Avian thermoregulation in the heat: scaling of heat tolerance and evaporative cooling capacity in three southern African arid-zone passerines

ABSTRACT Many birds can defend body temperature (Tb) far below air temperature (Ta) during acute heat exposure, but relatively little is known about how avian heat tolerance and evaporative cooling capacity varies with body mass (Mb), phylogeny or ecological factors. We determined maximum rates of evaporative heat dissipation and thermal end points (Tb and Ta associated with thermoregulatory failure) in three southern African ploceid passerines, the scaly-feathered weaver (Sporopipes squamifrons, Mb≈10 g), sociable weaver (Philetairus socius, Mb≈25 g) and white-browed sparrow-weaver (Plocepasser mahali, Mb≈40 g). Birds were exposed to a ramped profile of progressively increasing Ta, with continuous monitoring of behaviour and Tb used to identify the onset of severe hyperthermia. The maximum Ta birds tolerated ranged from 48°C to 54°C, and was positively related to Mb. Values of Tb associated with severe heat stress were in the range of 44 to 45°C. Rates of evaporative water loss (EWL) increased rapidly when Ta exceeded Tb, and maximum evaporative heat dissipation was equivalent to 141–222% of metabolic heat production. Fractional increases in EWL between Ta<40°C and the highest Ta reached by each species were 10.8 (S. squamifrons), 18.4 (P. socius) and 16.0 (P. mahali). Resting metabolic rates increased more gradually with Ta than expected, probably reflecting the very low chamber humidity values we maintained. Our data suggest that, within a taxon, larger species can tolerate higher Ta during acute heat stress. Highlighted Article: Heat tolerance varies with body size in African weavers in the Kalahari Desert.

[1]  W. C. Randall.  FACTORS INFLUENCING THE TEMPERATURE REGULATION OF BIRDS , 1943 .

[2]  P. F. Scholander,et al.  Heat regulation in some arctic and tropical mammals and birds. , 1950, The Biological bulletin.

[3]  C. Wenger.  THE REGULATION OF BODY TEMPERATURE , 1948, British medical journal.

[4]  Temperature Regulation and Water Requirements of the Brown and Abert Towhees, Pipilo fuscus and Pipilo aberti William R. Dawson , 1955 .

[5]  D. Farner,et al.  CHAPTER XIX – Energy Metabolism, Thermoregulation and Body Temperature1 , 1961 .

[6]  A. Brush.  Energetics, temperature regulation and circulation in resting, active and defeathered california quail, Lophortyx californicus , 1965 .

[7]  T. Cade,et al.  Water Economy and Metabolism of Two Estrildine Finches , 1965, Physiological Zoology.

[8]  R. C. Lasiewski,et al.  Evaporative water loss in birds—I. Characteristics of the open flow method of determination, and their relation to estimates of thermoregulatory ability , 1966 .

[9]  R. C. Lasiewski,et al.  Evaporative water loss in birds—II. A modified method for determination by direct weighing , 1966 .

[10]  K. Schmidt-Nielsen,et al.  Temperature regulation and evaporation in the pigeon and the roadrunner. , 1967, The American journal of physiology.

[11]  J. Rising.  A comparison of metabolism and evaporative water loss of baltimore and bullock orioles , 1969 .

[12]  Charles D. Fisher,et al.  Responses to Temperature by the Spotted Nightjar (Eurostopodus guttatus) , 1969 .

[13]  R. C. Lasiewski,et al.  Thermoregulatory Responses to Heat Stress in Four Species of Birds Weighing Approximately 40 Grams , 1972, Physiological Zoology.

[14]  W. Calder,et al.  Temperature Regulation of the Pyrrhuloxia and the Arizona Cardinal , 1973, Physiological Zoology.

[15]  J. Marder.  Body temperature regulation in the brown-necked raven (Corvus corax ruficollis). I. Metabolic rate, evaporative water loss and body temperature of the raven exposed to heat stress. , 1973, Comparative biochemistry and physiology. A, Comparative physiology.

[16]  Avian Biology Avian Biology, Vol. II D. S. Farner J. R. King , 1974 .

[17]  M Cabanac,et al.  Temperature regulation. , 1975, Annual review of physiology.

[18]  G. S. Bakken.  A heat transfer analysis of animals: unifying concepts and the application of metabolism chamber data to field ecology. , 1976, Journal of theoretical biology.

[19]  G. C. Whittow.  Regulation of Body Temperature , 1976 .

[20]  W. Weathers.  Physiological Thermoregulation in Heat-Stressed Birds: Consequences of Body Size , 1981, Physiological Zoology.

[21]  Z. Arad,et al.  Strain differences in heat resistance to acute heat stress, between the bedouin desert fowl, the white leghorn and their crossbreeds , 1982 .

[22]  W. Dawson,et al.  Evaporative losses of water by birds. , 1982, Comparative biochemistry and physiology. A, Comparative physiology.

[23]  W. Montevecchi.  Avian Incubation: Egg Temperature, Nest Humidity, and Behavioral Thermoregulation in a Hot Environment. American Ornithologists' Union, Washington, D.C. (1982), ix, (Ornithological Monographs, No. 30), +75. Price $9.00 , 1983 .

[24]  Cutaneous evaporation in heat-stressed spotted sandgrouse , 1986 .

[25]  Body and Egg Temperature Regulation in Incubating Pigeons Exposed to Heat Stress: The Role of Skin Evaporation , 1986, Physiological Zoology.

[26]  Y. Arieli,et al.  Heat balance of acclimated pigeons (Columba livia) exposed to temperatures up to 60°c ta , 1988 .

[27]  S. Hinsley,et al.  Black-Bellied Sandgrouse (Pterocles orientalis) and Pin-Tailed Sandgrouse (Pterocles alchata): Closely Related Species with Differing Bioenergetic Adaptations to Arid Zones , 1993, Physiological Zoology.

[28]  G. Walsberg,et al.  Variation in the respiratory quotient of birds and implications for indirect calorimetry using measurements of carbon dioxide production , 1995, The Journal of experimental biology.

[29]  S. J. Ambrose,et al.  Water and energy balance of captive and free-ranging spinifexbirds (Eremiornis carteri) North (Aves:Sylviidae) on Barrow Island, Western Australia , 1996 .

[30]  B. O. Wolf,et al.  Thermal Effects of Radiation and Wind on a Small Bird and Implications for Microsite Selection , 1996 .

[31]  D. Swanson,et al.  Sliding vs static cold exposure and the measurement of summit metabolism in birds , 1996 .

[32]  G. Walsberg,et al.  Respiratory and cutaneous evaporative water loss at high environmental temperatures in a small bird , 1996, The Journal of experimental biology.

[33]  W. Weathers.  Energetics and thermoregulation by small passerines of the humid, lowland tropics , 1997 .

[34]  E. Greene,et al.  Thermoregulatory responses of Bridled and Juniper Titmice to high temperature , 1998 .

[35]  Joseph B. Williams,et al.  The Role of Hyperthermia in the Water Economy of Desert Birds , 1999, Physiological and Biochemical Zoology.

[36]  Joseph B. Williams.  Heat production and evaporative water loss of dune larks from the Namib Desert , 1999 .

[37]  Joseph B. Williams,et al.  Physiological responses of Houbara bustards to high ambient temperatures. , 2002, The Journal of experimental biology.

[38]  Joseph B. Williams,et al.  Physiological Adjustments to Arid and Mesic Environments in Larks (Alaudidae) , 2002, Physiological and Biochemical Zoology.

[39]  Joseph B. Williams,et al.  Cutaneous and Respiratory Water Loss in Larks from Arid and Mesic Environments , 2002, Physiological and Biochemical Zoology.

[40]  R. Dmi’el,et al.  Heat balance of two starling species (Sturnus vulgaris andOnychognathus tristrami) from temperate and desert habitats , 1985, Journal of Comparative Physiology B.

[41]  G. Campbell,et al.  An evaluation of heat exchange in small birds , 2004, Journal of comparative physiology.

[42]  B. O. Wolf,et al.  Partitioning of evaporative water loss in white-winged doves: plasticity in response to short-term thermal acclimation , 2004, Journal of Experimental Biology.

[43]  L. Leon.  The thermoregulatory consequences of heat stroke: Are cytokines involved? , 2006 .

[44]  M. Muggeo,et al.  segmented: An R package to Fit Regression Models with Broken-Line Relationships , 2008 .

[45]  B. Tieleman,et al.  Nest Site Selection in a Hot Desert: Trade-Off Between Microclimate and Predation Risk , 2008 .

[46]  John R. B. Lighton,et al.  Measuring Metabolic Rates , 2008 .

[47]  Blair O. Wolf,et al.  Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves , 2010, Biology Letters.

[48]  Joseph B. Williams,et al.  Respiratory and cutaneous water loss of temperate-zone passerine birds. , 2010, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[49]  P. Withers,et al.  Effects of experiment start time and duration on measurement of standard physiological variables , 2011, Journal of Comparative Physiology B.

[50]  P. Hockey,et al.  The costs of keeping cool in a warming world: implications of high temperatures for foraging, thermoregulation and body condition of an arid‐zone bird , 2012, Global change biology.

[51]  B. O. Wolf,et al.  Feeling the heat: Australian landbirds and climate change , 2012 .

[52]  P. Hockey,et al.  Temperatures in Excess of Critical Thresholds Threaten Nestling Growth and Survival in A Rapidly-Warming Arid Savanna: A Study of Common Fiscals , 2013, PloS one.

[53]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[54]  A. McKechnie,et al.  Experimental Sources of Variation in Avian Energetics: Estimated Basal Metabolic Rate Decreases with Successive Measurements , 2014, Physiological and Biochemical Zoology.

[55]  B. O. Wolf,et al.  The Impact of Humidity on Evaporative Cooling in Small Desert Birds Exposed to High Air Temperatures , 2014, Physiological and Biochemical Zoology.