Roles of parasites in animal invasions

https://doi.org/10.1016/j.tree.2004.05.002Get rights and content

Abstract

Biological invasions are global threats to biodiversity and parasites might play a role in determining invasion outcomes. Transmission of parasites from invading to native species can occur, aiding the invasion process, whilst the ‘release’ of invaders from parasites can also facilitate invasions. Parasites might also have indirect effects on the outcomes of invasions by mediating a range of competitive and predatory interactions among native and invading species. Although pathogen outbreaks can cause catastrophic species loss with knock-on effects for community structure, it is less clear what impact persistent, sub-lethal parasitism has on native-invader interactions and community structure. Here, we show that the influence of parasitism on the outcomes of animal invasions is more subtle and wide ranging than has been previously realized.

Section snippets

Parasitism of natives and invaders

There are several causes and consequences of differences in parasitism between invaders and natives, including factors associated with the transmission of parasites between hosts and with the translocation of parasites with invaders.

Impacts of host and parasite characteristics on invasion success

Whether parasites survive the translocation process might depend on their mode of transmission. vertically transmitted parasites are more likely to be successfully introduced with their invading hosts than are parasites that rely on horizontal transmission. Vertical transmission is often associated with low parasite virulence, thus increasing the likelihood of both the parasite and the host surviving the invasion process. In addition, vertical transmission to new hosts is not dependent on host

Parasite-mediated competition

Parasites and predators have also been implicated historically in the more indirect mediation of interspecies interactions, primarily through shared natural enemies resulting in apparent competition (35, 36, 37, Table 1). Clearly, therefore, where invader and native hosts differ in prevalence and types of parasitism, there is a role for parasites in determining invader success or failure. Indeed, we must realize that interspecific interactions other than competition, such as predation, might

Parasite mediation of predation: natives and invaders sharing predators

Where invasive and native hosts differ in susceptibility to parasitism and/or in their responses to particular parasites, this might render them differentially vulnerable to shared predators (11, 47, Table 1). Of particular interest are indirectly transmitted parasites that manipulate the behaviour of their intermediate hosts to facilitate transmission to their final host [48]. For example, many species of acanthocephalan induce enhanced activity levels and photophilic (‘light loving’)

Parasite mediation of predation: natives and invaders at the same trophic level

It has been argued that potential of transmission of debilitating parasites by ingestion of infected material should select against cannibalism [51] and might also select against intraguild predation (IGP), where the species are often closely related 30, 52. However, both cannibalism and IGP are common in nature [52]. A recent study showed that a native amphipod G. d. celticus varies widely in the prevalence and burden of the microsporidian parasite Pleistophora mulleri, whereas none of three

Wider implications of parasitism for community structure

There is increasing consensus, therefore, that parasites can mediate the outcome of interspecific interactions, such as competition and predation, and that this might determine the outcome of invader–native interactions. Thus, many examples of two-host, one-parasite scenarios are now explicable in terms of which host ‘wins’. In invasion scenarios, the facilitation of the invasion process through parasites might lead to a species replacement, with the new resident having profoundly different

Concluding remarks

Parasites have wider ranging impacts on community interactions during animal invasions than was previously acknowledged. Future research should thus focus on the impacts of parasitism on broader community scales than has been previously attempted. The global scale of animal invasions necessitates the identification of general patterns of host and parasite characteristics associated with invasion success. Empirical testing of fundamental processes linked to parasitism, thought to facilitate

Acknowledgments

This study was funded by the Natural Environment Research Council, UK (grant GR3/12871). We thank Mark Briffa for comments about the article and John Spicer for discussion of physiological aspects.

Glossary

Glossary

Allee effects:
low density populations, and those with skewed sex ratios, might decline because individuals have lower reproductive rates (e.g. because mating encounters are rare) [34].
Apparent competition:
indirect interaction leading to negative effects of one species on another, mediated through a shared natural enemy, such as predators and parasites. For example, parasite-mediated apparent competition might occur when (i) the parasite differentially affects one competitor, reducing its

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