While there is good evidence linking animal introductions to impacts on native communities via disease emergence, our understanding of how such impacts occur is incomplete. Invasion ecologists have focused on the disease risks to native communities through "spillover" of infectious agents introduced with nonindigenous hosts, while overlooking a potentially more common mechanism of impact, that of "parasite spillback." We hypothesize that parasite spillback could occur when a nonindigenous species is a competent host for a native parasite, with the presence of the additional host increasing disease impacts in native species. Despite its lack of formalization in all recent reviews of the role of parasites in species introductions, aspects of the invasion process actually favor parasite spillback over spillover. We specifically review the animal-parasite literature and show that native species (arthropods, parasitoids, protozoa, and helminths) account for 67% of the parasite fauna of nonindigenous animals from a range of taxonomic groups. We show that nonindigenous species can be highly competent hosts for such parasites and provide evidence that infection by native parasites does spillback from nonindigenous species to native host species, with effects at both the host individual and population scale. We conclude by calling for greater recognition of parasite spillback as a potential threat to native species, discuss possible reasons for its neglect by invasion ecologists, and identify future research directions.
Invasion ecology urgently requires predictive methodologies that can forecast the ecological impacts of existing, emerging and potential invasive species. We argue that many ecologically damaging invaders are characterised by their more efficient use of resources. Consequently, comparison of the classical 'functional response' (relationship between resource use and availability) between invasive and trophically analogous native species may allow prediction of invader ecological impact. We review the utility of species trait comparisons and the history and context of the use of functional responses in invasion ecology, then present our framework for the use of comparative functional responses. We show that functional response analyses, by describing the resource use of species over a range of resource availabilities, avoids many pitfalls of 'snapshot' assessments of resource use. Our framework demonstrates how comparisons of invader and native functional responses, within and between Type II and III functional responses, allow testing of the likely population-level outcomes of invasions for affected species. Furthermore, we describe how recent studies support the predictive capacity of this method; for example, the invasive 'bloody red shrimp' Hemimysis anomala shows higher Type II functional responses than native mysids and this corroborates, and could -013-0550-8 have predicted, actual invader impacts in the field. The comparative functional response method can also be used to examine differences in the impact of two or more invaders, two or more populations of the same invader, and the abiotic (e.g. temperature) and biotic (e.g. parasitism) context-dependencies of invader impacts. Our framework may also address the previous lack of rigour in testing major hypotheses in invasion ecology, such as the 'enemy release' and 'biotic resistance' hypotheses, as our approach explicitly considers demographic consequences for impacted resources, such as native and invasive prey species. We also identify potential challenges in the application of comparative functional responses in invasion ecology. These include incorporation of numerical responses, multiple predator effects and trait-mediated indirect interactions, replacement versus non-replacement study designs and the inclusion of functional responses in risk assessment frameworks. In future, the generation of sufficient case studies for a meta-analysis could test the overall hypothesis that comparative functional responses can indeed predict invasive species impacts.Biol Invasions (2014) 16:735-753 DOI 10.1007/s10530
Summary1. Consumer-resource interactions (i.e. the functional response) underpin decades of ecological advancements. However, selecting, fitting and comparing functional response models using appropriate methods remains a non-trivial endeavour. 2. The R package FRAIR provides tools for selecting and differentiating various forms of consumer functional response models, a consistent interface for fitting and visualising response curves, and a selection of statistically robust methods for comparing fitted parameters. 3. Using real data from crustacean predator-prey systems, we demonstrate the utility of FRAIR, highlighting best practice and common analytical mistakes.
Summary 1. Biological invasions, still occurring worldwide at an alarming rate, are widely acknowledged as threats to the integrity and functioning of ecosystems. In addition to introducing disease, biological invasions have also been linked to sudden increases in the incidence or severity of previously existing diseases. We review and illustrate the potential direct and indirect impacts of introduced species on the dynamics of endemic parasites in freshwater ecosystems. 2. Introduced species may trigger and sustain disease emergence by acting as competent hosts for endemic parasites in which infection is amplified and then ‘spilled back’ to native hosts. In contrast, if introduced species are not suitable hosts for endemic parasites but become infected anyway, they may act as sinks for parasites and thus dilute disease risk for native hosts. 3. Another mechanism by which introduced species can influence endemic parasitic diseases is by altering the relative abundance of one of the parasite’s hosts in ways that could either enhance or reduce disease transmission to other native hosts in the parasite’s life cycle. 4. Introduced species may also alter disease incidence and severity in native hosts through trait‐mediated indirect effects. For example, the introduced species could change the exposure or susceptibility of native hosts to infection by causing alterations in their behaviour or immunocompetence. Also, by directly changing physicochemical conditions and modifying environmental stressors introduced species may indirectly affect native host exposure and/or resistance to disease. 5. A survey of parasites infecting introduced freshwater fish in four distinct geographical areas revealed that use of non‐indigenous hosts by endemic parasites is widespread, mostly involving parasites transmitted via the food chain. 6. We conclude by presenting a framework, based on risk assessment, for the prediction and possible mitigation of the impact of introduced species on endemic diseases and by calling for greater recognition of the potential role of invasive species as triggers of endemic disease emergence.
SUMMARY1. It is well recognised that non-indigenous species (NIS) can affect native communities via the 'spillover' of introduced parasites. However, two other potentially important processes, the 'spillback' of native parasites from a competent NIS host, where the latter acts as a reservoir leading to amplified infection in native hosts, and the 'dilution' of parasitism by a NIS host acting as a sink for native parasites, have either not been tested or largely overlooked. 2. We surveyed the helminth parasite fauna of native New Zealand fish in Otago streams that varied in the abundance of introduced brown trout Salmo trutta, to look for evidence of spillback and ⁄ or dilution. Spillover is not an issue in this system, with trout introduced as parasite-free eggs. 3. Seven native parasite species were present across 12 sites; significant inverse relationships with an index of trout abundance (i.e. dilution) were documented for three species infecting the native upland bully Gobiomorphus breviceps, and one species infecting the native roundhead galaxias Galaxias anomalus.4. An inverse relationship between bully energy status and infection intensity of one parasite species suggests that parasite dilution could have positive effects on bully populations. Our failure to detect similar relationships for the other parasites does not preclude the possibility that dilution is beneficial to native fish, since parasites may have subtle or unmeasured impacts. 5. The parasite dilution patterns reported are compelling in that they occurred across several native host and parasite species; as such they have important implications for invasion ecology, providing an interesting contrast to the largely negative impacts reported for NIS. Mechanisms potentially responsible for the patterns observed are discussed.
SummaryPredatory functional responses play integral roles in predator–prey dynamics, and their assessment promises greater understanding and prediction of the predatory impacts of invasive species. Other interspecific interactions, however, such as parasitism and higher-order predation, have the potential to modify predator–prey interactions and thus the predictive capability of the comparative functional response approach. We used a four-species community module (higher-order predator; focal native or invasive predators; parasites of focal predators; native prey) to compare the predatory functional responses of native Gammarus duebeni celticus and invasive Gammarus pulex amphipods towards three invertebrate prey species (Asellus aquaticus, Simulium spp., Baetis rhodani), thus, quantifying the context dependencies of parasitism and a higher-order fish predator on these functional responses. Our functional response experiments demonstrated that the invasive amphipod had a higher predatory impact (lower handling time) on two of three prey species, which reflects patterns of impact observed in the field. The community module also revealed that parasitism had context-dependent influences, for one prey species, with the potential to further reduce the predatory impact of the invasive amphipod or increase the predatory impact of the native amphipod in the presence of a higher-order fish predator. Partial consumption of prey was similar for both predators and occurred increasingly in the order A. aquaticus, Simulium spp. and B. rhodani. This was associated with increasing prey densities, but showed no context dependencies with parasitism or higher-order fish predator. This study supports the applicability of comparative functional responses as a tool to predict and assess invasive species impacts incorporating multiple context dependencies.
Interactions among multiple anthropogenic stressors threaten freshwater fish and pose challenges for fisheries management and conservation. Previous studies of multiple‐stressor effects on freshwater fish suggest a prevalence of antagonistic interactions. However, taxonomy, life stage and/or environmental context likely modify the magnitude and direction of fish responses to multiple stressors. Stressor intensity, impact mechanism, exposure time and ecosystem size may further affect interaction outcomes. Large‐scale studies quantifying how these variables moderate stressor interactions are lacking. To address this knowledge gap, we performed a meta‐analysis of 29 factorial multiple‐stressor experiments to examine the influence of seven potential moderator variables on the magnitude and direction of stressor interactions. Using weighted random‐effects meta‐analytic models, we demonstrate the importance of taxonomic identity and life stage for interaction outcomes. In particular, Cypriniformes showed stronger antagonisms than Salmoniformes, as did larval fish compared to juveniles. Interaction outcomes also varied among the measured fish responses with survival yielding stronger antagonisms than biomass. Increasing experimental duration and volume of the experimental units both drove interactions towards synergisms, supporting findings from previous studies that synergisms take time and space to develop. In an era when the number of stressors affecting freshwater systems is increasing rapidly, our study provides a vital step towards identifying generalities in multiple‐stressor outcomes and thus improved predictions of multiple‐stressor impacts. Furthermore, our meta‐analysis complements studies in real streams, rivers and lakes by providing an experimentally derived context for the growing number of multiple‐stressor assessments in research, management and conservation of freshwater fish.
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