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

Background Within 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 Findings The 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/Significance By 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.

[1]  M. Blumberg,et al.  Thermogenesis, myoclonic twitching, and ultrasonic vocalization in neonatal rats during moderate and extreme cold exposure. , 1996, Behavioral neuroscience.

[2]  R. Hudson,et al.  The Pattern of Behaviour of Rabbit Pups in the Nest , 1982 .

[3]  Heiko G. Rödel,et al.  Possible contribution of position in the litter huddle to long-term differences in behavioral style in the domestic rabbit , 2011, Physiology & Behavior.

[4]  J. Stevenson The evolution of sibling rivalry , 2000 .

[5]  H. Drummond,et al.  Thermal benefit of sibling presence in the newborn rabbit. , 2003, Developmental psychobiology.

[6]  Heiko G. Rödel,et al.  The effect of siblings on early development: a potential contributor to personality differences in mammals. , 2011, Developmental psychobiology.

[7]  Heiko G. Rödel,et al.  Why do heavy littermates grow better than lighter ones? A study in wild and domestic European rabbits , 2008, Physiology & Behavior.

[8]  Hanlon Fong,et al.  Animal Physiology: Adaptation and Environment , 1975, The Yale Journal of Biology and Medicine.

[9]  Heiko G. Rödel,et al.  Separating maternal and litter-size effects on early postnatal growth in two species of altricial small mammals , 2008, Physiology & Behavior.

[10]  Heiko G. Rödel,et al.  Optimal litter size for individual growth of European rabbit pups depends on their thermal environment , 2008, Oecologia.

[11]  T. Heim,et al.  The blood flow and oxygen consumption of brown adipose tissue in the new‐born rabbit , 1966, The Journal of physiology.

[12]  D. Nicholls,et al.  Thermogenic mechanisms in brown fat. , 1984, Physiological reviews.

[13]  D. Hull,et al.  The contribution of brown adipose tissue to heat production in the new‐born rabbit. , 1965, The Journal of physiology.

[14]  D. M. Jacksona,et al.  Can non-shivering thermogenesis in brown adipose tissue following NA injection be quantified by changes in overlying surface temperatures using infrared thermography ? , 2001 .

[15]  Robert N. Brandon,et al.  Adaptation and Environment , 1995 .

[16]  A. Bautista,et al.  Differential development of body equilibrium among littermates in the newborn rabbit. , 2009, Developmental psychobiology.

[17]  James Park Animal Physiology: Adaptation and Environment, Fifth Edition , 2001, The Yale Journal of Biology and Medicine.

[18]  K. Schmidt-Nielsen,et al.  Animal physiology: Adaptation and environment, 2nd edition , 1979 .

[19]  J R Alberts,et al.  Thermogenesis during ultrasonic vocalization by rat pups isolated in a warm environment: a thermographic analysis. , 1992, Developmental psychobiology.

[20]  Y. le Maho,et al.  One for all and all for one: the energetic benefits of huddling in endotherms , 2009, Biological reviews of the Cambridge Philosophical Society.

[21]  M. Blumberg,et al.  A comparative analysis of huddling in infant Norway rats and Syrian golden hamsters: does endothermy modulate behavior? , 2000, Behavioral neuroscience.

[22]  F. Trillmich,et al.  Sibling competition and cooperation in mammals: challenges, developments and prospects , 2007, Behavioral Ecology and Sociobiology.

[23]  L. Janský NON‐SHIVERING THERMOGENESIS AND ITS THERMOREGULATORY SIGNIFICANCE , 1973, Biological reviews of the Cambridge Philosophical Society.

[24]  M. Stanier Effect of body weight, ambient temperature and huddling on oxygen consumption and body temperature of young mice. , 1975, Comparative biochemistry and physiology. A, Comparative physiology.

[25]  Heiko G. Rödel,et al.  Features of the early juvenile development predict competitive performance in male European rabbits , 2009, Physiology & Behavior.

[26]  M. Blumberg,et al.  Competition and cooperation among huddling infant rats. , 2001, Developmental psychobiology.

[27]  D. Hull,et al.  THE EFFECT OF THE ENVIRONMENTAL TEMPERATURE ON THE GROWTH OF NEW-BORN RABBITS REARED IN INCUBATORS. , 1964, Biologia neonatorum. Neo-natal studies.

[28]  A. Bautista,et al.  Scramble competition in newborn domestic rabbits for an unusually restricted milk supply , 2005, Animal Behaviour.

[29]  J E Heath,et al.  Comparison of IR thermography and thermocouple measurement of heat loss from rabbit pinna. , 1988, The American journal of physiology.

[30]  D. Haig Huddling: Brown Fat, Genomic Imprinting and the Warm Inner Glow , 2008, Current Biology.

[31]  D. McCafferty The value of infrared thermography for research on mammals: previous applications and future directions , 2007 .

[32]  A. Bautista,et al.  Do newborn domestic rabbits Oryctolagus cuniculus compete for thermally advantageous positions in the litter huddle? , 2007, Behavioral Ecology and Sociobiology.

[33]  Y. le Maho,et al.  Role of huddling on the energetic of growth in a newborn altricial mammal. , 2007, American journal of physiology. Regulatory, integrative and comparative physiology.

[34]  B. Cannon,et al.  Brown adipose tissue thermogenesis in neonatal and cold-adapted animals. , 1986, Biochemical Society transactions.

[35]  P. Orgeur,et al.  Immediate postnatal sucking in the rabbit: its influence on pup survival and growth. , 2000, Reproduction, nutrition, development.

[36]  J. Speakman,et al.  The Contributions of Local Heating and Reducing Exposed Surface Area to the Energetic Benefits of Huddling by Short-Tailed Field Voles (Microtus agrestis) , 1992, Physiological Zoology.

[37]  J. Alberts,et al.  Huddling by rat pups: group behavioral mechanisms of temperature regulation and energy conservation. , 1978, Journal of comparative and physiological psychology.

[38]  H. T. Hammel Thermal properties of fur. , 1955, The American journal of physiology.

[39]  M. Blumberg,et al.  Thermoregulatory behavior in infant Norway rats (Rattus norvegicus) and Syrian golden hamsters (Mesocricetus auratus): arousal, orientation, and locomotion. , 2002, Journal of comparative psychology.

[40]  D. Hull,et al.  Brown adipose tissue and the response of new‐born rabbits to cold , 1964, The Journal of physiology.

[41]  Heiko G. Rödel,et al.  Development of behavior in the litter huddle in rat pups: within- and between-litter differences. , 2009, Developmental psychobiology.

[42]  M. Blumberg,et al.  Thermoregulatory competence and behavioral expression in the young of altricial species--revisited. , 1998, Developmental psychobiology.

[43]  M. Blumberg,et al.  Contributions of endothermy to huddling behavior in infant Norway rats (Rattus norvegicus) and Syrian golden hamsters (Mesocricetus auratus). , 2002, Journal of comparative psychology.

[44]  B. Jilge,et al.  Circadian Thermoregulation in Suckling Rabbit Pups , 2000, Journal of biological rhythms.

[45]  Hugh Drummond,et al.  Competition for Milk in the Domestic Rabbit: Survivors Benefit from Littermate Deaths , 2000 .

[46]  J. B. Weir New methods for calculating metabolic rate with special reference to protein metabolism , 1949, The Journal of physiology.

[47]  B. Cannon,et al.  Life without UCP1: mitochondrial, cellular and organismal characteristics of the UCP1-ablated mice. , 2001, Biochemical Society transactions.

[48]  W. Paterson,et al.  Estimating metabolic heat loss in birds and mammals by combining infrared thermography with biophysical modelling. , 2011, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[49]  V. Denenberg,et al.  Rabbit: Frequency of Suckling in the Pup , 1965, Science.

[50]  Gustav Fischer Verlag,et al.  INFRARED THERMOGRAPHY : PRINCIPLES AND APPLICATIONS , 1998 .

[51]  D. Lincoln Suckling: a time-constant in the nursing behaviour of the rabbit. , 1974, Physiology & behavior.

[52]  C. R. White,et al.  Mammalian basal metabolic rate is proportional to body mass2/3 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Jan Nedergaard,et al.  Brown adipose tissue: function and physiological significance. , 2004, Physiological reviews.

[54]  S. Rest,et al.  Circadian temperature rhythms in rabbit pups and in their does , 2001, Laboratory animals.

[55]  T Araki,et al.  Thermographic demonstration of nonshivering thermogenesis in human newborns after birth: its relation to umbilical gases , 1997, Journal of perinatal medicine.