Bioacoustics of Sciurus (Tenes) anomalus

ECOLOGY Population characteristics. —Population numbers of Sciurus anomalus can fluctuate considerably, presumably due to variation in food availability ( Kolosov et al. 1965 ; Vereshchagin 1967 ); however, numbers appear more stable than those of S. vulgaris ( Stroganova 1958 ) . Stroganova (1958) reported sighting 0.75–1.25 individuals/km of census transect in a nut orchard, whereas only 0.11 and 0.17 individuals/km were observed in mixed forest. Density was estimated at 1.04– 1.82 individuals/ha in oak-pine mixed forests in Lebanon (Abi- Said et al. 2014). Habitat loss due to incompatible agriculture, fire, and timber harvest has resulted in population declines in the Caucasus ( Vereshchagin 1967 ), Jordan ( Amr et al. 2006 ), and Iraq ( Hatt 1959 ). Habitat fragmentation is the major threat to the species on Lesbos (Matsinos and Papadopoulou 2004). S. anomalus was detected in an unburned pine forest but not in forest burned 9 years earlier ( Soyumert et al. 2010 ). Drought also appears to result in population decline ( Amr et al. 2006 ). Accidental mortality results from individuals entering water tanks from which they cannot escape ( Amr et al. 2006 ). S . anomalus becomes habituated to vehicle traffic and noise ( Amr et al. 2006 ). Wild boar ( Sus scrofa ), edible dormouse ( Glis glis ), and a variety of birds pilfer winter seed stores of S . anomalus ( Kolosov et al. 1965 ) . Eurasian lynx ( Lynx lynx ), wildcat ( Felis silvestris ), domestic cat ( Felis silvestris catus ), red fox ( Vulpes vulpes ), gray wolf ( Canis lupus ), European badger ( Meles meles ), beech marten ( Martes foina ), European pine marten ( M. martes ), least weasel ( Mustela nivalis ), northern goshawk ( Accipter gentilis ), Eurasian sparrowhawk ( A. nisus ), common buzzard ( Buteo buteo ), longlegged buzzard ( B. rufinus ), red kite ( Milvus milvus ), black kite ( M. migrans ), Eurasian eagle-owl ( Bubo bubo ), and tawny owls ( Stix aluco ) are known to prey upon squirrels ( Stroganova 1958 ; Kolosov et al. 1965 ; Heptner and Sludskii 1992; De Cupere et al. 2008 ). Space use. —In Israel , Sciurus anomalus prefers forest dominated by oaks ( Quercus calliprinos , Q. boissieri ) and pistachio ( Pistacia pataestina —Danford and Alston 1877; Ilani and Shalmon 1984; Gavish 1993 ) and was abundant in the last century in the wooded parts of the Upper Galilee and the Golan Heights ( Bodenheimer 1935 ). In Jordan , pure pine forests are preferred over mixed pine-oak ( Pinus-Quercus — Amr et al. 2006 ). Throughout Lebanon and the Zagros Mountains in Iraq and Iran , open oak forests are also important squirrel habitat ( Hatt 1959 ; Lewis et al. 1967 ; Atallah 1977 ). In Turkey , S. anomalus is found frequently in orchards and forests that are dominated by oak ( Quercus trojana ), juniper ( Juniperus excelsa ), walnut ( Juglans regia ), pine ( Pinus nigra ), willow ( Salix alba ), apples, pears, plums ( Pyrus elaeagnifolia , P. domestica , P. syria , P. malus ), hawthorn ( Crateagus aronia , C. monogyna ), and rose ( Rosa canina — Hoogstraal 1959 ; Osborn 1964 ; Albayrak and Arslan 2006). Beech ( Fagus ) forests ≤ 2,000 m in elevation are commonly inhabited in Caucasia but S. anomalus is also found in elm ( Ulmus ), chestnut ( Castanea ), maple ( Acer insigne ), ash ( Fraxinus ), cherry ( Prunus ), pear ( Caucasica ), poplar ( Populus ), alder ( Alnus ), and linden ( Tilia ), whereas pine forests appear to be avoided ( Dahl 1954 ; Stroganova 1958 ; Enukidze 1960 ; Bobrinskii et al. 1965 ; Kolosov et al. 1965 ; Ognev 1966 ). S . anomalus in Caucasia appears restricted to subtropical forest areas and fruit and nut plantations in elevations where snow is uncommon ( Stroganova 1958 ). On the Greek island of Lesbos, squirrels dwell in lower elevation chestnut ( Castanea sativa ) plantations, olives ( Olea europea ), walnut ( J. regia ), almonds ( Prunus dulcis ), pears ( Pyrus amygdaliformis ) as well as plantations and mixed natural forests of oak ( Q. aegilops , Q. coccifera ) and conifers ( Cupressus sempervirens , P. brutia , P. nigra —Hecht-Markou 1994) upward to the coniferous forest of Mt. Lepetymnos (1,009 m—Hecht-Markou 1994). Sciurus anomalus will migrate from one habitat to another dependent on the seasonal availability of food (Hecht-Markou 1994). Based upon the frequent resighting of squirrels in the same areas, S . anomalus probably demonstrates strong site fidelity; however, migrations are reported in response to food shortages ( Stroganova 1958 ). Sciurus anomalus nests in tree hollows lined with moss and dry leaves ( Stroganova 1958 ; Enukidze 1960 ; Ognev 1966 ; Gavish 1993 ) and may do so in groups ( Stroganova 1958 ; Hatt 1959 ). In Turkey , nests occur in oak ( Q. trojana ), walnut ( J. regia ), juniper ( J. excelsa ), and willow ( S. alba ) cavities (Albayrak and Arslan 2006). Nest cavities in trees are shallow extending to depths of 20–50 cm (Hecht-Markou 1994) and entrances, facing south and southeast ( Enukidze 1960 ), are located at heights of 5– 14 m . However, nests may also occur under rocks, tree roots, gravestones, and buildings ( Stroganova 1958 ; Kolosov et al. 1965 ). S . anomalus changes nests between seasons to eliminate ectoparasites, but it will reuse the nests in subsequent years (Hecht-Markou 1994). Diet. —Foods are most abundant in spring and summer, with shortages common in winter ( Stroganova 1958 ). Tree seeds are the primary food; oaks (including Q. calliprinos , Q. infecloria , Q. cerris ) are major food sources throughout the range of Sciurus anomalus ( Stroganova 1958 ; Ognev 1966 ; Lewis et al. 1967 ; Gavish 1993 ). Fir seeds (species not noted) are taken in Turkey ( Osborn 1964 ), Persian walnuts ( Julans regia ), chestnuts ( Castanea ), hazelnuts ( Corylus avellana ), beechnuts ( Fagus ), and apricot seeds ( Pruna ) are eaten in Caucasia ( Vinogradov et al. 1953 ; Ognev 1966 ). Pine ( Pinus pinea , P. brutia ) and cedar ( Cedrus lebani ) seeds are favorite foods in Lebanon ( Lewis et al. 1967 ; Abi-Said et al. 2014). Nine larders contained 7–62 nuts about 50% of which were chestnuts, 35% walnuts, and 15% hazelnuts ( Stroganova 1958 ; Kolosov et al. 1965 ). Buds and other vegetation ( Lewis et al. 1967 ), a variety of berries including Smilax excelsa ( Stroganova 1958 ; Ognev 1966 ), Cornelian cherries ( Stroganova 1958 ), the seeds and pulp of commercial fruits such as apples, pears, peaches, grapes, and plums ( Stroganova 1958 ), cereal grains ( Aegilops peregina ), and mushrooms ( Polyporus sulphureus — Stroganova 1958 ; Kolosov et al. 1965 ; Gavish 1993 ) can be significant components of the diets of S . anomalus . Insects ( Stroganova 1958 ) and bird eggs and nestlings ( Ognev 1966 ; Etemad 1978 ) also are eaten. Diseases and parasites. —Leptospirosis antibodies were reported for 6 of 57 Sciurus anomalus in Caucasia; antibodies for the following serological groups were identified: L. pyrogenes , L. autumnalis , L. australis , and L. bataviae ( Kakabadze et al. 1978 ) . Leishmania infantum was not detected in 3 individuals examined in Iran ( Fallah et al. 2006 ). Endoparasites identified include Cateaotaenia pusilla ( Enukidze 1960 ) , Taenia martis , Echinococcus granulosus (Enukidze and Nikolaishvili 1980) , Eimeria serbica ( Couch et al. 2005 ) , Syphacia , and Ascaris ( Enukidze 1960 ) . The ectoparasites, Ixodes ricinus (Acari— Enukidze 1960 ; Anderson and Magnarelli 1993), I. redikorzovi (Acari) , Ceratophyllus sciurorum (Siphonaptera—Stroganova 1958; Albayrak and Arslan 2006), C. cusimilis (Siphonaptera— Enukidze 1960 ), Enderleinellus krochinae (Anoplura—Durden and Musser 1994) , Enderleinellus nitzschi (Anoplura—Durden and Musser 1994) , Neohaematopinus syriacus (Anoplura— Durden and Musser 1994) are known to infest S . anomalus . A rich fungal community exists in the pelage. Dermatophytes most frequently isolated from skin lesions were Microsporum canis (3.3%), M. gypseum (3.3–9.5%), M. persicolor (3.3%), and Trichophyton mentagrophytes (3.3–14.3%). All samples from skin lesions and pelage showed the growth of saprophytes to include Mucor (38.3%), Penicillium (28.3%), Aspergillus (26.7%), Alternaria (23.3%), and Fusarium (20%). Malassezia , Rhodotorula , and Candida species were the most important yeasts isolated (Khosravi and Mahmoudi 2003; Rostami et al. 2010 ). Alopecia in a yearling female from Iran was attributed to infection by the dermatophyte Epidermophyton floccosum ( Hosseininejad et al. 2010 ) . Pelts are harvested in significant numbers in Caucasia ( Ognev 1966 ; Vereshchagin 1967 ) and are used for fur clothing and ornamentation ( Dahl 1954 ). However, Kolosov et al. (1965) considered the number of pelts to be commercially insignificant relative to S. vulgaris , likely because the quality of S . anomalus pelts is considerably less than that of the S. vulgaris (Vinogradov and Gromov 1952; Enukidze 1960 ; Bobrinskii et al. 1965 ). Recent harvest rates are not available. Carcasses of S . anomalus are used to feed other domestic animals ( Stroganova 1958 ). S . anomalus is consumed by humans in northeastern Iraq ( Harrison 1972 ) and Jordan (Mendelsshon and Yom-Tov 1999). Young squirrels are sold as pets in Turkey ( Osborn 1964 ), Iran ( Rostami et al. 2010 ), and Jordan (Mendelsshon and Yom-Tov 1999). S. anomalus is often fed in the wild to increase viewing opportunities in Turkey ( Masseti 2012 ). It is considered a pest in some regions of Caucasia where it invades nut and fruit orchards ( Vereshchagin 1967 ). Miscellaneous. —Surveys for discarded pine cones that have had seeds removed can provide information on occupancy by Sciurus anomalus ( Amr et al. 2006 ) . S. anomalus was the least common of 9 mammals trapped in the Zagros Mountains of Iran (1.2% of 198 individuals—Shayan et al. 2008); however, the species can be livetrapped successfully ( Gavish 1993 ). Camera traps were used to detect S . anomalus ( Soyumert et al. 2010 ; Abi-Said et al. 2014; İlemin 2014 ). Individuals have been maintained in captivity for> 2 weeks and can be sedated using a xylazine/diazepam intramuscular cocktail (xylazine 5 mg /kg, diazepam 30 mg /kg—Veshkini et al. 2011). S. anomalus is displayed in Iran’s Tehran Zoo ( Asadi et al. 2008 ). BEHAVIOR Although Sciurus anomalus is most often solitary, groups of ≤ 9 individuals can feed in seed-laden trees ( Amr et al. 2006 ). The vocalization is a high-pitched, metallic sounding “chit-chitchit” ( Ognev 1966 ) and is used in response to the presence of a potential predator ( Kolosov et al. 1965 ). The call resembles that of the green woodpecker ( Picus viridis — Stroganova 1958 ). Calling is rare in spring but during other seasons can serve as an index to squirrel abundance ( Stroganova 1958 ). Individuals mark their home ranges with urine and feces (Hecht-Markou 1994, 1999). Sciurus anomalus is diurnal ( Ognev 1966 ; Harrison and Bates 1991) and active year-round with a morning activity period from sunrise to 1100 h (Abi-Said et al. 2014), and often a midday lull, and evening activity lasting until about 1800 h in Israel ( Gavish 1993 ) and Jordan ( Amr et al. 2006 ), extending to 1900 h in Greece (Hecht-Markou 1994). During winter, activity peaks during midday ( Enukidze 1960 ). Activity is reduced in cloudy and rainy weather ( Stroganova 1958 ). Juveniles may remain inactive during cold periods (Hecht- Markou 1994 ). Sciurus anomalus forages on the ground as well as in trees. Many nuts are harvested from trees and eaten prior to falling ( Stroganova 1958 ). S . anomalus appears to larderhoard seeds within cavities or clefts in trees ( Hatt 1959 ; Ognev 1966 ), in middens ( Osborn 1964 ), or in abandoned stone buildings ( Stroganova 1958 ). One larder was located> 300 m from the nearest nut tree ( Stroganova 1958 ). Larders may contain 5–6 kg of seeds ( Enukidze 1960 ). Conversely, S . anomalus in Lesbos caches food in the leaf litter and loose soil. The cached food is pressed into the ground with 5–10 repeating movements of the head and the food is covered with earth or leaves using the forelegs and paws (Hecht-Markou 1994). Nuts are held in the paws and the lower incisors are used to gnaw and enlarge a hole in the shell; the nut meat is retrieved by the lower incisors ( Stroganova 1958 ; Enukidze 1960 ). Sciurus anomalus is a highly terrestrial relative to S. vulgaris ( Kolosov et al. 1965 ) but does spend time in trees (Harrison and Bates 1991; Gavish 1993 ), although leaps between trees are rare ( Stroganova 1958 ; Kolosov et al. 1965 ). Although an excellent swimmer, S. anomalus avoids water ( Ognev 1966 ). Major postures ( Gavish 1993 ) include an attentive (vigilant) posture in which the individual sits or stands erect with forepaws against chest, sitting in the crotch of a tree with body against the trunk while eating with feet drawn forward for support, and crouching on a branch with head and tail rested upon limbs during rest or sunbathing. S. anomalus often forages in trees in an inverted position and can descend trees head first with extreme rotation of the crurotalar joint ( Fig. 4 ). Another characteristic posture is crawling on its abdomen with legs spread (Hecht- Markou 1994 ). Tail may be held above head with guard hairs erect and sometimes curved upward away from the posterior dorsum. The tail can be held folded on the back or stretched as far as the ears. The tail lies flat when resting and drags behind when running. Sciurus anomalus runs to the nearest tree and escapes through the canopy when threatened. Autogrooming is accomplished with the mouth; 2 instances of face-wiping against branches forested areas in Turkey (Yiğit and Çolak 1998; De Marinis and Maseti 2009); however, habitat degradation and fragmentation are a concern (Albayrak and Arslan 2006) and the species is considered uncommon in the Artvin Province of northern Turkey ( Gokturk et al. 2011 ). S. anomalus is locally common in protected areas in Azerbaijan ( Guliyev 2014 ). Population decline is noted in many peripheral areas of the species range, dangerously so in Lebanon and Syria , where hunting pressure and habitat loss continue ( Lewis et al. 1967 ; Yiğit et al. 2008 ). S. anomalus syriacus is considered endangered in Jordan ( Amr 2000 ). It is also protected due to imperiled status on Lesbos (Karandinos and Legakis 1992). Climate change has the potential to negatively impact 98% of the habitat of S. anomalus through the 21st century ( Harrison et al. 2006 ).