Robert Poulin

Parasites in food webs: the ultimate missing links

Parasitism is the most common consumer strategy among organisms, yet only recently has there been a call for the inclusion of infectious disease agents in food webs. The value of this effort hinges on whether parasites affect food-web properties. Increasing evidence suggests that parasites have the potential to uniquely alter food-web topology in terms of chain length, connectance and robustness. In addition, parasites might affect food-web stability, interaction strength and energy flow. Food-web structure also affects infectious disease dynamics because parasites depend on the ecological networks in which they live. Empirically, incorporating parasites into food webs is straightforward. We may start with existing food webs and add parasites as nodes, or we may try to build food webs around systems for which we already have a good understanding of infectious processes. In the future, perhaps researchers will add parasites while they construct food webs. Less clear is how food-web theory can accommodate parasites. This is a deep and central problem in theoretical biology and applied mathematics. For instance, is representing parasites with complex life cycles as a single node equivalent to representing other species with ontogenetic niche shifts as a single node? Can parasitism fit into fundamental frameworks such as the niche model? Can we integrate infectious disease models into the emerging field of dynamic food-web modelling? Future progress will benefit from interdisciplinary collaborations between ecologists and infectious disease biologists.

The Diversity of Parasites

Parasitism is one of the most successful modes of life displayed by living organisms, as measured by how often it evolved and how many parasitic species are presently in existence. Studying the diversity of parasites is particularly relevant because sympatric diversification may be important in some parasite taxa, and because of the opportunity for independent tests of evolutionary hypotheses in the many separate lineages in which parasitism evolved. Our incomplete knowledge of existing parasite species-the result of a range of phenomena that includes inadequate sampling effort or the lumping of different cryptic species under one name-is not always a major obstacle for the study of parasite diversity. Patterns in the diversity of parasites may be associated with either host or parasite characteristics. The distribution of parasite diversity among host taxa does not simply reflect the species diversity of the host taxa themselves; life history and ecological traits of hosts appear to play important roles. These may determine the likelihood that hosts are colonized by parasite species over evolutionary time. It is not yet clear whether some host traits also favor intrahost speciation and diversification of parasites, and the formation of new parasite species. Certain features of parasites may also be associated with speciation and diversification. Only parasite body size has received much attention; the patterns observed are not greatly different from those of free-living species, with small-bodied parasite taxa being more speciose than related large-bodied taxa. Epidemiological parameters such as the basic reproductive rate of parasites, or R0, can also generate predictions regarding the distribution or evolution of parasite diversity. For instance, parasite taxa characterized by high R0 values may be more speciose than related taxa with lower values of R0; such predictions remain untested. Large-scale biogeographical patterns of diversity have only been well studied for metazoan parasites of marine fish; for these parasites, latitudinal patterns can be explained by effects of temperature on speciation rates and epidemiological variables, though other causes are possible. The emphasis for future research must shift from pattern description to the elucidation of the processes responsible for the structure and diversity of parasite faunas. A better integration of ecological and historical (or phylogenetic) approaches to the study of parasite diversity should make this objective possible.

Molecular ecology of parasites: elucidating ecological and microevolutionary processes

We review studies that have used molecular markers to address ecological and microevolutionary processes in parasites. Our goal is to highlight areas of research that may be of particular interest in relation to the parasitic lifestyle, and to draw attention to areas that require additional study. Topics include species identification, phylogeography, host specificity and speciation, population genetic structure, modes of reproduction and transmission patterns, and searching for loci under selection.

Phylogeny, Ecology, and the Richness of Parasite Communities in Vertebrates

The makeup of parasite communities is the result, among other factors, of interactions between the evolutionary history and ecological characteristics of hosts. This study evaluates the relative importance of some ecological factors (host body size, diet, habitat, latitude, and the mean number of parasite individuals per host) as determinants or correlates of parasite community richness in vertebrates, before and after controlling for potential effects of host phylogenetic relationships. Data were obtained from the literature on 596 parasite communities belonging to one of four distinct types: gastrointestinal parasite communities of fish, birds, or mammals, and ectoparasite communities of fish. There were positive correlations between the number of hosts sampled and mean species richness of the parasite community of each genus. In analyses treating host genera as independent statistical observations and using estimates of parasite species richness corrected for host sample size, positive correlations were observed between richness and host body size in gastrointestinal communities of all three groups of vertebrates. The mean number of parasite individuals per host also was correlated positively with species richness. In fish, richness increased with increases in the proportion of animal food in the host diet. Aquatic birds had richer parasite communities than their terrestrial counterparts, whereas marine fish had richer gastrointestinal parasite communities than freshwater fish. The richness of ectopar- asite communities on fish showed no association with any of the ecological variables investigated. Using host genera as independent points in the analyses may lead to biased results since some host lineages are descended from recent common ancestors, and are therefore not truly independent. The comparative analysis was repeated using phylogenetically indepen- dent contrasts derived from the phylogeny of hosts. Once the effects of host phylogeny were removed, somewhat different results were obtained: host body size showed no rela- tionship with parasite species richness in birds, and there was no evidence that habitat transitions resulted in significant changes in parasite species richness in any of the types of communities studied. Of the ecological factors studied, the comparative analyses suggest that only host body size can be an important determinant of parasite community richness in certain host groups. This study illustrates clearly the need to control for phylogeny in investigations of host-parasite interactions.

Global warming and temperature-mediated increases in cercarial emergence in trematode parasites

Global warming can affect the worlds biota and the functioning of ecosystems in many indirect ways. Recent evidence indicates that climate change can alter the geographical distribution of parasitic diseases, with potentially drastic consequences for their hosts. It is also possible that warmer conditions could promote the transmission of parasites and raise their local abundance. Here I have compiled experimental data on the effect of temperature on the emergence of infective stages (cercariae) of trematode parasites from their snail intermediate hosts. Temperature-mediated changes in cercarial output varied widely among trematode species, from small reductions to 200-fold increases in response to a 10 degrees C rise in temperature, with a geometric mean suggesting an almost 8-fold increase. Overall, the observed temperature-mediated increases in cercarial output are much more substantial than those expected from basic physiological processes, for which 2- to 3-fold increases are normally seen. Some of the most extreme increases in cercarial output may be artefacts of the methods used in the original studies; however, exclusion of these extreme values has little impact on the preceding conclusion. Across both species values and phylogenetically independent contrasts, neither the magnitude of the initial cercarial output nor the shell size of the snail host correlated with the relative increase in cercarial production mediated by rising temperature. In contrast, the latitude from which the snail-trematode association originated correlated negatively with temperature-mediated increases in cercarial production: within the 20 degrees to 55 degrees latitude range, trematodes from lower latitudes showed more pronounced temperature-driven increases in cercarial output than those from higher latitudes. These results suggest that the small increases in air and water temperature forecast by many climate models will not only influence the geographical distribution of some diseases, but may also promote the proliferation of their infective stages in many ecosystems.

Chapter 5 – Parasite Manipulation of Host Behavior: An Update and Frequently Asked Questions

Abstract Many taxa of parasites modify the behavior of their hosts in ways that improve their probability of transmission. Regardless of its evolutionary origins or underlying mechanisms, host manipulation is a widespread adaptive strategy yielding fitness benefits for parasites with various life cycles and transmission modes. This chapter focuses on recent developments that are expanding our understanding of this phenomenon. Currently, growing attention is being paid to the effect of parasites on whole suites of host behavioral traits as opposed to single traits, and to correlations among behaviors, which may be the target of manipulation instead of the traits themselves. At the same time, variation in the use of manipulation is being explored both among and within parasite species. On the one hand, models that take into account the potential costs of manipulation predict under what circumstances manipulation is likely to evolve as a transmission strategy. On the other hand, within manipulative species, manipulation may be a flexible strategy only adopted by individual parasites in certain conditions dictated by other parasites and by the host itself. This inter- and intraspecific variation in the use of host manipulation for transmission is due in large part to its unreliable effectiveness within complex natural systems where dead-ends await many manipulative parasites. Finally, recent neurological and proteomic studies of the pathways used by parasites to alter host behavior offer new insights into the evolution of manipulation. The chapter ends with a list of promising directions that provide an agenda for future research.

Parasitism, community structure and biodiversity in intertidal ecosystems.

There is mounting evidence that parasites can influence the composition and structure of natural animal communities. In spite of this, it is difficult to assess just how important parasitism is for community structure because very few studies have been designed specifically to address the role of parasites at the community level, no doubt because it is difficult to manipulate the abundance of parasites in field experiments. Here, we bring together a large amount of published information on parasitism in intertidal communities to highlight the potential influence of parasites on the structure and biodiversity of these communities. We first review the impact of metazoan parasites on the survival, reproduction, growth and behaviour of intertidal invertebrates, from both rocky shores and soft-sediment flats. Published evidence suggests that the impact of parasites on individuals is often severe, though their effects at the population level are dependent on prevalence and intensity of infection. We then put this information together in a discussion of the impact of parasitism at the community level. We emphasize two ways in which parasites can modify the structure of intertidal communities. First, the direct impact of parasites on the abundance of key host species can decrease the importance of these hosts in competition or predator-prey interactions with other species. Second, the indirect effects of parasites on the behaviour of their hosts, e.g. burrowing ability or spatial distribution within the intertidal zone, can cause changes to various features of the habitat for other intertidal species, leading to their greater settlement success or to their local disappearance. Our synthesis allows specific predictions to be made regarding the potential impact of parasites in certain intertidal systems, and suggests that parasites must be included in future community studies and food web models of intertidal ecosystems.

The disparity between observed and uniform distributions: A new look at parasite aggregation

A simple new measure of parasite aggregation is described, the index of discrepancy (D). It quantifies the difference between the observed parasite distribution, and the hypothetical distribution that corresponds to the ideal case where all hosts harbour the same number of parasites. This index, computed for parasite distributions obtained from the literature, is compared to 2 other measures of aggregation, the variance to mean ratio and the parameter k of the negative binomial distribution. Both k and D indicate that aggregation decreases when the prevalence of infection and the mean number of parasites per host increase, while the variance to mean ratio suggests the opposite. Since an increase in prevalence means that parasites exploit a greater proportion of the available hosts and are thus not concentrating in only a few, aggregation should be inversely proportional to prevalence. Unlike k and D, the variance to mean ratio is a host-centered measure that is not very sensitive to the distribution of parasites. The index of discrepancy, on the other hand, is not only much easier to compute than k, but focuses on the difference between an ideal, uniform distribution and the one actually displayed by parasites. Since what it measures is what parasitologists mean by aggregation, the new index appears to be a more adequate measure of aggregation than other measures currently used.

Density, body mass and parasite species richness of terrestrial mammals

We investigated the relationships between helminth species richness and body mass and density of terrestrial mammals. Cross-species analysis and the phylogenetically independent contrast method produced different results. A non-phylogenetic approach (cross-species comparisons) led to the conclusion that parasite richness is linked to host body size. However, an analysis using phylogenetically independent contrasts showed no relationship between host body size and parasite richness. Conversely, a non-phylogenetic approach generated a negative relationship between parasite richness and host density, whereas the independent contrast method showed the opposite trend – that is, parasite richness is positively correlated with host density. From an evolutionary perspective, our results suggest that opportunities for parasite colonization depend more closely on how many hosts are available in a given area than on how large the hosts are. From an epidemiological point of view, our results confirm theoretical models which assume that host density is linked to the opportunity of a parasite to invade a population of hosts. Our findings also suggest that parasitism may be a cost associated with host density. Finally, we provide some support for the non-linear allometry between density and mammal body mass (Silva and Downing, 1995), and explain why host density and host body mass do not relate equally to parasite species richness.

Nestedness versus modularity in ecological networks: two sides of the same coin?

1. Understanding the structure of ecological networks is a crucial task for interpreting community and ecosystem responses to global change. 2. Despite the recent interest in this subject, almost all studies have focused exclusively on one specific network property. The question remains as to what extent different network properties are related and how understanding this relationship can advance our comprehension of the mechanisms behind these patterns. 3. Here, we analysed the relationship between nestedness and modularity, two frequently studied network properties, for a large data set of 95 ecological communities including both plant-animal mutualistic and host-parasite networks. 4. We found that the correlation between nestedness and modularity for a population of random matrices generated from the real communities decreases significantly in magnitude and sign with increasing connectance independent of the network type. At low connectivities, networks that are highly nested also tend to be highly modular; the reverse happens at high connectivities. 5. The above result is qualitatively robust when different null models are used to infer network structure, but, at a finer scale, quantitative differences exist. We observed an important interaction between the network structure pattern and the null model used to detect it. 6. A better understanding of the relationship between nestedness and modularity is important given their potential implications on the dynamics and stability of ecological communities.