Melanie J. Hatcher

Diverse effects of parasites in ecosystems: linking interdependent processes

Community ecologists generally recognize the importance of species – such as pollinators – that have clear positive effects within ecosystems. However, parasites – usually regarded in terms of their detrimental effects on the individuals they infect – can also have positive impacts on other species in the community. We now recognize that parasites influence species coexistence and extirpation by altering competition, predation, and herbivory, and that these effects can, in turn, influence ecosystem properties. Parasites and pathogens act as ecosystem engineers, alter energy budgets and nutrient cycling, and influence biodiversity. Equally, because ecosystem properties – such as biodiversity – affect parasite populations, there is the potential for feedback between parasitism and ecosystem states. Using examples from animal and plant systems, we examine this potential bidirectional interdependence and challenge the conventional wisdom that parasites have only negative or inconsequential impacts on ecological communities.

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

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 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.

Parasite-mediated predation between native and invasive amphipods

Parasites can structure biological communities directly through population regulation and indirectly by processes such as apparent competition. However, the role of parasites in the process of biological invasion is less well understood and mechanisms of parasite mediation of predation among hosts are unclear. Mutual predation between native and invading species is an important factor in determining the outcome of invasions in freshwater amphipod communities. Here, we show that parasites mediate mutual intraguild predation among native and invading species and may thereby facilitate the invasion process. We find that the native amphipod Gammarus duebeni celticus is host to a microsporidian parasite, Pleistophora sp. (new species), with a frequency of infection of 0–90%. However, the parasite does not infect three invading species, G. tigrinus, G. pulex and Crangonyx pseudogracilis. In field and laboratory manipulations, we show that the parasite exhibits cryptic virulence: the parasite does not affect host fitness in single–species populations, but virulence becomes apparent when the native and invading species interact. That is, infection has no direct effect on G. d. celticus survivorship, size or fecundity; however, in mixed–species experiments, parasitized natives show a reduced capacity to prey on the smaller invading species and are more likely to be preyed upon by the largest invading species. Thus, by altering dominance relationships and hierarchies of mutual predation, parasitism strongly influences, and has the potential to change, the outcome of biological invasions.

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

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.

Disease emergence and invasions

Summary Emerging infectious diseases (EIDs) are recognized as having significant social, economic and ecological costs, threatening human health, food security, wildlife conservation and biodiversity. We review the processes underlying the emergence of infectious disease, focusing on the similarities and differences between conceptual models of disease emergence and biological invasions in general. Study of the IUCNs list of the worlds worst invaders reveals that disease is cited as a driver behind the conservation, medical or economic impact of nearly a quarter of the species on the data base. The emergence of novel diseases in new host species are, in essence, examples of invasions by parasites. Many of the ecological and anthropogenic drivers of disease emergence and classical invasions are also shared, with environmental change and global transport providing opportunities for the introduction and spread of invaders and novel parasites. 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. However, there are also differences in the intermediate phases, where host–parasite co‐evolution plays a crucial role in determining parasite establishment in novel hosts. Similar opportunities and constraints on control and management occur at the different phases of invasions and disease emergence. However, exploitation of host immune responses offers additional control opportunities through contact control and vaccination against EIDs. We propose that cross‐fertilization between the disciplines of disease emergence and invasion biology may provide further insights into their prediction, control and management.

Evolutionary ecology of vertically transmitted parasites: transovarial transmission of a microsporidian sex ratio distorter in Gammarus duebeni

Vertically transmitted parasites are transmitted from generation to generation of hosts usually via the hosts gametes. Owing to gamete size dimorphism, the major transmission route is transovarial and selection (on the parasite) favours strategies which increase the relative frequency of the transmitting (female) host sex. These strategies impose unusual selection pressures on the host, and coevolution between hosts and vertically transmitted parasites has been implicated in speciation, in the evolution of symbiosis, and in the evolution of novel systems of host reproduction and sex determination. We review the evolutionary implications of vertically transmitted parasites in arthropods before focusing on strategies of transmission of a parasitic sex ratio distorter in Gammarus duebeni . The efficiency of parasite transmission to new hosts is a key factor underlying the relationship between vertically transmitted parasites and their hosts. Vertically transmitted parasites must overcome 2 bottlenecks in order to ensure successful infection of future host generations: first, transmission from adult to gamete; and secondly, transmission to the germ-line of the infected host. We investigate these 2 processes with regard to transovarial transmission by a microsporidian parasite in Gammarus duebeni . Parasite transmission from adult to eggs is highly efficient, with 96% of eggs of infected mothers inheriting the infection, whereas transmission to germ-line within infected embryos is relatively inefficient (72%). We measure parasite distribution between cells of developing embryos, and use these distributions to infer possible mechanisms of parasite transmission to germ-line. Parasite distribution within the embryo is dependent on host cell lineage, and is not consistent with unbiased segregation between daughter cells. These results indicate that parasites segregate together at host cell division, and may reflect a strategy of differential segregation to the host germ-line. We consider alternative parasite strategies at the cell-level in terms of their evolutionary implications.

Parasites and biological invasions: parallels, interactions, and control

Species distributions are changing at an unprecedented rate owing to human activity. We examine how two key processes of redistribution - biological invasion and disease emergence - are interlinked. There are many parallels between invasion and emergence processes, and invasions can drive the spread of new diseases to wildlife. We examine the potential impacts of invasion and disease emergence, and discuss how these threats can be countered, focusing on biosecurity. In contrast with international policy on emerging diseases of humans and managed species, policy on invasive species and parasites of wildlife is fragmented, and the lack of international cooperation encourages individual parties to minimize their input into control. We call for international policy that acknowledges the strong links between emerging diseases and invasion risk.

Persistence of selfish genetic elements: population structure and conflict.

Selfish genetic elements are vertically transmitted factors that spread by obtaining a transmission advantage relative to the rest of the genome of their host organism, often with a cost to overall host fitness. In many cases, conventional population genetics theory predicts them spreading through populations, reaching fixation and becoming undetectable or sometimes driving the population extinct. However, in several well studied systems, these genetic elements are known to persist at relatively low, stable frequencies. Recent research suggests that several processes might explain these observations, including population structure, intragenomic conflict and coevolution.

Two species of feminizing microsporidian parasite coexist in populations of Gammarus duebeni

Abstract The amphipod crustacean Gammarus duebeni hosts two species of vertically transmitted microsporidian parasites, Nosema granulosis and Microsporidium sp. A. Here it is demonstrated that these co‐occurring parasite species both cause infected females to produce female‐biased broods. A survey of European G. duebeni populations demonstrates that these two parasites co‐occur in six of 10 populations. These findings contrast with the theoretical prediction that two vertically transmitted feminizing parasites should not coexist in a panmictic population of susceptible hosts at equilibrium. Possible explanations for the co‐occurrence of the two feminizing microsporidia in G. duebeni include the recent invasion of a new parasite, horizontal transmission of one or both parasites and the spread of alleles for resistance to the dominant parasite in host populations.

The less amorous Gammarus: predation risk affects mating decisions in Gammarus duebeni (Amphipoda)

We examined the trade-off between the behaviours associated with predator avoidance and mate acquisition in the mate-guarding amphipod crustacean Gammarus duebeni. We used laboratory experiments to investigate the impact of olfactory predator cues on activity, mate choice and mate-guarding behaviour of males and females. Pair formation declined under perceived risk of predation, reflecting reduced activity of both males and females and hence a reduced likelihood of encountering a mate. We also observed a reduction in the choosiness of both males and females. Under increased perceived predation risk, assessment of the female by the male was more likely to be followed by pair formation, and males showed a nonsignificant trend towards reduced discrimination in favour of large females and were less tenacious in their pair bond when they paired during exposure to predator cues. Females also showed less resistance behaviour, suggesting that both males and females trade off the costs of maximizing current reproductive success against the benefits of predator avoidance for survival and reproduction in the future. We discuss the implications of such context-dependent mating behaviours for ecological interactions between species and suggest that predators, via the effects of perceived predation risk on mate choice and mate guarding in the prey species, induce trait-mediated indirect effects with the potential to influence population dynamics and community structure.