Huddling behavior as critical phase transition triggered by low temperatures

Huddling is a grouping behavior where animals maintain close bodily contact and save energy. We tested the hypothesis that this thermoregulatory behavior behaves as a system with continuous (second-order phase) transition called critical when the environmental temperature (driving parameter) is near a critical value. To do so, we followed theoretical and experimental approaches, examining data from geometrical models, metabolic rate during huddling in small mammals, and also conducting an experiment on thermoregulatory huddling behavior with white mice. Our results support all predictions for systems under continuous-phase transition triggered by low temperatures, a phenomenon reported for first time in a biological system. We suggest that huddling behavior in social animals, a recognized adaptive behavior, may be considered a self-organized system coupled with an external driving parameter. © 2011 Wiley Periodicals, Inc. Complexity, 2011 © 2011 Wiley Periodicals, Inc.

[1]  J. Emlen,et al.  Fractal structure of sequential behaviour patterns: an indicator of stress , 1996, Animal Behaviour.

[2]  F. Bozinovic,et al.  Comparative energetics of South American cricetid rodents. , 1988, Comparative biochemistry and physiology. A, Comparative physiology.

[3]  F. Bozinovic,et al.  Patch use in a diurnal rodent: handling and searching under thermoregulatory costs , 1999 .

[4]  L. MauricioCanals,et al.  Geometría de los sistemas vivos y su importancia en Medicina , 2005 .

[5]  J. Deneubourg,et al.  The self-organizing exploratory pattern of the argentine ant , 1990, Journal of Insect Behavior.

[6]  Michael A. Huffman,et al.  Fractal Long‐Range Correlations in Behavioural Sequences of Wild Chimpanzees: a Non‐Invasive Analytical Tool for the Evaluation of Health , 2000 .

[7]  G. Lynch,et al.  Influence of Ambient Temperature, Nest Availability, Huddling, and Daily Torpor on Energy Expenditure in the White-Footed Mouse Peromyscus Leucopus , 1982, Physiological Zoology.

[8]  F. Bozinovic,et al.  Time and energy use under thermoregulatory constraints in a diurnal rodent , 2000 .

[9]  J R Alberts,et al.  Huddling by rat pups: multisensory control of contact behavior. , 1978, Journal of comparative and physiological psychology.

[10]  M. Kleiber.  The fire of life , 1961 .

[11]  A. Gębczyński.  Daily variation of thermoregulatory costs in laboratory mice selected for high and low basal metabolic rate , 2005 .

[12]  D. Makihara,et al.  Metabolic and thermoregulatory consequences of social behaviors between Microtus townsendii. , 1987, Comparative biochemistry and physiology. A, Comparative physiology.

[13]  R. Belknap,et al.  Bioenergetic benefits of huddling by deer mice (Peromyscus maniculatus). , 1986, Comparative biochemistry and physiology. A, Comparative physiology.

[14]  Y. Handrich,et al.  Energy saving in huddling penguins , 1997, Nature.

[15]  F. Bozinovic,et al.  Energetics and geometry of huddling in small mammals. , 1989, Journal of theoretical biology.

[16]  Robert A. Martin,et al.  Social facilitation of reduced oxygen consumption in Mus musculus and Meriones unguiculatus , 1980 .

[17]  John A. Sealander,et al.  The Relationship of Nest Protection and Huddling to Survival of Peromyscus at Low Temperature , 1952 .

[18]  C. B. Lynch,et al.  Effects of temperature and social interactions on huddling behavior in Mus musculus , 1983, Physiology & Behavior.

[19]  D. H. Wood.  Temperature adaptation in the freshwater snail, helisoma trivolvis (say), in an artificially heated reservoir in the southeastern United States , 1978 .

[20]  M. Gębczyński.  Social regulation of body temperature in the bank vole , 1969 .

[21]  Stuart A. Kauffman,et al.  The origins of order , 1993 .

[22]  Benton,et al.  Criticality and scaling in evolutionary ecology. , 1997, Trends in ecology & evolution.

[23]  Francisco Bozinovic,et al.  The influence of habitat on travel speed, intermittent locomotion, and vigilance in a diurnal rodent , 2002 .

[24]  S. Kauffman,et al.  Antichaos and adaptation. , 1991, Scientific American.

[25]  J. Deneubourg,et al.  Kinetics of larval gregarious behavior in the bark beetleDendroctonus micans (Coleoptera: Scolytidae) , 1990, Journal of Insect Behavior.

[26]  B. Wojciechowska,et al.  The effect of huddling on the resting metabolism rate of the European common vole Microtus arvalis (Pall). , 1968, Bulletin de l'Academie polonaise des sciences. Serie des sciences biologiques.

[27]  B. Weber.  Origins of Order in Dynamical Models , 1997 .

[28]  Y. Naito,et al.  Huddling behavior in emperor penguins: Dynamics of huddling , 2006, Physiology & Behavior.

[29]  Jean Paul Rigaut,et al.  An empirical formulation relating boundary lengths to resolution in specimens showing ‘non‐ideally fractal’ dimensions , 1984 .

[30]  Jean-Louis Deneubourg,et al.  Self-organizing spatial patterns in the Argentine ant: Iridomyrmex humilis (Mayr) , 1990 .

[31]  B. Weber.  Origins of Order in Dynamical Models. A review of Stuart A. Kauffman, The Origins of Order: Self Organization and Selection in Evolution. , 1998 .

[32]  F. T. Jung.  The Fire of Life , 1962 .

[33]  Yoshiyuki Kawazoe,et al.  A temporal model of animal behavior based on a fractality in the feeding of Drosophila melanogaster , 1993, Biological Cybernetics.

[34]  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.

[35]  R. Tertil.  The effect of behavioural thermoregulation on the daily metabolism of Apodemus agrarius (Pallas, 1771) , 1972 .

[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]  T. Gisiger.  Scale invariance in biology: coincidence or footprint of a universal mechanism? , 2001, Biological reviews of the Cambridge Philosophical Society.

[38]  F. Bozinovic,et al.  Geometrical aspects of the energetic effectivenes of huddling in small mammals , 1997 .

[39]  David A. Winkler,et al.  Critical-like self-organization and natural selection: Two facets of a single evolutionary process? , 2008, Biosyst..

[40]  Anna Fedyk,et al.  Social thermoregulation in Apodemus flavicollis (Melchior, 1834) , 1971 .

[41]  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.

[42]  J. Millar,et al.  The energetics of huddling by endotherms , 1984 .

[43]  Guy Theraulaz,et al.  Self-Organization in Biological Systems , 2001, Princeton studies in complexity.

[44]  G. Barrett,et al.  Importance of Social Grouping on Bioenergetics of the Golden Mouse, Ochrotomys nuttalli , 1981 .

[45]  L. C. Contreras.  Bioenergetics of huddling: test of a psycho-physiological hypothesis , 1984 .

[46]  J. Escós,et al.  Complexity of behavioural sequences and their relation to stress conditions in chickens (Gallus gallus domesticus): a non-invasive technique to evaluate animal welfare , 2004 .

[47]  C. Herreid,et al.  Thermal conductance in birds and mammals. , 1967, Comparative biochemistry and physiology.

[48]  Y. le Maho,et al.  Energy saving processes in huddling emperor penguins: from experiments to theory , 2008, Journal of Experimental Biology.

[49]  J. S,et al.  Self-Organized Huddles of Rat Pups Modeled by Simple Rules of Individual Behavior , 1997 .

[50]  Mauricio Canals,et al.  Modulating factors of the energetic effectiveness of huddling in small mammals , 1998 .