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Journal of Comparative Physiology B

, Volume 189, Issue 1, pp 131–141 | Cite as

Thermal physiology of a range-restricted desert lark

  • Ryno Kemp
  • Andrew E. McKechnieEmail author
Original Paper

Abstract

Much recent work on avian physiological adaptation to desert environments has focused on larks (Passeriformes: Alaudidae). We tested the prediction that the threatened red lark (Calendulauda burra), a species restricted to very arid parts of South Africa and which is not known to drink, exhibits highly efficient evaporative cooling and makes pronounced use of facultative hyperthermia when exposed to high air temperatures (Ta). We also predicted that C. burra possesses similarly low basal metabolic rate (BMR) and total evaporative water loss (EWL) at moderate Ta as reported for species from the deserts of the Middle East. Rest-phase thermoregulation in C. burra was characterized by an unusually low lower critical limit of thermoneutrality at Ta = ~ 21 °C and a BMR of 0.317 ± 0.047 W, the lowest BMR relative to allometrically-expected values yet reported in any lark. During the diurnal active phase, red larks were able to tolerate Ta up to 50 °C, with the onset of panting occurring at Ta = 38 °C. Maximum EWL was 1.475 ± 0.107 g h− 1 at Ta = 50 °C, equivalent to 620% of minimum EWL at thermoneutrality. The maximum ratio of evaporative heat dissipation to metabolic heat production was 1.58, a value towards the lower end of the range reported for passerines. Our data support the prediction that C. burra shows metabolic traits similar to those of other larks inhabiting extremely arid climates, but not the notion that evaporative cooling at high Ta in this species is more efficient than in most passerines.

Keywords

Alaudidae Basal metabolic rate Body temperature Calendulauda burra Evaporative water loss Heat tolerance 

Abbreviations

EWL

Evaporative water loss

BMR

Basal metabolic rate

RMR

Resting metabolic rate

EHL

Evaporative heat loss

MHP

Metabolic heat production

Mb

Body mass

Ta

Air temperature

Tb

Body temperature

Tlc

Lower critical limit of thermoneutrality

Tuc

Upper critical limit of thermoneutrality

Notes

Acknowledgements

We thank Black Mountain Mine for allowing us to conduct research on their property in the Koa River Valley and Kobus Smit of Vedanta Resources for his assistance and support. We are grateful to Clarise Kemp and Marc Freeman for assistance in the field, and to an anonymous reviewer whose constructive comments greatly improved the quality of the manuscript. All procedures were approved by the Animal Ethics Committee of the University of Pretoria (protocol EC41-17) and the Research Ethics and Scientific Committee of the South African National Biodiversity Institute (protocol P17-29). Red larks were captured under permit from the Northern Cape Department of Environment and Nature Conservation (FAUNA 1209/2017). This work was made possible by funding from the DST-NRF Centre of Excellence at the FitzPatrick Institute and is also based on research supported in part by the National Research Foundation of South Africa (Grant Number 110506). Any opinions, findings and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Research Foundation.

Compliance with ethical standards

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Supplementary material

360_2018_1190_MOESM1_ESM.docx (12 kb)
Supplementary material 1 (DOCX 12 KB)
360_2018_1190_MOESM2_ESM.jpg (3.9 mb)
Supplementary material 2: Typical red lark (Calendulauda burra) habitat at our study site at Black Mountain Conservation Area, Aggeneys, South Africa. (JPG 3945 KB)

Supplementary material 3: Red lark (Calendulauda burra) resting in a shaded microsite on a very hot day at Black Mountain Conservation Area, Aggeneys, South Africa. The air temperature at the time the video was recorded was 39 °C. (MP4 31812 KB)

References

  1. Alström P, Barnes KN, Olsson U, Barker FK, Bloomer P, Khan AA, Qureshi MA, Guillaumet A, Crochet P-A, Ryan PG (2013) Multilocus phylogeny of the avian family Alaudidae (larks) reveals complex morphological evolution, non-monophyletic genera and hidden species diversity. Mol Phylogenetics Evol 69(3):1043–1056CrossRefGoogle Scholar
  2. Aschoff J (1982) The circadian rhythm of body temperature as a function of body size. In: Taylor CR, Johansen R, Bolis L (eds) A companion to animal physiology. Cambridge University Press, Cambridge, pp 173–188Google Scholar
  3. Aschoff J, Pohl H (1970) Der Ruheumsatz von Vögeln als Funktion der Tageszeit und der Körpergröße. J für Ornithiol 111:38–47CrossRefGoogle Scholar
  4. Baker WC, Pouchot JF (1983) The measurement of gas flow. Part II. J Air Pollut Control Assoc 33(2):156–162CrossRefGoogle Scholar
  5. Bartholomew GA, Cade TJ (1963) The water economy of land birds. Auk 80:504–539CrossRefGoogle Scholar
  6. Bartoń K (2013) MuMIn: multi-model inference, R package version 1.9.13Google Scholar
  7. Cory Toussaint D, McKechnie AE (2012) Interspecific variation in thermoregulation among three sympatric bats inhabiting a hot, semi-arid environment. J Comp Physiol B 182:1129–1140CrossRefPubMedGoogle Scholar
  8. Cunningham SJ, Martin RO, Hojem CL, Hockey PAR (2013) Temperatures in excess of critical thresholds threaten nestling growth and survival in a rapidly-warming arid savanna: a study of common fiscals. PLoS One 8(9):e74613CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cunningham SJ, Thompson ML, McKechnie AE (2017) It’s cool to be dominant: social status alters short-term risks of heat stress. J Exp Biol 220:1558–1562CrossRefPubMedGoogle Scholar
  10. Dawson WR (1954) Temperature regulation and water requirements of the brown and Abert towhees, Pipilo fuscus and Pipilo aberti. In: Bartholomew GA, Crescitelli F, Bullock TH, Furgason WH, Schechtman AM (eds) University of California Publications in Zoology, vol 59. University of California Press, Berkeley, pp 81–123Google Scholar
  11. Dawson WR, Bartholomew GA (1968) Temperature regulation and water economy of desert birds. In: Brown GW (ed) Desert biology. Academic Press, New York, pp 357–394CrossRefGoogle Scholar
  12. Dawson WR, Fisher CD (1969) Responses to temperature by the spotted nightjar (Eurostopodus guttatus). Condor 71:49–53CrossRefGoogle Scholar
  13. Dawson WR, Schmidt-Nielsen K (1964) Terrestrial animals in dry heat: desert birds. In: Dill DB (ed) Handbook of physiology: adaptation to the environment. American Physiological Society, Washington, D.C., pp 481–492Google Scholar
  14. de Juana E, Suarez F, Ryan PG (2018) Larks (Alaudidae). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona. https://www.hbw.com/node/52302 (Retrieved from 18 June 2018)
  15. Dean WRJ, Ryan PG (2005) Red Lark. In: Hockey PAR, Dean WRJ, Ryan PG (eds) Roberts birds of southern Africa. The Trustees of the John Voelcker Bird Book Fund, Cape Town, pp 871–872Google Scholar
  16. du Plessis KL, Martin RO, Hockey PAR, Cunningham SJ, Ridley AR (2012) The costs of keeping cool in a warming world: implications of high temperatures for foraging, thermoregulation and body condition of an arid-zone bird. Glob Change Biol 18:3063–3070CrossRefGoogle Scholar
  17. Kearney MR, Porter WP, Murphy SA (2016) An estimate of the water budget for the endangered night parrot of Australia under recent and future climates. Clim Change Responses 3(1):14CrossRefGoogle Scholar
  18. Lighton JRB (2008) Measuring metabolic rates: a manual for scientists. Oxford University Press, OxfordCrossRefGoogle Scholar
  19. Londoño GA, Chappell MA, del Rosario Castañeda M, Jankowski JE, Robinson SK (2015) Basal metabolism in tropical birds: latitude, altitude, and the “pace of life”. Funct Ecol 29:338–346CrossRefGoogle Scholar
  20. Marder J, Gavrieli-Levin I (1986) Body and egg temperature regulation in incubating pigeons exposed to heat stress: the role of skin evaporation. Physiol Zool 69:532–538CrossRefGoogle Scholar
  21. McKechnie AE, Swanson DL (2010) Sources and significance of variation in basal, summit and maximal metabolic rates in birds. Curr Zool 56(6):741–758Google Scholar
  22. McKechnie AE, Wolf BO (2010) Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biol Let 6:253–256CrossRefGoogle Scholar
  23. McKechnie AE, Noakes MJ, Smit B (2015) Global patterns of seasonal acclimatization in avian resting metabolic rates. J Orn 156(1):367–376CrossRefGoogle Scholar
  24. McKechnie AE, Smit B, Whitfield MC, Noakes MJ, Talbot WA, Garcia M, Gerson AR, Wolf BO (2016a) Avian thermoregulation in the heat: evaporative cooling capacity in an archetypal desert specialist, Burchell’s sandgrouse (Pterocles burchelli). J Exp Biol 219:2137–2144CrossRefPubMedGoogle Scholar
  25. McKechnie AE, Whitfield MC, Smit B, Gerson AR, Smith EK, Talbot WA, McWhorter TJ, Wolf BO (2016b) Avian thermoregulation in the heat: efficient evaporative cooling allows for extreme heat tolerance in four southern Hemisphere columbids. J Exp Biol 219:2145–2155CrossRefPubMedGoogle Scholar
  26. McKechnie AE, Gerson AR, McWhorter TJ, Smith EK, Talbot WA, Wolf BO (2017) Avian thermoregulation in the heat: evaporative cooling in five Australian passerines reveals within-order biogeographic variation in heat tolerance. J Exp Biol 220(13):2436–2444CrossRefPubMedGoogle Scholar
  27. McWhorter TJ, Gerson AR, Talbot WA, Smith EK, McKechnie AE, Wolf BO (2018) Avian thermoregulation in the heat: evaporative cooling capacity and thermal tolerance in two Australian parrots. J Exp Biol 221(6):jeb168930CrossRefPubMedGoogle Scholar
  28. Noakes MJ, Smit B, Wolf BO, McKechnie AE (2013) Thermoregulation in African Green Pigeons (Treron calvus) and a re-analysis of insular effects on basal metabolic rate and heterothermy in columbid birds. J Comp Physiol B 183(7):969–982CrossRefPubMedGoogle Scholar
  29. Noy-Meir I (1973) Desert ecosystems: environment and producers. Annu Rev Ecol Syst 4:25–51CrossRefGoogle Scholar
  30. O’Connor RS, Wolf BO, Brigham RM, McKechnie AE (2017) Avian thermoregulation in the heat: efficient evaporative cooling in two southern African nightjars. J Comp Physiol B 187(3):477–491CrossRefPubMedGoogle Scholar
  31. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2009) nlme: Linear and nonlinear mixed effects models. R Package version 3.57Google Scholar
  32. Prinzinger R, Preßmar A, Schleucher E (1991) Body temperature in birds. Comp Biochem Physiol 99A(4):499–506CrossRefGoogle Scholar
  33. Scholander PF, Hock R, Walters V, Irving L (1950) Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation and basal metabolic rate. Biol Bull 99(2):259–271CrossRefPubMedGoogle Scholar
  34. Serventy DL (1971) Biology of desert birds. In: Farner DS, King JR (eds) Avian biology vol I. Academic Press, New York, pp 287–339Google Scholar
  35. Smit B, Whitfield MC, Talbot WA, Gerson AR, McKechnie AE, Wolf BO (2018) Avian thermoregulation in the heat: phylogenetic variation among avian orders in evaporative cooling capacity and heat tolerance. J Exp Biol 221(6):jeb174870CrossRefPubMedGoogle Scholar
  36. Smith EK, O’Neill J, Gerson AR, Wolf BO (2015) Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert doves and quail. J Exp Biol 218:3636–3646CrossRefPubMedGoogle Scholar
  37. Smith EK, O’Neill JJ, Gerson AR, McKechnie AE, Wolf BO (2017) Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert songbirds. J Exp Biol 220(18):3290–3300CrossRefPubMedGoogle Scholar
  38. Talbot WA, McWhorter TJ, Gerson AR, McKechnie AE, Wolf BO (2017) Avian thermoregulation in the heat: evaporative cooling capacity of arid-zone Caprimulgiformes from two continents. J Exp Biol 220(19):3488–3498CrossRefPubMedGoogle Scholar
  39. Taylor MR, Peacock F, Wanless RM (2015) The 2015 Eskom Red Data Book of Birds of South Africa, Lesotho and Swaziland. BirdLife South Africa, Johannesburg, South AfricaGoogle Scholar
  40. Thompson ML, Cunningham SJ, McKechnie AE (2018) Interspecific variation in avian thermoregulatory patterns and heat dissipation behaviours in a subtropical desert. Physiol Behav 188:311–323CrossRefPubMedGoogle Scholar
  41. Tieleman BI, Williams JB (2000) The adjustment of avian metabolic rates and water fluxes to desert environments. Physiol Biochem Zool 73(4):461–479CrossRefPubMedGoogle Scholar
  42. Tieleman BI, Williams JB (2002) Cutaneous and respiratory water loss in larks from arid and mesic environments. Physiol Biochem Zool 75(6):590–599CrossRefPubMedGoogle Scholar
  43. Tieleman BI, Williams JB, Buschur ME (2002) Physiological adjustments to arid and mesic environments in larks (Alaudidae). Physiol Biochem Zool 75(3):305–313CrossRefPubMedGoogle Scholar
  44. Tieleman BI, Williams JB, Bloomer P (2003a) Adaptation of metabolic rate and evaporative water loss along an aridity gradient. Proc R Soc Lond 270:207–214CrossRefGoogle Scholar
  45. Tieleman BI, Williams JB, Buschur ME, Brown CR (2003b) Phenotypic variation of larks along an aridity gradient: are desert birds more flexible? Ecology 84(7):1800–1815CrossRefGoogle Scholar
  46. Tieleman BI, Williams JB, Visser GH (2004) Energy and water budgets of larks in a life history perspective: parental effort varies with aridity. Ecology 85(5):1399–1410CrossRefGoogle Scholar
  47. Tracy CR, Welch WR, Pinshow B, Porter WP (2010) Properties of air: a manual for use in biophysical ecology, 4th edn. The University of Wisconsin Laboratory for Biophysical Ecology: Technical Report, no 4Google Scholar
  48. Trost CH (1972) Adaptations of horned larks (Eremophila alpestris) to hot environments. Auk 89:506–527Google Scholar
  49. 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
  50. Whitfield MC, Smit B, McKechnie AE, Wolf BO (2015) Avian thermoregulation in the heat: scaling of heat tolerance and evaporative cooling capacity in three southern African arid-zone passerines. J Exp Biol 218:1705–1714CrossRefPubMedGoogle Scholar
  51. Williams JB (1996) A phylogenetic perspective of evaporative water loss in birds. Auk 113(2):457–472CrossRefGoogle Scholar
  52. Williams JB (1999) Heat production and evaporative water loss of dune larks from the Namib desert. Condor 101:432–438CrossRefGoogle Scholar
  53. 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 203:3153–3159PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.DST-NRF Centre of Excellence at the FitzPatrick Institute, Department of Zoology and EntomologyUniversity of PretoriaPretoriaSouth Africa
  2. 2.South African Research Chair in Conservation Physiology, National Zoological GardenSouth African National Biodiversity InstitutePretoriaSouth Africa

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