Nowadays, invasive species are among the greatest threats to biodiversity, economy and public health. A better knowledge of the processes involved in biological invasions is therefore important to predict invasion pattern and success, in order to improve alien species management and native species conservation strategies. Since 1948, the Eastern grey squirrel (Sciurus carolinensis), a North-American alien species, has been repeatedly introduced in North-Western Italy (Piedmont, Liguria and Lombardy), causing local extinction of the native Eurasian red squirrel (Sciurus vulgaris) through exploitation competition for food. In Great Britain, where grey squirrels have been introduced since 1800, this replacement process is accelerated by the presence of Squirrelpox Virus (SQPV), which is carried by the invasive species without any pathogenic effect, but is lethal to red squirrels. SQPV is thus example of how parasites and pathogens can play an important role in biological invasions via two different processes. First, during the invasion process alien species often lose part of their parasite community (“parasite release”), with a positive impact on their population growth and consequently on their settlement and spread. Second, parasites may mediate the impact of invasive species on native taxa (“parasite-mediated competition”), acting as reservoir for local parasites or introducing in the environment novel parasites to which native species are not adapted . Our purpose is to explore gastro-intestinal helminths communities of grey and red squirrels in Italy in order to investigate the role of parasites in the settlement of the alien species and in its interaction with native red squirrel. We will test two independent hypotheses: the “parasite release” hypothesis by comparing helminths community of grey squirrel in Italy and in its native range and the “parasite-mediated competition” hypothesis by comparing helminths communities of different red squirrel populations, with and without contact with the invasive species. So far, we have sampled 6 populations (3 grey-only, 2 red-only and 1 red-grey area) in Piedmont and Lombardy by capturing both species with standard live-trapping techniques. Grey squirrels were euthanized immediately after capture, while red squirrels were marked and released after samples collection. All grey squirrels were then dissected, their gut extracted and washed to collect gastro-intestinal content. The samples obtained were examined using a stereo microscope to collect and classify helminths. For red squirrels, we performed coprological analysis (fecal egg count method) and tape tests to obtain indirect information on their gastro-intestinal parasites. Moreover, given the general lack of knowledge on helminths community of this species, to provide a check-list of red squirrel parasites we dissected roadkills collected from different sites in Northern Italy. We dissected 110 grey squirrels in which we identified four different species of gastro-intestinal nematodes: Strongyloides robustus (prevalence: 89%; intensity [mean ± SD]: 19.3 ± 24.2 parasites/host), Trichostrongylus calcaratus (prevalence: 17%; intensity: 2.1 ± 1.2), Trichuris muris (prevalence: 11%; intensity: 1.1 ± 0.3) and Aonchotheca annulosa (prevalence: 3%; intensity: 2.7 ± 1.2). The observed species richness is lower compared to the average richness reported for grey squirrel in their native range. S. robustus is a parasite common and abundant in North-American squirrels, but never recorded in Europe until now, thus likely brought here by grey squirrels during the invasion process. On the other hand T. calcaratus, T. muris and A. annulosa should be considered as non-specific or accidental species, the first two being typical of other hosts (cottontail rabbit, Sylvilagus floridanus, and wild mice, Apodemus spp., respectively) and the latter being a generalist species, common in a wide variety of small rodents. On the 20 red squirrel roadkills dissected until now we found only one nematode, Rodentoxyuris sciuri (prevalence: 95%; intensity [mean ± SD] 720.3 ± 1478.6 parasites/host), typical of this species and already recorded in red squirrels in Europe. Coprological analysis and tape tests on animals captured in red-only areas confirm this result, since we only found eggs referable to this species. On the other hand, in the red-grey area, coprological analysis on red squirrels faeces have shown the presence of eggs of the genus Strongyloides, identical in shape and size to those of S. robustus found in greys. Since no species of this genus have ever been reported in Eurasian red squirrel and since this parasite has free living larvae that infect the host through the skin (facilitating inter-specific transmission through habitat or nest sharing), this can be a case of parasite transmission from the grey squirrel to the native species. In conclusion, our results lend support to the parasite-release hypothesis, as grey squirrels in Italy miss several helminths species usually present in North-America,. such as Heligmodendrium hassalli, a nematode commonly reported in grey squirrel native range with prevalences up to 80%. Moreover, the lack of these parasites is suggested by the presence of some accidental species, probably exploiting vacant niches. Concerning parasite-mediated competition, all evidence suggests that S. robustus can be transmitted to the red squirrel, but to confirm this result further investigation on the presence of this nematode and on its pathogenic effect on red squirrels is needed.

Eastern grey squirrel (Sciurus carolinensis) settlement in Italy and its impact on Eurasian red squirrel (Sciurus vulgaris) : what is the role of parasites? / C. Romeo, N. Ferrari, L.A. Wauters, A. Martinoli, N. Saino. - In: HYSTRIX. - ISSN 0394-1914. - suppl. 2012:(2012), pp. 43-43. ((Intervento presentato al 8. convegno Congresso nazionale di teriologia tenutosi a Piacenza nel 2012.

Eastern grey squirrel (Sciurus carolinensis) settlement in Italy and its impact on Eurasian red squirrel (Sciurus vulgaris) : what is the role of parasites?

C. Romeo
Primo
;
N. Ferrari
Secondo
;
N. Saino
Ultimo
2012

Abstract

Nowadays, invasive species are among the greatest threats to biodiversity, economy and public health. A better knowledge of the processes involved in biological invasions is therefore important to predict invasion pattern and success, in order to improve alien species management and native species conservation strategies. Since 1948, the Eastern grey squirrel (Sciurus carolinensis), a North-American alien species, has been repeatedly introduced in North-Western Italy (Piedmont, Liguria and Lombardy), causing local extinction of the native Eurasian red squirrel (Sciurus vulgaris) through exploitation competition for food. In Great Britain, where grey squirrels have been introduced since 1800, this replacement process is accelerated by the presence of Squirrelpox Virus (SQPV), which is carried by the invasive species without any pathogenic effect, but is lethal to red squirrels. SQPV is thus example of how parasites and pathogens can play an important role in biological invasions via two different processes. First, during the invasion process alien species often lose part of their parasite community (“parasite release”), with a positive impact on their population growth and consequently on their settlement and spread. Second, parasites may mediate the impact of invasive species on native taxa (“parasite-mediated competition”), acting as reservoir for local parasites or introducing in the environment novel parasites to which native species are not adapted . Our purpose is to explore gastro-intestinal helminths communities of grey and red squirrels in Italy in order to investigate the role of parasites in the settlement of the alien species and in its interaction with native red squirrel. We will test two independent hypotheses: the “parasite release” hypothesis by comparing helminths community of grey squirrel in Italy and in its native range and the “parasite-mediated competition” hypothesis by comparing helminths communities of different red squirrel populations, with and without contact with the invasive species. So far, we have sampled 6 populations (3 grey-only, 2 red-only and 1 red-grey area) in Piedmont and Lombardy by capturing both species with standard live-trapping techniques. Grey squirrels were euthanized immediately after capture, while red squirrels were marked and released after samples collection. All grey squirrels were then dissected, their gut extracted and washed to collect gastro-intestinal content. The samples obtained were examined using a stereo microscope to collect and classify helminths. For red squirrels, we performed coprological analysis (fecal egg count method) and tape tests to obtain indirect information on their gastro-intestinal parasites. Moreover, given the general lack of knowledge on helminths community of this species, to provide a check-list of red squirrel parasites we dissected roadkills collected from different sites in Northern Italy. We dissected 110 grey squirrels in which we identified four different species of gastro-intestinal nematodes: Strongyloides robustus (prevalence: 89%; intensity [mean ± SD]: 19.3 ± 24.2 parasites/host), Trichostrongylus calcaratus (prevalence: 17%; intensity: 2.1 ± 1.2), Trichuris muris (prevalence: 11%; intensity: 1.1 ± 0.3) and Aonchotheca annulosa (prevalence: 3%; intensity: 2.7 ± 1.2). The observed species richness is lower compared to the average richness reported for grey squirrel in their native range. S. robustus is a parasite common and abundant in North-American squirrels, but never recorded in Europe until now, thus likely brought here by grey squirrels during the invasion process. On the other hand T. calcaratus, T. muris and A. annulosa should be considered as non-specific or accidental species, the first two being typical of other hosts (cottontail rabbit, Sylvilagus floridanus, and wild mice, Apodemus spp., respectively) and the latter being a generalist species, common in a wide variety of small rodents. On the 20 red squirrel roadkills dissected until now we found only one nematode, Rodentoxyuris sciuri (prevalence: 95%; intensity [mean ± SD] 720.3 ± 1478.6 parasites/host), typical of this species and already recorded in red squirrels in Europe. Coprological analysis and tape tests on animals captured in red-only areas confirm this result, since we only found eggs referable to this species. On the other hand, in the red-grey area, coprological analysis on red squirrels faeces have shown the presence of eggs of the genus Strongyloides, identical in shape and size to those of S. robustus found in greys. Since no species of this genus have ever been reported in Eurasian red squirrel and since this parasite has free living larvae that infect the host through the skin (facilitating inter-specific transmission through habitat or nest sharing), this can be a case of parasite transmission from the grey squirrel to the native species. In conclusion, our results lend support to the parasite-release hypothesis, as grey squirrels in Italy miss several helminths species usually present in North-America,. such as Heligmodendrium hassalli, a nematode commonly reported in grey squirrel native range with prevalences up to 80%. Moreover, the lack of these parasites is suggested by the presence of some accidental species, probably exploiting vacant niches. Concerning parasite-mediated competition, all evidence suggests that S. robustus can be transmitted to the red squirrel, but to confirm this result further investigation on the presence of this nematode and on its pathogenic effect on red squirrels is needed.
Settore VET/06 - Parassitologia e Malattie Parassitarie degli Animali
Settore BIO/07 - Ecologia
2012
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