C. R. Kennedy

Ecological versus phylogenetic determinants of helminth parasite community richness

SummaryWe examine patterns of community richness among intestinal parasitic helminth communities in fishes, herptiles, birds and mammals with respect to the comparative number of component species in a host population. We show that terrestrial hosts have, on average, fewer component species than aquatic hosts. We also show that the mean number of component species in aquatic hosts increases from fishes through herptiles to birds before declining slightly in mammals. For terrestrial hosts, the mean number of component species increases from herptiles, through birds, reaching a maximum in mammals. We conclude that: (i) habitat of the host is more important in determining community richness than is host phylogeny; (ii) the phenomenon of ‘host capture’ may be largely responsible for increased species richness in some host groups; (iii) aquatic birds harbour the richest intestinal helminth communities; and (iv) as we interpret them, our data refute the time hypothesis, which would predict that fishes as the oldest lifestyle should have the richest helminth communities.

Patterns in helminth communities: why are birds and fish different?

Recently, some authors (Kennedy, 1981; Price & Clancy, 1983) have argued that there are fundamental differences between the communities of helminths in fish and bird hosts. Such differences are foreshadowed by the work of Dogiel (1964) and are apparent from survey data (e.g. Threlfall, 1967; Bakke, 1972; Hair & Holmes, 1975 on birds, and compare Chubb, 1963; Mishra & Chubb, 1969; Wootten, 1973; Ingham & Dronen, 1980 on fish). Questions still remain, however, as to whether the distinctions are truly justified and whether the differences are really fundamental. In this paper, we address these questions by examining helminth diversity in a series of hosts. We then discuss and provide explanations for the observed differences.

Patterns in helminth communities in freshwater fish in Great Britain: alternative strategies for colonization

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 than fish and 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.

Helminth communities in freshwater fish: structured communities or stochastic assemblages?

The helminth parasites of freshwater fish have long proved an attractive field for parasitologists, and have spawned an extensive and voluminous literature. It was not until the seminal publications of Dogiel (1961, 1964), however, that attention was directed primarily to their ecology. Dogiel reviewed much of the existing literature in the light of ecological concepts, and examined the dependence of the parasite fauna as a whole, the parasitocoenosis, upon the environment. As well as laying down general principles, he discussed in detail (1961) the influence of physical factors, such as water chemistry and habitat size, and biological factors, such as host age, diet and migration, upon the composition of the parasite fauna of a host population. Dogiel’s reviews came to form the foundations not only for the study of the ecology of fish parasites, but also for the new discipline of ecological parasitology.

Maximum local helminth parasite community richness in British freshwater fish: a test of the colonization time hypothesis

The investigation of Price & Clancy (1983), which demonstrated a significant positive correlation between total helminth species number per host species and geographical range of freshwater fish host species in Britain, was re-examined using a different measure of parasite species richness. Re-calculation of the correlations between the two parameters after controlling for the effect of the composition of the list of fish by excluding, on biological and distributional grounds, 2 species of agnathans and 7 species of introduced teleosts, and for the effect of sampling effort by using helminth richness in the richest component community of each fish species rather than check-list data, reveals no significant relationship between helminth species richness and host range. Habitat and an omnivorous host diet now appear more significant determinants of helminth richness than the accumulation of parasites by predation. The findings provide little support for the interpretation of the relationship between helminth species richness and host range in terms of island biogeographic theory, but do support an alternative explanation in terms of the colonization time hypothesis, i.e. that helminth species richness is related to the time since the fish host arrived in Britain.

Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus : a study of three epizootic cycles over thirty-one years

Data are presented on 2 full epizootic cycles and the start of a third of Ligula intestinalis in roach Rutilus rutilus in a small lake, and the relationships of these cycles to the densities of rudd, Scardinius erythrophthalmus, and Great Crested Grebes, Podiceps cristatus, over 31 years. The parasite was introduced to the lake by P. cristatus in 1973 at a time when the roach population had increased in response to eutrophication to a level at which individual fish growth was stunted and the hithero dominant rudd population had declined in numbers as a consequence of inter-specific competition with roach. Ligula prevalence peaked at 28% in only 2 years: thereafter parasite-induced host mortality caused a decline in the roach population, releasing fish from stunting and allowing the rudd population to recover. The consequent improved growth of roach individuals and their short life-span reduced Ligula transmission rates and prevalence levels declined to approximately 1% although Ligula nevertheless persisted for a further 10 years. Following a massive winter-kill of the fish populations in 1984-1985, fish and Ligula numbers declined to barely detectable levels and the parasite disappeared from samples. Rudd recovered first, then roach and interspecific competition again led to a decline in rudd numbers. This increase in roach numbers led to a decrease in roach growth rates, which coincided with the re-colonization of the lake by Ligula. This second epizootic of Ligula peaked within 2 years in 1991-1992, when up to 78% of roach were infected with a maximum abundance of 2.2 parasites and intensity of 21 parasites. Heavy parasite-induced mortality of roach led to a decline in numbers, an improvement in individual growth rate and a reduction of Ligula transmission rates such that the epizootic died out in 1996. Similar conditions of roach numbers and growth prevailed at the start of a third cycle in 1998. The course of events over the second cycle was so similar to that of the first that it confirms the interpretations of that cycle. Comparison with other localities shows that epizootics of Ligula always coincide with rapid increases in roach numbers, for whatever cause, and stunted growth, which together attract piscivorous birds. At the start of a cycle Ligula is a major determinant of the population dynamics of the roach, but at the end of the cycle the fish population dynamics determine those of the parasite. The cycles are not regulated and the roach-Ligula system is inherently unstable.

Regional versus local helminth parasite richness in British freshwater fish: saturated or unsaturated parasite communities?

The relationships between regional species richness and local species richness were examined in respect of helminth parasite communities in 32 species of freshwater fish in the British Isles. Fish were divided into 5 categories, for each of which the goodness of fit of the relationship to linear, exponential and power function models was tested. For all categories of fish combined, there was a significant, positive curvilinear relationship. Nested within this were two other patterns. For introduced fish, a linear model provided the best fit; for euryhaline and relict species it was impossible to determine the best model, but for the other categories the relationship was curvilinear and was best fitted by a power function model. The linear relationship found for introduced fish was interpreted as a temporary situation, reflecting the shortage of time for the communities to become saturated. It corresponded to the linear part of the curvilinear relationship of the other categories, which is believed to represent the fundamental form of the relationship for parasite communities. The communities reached a saturation level of richness, corresponding to the asymptote of the curve, which fell well below regional species richness. Explanations for local saturation are discussed, but neither community structure nor supply-side ecology can yet be preferred. It is concluded that local patterns in helminth community richness, in contrast to those in fish assemblages, are not significantly influenced by patterns on a larger, regional spatial scale and so regional species richness is not a key determinant of local species richness, nor does a knowledge of regional patterns improve predictability of local patterns.

Host fragmentation and helminth parasites: Hedging your bets against extinction

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 fragmentation. 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.

Richness and diversity of intestinal metazoan communities in brown trout Salmo trutta compared to those of eels Anguilla anguilla in their European heartlands

The hypothesis that intestinal helminth communities in freshwater brown trout are dissimilar in composition and structure to those in the European eel was tested by an analysis of component communities from 72 localities and of infracommunities from 34 localities in the British Isles and Norway. Derived indices were then compared with published data from eels. Composition of helminth communities differed considerably between the two hosts as a group of 4 species occurred commonly in trout and so gave greater predictability to the community composition. These 4 species were trout specialists and in 97% of the localities a trout specialist dominated the community rather than a generalist acanthocephalan as is typical for eels. By contrast all measures of community structure and indices of richness and diversity indicated that helminth communities in trout were isolationist in character, species poor and exhibited low diversity at both component and infracommunity levels. All values of indices for trout helminth communities were strikingly similar to those obtained from eels. Evidence of interspecific interactions within the trout helminth communities and a limit of 4 to infracommunity species richness further enhanced the similarities and suggested a common determinant of community structure. The hypothesis was thus supported in respect of species composition but refuted in respect of community structure.

Physiological status of wild European eels (Anguilla anguilla) infected with the parasitic nematode, Anguillicola crassus.

The effect of the parasitic swimbladder nematode, Anguillicola crassus, on the physiological status of wild European eels (Anguilla anguilla) was investigated during an 18 month survey (February 1995 until September 1996), and compared with that of wild uninfected eels collected over the same time-period. Despite the occurrence of up to 15 blood-feeding adults in the swimbladder lumen of the infected eels and as many as 25 additional larvae in the swimbladder wall, there were no major differences in hormonal, metabolic or osmoregulatory status of the 2 groups of eels. Wild European eels appear to adapt to chronic parasitism with Anguillicola crassus. The possible adverse effects of additional simultaneous stressors are discussed.