J Comp Physiol B DOI 10.1007/s00360-014-0834-z

Original Paper

Torpor is not the only option: seasonal variations of the thermoneutral zone in a small primate Susanne Kobbe · Julia Nowack · Kathrin H. Dausmann 

Received: 14 November 2013 / Revised: 30 April 2014 / Accepted: 8 May 2014 © Springer-Verlag Berlin Heidelberg 2014

Abstract  The reddish-gray mouse lemur (Microcebus griseorufus) is one of only a few small mammals inhabiting the spiny forest of southwestern Madagascar. In this study we investigated the physiological adjustments which allow these small primates to persist under the challenging climatic conditions of their habitat. To this end we measured energy expenditure (metabolic rate) and body temperature of 24 naturally acclimatized mouse lemurs, kept in outdoor enclosures, during different seasons (summer, winter, and the transition period between the two seasons). Mouse lemurs displayed two main physiological strategies to compensate seasonal and diurnal fluctuations of ambient temperature. On the one hand, individuals entered hypometabolism with decreasing ambient temperature (Ta) during the transition period and winter, enabling them to save up to 21 % energy per day (92 % per hour) compared with the normal resting metabolic rate at comparable Ta. On the other hand, euthermic mouse lemurs also showed physiological adjustments to seasonality when resting: the lower critical temperature of the thermoneutral zone decreased from summer to winter by 7.5 °C, which allowed mouse lemurs to keep energy demands constant despite colder Tas during winter. In addition, the basal metabolic rate was substantially lowered prior to the winter period, which facilitated accumulation of fat reserves. The combination of physiological modifications during euthermia in addition to hypometabolism, which can be individually adjusted according to external

Communicated by G. Heldmaier. S. Kobbe (*) · J. Nowack · K. H. Dausmann  Department of Animal Ecology and Conservation, University of Hamburg, Biocentre Grindel, Martin‑Luther‑King Platz 3, 20146 Hamburg, Germany e-mail: Susanne.Kobbe@uni‑hamburg.de

parameters and respective body condition, is important as it allows M. griseorufus to cope with the environmental variability of an energetically challenging habitat. Keywords  Hypometabolism · Malagasy mouse lemurs · Metabolic rate (MR) · Pronounced seasonality · Seasonal body fattening

Introduction Species living in habitats with climatic variations cannot adapt to a consistent environmental and tropic condition, but have to cope with recurrent changes of these parameters. For example, varying ambient temperature (Ta) has a strong influence on animals’ metabolic functions and Ta extremes can cause functional constraints (Pörtner and Farrell 2008). Endothermic animals are able to maintain their body temperature (Tb) constant largely independent from Ta. However, extreme Ta as well as strong fluctuations of Ta can be energetically challenging. Indeed, any Ta above or below the thermoneutral zone (TNZ) affects an animal’s physiology and requires physiological thermoregulation, ultimately leading to an increase in energy demands. The TNZ is the range of Ta where standard metabolic processes suffice to maintain a high Tb, and thus there are no additional thermoregulatory costs and metabolic rates (MR) of euthermic animals are minimal. Mammals and birds have evolved a number of seasonal adjustments in their behavior, morphology and/or physiology, such as huddling, or changes in body mass, pelage insulation or MR to counter climatic variability (e.g., Scholander et al. 1950; Hart and Heroux 1955; Heldmaier 1989; Terrien et al. 2011; Nowack et al. 2013). Effective measures especially for small endotherms to save energy during periods of low Ta and food/

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water scarcity are hypometabolic states, such as hibernation and daily torpor (Geiser 2004; Heldmaier et al. 2004). A more subtle physiological response to environmental changes is, for example, a seasonal shift of the range of the TNZ (Heldmaier and Steinlechner 1981). The spiny forest of southwestern Madagascar is one of the driest and most unpredictable regions of the island, with pronounced seasonal as well as daily fluctuations in Ta, a low availability of food, a lack of water during the cool dry season, and high inter-annual variations in rainfall. This makes it an ideal habitat to investigate physiological responses of animal species to natural environmental variations. One of just a few small mammals inhabiting this region is the reddish-gray mouse lemur (Microcebus griseorufus, 60 g; Kollman 1910), a small, nocturnal Malagasy primate. Former studies showed that all individuals of M. griseorufus become torpid at some point during the winter, but to very varying degrees, presumably depending on body condition (Kobbe et al. 2011). Thus, individuals of the same population use different forms of hypometabolism, from occasional daily torpor, over regular daily torpor and prolonged torpor (1–3 days), to long-term hibernation to compensate food and water shortage during the cool winter months (Kobbe et al. 2011). Individuals that only engage in occasional bouts of daily torpor, however, experience long stretches of euthermia between torpor bouts, and have to sustain this physiological condition despite low Ta and reduced food and water availability. Mouse lemurs within the spiny forest do not only have to cope with seasonal, but also with extreme diurnal fluctuations of Ta (up to 30 °C), which should exceed their narrow TNZ for most time of the day (Scholander et al. 1950; Dausmann et al. 2009). An intriguing question therefore is, how these different Tas affect the energy expenditure of small endotherms like M. griseorufus throughout the year, and whether there are physiological adjustments to winter conditions in addition to hypometabolic responses. Especially in the light of a predicted increase of Ta in this region in the near future due to a generally changing global climate (+2 °C; Hannah et al. 2008), phenotypic flexibility and adaptability in this aspect might prove essential for survival. In this context, studies of physiological mechanisms in individuals under natural abiotic conditions are considered especially important, as animals might only be able to show all of their physiological possibilities, when they are not restricted by laboratory conditions (Bennett and Nagy 1977; Geiser et al. 2007; Warnecke et al. 2007). In this study we aimed to characterize the physiological responses and possibilities of M. griseorufus to the strong seasonal variations of climatic conditions with the following questions: How do levels of metabolic rate (MR) in euthermic mouse lemurs differ between seasons? How

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J Comp Physiol B

substantial are the energy savings of hypometabolism? Do mouse lemurs display physiological adjustments besides hypometabolism in response to environmental changes?

Materials and methods Study area, trapping and animals The study was conducted within the Tsimanampetsotsa National Park, a dry spiny forest area near Tulear at the southwestern coast of Madagascar (24°03′–24°12′S, 43°46′–43°50′E). The climate of this habitat is characterized by a rainy season between November and March (summer) with high daily Tas (ranging between 15 °C at night and 45 °C during daytime) and a dry season from May to September (winter) with warm days (up to 38 °C), low Ta at night (down to 6 °C) and low availability of food and water. Short transition periods with comparably moderate climatic conditions occur in April and October (Kobbe et al. 2011). Mouse lemurs were captured within a trapping grid system of 100 × 300 m with 96 Sherman live traps (7.7  × 7.7 × 30.5 cm) set every 20 m within the grid, 50–200 cm above the ground during one transition period (April 2008), during one summer (February and March 2009) and one winter (June and July 2009). During the transition period and in winter traps were baited in the afternoon and checked and closed early in the morning on four consecutive days each month. During summer traps were controlled four times a day between 1800 and 2400 h to release lactating females, allowing them to return to their newborns promptly, and closed thereafter. Only adult animals (>40 g) were selected for further measurements Measurements of MR and Tb in captive animals For measurements of MR mouse lemurs were individually kept in outdoor enclosures (1.50 × 1.50 × 1.50 m) placed near the trapping grid at the shady site of a tree experiencing natural variation of Ta, photoperiod and humidity. A diet of water, banana and cockroaches was supplied ad libitum. Each enclosure was equipped with branches and a wooden nest box (14 × 20 × 14 cm), which offered a front and a rear compartment, connected by a small passage. The latter was used by the animals as a sleeping quarter and served as the metabolic chamber. The rate of metabolism was measured as VO2 (rate of oxygen consumption) using a portable oxygen analyzer (OxBox, designed and constructed by T. Ruf and T. Paumann, FIWI, University of Veterinary Medicine Vienna) with chemo-electric oxygen sensors (Bieler and Lang, Achern, Germany; accuracy

Torpor is not the only option: seasonal variations of the thermoneutral zone in a small primate.

The reddish-gray mouse lemur (Microcebus griseorufus) is one of only a few small mammals inhabiting the spiny forest of southwestern Madagascar. In th...
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