As a consequence of the increase in infectious disease emergence in wildlife due to translocations of hosts and pathogens, in recent years the interest about the role played by parasites in alien species settlement and in their interactions with native species is growing. Here, we used native Eurasian red squirrels (Sciurus vulgaris) and alien Eastern grey squirrels (S. carolinensis) as model system in a broad study aimed at shedding light on host-parasite relationships in the context of biological invasions. First, we investigated macroparasite fauna of red squirrels over a wide geographic area, showing that the species has a poor parasite community (both in terms of species richness and diversity across habitats). In particular, the gastro-intestinal helminth community of red squirrels is dominated by a single species, the oxyurid Trypanoxyuris sciuri, hence, the native host may be particularly vulnerable to parasite spillover from alien species. Indeed, we recorded, for the first time in Europe, the presence of the Nearctic nematode Strongyloides robustus in two red squirrels co-inhabiting with alien grey squirrels. We then investigated macroparasite fauna of grey squirrels in Northern Italy, demonstrating that this invasion holds the premises for both spillover and spill-back mechanisms towards red squirrels to occur since grey squirrels introduced to Italy S. robustus and acquired the red squirrel's flea Cerathopyllus sciurorum. Nevertheless, despite the acquisition of some European parasites, the number of parasite species infecting grey squirrels in the introduction range is much lower than in their native range, thus supporting the enemy-release hypothesis. In a third step of the study, through indirect parasitological methods, we compared prevalence of the nematodes S. robustus and T. sciuri in red squirrels living in presence and absence of the alien congener. Our results show that infection by S. robustus is linked to grey squirrels' presence, confirming that red squirrels acquire this parasite via spillover from the invader. Interestingly, also prevalence of T. sciuri is higher in populations syntopic with grey squirrels, suggesting an increased susceptibility to infection induced by stress-mediated effects on the immune system. Finally, we conducted a survey of Ljungan virus and adenovirus infection in both sciurids, extending the host spectrum of Ljungan virus (i.e. a potential zoonoses previously thought to infect only small ground-dwelling rodents) to red squirrels and the distribution of adenoviral infections in squirrels to Southern Europe. Overall, our work highlights the importance of taking into account parasitological aspects when dealing with biological invasions. In particular, despite the role played by macroparasites in invasions is often neglected, we show that it should not be underestimated since they have the potential to mediate interactions between native species and invaders as much as microparasites do. We also show that a complete picture of parasites infecting native species is not only essential to detect alterations caused by invaders, but may also offer insights into their vulnerability to invasions, with hosts having poor parasite communities being more susceptible to competition mediated by parasites. Moreover, we demonstrate that the threat is not only posed by spillover of introduced parasites resulting in apparent competition, but that the presence of alien species may also alter pre-existent host-parasite dynamics and affect native hosts' response to local parasites. At the same time, our findings opened several new questions that will need to be addressed in the future. First, having confirmed that S. robustus spills over to the native species, the next step should be to investigate its impact on red squirrel fitness (i.e. survival and/or fecundity). However, in a parallel study on S. robustus infecting grey squirrels, we highlighted a density-dependence between parasite fecundity and intensity of infection, suggesting that the parasite is able to substantially affect immune response of its hosts. Similarly, it would be interesting to test if the presence of grey squirrels leads to an alteration of C. sciurorum temporal distribution or to an increase of flea abundance in red squirrels. We also show that grey squirrels lost many parasite species during the introduction process, but to test whether this loss actually translates into an effective advantage for the invading species, an experimental study at the biogeographical scale would be needed. Moreover, our results on Ljungan virus suggest that the role of arboreal sciurids in zoonotic diseases circulation could have been underestimated and should be investigated more deeply without forgetting that, despite we did not detect Ljungan virus infection in grey squirrels, the alien species may act as reservoir for other microparasites, increasing their presence in the environment or altering their dynamics, thus representing a threat for public health. In conclusion, we feel that similar, broad surveys on the role of parasites in biological invasions, should be extended to other alien vertebrates since they could offer new insights on the processes regulating the competition with native species and a more complete understanding of invaders' impacts on ecosystems and human activities.

Squirrels, invasions and parasites : lessons learnt and future perspectives / C. Romeo, L.A. Wauters, A. Martinoli, N. Saino, P. Lanfranchi, N. Ferrari. - In: HYSTRIX. - ISSN 0394-1914. - 25:suppl.(2014), pp. 54-54. (Intervento presentato al 9. convegno Congresso Italiano di Teriologia tenutosi a Civitella Alfedena (AQ) nel 2014).

Squirrels, invasions and parasites : lessons learnt and future perspectives

C. Romeo;N. Saino;P. Lanfranchi;N. Ferrari
2014

Abstract

As a consequence of the increase in infectious disease emergence in wildlife due to translocations of hosts and pathogens, in recent years the interest about the role played by parasites in alien species settlement and in their interactions with native species is growing. Here, we used native Eurasian red squirrels (Sciurus vulgaris) and alien Eastern grey squirrels (S. carolinensis) as model system in a broad study aimed at shedding light on host-parasite relationships in the context of biological invasions. First, we investigated macroparasite fauna of red squirrels over a wide geographic area, showing that the species has a poor parasite community (both in terms of species richness and diversity across habitats). In particular, the gastro-intestinal helminth community of red squirrels is dominated by a single species, the oxyurid Trypanoxyuris sciuri, hence, the native host may be particularly vulnerable to parasite spillover from alien species. Indeed, we recorded, for the first time in Europe, the presence of the Nearctic nematode Strongyloides robustus in two red squirrels co-inhabiting with alien grey squirrels. We then investigated macroparasite fauna of grey squirrels in Northern Italy, demonstrating that this invasion holds the premises for both spillover and spill-back mechanisms towards red squirrels to occur since grey squirrels introduced to Italy S. robustus and acquired the red squirrel's flea Cerathopyllus sciurorum. Nevertheless, despite the acquisition of some European parasites, the number of parasite species infecting grey squirrels in the introduction range is much lower than in their native range, thus supporting the enemy-release hypothesis. In a third step of the study, through indirect parasitological methods, we compared prevalence of the nematodes S. robustus and T. sciuri in red squirrels living in presence and absence of the alien congener. Our results show that infection by S. robustus is linked to grey squirrels' presence, confirming that red squirrels acquire this parasite via spillover from the invader. Interestingly, also prevalence of T. sciuri is higher in populations syntopic with grey squirrels, suggesting an increased susceptibility to infection induced by stress-mediated effects on the immune system. Finally, we conducted a survey of Ljungan virus and adenovirus infection in both sciurids, extending the host spectrum of Ljungan virus (i.e. a potential zoonoses previously thought to infect only small ground-dwelling rodents) to red squirrels and the distribution of adenoviral infections in squirrels to Southern Europe. Overall, our work highlights the importance of taking into account parasitological aspects when dealing with biological invasions. In particular, despite the role played by macroparasites in invasions is often neglected, we show that it should not be underestimated since they have the potential to mediate interactions between native species and invaders as much as microparasites do. We also show that a complete picture of parasites infecting native species is not only essential to detect alterations caused by invaders, but may also offer insights into their vulnerability to invasions, with hosts having poor parasite communities being more susceptible to competition mediated by parasites. Moreover, we demonstrate that the threat is not only posed by spillover of introduced parasites resulting in apparent competition, but that the presence of alien species may also alter pre-existent host-parasite dynamics and affect native hosts' response to local parasites. At the same time, our findings opened several new questions that will need to be addressed in the future. First, having confirmed that S. robustus spills over to the native species, the next step should be to investigate its impact on red squirrel fitness (i.e. survival and/or fecundity). However, in a parallel study on S. robustus infecting grey squirrels, we highlighted a density-dependence between parasite fecundity and intensity of infection, suggesting that the parasite is able to substantially affect immune response of its hosts. Similarly, it would be interesting to test if the presence of grey squirrels leads to an alteration of C. sciurorum temporal distribution or to an increase of flea abundance in red squirrels. We also show that grey squirrels lost many parasite species during the introduction process, but to test whether this loss actually translates into an effective advantage for the invading species, an experimental study at the biogeographical scale would be needed. Moreover, our results on Ljungan virus suggest that the role of arboreal sciurids in zoonotic diseases circulation could have been underestimated and should be investigated more deeply without forgetting that, despite we did not detect Ljungan virus infection in grey squirrels, the alien species may act as reservoir for other microparasites, increasing their presence in the environment or altering their dynamics, thus representing a threat for public health. In conclusion, we feel that similar, broad surveys on the role of parasites in biological invasions, should be extended to other alien vertebrates since they could offer new insights on the processes regulating the competition with native species and a more complete understanding of invaders' impacts on ecosystems and human activities.
sciurus vulgaris ; sciurus carolinensis ; parasite mediated competition ; enemy release
Settore VET/06 - Parassitologia e Malattie Parassitarie degli Animali
Settore BIO/07 - Ecologia
2014
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Utilizza questo identificativo per citare o creare un link a questo documento: https://hdl.handle.net/2434/239162
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