Claudia Romeo

Ljungan Virus and an Adenovirus in Italian Squirrel Populations

Abstract We report Ljungan virus infection in Eurasian red squirrels (Sciurus vulgaris) for the first time, and extend the known distribution of adenoviruses in both native red squirrels and alien gray squirrels (Sciurus carolinensis) to southern Europe.

Living on the Edge: Can Eurasian Red Squirrels (Sciurus vulgaris) Persist in Extreme High-elevation Habitats?

Abstract Studying intraspecific spatiotemporal variation in vital rates among populations over a range of environmental conditions is essential to reveal intrinsic and extrinsic factors affecting population dynamics. Mammal populations living at higher elevations often have higher adult survival, shorter breeding seasons, and lower reproductive output per season than at lower elevations. We studied dynamics of a Eurasian red squirrel (Sciurus vulgaris) population in high-elevation, mountain pine (Pinus mugo) forest with extreme winters, in the Central Italian Alps, and compared vital rates with populations in more productive habitats at lower elevations. Average density was 0.14 ± 0.07 squirrels ha−1 (range 0.07–0.30 ha−1), and numbers typically increased in summer–autumn as a result of seasonal reproduction and immigration. Mean persistence time was only 12.5 months, and there was a nearly complete population turnover in only two years. Local survival and recruitment rate were correlated with seasonal population growth rate, and partial effect of survival explained 80% of variation in growth rate. While reproductive rate in mountain pine habitat was more similar than in more productive habitats at lower elevations, density and autumn–winter survival were much lower. Thus, red squirrels did not show the adaptations observed in several other mammal species, but might invest heavily in early reproduction to compensate for short life expectancy.

Poor Parasite Community of an Invasive Alien Species: Macroparasites of Pallas's Squirrel in Italy

The aim of the present study was to investigate the macroparasite fauna of Pallass squirrel, Callosciurus erythraeus, native to SE Asia, recently introduced to Italy and co-occurring with the native Eurasian red squirrel Sciurus vulgaris. A total of 161 Pallass squirrels harboured a poor macroparasite fauna, characterized by two main ectoparasite species, the flea Ceratophyllus (M.) sciurorum sciurorum (prevalence 50%, mean intensity 1.0 ± 0.1) and the tick Ixodes ricinus (prevalence 47%, mean intensity 3.0 ± 0.7), and a few helminths (Rodentoxyuris sciuri, Trichuris muris, Strongyloides callosciureus) all with prevalence below 10%. All parasites, except S. callosciureus, are native to Europe and were acquired in the invaded range. The loss of native parasites might have contributed to their successful invasion. The acquisition of local parasites C. sciurorum and Trichuris sciuri, and the introduction of the Asiatic nematode S. callosciureus may lead to spill-back and spill-over processes towards red squirrels.

Diversity and host specificity of coccidia (Apicomplexa: Eimeriidae) in native and introduced squirrel species

Introduction of alien species into new areas can have detrimental effects on native ecosystems and impact the native species. The present study aims to identify coccidia infecting native and introduced squirrels in Italy, to gain insight into possible transmission patterns and role of monoxenous coccidia in mediating the competition between alien and native hosts. We collected 540 faecal samples of native red squirrels, Sciurus vulgaris, invasive alien grey squirrels, S. carolinensis, and introduced Pallass squirrels, Callosciurus erythraeus. Total prevalence of Eimeria spp. was 95.6% in S. vulgaris, 95.7% in S. carolinensis and only 4.1% in C. erythraeus. Morphological examination revealed 3 Eimeria morphotypes. Phylogenetic analyses of Eimeria DNA based on 18S, ITS, cox I markers displayed fairly distinct monophyletic clades in the microscopically indistinguishable E2 morphotype, proving indisputable distinction between the isolates from red and grey squirrels. Grey squirrels successfully introduced E. lancasterensis from their native range, but this species does not spill over to native red squirrels. Similarly, there is no evidence for the transmission of E. sciurorum from red to grey squirrels. The possible transmission and the potential role of monoxenous coccidia in mediating the competition between native and invasive squirrels in Italy were not confirmed.

Native and introduced squirrels in Italy host different Cryptosporidium spp.

The present study was undertaken to describe Cryptosporidium spp. infection in tree squirrels from 17 locations in Northern Italy. A total of 357 squirrels were examined, including species native to Europe (Sciurus vulgaris; n=123), and species introduced from North America (Sciurus carolinensis; n=162) and Southeast Asia (Callosciurus erythraeus; n=72). Faecal samples of all squirrels were examined for the presence of Cryptosporidium infection by microscopy (flotation method) and PCR/sequence analysis of the Cryptosporidium 18S rRNA, actin, and gp60 genes. Despite the overlapping ranges of native and introduced tree squirrel species in the study area, they host different Cryptosporidium spp. Sciurus vulgaris were exclusively infected with Cryptosporidium ferret genotype (n=13) belonging to three novel gp60 subtypes, VIIIb-VIIId. Sciurus carolinensis hosted C. ubiquitum subtype XIIb (n=2), Cryptosporidium skunk genotype subtype XVIa (n=3), and chipmunk genotype I subtype XIVa (n=1). Cryptosporidium chipmunk genotype I subtype XIVa was also found in two C. erythraeus. Comparing data from this and previous studies, we propose that Cryptosporidium skunk genotype and possibly C. ubiquitum subtype XIIb were introduced to Europe with eastern grey squirrels. Cryptosporidium chipmunk genotype I and ferret genotype were associated with high intensity infections, but there was no association with diarrhoea.

Limited diversity associated with duplicated class II MHC-DRB genes in the red squirrel population in the United Kingdom compared with continental Europe

The red squirrel (Sciurus vulgaris) population in the United Kingdom has declined over the last century and is now on the UK endangered species list. This is the result of competition from the eastern grey squirrel (S. carolinensis) which was introduced in the 19th century. However, recent evidence suggests that the rate of population decline is enhanced by squirrelpox disease, caused by a viral infection carried asymptomatically by grey squirrels but to which red squirrels are highly susceptible. Population genetic diversity provides some resilience to rapidly evolving or exotic pathogens. There is currently no data on genetic diversity of extant UK squirrel populations with respect to genes involved in disease resistance. Diversity is highest at loci involved in the immune response including genes clustered within the major histocompatibility complex (MHC). Using the class II DRB locus as a marker for diversity across the MHC region we genotyped 110 red squirrels from locations in the UK and continental Europe. Twenty-four Scvu-DRB alleles at two functional loci; Scvu-DRB1 and Scvu-DRB2, were identified. High levels of diversity were identified at both loci in the continental populations. In contrast, no diversity was observed at the Scvu-DRB2 locus in the mainland UK population while a high level of homozygosity was observed at the Scvu-DRB1 locus. The red squirrel population in the UK appears to lack the extensive MHC diversity associated with continental populations, a feature which may have contributed to their rapid decline.

Midichloria mitochondrii, endosymbiont of Ixodes ricinus: evidence for the transmission to the vertebrate host during the tick blood meal

Ticks are important vectors of a variety of pathogens affecting humans and other animals, but they also harbor numerous microorganisms whose role is still limitedly investigated. Ixodes ricinus harbors the endosymbiont Midichloria mitochondrii, which is localized in ovaries and in salivary glands. The bacterium is vertically transmitted and is present in 100% of wild adult females, while prevalence values drop after some generations under laboratory conditions. Molecular and serological evidences showed that M. mitochondrii molecules are transmitted to the vertebrate hosts by I. ricinus during the blood meal. Our work was focused on monitoring M. mitochondrii antigens and DNA in a vertebrate model after infestation with I. ricinus for a time-span of four months. Two groups of rabbits were infested with I. ricinus females, respectively from the wild (naturally infected with the symbiont) and laboratory strain (lab; considered devoid of M. mitochondrii after quantitative PCR investigations) and screened using molecular and serological assays at nine time points. M. mitochondrii presence was detected in rabbits infested with wild I. ricinus ticks, but surprisingly also in those infested with lab ticks, albeit at later time points. This result prompted a more sensitive molecular screening of lab ticks, which were found to harbor very low symbiont loads. Our results indicate that transmission of the bacterium occurs even at low bacterial loads, and that antibody response against M. mitochondrii antigens begins within one week post-infestation with wild I. ricinus. Circulating DNA was detected in the blood of rabbits belonging to both groups up to the end of the experiment, suggesting a replication of the symbiont inside the vertebrate host.