Natural History, Physiology and Energetic Strategies of Asellia Tridens (Chiroptera)

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Natural History, Physiology and Energetic Strategies of Asellia Tridens (Chiroptera) Mammalian Biology 78 (2013) 94–103 Contents lists available at SciVerse ScienceDirect Mammalian Biology journal homepage: www.elsevier.com/locate/mambio Original Investigation Natural history, physiology and energetic strategies of Asellia tridens (Chiroptera) Eran Amichai ∗, Eran Levin, Noga Kronfeld-Schor, Uri Roll, Yoram Yom-Tov Department of Zoology, Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel article info abstract Article history: We used radio-telemetry, observations and physiological measurements to study the basic biology and Received 20 February 2012 energetic strategies of Asellia tridens in northern Israel from 2009 to 2010. Between late May and early Accepted 21 June 2012 November, the bats occupied abandoned man-made structures in this area. Parturition occurred between Available online 25 July 2012 late June and mid-July, and juveniles were independent by late August. A. tridens foraged near the roost in a vegetation-rich, cluttered background environment, catching insects flying close to vegetation. Its Keywords: diet was diverse, with Coleoptera, Heteroptera, Diptera and Lepidoptera being the main diet components. Chiroptera During summer, males and females differed in their foraging patterns and energetic strategies: Lactating Foraging pattern Energetic strategies females departed for more frequent foraging bouts than males, and maintained euthermy throughout Reproductive cycle the day, while males became torpid on a daily basis. Torpor © 2012 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved. Introduction and Hymenoptera (Feldman et al., 2000; Whitaker and Yom-Tov, 2002). However, its natural history – foraging behaviour, prey pref- Asellia tridens (Geoffroy, 1813; Hipposideridae) is a medium- erence, home range, reproduction cycle, and seasonal movement – sized bat (forearm length ca. 50 mm, body mass ca. 12–13 g, is still poorly known. (Jones et al., 1993)). In its family it is the species most adapted Although mammals are generally considered to be euther- to arid environments and has the widest distribution, inhabit- mic, a large number of mammalian species use heterothermy ing Mediterranean to extremely arid habitats from North-western either for short period (daily) torpor or for long term hiberna- Africa through the Arabian Peninsula east to Pakistan (Nowak, tion. Heterothermy is common in temperate zones small mammals, 1994). In Israel it is the only Hipposiderid, where it is relatively including bats, and is usually associated with strong seasonality, common in the Jordan and Arava Valleys, (part of the Great Rift low winter temperatures and low food availability. Lately, how- Valley). In this area A. tridens is known to roost in colonies number- ever, it is becoming evident that heterothermy is not only present, ing several hundred to several thousand individuals (Mendelssohn but probably common, in tropical and sub-tropical species as well and Yom-Tov, 1999). It occupies maternity and summer roosts from (Geiser and Stawski, 2011; Levy et al., 2011a,b; Liu and Karasov, late spring (May) to mid autumn (November), but in most cases 2011; Lovegrove, 2000). its wintering locations are unknown (Mendelssohn and Yom-Tov, Male and female A. tridens arrive at the summer roosts in dif- 1999). Little work has been carried out on the biology of A. tri- ferent stages in their reproductive cycle, and are therefore subject dens. There is some information on its reproductive cycle: in Iraq it to different energetic demands and constraints (Gittleman and gives birth to a single pup around June, after a pregnancy period of Thompson, 1988; Kurta et al., 1989). We hypothesized that these 9–10 weeks, and lactation lasts about 40 days (Mendelssohn and differences between the sexes will result in different energetic Yom-Tov, 1999; Qumsiyeh, 1996). It produces echolocation calls strategies that will be evident in fat reserve accumulation and with a cf. component at 111–124 kHz lasting 3–10 ms that ends daily body temperature patterns, and that males, but not lactating with a terminal downward sweep of 19–21 kHz (Gustafson and females, will use daily torpor. Such differences have been described Schnitzler, 1979) and its flight morphology have been character- in species from temperate zones (Dietz and Kalko, 2006; Grinevitch ized as suitable for cluttered environments (Jones et al., 1993). Its et al., 1995), but it is unclear whether they exist in species with trop- guild association in the Dead Sea area is a cluttered environment bat ical or sub-tropical distribution, where ambient temperatures are and its diet in the area consists mostly of Coleoptera, Lepidoptera much higher. In this study we used temperature sensitive radio-transmitters to record skin temperatures and combine these data with exten- sive observations and measurements to present some data on ∗ Corresponding author. Tel.: +972 3 6409397; fax: +972 3 6409403. the ecophysiology and biology of A. tridens at the limit of its E-mail address: [email protected] (E. Amichai). distribution. 1616-5047/$ – see front matter © 2012 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.mambio.2012.06.006 E. Amichai et al. / Mammalian Biology 78 (2013) 94–103 95 Material and methods Three additional roosts were monitored occasionally (4–5 times each in the season) to provide comparisons from different regions: Study area Timna Cave colony in the southern Arava desert (29◦45N, 34◦59E), Tel-Azaz’yat colony in the Golan Heights (33◦13N, 35◦40E) and The bats were studied in the Beit-She’an valley (32◦33N, Kochav-Ya’ir colony in the eastern Mediterranean region (32◦13N, 35◦34E). This area is a part of the Great African Rift system, com- 35◦00E). prising low flatlands on the eastern and western sides of the Jordan River, about 11 km south of Lake Kineret. The Jordan River valley Observations is ca. 6 km wide, its floor is ca. 250 m below sea level, and it is enclosed on both sides by steep slopes. The climate is subtropi- Observations were carried out at least once a week during the cal, with dry and hot summers (mean daily maximal temperature summer (May through October) of 2009 and 2010. Number of indi- in July: 37.6 ◦C) and moderate winters (mean minimal tempera- viduals was estimated by counts on site and from photographs tures in February: 9.2 ◦C, mean maximal temperature in February: taken on site and examined later. Sex ratio estimate was possi- 19.2 ◦C, mean annual precipitation: 389.1 mm, Israel Meteorolog- ble due to the males’ easily visible penis. Behavioural observations ical Service). Water sources are abundant along the valley, with were carried out at least once every two weeks on emergence of numerous artificial (fishing ponds, reservoirs) and natural water the bats and during foraging, with the aid of bat detectors (D1000X, sources (springs), in addition to the Jordan River itself. Native PetterssonElektronik, Sweden). riparian vegetation is concentrated in streambeds and consists of Sudanian, Saharo-Sindian, Oriental and Mediterranean elements Measurements (Yom-Tov and Tchernov, 1988). A mixture of native and disturbed habitat vegetation exists on fishpond banks and along irrigation Bats were captured inside the roosts using hand nets. Bats were channels. Most of the valley area is used for agriculture, mainly not individually marked, but from 60 of the total 341 adults cap- grain fields and banana plantations west of the Jordan, and orchards tured a wing biopsy was taken for future genetic analysis, and an and palm tree plantations east of the Jordan. additional 20 were fitted with transmitters. Only two of those 80 Four roosts in the area were consistently monitored during bats have been recaptured, suggesting a negligible recapture rate. 2009–2010 (Fig. 1): three abandoned military bunkers on the slopes Captures were carried out during both seasons, at least once every (TY south, TY north and Keren) and an abandoned fortified building 10 days, often more frequently. Each time 3–8 individuals were cap- on the valley floor (Gesher). tured, measured and released back into the colony. Measurements were carried out outside the roost to minimize disturbance, so that usually less than a minute was spent inside the roost. Our obser- vations show that a few minutes after such disturbances the bats relax and resume normal behaviour. Each captured individual was weighed to an accuracy level of 0.1 g using digital scales (Micron, China), its forearm (FA) length measured to an accuracy level of 0.1 mm using a caliper (Mitutoyo, Japan), and its sex was deter- mined. Bats were classified as either adult or juvenile according to the degree of finger joint ossification (Kunz, 1988) and pelage col- oration (Dietz, 2007). Reproductive state was noted in males (testes developed/un-developed) and in females (pregnant/lactating/post lactating/not reproductive). Fat reserve levels were assessed visu- ally according to the size of the uropatagium fat store. A 7-level index was created, from 0 (empty fat stores) to 6 (completely full fat stores). This fat level index was compared to body fat percentages obtained from 23 individuals using a Dual Emission X-ray Absorp- tiometry (DEXA, PIXImus, General Electric, USA). This method scans a subject using X-ray beams of two different energies, enabling the determination of fat percentage according to absorption lev- els, as well as other information such as bone mineral density. Fat index was found to be highly correlated with body fat percentage (Spearman rank correlation, N = 23, R2 = 0.87, p < 0.05) and was sub- sequently used to represent fat reserve levels. Roost temperature was obtained from TY south, TY north and Keren to an accuracy level of 1 ◦C using ThermochroniButtons (Dallas Semiconductors, USA) set to record ambient temperature at 3 hour intervals through- out the season. iButtons were attached to cables hanging from the ceiling about 40 cm under the bats.
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