Final Report Summary - EIGIS (The Ecology and Immunogenetics of Parasites in Invasive Species)
Invasive species are those that have been accidentally or deliberately introduced into new habitats outside of their typical (native) range. Invasive species tend to undergo rapid expansion in population size and distribution which causes millions of Euros of economic damage, owing to perturbation of native species and communities. As such, invaders are recognised as a major economic problem and a conservation issue for native biota. Understanding why invasive species are successful is crucial to determining and implementing effective control strategies and one hypothesis as to why invasive species are so successful is that'enemies'in the invaded range that would otherwise regulate population density are absent; termed the Enemy Release Hypothesis. Typically, enemies are predators, but we also know that parasites and pathogens regulate populations and so can be classed as'enemies'. The main objective of the research fellowship; the'Ecology and Immunogenetics of Invasive Species'(EIGIS) was to determine the ecological and evolutionary role of parasites and pathogens in invasion ecology. As a model system we studied the host-parasite dynamics of a recent invader, the bank vole (Myodes glareolus) in the Republic of Ireland. This woodland rodent, native to the UK and mainland Europe was first noted in Ireland in the 1920's and has been spreading across the country since that time. This invasive species provided us with a unique opportunity to elucidate specifically the role of parasites, as opposed to predators, in the enemy release hypothesis because the suite of predators that regulate the vole population in the native habitat were also present in their invaded habitat.
Using multi-disciplinary tools including molecular ecology, ecoimmunology, parasitology and social network theory we have determined the rate of spread of the invasive vole, changes in the invaders'parasite community, evolutionary adaptations and impacts of the invader on the native flora and fauna. Most importantly, we determined, using over 500 samples, that the invasive vole has lost the majority of its parasite fauna. In the UK and mainland Europe (native vole range) we found the number of parasitic helminths (macrobiome) within the vole to be between 6 and 20 species. In contrast we found that the invasive vole in Ireland hosted a maximum of only 2 species of helminths. In addition we found that localised pockets of total biome depletion occurred, i. e. some vole populations were parasite-free. Spatially, we determined that the parasite-free populations were closest to the invasion front suggesting a link between dispersal and parasitism. Using population models we estimated that the invasive vole has spread across Ireland at a rate of 5-8km per year. Using an intensive capture-mark-recapture study very high estimates of density were produced (> 400ha-1), comparable with mainland populations undergoing'irruptions'. In contrast the density of the only native rodent species to Ireland, the wood mouse, Apodemus sylvaticus was low (< 25ha-1).
In collaboration with Birdwatch Ireland an analysis of over 300 bank vole skull samples from barn owl pellets across the country was carried to determine how the body size of voles changed with increasing distance from the point of introduction. We found that individuals were larger at the invasion front than populations near the introduction site where populations were older and more established. Associating parasite loss with demographic changes (e. g. increased density) and the evolution of increased competitive ability (e. g. increased body size) is difficult with single host-parasite studies. As such, a meta-analysis was conducted in collaboration with the Invasive Species Research Coordination Network (RCN) across different taxonomic groups to determine if invasive species are bigger, more fecund and found in higher densities in their native compared to their invasive range.
Within the Republic of Ireland the density of the native rodent showed a negative relationship with the invasive bank vole, suggesting an antagonistic interaction between the two species, which raises conservation concerns for the native biota. To this effect we investigated whether the invasive bank vole had spread to isolated islands within the Shannon estuary; an area close to its point source of introduction. We found these islands to be vole-free and as such conclude that the islands may be an important refuge for native fauna and be considered as conservation reserves.
Live-trapping sites for rodents were established at the invasion front and focal point of introduction to quantify inter-specific contact rates. The heterogeneity in contacts within a species was as expected, with contacts following a scale-free distribution. The population density of the native mouse was so low where the vole had been established for many years that estimates of inter-specific contact rates were not robust due to low sample sizes. As such, estimates were achieved from the invasion front only. Here, we found the population to be freely-mixed suggesting that direct or indirect competition was not yet taking place within these populations. In addition we did not identify any parasites that were shared between the mice and voles. As such, population regulation by spillover of parasites from the native mice is unlikely to occur, thereby allowing the invasive vole to continue spreading across the country.
In addition to determining whether the vole had undergone enemy release we also examined whether the parasites within the voles'community exhibited enemy release. To test this we selectively removed nematodes only from the macrobiome in voles in their native range. We observed an increased infectious output of the cestodes from voles in the native range. This'super-shedding'(releasing more parasitic stages than average) may be a function of competitive release of the parasites associated with removal of a competitor. Although the cestodes and nematodes are unlikely to directly compete we conclude that competition was likely mediated via host immunity. This observation has implications for disease control as treatment of one parasite may increase those remaining in the biome. Ecoimmunology is a growing tool and new approaches to this field are occurring all the time. Basic immune measurements were related to the macrobiome in the invasive population. However, because the voles only had a maximum of two helminths species assessing patterns was problematic. As such, in parallel with this research we developed a study examining auto and hyper-immune infections in previously collected data from wild and lab rats. We found clear differences in the immune profiles of wild and lab rodents indicating that the macrobiome likely plays a role in these profiles.
The control of invasive species is one of six key strategy areas for the European Union 2020 Biodiversity Strategy and recognising the increasing ecological disruption of invasive species the Commission are currently (2012) developing a strategy for control. Target groups include forestry workers and conservation organisations. Ongoing work establishing the immune profiles of wild rodents in association with parasite loss (biome depletion) and experimental biome repletion aim to elucidate the role of parasitic infection in auto and hyper-immune infections will be of wide-reaching interest to medical practitioners and the general public.
Using multi-disciplinary tools including molecular ecology, ecoimmunology, parasitology and social network theory we have determined the rate of spread of the invasive vole, changes in the invaders'parasite community, evolutionary adaptations and impacts of the invader on the native flora and fauna. Most importantly, we determined, using over 500 samples, that the invasive vole has lost the majority of its parasite fauna. In the UK and mainland Europe (native vole range) we found the number of parasitic helminths (macrobiome) within the vole to be between 6 and 20 species. In contrast we found that the invasive vole in Ireland hosted a maximum of only 2 species of helminths. In addition we found that localised pockets of total biome depletion occurred, i. e. some vole populations were parasite-free. Spatially, we determined that the parasite-free populations were closest to the invasion front suggesting a link between dispersal and parasitism. Using population models we estimated that the invasive vole has spread across Ireland at a rate of 5-8km per year. Using an intensive capture-mark-recapture study very high estimates of density were produced (> 400ha-1), comparable with mainland populations undergoing'irruptions'. In contrast the density of the only native rodent species to Ireland, the wood mouse, Apodemus sylvaticus was low (< 25ha-1).
In collaboration with Birdwatch Ireland an analysis of over 300 bank vole skull samples from barn owl pellets across the country was carried to determine how the body size of voles changed with increasing distance from the point of introduction. We found that individuals were larger at the invasion front than populations near the introduction site where populations were older and more established. Associating parasite loss with demographic changes (e. g. increased density) and the evolution of increased competitive ability (e. g. increased body size) is difficult with single host-parasite studies. As such, a meta-analysis was conducted in collaboration with the Invasive Species Research Coordination Network (RCN) across different taxonomic groups to determine if invasive species are bigger, more fecund and found in higher densities in their native compared to their invasive range.
Within the Republic of Ireland the density of the native rodent showed a negative relationship with the invasive bank vole, suggesting an antagonistic interaction between the two species, which raises conservation concerns for the native biota. To this effect we investigated whether the invasive bank vole had spread to isolated islands within the Shannon estuary; an area close to its point source of introduction. We found these islands to be vole-free and as such conclude that the islands may be an important refuge for native fauna and be considered as conservation reserves.
Live-trapping sites for rodents were established at the invasion front and focal point of introduction to quantify inter-specific contact rates. The heterogeneity in contacts within a species was as expected, with contacts following a scale-free distribution. The population density of the native mouse was so low where the vole had been established for many years that estimates of inter-specific contact rates were not robust due to low sample sizes. As such, estimates were achieved from the invasion front only. Here, we found the population to be freely-mixed suggesting that direct or indirect competition was not yet taking place within these populations. In addition we did not identify any parasites that were shared between the mice and voles. As such, population regulation by spillover of parasites from the native mice is unlikely to occur, thereby allowing the invasive vole to continue spreading across the country.
In addition to determining whether the vole had undergone enemy release we also examined whether the parasites within the voles'community exhibited enemy release. To test this we selectively removed nematodes only from the macrobiome in voles in their native range. We observed an increased infectious output of the cestodes from voles in the native range. This'super-shedding'(releasing more parasitic stages than average) may be a function of competitive release of the parasites associated with removal of a competitor. Although the cestodes and nematodes are unlikely to directly compete we conclude that competition was likely mediated via host immunity. This observation has implications for disease control as treatment of one parasite may increase those remaining in the biome. Ecoimmunology is a growing tool and new approaches to this field are occurring all the time. Basic immune measurements were related to the macrobiome in the invasive population. However, because the voles only had a maximum of two helminths species assessing patterns was problematic. As such, in parallel with this research we developed a study examining auto and hyper-immune infections in previously collected data from wild and lab rats. We found clear differences in the immune profiles of wild and lab rodents indicating that the macrobiome likely plays a role in these profiles.
The control of invasive species is one of six key strategy areas for the European Union 2020 Biodiversity Strategy and recognising the increasing ecological disruption of invasive species the Commission are currently (2012) developing a strategy for control. Target groups include forestry workers and conservation organisations. Ongoing work establishing the immune profiles of wild rodents in association with parasite loss (biome depletion) and experimental biome repletion aim to elucidate the role of parasitic infection in auto and hyper-immune infections will be of wide-reaching interest to medical practitioners and the general public.