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Physiological responses in rufous-collared sparrows to thermal acclimation and seasonal acclimatization

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Abstract

A large number of physiological acclimation studies assume that flexibility in a certain trait is both adaptive and functionally important for organisms in their natural environment; however, it is not clear how an organism’s capacity for temperature acclimation translates to the seasonal acclimatization that these organisms must accomplish. To elucidate this relationship, we measured BMR and TEWL rates in both field-acclimatized and laboratory-acclimated adult rufous-collared sparrows (Zonotrichia capensis). Measurements in field-acclimatized birds were taken during the winter and summer seasons; in the laboratory-acclimated birds, we took our measurements following 4 weeks at either 15 or 30°C. Although BMR and TEWL rates did not differ between winter and summer in the field-acclimatized birds, laboratory-acclimated birds exposed to 15°C exhibited both a higher BMR and TEWL rate when compared to the birds acclimated to 30°C and the field-acclimatized birds. Because organ masses seem to be similar between field and cold-acclimated birds whereas BMR is higher in cold-acclimated birds, the variability in BMR cannot be explained completely by adjustments in organ masses. Our findings suggest that, although rufous-collared sparrows can exhibit thermal acclimation of physiological traits, sparrows do not use this capacity to cope with minor to moderate fluctuations in environmental conditions. Our data support the hypothesis that physiological flexibility in energetic traits is a common feature of avian metabolism.

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Abbreviations

BMR:

Basal metabolic rate

Cw:

Wet thermal conductance

CWL:

Cutaneous water loss

RWL:

Respiratory water loss

Tb:

Body temperature

TEWL:

Total evaporative water loss

References

  • Araya MB (1996) Guía De Campo De las aves de Chile. Editorial Universitaria, Santiago

    Google Scholar 

  • Arens JR, Cooper SJ (2005) Metabolic and ventilatory acclimatization to cold stress in house sparrows (Passer domesticus). PhysiolBiochem Zool 78:579–589

    Article  Google Scholar 

  • Bennett AF, Lenski RE (1999) Experimental evolution and its role in evolutionary physiology. Am Zool 39:346–362

    Google Scholar 

  • Bozinovic F, Bacigalupe LD, Vasquez RA, Visser GH, Veloso C, Kenagy GJ (2004) Cost of living in free-ranging degus (Octodon degus): seasonal dynamics of energy expenditure. Comp Biochem Physiol A 137:597–604

    Article  Google Scholar 

  • di Castri F, Hajek E (1976) Bioclimatología de Chile. Editorial Universidad Católica, Santiago

    Google Scholar 

  • Chastel O, Lacroix A, Kersten M (2003) Pre-breeding energy requirements: thyroid hormone, metabolism and the timing of reproduction in house sparrows Passer domesticus. J Avian Biol 34:298–306

    Article  Google Scholar 

  • Christians JK (1999) Controlling for body mass effects: is part-whole correlation important? Physiol Biochem Zool 72:250–253

    Article  PubMed  CAS  Google Scholar 

  • Cooper SJ (2000) Seasonal energetics of Mountain Chickadees and Juniper Titmice. Condor 102:635–644

    Article  Google Scholar 

  • Cooper SJ (2002) Seasonal metabolic acclimatization in mountain chickadees and juniper titmice. Physiol Biochem Zool 75:386–395

    Article  PubMed  Google Scholar 

  • Cooper SJ, Swanson DL (1994) Seasonal acclimatization of thermoregulation in the black-capped Chickadee. Condor 96:638–646

    Article  Google Scholar 

  • 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–R340

    PubMed  CAS  Google Scholar 

  • Dawson WR (1984) Physiological-studies of desert birds—present and future considerations. J Arid Environ 7:133–155

    Google Scholar 

  • Dawson WR, Marsh RL, Buttemer WA, Carey C (1983a) Seasonal and geographic-variation of cold resistance in house finches Carpodacus mexicanus. Physiol Zool 56:353–369

    Google Scholar 

  • Dawson WR, Marsh RL, Yacoe ME (1983b) Metabolic adjustments of small passerine birds for migration and cold. Am J Physiol 245:R755–R767

    PubMed  CAS  Google Scholar 

  • Dawson WR, Buttemer WA, Carey C (1985) A reexamination of the metabolic response of house finches to temperature. Condor 87:424–427

    Article  Google Scholar 

  • Feder ME, Bennett AF, Huey RB (2000) Evolutionary physiology. Ann Rev Ecol System 31:315–341

    Article  Google Scholar 

  • Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Ann Rev Ecol Syst 19:207–233

    Article  Google Scholar 

  • Gelineo S (1964) Organ systems in adaptation: the temperature regulating system. In: Dill DB (ed) Handbook of physiology, Sect. 4. Adaptation to environment. American Physiological Society, Washington, DC, pp 259–282

    Google Scholar 

  • Goodall JD, Jonson AW, Philippi RA (1951) Las aves de Chile, su conocimiento y sus costumbres, vol II. Platt Establecimientos Gráficos, Buenos Aires

    Google Scholar 

  • Haugen MJ, Tieleman BI, Williams JB (2003a) Phenotypic flexibility in cutaneous water loss and lipids of the stratum corneum. J Exp Biol 206:3581–3588

    Article  PubMed  Google Scholar 

  • Haugen M, Williams JB, Wertz P, Tieleman BI (2003b) Lipids of the stratum corneum vary with cutaneous water loss among larks along a temperature-moisture gradient. Physiol Biochem Zool 76:907–917

    Article  PubMed  CAS  Google Scholar 

  • Hinsley SA, Ferns PN, Thomas DH, Pinshow B (1993) Black-Bellied Sandgrouse (Pterocles-Orientalis) and Pin-Tailed Sandgrouse (Pterocles alchata)—Closely related species with differing bioenergetic adaptations to arid zones. Physiol Zool 66:20–42

    Google Scholar 

  • Hudson JW, Kimzey SL (1966) Temperature regulation and metabolic rhythms in populations of house sparrow Passer domesticus. Comp Biochem Physiol 17:203–217

    Article  PubMed  CAS  Google Scholar 

  • de Jong G (1995) Phenotypic plasticity as a product of selection in a variable environment. Am Nat 145:493–512

    Article  Google Scholar 

  • Karasov WH (1996) Avian energetics and nutritional ecology. Chapman and Hall, New York

    Google Scholar 

  • Kenagy GJ, Nespolo RF, Vasquez RA, Bozinovic F (2002) Daily and seasonal limits of time and temperature to activity of degus. Rev Chil Hist Nat 75:567–581

    Google Scholar 

  • Kersten M, Bruinzeel LW, Wiersma P, Piersma T (1998) Reduced basal metabolic rate of migratory waders wintering in coastal Africa. Ardea 86:71–80

    Google Scholar 

  • King JR, Farner DS (1961) Energy metabolism, thermoregulation and body temperature. In: Marshall AJ (ed) Biology and comparative physiology of birds, vol II. Academic Press, New York, pp 215–288

    Google Scholar 

  • Kingsolver JG, Huey RB (1998) Evolutionary analyses of morphological and physiological plasticity in thermally variable environments. Am Zool 38:545–560

    Google Scholar 

  • Klaassen M, Oltrogge M, Trost L (2004) Basal metabolic rate, food intake, and body mass in cold-and warm-acclimated Garden Warblers. Comp Biochem Physiol A 137:639–647

    Article  Google Scholar 

  • Leroi AM, Bennett AF, Lenski RE (1994) Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation assumption. Proc Natl Acad Sci 91:1917–1921

    Article  PubMed  CAS  Google Scholar 

  • Lide DR (2001) CRC handbook of chemistry and physics, 82th edn. CRC Press, Boca Raton

    Google Scholar 

  • McKechnie AE (2008) Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J Comp Physiol B 178:235–247

    Article  PubMed  Google Scholar 

  • McNab BK (2003) Ecology shapes bird bioenergetics. Nature 426:620–621

    Article  PubMed  CAS  Google Scholar 

  • Menon GK, Baptista LF, Brown BE, Elias PM (1989) Avian epidermal differentiation II. Adaptive response of permeability barrier to water deprivation and replenishment. Tissue Cell 21:83–92

    Article  PubMed  CAS  Google Scholar 

  • Moran NA (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989

    Article  Google Scholar 

  • Mueller P, Diamond J (2001) Metabolic rate and environmental productivity: well-provisioned animals evolved to run and idle fast. Proc Natl Acad Sci 98:12550–12554

    Article  PubMed  CAS  Google Scholar 

  • Muñoz-Garcia A, Williams JB (2005) Cutaneous water loss and lipids of the stratum corneum in house sparrows Passer domesticus from arid and mesic environments. J Exp Biol 208:3689–3700

    Article  PubMed  Google Scholar 

  • O’Connor TP (1995) Seasonal acclimatization of lipid mobilization and catabolism in-house finches (Carpodacus mexicanus). Physiol Zool 68:985–1005

    CAS  Google Scholar 

  • Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233

    Article  Google Scholar 

  • Piersma T, Lindstrom A (1997) Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol Evol 12:134–138

    Article  Google Scholar 

  • Piersma T, Vezina F (2007) Acclimation in long-distance migrant birds that routinely move between contrasting temperature regimes: experimental studies on red knots. Comp Biochem Physiol A 146:S206

    Google Scholar 

  • Piersma T, Cadee N, Daan S (1995) Seasonality in basal metabolic-rate and thermal conductance in a long-distance migrant shorebird, the knot (Calidris canutus). J Comp Physiol B 165:37–45

    Article  Google Scholar 

  • Piersma T, Bruinzeel L, Drent R, Kersten M, VanderMeer J, Wiersma P (1996) Variability in basal metabolic rate of a long-distance migrant shorebird (Red Knot, Calidris canutus) reflects shifts in organ sizes. Physiol Zool 69:191–217

    Google Scholar 

  • Piersma T, Gudmundsson GA, Lilliendahl K (1999) Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. Physiol Biochem Zool 72:405–415

    Article  PubMed  CAS  Google Scholar 

  • Porter WP, Budaraju S, Stewart WE, Ramankutty N (2000) Calculating climate effects on birds and mammals: Impacts on biodiversity, conservation, population parameters, and global community structure. Am Zool 40:597–630

    Article  Google Scholar 

  • Repasky RR (1991) Temperature and the Northern distributions of wintering birds. Ecology 72:2274–2285

    Article  Google Scholar 

  • Root T (1988) Energy constraints on avian distributions and abundances. Ecology 69:330–339

    Article  Google Scholar 

  • Sabat P, Bozinovic F (1994) Cambios estacionales en la actividad de enzimas digestivas en el pequeño marsupial chileno Thylamys elegans: disacaridasas intestinales. Rev Chil Hist Nat 67:221–228

    Google Scholar 

  • Sabat P, Novoa FF, Bozinovic F, Martínez del Rio C (1998) Dietary flexibility and intestinal plasticity in birds: a field and laboratory study. Physiol Zool 71:226–236

    PubMed  CAS  Google Scholar 

  • Sabat P, Cavieres G, Veloso C, Canals M (2006) Water and energy economy of an omnivorous bird: population differences in the rufous-collared sparrow (Zonotrichia capensis). Comp Biochem Physiol A 144:485–490

    Article  Google Scholar 

  • Schleucher E, Withers PC (2001) Re-evaluation of the allometry of wet thermal conductance for birds. Comp Biochem Physiol A 129:821–827

    CAS  Google Scholar 

  • Swanson DL (1991) Seasonal adjustments in metabolism and insulation in the dark-eyed Junco. Condor 93:538–545

    Article  Google Scholar 

  • Swanson DL (1993) Cold tolerance and thermogenic capacity in dark-eyed juncos in winter—geographic-variation and comparison with American Tree Sparrows. J Therm Biol 18:275–281

    Article  Google Scholar 

  • Swanson DL, Olmstead KL (1999) Evidence for a proximate influence of winter temperature on metabolism in passerine birds. Physiol Biochem Zool 72:566–575

    Article  PubMed  CAS  Google Scholar 

  • Tieleman BI (2007) Differences in the physiological responses to temperature among stonechats from three populations reared in a common environment. Comp Biochem Physiol A 146:194–199

    Article  Google Scholar 

  • Tieleman BI, Williams JB (2000) The adjustment of avian metabolic rates and water fluxes to desert environments. Physiol Biochem Zool 73:461–479

    Article  PubMed  CAS  Google Scholar 

  • Tieleman BI, Williams JB (2002) Cutaneous and respiratory water loss in larks from arid and mesic environments. Physiol Biochem Zool 75:590–599

    Article  PubMed  Google Scholar 

  • Tieleman BI, Williams JB, LaCroix F, Paillat P (2002) Physiological responses of Houbara bustards to high ambient temperatures. J Exp Biol 205:503–511

    PubMed  Google Scholar 

  • Tieleman BI, Williams JB, Bloomer P (2003a) Adaptation of metabolism and evaporative water loss along an aridity gradient. Proc R Soc Lond B 270:207–214

    Article  Google Scholar 

  • Tieleman BI, Williams JB, Buschur ME, Brown CR (2003b) Phenotypic variation of larks along an aridity gradient: are desert birds more flexible? Ecology 84:1800–1815

    Article  Google Scholar 

  • Via S (1993) Adaptive phenotypic plasticity: target or by-product of selection in a variable environment? Am Nat 142:352–365

    Article  Google Scholar 

  • Walsberg GE, Wolf BO (1995) Variation in the respiratory quotient of birds and implications for indirect calorimetry using measurements of carbon dioxide production. J Exp Biol 198:213–219

    PubMed  Google Scholar 

  • Weber TP, Piersma T (1996) Basal metabolic rate and the mass of tissues differing in metabolic scope: migration-related covariation between individual knots Calidris canutus. J Avian Biol 27:215–224

    Article  Google Scholar 

  • Wiersma P, Munoz-Garcia A, Walker A, Williams JB (2007) Tropical birds have a slow pace of life. Proc Natl Acad Sci 104:9340–9345

    Article  PubMed  CAS  Google Scholar 

  • Williams JB (1996) A phylogenetic perspective of evaporative water loss in birds. Auk 113:457–472

    Google Scholar 

  • Williams JB (1999) Heat production and evaporative water loss of Dune Larks from the Namib desert. Condor 101:432–438

    Article  Google Scholar 

  • Williams JB, Tieleman BI (2000) Flexibility in basal metabolic rate and evaporative water loss among hoopoe larks exposed to different environmental temperatures. J Exp Biol 203:3153–3159

    PubMed  CAS  Google Scholar 

  • Withers PC, Williams JB (1990) Metabolic and respiratory physiology of an arid-adapted Australian bird, the Spinifex pigeon. Condor 92:961–969

    Article  Google Scholar 

  • Withers PC (1977) Measurements of metabolic rate, VCO2, and evaporative water loss with flow through mask. J Appl Physiol 42:120–123

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Bradley Bakken, Alfredo Kirkwood, Catalina Sabando and Ariovaldo Cruz-Neto and two anonymous referees for their useful comments on a previous version of our manuscript. Sandra Gonzalez and Andres Sazo provided invaluable assistance in the field and in the laboratory. Funded by Fondecyt 1050196 to PS. All the experiments comply with the current laws of Chile, where the experiments were performed.

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Authors and Affiliations

  1. Departamento de Ciencias Ecologicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile

    Karin Evelyn Maldonado, Grisel Cavieres, Claudio Veloso, Mauricio Canals & Pablo Sabat

  2. Center for Advanced Studies in Ecology and Biodiversity, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago, Chile

    Pablo Sabat

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  1. Karin Evelyn Maldonado
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  2. Grisel Cavieres
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  3. Claudio Veloso
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  4. Mauricio Canals
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  5. Pablo Sabat
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Correspondence to Pablo Sabat.

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Communicated by I. D. Hume.

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Maldonado, K.E., Cavieres, G., Veloso, C. et al. Physiological responses in rufous-collared sparrows to thermal acclimation and seasonal acclimatization. J Comp Physiol B 179, 335–343 (2009). https://doi.org/10.1007/s00360-008-0317-1

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  • DOI: https://doi.org/10.1007/s00360-008-0317-1

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