Parasitism may enhance rather than reduce the predatory impact of an invader

Abstract

Invasive species can have profound impacts on communities and it is increasingly recognized that such effects may be mediated by parasitism. The 'enemy release' hypothesis posits that invaders may be successful and have high impacts owing to escape from parasitism. Alternatively, we hypothesize that parasites may increase host feeding rates and hence parasitized invaders may have increased community impacts. Here, we investigate the influence of parasitism on the predatory impact of the invasive freshwater amphipod Gammarus pulex. Up to 70 per cent of individuals are infected with the acanthocephalan parasite Echinorhynchus truttae, but parasitized individuals were no different in body condition to those unparasitized. Parasitized individuals consumed significantly more prey (Asellus aquaticus; Isopoda) than did unparasitized individuals. Both parasitized and unparasitized individuals displayed Type-II functional responses (FRs), with the FR for parasitized individuals rising more steeply, with a higher asymptote, compared with unparasitized individuals. While the parasite reduced the fitness of individual females, we predict a minor effect on population recruitment because of low parasite prevalence in the peak reproductive period. The parasite thus has a large per capita effect on predatory rate but a low population fitness effect, and thus may enhance rather than reduce the impact of this invader.

Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach

“…It is again noteworthy that the biological control literature uses comparative functional responses to make such comparisons, but with different questions in mind. Thus, while Dick et al (2010) explicitly tested the enemy release hypothesis, a study by Farrokhi et al (2010) on Wolbachia-infected parasitoid wasps essentially did the same, but the context was to test the effects of parasitism on the biocontrol efficacy of a control agent (see also Bayoumy 2011). Jones et al (2011) used functional responses of an invasive stoat to examine the dynamics of this predator and its mammal prey.…”

“…Authors then began explicitly comparing invader and native species with functional responses, such as Haddaway et al (2012), who showed an invasive crayfish has a higher functional response than a native. However, this study, as with most others (see Bollache et al 2008;Dick et al 2010), did not explicitly link differential functional responses to actual field patterns of impact on particular prey species; rather, the prey species were chosen to illustrate the methodology and general pattern of higher functional responses of invaders compared to natives. More recently, however, Dick et al (2013) demonstrated that the invasive 'bloody red' shrimp Hemimysis anomala has a higher functional response to several prey species than trophically analogous native species (that are also themselves invasive in some regions) and, more intriguingly, that the greatest invader/native differentials in functional responses were associated with the greatest field impacts of the invader (Fig.…”

“…see Kestrup et al 2011). Further, since factors such as parasitism of invaders/ natives can be included in study designs, the methodology allows for the robust testing of other major hypotheses in invasion ecology, such as 'enemy release' (see Dick et al 2010; Fig. 2 …”

“…Dick et al (2010) then used the comparative functional response method within an invasive species, showing that an invasive predatory amphipod, Gammarus pulex, had a higher Type II functional response when parasitized with an acanthocephalan worm, counter to the enemy release hypothesis, illustrating the utility of the method in tests of major invasion biology hypotheses (see below). It is again noteworthy that the biological control literature uses comparative functional responses to make such comparisons, but with different questions in mind.…”

Functional responses can unify invasion ecology

“…Although abiotic and biotic context-dependencies have been a major challenge to ecological impact prediction in invasion ecology Kumschick et al 2015), we contend that functional responses can go a long way to mitigate this problem. By explicitly incorporating relevant context-dependencies into functional response study designs and hypothesis testing, both explanatory and predictive power are enhanced (Dick et al 2010;Paterson et al 2015;Barrios-O'Neill et al 2016); for example, functional responses of invasive meso-predators may be affected by the presence of higher predators (Barrios-O'Neill et al 2014) and impact predictions from such studies can be made even with regards to the complex world of real communities. Similarly, consideration of changes or differences in the physical environment, such as habitat complexity and water chemistry, can allow impact prediction, owing to shifts in the shape and magnitude of functional responses under such context-dependencies (e.g.…”