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Feeding Habits of the Asiatic Red-Bellied Squirrel Callosciurus Erythraeus Introduced in Argentina

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Feeding Habits of the Asiatic Red-Bellied Squirrel Callosciurus Erythraeus Introduced in Argentina Published by Associazione Teriologica Italiana Volume 29 (2): 223–228, 2018 Hystrix, the Italian Journal of Mammalogy Available online at: http://www.italian-journal-of-mammalogy.it doi:10.4404/hystrix–00125-2018 Research Article Feeding habits of the Asiatic red-bellied squirrel Callosciurus erythraeus introduced in Argentina Agustín Zarco1,∗, Verónica V. Benítez2, Laura Fasola3, Guillermo Funes4, M. Laura Guichón5,∗ 1Instituto Argentino de Investigaciones de las Zonas Áridas – CONICET and Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Cuyo, Mendoza, Argentina 2Ecología de Mamíferos Introducidos, Departamento de Ciencias Básicas, Instituto de Ecología y Desarrollo Sustentable, Universidad Nacional de Luján, Luján, Buenos Aires, Argentina 3Dirección Regional Patagonia Norte de la Administración de Parques Nacionales, San Carlos de Bariloche, Río Negro, Argentina 4Instituto Multidisciplinario de Biología Vegetal – CONICET and Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba, Argentina 5Instituto de Investigaciones en Biodiversidad y Medioambiente, Universidad Nacional de Comahue (INIBIOMA, UNCo – CONICET), Centro de Ecología Aplicada del Neuquén (CEAN), Junín de los Andes, Neuquén, Argentina Keywords: Abstract invasive squirrel faeces analysis Knowledge of food habits of invasive species is necessary to predict invasion success and potential behaviour interactions in the invaded community. The Asiatic red-bellied squirrel Callosciurus erythraeus diet has been introduced in Asia, Europe and South America. We studied feeding habits of red-bellied squirrels in Argentina in two sites 600 km apart where wild populations have become established. Article history: We used both faecal microhistological analysis and behavioural records to describe diet composition Received: 27 August 2018 and feeding habits. We also analysed diet selection and the potential role of the squirrels as seed Accepted: 13 December 2018 disperser. Squirrels consumed items from 35 species of exotic trees and shrubs and one native tree species; fruits and seeds represented the bulk of the diet in all seasons (faeces analysis: >44%; behavioural observations: >38%). Squirrels also consumed epiphytic and climbing plants, ferns, Acknowledgements The authors wish to thank Paula Tecco, Irene Lett, Melisa Giorgis and invertebrates, fungi, lichens, mosses and bird eggs. Diet composition varied throughout the year Heyke Zimmerman for helping us with botanical identification. We thank according to food availability. We did not find evidence of endozoochoric dispersal but we observed two anonymous referees for comments and suggestions on a previous squirrels carrying and dropping nuts and acorns during transport. The consumption of a wide version of the manuscript and Susan Walker, who corrected the English range of food items and species, the ability to modify the diet according to food availability, and writing. The study was funded by Universidad Nacional de Luján and CONICET. the capacity to hoard food indicate that feeding habits of red-bellied squirrels favour their invasive Author contributions: all authors designed the study; GF and MLG potential. developed the protocols for data collection; AZ, VVB and LF collec- ted the data; AZ and MLG analysed the data; AZ and MLG wrote the manuscript; all authors provided comments throughout the manuscript preparation. Introduction or mitigation actions such as using toxic baits or scaring devices (Wil- liamson, 1996; Holway and Suarez, 1999). Exotic species usually face several barriers at different stages of the invasion process (Blackburn et al., 2011). Characteristics of the spe- Squirrels are successful invaders; introduced populations of 18 squir- cies, of the recipient community and of the introduction event are all rel species have already been reported in 23 countries over five con- important aspects affecting establishment and invasion (Williamson, tinents (Bertolino, 2009; Jessen et al., 2010). These populations have 1996). The probability of surviving and reproducing in a new habitat originated from escapes or releases related to the pet market, to en- is strongly linked to resource availability and predator pressure (Black- rich wildlife or as game animals for their fur (Palmer et al., 2007; Ber- burn et al., 2011). The complexity of multiple and new interactions es- tolino, 2009). Exotic squirrels cause economic losses and environ- tablished within the recipient community, and the variable conditions mental damages that include disease transmission (e.g., Eastern grey that can be found in the new habitat, challenge any attempt at gener- squirrel Sciurus carolinensis, Chantrey et al., 2014), damage to planta- alisation. However, the capacity of animals to modify their behaviour tions (e.g., Eastern fox squirrel Sciurus niger, Bertolino, 2009), reduced in response to novel conditions is a key attribute for their success as survival of native seeds (e.g., Barbary ground squirrel Atlantoxerus invaders (Sol and Lefebvre, 2000; Wright et al., 2010). Plasticity in getulus, Nogales et al., 2005), bark stripping (e.g., Finlayson’s squir- foraging behaviour can play an important role when individuals are rel Callosciurus finlaysonii, Bertolino et al., 2004), predation on nat- released into unknown habitats. Examples of successful invaders in- ive birds (e.g., American red squirrel Tamiasciurus hudsonicus, Martin clude species that are generalist and opportunistic foragers (Holway and Joron, 2003), and competition with native fauna (e.g., Asiatic red- and Suarez, 1999; Rehage et al., 2005). These could constitute strong bellied squirrel Callosciurus erythraeus, Mazzamuto et al., 2017). traits for invasion success especially if they are combined with behavi- The Asiatic red-bellied squirrel C. erythraeus (Pallas, 1779) has oural flexibility (Wright et al., 2010). Data on feeding habits of a spe- been successfully introduced in Italy, France, Belgium, The Nether- cies in its native and introduced ranges can help understand its invasive lands, Hong Kong, Japan, and Argentina (Bertolino and Lurz, 2013; success and predict the risk of invasion of different habitats. Foraging Lurz et al., 2013; Mazzamuto et al., 2016a). This is the first known behaviour also provides important information to design management introduction of a squirrel into South America and it has achieved the status of an established invasion of major proportions in Argentina (Guichón and Doncaster, 2008). The invaded range increases gradu- ally from already colonized areas and abruptly from transportation ∗Corresponding author Email addresses: [email protected] (Agustín Zarco), and release of individuals into new areas (Guichón et al., 2015). The [email protected] (M. Laura Guichón) main invasion focus in the country has been originated by the intro- Hystrix, the Italian Journal of Mammalogy ISSN 1825-5272 14th December 2018 ©cbe2018 Associazione Teriologica Italiana doi:10.4404/hystrix–00125-2018 Hystrix, It. J. Mamm. (2018) 29(2): 223–228 duction of 10 individuals in the Argentine Pampas in 1970 (Aprile and Chicco, 1999). This first population occupied 680 km2 in 2004 (Guichón et al., 2005) and in the next five years it had doubled the in- vaded area (>1300 km2 in 2009, Benitez et al., 2013). This squirrel causes economic damage in agricultural and urban areas by debark- ing, eating fruits and seeds, and chewing through cables and irrigation pipes (Guichón et al., 2005; Pedreira et al., 2017). Moreover, its spread could affect indigenous birds (Azuma, 1998; Messetta et al., 2015) and transmit diseases and parasites to humans or other animals (Dozières et al., 2010; Gozzi et al., 2013; Deng et al., 2016; Mazzamuto et al., 2016b). The formation of several invasion foci in Argentina favoured by the squirrel’s charismatic appeal and ability to establish in new and different habitats (Benitez et al., 2013; Borgnia et al., 2013; Guichón et al., 2015) indicate a high probability of a marked increase in abundance and distribution in the coming years (Guichón and Doncaster, 2008). In this study we analysed the feeding habits of red-bellied squir- rels in two different biogeographical regions in Argentina. We used faecal analysis and behavioural observations to achieve a comprehens- ive description of their diet composition and foraging behaviour. Un- der the hypothesis that this species has a generalist and opportunistic diet, we predicted that: 1) squirrels will eat a wide range of plant spe- cies and items, and 2) squirrels will select food resources according to their site and seasonal availability. We also assessed the potential role of these squirrels as endozoochoric and/or epizoochoric disperser of exotic plants. Methods Study areas This study was conducted in two sites 600 km apart where the red- bellied squirrel has been introduced in Argentina (Benitez et al., 2013): (1) La Cumbrecita (31°530 S, 64°460 W, 1360 m a.s.l., Córdoba province), a small mountain and tourist village, where squirrels were Figure 1 – Location of the two study sites (LC: La Cumbrecita, J: Jáuregui) in Argentina. released in the year 2000, and (2) Jáuregui (34°360 S, 59°90 W, 25 m a.s.l., Buenos Aires province), a small rural town in the Pampas region, where squirrels were introduced in 1970 and which is the core of the main invasion focus in Argentina (Fig. 1). In both sites, arboreal veget- red-bellied squirrel as described by Fasola et al. (2005). All faeces ation is mainly composed of exotic species used in commercial
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