Published by Associazione Teriologica Italiana Volume 25 (2): 97–102, 2014 Hystrix, the Italian Journal of Mammalogy Available online at: http://www.italian-journal-of-mammalogy.it/article/view/10276/pdf doi:10.4404/hystrix-25.2-10276 Research Article Gastro-intestinal helminths in the red-bellied squirrel introduced in Argentina: accidental acquisitions and lack of specific parasites Ana Cecilia Gozzia,∗, María Laura Guichóna,b, Verónica Victoria Beniteza, Adrián Troyellia, Graciela Teresa Navonec aEcología de Mamíferos Introducidos, Departamento de Ciencias Básicas, Universidad Nacional de Luján, Rutas 5 y 7, Luján (6700), Buenos Aires, Argentina bpresent address: Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA, UNCo-CONICET), basado en Centro de Ecología Aplicada del Neuquén (CEAN), Ruta Provincial N861 Km. 3 (CC N87), Paraje San Cabao, (8371) Junín de los Andes, Neuquén, Argentina cCentro de Estudios Parasitológicos y de Vectores (CEPAVE), Centro Científico Tecnológico (CCT), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) La Plata; Universidad Nacional de La Plata (UNLP). Boulevar 120 S/N entre Avda 60 y calle 64 (B1902CHX), La Plata, Argentina Keywords: Abstract Invasive squirrel helminth survey Introduced species may lose their natural parasites when invading a new habitat, may acquire new, nematodes local parasites or may introduce parasites from their native range. We studied the gastro-intestinal parasite release helminth fauna associated with the red-bellied squirrel Callosciurus erythraeus (Pallas, 1778) in- troduced in Argentina to evaluate its role as a host of either specific or acquired parasites in two Article history: invasion foci. We analyzed entire digestive tracts of 72 red-bellied squirrels captured in the main Received: 19 August 2014 invasion focus (Luján, province of Buenos Aires) between February and May 2011, and in a second- Accepted: 7 November 2014 ary focus (Cañada de Gómez, province of Santa Fe) in December 2008. We only found two nemat- ode specimens: an adult male belonging to the genus Pterygodermatites (Paucipectines) Quentin, 1969 and another adult male belonging to the genus Stilestrongylus (Freitas, Lent and Almeida, Acknowledgements 1973). None of these genera were previously listed for the red-bellied squirrel in introduced areas, We thank the owner and personnel of the ranch Del Sel for assist- ance in the field. María Cristina Estivariz for the drawings and Dr. but a species of the genus Pterygodermatites was previously reported for this squirrel in its nat- Cecilia Ezquiaga for laboratory training. This study was supported by ive habitat. These results indicate that, to date, the red-bellied squirrel in Argentina is accidentally the Universidad Nacional de Luján and the Agencia Nacional de Promo- parasitised by nematodes acquired in its new environment and has no specific gastro-intestinal hel- ción Científica y Tecnológica - Proyectos de Investigación Científica y minths. This could be related with a “founder effect” and/or the lack of sciurid rodents that prevent Tecnológica ANPCYT-PICT 32195. the red-bellied squirrel to be colonized by pre-adapted helminth taxa. Other factors that may play a role are the small number of mammals with arboreal habits and some “encounter barriers” in the new environment that prevent the acquisition of helminths with a wide host spectrum. Introduction the 10 red-bellied squirrels introduced in Argentina in 1970 that had Successful introduced species may show a pattern of low diversity and been acquired in a pet shop in The Netherlands and taken to a large prevalence of parasites in the new environment (Torchin et al., 2003; ranch in the Pampas. This arboreal squirrel successfully established in Torchin and Mitchell, 2004). This pattern is usually linked with the rural and urban areas of the Pampas (Guichón et al., 2005; Guichón and loss of native specific parasites (Keane and Crawley, 2002; Torchin et Doncaster, 2008), and has already settled in other sites of three Argen- al., 2003; Torchin and Mitchell, 2004), and with the low acquisition of tinean provinces as a result of repeated translocations and illegal pet new parasites from co-inhabiting hosts in the invaded area (Torchin and trade (Benitez et al., 2013). Mitchell, 2004; Pisanu et al., 2009). The acquisition of parasites in the Several parasitological studies on different introduced species be- new environment will depend in part, on the ability of native parasites longing to different taxa have assessed their role as new hosts in the to develop in a wide spectrum of hosts and/or if they are parasites of new environment, finding poorer parasites communities in the new en- hosts phylogenetically related to the introduced host (Asakawa, 2005; vironment in relation to the native range of the analysed species (Marr Pisanu et al., 2009). The potential advantage of introduced species over et al., 2008; Torchin et al., 2003; Ross et al., 2010). Introduced squirrels native species due to the benefit caused by the loss of their natural en- such as Tamias sibiricus Laxmann, 1769 in France were found to intro- emies may enhance their success in the invasion process as stated by the duce helminth fauna in the invaded area, while they may also acquire Enemy Release Hypothesis (Torchin et al., 2003; Torchin and Mitchell, other helminths from co-inhabiting hosts, especially if helminth para- 2004). At the same time, introduced species can also introduce para- sites have a large spectrum of host species with similar behaviour, life- sites from their native range and in some cases transfer them to native history and habitats (Pisanu et al., 2007, 2009). Recently, a common hosts (Smith and Carpenter, 2006; Taraschewski, 2006; Bordes et al., species of nematode, Strongyloides robustus Chandler, 1942, parasite 2007). of North American Eastern grey squirrels Sciurus carolinensis Gmelin, The Asiatic red-bellied squirrel, Callosciurus erythraeus (Pallas, 1788, was found in two red squirrels Sciurus vulgaris Linnaeus, 1758 1778), was intentionally introduced into Japan, Argentina, and three captured in Italy (Continental Region), suggesting that this nematode European countries (Belgium, France, and The Netherlands) (Lurz et species may spillover from the introduced grey squirrel towards the nat- al., 2013). Most squirrel introductions are intentional and related to ive red squirrel (Romeo et al., 2013, 2014). Moreover, the grey squir- pet trade (Palmer et al., 2007; Bertolino, 2009), which was the case of rel acquired local parasites in Italy but the number of parasites acquired did not compensate the number of parasite species lost from their native range (Romeo et al., 2014). ∗Corresponding author Although there are no helminthological studies conducted on the Email address: [email protected] (Ana Cecilia Gozzi) red-bellied squirrel in Argentina, helminth fauna described for this spe- Hystrix, the Italian Journal of Mammalogy ISSN 1825-5272 18th December 2014 ©cbe2014 Associazione Teriologica Italiana doi:10.4404/hystrix-25.2-10276 Hystrix, It. J. Mamm. (2014) 25(2): 97–102 cies in other introduced areas comprises both native specific parasites ethanol and cleared in temporary mounts of glycerine alcohol for iden- introduced with the founders (Asakawa, 2005; Sato et al., 2007), and tification. Drawings of worms and of the transverse section of the pat- acquired parasites from co-inhabiting hosts (Dozières et al., 2010). The tern of longitudinal ridges (synlophe) were done under a microscope aim of this study was to describe the gastro-intestinal helminths fauna Olympus BX 51 equipped with a camera lucida. associated with the red-bellied squirrel in Argentina in order to evalu- ate its role as a host of specific or acquired parasites within the invaded Results community. We will consider specific parasite species those species that are characteristic of sciurid rodents and/or have been reported in Two nematodes belonging to two different families were found in two the native range of the red-bellied squirrel. red-bellied squirrels captured in the main invasion focus in Luján (n=40), while no helminths were found in the squirrels captured in the secondary focus in Cañada de Gómez (n=32). One adult male be- Materials and methods longing to the family Rictulariidae (Nematoda: Spirurida) was found in a male squirrel. The specimen studied had features that correspon- We analyzed the entire digestive tracts of 72 red-bellied squirrels cap- ded to the genus Pterygodermatites Wedl, 1861, given its denticulate, tured during control campaigns conducted in two invasion foci in Ar- hexagonal oral opening, large buccal cavity with teeth, the presence of gentina. Between February and May 2011, we collected 40 visceral 38 pairs of combs and cuticular spines distributed in two rows on the samples of squirrels (mature:immature ~: 9:13; mature:immature |: 0 0 ventral surface of the body and the presence of four fan-like cuticular 8:10) captured in Luján, province of Buenos Aires (34°33 S, 59°7 processes anterior to the cloacal opening (Fig. 1; Tab. 1). In addition, W), which is the main invasion focus in the country, originated in 1970. the apical oral opening allows us to locate this specimen within the In December 2008, we obtained 32 visceral samples of squirrels (ma- subgenus Paucipectines Quentin, 1969. The other intestinal parasite ture:immature ~: 13:3; mature:immature |: 14:2) in a secondary in- was an adult male belonging to the family Heligmonellidae (Nematoda: vasion focus in Cañada de Gómez, province of Santa Fe (32°490 S, 0 Strongylida: Trichostrongylina: Nippostrongylinae) found in a female 61°20 W), that originated in 1999 by the release of squirrels translo- squirrel. This specimen had a synlophe with 24 spines with greater cated from the main focus in Luján, located 285 km away. Estimated number of ridges dorsally, asymmetrical copulatory bursa with extern- density of squirrels in Luján is at least three times higher than in Cañada odorsal rays differing in size, and hypertrophied genital cone (Fig. 1), de Gómez; 15.3 squirrel/ha and 4.86 squirrel/ha, respectively (Benitez which are all features belonging to the genus Stilestrongylus (Freitas, et al., 2013).