Patterns in helminth communities in freshwater fish in Great Britain ...

Parasitology (1988), 96, 519-532

519

With 1 figure in the text

Patterns in helminth communities in freshwater fish in Great Britain: alternative strategies for colonization G. W. ESCH 1 *, C. R. K E N N E D Y 2 ! , A. 0 . BUSH 3 and J. M. AHO 4 1 Department of Biology, Wake Forest University, Winston-Salem, N. Carolina 27109, USA 2 Department of Biological Sciences, The University, Exeter EX4 4PS, UK 3 Department of Zoology, Brandon University, Brandon, Manitoba R1A 6^49, Canada 4 Savannah River Ecology Laboratory, University of Georgia, Drawer E, Aiken, South Carolina 29801, USA (Accepted 19 November 1987) SUMMARY Examples of the apparently stochastic nature of freshwater fish helminth communities illustrating the erratic and unpredictable occurrence and distribution of many species are provided for six species of fish from several localities throughout Britain. By focussing on parasite colonization strategies two categories of helminths are recognized: autogenic species which mature in fish and allogenic species which mature in vertebrates other thanfishand have a greater colonization potential and ability. Three groups of fish are distinguished: salmonids, in which helminth communities are generally dominated by autogenic species which are also responsible for most of the similarity within and between localities; cyprinids, in which they are dominated by allogenic species which are also responsible for most of the similarity within and between localities; and anguillids, whose helminth communities exhibit intermediate features with neither category consistently dominating nor providing a clear pattern of similarity. Recognition and appreciation of the different colonization strategies of autogenic and allogenic helminths in respect of host vagility and ability to cross land or sea barriers and break down habitat isolation, and their period of residence in a locality, whether transient or permanent, provides an understanding of, and explanation for, the observed patchy spatial distribution of many helminths. Comparison with other parts of the world indicates that colonization is a major determinant of helminth community structure.

INTRODUCTION

Previous attempts to detect and explain patterns in helminth communities in freshwater fish in Great Britain have achieved very limited success due, at least in part, to the erratic and unpredictable occurrence and distribution of many parasite species. Physico-chemical features of the habitat (Chubb, 1970; Kennedy, 1978a) and host geographical range (Price & Clancy, 1983) have been shown to have some influence on helminth community richness, but the source of much of the variation in community structure and composition still remains unexplained (Kennedy, 1981). Helminth communities in the same species of fish often show low degrees of similarity in composition, numbers and dominance between localities: they appear to be stochastic assemblages with many vacant niches. Accidental or chance introductions and colonization events appear to play a major role in determining their composition and in filling in the niches (Kennedy, 1981, 1985; Kennedy, Laffoley, Bishop, Jones & Taylor, 1986). * Arrangement of authors' names was determined by random draw and does not imply seniority. t Reprint requests to C. R. Kennedy.

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In several respects they are very different from helminth communities in birds, which are richer, more diverse and more predictable (Kennedy, Bush & Aho, 1986). In the present paper, further examples of the stochastic nature of freshwater fish helminth communities in Britain are provided. By taking a more holistic approach and focusing on colonization strategies, we seek to understand and explain patterns in communities of helminths in freshwater fish in Britain. We then discuss the wider applicability of the findings and conclusions. MATERIALS AND METHODS

Before proceeding further, an explanation of the concepts and terminology employed is warranted. Parasites may use fish as definitive or intermediate hosts. Amongst the latter set are two types: those that use fish as both intermediate and definitive hosts and those that use fish as intermediate hosts only. These latter mature in vertebrates other than fishes, generally in birds or mammals. They are capable of being moved relatively easily by their definitive host from one aquatic locality to another: these we refer to as allogenic species. All the remaining species, which mature in fish, we refer to as autogenic species. The terms allogenic and autogenic are used as defined by Lincoln, Boxshall & Clark (1982). Autogenic species can thus only colonize new aquatic localities by the natural migration, or human assisted movements, of fish and/or invertebrate intermediate hosts harbouring intact parasites into the new localities. Allogenic species may colonize this same way, or in contrast, by the liberation of helminth eggs from birds or mammals into new localities. We also distinguish two groups of hosts for autogenic species; euryhaline hosts and stenohaline hosts. We further consider two groups of definitive hosts which harbour allogenic helminths in any particular locality: some may be transients, whose stay in the locality is brief and temporary; others are residents, whose stay is longer and more permanent. Despite the large quantity of survey data available in the literature, few studies provide information on individual hosts and instead only present sample summaries of infection parameters. For analyses of community composition and similarity, data on individual hosts are essential. Precise enumeration of all parasites is also a requisite for our analyses, but some published studies do not list actual numbers of very common parasites such as digenean metacercariae. It was thus generally necessary to rely on data sets collected by one of us (C.R.K.). Where data from other sources have been used, they are indicated as such. Use of our data had the advantage of ensuring taxonomic consistency, comparability and completeness in the treatment of samples. All samples were taken from Britain as its small size and isolation made it possible to obtain a fairly wide geographical and topographical coverage. Whilst the fish helminth fauna is restricted in composition, it is well known. Adult fish of 6 species, representing 4 families (Salmonidae, euryhaline: Cyprinidae, stenohaline: Percidae, stenohaline: and Anguillidae, euryhaline), were examined. Wherever possible, a sample of at least 10 and more often > 20 fish of each species was taken from each locality during the summer months. Fish were captured by appropriate methods, including traps, seine nets, gill nets and electro-fishing. Details of locations, sample size and parasite composition are given in Tables 1-6. Fish were examined as soon as possible after capture: the whole fish including eyes, skin and gills, but excluding the blood system, was searched for parasites using standard methods. The investigation was concerned only with helminths and all individuals of all species were counted. To describe helminth communities in each fish species at each locality, we used the

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Characteristics Number of fish examined Total no. of helminth species No. of autogenic species No. of allogenic species Total no. of helminth individuals Proportion of autogenic individuals Proportion of allogenic individuals Berger-Parker dominance index Character of dominant species { Identity of dominant species§ Mean % similarity between individual fish (autogenic spp.) Mean % similarity between individual fish (allogenic spp.)

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SW, Southwest England; S, South England; N, North England. Taken, with permission, from unpublished reports (Stewart, 1973). AL, allogenic species; AU, autogenic species. Ds, Diplostomum spathaceum; Tc, Tylodelphys clavata; Al, Acanthocephalus lucii.

similarity index Cxy = E^min (pXi,pyi), where pxi = xJX, the proportion of species i in community X, and pyi = YJY, the proportion of species i in community Y (Hurlbert, 1978), which measures the minimum proportion of overlap in the numbers of individuals of the same species between two communities. For each species of fish in each locality, the percentage similarity between each pair offish in a sample was determined separately, and the mean of all possible pair combinations was obtained. This procedure was carried out for autogenic and allogenic species separately. Comparison of community similarity between localities was carried out in a similar manner, resulting in a mean value for each pair of localities. This procedure was also followed separately for autogenic and allogenic species. Since our intent is to focus on similarity, and to be meaningful that similarity must be calculated between each pair of fish, the derived data (mean percentage similarity) which form the basis of our study are not independent. This has the advantage that we are using the best measure of similarity available, but it has the disadvantage that we are unable to test for significant differences in variance, since the most basic assumption of a statistical test is that samples be independent. We are unaware of any significance test(s) that allow this assumption to be violated.

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* SW, Southwest England; N, North England; E, East England; C.I., Channel Islands. t AU, autogenic species; AL, allogenic species. X Pt, Paraquimperia tenerrima; By, Pseudodactylogyrus sp. (species not yet determined but all individuals are considered to belong to the same taxon). Ac, Acanthocephalus clavula; Be, Bothriocephalus claviceps, Bs, Biplostomum spathaceum; Et, Echinorhynchus truttae.

Characteristics Number of fish examined Total no. of helminth species No. of autogenic species No. of allogenic species Total no. of helminth individuals Proportion of autogenic individuals Proportion of allogenic individuals Berger-Parker dominance index Character of dominant speciesf Identity of dominant speciesj Mean % similarity between individual fish (autogenic spp.) Mean % similarity between individual fish (allogenic spp.)

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Table 6. Characteristics of the helminth parasite communities of eels

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Colonization and

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RESULTS

When helminth communities in each species offish in each locality are compared, it is apparent (Tables 1-6) that there is considerable variation in all the parameters measured. Brown trout, Salmo trutta, may harbour (Table 1) as few as 3 or as many as 9 species of helminths, and the proportion of allogenic species may range from 0 to 50%. In the majority of localities, the proportion of autogenic species exceeds that of allogenic, but in Malham Tarn the two occur in similar proportions. In Dunalastair reservoir, allogenic species form a greater proportion of individuals in the communities although there are collectively more autogenic species. The dominance also varies, from 0-42 to 0-96, but in only two localities are the communities dominated by an allogenic species. The remaining localities are dominated by an autogenic species, although the species identity may vary. In all localities except Dunalastair, it is the autogenic component of the communities that confers the greatest degree of similarity between individuals. In general, brown trout helminth communities appear to be characterized by the dominance of autogenic species and individuals, although this pattern, the richness of the community, and the identity of the dominant species can change from locality to locality. The cyprinids (roach Rutilus rutilus, dace Leuciscus leuciscus and bream Abramis brama) and the percid (perch Perca fluviatilis) can be considered together as they exhibit many features of helminth community structure in common. Species number is again variable from locality to locality (ranges 1-7, 8-9, 2-8 and 1-5 for roach, dace, bream and perch respectively, Tables 2-5). However, in the case of roach and dace, the proportion of allogenic individuals greatly exceeds that of autogenic in all localities. In perch this is true of all localities except one, and in bream it is true of two of the four localities. Dominance follows an identical pattern. All the roach localities, except one, and all the dace localities are dominated by the same allogenic species, Diplostomum spathaceum. This species also dominates two of the bream localities and one of the perch's. The atypical roach locality, Swindon Lake, is dominated by another allogenic species, Tylodelphys clavata, as are the remaining perch localities. The atypical perch locality, the Leeds and Liverpool canal, is uniquely dominated by an autogenic species. In all roach and dace localities and in all bar one (each) bream and perch localities it is the allogenic component of the community that contributes most towards the similarity between individual fish. Only two samples of chub, Leuciscus cephalus, and of gudgeon, Gobio gobio, could be obtained so data are not included in the tables. However, the helminth communities in both species showed characteristics similar to those in other species of cyprinids in that the allogenic component of the communities contributed more to similarity within each locality. In general, therefore, helminth communities in cyprinids and the percid appear, in constrast to those in trout, to be characterized by the dominance of allogenic species and individuals, and often by one particular species of helminth. Eels, Anguilla anguilla, also harbour a variable number of helminth species (Table 6). In no localities were there more allogenic species than autogenic ones. In all localities except one (Shobrooke), the proportion of autogenic individuals exceeded that of allogenic. All localities, with two exceptions, were also dominated by an autogenic species, the identity of which varied. The only allogenic species found in eels at all was D. spathaceum, the same species that dominates cyprinid helminth communities, and this species was dominant in two localities. Similarity between individual fish in most localities was due primarily to autogenic species, but in a few to allogenic species.

527

Colonization and helminth communities 100

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Fig. 1. Summary of matrices of percentage similarity index comparisons of helminth fauna of each species of fish between localities. The horizontal lines indicate the median percentage similarities, the boxes enclose the 25 and 75% quartiles, and the vertical lines indicate the range. The numbers refer to the number of paired comparisons: in the case of dace, there are too few comparisons for the quartiles to be meaningful.

Overall, eel helminth communities are less predictable than those of trout and cyprinids. They exhibit intermediate features in that autogenic species and individuals are usually more common, but there is no consistent dominance by either autogenic or allogenic species. The results from comparing helminth communities within each species of fish between all localities separately for autogenic and allogenic species are summarized in Fig. 1. In brown trout, both the median and range of similarities are greater for autogenic species. Moreover, this component confers greater similarity between localities than does the allogenic component. By contrast, for the three cyprinid species and perch, both the median and range of similarities are greater for allogenic species and this component provides more similarity between localities than does the autogenic component. Chub and gudgeon also conform to this pattern. Eels again occupy an intermediate position; median similarity is higher for autogenic species but the range is wider for allogenic species. The difference in similarity between the autogenic and allogenic components is marginal. Comparison of community similarities between localities thus confirms the conclusions reached by comparing similarity within localities. There are three groups of fish: trout, where most similarity within and between localities is due to autogenic species; cyprinids and perch where it is due to allogenic species; and eels, where neither component consistently dominates the community nor provides a clear pattern of similarity.

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DISCUSSION

No-one is likely to dispute the contention that colonization plays an important part in structuring helminth communities. However, the erratic pattern of occurrence and distribution of helminth species, and the resulting variability in community composition and organization exemplified by the parameters shown in Tables 1 6 , often make interpretation and recognition of patterns in community structure very difficult. Factors such as the physico-chemical characteristics of a locality (Chubb, 1970), and especially its size (Kennedy, 1978a), and the geographical range of the host (Price & Clancy, 1983) may influence the composition of helminth communities in any specific host in any particular locality, and their importance and that of factors such as host vagility and diet have been discussed by us elsewhere (Kennedy et al. 1986). The effect of some factors such as the density of other potential host species on the number of parasites in a community is still unknown, and would be exceptionally difficult to determine. The effect of others, such as the possibility that the position of the host in the food chain is an important determinant of community structure, can be discounted in the present study, since all the six species offishexamined feed on invertebrates all through their life and three species, trout, perch and eels which belong to three different groups in our analysis (Fig. 1) feed on fish in addition when large (Maitland, 1972). Thus, an attempt has been made to minimize the influence of other factors by choice of host species and locality. More importantly, perhaps, we are here attempting to examine patterns on a broad scale and one that subsumes the influence of these other factors, whilst recognizing that some of the variation in our data can almost certainly be attributed to them. In attempting to understand patterns in helminth community structure, it is important to distinguish between colonization potential and colonization ability. The superior colonization potential of allogenic species may not always be realized and turned into ability. This is because (1) allogenic species may be introduced into a locality by transient hosts which have less time and opportunity to seed the locality with eggs than resident hosts; and/or (2) the opportunity for successful introduction of a new parasite into a locality may be very limited as a consequence of the very short periods when transmission of the parasite to its next host or stage is possible, i.e. when transmission windows are very narrow (Tinsley & Earle, 1983; Kennedy, 1987). Parasites introduced by transient hosts may miss the window, whereas those introduced by residents will have a greater opportunity of encountering it. A narrow transmission window at any stage of the life-cycle may thus be sufficient to minimize, or possibly preclude, the probability of colonization. Colonization of course also requires the requisite population densities of all necessary hosts in the locality. Despite these constraints, it should be obvious that allogenic species are likely to have greater colonization potential than autogenic species. These latter can only colonize as a result of the movement of a whole freshwater host, fish or invertebrate, with its parasites from the original locality to a new one. This requires crossing barriers such as the land and sea. It is thus entirely unsurprising to find in so many fish species that similarity in helminth communities between fish within, and between, localities is due to allogenic species, since the greater vagility of their hosts allows allogenic species to exploit their greater colonization potential. In many instances, however, allogenic species also show a patchy and erratic distribution (Tables 1-6), but this may often be related to the transient nature of their definitive hosts or to the distances they have to cover from the source to the colonization site, or to both.

Colonization and helminth communities

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A good example of this patchy distribution is the colonization of Slapton Ley, an isolated lake in southwest England. The lake attracts large populations of several species of both migratory and transient birds. Despite this, the fish helminth community remained unchanged for many years. However, within one year of the arrival of a pair of resident great-crested grebes, Podiceps cristatus, two allogenic species successfully colonized the lake, followed three years later by a third species (Kennedy, 1985). Two of these species subsequently colonized Widdecombe Ley, 7 km distant, within a year of their establishment in Slapton Ley (Kennedy, 1985; Kennedy, unpublished observations). When an allogenic species exhibits little specificity to both definitive and second intermediate hosts and can therefore be introduced by either transients or residents easily, its colonization potential will be high and its distribution should be widespread. This is the case with Diplostomum spathaceum: this species dominated most of the cyprinid helminth communities studied (Tables 2-4) and was responsible for most of the similarity between them. In some localities it also dominated trout, perch and eel helminth communities (Tables 1, 5 and 6). By contrast to these allogenic species, we predict that autogenic species, because of their more limited colonization potential, would be even patchier in distribution and more erratic in occurrence. The findings from cyprinids and percids (Tables 2—5) that autogenic species contribute little or nothing to helminth community similarity between, and within, localities are in accord with this prediction. In trout, however, autogenic species were generally the dominant element and responsible for most of the similarity within, and between, localities (Table 1). This appears to relate in part to the euryhaline and anadromous nature of the fish. Helminths able to tolerate variable salinity are likely to be more widespread as they stand a better chance of being introduced into new localities by fish straying when returning to freshwater, and it is often these marine tolerant helminths that are responsible for such similarity. For example, the most common autogenic species in charr, Salvelinus alpinus, in Northern Norway and its Arctic islands is frequently Eubothrium salvelini (Kennedy, 19786). This species is able to tolerate the short periods of marine residence of its hosts (Kennedy, 1978c). Because of this, it is found in charr at the extreme limits of the fish's geographical range (Chubb, 1970; Conneely & McCarthy, 1984; Hoffman, Kennedy & Meder, 1986), and it confers a substantial measure of similarity between the autogenic component of the helminth community in different localities (Kennedy, 19786). The related species, E. crassum, may make a similar contribution in trout helminth communities where it is widespread in trout as in Northern Norway (Kennedy, 1978a, c). In Britain, many localities no longer harbour anadromous salmonids and therefore the dominant autogenic species in trout is far more variable (Table 1). The identity in Britain of the dominant autogenic species in trout must thus largely reflect chance introductions and stochastic processes. Hence, the degree of similarity between the helminth communities in different localities is far lower than in species such as roach which are dominated by a single common and widespread allogenic species. Autogenic species in eels do not confer the same degree of similarity as is the case with trout, neither do allogenic species dominate to the same extent as in cyprinids and perch. We interpret this intermediate position in eels as being the result of two different features of their biology (1) they are catadromous, thus showing features similar to other euryhaline species such as trout; and (2) the adults can cross both terrestrial barriers, to a limited extent, and estuarine barriers and thereby reduce or eliminate the isolation characteristic of most stenohaline species. PAR 98

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Patchiness within the autogenic components can also be increased by hosts acquiring elements of the parasite fauna of the dominant vertebrates in a locality (Dogiel, 1964). For example, in the west of Ireland, trout, pike Esox lucius, and eels in Lough Corrib harbour Camallanus lacustris acquired from perch, while pike harbour Diphyllobothrium sp., Cucullanus truttae and Cystidicoloides tenuissima, all salmonid parasites acquired from trout (Conneely & McCarthy, 1984). Movement offish for stocking purposes may further enhance patchiness; the patchy distribution of Bothriocephalus acheilognathi, for example, is due almost entirely to stocking programmes of fish (Andrews, Chubb, Coles & Darsley, 1981). This is also true in North America where the parasite was introduced in the early 1970s (Hoffman, 1980; Riggs & Esch, 1987). Though the present study focusses on the British Isles, we believe that the concepts and conclusions are applicable on a much broader scale. Indeed, their applicability to Norway, for example, has already been demonstrated. Further examples can be found from many parts of the world. The restriction of Ligula intestinalis to the high plateau of southwestern China and its erratic distribution there is believed to be due to the restricted distribution of Larus ridibundus colonies and their small transient range (Liao & Liang, 1987; Liao, personal communication). In South Dakota, USA, the disappearance of resident bird hosts has been shown to be responsible for the local extinction and subsequent patchy distribution of several species of allogenic parasites offish (Hugghins, 1957). In the USSR, rapid colonization of new reservoirs by allogenic species such as L. intestinalis, transported by transient and resident birds, has been documented on several occasions (Bauer & Stolyarov, 1961; Dubinina, 1980). The paucity of allogenic species in eels is evident in the USA (Hoffman, 1967), Canada (Margolis & Arthur, 1979), New Zealand (Hine, 1978) and central Europe (Moravec, 1985). The similarity of the autogenic component of the helminth communities of salmonids is evident in Kamchatka (Konovalov, 1975), and there is a well-documented example in Canada of parasites of salmonid fish dominating all parasite communities in a lake (Leong & Holmes, 1981). On the basis of the present data and the other examples, we believe that colonization is a major determinant of helminth community structure, at least in aquatic ecosystems. Such a conclusion may not at first sight appear to be particularly novel, and it has certainly been foreshadowed and implied in the work of Dogiel (1964) amongst others. These earlier ideas on colonization, however, are largely intuitive paradigms, and they have never previously been quantified or documented in the manner which we have attempted. Perhaps more importantly, our conclusions relating to the different contributions of autogenic and allogenic species to community structure in the three groups offish hosts are novel and unexpected, and are not simply logical consequences of the dispersal abilities of the helminths themselves. An understanding of colonization strategies, therefore, including the separation of autogenic and allogenic species and recognition of the differing roles of both transient/resident and euryhaline/stenohaline host species, provides important clues for evaluating the stochastic nature of parasite community structure. The authors wish to acknowledge the generous financial support provided by the Savannah River Ecology Laboratory which enabled them to meet, discuss and prepare this paper. They also acknowledge their debt to the many people with whom they have discussed their ideas, and especially the valuable contribution from the Parasite Ecology Laboratory at Exeter. The Archie Fund of Wake Forest University supported travel of G.W.E. to the University of Exeter in the spring of 1987, A.O.B. was funded by Grant A-8090 from NSERC Canada, and J.M.A. by contract De-AC0976SR00819 between the US Department of Energy and the University of Georgia's Savannah River Ecology Laboratory.

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R. J., BOXSHALL, G. A. & CLARK, P. F. (1982). A Dictionary of Ecology, Evolution and Systematics. Cambridge: Cambridge University Press. MAITLAND, P. S. (1972). A key to the freshwater fishes of the British Isles with notes on their distribution and ecology. Scientific Publications of the Freshwater Biological Association 27, 1-139. MARGOLIS, L. & ARTHUR, J. R. (1979). Synopsis of the parasites of fishes of Canada. Bulletin of the Fisheries Research Board of Canada 199, 1-269. MORAVEC, F. (1985). Occurrence of endoparasitic helminths in eels (Anguilla anguilla (L.)) from the Macha Lake fishpond system, Czechoslovakia. Folia Parasitologica (Praha) 32, 113-25. LINCOLN,

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