INTRODUCTION
The recognition and emergence of fish parasitology as an essentially ecological discipline can be related directly to the publications of Dogiel et al. (Reference Dogiel, Dogiel, Petrushevski and Polyanski1961) and Dogiel (Reference Dogiel1964). Based on the massive amount of research and surveys that had been carried out on freshwater fishes and their parasites in the then Soviet Union, most of which was until then unknown to western parasitologists, Dogiel (Reference Dogiel, Dogiel, Petrushevski and Polyanski1961) emphasized the relationships between parasite communities and their environment, both biotic and abiotic. This, and the contributions to ecological theory from researchers such as Andrewartha and Birch (Reference Andrewartha and Birch1954) and MacArthur and Wilson (Reference MacArthur and Wilson1967), stimulated a massive growth in interest in the ecology of parasites of freshwater fish over subsequent decades.
Fish are in some respects particularly suitable hosts for studying the ecology of parasites. Many species are very abundant, methods of catching them are well known and so it can often be relatively easy to obtain large samples. Since each individual fish harbours a parasite infrapopulation and infracommunity (this and all definitions as in Bush et al. Reference Bush, Lafferty, Lotz and Shostack1997) it is possible to sample replicate habitats, which in turn permits a rigorous statistical analysis of the data collected. On the other hand, it can be very difficult to test conclusions derived from field studies by controlled infections. Most ecological research on fish parasites has therefore still to be undertaken in the field, and is unsupported by laboratory experiments. It is therefore necessary to adopt the approach of MacArthur (Reference MacArthur1972): namely, to search for patterns that are replicable in time and /or space.
The approach adopted here is to take a retrospective view of developments in research into the ecology of metazoan parasites of freshwater fish over the last half century, in order to identify the important landmarks and publications that have significantly advanced the field. It aims to concentrate on the broader picture and identify major contributions, supported by a few examples, rather than concentrating on details and numerous case studies. Ecology is here taken to mean the study of the factors that influence the distribution and abundance of parasites (Andrewartha and Birch, Reference Andrewartha and Birch1954). Evolutionary ecology is not emphasized as such, as it has been the subject of major reviews by Price (Reference Price1980) and Poulin (Reference Poulin2007a).
MODELS OF HOST-PARASITE SYSTEMS
Early ecological studies, reviewed by Kennedy (Reference Kennedy, Taylor and Muller1970), had focused largely on seasonality of occurrence of parasites in fishes. It became apparent that whilst some species showed a similar pattern of seasonal change in several localities and/or hosts, others did not, but rather showed considerable variation. Thus, the problems arising from the lack of replicability of observed patterns in time and space was evidenced even in these early investigations. Whilst they provided examples of short-term parasite population changes, and thus contributed to an understanding of parasite population dynamics, there was no theoretical basis for predictions against which to evaluate their findings nor were they testing hypotheses.
The first major development in parasite ecology was the recognition by Crofton (Reference Crofton1971a, Reference Croftonb) that parasitism as a life style could be quantified and that host-parasite relationships could be modelled mathematically. An essential factor in both papers was his focus on the role of parasite-induced host mortality and his recognition of the importance of quantifying the distribution of parasites within a population of hosts. Parasites are not normally distributed randomly or uniformly throughout a host population but in an aggregated manner such that a few hosts have very heavy infections whilst others have light infections or are uninfected. The pattern of aggregation can generally be described by the negative binomial model or, more simply, by the variance to mean ratio of parasite abundance in the host population. Departures from an aggregated distribution are known and may be interesting ecologically: for example, a random dispersion might be a consequence of a very low parasite density and a uniform distribution might be evidence of intraspecific competition. The model revealed that inter-related persistence was possible for host and parasite populations and the numbers of hosts and parasites could attain an equilibrium level, either linear or cyclical, under certain conditions and especially if parasite-induced host mortality was density dependent. His recognition that parasites exhibit aggregated distributions has proved to be one of the most important developments in ecological parasitology and it may indeed be the only general law in parasite ecology (Poulin, Reference Poulin2007b).
The importance of aggregation was rapidly recognized by Anderson (Reference Anderson1978), Anderson and May (Reference Anderson and May1978) and May and Anderson (Reference Anderson1978). Crofton's model was essentially deterministic, but they were able to refine and develop a model that treated some of the variables as stochastic. Their conceptual models of host parasite systems focused on the conditions that lead to stability or instability of host-parasite systems and identified the factors that had the potential to regulate the systems or to destabilize them. Aggregation, the operation of density-dependent processes on parasite establishment or reproduction and parasite-induced host mortality, if dead hosts were removed from the system, could stabilize the system; whereas asexual reproduction by parasites, parasite effects on host reproduction and time lags could destabilize the system. These factors could compensate for each other and give parasites the potential to regulate host populations around an equilibrial level or through cyclic oscillations. The balance of the factors in any locality or host-parasite system would determine the population dynamics of the parasite and host, and for the parasite to persist over a long period regulation had to take place. These models provided the much needed theoretical background to parasite population dynamics and, like all good mathematical models, stimulated thinking and generated testable hypotheses.
POPULATION REGULATION AND LONG-TERM STUDIES
The focus of ecological investigations now switched towards testing these hypotheses by identifying the presence and operation of regulatory factors in parasite-fish systems. Aggregated distributions were the norm, but the significance of intra-specific competition and parasite-induced host mortality was unclear. Both field and laboratory studies identified the existence of intra-specific competition in populations of several parasites. Density-dependent establishment and survival of acanthocephalans (Uznanski and Nickol, Reference Uznanski and Nickol1982; Brown, Reference Brown1986) have been demonstrated in fish in the laboratory. Based on field data, Ashworth and Kennedy (Reference Ashworth and Kennedy1999) postulated density-dependent regulation of a nematode population and this was subsequently confirmed in experimental laboratory infections (Fazio et al. Reference Fazio, Sasal, Da Silva, Furnet, Boissier, Lecompte-Finiger and Moné2008). Holmes et al. (Reference Holmes, Hobbs, Leong and Esch1977) suggested that competition through density-dependent effects on parasite reproduction might be regulating the infrapopulations of an acanthocephalan in one of its host species in Cold Lake, Alberta, Canada. Their models predicted that this would be sufficient to regulate the whole suprapopulation if the flow of parasites through this species was sufficient. Later, Kennedy (Reference Kennedy1996) reported intra-specific competition for space between cestodes in a field study. However, demonstrating the existence of intra-specific competition in the field or laboratory is not per se evidence that it actually regulates parasite populations in the field. Parasite-induced host mortality can also often be identified in the field, though it may be very difficult to quantify. Moreover, as Holmes (Reference Holmes, Anderson and May1982) has pointed out, it can be very difficult to determine whether such mortality is additive, which could be regulatory, or compensatory, and which could not. His review concluded that it was generally compensatory in vertebrate hosts, but additive in invertebrate hosts.
Unfortunately, the majority of field studies are of short duration only and so even when regulatory or de-stabilizing factors are detected there is insufficient evidence to show whether the populations are stable or not. Only long-term field studies can provide evidence of stability but there are very few such studies. Smith (Reference Smith1973) showed that a cestode population maintained relatively consistent levels of recruitment and prevalence over 15 years in a population of salmon in a Canadian Lake, but also that the parasite population was very sensitive to climatic, host and habitat perturbations that affected recruitment. Kennedy and Rumpus (Reference Kennedy and Rumpus1977) demonstrated a remarkable degree of stability in an acanthocephalan population in its fish and intermediate hosts for over 9 years. Whilst this might have been due to regulation through intra-specific competition (Brown, Reference Brown1986), it could just as easily reflect the stability of the physico-chemical conditions in a river which was itself very closely regulated by man. In the River Shannon, Ireland, a large and stable river system, acanthocephalan populations persisted in eels for 18 years at remarkably stable levels (Kennedy and Moriarty, Reference Kennedy and Moriarty2002), apart from a temporary decline, due to changes in host movements in the system, which was reversed. No regulatory factors were identified as such, and again the parasite stability could have reflected stability in habitat conditions over the period. In some small and far less stable managed rivers there is evidence of parasite populations in eels changing over long periods with some species being maintained over 13 years only by invasion from other parts of the metapopulation (Kennedy, Reference Kennedy1993) whilst others increased throughout the periods. Large changes in abundance of several parasite species in eels over 9 years resulting from natural introductions of some species and steep declines in populations of others have been detected in another small river (Kennedy, Reference Kennedy1997). These two systems appear to be inherently unstable.
An apparent example of long-term stability in linked parasite and host populations from a small lake in southern England was reported by Kennedy et al. (Reference Kennedy, Shears and Shears2001). Over a period of 32 years, 3 linked cycles of Ligula intestinalis and its host Rutilus rutilus were detected. This would seem to suggest a regulated system as postulated by Anderson (Reference Anderson1978), but there is a paradox in that there was no evidence of any regulatory factors operating. Rather, there was evidence of several destabilizing factors: the parasite deleteriously affected the reproduction of its host; parasite-induced host mortality was density independent and infected fish were not taken out of the system; parasite aggregation was never severe and there were long time-lags in the system. Persistence of this host-parasite system was not the result of any density-dependent compensation. Closer analysis of the data-set indicated that the parasite may not have actually even persisted in the lake at all. At the end of each cycle the host and parasite populations collapsed, and it was suggested that Ligula was re-introduced to the lake as the fish population recovered. Ligula is probably a super tramp (sensuDiamond, Reference Diamond, Cody and Diamond1975) as it is very vagile and is transmitted from habitat to habitat by aquatic birds: it invades a lake, causes severe mortality in its fish host population and is then transferred by birds to another locality. Persistence in this lake was therefore more apparent than real as the 3 cycles were independent and unregulated. This system was inherently unstable but this would not have been apparent from any short-term study that considered only one of the cycles.
Overall, therefore, whilst there is evidence that regulatory factors can operate on fish parasite populations no study has as yet demonstrated convincingly that they play a significant part in stabilizing host and parasite populations around equilibrium levels. Persistence of a parasite population is not evidence of stability, although it may be a consequence of it. It may equally reflect stability of climatic or physico-chemical conditions in a habitat and in none of these long-term studies can the role of these factors as the major determinants of parasite persistence or apparent stability be excluded. Until evidence from more long-term studies is available, the null hypothesis that most parasite populations in freshwater fish are unregulated and unstable must be accepted. This supports the view of Price (Reference Price1980) that parasite populations live in non-equilibrium conditions even if they may appear to be stable, because probabilities of colonization are low and those of extinction are high, whilst resources are patchy and the patches themselves ephemeral.
COMMUNITIES
Richness and diversity
The attempts to identify patterns and processes in communities of parasites have tended to follow the approaches adopted by ecologists studying communities of free-living animals by focusing on the same topics of richness, the niche and inter-specific competition, variability and replicability.
It has long been recognized that parasite component communities differ in richness and diversity both within a host species by locality and between host species within, and by, locality. A review of parasite species richness in a range of examples of fish, reptile, bird and mammal hosts by Kennedy et al. (Reference Kennedy, Bush and Aho1986) identified aquatic birds as harbouring the richest helminth communities and freshwater fish as often harbouring the poorest. They related this poverty to poikilothermy, a poorly differentiated alimentary tract, diet and relatively poor host vagility. They later (Bush et al. Reference Bush, Aho and Kennedy1990) considered that host ecology was a more important determinant of parasite community richness than host phylogeny, and demonstrated that species flocks made relatively little contribution to helminth community richness in parasites of freshwater fish (Kennedy and Bush, Reference Kennedy and Bush1992). A different approach was adopted by Price (Reference Price, Strong, Simberloff, Abele and Thistle1984) and by Holmes and Price (Reference Holmes, Price, Kikkawa and Andersen1986), based on the review by Holmes (Reference Holmes1973) and subsequent studies. They considered that parasite component communities could be arranged along an axis from isolationist communities to interactive communities. All parasite species showed niche selection to a greater or lesser degree, but isolationist communities were species poor and the species were independent of each other. By contrast, interactive communities were species rich, with species co-occurring regularly at densities such that there was often evidence of species packing, and in which species interacted in the present or had done so in the past. Communities could be located anywhere along this continuum, and those of freshwater fish tended to be found towards the isolationist end (see also Poulin and Luque (Reference Poulin and Luque2003) for further discussion of this continuum). The concept of core and satellite species also assisted understanding of the structure of species-rich helminth communities, but cannot be applied to the poorer communities in freshwater fish.
Based on a study of parasites of eels, Kennedy (Reference Kennedy, Esch, Bush and Aho1990) found that infracommunities were species poor and exhibited low diversity, whilst component communities were very variable in species richness and dominated by generalist species in the habitat. The structure of such infracommunities suggested the influence of stochastic factors: there were empty niche spaces, individual infracommunities were dominated by different species and there was a great deal of variation between them. Each fish appeared to be an independent sampler of the parasites available and evidence for interactions was very weak. Overall, he concluded that most helminth communities in fish can be considered isolationist in nature and to be essentially stochastic assemblages rather than structured communities.
Niche and inter-specific competition
Studies on the ecology of free-living species, focusing on the niche, inter-specific competition and community diversity and replicability, have provided a theoretical background for the study of parasite communtities. The position and distribution of parasites on gill arches or along the alimentary tract of their host can be measured fairly precisely, and this has been widely accepted as an index of the niche of each species. It is thus possible in single species infections to determine the fundamental niche of any species, and in multiple species infections to measure the realised niche of each species in the infracommunity. Ecological theory suggests that inter-specific competition operates at the infracommunity level and could be evident as a niche shift by one or more species in the presence of a suspected competitor i.e. a functional response. Evidence for inter-specific competition can also come from a numerical response, when infrapopulations of one or more species decline in the presence of another i.e. there are strong negative associations between the species.
Theoretical considerations based on mathematical models (Dobson, Reference Dobson1985) suggested that inter-specific competition should be uncommon in nature since each potential competitor would be likely to exhibit aggregated distributions in its host population. Therefore, the probability of any two species occurring at high densities in the same host individual infracommunity would be low and would decline as the levels of aggregation increased. Nevertheless, functional responses have been reported from the field between a species of acanthocephalan and a cestode (Chappell, Reference Chappell1969; Grey and Hayunga, Reference Grey and Hayunga1980) in the alimentary tract of fish, between species of larval digeneans in the eyes of perch (Kennedy, Reference Kennedy2001a) and they have also been demonstrated between two species of acanthocephalan in laboratory infections (Bates and Kennedy, Reference Bates and Kennedy1990). Numerical responses have been observed on many occasions in field investigations e.g. by Vidal-Martinez and Kennedy (Reference Vidal-Martinez and Kennedy2000), Kennedy (Reference Kennedy2001a) and by Vidal-Martinez and Poulin (Reference Poulin and Luque2003). No evidence has yet been found to suggest that species interact and no niche shifts or competitive exclusions have been observed between closely related species of monogeneans on fish gills (Šimková et al. Reference Šimková, Sasal, Kadlec and Gelnar2001; Karvonen et al. Reference Karvonen, Bagge and Valtonen2007). Aggregation of individuals in a niche in these communities appears to relate to the probability of improving cross-fertilization between individuals, as suggested by Rohde (Reference Rohde1979, Reference Rohde1994), rather than to competition.
Vidal-Martinez and Poulin (Reference Poulin and Luque2003) investigated temporal and spatial replicability in parasite community structure in several species of fish and recognized some negative associations between pairs of species in some localities but these were not repeated in others. They concluded that associations may not be characteristic of parasite communities in a particular host species but rather a feature of certain communities at specific times and places. Interspecific interactions were not important in structuring parasite communities, but distance between localities was an important determinant of community predictability. Dezfuli et al. (Reference Dezfuli, Giari, DeBiaggi and Poulin2001) also found that the extent of co-occurrences of helminth species in brown trout did not differ from those predicted by a null model and there was little replicability of composition and no consistent role of competition. Very similar conclusions were reached by Poulin and Guégan (Reference Poulin and Guégan2000) and Poulin and Valtonen (Reference Poulin and Valtonen2001, Reference Poulin and Valtonen2002).
It is difficult not to agree with the evaluation of Poulin (Reference Poulin2001a) that although the role of inter-specific competition as a structuring process in communities has been at the centre of much research, there is no agreement regarding its importance. Evidence that species interact in the laboratory may have little relevance to the field where infrapopulation densities may be far lower. Patterns in the field are at best hard to detect and often do not differ from those predicted by null models. Even when they do so differ, there may be equally plausible alternative explanations. Nevertheless, inter-specific competition has been demonstrated in isolationist parasite communities in freshwater fish in both the field and the laboratory and its potential importance cannot be ignored, even though it may prove impossible to assign a general role to it and it may have to be evaluated case by case.
Community structure and replicability
Many investigations have indicated that there is little replicability in richness, composition and structure in time and space in parasite communities of freshwater fishes. A number of recent investigations have focused specifically on trying to identify nested i.e. non-random patterns within such communities by comparing findings with null models based on randomness. Patterns and nestedness can be detected on occasion (Kennedy and Guégan, Reference Kennedy and Guégan1994; Carney and Dick, Reference Carney and Dick2000), but they can be completely absent from other investigations or, if detected, are not consistent when comparing communities in the same species in space (Vidal-Martinez and Poulin, Reference Vidal-Martinez and Poulin2003). Local host factors generally predominate and Rohde (Reference Rohde2005) considered that parasite communities, like parasite populations, are non-equilibrial systems in which contingencies dominate. More recently Timi and Poulin (Reference Timi and Poulin2008) have shown clearly that the probability of detecting a nested pattern depends strongly upon the null model chosen for the analysis. Random structure occurs in nearly all communities, even if they also exhibit some nestedness, and indeed departures from random appear to be the exceptions and not the norm.
Such general conclusions must still be considered tentative for a number of reasons. Firstly, the range of host species studied is actually very restricted. Most examples come from northern temperate regions and very few from the southern hemisphere or tropical conditions. The few studies that are available from the tropics show conflicting results. Choudhury and Dick (Reference Choudhury and Dick2000) reviewed publications on the richness of parasite communities in tropical fish and concluded, perhaps surprisingly, that tropical communities were less rich than northern temperate ones. Poulin (Reference Poulin2001b) queried this conclusion as he considered the data set to be too heterogeneous for such an analysis. There are also several examples that do not fit this pattern. Helminth communities in eels in tropical Queensland, Australia were significantly richer and more diverse than those in their congeners in Britain (Kennedy, Reference Kennedy1995) or the USA (Marcogliese and Cone, Reference Marcogliese and Cone1998). Moreover, helminth communities in some species of cichlids in Mexico were far richer than any reported from temperate species of fish (Salgado-Maldonado and Kennedy, Reference Kennedy1997). Secondly, even within a restricted area, variation in parasite community richness and composition of a helminth community in the same host species may change dramatically over time in one locality (Kennedy, Reference Kennedy1993, Reference Kennedy1997) but remain stable in another (Kennedy and Moriarty, Reference Kennedy and Moriarty2002). Neighbouring communities may be more similar than distant ones (Poulin and Morand, Reference Poulin and Morand1999) but this is by no means always the case even in different parts of the same metapopulation (Kennedy, Reference Kennedy2001b). Thirdly, parasite community richness in a host species may depend on whether the host is in the heartland of its distribution or occurs among alien species distant from its heartland (Kennedy and Bush, Reference Kennedy and Bush1994; Guégan and Kennedy, Reference Guégan and Kennedy1993). Fourthly, communities may be structured differently in other parts of the world in relation to richness of host communities. For example, many freshwater fish species present in Britain are absent from Ireland, but because fish communities are consequently simpler in Ireland, parasites may be forced into using fewer or less-favoured host species. This may result in more frequent concurrent infections and a higher frequency of inter-specific interactions and a more determinant parasite community structure (Byrne et al. Reference Byrne, Holland, Kennedy and Poole2003). In Brazil, where fish communities can be far richer, Takemoto et al. (Reference Takemoto, Pavanelli, Lizana, Luque and Poulin2005) found that differences in the population densities of 53 different species of fish were the sole significant predictor of parasite community richness.
Even when there is apparently a clear and replicable pattern in parasite community richness an exception may later appear. As part of a long-term ongoing investigation into parasite communities in eels, Kennedy and Guégan (Reference Kennedy and Guégan1996) looked at the relationship between component community richness and maximum infracommunity richness in large samples taken from 64 localities in the British Isles and samples taken from one locality over 17 years. The relationship between these two variables was not linear but curvilinear and was best described by a power or polynomial function. All infracommunities were species poor, and they became increasingly independent of component community richness and appeared saturated at levels well below that of the component community. This was considered not to be due to supply side processes, pool exhaustion or transmission rates, but it was compatible with there being a limited number of niches available and possible competition for them. However, a later study by Norton et al. (Reference Norton, Lewis and Rollinson2004a, Reference Norton, Rollinson and Lewisb) in one English river revealed a very different relationship between the same two variables and in component community richness. The relationship was not asymptotic, but maximal infracommunity richness appeared to be a fixed proportion of component community richness. Both maximal infracommunities and component community were potentially rich and comparable with those of some bird and mammal hosts. The species composition of the infracommunities appeared to be random and they were unsaturated. As yet there is no explanation of why this one system should produce such different results: possibly it is just one more example of the variability that confounds all attempts to understand community structure and richness and is equally evident in attempts to interpret the role of nestedness in patterns.
Susceptibility of communities to invasions
The ability of a parasite community to be invaded can potentially assist understanding of the processes determining community structure. There is no doubt that the frequency and extent of invasions and introductions is increasing. These may have a serious impact on the recipient native parasite communities as well as on host populations, and they can also indicate whether there are vacant niches in the recipient parasite community or whether it is so tightly packed that invasions are likely to fail. The dissemination of fish parasites throughout freshwater localities is due primarily to the movements of fish or bird hosts, whether natural or anthropochore (Kennedy, Reference Kennedy and Kennedy1976), and allogenic species (sensuEsch et al. Reference Esch, Kennedy, Bush and Aho1988) are dispersed naturally more readily than autogenic species and so can confer more similarity between communities. Many, perhaps even most, invasions fail as the conditions for success are very restrictive in time and place, although it would seem likely that the isolationist parasite communities of fish are more susceptible to invasions than species-rich interactive communities (Kennedy, Reference Kennedy, Pike and Lewis1994). Those that succeed may have major and deleterious impacts on their new host populations (Dogiel, Reference Dogiel, Dogiel, Petrushevski and Polyanski1961) and so on the populations of their parasites. Invading parasites may also transfer to native host species, with subsequent disturbance of their normal parasite communities, as evidenced by the number of species introduced into Hawaii (Font, Reference Font1998) and the spread of Bothriocephalus acheilognathi through Europe and especially through native Australian fish species (Dove and Fletcher, Reference Dove and Fletcher2000) and the impact of an American species of acanthocephalan throughout the River Rhine (Taraschewski et al. Reference Taraschewski, Moravec, Lamah and Anders1987; Sures et al. Reference Sures, Knopf, Wurtz and Hirt1999; Sures and Streit, Reference Sures and Streit2001). Invasions have occurred in other communities but these have only been recognized as such some time after the invasion. The source and time of the invasion of the English strain of Pomphorhynchus laevis into the River Culm is not known (Kennedy, Reference Kennedy2001b) but the Irish strain of the same species (O'Mahony et al. Reference O' Mahony, Bradley, Kennedy and Holland2004) invaded the River Otter around 1990 (Kennedy, Reference Kennedy1997). In both cases the invader came to dominate the community for a period, suggesting that it was not previously saturated. In fact, all the above examples suggest that parasite communities in fish are not saturated with species but that vacant niches do exist.
CONCLUSIONS
It is evident from the foregoing account that the stated aim of research into the ecology of parasites of fishes of detecting repeatable patterns, and then identifying the determinant processes and principles producing them, is still a long way from success. Progress has been more satisfactory in the field of population dynamics, where it has been possible to identify publications that have advanced developments in the subject. It is clear, if nothing else, that aggregated parasite distributions are the norm and that parasite-induced host mortality does not of necessity result in the local extinction of either or both partners. There is now a sound basis for constructing hypotheses which can be tested in the field and laboratory, in that it appears that most parasite populations in freshwater fish exist in non-equilibrial conditions. Other regulatory factors may be evident, but their significance and the conditions under which they operate as such are still far from being understood. There is no unequivocal example of fish host and parasite populations undergoing linked stable cycles. It is clear that local habitat conditions may have considerable influence on the population dynamics and apparent stability in populations may be due primarily to environmental stability. It is therefore sensible to adopt the null hypothesis that parasite populations are not stable and regulated until there is convincing evidence to the contrary.
Progress in understanding parasite community dynamics has been far slower and this directly parallels the situation with free-living organisms. Communities of free-living animals are complex, and those of the parasites superimposed on them must be even more so. Lawton (Reference Lawton1999) summarized community ecology of free-living animals as being messy, because there is so much local variation that it is very difficult, if not impossible, to find useful generalizations. His views would seem to apply equally to parasite communities in freshwater fish: patterns of any sort are very hard to identify, and even when detected are seldom if ever replicable but are contingent upon local and temporary circumstances. It is thus very difficult to recognize significant developments or advances in this field and to relate them to particular publications. The plethora of publications currently seems to demonstrate the absence of any clear patterns in parasite community richness or replicability or in structuring processes. All that can be said at this stage is that parasite communities in freshwater fish appear in general to be species poor, unstructured and isolationist in nature but all three generalizations can be overturned in some locality.
Difficulties in detecting patterns must arise, at least in part, from the short-term nature of so many investigations. There seems to be an assumption, implicit and seldom stated, that samples taken over a short period of time are representative of the system over a longer period. This assumption may often be incorrect. Examination of any long-term data set of parasite populations or communities over randomly selected short-term periods can indicate clearly how easy it is to reach incorrect conclusions. Identification of regulatory mechanisms at one moment in time does not of necessity mean that they operate to produce stability of the population or community. Evidence that a population or community does not persist strongly suggests that it is unregulated, but evidence of persistence does not per se indicate stability, equilibrium or regulation. All too often other explanations are equally acceptable. There is still a very real need for more long-term investigations.
Given the amount of research that has been carried out over the last half century, such conclusions may be disappointing, but there has in reality been a great deal of progress. Field programmes are now planned far more carefully and a look-and-see approach has largely been replaced by hypothesis testing with quantitative data being analysed statistically and far more rigorously and results tested against null models or specific predictions. There is also much more exchange of ideas between ecological parasitologists working on fish and those working on other vertebrates. Texts continue to appear on ecological parasitology, including Poulin (Reference Poulin2007a), Bush et al. (Reference Bush, Fernández, Esch and Seed2001) and Rohde (Reference Rohde2005). Even more significant, perhaps, is the exchange of views between ecologists studying parasites and ecologists studying free-living animals evidenced by the inclusion in general ecology text books of examples from parasite ecology e.g. chapters in Kikkawa and Anderson (Reference Kikkawa and Anderson1986) and Townsend et al. (Reference Townsend, Harper and Begon2000).
Such a diversity of approaches and exchange of ideas is essential in any attempt to understand parasite ecology. It may also be necessary to widen the coverage of field investigations, as there are still far too few studies in tropical biomes, for example, and in southern America and Africa. It can also prove helpful to focus on systems that are simpler, for example those in Ireland, where it may be easier to detect patterns. Put another way, it seems unlikely that more and more specific examples from northern temperate systems will help to produce generalizations, other than fortuitously. It may also be that novel approaches are required. Poulin (Reference Poulin2007b) has suggested that it may be helpful to focus on parasite biomass or relative numbers as has been done in studies by Mouillot et al. (Reference Mouillot, George-Nascimento and Poulin2003, Reference Mouillot, George-Nascimento and Poulin2005) and the recent study by Munoz and George-Nascimento (Reference Munoz and George-Nascimento2008) has shown that conclusions based on parasite volumes are complementary to those based on parasite numbers. In this context, it may be salient to note that the winners of inter-specific competitions between large cestodes and smaller acanthocephalans are generally the acanthocephalans. However, it is really still too soon to evaluate these novel approaches as they need to stand the test of time. The search for patterns in space and time must continue. Even if they are difficult to detect, knowledge of why this may be so must assist our understanding. If no replicable patterns in space and time are found it is of course possible that neither patterns nor order exist, but we are still a long way from establishing that this is the case.
