Huddling behaviour and energetics of Sminthopsis spp. (Marsupialia, Dasyruidae) in response to environmental challenge
Introduction
Behavioural adaptations are an important consideration in the study of the physiology of mammals because behaviour can greatly influence energy requirements [1]. At low ambient temperature (Ta), many species of small mammal huddle, thereby reducing the thermal conductance of individuals within the group and reducing the energetic cost of living for each individual (e.g. [1], [2], [3]). Huddling can provide a saving of up to a third of daily energy expenditure [4], [5], [6], [7], [8]. In this study we examine the social and behavioural ecology in conjunction with physiology for two small, arid-zone, carnivorous marsupials (dunnarts).
The stripe-faced dunnart (Sminthopsis macroura) and the Ooldea dunnart (Sminthopsis ooldea) are small, carnivorous, nocturnal marsupials that are superficially similar in ecology, habits, size and body mass (S. macroura 15–25 g, S. ooldea 10–18 g [9], [10]). S. macroura is widespread across the north and east of continental Australia, while S. ooldea is confined to a smaller, “hyper-arid” (sensu [11], [12]) distribution around the conjoined borders of Western Australia, South Australia and the Northern Territory [13] in continental Australia, characterised by the highest daily and seasonal temperature fluctuations, highest evaporation and lowest rainfall on the continent. Although aspects of the energetics of S. macroura have been studied extensively in the laboratory [14], [15], [16], [17], [18], [19], basal metabolic rate (BMR) and patterns of thermoregulatory response across a range of Tas have only been measured recently for S. ooldea [20], [21]. When acclimated to different Ta, the thermoregulatory strategy of S. macroura was to thermoregulate effectively (i.e. to maintain constant body temperature, Tb) during thermal challenge with no alteration in BMR, but to increase the maximum metabolic rate when acclimated to cold conditions. Sminthopsis ooldea was more thermolabile (i.e. less likely to maintain constant Tb), and the lower cost of this strategy was fixed, regardless of the chronic thermal regimes [20]. The energetic advantages of using torpor during thermo-energetic challenge have been well-established for both species [1], [15], [17], [18], [19], [20], [21], and is torpor apomorphic amongst dasyurid marsupials [1], [22], [23]. The social behaviour of Sminthopsis is less well studied than physiology. Ewer [24] found that another dunnart, Sminthopsis crassicaudata, had explicit social behaviours and formed dynamic hierarchies that were subsequently maintained by ritualised interactions. Morton [25], [26] and Frey [27] found that S. crassicaudata commonly formed mixed-sex groups of two to eight individuals when resting in burrows in autumn and winter, but that the average group size was highly variable. Although these studies suggest that social grouping by S. crassicaudata is not obligate, Morton [25] found that very rarely was the entire population solitary. While social interactions in cold conditions are often considered an adaptation to reduce energy expenditure through reduced thermal conductance, the energetic consequences of sociality have never been quantified for Sminthopsis. Given that the thermoregulatory strategy of S. macroura may contribute to its broad distribution, and the thermoregulatory strategy of S. ooldea might contribute to its narrower distribution [20], we hypothesise that S. macroura may have additional behavioural flexibilities that act in concert with physiology to help it to respond to climatic variability, whereas S. ooldea may not.
We examine here the propensity of S. macroura and S. ooldea to socialise and to huddle under a range of thermal conditions, and quantify the energy savings resulting from huddling. For social aggregation to occur at low Ta, aggressive interactions must decrease. We first hypothesise that group size (number of individuals using the same nestbox) will increase as Ta decreases, and that along with that the rate of aggressive encounter and/or the aggression levels associated with these encounters. We expect S. macroura to have more flexible social interactions than S. ooldea, which is more likely to rely constantly on combined social behaviours and thermolability [20]. We further hypothesise that in a freely-socialising environment, S. macroura will huddle and reduce their individual energetic requirements of thermoregulation, but that S. ooldea may do so to a greater extent. The mechanism for energy saving by huddling mammals is reduced thermal conductance per capita by virtue of their physical contact decreasing exposed surface area, so we also expect a decrease in individual thermal conductance and metabolic rate for huddled S. macroura.
Section snippets
Animals and housing
Sminthopsis macroura were captured from various sites across Western Australia, and S. ooldea were captured at Lorna Glen Station (26.227° S, 121.5597° E). The dunnarts were transferred to the University of Western Australia (Crawley campus) within a week of capture. The initial study was free socialisation, in which two experimental “colonies”, each consisting of six individuals, were established for each species. Each colony was housed in an octagonal communal arena, consisting of eight
General behavioural responses
The activity period of S. macroura was longer at the higher, compared to the lower, Ta regimes (F3,88 = 15.1; p = 5.29 × 10− 8); SNK post-hoc tests were significant for all Ta regime comparisons with the exception of the 18–28 °C vs. 25–35 °C regimes(p = 0.533; Table 1). S. macroura were found randomly in nest boxes (they were found in their original nest box on 13.7 ± 1.5% mornings, compared to 16.7% expected at random; χ27 = 11.8, p = 0.107) across all Ta regimes (546 box mornings in total), so the dunnarts
Discussion
There has recently been considerable interest in integrating the behavioural and physiological means that small animals use to manage their energy budget in environments with a thermoregulatory cost (mostly cold in winter), both at the interspecific level (e.g. [35], [36]) and intraspecific level (e.g. [37]). We found a complex and different mix of behavioural and physiological responses to the challenge of lowered Ta in the dunnart species that we studied here. In addition to generally
Conclusions
The two species of dunnart studied here have two distinct patterns of social behaviour in response to climatic conditions. S. macroura has flexible social behaviours where aggression is reduced, and the propensity to huddle increases at chronic low temperatures, whereas S. ooldea shows very little flexibility in its social behaviour under different Ta regimes. These differences in social behaviours have implications for the energetics of individual dunnarts, whereby S. macroura reduces
Acknowledgments
This work was supported by School of Animal Biology, UWA and the Holsworth Wildlife Research Endowment (ANZ Philanthropy Partners). We acknowledge the School of Animal Biology, UWA for infrastructural support for this research. Dr. Karl Brennan (DPaW Kalgoorlie) and Mr. Keith Morris (DPaW Woodvale) are acknowledged for access to Lorna Glen Station, and Bill Muir, Gary Hearle, Mark Harbour, Ryan Ellis and Judy Dunlop (DPaW Western Australia), Dr Scott Thompson, Dr. Jessica Oates and Dr Graham
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