Journal of Comparative Physiology B

, Volume 183, Issue 7, pp 969–982 | Cite as

Thermoregulation in African Green Pigeons (Treron calvus) and a re-analysis of insular effects on basal metabolic rate and heterothermy in columbid birds

  • Matthew J. Noakes
  • Ben Smit
  • Blair O. Wolf
  • Andrew E. McKechnie
Original Paper
First Online:
Received:
Revised:
Accepted:

Abstract

Columbid birds represent a useful model taxon for examining adaptation in metabolic and thermal traits, including the effects of insularity. To test predictions concerning the role of insularity and low predation risk as factors selecting for the use of torpor, and the evolution of low basal metabolic rate in island species, we examined thermoregulation under laboratory and semi-natural conditions in a mainland species, the African Green Pigeon (Treron calvus). Under laboratory conditions, rest-phase body temperature (T b) was significantly and positively correlated with air temperature (T a) between 0 and 35 °C, and the relationship between resting metabolic rate (RMR) and T a differed from typical endothermic patterns. The minimum RMR, which we interpret as basal metabolic rate (BMR), was 0.825 ± 0.090 W. Green pigeons responded to food restriction by significantly decreasing rest-phase T b, but the reductions were small (at most ~5 °C below normothermic values), with a minimum T b of 33.1 °C recorded in a food-deprived bird. We found no evidence of the large reductions in T b and metabolic rate and the lethargic state characteristic of torpor. The absence of torpor in T. calvus lends support to the idea that species restricted to islands that are free of predators are more likely to use torpor than mainland species that face the risk of predation during the rest-phase. We also analysed interspecific variation in columbid BMR in a phylogenetically informed framework and verified the conclusions of an earlier study which found that BMR is significantly lower in island species compared to those that occur on mainlands.

Keywords

Columbidae Evolution Hypothermia Islands Thermoregulation 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We thank Dr Dorianne Elliott of the Onderstepoort Bird and Exotic Animal Hospital for implanting and explanting iButtons, as well as Swawel Vet, Pretoria, for sponsoring veterinary products. We also thank two anonymous reviewers who provided constructive comments and insights that greatly improved the quality of this paper. This study was approved by the University of Pretoria Animal Use and Care Committee (project EC077-11), and complies with current South African laws. The work was made possible by funding from the DST/NRF Centre of Excellence at the Percy FitzPatrick Institute, the University of Pretoria, and the National Science Foundation, USA (IOS-1122228).

Supplementary material

360_2013_763_MOESM1_ESM.docx (29 kb)
Supplementary material 1 (DOCX 28.5 kb)

References

  1. Anderson KJ, Jetz W (2005) The broad-scale ecology of energy expenditure of endotherms. Ecol Lett 8:310–318CrossRefGoogle Scholar
  2. Baker WC, Pouchot JF (1983) The measurement of gas flow. Part II. J Air Pollut Control Assoc 33:156–162CrossRefGoogle Scholar
  3. Baptista LF, Trail PW, Horblit HM (1997) Family Columbidae (pigeons and doves). In: del Hoyo J, Elliot A, Sargatal J (eds) Handbook of the birds of the world vol 4 Sandgrouse to cuckoos. Lynx Edicions, Barcelona, pp 60–243Google Scholar
  4. Bauer AM, Vindum JV (1990) A checklist and key to the herpetofauna of New Caledonia, with remarks on biogeography. Proc Calif Acad Sci 47:17–45Google Scholar
  5. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745PubMedGoogle Scholar
  6. Blondel J, Dias PC, Perret P, Maistre M, Lambrechts MM (1999) Selection-based biodiversity at a small spatial scale in a low-dispersing insular bird. Science 285:1399–1402PubMedCrossRefGoogle Scholar
  7. Boyles JG, Smit B, McKechnie AE (2011) A new comparative metric for estimating heterothermy in endotherms. Physiol Biochem Zool 84:115–123PubMedCrossRefGoogle Scholar
  8. Brigham RM, McKechnie AE, Doucette LI, Geiser F (2012) Heterothermy in caprimulgid birds: a review of inter- and intraspecific variation in free-ranging populations. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world: thermoregulatory and metabolic adaptation. Springer, Heidelberg, pp 175–187CrossRefGoogle Scholar
  9. Clegg SM, Degnan SM, Moritz C, Estoup A, Kikkawa J, Owens IPF (2002) Microevolution in island forms: the roles of drift and directional selection in morphological divergence of a passerine bird. Evolution 56:2090–2099PubMedGoogle Scholar
  10. Cory Toussaint D, McKechnie AE (2012) Interspecific variation in thermoregulation among three sympatric bats inhabiting a hot, semi-arid environment. J Comp Physiol B 182:1129–1140PubMedCrossRefGoogle Scholar
  11. Cowles GS, Goodwin D (1959) Seed digestion by the fruit-eating pigeon Treron. Ibis 101:253–254Google Scholar
  12. Daan S, Masman D, Groenewold A (1990) Avian basal metabolic rates: their association with body composition and energy expenditure in nature. Am J Physiol 259:R333–R340PubMedGoogle Scholar
  13. Dawson WR, Whittow GC (2000) Regulation of body temperature. In: Sturkie PD (ed) Avian physiology. Academic Press, New York, pp 343–390CrossRefGoogle Scholar
  14. Dean WRJ (2005) African Green-Pigeon. In: Hockey PAR, Dean WRJ, Ryan PG (eds) Roberts birds of southern Africa. The Trustees of the John Voelcker Bird Book Fund, Cape TownGoogle Scholar
  15. Downs CT, Brown M (2002) Nocturnal heterothermy and torpor in the Malachite sunbird (Nectarinia famosa). Auk 119:251–260Google Scholar
  16. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  17. Geiser F (1993) Metabolic rate reduction during hibernation. In: Carey C, Florant GL, Wunder BA, Horwitz B (eds) Life in the cold: ecological, physiological and molecular mechanisms. Westview Press, BoulderGoogle Scholar
  18. Geiser F (2004) Metabolic rate and body temperature reduction during daily torpor. Ann Rev Physiol 66:239–274CrossRefGoogle Scholar
  19. Geiser F, Holloway JC, Körtner G, Maddocks TA, Turbill C, Brigham RM (2000) Do patterns of torpor differ between free-ranging and captive mammals and birds? In: Heldmaier G, Klingenspor M (eds) Life in the cold: 11th international hibernation symposium. Springer, Berlin, pp 95–102Google Scholar
  20. Genz A, Bretz F, Miwa T, Mi X, Leisch F, Scheipl F, Hothorn T (2011) mvtnorm: Multivariate normal and t distributions. R package version 0.9-9991Google Scholar
  21. Gibb GC, Penny D (2010) Two aspects along the continuum of pigeon evolution: a South-Pacific radiation and the relationship of pigeons within Neoaves. Mol Phylogenet Evol 56:698–706PubMedCrossRefGoogle Scholar
  22. Gibbs D, Barnes E, Cox J (2001) Pigeons and doves: a guide to the pigeons and doves of the world. Christopher Helm Publishers, LondonGoogle Scholar
  23. Goodwin D (1983) Pigeons and doves of the world. Cornell University Press, IthacaGoogle Scholar
  24. Grant PR (1968) Bill size, body size, and the ecological adaptations of bird species to competitive situations on islands. Syst Biol 17:319–333CrossRefGoogle Scholar
  25. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768PubMedCrossRefGoogle Scholar
  26. Heldmaier G, Ruf T (1992) Body temperature and metabolic rate during natural hypothermia in endotherms. J Comp Physiol 162:696–706Google Scholar
  27. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometr J 50:346–363CrossRefGoogle Scholar
  28. Jensen C, Bech C (1992a) Oxygen consumption and acid-base balance during shallow hypothermia in the pigeon. Respir Physiol 88:193–204PubMedCrossRefGoogle Scholar
  29. Jensen C, Bech C (1992b) Ventilation and gas exchange during shallow hypothermia in pigeons. J Exp Biol 165:111–120Google Scholar
  30. Jetz W, Freckleton RP, McKechnie AE (2008) Environment, migratory tendency, phylogeny and basal metabolic rate in birds. PLoS ONE 3:e3261PubMedCrossRefGoogle Scholar
  31. Jetz W, Thomas GE, Joy JB, Hartmann K, Mooers AO (2012) The global diversity of birds in space and time. Nature 491:444–448PubMedCrossRefGoogle Scholar
  32. Karasov WH (1990) Digestion in birds: chemical and physiological determinants and implications. In: Morrison ML, Ralph CJ, Verner J, Jehl JR (eds) Studies in avian biology No 13. Cooper Ornithological Society, Los Angeles, pp 391–415Google Scholar
  33. Kendeigh SC, Dol’nik VR, Gavrilov VM (1977) Avian energetics. In: Pinowski J, Kendeigh SC (eds) Granivorous birds in ecosystems. Cambridge University Press, Cambridge, pp 129–204Google Scholar
  34. Lambert LR (1989) Pigeons as seed predators and dispersers of figs in a Malaysian lowland forest. Ibis 131:521–527CrossRefGoogle Scholar
  35. Lasiewski RC, Acosta AL, Bernstein MH (1966) Evaporative water loss in birds-I. Characteristics of the open flow method of determination, and their relation to estimates of thermoregulatory ability. Comp Biochem Physiol 19:445–457CrossRefGoogle Scholar
  36. Laurila M, Hohtola E (2005) The effect of ambient temperature and simulated predation risk on fasting-induced nocturnal hypothermia of pigeons in outdoor conditions. J Therm Biol 30:392–399CrossRefGoogle Scholar
  37. Lavin SR, Karasov WH, Ives AR, Middleton KM, Garland T (2008) Morphometrics of the avian small intestine compared with that of nonflying mammals: a phylogenetic approach. Physiol Biochem Zool 81:526–550PubMedCrossRefGoogle Scholar
  38. Lighton JRB (2008) Measuring metabolic rates: a manual for scientists. Oxford University Press, OxfordCrossRefGoogle Scholar
  39. Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156:201–219PubMedCrossRefGoogle Scholar
  40. MacMillen RE, Trost CH (1967) Nocturnal hypothermia in the inca dove Scardafella inca. Comp Biochem Physiol 23:243–253PubMedCrossRefGoogle Scholar
  41. Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org
  42. Maldonado KE, Cavieres G, Veloso C, Canals M, Sabat P (2009) Physiological responses in rufous-collared sparrows to thermal acclimation and seasonal acclimatization. J Comp Physiol B 179:335–343PubMedCrossRefGoogle Scholar
  43. Matson KD (2006) Are there differences in immune function between continental and insular birds? Proc R Soc B 273:2267–2274PubMedCrossRefGoogle Scholar
  44. McKechnie AE (2008) Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J Comp Physiol B 178:235–247PubMedCrossRefGoogle Scholar
  45. McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses: a review. Condor 104:705–724CrossRefGoogle Scholar
  46. McKechnie AE, Lovegrove BG (2003) Facultative hypothermic responses in an Afrotropical arid-zone passerine, the red-headed finch (Amadina erythrocephala). J Comp Physiol B 173:339–346PubMedCrossRefGoogle Scholar
  47. McKechnie AE, Lovegrove BG (2006) Evolutionary and ecological determinants of avian torpor: a conceptual model. Acta Zool Sinica 52(suppl.):409–413Google Scholar
  48. McKechnie AE, Mzilikazi N (2011) Heterothermy in Afrotropical birds and mammals: a review. Int Comp Biol 51:349–363CrossRefGoogle Scholar
  49. McKechnie AE, Smit B (2010) Thermoregulation under seminatural conditions in two species of African barbets (Piciformes: Lybiidae). Ostrich 81:97–102CrossRefGoogle Scholar
  50. McKechnie AE, Wolf BO (2010) Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biol Lett 6:253–256PubMedCrossRefGoogle Scholar
  51. McKechnie AE, Chetty K, Lovegrove BG (2007) Phenotypic flexibility in basal metabolic rate in Laughing Doves: responses to short-term thermal acclimation. J Exp Biol 210:97–106PubMedCrossRefGoogle Scholar
  52. McNab BK (1994) Energy conservation and the evolution of flightlessness in birds. Am Nat 144:628–642CrossRefGoogle Scholar
  53. McNab BK (2000) The influence of body mass, climate, and distribution on the energetics of South Pacific pigeons. Comp Biochem Physiol A 127:309–329Google Scholar
  54. McNab BK (2009) Ecological factors affect the level and scaling of avian BMR. Comp Biochem Physiol A 152:22–45CrossRefGoogle Scholar
  55. Nicholson SE, Kim J (1997) The relationship of the El Niño-Southern Oscillation to African rainfall. Int J Climatol 17:117–135CrossRefGoogle Scholar
  56. Nowak RM, Paradiso JL (1999) Walker’s mammals of the world. John Hopkins University Press, BaltimoreGoogle Scholar
  57. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884PubMedCrossRefGoogle Scholar
  58. Pereira SL, Johnson KP, Clayton DH, Baker AJ (2007) Mitochondrial and nuclear DNA sequences support a Cretaceous origin of Columbiformes and a dispersal-driven radiation in the paleogene. Syst Biol 56:656–672PubMedCrossRefGoogle Scholar
  59. Philander SGH (1983) El Niño Southern Oscillation phenomena. Nature 302:295–301CrossRefGoogle Scholar
  60. Phillips NH, Berger RJ (1991) Regulation of body temperature, metabolic rate, and sleep in fasting pigeons diurnally infused with glucose or saline. J Comp Physiol B 161:311–318PubMedCrossRefGoogle Scholar
  61. Piersma T (2002) Energetic bottlenecks and other design constraints in avian annual cycles. Int Comp Biol 42:51–67CrossRefGoogle Scholar
  62. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2009) nlme: Linear and nonlinear mixed effects models. R package version 3.1-94Google Scholar
  63. Prinzinger R, Siedle K (1988) Ontogeny of metabolism, thermoregulation and torpor in the house martin Delichon u. urbica (L.) and its ecological significance. Oecologia 76:307–312CrossRefGoogle Scholar
  64. Prinzinger R, Preßmar A, Schleucher E (1991) Body temperature in birds. Comp Biochem Physiol 99A:499–506CrossRefGoogle Scholar
  65. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  66. Rashotte ME, Henderson D, Phillips DL (1988) Thermal and feeding reactions of pigeons during food scarcity and cold. In: Bech C, Reinertsen RE (eds) Physiology of cold adaptation in birds. Plenum Press, New York, pp 255–264Google Scholar
  67. Rashotte ME, Pastukhov IF, Poliakov EL, Henderson RP (1991) Vigilance states and body temperature during the circadian cycle in fed and fasted pigeons (Columba livia). Am J Physiol 275:R1690–R1702Google Scholar
  68. Reinertsen RE (1983) Nocturnal hypothermia and its energetic significance for small birds living in the arctic and subarctic regions. A review. Polar Res 1:269–284CrossRefGoogle Scholar
  69. Reinertsen RE, Haftorn S (1986) Different metabolic strategies of northern birds for nocturnal survival. J Comp Physiol 156:655–663Google Scholar
  70. Rouys S, Theuerkauf J (2003) Factors determining the distribution of introduced mammals in nature reserves of the southern province, New Caledonia. Wildl Res 30:187–191CrossRefGoogle Scholar
  71. Schleucher E (2001) Heterothermia in pigeons and doves reduces energetic costs. J Therm Biol 26:287–293CrossRefGoogle Scholar
  72. Schleucher E (2002) Metabolism, body temperature and thermal conductance of fruit-doves (Aves: Columbidae, Treronidae). Comp Biochem Physiol A 131:417–428CrossRefGoogle Scholar
  73. Schleucher E (2004) Torpor in birds: taxonomy, energetics and ecology. Physiol Biochem Zool 77:942–949PubMedCrossRefGoogle Scholar
  74. Scholander PF, Hock R, Walters V, Johnson F, Irving L (1950) Heat regulation in some arctic and tropical mammals and birds. Biol Bull 99:237–258PubMedCrossRefGoogle Scholar
  75. Skinner JD, Chimimba CT (2005) The mammals of the southern African subregion, 3rd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  76. Smit B, McKechnie AE (2010a) Avian seasonal metabolic variation in a subtropical desert: basal metabolic rates are lower in winter than in summer. Funct Ecol 24:330–339CrossRefGoogle Scholar
  77. Smit B, McKechnie AE (2010b) Do owls use torpor? Winter thermoregulation in free-ranging Pearl-spotted Owlets and African Scops-owls. Physiol Biochem Zool 83:149–156PubMedCrossRefGoogle Scholar
  78. Stone RC, Hammer GL, Marcussen T (1996) Prediction of global rainfall probabilities using phases of the Southern Oscillation index. Nature 384:252–255CrossRefGoogle Scholar
  79. Strahan R (1991) Complete book of Australian mammals. Cornstalk, SydneyGoogle Scholar
  80. Tieleman BI, Williams JB (2000) The adjustment of avian metabolic rates and water fluxes to desert environments. Physiol Biochem Zool 73:461–479PubMedCrossRefGoogle Scholar
  81. Tieleman BI, Williams JB, Bloomer P (2003) Adaptation of metabolic rate and evaporative water loss along an aridity gradient. Proc R Soc Lond 270:207–214CrossRefGoogle Scholar
  82. Tieleman BI, Dijkstra TH, Lasky JR, Mauck RA, Visser GH, Williams JB (2006) Physiological and behavioural correlates of life-history variation: a comparison between tropical and temperate zone House Wrens. Funct Ecol 20:491–499CrossRefGoogle Scholar
  83. van de Ven TMFN, Mzilikazi N, McKechnie AE (2013) Seasonal metabolic variation in two populations of an Afrotropical euplectid bird. Physiol Biochem Zool 86:19–26PubMedCrossRefGoogle Scholar
  84. Walker LE, Walker JM, Palca JW, Berger RJ (1983) A continuum of sleep and shallow torpor in fasting doves. Science 221:194–195PubMedCrossRefGoogle Scholar
  85. Walsberg GE, King JR (1978) The relationship of the external surface area of birds to skin surface area and body mass. J Exp Biol 76:185–189Google Scholar
  86. Weathers WW (1979) Climatic adaptation in avian standard metabolic rate. Oecologia 42:81–89Google Scholar
  87. Weathers WW (1981) Physiological thermoregulation in heat-stressed birds: consequences of body size. Physiol Zool 54:345–361Google Scholar
  88. White CR, Blackburn TM, Martin GR, Butler PJ (2007) The basal metabolic rate of birds is associated with habitat temperature and precipitation, not productivity. Proc R Soc B 274:287–293PubMedCrossRefGoogle Scholar
  89. Wiersma P, Muñoz-Garcia A, Walker A, Williams JB (2007) Tropical birds have a slow pace of life. Proc Natl Acad Sci USA 104:9340–9345PubMedCrossRefGoogle Scholar
  90. Withers PC (1992) Comparative animal physiology. Saunders College Publishing, Fort WorthGoogle Scholar
  91. Wright NA, Steadman DW (2012) Insular avian adaptations on two Neotropical continental islands. J Biogeogr 39:1891–1899PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Matthew J. Noakes
    • 1
  • Ben Smit
    • 1
  • Blair O. Wolf
    • 2
  • Andrew E. McKechnie
    • 1
  1. 1.Department of Zoology and Entomology, DST/NRF Centre of Excellence at the Percy FitzPatrick InstituteUniversity of PretoriaPretoriaSouth Africa
  2. 2.UNM Biology DepartmentUniversity of New MexicoAlbuquerqueUSA

Personalised recommendations