Armand M. Kuris

Introduced species and their missing parasites

Damage caused by introduced species results from the high population densities and large body sizes that they attain in their new location. Escape from the effects of natural enemies is a frequent explanation given for the success of introduced species. Because some parasites can reduce host density and decrease body size, an invader that leaves parasites behind and encounters few new parasites can experience a demographic release and become a pest. To test whether introduced species are less parasitized, we have compared the parasites of exotic species in their native and introduced ranges, using 26 host species of molluscs, crustaceans, fishes, birds, mammals, amphibians and reptiles. Here we report that the number of parasite species found in native populations is twice that found in exotic populations. In addition, introduced populations are less heavily parasitized (in terms of percentage infected) than are native populations. Reduced parasitization of introduced species has several causes, including reduced probability of the introduction of parasites with exotic species (or early extinction after host establishment), absence of other required hosts in the new location, and the host-specific limitations of native parasites adapting to new hosts.

Eradication revisited: dealing with exotic species

Invasions of nonindigenous species threaten native biodiversity, ecosystem functioning, animal and plant health, and human economies. The best solution is to prevent the introduction of exotic organisms but, once introduced, eradication might be feasible. The potential ecological and social ramifications of eradication projects make them controversial; however, these programs provide unique opportunities for experimental ecological studies. Deciding whether to attempt eradication is not simple and alternative approaches might be preferable in some situations.

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.

Ecosystem energetic implications of parasite and free-living biomass in three estuaries

Parasites can have strong impacts but are thought to contribute little biomass to ecosystems. We quantified the biomass of free-living and parasitic species in three estuaries on the Pacific coast of California and Baja California. Here we show that parasites have substantial biomass in these ecosystems. We found that parasite biomass exceeded that of top predators. The biomass of trematodes was particularly high, being comparable to that of the abundant birds, fishes, burrowing shrimps and polychaetes. Trophically transmitted parasites and parasitic castrators subsumed more biomass than did other parasitic functional groups. The extended phenotype biomass controlled by parasitic castrators sometimes exceeded that of their uninfected hosts. The annual production of free-swimming trematode transmission stages was greater than the combined biomass of all quantified parasites and was also greater than bird biomass. This biomass and productivity of parasites implies a profound role for infectious processes in these estuaries.

Homage to Linnaeus: How many parasites? How many hosts?

Estimates of the total number of species that inhabit the Earth have increased significantly since Linnaeuss initial catalog of 20,000 species. The best recent estimates suggest that there are ≈6 million species. More emphasis has been placed on counts of free-living species than on parasitic species. We rectify this by quantifying the numbers and proportion of parasitic species. We estimate that there are between 75,000 and 300,000 helminth species parasitizing the vertebrates. We have no credible way of estimating how many parasitic protozoa, fungi, bacteria, and viruses exist. We estimate that between 3% and 5% of parasitic helminths are threatened with extinction in the next 50 to 100 years. Because patterns of parasite diversity do not clearly map onto patterns of host diversity, we can make very little prediction about geographical patterns of threat to parasites. If the threats reflect those experienced by avian hosts, then we expect climate change to be a major threat to the relatively small proportion of parasite diversity that lives in the polar and temperate regions, whereas habitat destruction will be the major threat to tropical parasite diversity. Recent studies of food webs suggest that ≈75% of the links in food webs involve a parasitic species; these links are vital for regulation of host abundance and potentially for reducing the impact of toxic pollutants. This implies that parasite extinctions may have unforeseen costs that impact the health and abundance of a large number of free-living species.

The rising tide of ocean diseases: unsolved problems and research priorities

New studies have detected a rising number of reports of diseases in marine organisms such as corals, molluscs, turtles, mammals, and echinoderms over the past three decades. Despite the increasing disease load, microbiological, molecular, and theoretical tools for managing disease in the worlds oceans are under-developed. Review of the new developments in the study of these diseases identifies five major unsolved problems and priorities for future research: (1) detecting origins and reservoirs for marine diseases and tracing the flow of some new pathogens from land to sea; (2) documenting the longevity and host range of infectious stages; (3) evaluating the effect of greater taxonomic diversity of marine relative to terrestrial hosts and pathogens; (4) pinpointing the facilitating role of anthropogenic agents as incubators and conveyors of marine pathogens; (5) adapting epidemiological models to analysis of marine disease.

Hosts as Islands

Island biogeography theory predicts that the equilibrium number of species on an island, the net number of species resulting from immigration less extinction, is related to the area of the island and its distance from a source region (MacArthur and Wilson 1963, 1967). In numerous studies the relationship between species number, S, and island area, A, has been well described by the power function S = cAz, where c and z are fitted constants. May (1975) has shown that such speciesarea curves are to be expected if the relative abundance of species assumes a lognormal distribution. In such cases z values should lie within the range 0.150.39. As often noted, the species-area relation is an empirical description. Causal mechanisms include the correlation of island area with habitat diversity, and sampling artifact if the number of samples is correlated with island size, as well as the immigration-extinction equilibrium theory (see Connor and McCoy 1979 for review of these hypotheses). All three hypotheses are subsumed by the island paradigm. This body of theory has been used as a powerful tool for the analysis of species richness on real islands and for isolated habitats considered as islands (reviewed in Simberloff 1974; Connor and McCoy 1979). Following Janzens (1968) suggestion, a number of researchers have attempted to apply island biogeography theory, especially the species-area curve, S = cAz, to situations involving animal hosts as islands for parasites (Dritschilo et al. 1975), symbionts of unspecified trophic relationships (Abele 1976; Abele and Patton 1976; Uebelacker 1977), and plant hosts as islands for herbivorous insects (see Strong 1979 for review) and mites (Tepedino and Stanton 1976). Hosts may be regarded as islands at three levels of organization: (1) individuals; (2) populations; (3) species. The studies of Abele (1976), Abele and Patton (1976), Tepedino and Stanton (1976), and Uebelacker (1977) treat individual host organisms or colonies as islands. Seifert (1975), Ward and Lakhani (1977), Lawton (1978), Freeland (1979), and Raupp and Denno (1979) study species richness using host populations as islands. Strong (1974c) and Strong et al. (1977) use the acreage of crops (cacao and sugar cane, respectively) planted in various political units (countries, states, and colonies) as islands. The remaining studies treat the geographic ranges of the host species as islands. The establishment and maintenance of species diversity is one of the central

Parasites and marine invasions.

Introduced marine species are a major environmental and economic problem. The rate of these biological invasions has substantially increased in recent years due to the globalization of the worlds economies. The damage caused by invasive species is often a result of the higher densities and larger sizes they attain compared to where they are native. A prominent hypothesis explaining the success of introduced species is that they are relatively free of the effects of natural enemies. Most notably, they may encounter fewer parasites in their introduced range compared to their native range. Parasites are ubiquitous and pervasive in marine systems, yet their role in marine invasions is relatively unexplored. Although data on parasites of marine organisms exist, the extent to which parasites can mediate marine invasions, or the extent to which invasive parasites and pathogens are responsible for infecting or potentially decimating native marine species have not been examined. In this review, we present a theoretical framework to model invasion success and examine the evidence for a relationship between parasite presence and the success of introduced marine species. For this, we compare the prevalence and species richness of parasites in several introduced populations of marine species with populations where they are native. We also discuss the potential impacts of introduced marine parasites on native ecosystems.

Trophic strategies, animal diversity and body size

A primary difference between predators and parasites is the number of victims that an individual attacks throughout a life-history stage. A key division within natural enemies is whether a successful attack eliminates the fitness of the prey or the host. A third distinctive axis for parasites is whether the host must die to further parasite development. The presence or absence of intensity-dependent pathology is a fourth factor that separates macroparasites from microparasites; this also distinguishes between social and solitary predators. Combining these four dichotomies defines seven types of parasitism, seven corresponding parasites, three forms of predation and, when one considers obligate and facultative combinations of these forms, four types of predator. Here, we argue that the energetics underlying the relative and absolute sizes of natural enemies and their victims is the primary selective factor responsible for the evolution of these different trophic strategies.

Release from parasites as natural enemies: increased performance of a globally introduced marine crab

Introduced species often seem to perform better than conspecifics in their native range. This is apparent in the high densities they may achieve or the larger individual sizes they attain. A prominent hypothesis explaining the success of introduced terrestrial species is that they are typically free of or are less affected by the natural enemies (competitors, predators, and parasites) they encounter in their introduced range compared to their native range. To test this hypothesis in a marine system, we conducted a global assessment of the effect of parasitism and predation on the ecological performance of European green crab populations. In Europe, where the green crab is native, crab body size and biomass were negatively associated with the prevalence of parasitic castrators. When we compared native crab populations with those from introduced regions, limb loss (an estimator of predation) was not significantly lower in introduced regions, parasites infected introduced populations substantially less and crabs in introduced regions were larger and exhibited a greater biomass. Our results are consistent with the general prediction that introduced species suffer less from parasites compared to populations where they are native. This may partly explain why the green crab is such a successful invader and, subsequently, why it is a pest in so many places.