Parasites may play an important role in biological invasions through two main mechanisms: enemy release and apparent competition. First, alien species may lose part of their parasite fauna during the introduction process and this release from natural enemies may enhance their performances in the new range. Furthermore, parasites may mediate the competition between alien and native species: invaders may transmit alien parasites to naive native species (spillover) or acquire local parasites, increasing their environmental abundance and their impact on native hosts (spillback) and/or altering the pre-existent host-parasite dynamics. In this study, I investigate the above-mentioned processes, using native Eurasian red squirrels (Sciurus vulgaris) and North American Eastern grey squirrels (S. carolinensis) introduced to Italy as a model system. First, I conducted a broad survey of the macroparasite fauna of native red squirrels over a wide geographic area and across different habitats. My results show that the native sciurid has a naturally poor parasite community, likely a consequence of both its arboreal habits and its isolation from other congeners. Both parasite richness and diversity are indeed low, especially for gastro-intestinal helminth fauna, dominated by a single nematode species, the oxyurid Trypanoxyuris sciuri. This finding highlights that the species may be particularly vulnerable to parasite spillover from the alien congener and other invasive species. A parallel survey on the macroparasite fauna of grey squirrels was carried out to detect whether the alien host lost, acquired or introduced to Italy any parasite species. Through this investigation I demonstrated that grey squirrels lost part of their parasite fauna during the introduction process and, although they acquired some European parasites, their number does not compensate the number of species lost, with a resulting parasite richness in Italian populations much lower than in grey squirrels' native range. The helminth community of grey squirrels introduced to Italy is dominated by the North American nematode Strongyloides robustus, whereas the most common arthropod is the flea Ceratophyllus sciurorum, acquired from red squirrels. Hence, this part of the study gives support to the enemy release hypothesis and shows that this biological invasion holds the premises for both spillover and spill-back mechanisms towards native red squirrels to occur. In the following part of the study, grey squirrels and their dominant nematode, S. robustus, were used as a model to assess the performance of indirect parasitological methods and the relationship between helminth fecundity and intensity. My results reveal that, while flotation is a valid method to survey infection status in living hosts, faecal egg counts do not provide a reliable estimate of S. robustus intensity of infection, since density-dependence in nematode fecundity leads to a non-linear relationship between the amount of eggs shed in faeces and parasite load. Next, I investigated prevalence of alien S. robustus and local T. sciuri in living red squirrels to detect whether presence of grey squirrels affects the endo-macroparasite community of the native host. I used indirect methods (flotation and tape-tests) to compare infection status in populations of red squirrels living in presence and absence of the alien congener. Results show that S. robustus infection is linked to grey squirrel presence, thus confirming that red squirrels acquire this North American nematode via spillover from the invader. Interestingly, also prevalence of T. sciuri is significantly higher in red squirrels co-inhabiting with the alien species, suggesting that susceptibility to infection in red squirrels may increase as a consequence of higher stress levels induced by interspecific competition. Finally, infections by Ljungan virus (a potential zoonoses) and adenoviruses (known to cause gastrointestinal disease and mortality in squirrels in Northern Europe) were investigated in both red and grey squirrels to shed some light on the role played by arboreal sciurids in microparasite circulation. I reported for the first time Ljungan virus in red squirrels, indicating that this infection is not limited to small ground-dwelling rodents, and extended the known distribution of adenoviruses in squirrels to Southern Europe. Besides, the low adenovirus prevalence found in grey squirrels confirms that the alien species is not the source of infection in red squirrels as had been previously presumed. Overall, the present thesis highlights the importance of taking into account parasitological aspects when dealing with biological invasions. In particular, the model red-grey squirrel teaches that i) macroparasites have the potential to affect biological invasions as much as microparasites do; ii) an exhaustive knowledge of native species parasite fauna is fundamental to investigate apparent competition; iii) apart from introducing alien parasites, alien species may affect native species parasite communities through other mechanisms; iv) inference of parasitological parameters from indirect methods should always be considered carefully.

PARASITES AND BIOLOGICAL INVASIONS: ALIEN GREY SQUIRREL (SCIURUS CAROLINENSIS) AND NATIVE RED SQUIRREL (S. VULGARIS) AS MODEL SYSTEM / C.r. Romeo ; Tutor: N. Saino ; Coordinatore: N. Saino. DIPARTIMENTO DI BIOSCIENZE, 2014 Mar 05. 26. ciclo, Anno Accademico 2013. [10.13130/romeo-claudia-rosa_phd2014-03-05].

PARASITES AND BIOLOGICAL INVASIONS: ALIEN GREY SQUIRREL (SCIURUS CAROLINENSIS) AND NATIVE RED SQUIRREL (S. VULGARIS) AS MODEL SYSTEM

C.R. Romeo
2014

Abstract

Parasites may play an important role in biological invasions through two main mechanisms: enemy release and apparent competition. First, alien species may lose part of their parasite fauna during the introduction process and this release from natural enemies may enhance their performances in the new range. Furthermore, parasites may mediate the competition between alien and native species: invaders may transmit alien parasites to naive native species (spillover) or acquire local parasites, increasing their environmental abundance and their impact on native hosts (spillback) and/or altering the pre-existent host-parasite dynamics. In this study, I investigate the above-mentioned processes, using native Eurasian red squirrels (Sciurus vulgaris) and North American Eastern grey squirrels (S. carolinensis) introduced to Italy as a model system. First, I conducted a broad survey of the macroparasite fauna of native red squirrels over a wide geographic area and across different habitats. My results show that the native sciurid has a naturally poor parasite community, likely a consequence of both its arboreal habits and its isolation from other congeners. Both parasite richness and diversity are indeed low, especially for gastro-intestinal helminth fauna, dominated by a single nematode species, the oxyurid Trypanoxyuris sciuri. This finding highlights that the species may be particularly vulnerable to parasite spillover from the alien congener and other invasive species. A parallel survey on the macroparasite fauna of grey squirrels was carried out to detect whether the alien host lost, acquired or introduced to Italy any parasite species. Through this investigation I demonstrated that grey squirrels lost part of their parasite fauna during the introduction process and, although they acquired some European parasites, their number does not compensate the number of species lost, with a resulting parasite richness in Italian populations much lower than in grey squirrels' native range. The helminth community of grey squirrels introduced to Italy is dominated by the North American nematode Strongyloides robustus, whereas the most common arthropod is the flea Ceratophyllus sciurorum, acquired from red squirrels. Hence, this part of the study gives support to the enemy release hypothesis and shows that this biological invasion holds the premises for both spillover and spill-back mechanisms towards native red squirrels to occur. In the following part of the study, grey squirrels and their dominant nematode, S. robustus, were used as a model to assess the performance of indirect parasitological methods and the relationship between helminth fecundity and intensity. My results reveal that, while flotation is a valid method to survey infection status in living hosts, faecal egg counts do not provide a reliable estimate of S. robustus intensity of infection, since density-dependence in nematode fecundity leads to a non-linear relationship between the amount of eggs shed in faeces and parasite load. Next, I investigated prevalence of alien S. robustus and local T. sciuri in living red squirrels to detect whether presence of grey squirrels affects the endo-macroparasite community of the native host. I used indirect methods (flotation and tape-tests) to compare infection status in populations of red squirrels living in presence and absence of the alien congener. Results show that S. robustus infection is linked to grey squirrel presence, thus confirming that red squirrels acquire this North American nematode via spillover from the invader. Interestingly, also prevalence of T. sciuri is significantly higher in red squirrels co-inhabiting with the alien species, suggesting that susceptibility to infection in red squirrels may increase as a consequence of higher stress levels induced by interspecific competition. Finally, infections by Ljungan virus (a potential zoonoses) and adenoviruses (known to cause gastrointestinal disease and mortality in squirrels in Northern Europe) were investigated in both red and grey squirrels to shed some light on the role played by arboreal sciurids in microparasite circulation. I reported for the first time Ljungan virus in red squirrels, indicating that this infection is not limited to small ground-dwelling rodents, and extended the known distribution of adenoviruses in squirrels to Southern Europe. Besides, the low adenovirus prevalence found in grey squirrels confirms that the alien species is not the source of infection in red squirrels as had been previously presumed. Overall, the present thesis highlights the importance of taking into account parasitological aspects when dealing with biological invasions. In particular, the model red-grey squirrel teaches that i) macroparasites have the potential to affect biological invasions as much as microparasites do; ii) an exhaustive knowledge of native species parasite fauna is fundamental to investigate apparent competition; iii) apart from introducing alien parasites, alien species may affect native species parasite communities through other mechanisms; iv) inference of parasitological parameters from indirect methods should always be considered carefully.
5-mar-2014
Settore BIO/07 - Ecologia
Settore VET/06 - Parassitologia e Malattie Parassitarie degli Animali
alien species ; parasites ; biological invasions ; enemy release ; apparent competition ; Sciurus vulgaris ; Sciurus carolinensis ; helminths
SAINO, NICOLA MICHELE FRANCESCO
SAINO, NICOLA
Doctoral Thesis
PARASITES AND BIOLOGICAL INVASIONS: ALIEN GREY SQUIRREL (SCIURUS CAROLINENSIS) AND NATIVE RED SQUIRREL (S. VULGARIS) AS MODEL SYSTEM / C.r. Romeo ; Tutor: N. Saino ; Coordinatore: N. Saino. DIPARTIMENTO DI BIOSCIENZE, 2014 Mar 05. 26. ciclo, Anno Accademico 2013. [10.13130/romeo-claudia-rosa_phd2014-03-05].
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