Albert O. Bush

Parasitology Meets Ecology on Its Own Terms: Margolis et al. Revisited.

We consider 27 population and community terms used frequently by parasitologists when describing the ecology of parasites. We provide suggestions for various terms in an attempt to foster consistent use and to make terms used in parasite ecology easier to interpret for those who study free-living organisms. We suggest strongly that authors, whether they agree or disagree with us, provide complete and unambiguous definitions for all parameters of their studies.

Parasite communities : patterns and processes

1 Patterns and processes in helminth parasite communities: an overview.- 2 Host populations as resources defining parasite community organization.- 3 Spatial scale and the processes structuring a guild of larval trematode parasites.- 4 Guild structure of larval trematodes in molluscan hosts: prevalence, dominance and significance in competition.- 5 Helminth communities in marine fishes.- 6 Helminth communities in freshwater fish: structured communities of stochastic assemblages?.- 7 Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes.- 8 Helminth communities in avian hosts: determinants of pattern.- 9 Helminth community of mammalian hosts: concepts at the infracommunity, component and compound community levels.- 10 Models for multi-species parasite-host communities.- 11 Free-living communities and alimentary tract helminths: hypotheses and pattern analyses.- 12 Concluding remarks.

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.

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.

Species richness in helminth communities: the importance of multiple congeners.

Using data sets derived from published literature, the contribution of congeneric species to helminth component community richness is evaluated. Consideration of the frequency distribution of congeners in relation to host and parasite groups reveals that the distributions are unimodal, that singletons are the commonest class and that the frequency of occurrence of congeners decreases with increasing number of species per genus. Congeners may be found in any group of hosts or parasites, but are more common amongst cestodes of aquatic birds. Two patterns of occurrence of congeneric species are recognized: one in which from a few to multiple congeners are found within a single helminth genus, exemplified by dactylogyrid monogeneans and cloacinid nematodes, and the other in which there is a simultaneous occurrence of congenerics and confamilials such that there are several genera involved, but each represented by fewer species, exemplified by strongyles in horses. The question of whether these patterns can be considered examples of species flocks is discussed. We conclude that multiple congeners and species flocks are interesting phenomena but, except in isolated cases, they make insignificant contributions to community richness.

THE ECOLOGY OF “CROWDING”

There are 2 elements that make ‘‘crowding’’ interesting— mechanism (causality) and manifestation (effect). In our companion paper, Larry Roberts addresses mechanisms. Here, we focus on manifestation. As ecologists, it is difficult to get too excited about Clark Read’s paper on the ‘‘crowding effect’’ in cestodes, at least initially. The paper acknowledges clearly that the phenomenon has been observed repeatedly, is mostly a discussion of appropriate techniques, and concludes with a brief overture to causality. Recalling a popular television commercial from several years ago, ‘‘Where’s the beef?’’ The answer lies in the implication of crowding. Simply stated, crowding means too many of something. In the case of worms in the gut of a host, it is obvious that there exists a finite number of individuals that can physically fit into a gut. Crowding is a common phenomenon, certainly not restricted to tapeworms in the small intestine of a rat. It is very, very common in managed systems where the intent is to get the ‘‘biggest bang for the buck.’’ For example, gardeners know that too many plants in a prescribed area will result in a poor crop; so too do aquaculturists raising fishes, crustaceans, or shellfish. Under such artificial conditions, the remedy for alleviating crowding is simple, at least in theory. Either reduce (thin) the target population or artificially enhance the environment. The latter may be accomplished by supplemental feeding, removing toxic wastes, and so forth. Trivial observations perhaps but ‘‘crowding’’ is overwhelmingly common, at least where humans have intervened. But, what of the ecology of crowding in a natural context? We consider crowding as being important ecologically in 2 contexts—first as it relates to predator–prey relationships and second as it relates to the much-maligned idea of competition. In a food web, crowding will always impact most severely on the prey population. If there are too many predators, e.g., the predators are crowded, more prey will be taken simply because there are more things to eat them. Similarly, if there are too many prey, predators will find and, perhaps, capture them more easily. However, our focus here is not on predator–prey relationships, rather it is on crowding as it might relate to parasites in a host. At the time Clark Read’s paper was published, ecology was more qualitative natural history than the quantitative science we know today. If predator–prey interactions could not account for the observed patterns on the distribution and abundance of organisms, then surely the answer must lie in competition. It is perhaps for that reason, that competition was apparently so pervasive that Read ignored manifestation in his paper. Why emphasize what was so readily obvious? Basically, competition takes 2 forms: interference and exploitation. With interference competition, organisms may impact on others in a direct fashion, for example, releasing toxins.

Recruitment-driven, spatially discontinuous communities: a null model for transferred patterns in target communities of intestinal helminths.

Populations and therefore communities of intestinal helminths of vertebrates are fueled by recruitment of new individuals from outside the host. The source of new individuals is often an intermediate host that harbors several infective propagules of 1 or more species. Hence these source communities are transmitted in packets of infective propagules to target communities in definitive hosts. Packets not only provide recruits to target communities, but, because a packet of propagules possesses its own structure, it may also transmit structure to the target community. We use this system to examine the contribution that structure in the source pool of propagules makes to the structure of recruitment-driven target populations and communities. By treating the dynamics of such target populations and communities as immigration-death processes, we conclude: (1) Unlike a birth-driven population a recruitment-driven target population will grow to an asymptotic limit even in the absence of density-dependent processes or reaching carrying capacity; (2) the frequency distribution of the number of recruits entering target populations will determine the frequency distribution of adults in target populations; (3) interspecific associations among species in the source community will be transmitted to target communities, but the magnitude of the transmitted associations will depend upon the relative survival rates of the species; and (4) for associations of equal magnitude in a source community, the magnitude of a transferred negative association will be less than the magnitude of a positive association in a target community. Two examples of source communities in salt marsh crabs reveal that source infracommunities exist with the hypothesized structure. Further, the source helminth communities display a greater number of positive than negative interspecific associations. The inequity in transfer and the existence of a greater proportion of positive associations in source communities may explain the widespread occurrence of excess positive associations that has been noted in recruitment-driven communities.

Helminth communities in avocets: importance of the compound community.

This paper reports patterns of similarity and overlap in species presence and patterns of linear distribution of intestinal helminths in 22 avocets from 4 populations. Avocets collected from ephemeral bodies of water in Alberta and Manitoba had communities composed largely of species that are avocet specialists plus some that are host generalists. The composition of helminth communities in these hosts was similar to that reported in earlier surveys of avocet helminths. There was little evidence for competition between helminth species in these communities. In contrast, avocets collected from permanent bodies of water in Alberta had communities composed largely of species that are specialists in various duck species, particularly lesser scaup. These helminths were superimposed on the normal community, fitting into linear gaps along the intestine but also overlapping the distributions of avocet specialists. These lesser scaup specialists exhibit interactive patterns amongst themselves and, to some extent, with avocet specialists. Helminth communities in avocets from ephemeral bodies of water have vacant niches and are largely isolationist in nature. Those in avocets from permanent bodies of water are saturated and are more interactive in nature.