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Invasive species disrupt native communities world-wide, affecting biodiversity, community structure and processes across a range of ecosystems (Elton 1958; Williamson 1996; Davis 2009). Invasions can have devastating impacts on natural communities, on agriculture and on human health. Hence, understanding, predicting and managing biological invasions represents a global challenge. From individuals to ecosystems, parasites are pervasive. Parasites, by definition, cause harm to their hosts. Furthermore, parasites can have both positive and negative effects on populations of non-host species, with consequences that cascade throughout communities (Hatcher, Dick & Dunn 2012a). Here, we investigate, across scales, the role of parasites and pathogens and the infections they cause in invasion ecology. The need to synthesize, and to predict and understand ‘Invasions and Infections’, brought leading ecologists together at the British Ecological Society Annual Meeting (UK 2011). In this special issue of Functional Ecology, we bring together a series of studies, stimulated by this meeting, that consider the wide ranging effects of parasites in biological invasions.

Historically, ecological studies have tended to focus on competitive and predatory interactions, often ignoring the role of parasites in ecological communities. However, although often inconspicuous, parasites are ubiquitous and parasitism may be the most common consumer strategy of all (Lafferty et al. 2008). Recent studies have highlighted the abundance and importance of parasites in ecological communities (Hatcher & Dunn 2011; Tompkins et al. 2011). For example, parasites dominate food web links in a salt marsh ecosystem in California, and the biomass of parasitic trematodes equals that of shrimp, worms, fish and birds combined (Lafferty, Dobson & Kuris 2006; Kuris et al. 2008). Parasites not only have direct effects on individual host fitness. They can act as keystone species in determining coexistence outcomes for competing species; they can alter predator–prey and herbivore–plant interactions; and they can alter the success of other parasites in the community (Telfer et al. 2010; Hatcher & Dunn 2011). As a result, the effects of parasites may cascade through the community, driving changes in biodiversity and eco-system function (Hatcher, Dick & Dunn 2012a). For example, the outbreak of rinderpest in East Africa in the 1890s led to massive herbivore mortality and consequent changes in plant community compositions. The eradication of the disease in the 1960s resulted in increased herbivore abundance which in turn led to increased carnivore densities, and these long-term trophic changes have altered the carbon budget of the Serengeti ecosystem (Thomas, Renaud & Gue′gan 2005; Holdo et al. 2009).

The last decade has seen a burgeoning interest in the role that parasites can play in determining the impact and success of biological invasions (Prenter et al. 2004; Dunn 2009; Tompkins et al. 2011). Biological invasions often lead to altered host–parasite relationships that in turn influence a range of community interactions. Indeed, parasitic disease is cited as a driver behind the economic, medical or conservation impact of nearly a quarter of species listed on the IUCN ‘world's worst invaders’ list (Hatcher, Dick & Dunn 2012b). Invasive species may benefit from loss of natural enemies, including parasites (Mitchell & Power 2003; Torchin et al. 2003; Roy & Handley 2012). Biological invasion can also lead to novel host–parasite interactions, with the outcome dependent on immunological, behavioural and ecological factors (Ugelvig & Cremer 2012; White & Perkins 2012). Invaders may acquire parasites from the new environment, with the potential to amplify the impact of the parasite on native species. Furthermore, they may introduce novel parasites providing opportunity for emerging diseases in native hosts (Strauss, White & Boots 2012); emerging infectious diseases are themselves examples of biological invaders (Hatcher, Dick & Dunn 2012b). The changes in host–parasite relationships that result from the biological invasions can have profound effects on parasite–host dynamics, on the success of an introduced species and on its impact on the recipient community (Dunn et al. 2012; Roy & Handley 2012; Strauss, White & Boots 2012).

The rapid development of research into infection and invasions stimulated a Thematic Topic ‘Parasites and Invasions’ at the 2011 British Ecological Society Annual Meeting in Sheffield, chaired by Alison Dunn and Sarah Perkins. We were pleased to welcome speakers from twelve institutes in four countries, with a keynote talk from Mark Torchin of the Smithsonian Research Institute in Panama. The session stimulated lively discussions which continued after the session into the pubs of Sheffield. We were, therefore, delighted when Chuck Fox asked us to edit this special issue of Functional Ecology which brings together studies from key groups in this growing research area. This issue looks at parasitic infections and invasions from a number of perspectives.

The first three studies consider how changes in host–parasite relationships may influence invasion success and impact. Helen Roy & Lori Handley explore new tools to investigate the processes of enemy release, parasite spillover and spillback. They explore the various changes in host–parasite relationships that may influence invasion success and impact, looking at enemy release, parasite spillover and spillback in the context of invasive insects, looking in particular at the harlequin ladybird Harmonium axyridis, a predator that was initially introduced for biocontrol. They argue that, whilst the need to study invasions within a community context is accepted (e.g. Shea & Chesson 2002), many studies of parasites in invasions tend to focus on pairwise interactions. Recent studies illustrate that the effects of parasites extend beyond the host population to influence biological communities and ecosystem functioning (Tompkins et al. 2011; Hatcher, Dick & Dunn 2012a), with some notable examples of community-wide effects discussed in this issue (Dunn et al. 2012). Roy & Handley propose ecological network analysis as a method to explore the strength of interspecific interactions and community robustness to disturbance. In the context of invasions, they describe predicted parasite community characteristics under the processes of enemy release, spillover and spillback and explore the use of molecular sequence data to understand ecological network structure.

Alex Strauss, Andrew White & Mike Boots consider the role of parasites as novel weapons that mediate the outcome of biological invasions. Such novel weapons include native parasites for which the invasive species provides a new reservoir for parasite spillback to native hosts; and novel parasites that spillover from invading to native hosts. The authors argue that spillover diseases represent indirect mutualisms that can drive both species invasions and disease emergence. A review of disease-mediated invasions reveals that spillback is more common amongst plant invasions, whilst spillover if more often reported for animal invasions, reflecting the phylogenetic similarities common in species replacements by animal invaders. Strauss, White & Boots then review disease-mediated displacement of the UK red squirrel by the invasive grey squirrel. The authors argue that cases of disease-mediated invasion may be more common than we realize. The authors call for more biological realism in invasion models and specifically highlight the importance of stochastic fade-out of the population during invasion, as well as more deterministic factors specific to the host–parasite system, such as age structure and immunity.

Ali Dunn and colleagues (Mark Torchin, Mel Hatcher, Peter Kotanen, Dana Blumenthal, Jeb Byers, Courtney Coon, Victor Frankel, Bob Holt, Ruth Hufbauer, Andrew Kanarek, Kristina Schierenbeck, Lorne Wolfe & Sarah Perkins) explore the indirect effects of parasites in a range of trophic interactions between native and invasive species. Such effects may be density-mediated or trait-mediated. Trait-mediated effects of parasites are often overlooked despite parasites having wide reaching effects on host behaviour and life histories. The authors consider the influence of parasitism on competitive interactions as well as on consumer–resource interactions, using a breadth of examples from plant and animal invasions. They illustrate the importance of the indirect effects of parasites in key invasion processes including enemy release, apparent competition, parasite-mediated competition and consumer–resource interactions. They also consider the host-mediated indirect effects on parasite–parasite interactions within a host, demonstrating that these effects may be mediated by competition for resources, as well as by host immune responses. These indirect effects are important at a range of biological scales from within a host to the whole eco-system in determining invasion success and impact.

In the fourth study, Mel Hatcher, Jaimie Dick & Ali Dunn explore the ecological and evolutionary parallels and differences between the processes of invasion and emergent disease. Biological invasions can be modelled as a series of stages with ecological and evolutionary barriers affecting the progress between stages (e.g. Kolar & Lodge 2001; Blackburn et al. 2011), and these conceptual models are useful in understanding the abiotic and biotic processes that determine invasion success. Hatcher and colleagues argue that the emergence of novel disease in a new host is, in essence, an example of a biological invasion. Emerging infectious diseases can have world-wide economic, medical, social and conservation impacts; they threaten human and agricultural populations as well as natural populations with disease outbreaks having potential community-wide effects. Well-known examples include the 2009 human flu pandemic, the loss of American chestnuts to chestnut blight and the 1967 and 2001 outbreaks of foot and mouth disease in cattle in the UK. Hatcher et al. illustrate that the phases of disease emergence and biological invasions have many parallels, particularly the early and late phases, where demographic and anthropogenic factors are key drivers and where opportunities and constraints on control and management occur. However, host–parasite co-evolution plays a crucial role in determining parasite establishment in novel hosts; whilst exploitation of host immune responses offers additional control opportunities against emerging infectious diseases.

As parasites mediate invasions, so too can community change under biological invasions influence parasite population dynamics and communities, a subject explored by Sandra Telfer & Kevin Bown in the fifth study. Recent years have seen a rapid increase in our awareness of how parasites influence invasion outcomes. Telfer & Bown, argue that changes in the structure and interactions of invaded communities can, in turn, influence parasite population dynamics and communities. When parasites are themselves introduced, establishment and spread depends on the abundance of competent hosts or vectors in the invaded community. The authors also explore the impact of invasions on native parasites noting that the mode of transmission (frequency/density dependent) affects likelihood of amplification vs. dilution effects. These authors also point out the need to consider interactions in the context of the community, as illustrated in the replacement of native snails by the Japanese mud snails. Here, invader driven declines in native hosts are predicted to lead to local extinction of multiple parasites (Torchin, Byers & Huspeni 2005). The authors go on to consider the importance of the parasite community in parasite population dynamics, as illustrated by the negative correlation between intestinal nematodes and introduced bovine tuberculosis in buffalo (Michel et al. 2006). They call for consideration of community (host and parasite) level interactions to inform theoretical and empirical studies of disease risk.

Social insects, including some species of ants and termites feature on the IUCN's list of the ‘world's worst invaders’, worthy of their place on this list perhaps because of the dramatic behavioural changes induced during invasion. In the sixth study, Line Ugelvig & Sylvia Cremer describe how infections may be altered by the interaction between social immunity and unicoloniality. Invasive social insects form huge supercolonies; a feature of the invaded range whilst their native counterparts remain relatively benign – forming only small territorial groups. A mechanism promoting the supercolony, otherwise known as unicoloniality, could be that of social immunity – collective anti-parasite behavioural defences including prophylactic removal of infected nest mates (Cremer, Armitage & Schmid-Hempel 2007). Whilst unicoloniality and the social immunity behaviours that accompany it provide a powerful colony-level protection against epidemics, the population genetic processes associated with invasions may interact with unicoloniality to increase the potential for epidemics. Social insects may be particularly vulnerable to these effects as their effective population sizes are very small compared with the number of individuals per population, because only the queens and males reproduce. As such, disease spread is likely to be facilitated in these genetically homogenous populations. In addition, reduced genetic diversity at the colony-level has been found to compromise the efficiency of social immune responses (Ugelvig et al. 2010). Taken together, these factors may instead lead to long-term instability of unicolonial invasive species. This review highlights the importance of observations across scales, from individual to colony, but also the interaction between behavioural and genetic process to give an overview of what is known to date on altered host–parasite interactions in unicolonial social insects, whilst highlighting how their social lifestyle and their interaction with parasites may contribute to invasion success or failure.

Ecological and population genetic processes can also alter physiological immunity under relaxed parasite-mediated selection associated with parasitic enemy release. In the final study, White & Perkins examine the physiological changes in immunity that occur in invaders, and the population genetic processes acting upon them during establishment and range expansion, an area that has attracted interest in recent years (Shine, Brown & Phillips 2011). Invasive species tend to ‘lose’ their parasites. They should thus invest less of their resources into energetically expensive aspects of the immune system and instead invest more energy in dispersal, growth and reproduction (Blossey & Nötzold 1995). Parasite loss either during establishment or during range expansion is expected to lead to loss of resistance (Duncan, Fellous & Kaltz 2011). As an invasive species expands its range, selection will strongly favour increased growth and reproduction, traits that may trade-off against immune function. White & Perkins argue that relaxed parasite-mediated selection should be particularly pronounced at the wave-front of the invasion during the range expansion stage. Invaders also lose genetic diversity during the process and possibly specific alleles important in fighting parasites, an effect that may make the population vulnerable to novel pathogens or those arriving with subsequent waves of invasion of the same or similar species; an important observation in terms of invasive species control. Of all the areas reviewed in the Special Feature, this one calls loudest for more empirical studies. The ecoimmunology of invasions has been discussed for a few years now (Lee & Klasing 2004), but as yet no biogeographical comparisons of ecoimmunology have been carried out, and there is currently little empirical data on the ecoimmunology and immunogenetics of invasions.

The studies in this Special Feature highlight the importance of parasites at all ecological levels, from the individual to the ecosystem, in all types of ecological communities, whether terrestrial, freshwater, marine or managed. But there is still a need for further work. As is typical with an assimilation of the current literature, the authors collectively call for increased empirical studies. Whilst certain areas are well-enough studied for us to start generalizing across studies (e.g. Dunn et al. 2012, in this issue), other topics suffer from a paucity of empirical work that prevents generalization. For example, there are only a handful of studies of disease-mediated invasions (described by Strauss et al. 2012), whilst White & Perkins found that there are no biogeographical ecoimmunological comparisons, instead drawing on analogous research such as range expansions. Typically, where empirical studies are lacking, we must draw on theory but here there is also room for improvement and development. Telfer & Bown, this issue suggest that future studies should aim to further elucidate the key processes influencing disease dynamics in multi-host (and multi-parasite) communities, thereby informing predictions of how invasive host and parasite species, and changes in biodiversity, will influence disease risk. Strauss, White & Boots suggest that considerable improvements could be made to theoretical studies by incorporating more biological realism into models. As we reveal the greater layers of complexity in ‘Invasions and Infections’, the extent of which is revealed in this issue, so there is increasing need to add this biological realism to our models. There is, however, a trade-off in the level of biological realism introduced and the tractability of model. This brings us back to the need for further empirical studies that can inform us on the importance of direct and indirect effects of parasites in invasions.

One important observation made by contributors in this special feature is that pairwise host–parasite interactions are important, but that they represent only one part of a more complex story. The parasite community within a host is itself a fully interacting community. Furthermore, this community of parasites indirectly affects non-host species within an ecological community. As such, we specifically propose that empirical studies must go beyond a one host-one parasite paradigm and must acknowledge the scale of the ‘invasions and infections’ theme described in this issue, from molecular modifications (e.g. immunogenetics) to trophic cascades resonating through an ecosystem. Such studies will require greater integration between fields. Indeed, an interesting emphasis in several of the studies is the need for greater cross-disciplinary interactions to provide insight into the prediction, control and management of invasions, between disease emergence and invasion biology (Hatcher, Dick & Dunn 2012b), ecological network analysis and parasitology (Roy & Handley 2012), immunology and ecology (White & Perkins 2012), behaviour and genetics (Ugelvig & Cremer 2012) and theoretical and empirical approaches (Strauss, White & Boots 2012). Such approaches should provide novel insight into the interactions between infection and invasions and their impact at multiple scales.

References

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