Host fragmentation and helminth parasites: Hedging your bets against extinction

THE FUTURE OF PARASITISM

In?er~at~~al

Pergamon

Jowrnaifor faT~j~al5g~, Vol. 24. No. 8, pp. 1333-1343. 1994 Copyright 0 1994 Australian Society for Parasitology Elswier Science Ltd Printed in Great Britain. All rights reserved 0020-7519194 $7.00 + 0.00

HOST FRAGMENTATION AND ~EL~INT~ PARASITES: YOUR BETS AGAINST EXTINCTION

HEDGING

ALBERT 0. BUSH* and CLIVE R. KENNEDY? * Department of Zoology, Brandon University, Brandon, Manitoba, Canada R7A 6A9 t Department of Biological Sciences, Hatherly Laboratories, University of Exeter, Exeter EX4 4PS, U.K. Abstract-Bush A. 0. and Kennedy C. R. 1994.Host fragmentation and helminth parasites: hedging your bets against extinction. International Journal for Parasitology 24: 1333-1343. We consider the probability of parasite extinction due to anthropogenic fragmentation of host populations and in the absence of host extinction. We conclude that extinction at infrapopulation and infracommunity levels is both common and trivial. Extinction may occur in communities at higher levels but only if metapopulations or suprapopulations become extinct. Suprapopulations are highly complex and unlikely to become extinct in the face of simple host fra~entation. We acknowledge parasite metapopulations as being the most likely to become extinct, but only locally. Our reasoning for this is that, in the absence of complete host extinction, populations of the parasite in other fragments are likely to serve as sources for reinvasion (e.g. a rescue effect). We identify a number of features that may act as hedges against extinction for many parasites and conclude by attempting to identify what form an extinction might take. INDEX KEY WORDS: extinction; hel~nth; host capture; host fragmentation; host specificity; rescue effect; parasite; parasite communities; parasite populations; progenesis; rapid evolution; reproductive

potential.

INTRODUCTION With his seminal paper “Parasites Lost?“, Sprent (1992) has presented us with a great challenge“Is there a future for parasitism?‘. His view is that environmental change, which can be accelerated and amplified by anthropogenic forces, can result in habitat destruction which can lead to host population decline. Such a decline could then result in fragmentation of host populations which in turn could promote parasite extinction. Extinction, however, appears to be a rather common process. Indeed, Simpson (1952) suggests that >99% of all species that have ever lived are now extinct and that the fate for all species is probably extinction. Stork (1993) argues, somewhat humorously, that most species are twice as likely to become extinct as they are likely to be described. As biologists, we appreciate that extinction is not a simple process. For those of us who work with extant populations and communities, we recognize [“Jurassic Park” (Crichton, 1990) notwithstanding!] the finality of extinction. But we also recognize that global species extinction only occurs when the last population of a species has disappeared and this

$Order of authorship does not imply seniority.

subsumes that all local populations have become extinct. With the exception of mass extinctions (see below) this is likely to be a slow process. With these realities in mind, and with our increasing concern for the environment, words such as “conservation,” and “preservation” “extinction”, have been resurrected as ecological buzzwords and have led to the coining of even more buzzwords (e.g. “biodiversity” Wilson, 1988). Concern for anthiopogenic extinction is very real today as evidenced by the creation of new journals within the past decade (e.g. Conservation Biology, Biodiversily and Conservation) and by worldwide participation in the “United Nations Conference on Environment and Development” meeting in Rio de Janeiro in 1992 where 156 countries signed the Biodiversity Convention. Unfortunately, despite the considerable effort and energy expended on the implications of extinctions, a perusal of the extant literature would suggest that it is a problem only for macroscopic free-living plants and animals. This is perhaps understandable since the concept of ‘conserving’ parasites seems a classic oxymoron. Thousands of careers and billions of dollars have been devoted solely to trying to eradicate some parasites. Nonetheless, if “biodiversity” is 1333

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truly meaningful, parasites are a very real part of that diversity. Others in this issue address the origins and diversification of various parasitic taxa, or focus specifically on the effects that complete host extinctions might have on parasites. We have been asked to consider the impact that host fragmentation might have on the extinction of parasite populations and communities. We begin with some caveats and definitions pertinent to the arguments we will present. We then discuss fragmentation of host species and how this might impact on parasite populations and communities. We follow this with our interpretation of how parasites can hedge their bets against extinction and we conclude with some specific predictions. CAVEATS

AND DEFINITIONS

At the very outset, we acknowledge that we make very broad generalizations and, as such, some exceptions probably exist for most of our examples. Nonetheless, the nature of the topic demands generalizations since too few specific data, addressing the topic explicitly, exist. We use the terms patch and fragment to refer to a host individual and host population, respectively. We use the terms infrapopulation (Esch, Gibbons & Bourke, 1975), metapopulation (Levins, 1970) and suprapopulation (Esch et al., 1975) to describe variously more inclusive populations of a given species of parasite. [Since “suprapopulation” is itself defined using the term “ecosystem”, which has no specific meaning (it is usually detined by the whims of the investigators or the nature of the study), we use the term in its most holistic sense to differentiate it from metapopulation and to equate it with a compound community]. At the level of the parasite community, we use the analogous terms infracommunity, component community and compound community as originally proposed by Root (1973) and as applied to parasites by Holmes & Price (1986). The concept of extinction, at either the infrapopulation or infracommunity levels, is trivial; each time a host dies, from whatever cause, all infrapopulations and thus the infracommunity they comprise, become extinct. We will not consider these further. At the other extreme, extinctions of parasite suprapopulations or compound communities are highly unlikely and far too complex to deal with here. Clearly, mass extinctions (see below) might yield such a result, but that is tangential to our topic. Further, we recognize that, although compound communities might go extinct, theydo not necessarily have the same parasite species from one locality to the next. For that reason, when we discuss, briefly, extinction of component commu-

nities, we will actually focus on community resilience (e.g. the ability to rebound after a local extinction of a component community even though the identity of the parasite species may change). We use the term “parasite” loosely; our focus is on, and our examples derive largely from, the parasitic endohelminths, the group we know best. Further, our examples reflect an inherent bias in our knowledge of the literature and focus-heavily on North America and Britain. Among parasites, we recognize a continuum ranging from a “host-specialist” to a “hostgeneralist”. We consider a specialist as one with the bulk of its metapopulation in a single host species (e.g. Leong & Holmes, 1981). As such, other hosts are ‘sinks’ and the parasite metapopulation could not survive in these hosts. In contrast, we recognize a generalist as being a species whose metapopulation may be spread over many different host species. We recognize 3 mechanisms leading to global extinctions: mass extinctions (such as those at the Cretaceous/Tertiary boundary), background extinctions (e.g. the gradual disappearance of species over time) and anthropogenic extinctions (e.g. those enhanced by human insult to the environment). (For parasites, anthropogenic extinctions could translate into extinctions due to accelerated host fragmentation-precisely the concern of Sprent, 1992). Further, we distinguish between local, temporal and global extinctions. Local extinctions are those in which a metapopulation or component community becomes extinct within a fragmented host population. Temporal extinctions occur in migratory hosts where the metapopulations or component communities become extinct but only on a cyclical basis. Global extinctions are what ecologists fear most and are self-explanatory. Embedded in the idea of extinction of parasites must be an appreciation for the niche of the parasite. Most parasites have complex life cycles that serve to increase the complexity and number of niche axes. We consider it germane to consider extinction in patches or fragments only where all elements of the niche are available. Mass extinctions can lead to the extinction of any parasite population or community. Others in this issue, by discussing diversification, will address background extinctions. We will focus primarily on anthropogenic and local extinctions of parasite metapopulations. HOST FRAGMENTATION

Parasites live in patches (host individuals) and fragments (host populations). Price (1980) has emphasized that patchiness is normal for parasites, that the probability of colonization of a patch should be low and, within a fragment, the probability of a

Hedging your bets against extinction parasite going extinct should be high. That parasites continue to persist suggests that they have adapted, through evolutionary time, to the dual obstacles imposed by exploiting patches within fragments. On the other hand, we know that the frequency and magnitude of anthropogenic factors fragmenting host populations are increasing. This could lead to situations, in ecological time, where host fragmentation may prove too difficult for parasites to overcome. Several theoretical treatments of parasite population dynamics suggest a threshold host population size below which there are too few hosts for transmission of the parasite to occur (e.g. Anderson, 1982, Keymer, 1982, Warren, Anderson, Capasso, Cliff, Dietz, Fenner, T-W-Fiennes, Grossman, Knolle, Mann, Molineaux, Schad & Schenzie, 1982). We are unaware of empirical tests of this hypothesis but it certainly appears intuitive. Likewise, it seems clear that there exists a threshold population size of the parasites themselves necessary to prevent extinction; as populations of parasites decrease in size, the of stochastic extinction increases. probability Another aspect of host fragmentation is that, if it happens too frequently, distances between fragments may become too great for the parasites to overcome. This will clearly be true for autogenic parasites but should also apply to allogenic parasites over time. There are many studies whose goal is to compare parasites in the same host species from host populations that have been fragmented due to historical factors (e.g. fish populations in glacial lakes). Assuming all elements of the parasite’s niche are present in each of the examined fragments (as we argue above), the absence of a specific parasite species’ metapopulation from one or more of the fragments might be indicative of local extinction. Such local extinctions can never be identified explicitly however, because we can never be sure that the species of parasite in question had ever colonized the fragment from which it is absent. By similar reasoning (and again assuming all elements for each species’ metapopulation are present), finding completely different component communities in hosts from different fragments might be indicative of local extinction of component communities. For both metapopulations and component communities, we fail to be able to conclusively recognize non-anthropogenic extinctions because no “before” and “after” studies exist. We do wish to acknowledge at this point that, for migratory hosts, we can recognize examples where the identity of the component community (and thus the collective metapopulations) changes (e.g. Bush, 1990). This is a form of temporal extinction. Since anthropogenic factors can accelerate or

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amplify host fragmentation, they can tell us much about extinctions of parasite metapopulations and component communities. The reason is that anthropogenic host fragmentations typically occur in ecological rather than evolutionary time and consequently, it is possible to obtain before and after studies. There are studies suggesting that anthropogenic influences, impacting on host metapopulations, can cause the local extinction of parasite metapopulations and even component communities. Boggs, McMurry, Leslie, Engle & Lochmiller (1991) present data on parasites in cotton rats (Sigmodon hispidus) which had been collected before and after intentional host-habitat modification. In this study, the anthropogenic factors were herbicides and prescribed burning. In a winter collection of rats on a control site, 5 of 8 were infected with the nematode Protospirura murk In winter collections on a site with Tebuthiuron’ (10 hosts), Tebuthiuron@ with burning (13 hosts), Triclopyr@ (15 hosts) and Triclopyr@ with burning (12 hosts), no P. muris were recorded. Because of the very small sample sizes and the short duration of this experiment, these data, although suggestive of local extinction, must be interpreted with caution. Black (1983) determined that the swimbladder nematode, Cystidicola stigmatura, was present in lake trout (Salvelinus namaytush) in the 5 Great Lakes at the turn of the century but that it is now extinct. Later (Black, 1985) he studied the reproductive biology of C. stigmatura in Arctic char (Salvelinus alpinus) the parasite’s other definitive host. He found that parasite reproductive output was a function of host size and age, with the majority of egg output occurring in old fish. Based on these observations, he reasoned that the extinction of C. stigmatura in the Great Lakes may have resulted from the exploitation of lake trout stocks which had been stressed by overfishing and predation by lampreys, Petromyzon marinus. Kennedy (1993) provides an example for both metapopulation and component community extinction. He examined the parasites of eels, Anguilla anguilla, over a 13-year period in a small river that had been subject to extensive anthropogenic disturbance and management during the interval. This is a particularly useful study because of its duration and because of the large sample size of hosts examined. He found that some metapopulations, for example the acanthocephalan Acanthocephalus clavula (a specialist in eels), went locally extinct in these hosts during 1984. During the previous five years, this parasite accounted for 63% of all parasites found. Eight years after the local extinction event, A. clavula accounted for only 1% of the parasites found. We interpret its appearance after

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the extinction as being due to a rescue effect from the River Exe. Data from the same study show that the species richness in the component community, which averaged three species from 1979 through 1983, fell to zero in 1984. In other words, the component community went extinct (but only for one year). Kennedy (1993) attributed these fluctuations to changes in the invertebrate community resulting from anthropogenic factors. We wish to emphasize, however, that the examples we cite above are only examples of local extinctions. They are not examples of complete or global extinctions. In summary, we acknowledge that parasite metapopulations and parasite component communities in migratory hosts become temporally extinct on a regular basis. Also, that parasite metapopulations (and, more rarely, component co~unities) may become locally extinct. Examples of global extinctions are rare. Stork & Lyal (1993) argue that two species of passenger pigeon (Ectopistes migrutorius) louse went extinct with the demise of their host. As the authors note, lice are extremely host-specific, a feature we suggest (see “Host Specificity”) enhances the probability of parasite extinction. Global extinctions may well have been more common in the past; for example, what of the parasite metapopulations and component communities in such hosts as the dinosaurs? Because these and many other hosts or potential hosts went extinct before parasitological examinations were possible, we can never know the answer. Even in the absence of mass extinctions, we often lack requisite data. For example, when the moas of New Zealand went extinct over a century ago, did they take with them parasite metapopulations or are those parasites found today in other ratites (e.g. the kiwi, emu, cassowary, rhea and ostrich)? It is also possible that parasite metapopulations or component communities, composed of host-specialists and occurring in endangered species, may currently be on the verge of extinction (e.g. Papasula abotti, found only on Christmas Island). However, to demonstrate such a pattern would require the examination of host species that are clearly not available for analysis. HEDGING YOUR BETS AGAINST EXTINCTIONS Our thesis then, is that global extinctions of parasite species (i.e. suprapopulations) are unknown and are highly unlikely. It follows then that the global extinction of parasite co~unities (i.e. compound) is even more unlikely since it would require the global extinction of two or more suprapopulations. We have provided some examples of metapopulation extinctions and their impact on component communities. The concept of extinction (as commonly

defined) is probably not germane to parasite component communities; rather, the appropriate question seems to be one of resilience. For example, we did note one instance where a component community disappeared for a very short time to be replaced by a component community composed of somewhat different parasite species. In other words, some, but not all, of the former component community species recolonized. For the remainder of this paper, we will focus primarily on parasite metapopulations. We believe that parasite metapopulations are unlikely to become globally extinct because the parasites possess so many adaptations to enhance their perpetuation. In fact, the very process of host fragmentation may serve to preserve species. Under such a scenario, some fragments may act as sources for the repopulation of depleted fragments (i.e. a rescue effect). For this positive effect of host fragmentation to occur however, the distance between fragments may be crucial. For example, if a parasite metapopulation becomes extinct in one region but not another, there must be a finite probability that the parasite can reach the first region from the second. As the distance between fragments becomes very large, there is a much greater chance that only allogenie parasites may be rescued. Although adaptations to decrease the probability of extinction are probably numerous, we focus here, by way of selected examples, on “plasticity” (the inherent ability to change) which we believe has the most significant impact on a parasite’s persistence. Parasitologists have long been constrained by what they could observe. For example, historically, we differentiated species A from species B because of some suite of morphological characters. However, it has been demonstrated ex~rimentally that individual parasites of the same species may differ, significantly, in various morphometrics when found in different host species (e.g. Kinsella, 1971, Bush & Kinsella, 1972). Recent studies at the molecular level (e.g. Bullini, Nascetti, Paggi, Orecchia, Mattiucci & Berland 1986; Lydeard, Mulvey, Aho & Kennedy, 1989) confirm that parasites have the potential for high genetic diversity. In other words, what may appear to be a narrow and specific parasite may simply reflect that its potential plasticity has not been challenged. We will begin with a discussion of host specificity, followed by host capture, progenesis, rapid evolution and high reproductive rates. We have imposed categories on what we consider to be plastic features for convenience in presentation. They are not necessarily independent of one another (e.g. host specificity vs host capture).

Hedging your bets against extinction Host specz$city

“La notion de specificite parasitaire a toujours CtC au centre de la parasitologie.” (Chabaud,l981). Cameron (1964) made a similar argument but with the inclusion of an important caveat “Host specificity is one of the fundamental characteristics of parasitism but it is seldom absolute, and to a variable degree it is relative.” The important words are “seldom absolute” and most parasitologists consider parasites as falling on a continuum of host-specialist through host-generalist. Clearly, a major hedge against metapopulation extinction can be accomplished by increasing the number of hosts (intermediate, vector and definitive) in which the species can survive and by maintaining high prevalences in such hosts. Our concept of how this works is shown in Fig. 1 where the larger, darker spheres represent a greater hypothetical probability of extinction than the smaller, lighter spheres. The best hedge against metapopulation extinction would be to have large numbers of intermediate hosts/vectors and definitive hosts (line A). (Note however, there is always a finite probability of extinction.) Even when there are fewer intermediate hosts than definitive hosts (line B), the probability of extinction is still less than a scenario with very few intermediate hosts coupled with many definitive hosts (line C). Clearly, different ratios of

/”

A

.

..:

..’

C ___

Few

a Many

Number and prevalence of definitive hosts

Fig. 1. Host specificity as a hedge against extinction: hypothetical probability for the extinction of a parasite metapopulation. The larger and darker the sphere, the greater the likelihood of becoming extinct. Examples are hypothetical and for comparative purposes only, no inference should be drawn from the actual size or shading of the spheres. For clarity, we have varied only the number of intermediate hosts. Recognize that there is a probability for extinction anywhere within the axes.

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intermediate hosts and definitive hosts would result in the spheres being located anywhere within the axes and there may well be situations where the number of intermediate hosts would outnumber the definitive hosts (a feature we have omitted for clarity). For one-host parasites, only some variation (i.e. number of definitive hosts) on line C would be appropriate. A good example of the importance, for a parasite, of being a host-generalist can be seen in the parasites of puma (F&s concolor). Originally, this host was the most widely distributed native mammal in the New World. The puma has been extirpated throughout much of its former range and now occurs in highly fragmented populations (Anderson, 1983). The smallest (estimated population size of 20-50 animals) and most isolated (>lSOO km to the next nearest population) population is that in remote areas of southern Florida. In an examination of 7 animals, Forrester, Conti & Belden (1985) found 13 different endohelminths. Eleven of these could be identified to species and are found in a range of other, more common hosts. (Even the 6 species of ticks found on the puma are found on one or more of horses, feral pigs or white-tailed deer.) Clearly, if there were a parasite species specific to puma, it would be a prime candidate for a metapopulation extinction in this population. A second example is the parasite population found in a host species on the verge of extinction. The black-footed ferret (Mustela nigripes) had an estimated population of >I/2 million individuals in 1920. Today, it is considered the most endangered mammal in North America, is thought to be extirpated in the wild and survives only as a captive population of c 20 animals (Clark, 1987). Prior to their extirpation in the wild, Boddicker (1968) examined 7 animals and found only the nematode Molineus mustelae, normally a parasite of weasels, present. Two ectoparasites, a tick and a flea, found on the pelage of black-footed ferrets are common on other sympatric mammals. Similar to the example on pumas noted above, were there any parasites specific to the ferrets, those parasites (in this case it would be the suprapopulation) would be excellent candidates for global extinction with the final demise of the ferrets. Host capture

A requisite of becoming a host-generalist is to acquire additional hosts. The term host capture has been used in several ways; here, we use it to mean the acquisition, by a parasite or parasite group, of a host or host group not normally associated with it.

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By this simple definition, host capture is a hedge against extinction. We do caution that host capture is not an immediate process (i.e. a parasite does not simply colonize a new host species because the population of its regular host is diminishing). For example, when the phylogenetic distance between normal and acquired host is great [e.g. birds and mammals acquiring tetrabothriid cestodes from fish (Hoberg, 1987)], the process requires evolutionary time. The cestode genus Bothriocephalus is quite speciose and is typically parasitic in fishes. Some species (e.g. B. acheilognathi) have an extremely broad host range. Others appear to have a narrower range, but always in fishes. Recently however, Scholz & Moravec (1990) reported B. claviceps, a specialist in eels, in the newt, Triturus vulgaris. Curiously, one species, B. rarus, is a common parasite in red-spotted newts, Notophthalmus viridescens in North America (Jarroll, 1980) and has not been reported from fishes (Schmidt, 1986). This appears to be an example of capturing a new host group (Amphibia) by a genus of cestodes that spans the continuum from hostspecialist to host-generalist. The nematode Camallanus lacustris is normally a parasite in perch (PercaJluviatillis). Although it has been reported regularly in eels, A. anguilla, it had not been demonstrated that eels are suitable definitive hosts (Moravec, 1985). Recently, Nie & Kennedy (1991) have shown that eels can maintain a metapopulation of this parasite in a small lake where perch have gone extinct. These observations suggest that the nematode has acquired eels as a definitive host in the absence of a customary definitive host. As a final example of host capture, we use data on the acanthocephalan Pomphorhynchus laevis. This parasite is thought to have originated in Europe, where it is still common. It uses cyprinid fishes as its principal hosts and whichever freshwater species of Gammarus that is locally available as an intermediate host. Occasionally, it is found in brown trout (Salmo trutta). When England was still connected to Europe following the last ice age, Kennedy, Bates & Brown (1989) speculate that P. laevis migrated to the British Isles and split into three races through the capture of new intermediate and definitive hosts. The British strain retains the same final hosts (primarily chub, Leuciscus cephalus, and barbel, Barbus barbus [and it still retains the property of its continental source in being able to infect brown trout on occasion]), as the source population in Europe but requires the amphipod Gammarus pulex as its intermediate host (even though other species of Gammarus are present). Another strain of P. laevis

and marine became marine, using euryhaline amphipods such as G. locusta and G. zaddachi as intermediate hosts and flounder, Platichthysflesus as its definitive host. Both of these strains are thought to have arisen by natural causes. The third strain is the Irish strain, thought to have arisen due to anthropogenic factors (the introduction of nonsalmonids to the island). Once reaching Ireland, P. laevis had to adapt to the local freshwater amphipod G. duebeni (G. pulex, until very recently, was absent), and to the overwhelming abundance of salmonids. In Ireland, it is now considered specific to brown trout and salmon, S. salar. In each of the above ‘strains’ we see evidence for capturing new intermediate and/or definitive hosts. Rapid evolutionary rates

We now know that some parasites are capable of rapid evolution when they are exposed to naive hosts. This appears to be a major mechanism allowing for host generalizing via host capture. [But see Jaenike (1993) who suggests that host specificity may be an alternative outcome of rapid evolution]. Under laboratory conditions, Lichtenfels (1971) has shown that the nematode Nippostrongylus brasiliensis changes phenotype after 150 generations in a different host species. He demonstrated that parasite strains adapted to hamsters (Mesocricetus auratus) differed significantly in several morphological details from strains maintained in the normal rat host (Rattus norvegicus). From an evolutionary perspective, his most significant finding was that of no difference in egg production between the two strains even though the female worms of the hamster-adapted strain were smaller. The immune response develops more quickly in hamsters than in rats and the parasites seem to overcome that obstacle by spending less time and energy on somatic growth (hence the smaller adult parasites in hamsters). Lichtenfels (1971) concludes that “. . . evolution of genetically divergent populations can occur in a very short time.” Fasciola hepatica and F. gigantica typically use the snails Lymnaea truncatula and L. auricularia (or subspecies of these 2) as intermediate hosts. When the parasites were introduced outside of Europe, for example to Australia, the native Australian L. tomentosa was a fully suitable host for both species of parasite. Boray (1966) notes that L. tomentosa now serves as the sole intermediate host for F. hepatica in Australia and that it is a better host for the Australian strain of F. hepatica than it is for the European strain. Based on these data, he suggested that a new flukesnail relationship could evolve rapidly.

Hedging your bets against extinction Hymenolepis diminuta is a parasite with many purported strains. Using enzyme isoelectric focusing, Dixon & Arai (1991) have shown a genetic basis for several strains. Comparing a Japanese strain collected from Rattus rat&s with a laboratory strain maintained in R. norvegicus, Kino and Kennedy (1987) note the Japanese strain showed a “. . . relative genetic incompatibility with R. norvegicus . . .“. In addition to strain differences in the definitive host, they also noted differences in the adaptation of the two strains to intermediate hosts. Schom, Novak & Evans (1981) compared, directly, heretability data on H. citelli in its intermediate host, Tribolium confusum, by examining infection parameters after 3 years and again after 5 years. (The two year interval was equivalent to approximately 16 generations of the parasite.) They found that intermediate host mortality was lower after 5 years (67 vs 93% with the earlier generation). In contrast, mean population size surviving to 15 days decreased from 14.1 cysticercoids/beetle in the earlier generation to approximately 7 cysticercoids/beetle in the later generation. They conclude that the changes were the result of high selection pressure, by T. confusum to reduce high infectivity of H. citelli and thus improve intermediate host survivorship. Progenesis

In the platyhelminths, the act of progenesis appears to be a good hedge against extinction. Among the Digenea, it appears to be quite common in the family Microphallidae but has also been reported in other families (e.g. Macroderoididae, Lecithiodendriidae, Hemiuridae). In Cestoda, the process has also been reported in a number of families (e.g. Caryophyllidea, Davaineidae, Hymenolepididae). The process is similar between the two groups but with a greater likelihood that digeneans will become progenetic in invertebrate intermediate hosts and cestodes will become progenetic in vertebrate intermediate hosts. Our concept of progenesis is that it represents an abbreviated life cycle which can serve to perpetuate a parasite in those instances where the definitive host (s) is (are) absent. Grabda-Kazubska (1976) identified an interesting pattern of what appears to be an evolutionary process of life cycle abbbreviation among some plagiorchid digeneans. Paralepoderma cloacicola has a typical 3-host cycle involving the freshwater snail, host, Planorbis planorbis, as first intermediate tadpoles as second intermediate hosts and aquatic snakes as definitive hosts. Others, (e.g. P. brumpti), use a mollusc as first intermediate host with the parasite maturing and producing viable eggs in

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tadpoles. Metacercariae fed to snakes do, however, excyst and produce viable eggs. A final abbreviation in this genus is seen in P. progeneticum. In this stages, including the species, all developmental metacercariae, occur in the snail. It is the pattern exhibited by P. brumpti that seems to offer the best hedge against extinction. In the absence of a suitable definitive host, the cycle can be maintained as a 2host system. In the presence of a suitable definitive host, the parasite can take advantage of such a host for cross-fertilization and for dispersal. Font (1980) has noted a similar pattern for species of Alloglossidium. Alloglossidium corti has a typical 3-host life cycle similar to P. cloacicola, A. renale has eliminated the vertebrate definitive host similar to P. progeneticum and A. progeneticum shows an intermediate pattern as does P. brumpti in the case of A. progeneticum, however, it is unclear if the vertebrate host can be dispensed with completely because of the presence of a metacercarial cyst. Font (1980) speculates that dispersal from the crayfish may be accomplished through predation by a vertebrate or by death and decomposition of the crayfish. In the latter case, the ability to cycle in the absence of a vertebrate definitive host is also an example of reducing the probability of extinction. One example of progenesis in a cestode is particularly germane to our arguments. Janicki (1930) noted that Amphilina foliacea a parasite in sturgeon, Acipenser spp., lives in, and becomes gravid in, the body cavity, is unsegmented, has only one set of reproductive organs and has only one intermediate host (a crustacean). Janicki proposed that the reproductive stage now found in sturgeons was once a plerocercoid (e.g. the sturgeon served as a second intermediate host) that was infective to some predator. Prior to the extinction of that predator (Janicki reasoned it was a large, piscivorous Mesozoic reptile), A. foliacea became progenetic in the body cavity (an unusual location for a gravid cestode) of its former second intermediate host. Dubinina (1964) examined life history patterns of cestodes in the family Ligulidae and presents data that suggest how parasites might become progenetic and obviate the need for an obligate definitive host. She found that Ligula intestinalis and L. colymbi, unlike most other pseudophyllideans, have an extremely long developmental period (>425 days and >365 days, respectively) in the second intermediate (fish) host, and an extremely short life span (2-5 days and 4-7 days, respectively) in the definitive host (aquatic bird). Another ligulid, Schistocephalus solidus, survives in its bird definitive host for ~100 hrs. Dubinina attributes the long development time

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in the second intermediate host as a consequence of the considerable growth and development that takes place. In fact, when infective to the definitive hosts, ligulids are essentially full-grown and organ development is complete. She notes “According to the extent of development of their genital system the plerocercoids of Ligulidae, especially of the genus Schistocephalus, when capable of invasion, are nearing the progenetic stage”. It appears that the bird hosts of these ligulids are more important for dissemination in space rather than in time and the parasites might be evolving towards the loss of their current definitive host. An alternative hypothesis, not considered by Dubinina, is that the long developmental stage in fishes might be an adaptation against possible temporal extinction because of the migratory nature of its bird definitive host. High reproductive potential

High fecundity has long been held as a characteristic feature of most parasites and, whether it is an adaptation to a purportedly difficult life cycle, or a consequence of living in an energy rich environment (e.g. Jennings & Calow, 1975), the functional result is massive numbers of offspring. Production of large numbers of eggs or larvae is one method by which the reproductive potential may be increased. For example, some cestodes may produce between 50 million and 150 million eggs/year (Rogers, 1962), female ascarids may produce >200,000 eggs/day (Rogers, 1962); female acanthocephala may produce >250,000 eggs/day (Kates, 1944). Additional features, common to many platyhelminths, are their ability for asexual proliferation and their almost universal tendency towards hermaphrodism. Among the Digenea, all species exhibit some form of asexual reproduction in the first intermediate host. Although not as widespread in Cestoda, asexual reproduction does occur in the intermediate hosts of some (e.g. the taeniids, mesocestoidids). It is important to remember that more than merely representing an increase in the number of infective stages, the process is actually an amplification of a successful genotype. Being hermaphroditic can be viewed as both a hedge against extinction and as a possible route to extinction. It acts as a hedge because each individual can be viewed as a propagule. If any given patch has a probability of colonization, it seems reasonable that such a probability will be higher for one individual colonizer than for two. However, by its very nature, such a propagule would represent the epitome of a “founder effect” with all of its attendant ramifications of low genetic diversity for facilitating extinction.

PREDICTIONS AND CONCLUSIONS Unlike the concerns expressed by Sprent (1992), it should be clear that we are not too worried about the extinction of parasite populations and communities. We acknowledge that infrapopulations and infracommunities become extinct frequently, but the argument is trivial. We do not see any evidence that component communities are in any danger of being lost. This is largely however, a semantic argument. As both Bush (1990) and Kennedy (1993) have noted, component communities might be characterized by having an alternation of guilds or a fixed number of niches. As such, we might expect similar, derived measures of community richness and diversity between component communities, with no reference to parasite species’ identity. This is a somewhat novel approach and most of us are not accustomed to thinking of our data in such terms. We therefore do not know how utilitarian those ideas might prove. But in terms of parasite species composition, there can be no expectation that the component level of community organization should include precisely the same species. In fact, it is the variance in patterns of species’ presence and absence that stimulates much debate in ecological parasitology (e.g. Kennedy & Bush, 1994). We are therefore left with considering parasite extinction at the two higher levels of populations and at the level of the compound community. Suprapopulations are extremely complex involving virtually all stages (free-living or parasitic) in all hosts (intermediate, vector, paratenic or definitive). It is clear that mass extinctions of hosts would result in the loss of suprapopulations but we think it highly unlikely that host fragmentation, in the absence of host extinction, could achieve such a result. We can find no data that even hint at such a possibility. Since compound communities are composed of suprapopulations, it follows that their extinction is even less likely. By default then, we are left with predicting that if some level of parasite were to become extinct because of host fragmentation, it would be a local parasitic metapopulation. What form would such an extinction take? First, we believe that the parasite species must not be capable of direct transmission between mother and offspring. Otherwise, host fragmentation would be insufficient to cause extinction. Second, we believe the parasite would have to be extremely specific to the definitive host involved in the life cycle. To be specific to only one might allow for the other hosts to maintain the parasite until the specific host was again available (e.g., a rescue effect). Related to this, a parasite with long-lived infective stages in intermediate hosts (i.e.,

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Hedging your bets against extinction ‘resting stages’) would act as a hedge against extinction allowing the parasite to await the return of an appropriate definitive host. (Alternatively, in a one host system such as in some Nematoda, resting stages such as eggs might provide a bridge to the reappearance of the required host). Finally, embedded in being host specific is that the host should be phylogenetically distant from sympatric species. A good example of a parasite that seems to fit most of the criteria for extinction is the cestode Haplobothrium globuliforme in the bowfin, Amia calva. We consider this a particularly good example for several reasons. The parasite is clearly unique and thus not subject to possible taxonomic confusion, a strong possibility when suggesting extinction where conspecific parasites exist. Also, bowfin have a very wide distribution in eastern North America (Burgess & Gilbert, 1978) and their parasites have been examined from a number of geographic areas (Aho, Bush & Wolfe, 1991). Most studies on bowfin report the presence of H. globuliforme. Where the bowfin has been examined, most other possible definitive hosts have been examined and thus the absolute specificity of the cestode for bowfin has been established. Bowfin are clearly fragmented in distribution and, because they exist in a number of small lakes and streams, the opportunity for local extinction of the cestode metapopulation is a distinct possibility. But again, in the absence of the complete extinction of bowfin, global extinction seems unlikely. Sprent (1992) is concerned that host declines due to fragmentation of their populations could lead to the extinction of parasites (see also R&a, 1992). We do not see this as a likely scenario. When it does occur at the metapopulation level, the rescue effect from source populations seems sufficient to ensure re-colonization thus preventing global extinction. Although data on extinction of hosts is well documented in the extant literature, we rarely find evidence that parasites have become globally extinct (but see Stork & Lyal, 1993). We do acknowledge that this latter feature may be a function of sampling (e.g. the lack of before and after studies, the inability to study rare hosts) and we thus see why Sprent was pessimistic. We do not share that pessimism however; we have more faith in the ability of the parasites to hedge their bets. authors thank Drs Ian Beveridge and Peter Boreham, Co-editors of this special issue in honour of Prof. Sprent, for the invitation to provide our admittedly speculative ideas. The research of C.R.K. is supported by the University of Exeter and that of A.O.B. by Operating Grant No. 8090 from the Natural Sciences and Engineering Research Council of Canada.

Acknowledgements-The

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