites. He noted that not all acanthocephalans). They observed that hosts were of equal quality where a parasite when biotas are introduced, animals in one was concerned and delineated the following biota that have no apparent ecological three types of hosts: 1) required - the equivalent (competitor) in the other may parasite is well-adapted to this host, which nonetheless go extinct. In many cases, this is necessary for its survival; 2) suitable- the occurs in the smaller of the groups, and is parasite can mature in this host, but consistent with the notion that more cannot maintain its population with this pathogenic organisms can be successfully host alone; and 3) unsuitable- the parasite propagated in larger groups. Thus, over can establish, but cannot reproduce. evolutionary time, parasites may have been Holmes (1979) observed that because a selective force on many aspects of bio- parasites can often be exchanged among logy, from the molecular to the biogeo- host, the host community composition graphic level (Price et al. 1986). should influence that of the parasites, and that such current ecological conditions Environmental Influences might obscure historical host-parasite asso- ciations (Holmes 1983). (Other influential The temperature at which the host lives factors in his model included parasite can influence the likelihood of being fecundity, rate of establishment and 164 MOORE

maturation, life span, and host mortality). host growth and survivorship that resulted For instance, if a competitor of the defin- from reduced reproductive effort. In itive host were introduced, the supra- addition, parasitic castration has a variety population of the parasite (all the parasites of effects other than reduced reproduction. of that species in the host populations; These can include alterations in internal Esch et al. 197 5) would be expected to chemistry, secondary sexual characteristics, decrease. The infrapopulation levels might internal organs, and sexual/parental beha- increase, however, if diet were restricted vior. Baudoin (1975) noted that castrated and more intermediate hosts were eaten. hosts often grew more than noncastrated In another scenario, the introduction of conspecifics. alternate prey might serve to decrease Sousa (1983) studied the interactions infrapopulations if fewer intermediate of several trematode species with the hosts were eaten. This might not affect marine prosobranch Cerithidea californica the suprapopulation if it allowed an in- in the field. He discovered that these crease in the definitive host population. infections did not necessarily result in The introduction of a predator on the gigantism, but that their effect on growth definitive host could decrease the parasite was related to the age of the snail, with population in at least two ways: 1) trans- enhanced growth most readily observed mission rates might decrease due to the in sexually mature snails. He hypothesized combination of fewer definitive hosts and that among such snails, life history attri- an increased number of individuals of the butes could affect the occurrence of intermediate host species; and 2) if para- gigantism in trematode-snail associations. sites exhibited a clumped distribution in In the case of short-lived gastropods the definitive host, along with an adverse (predominantly freshwater), reproduction effect on its ability to escape predators, is an energy-intensive activity and the predation on heavily-infected hosts could elimination of that activity by parasitic destroy a · large proportion of parasites. castration may liberate many resources In a similar vein, Pence et al. (1983) for enhanced growth. Iteroparous, long- suggested that the "secondary commu- lived snails (usually marine) may have a nity" of parasites within a host (those smaller proportion of their energy budget shared by other host species) might be devoted to reproduction. Elimination of more likely to be involved in parasitic the gonads in these animals, as well as in outbreaks and epidemics than the "pri- sexually immature snails, liberates less mary community" in that host, in part energy and may not result in notably because members of the secondary com- increased growth. Sousa emphasized the munity did not depend on that specific diversity in snail-trematode interactions host for survival. Clearly, external con- and qualified his model with the ob- ditions - both biotic and abiotic - and servation that no single model was likely their effect on trophic interactions can to describe all such interactions. Working influence parasites tucked away and with a bivalve, Transennella tantilla, unseen within their hosts. Kabat ( 1986) also concluded that dis- tribution of reproductive activity over Reproductive A Iterations time could influence the outcome of trematode-mollusc interactions. Castration The castration of a host by its parasite was not complete in these animals, which is one of the more dramatic ecological are sequential brooders (i.e., not all brooded effects that parasites can have and its offspring are at the same developmental impact has been considered in the con- state). Kabat speculated that total cas- texts of individual evolutionary strategy tration may be more likely for a syn- (e.g. Baudoin 1975, Sousa 1983, Minchella chronous brooder, perhaps because of a 19 85) and population influences (e.g. threshold in the energy required. Obrebski 1975). Kuris (1974) considered Minchella (1985) discussed possible the trophic role of a parasitic castrator molluscan responses to parasitism and and stated it was similar to that of a para- asked why resistance to infection was not sitoid, among other things, "killing" one more common. Minchella & LoVerde (1983) host per parasite. Baudoin (1975) noted determined that in the presence of sus- that parasitic castration could enhance ceptible snails and schistosome miracidia parasite fitness through the increase in (the infective stage), resistant snails exhib- NORTH AMERICAN ECOLOGICAL HELMINTHOLOGY 165

ited lower reproductive success. Minchella mortality, 3) immunity, and 4) trans- (1985) then noted that the evolution of mtsston. They noted that because of resistance depended not only on the changes in virulence, the ability of a presence of appropriate genotypes, the parasite to regulate the population of effect of the parasite and the probability its host may vary over time. Cyclic vari- of encountering it, but also on the cost ation in prevalence itself can result of resistance as compared to those factors. from stochastic fluctuations in preva- Other responses are available to molluscs, lence or temporal variation in transmission. and these include fecundity compensation May & Anderson (1978) indicated that (early reproduction prior to castration) the results of these models may be useful and gigantism, which he expected to for public health consideration of chemo- encounter as a host adaptation primarily therapy. They further explored the role in long-lived snails with some possibility of immunity in host populations (Ander- of outliving the infection. son&May 1985a), mathematically modelling helminth population dynamics in a host population whose individuals are hetero- Population Effects geneous in their ability to acquire immu- nity. (See Wassom et al. 197 4 and Amason In a series of papers, Anderson and May et al. 1986 for other considerations of host have explored host-parasite interactions heterogeneity in susceptibility). In such a at the population level (Anderson & May case, mass chemotherapy may result in 1978, 1979, May & Anderson 1978, 1979, an increased average worm burden. They May 1983, 1985a). (The reader is urged suggested selective treatment for indi- to consult these papers for detail). In viduals that are predisposed to heavy their models, Anderson and May assumed infection (but see Cheever 1986, Anderson that host mortality rates increase with et al. 1986). Schad & Anderson (1985) parasite levels. Using this and other presented evidence that in the case of assumptions about transmission rates and hookworms in humans, which occur in effects of parasite density and distribution, clumped distributions, pre- and post- they emphasized the importance of treatment hookworm levels were signifi- threshold host densities (for parasite cantly associated, suggesting that targeted persistence), host mortality rates, and, treatment might be efficacious. Host m the case of macroparasites, parasite genetics has also been shown to be im- reproductive rates in the regulation of portant in the distribution of cestodes host populations. (Unlike those of micro- in the white-footed deer mouse (Wassom parasites, the propagules of macroparasites eta/.1974,1986). do not remain within the host). They In a review of population models of found at least three stabilizing influences human-parasite interactions, Anderson & in host-parasite relationships. First, some May (1985b) and May (1985b) listed areas types of functional relationships between of research that are important for future parasite-induced death and parasite burden progress. These include basic aspects are stabilizing; others are not. Second, of helminth demography (reproduction, this relationship is linear and if parasites longevity), the influences of host age and are clumped in distribution, they may parasite density, and the origin and impli- regulate host population growth. Finally, cations of aggregated distributions. density-dependent constraints on parasite Holmes (1982) agreed that parasites populations acting within the host can do injure and kill their hosts. He indicated have a stabilizing influence. May and that additive mortality (above that expe- Anderson also discovered destabilizing rienced by a parasite-free host population) influences, which included a negative was likely in invertebrate host-parasite effect of parasites on host reproduction, associations and in the case of some in- temporal lags between transmission and troduced species associated with native reproduction of parasites, and within- faunal extinctions, but he questioned host parasite reproduction that enhances whether the effects of parasites were parasite population size. additive for vertebrate host populations Anderson and May listed at least four (but see Toft 1986). If disease, similar to factors that influence disease patterns: some forms of predation, primarily strikes 1) the host as parasite habitat, 2) host low-status, "surplus" animals, then ensuing 166 MOORE

mortality is compensatory - it replaces result of selection or simply coincidental other risks - and is not additive. In such with other factors in the pond. a case, parasites might act as agents of In considering the regulation of parasite selection but fail to exert a regulatory populations, Holmes et al. (1977) stated influence. Holmes (1982) agreed with that there were two prerequisites for Anderson and May on many points, but population regulation: I) reproductive argued that parasites, in many instances, activity must have the potential to increase were probably a source of compensatory population size, and 2) a feedback mechan- mortality, not additive mortality, and ism that prevents such increase must exist. stressed the need for more field studies. They cited Bradley (1972, 1974) in em- Getz & Pickering (1983) also urged in- phasizing transmission and immunity as creased study of individual host-parasite important limits to parasite population associations. growth. To this they added the influence Recent field work on parasite-induced of parasite-parasite competition. In a mortality has supported this call for know- modelling/simulation exercise, they showed ledge of specific systems. For instance, that a parasite suprapopulation might be Uznanski & Nickol ( 1980) observed no regulated by the occurrence of competitive effect of the acanthocephalan, Lepto- interactions in only one host species, rhynchoides thecatus, on the growth, provided the other species were inade- reproduction or survivorship of its am- quate to maintain the parasite population. phipod intermediate host. (They did not As has been recognized, the host may examine behavioral effects or predation influence infrapopulation size by a com- risk). Keith et al. (1985) found no con- plete or partial immune response. Para- sistent, single relationship between the sitologists have discovered even more prevalence of a variety of parasites of subtle and unexpected host influences snowshoe hares and the cyclicity of the on parasite levels. Possibly related to host population. They felt that their host immunity is the phenomenon of indicator (prevalence - i.e., presence/ arrested development, a condition seen in absence) might be too coarse and that some nematodes that temporarily cease parasite species might differ in the com- development within the host until some binations of factors that could influence future time. Schad (1977) reviewed this population size. Keith et al. (1986) did literature, and while he noted that arrested find intensities of some parasites related development might be controlled by host to decreased body weight, and intensity resistance or be a parasite response to of Obeliscoides cuniculi was positively adverse conditions, he emphasized its associated with likelihood of death from role in parasite population regulation. trapping, handling or predation. Granath & In the case of mammals, populations Esch (1983) determined that mosquito- of parasites may also appear where they're fish mortality from Bothriocephalus was least expected - in neonates - as a result influenced by several factors, including of transmammary transmission from in- temperature-dependent growth and size. fected mothers. Stone & Smith (1973) In a study that clearly showed the im- reviewed this literature, which deals pri- portance of multiple influences on parasite- marily with nematodes. Recently, cestodes host relationships, Lemly & Esch ( 1984) (Mesocestoides corti; Conn & Etges 1983) found that heavily infected juvenile bluegill and trematodes (A/aria marcianae; Shoop & sunfish died as a result of the interaction Corkum 1983) have also been shown to of decreasing temperatures (with associated enter new hosts in this manner (see also decreasing feeding) and of lipid depletion Miller 1981 ). Transplacental transmission associated with trematode larvae. If tem- is also known to occur in some species peratures remained high, bluegill continued (e.g., Hibler et al. 1972, Todd & Howland to feed and replaced lipids. McPhail & Peac- 1983). ock (1983) observed that seasonal differen- Host diet can influence levels of para- ces in prevalence can affect the impact of the sites that are transmitted in the food chain parasite on the host population. In their (Price & Clancy 1983). Campbell et al. cestode (Schistocephalus solidus) - stick- (1980) documented relationships between leback system, cestode larva prevalence the foraging habits of some deep sea fish was highest after the fish reproductive species and their parasite fauna. They season. They noted that this could be a also noted that differences in host habitat NORTH AMERICAN ECOLOGICAL HELMINTHOLOGY 167 and age-related dietary shifts influenced view that well-adapted, coevolved host- this fauna, as did host community di- parasite relationships tend to be benign versity. In a study of flatfish, Scott (198 2) has little factual or theoretical basis. noted the roles of host diet, age, sex, Holmes (1983:178) asked, "Because and geographic distribution in parasite the net reproductive rate of the parasite community composition. Amin (1985) is a function of both its reproduction per found that the numbers of the acantho- unit time and its length of life, under what cephalan Echinorhynchus·salmonis in hosts circumstances should a parasite be selected increased with host age while other acantho- to emphasize the former?". He suggested cephalans decreased, a trend he attributed, that increased reproductive rate would in part, to host diet. [See also George- be favored by factors such as the presence Nascimento & Vergara (1982) for Southern of a large, expanding population of hemisphere corroboration of host dietary susceptible hosts, life cycle attributes influence on levels of the nematode Prolep- that include host death as a necessary tus acutus]. part of transmission, and short-lived hosts. Recently, Kennedy et al. (1986) have Holmes (1983) discussed the following compared intestinal helminth communities three models of host-parasite coevolution: in fish and birds (plus one mammal). 1) The mutual aggression model, in which They found the ectotherms to be rela- the parasite increases exploitation and tively depauperate in both richness and the host increases defense; 2) the prudent abundance, and concluded that a variety parasite model, in which parasites are of factors contribute to helminth com- favored that limit damage to the host; munity diversity. While these factors and 3) the incipient mutualism model, certainly include breadth of host diet, in which both parasite and host are selected as well as inclusion of intermediate host to benefit one another. species in that diet, they also encompass Anderson & May (1982) reviewed the the diversity of habitats visited by the host-parasite coevolution and pathogenic- host and the exposure to penetration by ity literature that has been based on parasites that enter through non-dietary population genetics models and epidemio- means. The increased energy requirements logical models. They cautioned that many and intestinal differentiation of endotherms coevolutionary outcomes are possible, are yet other factors that may favor rich given a variety of relationships between communities. virulence and transmission. May & Anderson (1983) concluded that polymorphisms Coevolution probably result from the coevolution of hosts with a wide variety of parasites The evolution of virulence/avirulence is an and that "well-balanced" associations are active area of research emerging from not necessarily avirulent. Levin & Pimentel evolutionary theory that is closely related (19 81) theorized that a combination of to the work described in the previous intra- and interdemic selection pressures section. This is in part because virulence to increase and decrease virulence, respec- and parasite reproductive rate are used tively, could yield intermediate levels of synonymously, a habit that may give a pathogenicity. (see also Lewontin 1970). parasitologist pause, for the effect that a Bremermann &Pickering (1983) showed that parasite has on its host is often determined within-host competition among parasites by factors far more numerous and complex could affect the evolution of virulence. than the number of offspring it produces. In specific studies of the evolution of The reasoning behind the equation of virulence, protozoa have received more these two terms is nonetheless logical: attention than have helminths. Ewald In the case of two parasites that share (1983) predicted that vector-transmitted nearly identical biology and host-parasite pathogens should be more severe, for the attributes, the one that produces more transmission cost involved in immobilizing offspring will probably demand more the host is reduced. He tested this and host resources. [See Bremermann & Picker- some related predictions using a correlative, ing (1983) for a more complex definition comparative approach, and concluded that of virulence that includes parasite re- vector-borne diseases are more severe production, infectiousness, and disease than those without vectors. According severity]. At any rate, the traditional to Ewald, the implications of this for 168 MOORE

public health include the following pre- proposed to evaluate resistance via plumage dictions: 1) severity can be expected from and fur quality, the appearance of bare currently pathogenic vector-transmitted skin patches, and courtship behavior diseases and new benign vector-transmitted involving energy expenditure or urinary diseases, and 2) diseases of recent origin marking. They stated that their hypothesis that do not depend on vectors should - that animals exhibiting well developed tend towards avirulence. epigamic traits should be subject to a Gill & Mock (1985) studied the trypanos- wide variety of parasites - would be omes of the newt, Notophthalmus virid- refuted if, within a species, preferred escens, in an attempt to discover if hosts and mates had the most parasites, and would parasites could mutually regulate their be supported if, among species, those that populations and if there were evidence exhibit the greatest evidence of sexual for decreased virulence. They reviewed selection are those especially subject to the literature in this area and noted that parasitism. A comparison of the occurrence if there were a period in a host's life during of six blood parasites and three passerine which transmission could not occur, courtship displays revealed significant asso- parasite avirulence would be favored by ciations that are consistent with the Hamil- natural selection during this time. In the ton and Zuk model. "For the present eft stage of newt development, trypano- we conclude that eugenic sexual selection some prevalence is low and trypanosomes can work and may be common, and that cannot be transmitted until the newt our results hint at chronic disease as one reenters the pond some years later. They agitator of the dynamic polymorphism surmised that the trypanosomes allowing that such selection requires". (Hamilton & the eft to live until this time would be Zuk 1982:386). favored by natural selection, and that In a simulation study addressing this the trypanosome population of a pond hypothesis, Kirkpatrick (1986) found would then be influenced by these entering, that the alleles for male secondary sexual avirulent protozoans. Gill and Mock traits and female preference for these predicted increases in virulence as ponds traits will not necessarily spread if they age. They outlined three general models are rare. If female preference for male of pathogen evolution: 1) increasing traits is common enough, however, then pathogenicity in the presence of simul- a "runaway" process is possible. [See taneous infection by alternative geno- Kirkpatrick (1986) for further discussion]. types, 2) interdemal selection that incor- Hosts have been shown to exert a selec- porates transmission difficulties associated tive influence on their parasites, as well. with host death, and 3) avirulence favored After 16 generations of Hymenolepis by lack of transmission opportunities. citelli in Tribolium confusum, Schorn et al. Hamilton (1980) and Rice (1983) have (1981) found reduced infectivity of the hypothesized that sexual reproduction parasite. This corresponded with reduced may be favored by short-lived, rapidly- host mortality. LoVerde et al. (1985) evolving parasites. Hamilton observed that found that the allelic frequencies of a strain frequency-dependent selection mediated by of mansoni formerly kept in parasites would be most severe against baboons and passed for four generations the most common genotype, and that through mice became similar to frequencies in the presence of increasingly intense found in a strain that had inhabited mice selection and moderate fecundity, sexually for twelve years. reproducing animals are at an advantage. Brooks (Brooks et al. 1981, Brooks & Rice noted that a genetically divergent Glen 1982, Mitter & Brooks 1983, Brooks offspring might escape the pathogens et al. 1985, Glen & Brooks 1986) has accumulated by its parents. approached the study of coevolution from Hamilton & Zuk (1982) extended the role the standpoint of phylogenetic systematics. of parasites to that of an influence in Brooks ( 1 979) identified two processes sexual selection. In their model, the host that might commonly be considered and the parasite population each have coevolution: co -accomodation without two alternative genotypes (H, h and P, p ). speciation, and co-speciation with con- H confers resistance to p, susceptibility comitant host-parasite speciation. In the to P, and h does the opposite, producing papers cited above, Brooks and various co- a stable limit cycle. Hamilton and Zuk workers have used phylogenetic analyses NORTH AMERICAN ECOLOGICAL HELMINTHOLOGY 169

of parasites and their hosts to investigate body size and reproductive success. Dobson such divergent topics as biogeography (1986) found that both nutrition and and speciation of freshwater stingrays and parasite density contributed to variation their parasites, competing hypotheses of in body size and reproduction, and that hominoid phylogeny, and the importance cestodes and acanthocephalans differed of adaptive radiation versus developmental in their responses to changes in carbo- constraint in digenean trematodes. Such hydrate level, perhaps because of differ- approaches may also be informative in the ences in degree of flexibility possible in study of communities, as we shall see in their body plans. He emphasized that subsequent sections. natural selection acts on such individual variation. Resource use is an important aspect PARASITE COMMUNITIES of all community studies and in the case of parasites, location in the host is com- Because no parasite community exists monly used as an indicator of resource independently of the host it occupies, use. Within hosts, intestines can be viewed parasite community interactions have a as resource gradients and the distributions host component. The work I review below, of many environmental factors therein therefore, is not meant to be cast as in- are highly correlated (Read 1971 ). Location dependent of host biology, but it does is therefore an important indicator of emphasize the role of other parasites in resource use and bears discussion here prior parasite ecology. Conversely, the nature to examination of parasite community of a parasite community may influence interactions. Holmes' (1973) extensive the host: A diverse community may exert review of helminth site selection focussed a protective influence against the effects on this aspect of parasite communities. of a heavy monospecific infection (Holmes One influence on location is mate- 1979, 1983). finding. Bone (1982a, b) has reviewed much of the literature dealing with phero- Infrapopulations mones of Platyhelminthes, Nematoda and Acanthocephala. Most Platyhelminthes are Parasites can affect one another's reproduc- monoecious, but outcrossing appears to be tive success in a density-dependent way, common and in some species, single-worm a phenomenon long observed in cestodes infections may not mature readily. Mate- and studied in detail by Read (e.g., 1951, location mechanisms are common among 1959) and Roberts (e.g.. 1961, 1966). trematodes, and are especially important [See also Nollen (1983) and Fried & Free- for schistosomes, which are dioecious. borne (1984) for recent work on crowding Such mechanisms are not always flawless, in the trematode Philophthalmus gralli]. and Fried & Wilson (1981) have shown Lejambre et al. (1971) showed that fecal that interspecific pairing between the nematode egg output was correlated trematodes Zygocotyle lunata and Echi- more closely with total worm weight than nostoma revolutum occurs at frequencies number Recently, Insler & Roberts (1980), comparable to those of intraspecific pairing Roberts & Insler (1982), and Zavras & Ro- in the two species. Bone (1982a) speculated berts (1984, 1985) have performed a series that chemical releasers for this behavior of experiments in an attempt to isolate may not be specific and other factors factors that could contribute to stunted may contribute to reproductive isolation. growth in crowded cestodes (Hymenolepis Much less is known about reproductive diminuta). Zavras & Roberts (1985) con- behavior of cestodes. In the case of nema- cluded that among other influences (e.g., todes (dioecious), five zooparasitic species pH, carbohydrate availability), substances have been studied, with most attention such as succinate, acetate, D-glucosaminic devoted to Nippostrongylus brasiliensis acid and cGMP that are released by para- and . Male response to sites may contribute to the crowding chemical attractants in these species is effect by reducing the growth rates of stronger than that of females. In the case other worms. of Moniliformis dubius (Acanthocephala), Taxa of parasites may differ in the chemical recognition may be important extent to which they can exhibit res- for determining both species and sex of ponses to the environment in terms of potential mates (Bone 1982b). In the 170 MOORE latter instance, males place copulatory was relatively rare; "selective site seg- caps on both females and other males, but regation" (non-overlapping niches) was inseminate only females, a behavior which observed more commonly and Holmes may be a product of sexual selection. viewed this as an indication of the general Capped males are unable to reproduce maturity of helminth communities. Holmes (Abele & Gilchrist 1977). (1973) hypothesized that interactive site In addition to modifying location in segregation characterized more recent com- response to sexual cues, parasites select munity associations and that when para- locations based on physicochemical cues. sites are long-lived and commonly coexist, Initially, workers did not consider parasite it is replaced by genetically based selec- mobility within the host small intestine, tive segregation (see also Bush & Holmes but Read & Kilejian ( 1969) demonstrated 1983). Price objected to the contention circadian migratory activity modified by that parasite communities are mature, host feeding schedule in the cestode H claiming that parasites generally form non- diminuta. Such movements have both equilibria! communities. Positive association ontogenetic and circadian components among parasites has also been observed (Cannon & Mettrick 1970). Arai (1980) has (Holmes 1973, Hobbs 1980, Lotz & Font reviewed more recent work on migration 1985). in this worm and its relatives. Sukhdeo & Some workers have emphasized aspects Mettrick (1984) noted that major gradients of helminth communities other than were those of food and gastric, pancreatic competition. In a review primarily of and biliary secretions. They altered the monogenetic trematodes, Rohde (1979) location of these substances through observed that selective niche restriction ligation or surgery. They concluded that could result from intraspecific selection these cues were interactive and none was (e.g., mate location). Brooks (1980a, of singular importance. Moreover, the b, 1985) emphasized the role of phy- scolex of the worm was not always sen- logeny in structuring parasite communities. sitive to the same substances that influence Holmes & Price ( 1980) did not deny this the rest of the biomass. role, but did object to Brooks' assignment Site selection of nematodes has also of major importance to it. Toft (1986) been investigated. Sukhdeo & Croll (1981a) has hypothesized that competition should determined that bile was important for be relatively less important for parasites both establishment and location of Ne- than for predators. matospiroides dubius. In the case of Recently, Holmes (1986a) has cast this Heligmosomoides polygyrus, bile influenced controversy in a different perspective, larval site selection, but adult location asking not "Do interactions among hel- was more sensitive to stomach content minths structure communities of intestinal entry sites (Sukhdeo & Mettrick 1983). helminths?" but "Under what conditions Sukhdeo & Croll ( 1981 b) found that al- do interactions become particularly im- though surgically implanted T. spiralis larvae portant in structuring such communities?". could establish anywhere in the small Holmes & Price ( 1986) have enlarged upon intestine, the location of orally transmitted these remarks explicitly considering the worms was influenced by intestinal motil- assumptions that underlie a range of ity, inoculum size, and size of the delivery hypotheses about parasite communities apparatus. and the predictions that emerge from those hypotheses. They view parasite-parasite interactions in at least three ways - at the Multiple Species level of the infracommunity (within host individual), the component community The community ecology of parasitic (within host population or species), and the helminths is a field with much controversy, compound community (within host com- most of it centering on the role of com- munity, especially over several habitats). petition. Holmes (1973) reviewed research The elements of this hierarchy are inter- on parasitic communities within hosts, dependent. For instance, Holmes (1986b) and noted that competitive exclusion noted that interactions within hosts are was apparently common and that "inter- important in terms of predictable com- active site segregation" (spatial niche shift munity structure and possible coevolution in the presence of possible competitors) only when the species involved regularly NORTH AMERICAN ECOLOGICAL HELMINTHOLOGY 171 co-occur. Although interactions occur in ualistic response hypothesis states that the infracommunity, the degree of co- coevolutionary processes and increasing occurrence must be measured at the specialization on the part of parasites component and compound community can result in adaptation to narrow niches levels. Concepts diminishing the importance that is independent of other parasite of infracommunity interactions are usually species. characterized by assumptions that mini- Holmes & Price (1986) observed that mize co-occurrence, and Holmes suggested the competition hypothesis was compat- that structure might be more readily ible with what they called interactive observed if dominant species groups or communities, characterized by species that guilds were the object of greatest attention. readily colonized the host, resulting in I will review infracommunity and com- high populations of animals that com- ponent community work here, but studies monly co-ocurred. These are equilibria}, of compound communities are beyond saturated communities. Isolationist com- the scope of this paper. At the compound munities, unsaturated and nonequilibrial, level, species specificity (Pence & Eason characterized by low probabilities of 1980) and relative numbers of hosts (Leong colonization and co-occurrence and by & Holmes 1981) contribute to community low population levels, are appropriately composition. See Holmes & Price (1986) aligned with the remaining two hypotheses. for further discussion. Interactive and isolationist communities can be seen as the extremes of a continuum along which parasite communities occur. !nfracommunity [I urge the reader to consult Holmes & Price (1986) for greater detail about this It is at this level that individual parasites and other levels of parasite communities]. interact. Individuals of a species of host The most detailed recent work on infra- can be considered replicate communities, communities includes that of Bush&Holmes and one can examine presence/absence (1986b) and Lotz & Font (1985). Bush data, intensity, growth, maturation, fecun- and Holmes studied a complex, diverse dity and location (both shifts and differ- community of intestinal helminths of ences in dispersion) as indicators of inter- lesser scaup. They found all parts of the actions. Such interactions can even small intestine occupied by the 29 species appear in low diversity communities, that made up 99% of the parasite indi- provided species use similar resources. viduals. In an association analysis (Bush & Holmes (1986b) found Hanski's (1982) Holmes 1986a), they were able to identify concepts of core species (those occuring core and secondary species, and in their at high densities in most patches) and study of infracommunities (Bush & Holmes satellite species (low densities, few patches) 1986b), they found that in individual birds, to be useful in studying replicate commu- each of these species occupied only a small nities (see Bush & Holmes 1986a). He portion of its potential range. This result, cautioned against summing across commu- along with the shortage of vacant niches nities for evidence of within-host inter- and the evenly dispersed locations and action and noted that the positive asso- ranges of helminths, led Bush and Holmes ciation often observed between core to conclude that these communities were species could result from similar exposure interactive. Differences in radial distribution of the host to associated parasite groups, were also observed (see also Schad 1963), similar aspects of host quality for the and three guilds were identified: small, groups, or mutualism. paramucosal absorbers (cestodes and acan- In a thorough and thoughtful review, thocephalans), larger mid-lumenal absorb- Holmes & Price (1986) delineated three ers, and active ingesters (trematodes). hypotheses relevant to the study of infra- In these communities, the core species communities. The competition hypothesis were the most abundant and exhibited states that competition has been and the earliest and fastest colonization. Most continues to be an important organizing of the core species specialized on scaup. force in parasite communities. The popu- They were in the absorber guilds and used lation concentration hypothesis emphasizes one of two commonly consumed inter- that niche restriction might be necessary mediate hosts, resulting in high levels for successful mate location. The individ- of co-occurrence. The secondary species 172 MOORE

occupied spaces left open by core species. noted that as aggregation intensified, intra- They were moderately abundant and exhib- specific interactions would become increas- ited moderate colonization rates. Satellite ingly important relative to interspecific (rare) species arrived later and were essen- interactions and that the pattern of parasite tially random in location. distribution among hosts may be at least Detailed analyses of infracommunity as important as resource use in parasite structure may well be necessary for under- communities. Such an approach involves standing helminth community structure. not only scrutiny of the infracommunity, Bush & Holmes (1986b) noticed that Holmes but also consideration of component and associates, ·in earlier studies of the and compound communities. same host-parasite system on a coarser scale, had failed to find evidence for inter- active segregation. Component Communities In a detailed study that compared parasite communities (largely trematodes) Students of component communities are in two host populations, Lotz & Font (1985) concerned with community interactions found little evidence for parasite-parasite at the host species level. Holmes & Price interaction. They used different analytical (1986) identified four hypotheses that methods from those of Bush & Holmes have been put forward to account for (1986a, b) and their communities did not patterns at this level. The cospeciation contain as many parasites. They concluded hypothesis was formulated by Brooks that the host immune response kept (1980a, b) and is based on the idea that parasites at population levels below those parasite communities cospeciate with the at which competition might occur. Referring host group and reflect historical events. to some related parasites of European The island size hypothesis is rooted in the bats, Lotz and Font speculated that some MacArthur & Wilson ( 1967) theory of island within-host distributional characteristics of biogeography and predicts that larger at least one species were perhaps of histor- islands should have more species of para- ical origin in that they were shared by a sites. (There is, however, some confusion European congener. about what "island size" should be - host Positive associations among parasites range? host population size?). The island have been observed (e.g., Hobbs 1980, distance hypothesis, also emerged from Lotz & Font 1985). The mechanisms that the theory of island biogeography, holds support these are often not clear, and the likelihood of reaching a host as a major possibilities range from mutualistic inter- influence on parasite communities. Finally, actions (e.g., Ewing et al. 1982) to similar the time hypothesis states that increasing habitat requirements (Hobbs 1980) or use species number requires time, and older of the same intermediate host (Bush & communities will have more parasite Holmes 1986a, b). In fact, precise mech- species. anisms of parasite-parasite interactions, Holmes & Price ( 1986) noted that as whether positive or negative, are often formulated by Brooks (1980a), the cospe- unknown. The influence of the host ciation hypothesis is largely independent immune system can act in either direction of ecological interactions. The island bio- and is a feature unique to parasite commu- geographic hypotheses yield predictions nities. Holmes (1983) reviewed examples of about species number, not about more the immune system enhancing (immuno- subtle interactions. Nonetheless, in young suppression) or depressing (e.g., cross- communities characterized by larger island immunity, Schad 1966) parasite-parasite distances, isolationist traits might be co-occurrence. Bristol et al. (1983, and expected. Holmes & Price ( 1986) also noted references therein) describe such inter- that one implication of the cospeciation actions between vastly different taxa hypothesis is that no island/host species (nematodes and protozoa). Is ever empty, a problem for the time hy- Dobson (1985) recently considered the pothesis. relationship of competition and parasite In fact, the use of hosts as islands has population dynamics, emphasizing the engendered a lively debate in the ecological importance of parasites' distributions among literature. Students of herbivorous hosts, together with pathogenicity, as an communities have explored this concept influence on continued coexistence. He most widely. Freeland's (1979) study NORTH AMERICAN ECOLOGICAL HELMINTHOLOGY 173 of primate social groups as islands is one Some hosts are long -lived enough to of the more notable endoparasite studies acquire what appears to be a full comple- using this approach. He found that number ment of parasites; others are not. In the of protozoan species was related to Cerco- case of some types of parasite transmission, cebus albigena group size, that entry of island distance and its analogues are much nonmembers into Cercopithecus mitis more meaningful than for other trans- groups increased protozoan species richness, mission modes. The objections of Kuris but that all groups of Papio anubis had et al. (1980) should be studied and kept equivalent protozoan fauna. This last in mind in the attempt to combine produc- species, living in the savannah, had a tive questions with tractable systems. higher rate of intergroup exchange than Price & Clancy (1983) studied checklists forest-dwelling primates. Freeland specu- of the parasitic helminth fauna of British lated that disease-related selection on freshwater , questioning how diet such social behavior may vary across and area of host range were related to habitats. [See Betterton (1979) for a parasite species number. They found that consideration of mainland versus island host range accounted for most of the effects on species richness]. variation (68%) in number of parasite Kuris et a/. (1980) objected to the use species. Host length was a significant of hosts as islands. They reviewed the influence only in the cases of acantho- literature on that topic and delineated cephalans and nematodes. For all para- three ways of approaching host-islands: sites but the Monogenea, which are not individual hosts, host populations, and transmitted through feeding, the feeding host species. At each of these levels, class of the host accounted for a signif- hosts differ from true islands. Thus, un- icant amount of variation in parasite like islands, individual hosts may defend species number. (Feeding class was taken against colonist parasites, which in turn to mean major class of food- invertebrates, may threaten the existence of the host. , fish, et cetera. Thus, both bio- Interisland distance may fluctuate and geographic and dietary factors were shown there may be seasonal and ontogenetic to affect species richness. differences in host quality. The host itself The cospeciation hypothesis has been may be short-lived, and its parasite commu- directly addressed by Brooks ( 1980a, b, nity may not reach equilibrium. At the 1985, Brooks & Wiley 1986 and Holmes & level of host populations, Kuris and co- Price (1980). Holmes (1971) published a workers criticized the use of agricultural study of two blood flukes of rockfish that systems as islands, and noted that features occupied different sites in the fish's heart, such as host density, range, variation, a difference he found to be intensified in dispersion, and overlap with other host concurrent infections. Holmes ( 1973:341) species can all affect the application of said, " ... niche segregation between the island biogeographic theory to host- two appears to be basically genetically parasite systems. At the level of the host entrained, but reinforced by interactive species, they stressed that coevolved site segregation". Brooks (1980a, b) noted characteristics could substantially influence that while Holmes (1973 ), Rohde (1979) the fit of island biogeographic theory to and Price ( 1980), came to different con- these systems. Other workers (e.g., Lawton clusions about historical influences on et al. 1981, Rey et al. 1981) rose to the current parasite communities, none had defense of the application of island biogeo- considered the role of parasite-host coevo- graphic theory to host-parasite systems, and lution and phylogeny in t:.he structure of the disparate views have yet to converge. these communities. Citing the rockfish In general, nothing but an island is truly (Holmes 1971) example specifically, he an island. All other sorts of disjunct habitats developed phylogenetic models that could are simply analogous to islands and share account for these observations without some, but not all, of their attributes. If involving the historical influences of the extension of island biogeographic colonization, competition or sexual se- theory to these analogous situations is lection, respectively. to be pursued in a reasonable manner, Holmes & Price (1980) agreed that phylo- then the analogy must be formulated in genetic considerations would illuminate a way that makes good biological sense ecological studies, but concluded that an for the specific communities in question. evolutionary study of the blood flukes 174 MOORE of rockfish (e.g., Holmes 1971) showed considered a trophic level, they are diverse that one species had entered as a rela- in their nutritional requirements. The tively recent colonist, and that this system parasite interactions that may result from had not experienced lengthy coevolution. such requirements in a limited environ- They argued that the abundance of para- ment can, along with other factors, in- site species with little host specificity fluence the array of parasites available generally indicated a large potential for to a host or host community and, by host shifts and colonization, and that extension, the ecology of the host (s). Brooks' arguments were limited to lengthy, coevolved host-parasite associations. They speculated that while entire communities ACKNOWLEDGEMENTS had probably not coevolved, perhaps subunits had, and they developed criteria I thank Daniel Brooks, John Hohnes, Peter Price, and Joseph Schall for sharing material yet to be published, for distinguishing between non-interactive and Mario George-Nascimento for sharing ideas and and saturated communities. additional literature I had yet to contemplate. Mario Mitter & Brooks (1983) addressed the George-Nascimento, John Holmes, and an anonymous phylogenetic techniques useful in studying reviewer made suggestions that were helpful in improving coevolved communities, using specific an earlier version of this manuscript. I wrote this paper examples such as primate pinworms, while supported in part by NSF BSR-8452076. lower vertebrates and their trematodes, termites and termitophilous beetles and some phytophagous and their LITERATURE CITED host plants. They emphasized differences ABELE LG & S GILCHRIST (1977) Homosexual rape in patterns produced by colonization versus and sexual selection in acanthocephalan association by descent. Brooks (1985) worms. Science 197:81-83. and Brooks & Wiley (1986) have continued AMIN OM (1985) The relationship between the size of to explore aspects of historical ecology. some salmonid fishes and the intensity of Brooks (1985) disagreed with the phy- their acanthocephalan infections. Canadian Journal of Zoology 63: 924-927. logeny produced by Holmes & Price (1980), ANDERSON RC (1972) The ecological relationships and in his analysis, found host and parasite of meningeal worms and native cervids in cladograms to be congruent. He concluded North America. Journal of Wildlife Diseases that the rockfish trematode community 8: 304-310. ANDERSON RM & RM MAY (1978) Regulation and described by Holmes ( 1971) was histori- stability of host-parasite population inter- cally determined. Brooks & Wiley (1986) actions. I. Regulatory processes. Journal of urged the testing of competition hypo- Ecology 47: 219-247. theses against historical models. ANDERSON RM & RM MAY (1979) Population biology of infectious diseases: Part I. Nature 280: 361-367. ANDERSON RM & RM MAY (1982) Coevolution of CONCLUDING REMARKS hosts and parasites. Parsitology 85: 411-426. ANDERSON RM & RM MAY (1985a) Herd immunity In a narrow sense, parasites influence and to hehninth infection and implications for parasite control. Nature 315: 493-496. participate in trophic interactions when ANDERSON RM & RM MAY (1985b) Hehninth in- they alter the encounter rates between fections of humans: mathematical models, predators and their prey or host feeding population dynamics, and control. Advances patterns. Beyond such alterations, they in Parasitology 24: 1-101. ANDERSON RM, JA CROMBIE & RM MAY (1986) can affect the abundance and distribution [Reply to Cheever]. Nature 320: 195-196. of their hosts through effects on host ARAI HP (1980) Migratory activity and related phe- reproduction, direct pathogenicity, or nomena in Hymenolpeis diminuta. In: Arai HP mediation of interactions between (ed) Biology of the tapeworm Hymeno- free-living organisms. [As Holmes and lepis diminuta: 615-637. Academic Press, New York. Price (1986) observed, parasites both ARNASON AN, TA DICK & DL WASSOM (1986) A respond to and engender patchy biotic model to assess survival mechanisms of para- environments). Because many para- sites in a genetically defined host system. sites are transmitted through host diets, Parasitology 92: 253-267. they can be indicators of host foraging BARBEHENN KR (1969) Host-parasite relationships and species diversity in mammals: an hypo- habits. Hosts, by their dietary preferences, thesis. Biotropica 1: 29-35. can influence parasite community charac- BAUDOIN M (1975) Host castration as a parasitic strategy. teristics. Although parasites are often Evolution 29: 335-352. NORTH AMERICAN ECOLOOICAL HELMINTHOLOOY 175

BECKAGE NE (1985) Endocrine interactions between BROOKS DR, RT O'GRADY & DR GLEN (1985) endoparasitic insects and their hosts. Annual Phylogenetic analysis of the Digenea (Platy- Review of Entomology 30: 371-413. helminthes: Cercomeria) with comments on BETHEL WM & JC HOLMES (1974) Correlation of their adaptive radiation. Canadian Journal of development of altered evasive behavior in Zoology 63: 411-443. Gammarus lacustris (Amphipoda) harboring BROOKS DR, TB THORSON & MA MAYES (1981) cystacanths of Polymorphus paradoxus (Acan- Freshwater stingrays (Potamotrygonidae) and thocephala) with infectivity to the definitive their helminth parasites: testing hypotheses host. Journal of Parasitology 60: 272-274. of evolution and coevolution. 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