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Oecologia

, Volume 180, Issue 2, pp 371–381 | Cite as

Social huddling and physiological thermoregulation are related to melanism in the nocturnal barn owl

  • Amélie N. DreissEmail author
  • Robin Séchaud
  • Paul Béziers
  • Nicolas Villain
  • Michel Genoud
  • Bettina Almasi
  • Lukas Jenni
  • Alexandre Roulin
Behavioral ecology - Original research

Abstract

Endothermic animals vary in their physiological ability to maintain a constant body temperature. Since melanin-based coloration is related to thermoregulation and energy homeostasis, we predict that dark and pale melanic individuals adopt different behaviours to regulate their body temperature. Young animals are particularly sensitive to a decrease in ambient temperature because their physiological system is not yet mature and growth may be traded-off against thermoregulation. To reduce energy loss, offspring huddle during periods of cold weather. We investigated in nestling barn owls (Tyto alba) whether body temperature, oxygen consumption and huddling were associated with melanin-based coloration. Isolated owlets displaying more black feather spots had a lower body temperature and consumed more oxygen than those with fewer black spots. This suggests that highly melanic individuals display a different thermoregulation strategy. This interpretation is also supported by the finding that, at relatively low ambient temperature, owlets displaying more black spots huddled more rapidly and more often than those displaying fewer spots. Assuming that spot number is associated with the ability to thermoregulate not only in Swiss barn owls but also in other Tytonidae, our results could explain geographic variation in the degree of melanism. Indeed, in the northern hemisphere, barn owls and allies are less spotted polewards than close to the equator, and in the northern American continent, barn owls are also less spotted in colder regions. If melanic spots themselves helped thermoregulation, we would have expected the opposite results. We therefore suggest that some melanogenic genes pleiotropically regulate thermoregulatory processes.

Keywords

Huddling Melanin Metabolic rate Oxygen consumption Pleiotropy Temperature Thermoregulation 

Notes

Acknowledgments

We thank Cécile A. Dreiss, Anne-Lyse Ducrest and two anonymous referees for their constructive comments.

Author contribution statement

PB conducted the field and laboratory work on body temperature, a project designed by BA, LJ and AR. RS, PB & MG designed the oxygen consumption experiment and RS conducted this experiment and analysed the data. NV analysed the social thermoregulation videos, a project designed by AD. AD and AR supervised the project and wrote the manuscript.

References

  1. Almasi B, Roulin A (2015) Signalling value of maternal and paternal melanism in the barn owl: implication for the resolution of the lek paradox. Biol J Linn Soc 115:376–390. doi: 10.1111/bij.12508 CrossRefGoogle Scholar
  2. Almasi B, Roulin A, Jenni L (2013) Corticosterone shifts reproductive behaviour towards self-maintenance in the barn owl and is linked to melanin-based coloration in females. Horm Behav 64:161–171. doi: 10.1016/j.yhbeh.2013.03.001 CrossRefPubMedGoogle Scholar
  3. Ancel A, Visser H, Handrich Y, Masman D, LeMaho Y (1997) Energy saving in huddling penguins. Nature 385:304–305. doi: 10.1038/385304a0 CrossRefGoogle Scholar
  4. Ancillotto L, Serangeli MT, Russo D (2012) Spatial proximity between newborns influences the development of social relationships in bats. Ethology 118:331–340. doi: 10.1111/j.1439-0310.2011.02016.x CrossRefGoogle Scholar
  5. Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268. doi: 10.1016/s0306-4565(01)00094-8 CrossRefGoogle Scholar
  6. Angilletta MJ, Cooper BS, Schuler MS, Boyles JG (2010) The evolution of thermal physiology in endotherms. Front Biosci E2:861–881CrossRefGoogle Scholar
  7. Burness G, Armstrong C, Fee T, Tilman-Schindel E (2010) Is there an energetic-based trade-off between thermoregulation and the acute phase response in zebra finches? J Exp Biol 213:1386–1394. doi: 10.1242/jeb.027011 CrossRefPubMedGoogle Scholar
  8. Caro T (2013) The colours of extant mammals. Semin Cell Dev Biol 24:542–552. doi: 10.1016/j.semcdb.2013.03.016 CrossRefPubMedGoogle Scholar
  9. Challis BG et al (2004) Mice lacking pro-opiomelanocortin are sensitive to high-fat feeding but respond normally to the acute anorectic effects of peptide-YY3-36. Proc Natl Acad Sci USA 101:4695–4700. doi: 10.1073/pnas.0306931 PubMedCentralCrossRefPubMedGoogle Scholar
  10. Clusella-Trullas S, Terblanche JS, Blackburn TM, Chown SL (2008) Testing the thermal melanism hypothesis: a macrophysiological approach. Funct Ecol 22:232–238. doi: 10.1111/j.1365-2435.2007.01377.x CrossRefGoogle Scholar
  11. Crompton AW, Taylor CR, Jagger JA (1978) Evolution of homeothermy in mammals. Nature 272:333–336. doi: 10.1038/272333a0 CrossRefPubMedGoogle Scholar
  12. Dawson RD, Lawrie CC, O’Brien EL (2005) The importance of microclimate variation in determining size, growth and survival of avian offspring: experimental evidence from a cavity nesting passerine. Oecologia 144:499–507. doi: 10.1007/s00442-005-0075-7 CrossRefPubMedGoogle Scholar
  13. Dikmen S, Cole JB, Null DJ, Hansen PJ (2012) Heritability of rectal temperature and genetic correlations with production and reproduction traits in dairy cattle. J Dairy Sci 95:3401–3405. doi: 10.3168/jds.2011-4306 CrossRefPubMedGoogle Scholar
  14. Dreiss AN, Roulin A (2010) Age-related change in melanin-based coloration of Barn owls (Tyto alba): females that become more female-like and males that become more male-like perform better. Biol J Linn Soc 101:689–704. doi: 10.1111/j.1095-8312.2010.01503.x CrossRefGoogle Scholar
  15. Dreiss AN, Henry I, Ruppli CA, Almasi B, Roulin A (2010) Darker eumelanic barn owls better withstand food depletion through resistance to food deprivation and lower appetite. Oecologia 164:65–71. doi: 10.1007/s00442-010-1680-7 CrossRefPubMedGoogle Scholar
  16. Dreiss AN et al (2012) Local adaptation and matching habitat choice in female barn owls with respect to melanic coloration. J Evol Biol 25:103–114. doi: 10.1111/j.1420-9101.2011.02407.x CrossRefPubMedGoogle Scholar
  17. Dreiss AN, Ruppli CA, Oberli F, Antoniazza S, Henry I, Roulin A (2013) Barn owls do not interrupt their siblings. Anim Behav 86:119–126. doi: 10.1016/j.anbehav.2013.04.019 CrossRefGoogle Scholar
  18. Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510. doi: 10.1016/j.tree.2008.06.001 CrossRefPubMedGoogle Scholar
  19. Dunn EH (1975) Timing of endothermy in development of altricial birds. Condor 77:288–293. doi: 10.2307/1366224 CrossRefGoogle Scholar
  20. Duplessis MA, Weathers WW, Koenig WD (1994) Energetic benefits of communal roosting by acorn woodpeckers during the nonbreeding season. Condor 96:631–637. doi: 10.2307/1369466 CrossRefGoogle Scholar
  21. Durant JM (2002) The influence of hatching order on the thermoregulatory behaviour of barn owl Tyto alba nestlings. Avian Sci 2:167–173Google Scholar
  22. Edwards TC (1987) Standard rate of metabolism in the common barn owl (Tyto alba). Wilson Bull 99:704–706Google Scholar
  23. Else PL, Hulbert AJ (1981) Comparison of the mammal machine and the reptile machine—energy production. Am J Physiol 240:R3–R9PubMedGoogle Scholar
  24. Forbes S (2002) Sibling symbiosis in nestling birds. Auk 124:1–10. doi:10.1642/0004-8038(2007)124[1:SSINB]2.0.CO;2Google Scholar
  25. Galeotti P, Rubolini D, Sacchi R, Fasola M (2009) Global changes and animal phenotypic responses: melanin-based plumage redness of scops owls increased with temperature and rainfall during the last century. Biol Lett 5:532–534. doi: 10.1098/rsbl.2009.0207 PubMedCentralCrossRefPubMedGoogle Scholar
  26. Gilbert C et al (2010) One for all and all for one: the energetic benefits of huddling in endotherms. Biol Rev 85:545–569. doi: 10.1111/j.1469-185X.2009.00115.x PubMedGoogle Scholar
  27. Hegna RH, Nokelainen O, Hegna JR, Mappes J (2013) To quiver or to shiver: increased melanization benefits thermoregulation, but reduces warning signal efficacy in the wood tiger moth. Proc R Soc Lond B. doi: 10.1098/rspb.2012.2812 Google Scholar
  28. Heppner F (1970) The metabolic significance of differential absorption of radiant energy by black and white birds. Condor 72:50–59CrossRefGoogle Scholar
  29. Hetem RS et al (2009) Body temperature, thermoregulatory behaviour and pelt characteristics of three colour morphs of springbok (Antidorcas marsupialis). Comp Biochem Physiol A 152:379–388. doi: 10.1016/j.cbpa.2008.11.011 CrossRefGoogle Scholar
  30. Hudson R, Bautista A, Reyes-Meza V, Montor JM, Rodel HG (2011) The effect of siblings on early development: a potential contributor to personality differences in mammals. Dev Psychobiol 53:564–574. doi: 10.1002/dev.20535 CrossRefPubMedGoogle Scholar
  31. Irving L, Krog J (1954) Body temperatures of arctic and subarctic birds and mammals. J Appl Physiol 6:667–680PubMedGoogle Scholar
  32. Järvistö PE, Calhim S, Schuett W, Velmala W, Laaksonen T (2015) Foster, but not genetic, father plumage coloration has a temperature-dependent effect on offspring quality. Behav Ecol Sociobiol 69:335–346. doi: 10.1007/s00265-014-1846-0 CrossRefGoogle Scholar
  33. Jones KMM, Boulding EG (1999) State-dependent habitat selection by an intertidal snail: the costs of selecting a physically stressful microhabitat. J Exp Mar Biol Ecol 242:149–177. doi: 10.1016/S0022-0981(99)00090-8 CrossRefGoogle Scholar
  34. Karell P, Ahola K, Karstinen T, Valkama J, Brommer JE (2011) Climate change drives microevolution in a wild bird. Nat Commun 2:208. doi: 10.1038/ncomms1213 PubMedCentralCrossRefPubMedGoogle Scholar
  35. Karpestam E, Wennersten L, Forsman A (2012) Matching habitat choice by experimentally mismatched phenotypes. Evol Ecol 26:893–907. doi: 10.1007/s10682-011-9530-6 CrossRefGoogle Scholar
  36. Kearney M, Shine R, Porter WP (2009) The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proc Natl Acad Sci USA 106:3835–3840. doi: 10.1073/pnas.0808913106 PubMedCentralCrossRefPubMedGoogle Scholar
  37. Kittilsen S et al (2009) Melanin-based skin spots reflect stress responsiveness in salmonid fish. Horm Behav 56:292–298. doi: 10.1016/j.yhbeh.2009.06.006 CrossRefPubMedGoogle Scholar
  38. Koskenpato K, Ahola K, Karstinen T, Karell P (2015) Is the denser contour feather structure in pale grey than in pheomelanic brown tawny owls (Strix aluco) an adaptation to cold environments? J Avian Biol. doi: 10.1111/jav.00746 Google Scholar
  39. Lichtenbelt WDV, Westerterp-Plantenga MS, van Hoydonck P (2001) Individual variation in the relation between body temperature and energy expenditure in response to elevated ambient temperature. Physiol Behav 73:235–242CrossRefGoogle Scholar
  40. Lichtenbelt WDV, Schrauwen P, Van De Kerckhove SV, Westerterp-Plantenga MS (2002) Individual variation in body temperature and energy expenditure in response to mild cold. Am J Physiol Endocrinol Metab 282:E1077–E1083. doi: 10.1152/ajpendo.00020.2001 CrossRefGoogle Scholar
  41. Lute B et al (2014) Biphasic effect of melanocortin agonists on metabolic rate and body temperature. Cell Metab 20:333–345. doi: 10.1016/j.cmet.2014.05.021 PubMedCentralCrossRefPubMedGoogle Scholar
  42. McKechnie AE, Lovegrove BG (2001) Thermoregulation and the energetic significance of clustering behavior in the white-backed mousebird (Colius colius). Physiol Biochem Zool 74:238–249. doi: 10.1086/319669 CrossRefPubMedGoogle Scholar
  43. McNab BK (1997) On the utility of uniformity in the definition of basal rate of metabolism. Physiol Zool 70:718–720CrossRefPubMedGoogle Scholar
  44. Mosher JA, Henny CJ (1976) Thermal adaptiveness of plumage color in screech owls. Auk 93:614–619Google Scholar
  45. Muri D et al (2015) Thermoregulation and microhabitat choice in the polymorphic asp viper (Vipera aspis). J Therm Biol 53:107–112. doi: 10.1016/j.jtherbio.2015.06.009 CrossRefPubMedGoogle Scholar
  46. Nespolo RF, Bacigalupe LD, Bozinovic F (2003) Heritability of energetics in a wild mammal, the leaf-eared mouse (Phyllotis darwini). Evolution 57:1679–1688CrossRefPubMedGoogle Scholar
  47. Olson JM (1992) Growth, the development of endothermy, and the allocation of energy in red-winged blackbirds (Agelaius phoeniceus) during the nestling period. Physiol Zool 65:124–152CrossRefGoogle Scholar
  48. Parkash R, Sharma V, Kalra B (2010) Correlated changes in thermotolerance traits and body color phenotypes in montane populations of Drosophila melanogaster: analysis of within- and between-population variations. J Zool 280:49–59. doi: 10.1111/j.1469-7998.2009.00641.x CrossRefGoogle Scholar
  49. Py I, Ducrest AL, Duvoisin N, Fumagalli L, Roulin A (2006) Ultraviolet reflectance in a melanin-based plumage trait is heritable. Evol Ecol Res 8:483–491Google Scholar
  50. Reyes-Meza V, Hudson R, Martinez-Gomez M, Nicolas L, Rodel HG, Bautista A (2011) Possible contribution of position in the litter huddle to long-term differences in behavioral style in the domestic rabbit. Physiol Behav 104:778–785. doi: 10.1016/j.physbeh.2011.07.019 CrossRefPubMedGoogle Scholar
  51. Roulin A (2004a) Effects of hatching asynchrony on sibling negotiation, begging, jostling for position and within-brood food allocation in the barn owl, Tyto alba. Evol Ecol Res 6:1083–1098Google Scholar
  52. Roulin A (2004b) Proximate basis of the covariation between a melanin-based female ornament and offspring quality. Oecologia 140:668–675. doi: 10.1007/s00442-004-1636-x CrossRefPubMedGoogle Scholar
  53. Roulin A, Ducrest AL (2011) Association between melanism, physiology and behaviour: a role for the melanocortin system. Eur J Pharmacol 660:226–233CrossRefPubMedGoogle Scholar
  54. Roulin A, Jensen H (2015) Sex-linked inheritance, genetic correlations and sexual dimorphism in three melanin-based color traits in the barn owl. J Evol Biol 28:655–666. doi: 10.1111/jeb.12596 CrossRefPubMedGoogle Scholar
  55. Roulin A, Randin C (2015) Gloger’s rule in North American barn owls. Auk 132:321–332. doi: 10.1642/AUK-14-167.1 CrossRefGoogle Scholar
  56. Roulin A, Kolliker M, Richner H (2000) Barn owl (Tyto alba) siblings vocally negotiate resources. Proc R Soc Lond B 267:459–463. doi: 10.1098/rspb.2000.1022 CrossRefGoogle Scholar
  57. Roulin A, Bize P, Tzaud N, Bianchi M, Ravussin P-A, Christe P (2005) Oxygen consumption in offspring tawny owls Strix aluco is associated with colour morph of foster mother. J Ornithol 146:390–394. doi: 10.1007/s10336-005-0096-3 CrossRefGoogle Scholar
  58. Roulin A et al (2008) Corticosterone mediates the condition-dependent component of melanin-based coloration. Anim Behav 75:1351–1358. doi: 10.1016/j.anbehav.2007.09.007 CrossRefGoogle Scholar
  59. Roulin A, Wink M, Salamin N (2009) Selection on a eumelanic ornament is stronger in the tropics than in temperate zones in the worldwide-distributed barn owl. J Evol Biol 22:345–354. doi: 10.1111/j.1420-9101.2008.01651.x CrossRefPubMedGoogle Scholar
  60. Roulin A, Altwegg R, Jensen H, Steinsland I, Schaub M (2010) Sex-dependent selection on an autosomal melanic female ornament promotes the evolution of sex ratio bias. Ecol Lett 13:616–626. doi: 10.1111/j.1461-0248.2010.01459.x CrossRefPubMedGoogle Scholar
  61. Roulin A, Da Silva A, Ruppli CA (2012) Dominant nestlings displaying female-like melanin coloration behave altruistically in the barn owl. Anim Behav 84:1229–1236. doi: 10.1016/j.anbehav.2012.08.033 CrossRefGoogle Scholar
  62. Roulin A, Mangels J, Wakamatsu K, Bachmann T (2013) Sexually dimorphic melanin-based colour polymorphism, feather melanin content, and wing feather structure in the barn owl (Tyto alba). Biol J Linn Soc 109:562–573. doi: 10.1111/bij.12078 CrossRefGoogle Scholar
  63. Scantlebury M, Bennett NC, Speakman JR, Pillay N, Schradin C (2006) Huddling in groups leads to daily energy savings in free-living African four-striped grass mice, Rhabdomys pumilio. Funct Ecol 20:166–173. doi: 10.1111/j.1365-2435.2006.01074.x CrossRefGoogle Scholar
  64. Schmidt-Nielsen K (1997) Animal physiology. Adaptation and environment, 5th edn. Cambridge University Press, CambridgeGoogle Scholar
  65. Sinha PS, Schioth HB, Tatro JB (2004) Roles of the melanocortin-4 receptor in antipyretic and hyperthermic actions of centrally administered alpha-MSH. Brain Res 1001:150–158. doi: 10.1016/j.brainres.2003.12.007 CrossRefPubMedGoogle Scholar
  66. Sirkiä PM, Virolainen M, Laaksonen T (2010) Melanin coloration has temperature-dependent effects on breeding performance that may maintain phenotypic variation in a passerine bird. J Evol Biol 23:2385–2396. doi: 10.1111/j.1420-9101.2010.02100.x CrossRefPubMedGoogle Scholar
  67. Sirkiä PM, Virolainen M, Lehikoinen M, Laaksonen T (2013) Fluctuating selection and immigration as determinants of the phenotypic composition of a population. Oecologia 173:305–317. doi: 10.1007/s00442-013-2593-z CrossRefPubMedGoogle Scholar
  68. Tanaka K (2007) Thermal biology of a colour-dimorphic snake, Elaphe quadrivirgata, in a montane forest: do melanistic snakes enjoy thermal advantages? Biol J Linn Soc 92:309–322. doi: 10.1111/j.1095-8312.2007.00849.x CrossRefGoogle Scholar
  69. Thouzeau C, Duchamp C, Handrich Y (1999) Energy metabolism and body temperature of barn owls fasting in the cold. Physiol Biochem Zool 72:170–178. doi: 10.1086/316659 CrossRefPubMedGoogle Scholar
  70. Walsberg GE (1991) Thermal effects of seasonal coat change in 3 sub-arctic mammals. J Therm Biol 16:291–296. doi: 10.1016/0306-4565(91)90020-3 CrossRefGoogle Scholar
  71. Walsberg GE, Campbell GS, King JR (1978) Animal coat color and radiative heat gain: re-evaluation. J Comp Physiol 126:211–222CrossRefGoogle Scholar
  72. Willis CKR, Brigham RM (2007) Social thermoregulation exerts more influence than microclimate on forest roost preferences by a cavity-dwelling bat. Behav Ecol Sociobiol 62:97–108. doi: 10.1007/s00265-007-0442-y CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Amélie N. Dreiss
    • 1
    • 2
    Email author
  • Robin Séchaud
    • 1
  • Paul Béziers
    • 1
  • Nicolas Villain
    • 1
    • 3
  • Michel Genoud
    • 1
  • Bettina Almasi
    • 4
  • Lukas Jenni
    • 4
  • Alexandre Roulin
    • 1
  1. 1.Department of Ecology and EvolutionUniversity of LausanneLausanneSwitzerland
  2. 2.Institute of Ecology and EvolutionUniversity of BernBernSwitzerland
  3. 3.UMR 7179 CNRS, Museum National d’Histoire NaturelleBrunoyFrance
  4. 4.Swiss Ornithological InstituteSempachSwitzerland

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