J Comp Physiol B DOI 10.1007/s00360-012-0705-4 ORIGINAL PAPER The tradeoff between torpor use and reproduction in little brown bats (Myotis lucifugus) Yvonne A. Dzal • R. Mark Brigham Received: 10 May 2012 / Revised: 17 August 2012 / Accepted: 24 August 2012 Ó Springer-Verlag 2012 Abstract In mammals, reproduction, especially for bats did not vary with reproductive condition, suggesting females is energetically demanding. Therefore, during the that even short, shallow bouts of torpor produce substantial reproductive period females could potentially adjust pat- energy savings, likely obviating the need to spend more terns of thermoregulation and foraging in concert to min- time foraging. Our data clearly show that torpor use and imise the energetic constraints associated with pregnancy reproduction are not mutually exclusive and that torpor use and lactation. We assessed the influence of pregnancy, (no matter how short or shallow) is an important means of lactation, and post-lactation on torpor use and foraging balancing the costs of reproduction for M. lucifugus. behaviour by female little brown bats, Myotis lucifugus. We measured thermoregulation by recording skin temper- Keywords Torpor Á Reproduction Á Bats Á Myotis ature and foraging by tracking bats which carried temper- lucifugus Á Foraging Á Thermoregulation ature-sensitive radio-tags. We found that individuals, regardless of reproductive condition, used torpor, but the Abbreviations patterns of torpor use varied significantly between repro- MR Metabolic rate ductive (pregnant and lactating) females and post-lactating Tb Body temperature females. As we predicted, reproductive females entered Ta Ambient temperature torpor for shorter bouts than post-lactating females. Tsk Skin temperature Although all females used torpor frequently, pregnant Troost Roost temperature females spent less time in torpor, and maintained higher LMM Linear mixed model skin temperatures than either lactating or post-lactating ANOVA Analysis of variance females. This result suggests that delayed offspring AIC Akaike information criterion development which has been associated with torpor use AICC Bias-corrected Akaike information criterion during pregnancy, may pose a higher risk to an individual’s reproductive success than reduced milk production during lactation. Conversely, foraging behaviour of radio-tagged Introduction Torpor is a temporary state of heterothermy defined by a Communicated by H. V. Carey. reduction in metabolic rate (MR) and other physiological processes (i.e. heart rate, breathing rate, body temperature Present Address: (T )) (Geiser and Ruf 1995; Geiser 2004). Although torpor Y. A. Dzal (&) b Department of Zoology, University of British Columbia, use results in a pronounced reduction in daily energy Vancouver, BC V6T 1Z4, Canada expenditure (Geiser 1994, 2004), there are other advanta- e-mail: [email protected]; [email protected] ges to torpor use that are often overlooked, such as accu- mulation of fat, reduction of water requirements, and sperm Y. A. Dzal Á R. M. Brigham Department of Biology, University of Regina, storage (for a full review see Geiser and Brigham 2012). Regina, SK S4S 0A2, Canada Supporting a high MR, typical of endothermic mammals, 123 J Comp Physiol B requires high levels of energy intake which is accom- 1994, 2004), assessments of torpor use in pregnant and plished through foraging. However, when food abundance lactating individuals are limited to a few mammals (for declines, the cost of maintaining an elevated MR may example, bats: Chruszcz and Barclay 2002; Willis et al. become prohibitively expensive. 2006; dormice: Fietz et al. 2005; dunnarts: Morton 1978; Body size has an important effect on an endothermic Geiser et al. 2005; lemurs: Randrianambinina et al. 2003; animal’s energy demand to maintain normothermy (for a mouse-opossums Bozinovic et al. 2005; mulgaras: Geiser review see McNab 2006). Small endotherms have higher and Pavey 2007; and prairie dogs: Lehmer et al. 2003). mass-specific MRs than larger ones to compensate for the Like most mammals, female Myotis lucifugus (little brown higher rate of heat and water loss in relation to their larger bat) invest substantial amounts of energy in reproduction. surface area (Geiser and Pavey 2007). The large surface Regulating Tb at high levels during the reproductive season area of small animals facilitates heat loss, therefore, is especially challenging for this species because not only maintaining Tbs at euthermic levels during times of low do they primarily eat insects, a food source whose avail- ambient temperatures (Tas) is energetically costly. Low ability is temperature dependent (Racey and Swift 1985; Ta not only increases the energetic costs of maintaining Speakman and Racey 1989; Park et al. 2000), but their euthermic Tbs but typically, it also decreases the abundance small and irregular body shape, and large wing surface area and availability of food. This energetic dilemma can be lead to high levels of heat loss. While this species has been further exacerbated during the reproductive season, the focus of numerous ecological and physiological studies, because in addition to the normal energetic costs of nor- and individuals are known to enter torpor both in the lab- mothermy, reproductive female mammals must dedicate a oratory and field (e.g. Fenton and Barclay 1980; Kurta substantial proportion of their energy budget to support et al. 1989), there are no data on the extent of torpor use by foetal growth, milk production, and nutrient acquisition free-ranging reproductive individuals. Thus, the aim of our (Farmer 2003). study was to assess the thermoregulatory and foraging To manage energetic constraints brought on by repro- strategies of M. lucifugus during the reproductive season. ductive condition or unpredictable weather, it should be We examined whether torpor patterns (frequency, duration, advantageous for endotherms to employ heterothermic and depth) varied among pregnant, lactating, and post- responses. Yet not all small endotherms use torpor when lactating females under natural conditions. Because faced with an energetic imbalance. This could be due to a reproduction is energetically costly, we hypothesised that tradeoff between using torpor for energy savings and the female bats would enter torpor on a regular basis, espe- costs associated with a reduction of nutrient absorption that cially when Ta, and consequently, food abundance coincides with declining Tb (Holloway and Geiser 1995), declined. Given that torpor use has been suggested to delay or the costs associated with daily arousal from torpor which foetal and juvenile development and decrease milk pro- have often been underestimated and may limit energetic duction, we predicted that pregnant and lactating females savings (Ko¨rtner et al. 2008). It has been suggested that would use shorter and shallower torpor bouts than post- torpor and reproduction are functionally incompatible (see lactating females. If pregnant and lactating females use Kenagy 1989), but more recently there has been accumu- torpor for shorter periods than post-lactating females then lating evidence which suggests this is not true. Torpor use they might be expected to make up the energy deficit by by females during the reproductive season has been foraging for longer periods (and presumably eating more) reported for some species from all three mammalian sub- than post-lactating females. By foraging longer, pregnant classes (Morton 1978; Chruszcz and Barclay 2002; Geiser and lactating females are more likely to acquire enough et al. 2005; Willis et al. 2006). However, it appears that energy to support the increased costs associated with when reproductive mammals do use torpor, they often use reproduction, while minimising the costs associated with it less than non-reproductive animals (see Landau and using torpor. Dawe 1960; Audet and Fenton 1988; Csada and Brigham 1994; Lausen and Barclay 2003; Nicol and Andersen 2006). Variation in torpor expression throughout the Methods reproductive stages of female mammals may, at least in some instances, be due to delayed foetal development Study site and species (Racey 1973; Krishna and Dominic 1982; Hoying and Kunz 1998), restricted or reduced milk production (Wilde We radio-tracked a total of 35 adult female M. lucifugus et al. 1999), all of which likely compromise reproductive from three maternity colonies from June to August of 2008 success. and 2009. Each colony roosted in a human-made structure Although torpor in mammals has been well studied located in Upstate New York: Fort Edward (43°090N, during the non-reproductive season (for reviews see Geiser 73°3400W), Greenwich (43°070N, 73°340W), and Willsboro 123 J Comp Physiol B 0 0 (44°21 N, 73°23 W). We captured bats by picking them off Torpor onset À 1SE¼ ½ðÞ0:041 ðÞbody mass the walls of roosts, or using mist-nets or a harp trap set in ð1Þ þðÞ0:040 ðÞþðTa 31:083Þ known foraging areas or in proximity to maternity colonies. All bats caught were banded with a metal split ring (to The Tsk threshold used to differentiate torpor from ensure we did not affix radio-tags to the same bat twice), normothermia ranged from 31.3 to 33.0 °C for different and we recorded reproductive condition and body mass individuals (pregnant 31.8–33.0 °C; lactating 31.3– (±0.1 g). To prevent overlap in our classification of 33.0 °C; post-lactating 31.4–33.0 °C). We classified a bat reproductive condition, we only affixed radio-tags to as being torpid anytime that Tsk fell below the torpor