Private Heat for Public Warmth: How Huddling Shapes Individual Thermogenic Responses of Rabbit Pups

Abstract

BackgroundWithin their litter, young altricial mammals compete for energy (constraining growth and survival) but cooperate for warmth. The aim of this study was to examine the mechanisms by which huddling in altricial infants influences individual heat production and loss, while providing public warmth. Although considered as a textbook example, it is surprising to note that physiological mechanisms underlying huddling are still not fully characterised.Methodology/Principal FindingsThe brown adipose tissue (BAT) contribution to energy output was assessed as a function of the ability of rabbit (Oryctolagus cuniculus) pups to huddle (placed in groups of 6 and 2, or isolated) and of their thermoregulatory capacities (non-insulated before 5 days old and insulated at ca. 10 days old). BAT contribution of pups exposed to cold was examined by combining techniques of infrared thermography (surface temperature), indirect calorimetry (total energy expenditure, TEE) and telemetry (body temperature). Through local heating, the huddle provided each pup whatever their age with an ambient “public warmth” in the cold, which particularly benefited non-insulated pups. Huddling allowed pups facing a progressive cold challenge to buffer the decreasing ambient temperature by delaying the activation of their thermogenic response, especially when fur-insulated. In this way, huddling permitted pups to effectively shift from a non-insulated to a pseudo-insulated thermal state while continuously allocating energy to growth. The high correlation between TEE and the difference in surface temperatures between BAT and back areas of the body reveals that energy loss for non-shivering thermogenesis is the major factor constraining the amount of energy allocated to growth in non-insulated altricial pups.Conclusions/SignificanceBy providing public warmth with minimal individual costs at a stage of life when pups are the most vulnerable, huddling buffers cold challenges and ensures a constant allocation of energy to growth by reducing BAT activation.

Interplay between group size, huddling behavior and basal metabolism: an experimental approach in the social degus

“…In fact, huddling promotes local heating and reduces the cold challenge, because single degus experienced colder conditions compared with degus huddling in a group of five (Fig. 2), a phenomenon that has been also recently demonstrated in rabbit pups (Gilbert et al, 2012). It is therefore likely that the individual minimum energy requirement decreases in degus that huddle for long periods, as occurs with the energy expenditure of this species when grouped (Canals et al, 1989;Kotze et al, 2008).…”

“…Thus, decreasing thermogenic response by means of huddling may lead to a decrease in food needs and thus an increase in the allocation of time to activities other than foraging. Alternatively, because energy is limited for animals, the energy saved by huddling may be allocated to other biological functions or activities, while acting as a selective pressure important for life in groups in rodents (Gilbert et al, 2012;Ebensperger and Wallen, 2002;Schradin et al, 2006). For example, in O. degus, some activities associated with foraging may be energetically costly, such as digging in dry areas with low humidity (Ebensperger and Bozinovic, 2000), exploration behavior in open spaces at low temperatures after foraging, and building burrows (Torres-Contreras and Bozinovic, 1997; Quispe et al, 2009).…”

“…Recently, Gilbert et al (Gilbert et al, 2012) documented that local heating is crucial in reducing the extent of the cold challenge in huddling rabbit pups. Through thermal images, they demonstrated that at 14°C, the mean surface temperature of the huddle was higher than the mean temperature of isolated pups.…”

“…Thus, decreasing thermogenic response by means of huddling may lead to a decrease in food needs and thus an increase in the allocation of time to activities other than foraging. Alternatively, because energy is limited for animals, the energy saved by huddling may be allocated to other biological functions or activities, while acting as a selective pressure important for life in groups in rodents (Gilbert et al, 2012; Ebensperger and Wallen, 2002;Schradin et al, 2006 In this way, individuals can regulate the levels of energy expenditure to maintain their functional capabilities in variable thermal environments through plastic and adaptive changes in metabolic rate, and reassign the energy saved to other activities (Nespolo, 2000). However, Bozinovic et al (Bozinovic et al, 2004) reported that the BMR in O. degus in the wild is not altered by seasonality in a Mediterranean environment of central Chile.…”

Diurnality as an energy-saving strategy: energetic consequences of temporal niche switching in small mammals

“…Restassociated energy-saving strategies, such as huddling and nest insulation, reduce thermal conductance, thereby decreasing energy expenditure at T a below T LC ( Fig. 1) (Gilbert et al, 2012). During the active phase, energy expenditure is elevated.…”