149 Do Owls Use Torpor? Winter Thermoregulation in Free-Ranging Pearl-Spotted Owlets and African Scops-Owls Ben Smit* 6,500 g, and in a much wider variety of ecological contexts Andrew E. McKechnie† than previously thought (Ko¨rtner et al. 2000; McKechnie and DST/NRF Centre of Excellence at the Percy FitzPatrick Lovegrove 2002). Within the Coraciiformes, for instance, het- Institute, School of Animal, Plant and Environmental erothermy occurs in both the smallest and largest representa- Sciences, University of the Witwatersrand, Private Bag 3, tives, namely, the 5-g Puerto Rican tody Todus mexicanus and Wits 2050, South Africa the 360-g laughing kookaburra Dacelo novaeguineae (Merola- Zwartjes and Ligon 2000; Cooper et al. 2008). Accepted 3/6/2009; Electronically Published 11/24/2009 Torpor, often defined as a reduction in rest-phase Tb below 30ЊC (Hudson 1978; Reinertsen 1996; Schleucher 2001; re- viewed by Barclay et al. 2001), appears to be particularly im- portant in offsetting the energetic costs of thermoregulation in ABSTRACT birds whose food resources exhibit large spatial or temporal Numerous avian taxa use torpor, which involves pronounced fluctuations in availability, for example, frugivores (Coliidae reductions in body temperature (Tb) to below normothermic and Columbidae), nectarivores (Trochilidae and Nectariniidae), levels. However, the occurrence of this phenomenon in owls and insectivores (Todidae, Apodidae, Caprimulgidae, and Hi- (Strigidae) remains largely unknown. We investigated winter rundinidae; McKechnie and Lovegrove 2002; Schleucher 2004). patterns of thermoregulation in the crepuscular 80-g pearl- However, to better understand the adaptive value and evolution spotted owlet Glaucidium perlatum and the strictly nocturnal of avian torpor, a more thorough assessment of the phylogenetic 61-g African scops-owl Otus senegalensis by obtaining telemetric distribution of this trait is needed (McKechnie and Lovegrove measurements of skin temperature (Tskin) from free-ranging 2002; Schleucher 2004). individuals in the Kalahari Desert of southern Africa. Pearl- One of the most puzzling phylogenetic patterns in the oc- spotted owlets remained homeothermic throughout the study currence of avian torpor concerns the order Strigiformes (sensu period, whereas African scops-owls routinely used shallow tor- Sibley and Ahlquist [1990], but see Hackett et al. [2008]), which עЊ Њ Њ por, with Tskin reduced by 3.3 –8.6 C (pooled mean, 5.3 contains the suborders Caprimulgi (nightjars and allies) and 1.1ЊC) below normothermic levels for 3–4 h after sunrise. The Strigi (owls). Whereas the capacity for pronounced torpor is mean lowest Tskin recorded in three African scops-owl individ- widespread in caprimulgids (Lane et al. 2004), it has not been -0.1ЊC . The thermoregulatory differences be- reported in owls (Ligon 1969; Hohtola et al. 1994), an obserעuals was29.0Њ tween these two species may be related to their diets and activity vation that is surprising in view of the close phylogenetic re- patterns. African scops-owls are almost exclusively insectivo- lationship of these two groups (Sibley and Ahlquist 1990). Only rous and experience a marked reduction in food availability on shallow reductions in Tb have been reported in two relatively cold winter nights. In contrast, pearl-spotted owlets have more large owl species, the snowy owl Nyctea scandiaca and the barn flexible activity patterns and include larger or diurnal vertebrate owl Tyto alba (Gessaman and Folk 1969; Thouzeau et al. 1999). prey in their diet. In the latter study, barn owls that were starved in the cold for Њ 8 d never reduced Tb by more than 5 C, despite Mb loss of 125% (Thouzeau et al. 1999). Several studies of smaller species, however, failed to document any evidence whatsoever for het- erothermic responses, leading the authors to conclude that Introduction small owls can endure extended periods of energy stress without Many birds are heterothermic endotherms and downregulate using torpor (Ligon 1969; Hohtola et al. 1994). body temperature (Tb) to below normothermic levels during It is noteworthy, however, that all thermoregulatory studies the rest phase. Heterothermic responses have been reported in on owls to date have been carried out under artificial conditions ! 11 orders, in species ranging in body mass (Mb)from 3to in laboratories, and we know very little about how wild owls thermoregulate in natural habitats. Data from free-living birds * Corresponding author; [email protected]. are particularly important in light of recent studies showing †Present address: Department of Zoology and Entomology, University of Pre- that many birds use torpor only under natural conditions toria, Pretoria 0002, South Africa. (Brigham et al. 2000; Ko¨rtner et al. 2001; Fletcher et al. 2004; Physiological and Biochemical Zoology 83(1):149–156. 2010. ᭧ 2010 by The Lane et al. 2004; Cooper et al. 2008). University of Chicago. All rights reserved. 1522-2152/2010/8301-8134$15.00 In arid environments with unpredictable rainfall and low DOI: 10.1086/605457 productivity, torpor is thought to play an important role in 150 B. Smit and A. E. McKechnie balancing energy in many endotherms (Geiser 2004). To further Skin Temperature Recording explore the occurrence of torpor in owls, we investigated pat- terns of thermoregulation in free-living pearl-spotted owlets Skin temperature (Tskin) was measured using temperature- Glaucidium perlatum and African scops-owls Otus senegalensis sensitive VHF transmitters (2.5 g, model PD-2T, Holohil Sys- in the Kalahari Desert of South Africa. The Kalahari Desert tems, Carp, Ontario, Canada) emitting a frequency between region is characterized by extremes of temperature, arid winters, 150.061 and 150.741 MHz. These transmitters were calibrated and unpredictable precipitation during summer (Lovegrove in a temperature-controlled water bath at temperatures between 1993). Small owls inhabiting this area are thus likely to expe- 5Њ and 45ЊC, using the mercury thermometer (resolution p rience food shortages during cold and dry winter nights when 0.2ЊC). A broadband communications receiver (IC-R10, Icom, the availability of arthropod prey is reduced. Bellevue, WA) was used to obtain signals from the transmitters during calibration. The relationships between pulse rate and Material and Methods temperature were best described by second-order polynomial regressions, with all r2 values 1 0.995. Shortly after each owl Study Site was captured, a transmitter was secured dorsally beneath the Free-ranging pearl-spotted owlets and African scops-owls were feathers in the interscapular region, using a harness constructed studied in Molopo Nature Reserve (25Њ47ЈS, 22Њ56ЈE) at an from clothing elastic inserted through a 6.5-mm Teflon ribbon elevation of approximately 1,000 m above sea level in the (Telonics, Mesa, AZ), a design modified from Figure 18.2 of Northwest Province, South Africa, from June 1 to August 9, Kenward (2000), following McKechnie et al. (2007). This 2007 (austral winter). This reserve falls within the semiarid method has been widely used for the measurement of Tskin in Kalahari Desert region, where the climate varies seasonally be- free-ranging caprimulgids (Brigham 1992; Brigham et al. 2000; tween dry and cool winters (May to August) with frequent McKechnie et al. 2007), and loose harnesses can be readily subzero temperatures at night and hot summers (November to detected from Tskin readings that vary unpredictably. Owls, how- March) with spatially and temporally unpredictable patterns of ever, are more likely to damage harnesses than are nightjars; if SD annual rainfall there were any indications that a harness had come loose, we ע rainfall (Lovegrove 1993). The mean recorded in Molopo Nature Reserve over a 50-yr period was excluded data from that individual. -mm (Meyer et al. 2007). Our study took place in The signals emitted by Holohil transmitters have been re 105 ע 332 the southern part of the reserve, where the vegetation consisted ported to drift, and they should be recovered after data col- mainly of mixed Acacia spp. and Boscia albitrunca savannah lection and recalibrated (J. B. Williams, personal communi- on deep red sand and scrub on irregular dry calcrete pans. cation). We recovered transmitters from two African scops-owls 5 wk after they were tagged and recalibrated them at three temperatures (19Њ,29Њ, and 39ЊC) in the water bath. At 39ЊC, Air Temperature Recording the pulse rates of both transmitters were higher than they were Air temperature (Ta) was measured in the study area using two during initial calibration (equivalent to a mean change in Tskin temperature-sensitive data loggers (iButton Thermochron, Dal- readings of 1.2ЊC), but at 19Њ and 29ЊC, the pulse rates were las Semiconductor, Dallas, TX). The iButtons were housed in identical to initial calibration. Since we were not able to retrieve ventilated polystyrene cups suspended in the shade about 2 m transmitters from any of the pearl-spotted owlets, we examined ! above the ground, at two sites about 6 km apart ( 10 m dif- Tskin values of the pearl-spotted owlets to investigate whether ference in altitude). Before the study, the iButtons were cali- there were any consistent changes in Tskin that might be the brated in a temperature-controlled water bath (model ME, Ju- result of transmitter drift. We compared each individual’s night- labo Labortechnik, Seelbach, Germany), using a mercury time (1800 to 0500 hours) Tskin data recorded during the first thermometer (resolution p 0.2ЊC ) with an accuracy traceable 4 d to the last 4 d of data collection but found no significant to the U.S. National Bureau of Standards, over the approximate differences. Ta range experienced at the study site during winter. We recorded Tskin from June 1, 2007, to August 9, 2007, in eight pearl-spotted owlets (data collection per individual of 39, 39, 36, 32, 20, 12, 11, and 3 d) and four African scops-owls Capture of Birds (28, 22, 6, and 4 d of data collection). We used a broadband Eight pearl-spotted owlets (three males, five females) and four communications receiver (IC-R10, Icom, Bellevue, WA) to ob- African scops-owl (all males) were caught during June and July tain signals from the transmitters.