Chronic, sublethal effects of high temperatures will cause severe declines in southern African arid-zone birds during the 21st century
Edited by William J. Bond, University of Cape Town, Cape Town, South Africa, and approved May 22, 2019 (received for review December 14, 2018)
Significance
We synthesized physiological and behavioral data to evaluate the risks of acute, lethal effects of extreme heat events versus the sublethal costs of chronic exposure to sustained hot weather for birds inhabiting southern Africa’s Kalahari Desert over the course of the 21st century. The risk of mass mortality events similar to those predicted for the American southwest and sometimes observed in Australia will remain low for Kalahari birds. However, the sublethal costs of chronic exposure, manifested as progressive loss of body condition, delayed fledging, reduced fledging size, and outright breeding failure, will likely drive major population declines. We anticipate that much of the Kalahari’s avian biodiversity will be lost by the end of the century.
Abstract
Birds inhabiting hot, arid regions are among the terrestrial organisms most vulnerable to climate change. The potential for increasingly frequent and intense heat waves to cause lethal dehydration and hyperthermia is well documented, but the consequences of sublethal fitness costs associated with chronic exposure to sustained hot weather remain unclear. Using data for species occurring in southern Africa’s Kalahari Desert, we mapped exposure to acute lethal risks and chronic sublethal fitness costs under past, present, and future climates. For inactive birds in shaded microsites, the risks of lethal dehydration and hyperthermia will remain low during the 21st century. In contrast, exposure to conditions associated with chronic, sublethal costs related to progressive body mass loss, reduced nestling growth rates, or increased breeding failure will expand dramatically. For example, by the 2080s the region will experience 10–20 consecutive days per year on which Southern Pied Babblers (Turdoides bicolor) will lose ∼4% of body mass per day, conditions under which this species’ persistence will be extremely unlikely. Similarly, exposure to air temperature maxima associated with delayed fledging, reduced fledgling size, and breeding failure will increase several-fold in Southern Yellow-billed Hornbills (Tockus leucomelas) and Southern Fiscals (Lanius collaris). Our analysis reveals that sublethal costs of chronic heat exposure are likely to drive large declines in avian diversity in the southern African arid zone by the end of the century.
Acknowledgments
We thank two anonymous reviewers whose comments improved the quality of the manuscript. This work is based on research supported by the National Research Foundation of South Africa Grant 110506 (to A.E.M.) and the DST-NRF Centre of Excellence at the FitzPatrick Institute. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Research Foundation.
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References
1
W. R. Dawson, K. Schmidt-Nielsen, “Terrestrial animals in dry heat: desert birds” in Handbook of Physiology: Adaptation to the Environment, Dill DB, Ed. (American Physiological Society, Washington, DC, 1964), pp. 481–492.
2
D. L. Serventy, “Biology of desert birds” in Avian Biology, D. S. Farner, J. R. King, Eds. (Academic Press, New York, 1971), vol. I, pp. 287–339.
3
K. J. Iknayan, S. R. Beissinger, Collapse of a desert bird community over the past century driven by climate change. Proc. Natl. Acad. Sci. U.S.A. 115, 8597–8602 (2018).
4
A. E. McKechnie, B. O. Wolf, Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biol. Lett. 6, 253–256 (2010).
5
T. P. Albright et al., Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration. Proc. Natl. Acad. Sci. U.S.A. 114, 2283–2288 (2017).
6
J. A. Welbergen, S. M. Klose, N. Markus, P. Eby, Climate change and the effects of temperature extremes on Australian flying-foxes. Proc. Biol. Sci. 275, 419–425 (2008).
7
K. L. du Plessis, R. O. Martin, P. A. R. Hockey, S. J. Cunningham, A. R. Ridley, 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, 3063–3070 (2012).
8
I. Catry, T. Catry, P. Patto, A. M. Franco, F. Moreira, Differential heat tolerance in nestlings suggests sympatric species may face different climate change risks. Clim. Res. 66, 13–24 (2015).
9
S. J. Cunningham, R. O. Martin, C. L. Hojem, P. A. R. Hockey, 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, e74613 (2013).
10
T. M. F. N. van de Ven, “Implications of climate change on the reproductive success of the Southern Yellow-billed Hornbill Tockus leucomelas,” PhD thesis, University of Cape Town, Cape Town, South Africa (2017).
11
E. M. Wiley, A. R. Ridley, The effects of temperature on offspring provisioning in a cooperative breeder. Anim. Behav. 117, 187–195 (2016).
12
S. J. Cunningham, A. C. Kruger, M. P. Nxumalo, P. A. R. Hockey, Identifying biologically meaningful hot-weather events using threshold temperatures that affect life-history. PLoS One 8, e82492 (2013).
13
L. O’Connor, Death Valley records planet’s hottest month, scientists warn it may become uninhabitable. Huffington Post (2018). https://www.huffingtonpost.com/entry/death-valley-records-planets-hottest-month-again_us_5b61e5eae4b0b15aba9f183b.
14
E. K. Smith, J. O’Neill, A. R. Gerson, B. O. Wolf, Avian thermoregulation in the heat: Resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert doves and quail. J. Exp. Biol. 218, 3636–3646 (2015).
15
M. C. Whitfield, B. Smit, A. E. McKechnie, B. O. Wolf, Avian thermoregulation in the heat: Scaling of heat tolerance and evaporative cooling capacity in three southern African arid-zone passerines. J. Exp. Biol. 218, 1705–1714 (2015).
16
A. E. McKechnie et al., Avian thermoregulation in the heat: Efficient evaporative cooling allows for extreme heat tolerance in four southern hemisphere columbids. J. Exp. Biol. 219, 2145–2155 (2016).
17
M. L. Thompson, S. J. Cunningham, A. E. McKechnie, Interspecific variation in avian thermoregulatory patterns and heat dissipation behaviours in a subtropical desert. Physiol. Behav. 188, 311–323 (2018).
18
D. E. Robinson, G. S. Campbell, J. R. King, An evaluation of heat exchange in small birds. J. Comp. Physiol. B 105, 153–166 (1976).
19
G. S. Bakken, A heat transfer analysis of animals: Unifying concepts and the application of metabolism chamber data to field ecology. J. Theor. Biol. 60, 337–384 (1976).
20
B. I. Tieleman, H. J. van Noordwijk, J. B. Williams, Nest site selection in a hot desert: Trade-off between microclimate and predation risk? Condor 110, 116–124 (2008).
21
G. S. Grant, Avian incubation: Egg temperature, nest humidity, and behavioral thermoregulation in a hot environment. Ornithol. Monogr. 30, 1–100 (1982).
22
N. Cleere, “Family Caprimulgidae (nightjars) ” in Handbook of the Birds of the World Barn-owls to Hummingbirds, J. del Hoyo, A. Elliot, J. Sargatal, Eds. (Lynx Edicions, Barcelona, 1999), vol. 5, pp. 302–386.
23
R. S. O’Connor, R. M. Brigham, A. E. McKechnie, Roosting in exposed microsites by a nocturnal bird, the rufous-cheeked nightjar: Implications for water balance under current and future climate conditions. Can. J. Zool. 96, 1122–1129 (2018).
24
S. J. Cunningham, R. O. Martin, P. A. Hockey, Can behaviour buffer the impacts of climate change on an arid-zone bird? Ostrich 86, 119–126 (2015).
25
S. Abdu, A. E. McKechnie, A. T. Lee, S. J. Cunningham, Can providing shade at water points help Kalahari birds beat the heat? J. Arid Environ. 152, 21–27 (2018).
26
B. Smit, S. Woodborne, B. O. Wolf, A. E. McKechnie, Differences in the use of surface water resources by desert birds is revealed using isotopic tracers. Auk 136, 1–13 (2019).
27
A. R. Ridley, N. J. Raihani, Variable postfledging care in a cooperative bird: Causes and consequences. Behav. Ecol. 18, 994–1000 (2007).
28
J. L. Gardner, T. Amano, W. J. Sutherland, M. Clayton, A. Peters, Individual and demographic consequences of reduced body condition following repeated exposure to high temperatures. Ecology 97, 786–795 (2016).
29
C. K. Ghalambor, T. E. Martin, Fecundity-survival trade-offs and parental risk-taking in birds. Science 292, 494–497 (2001).
30
H. Weimerskirch, P. A. Prince, L. Zimmermann, Chick provisioning by the yellow‐nosed albatross Diomedea chlororhynchos: Response of foraging effort to experimentally increased costs and demands. Ibis 142, 103–110 (2000).
31
F. Engelbrecht et al., Projections of rapidly rising surface temperatures over Africa under low mitigation. Environ. Res. Lett. 10, 085004 (2015).
32
J. Marder, U. Arieli, Heat balance of acclimated pigeons Columba livia exposed to temperatures of up to 60°C Ta. Comp. Biochem. Physiol. 91A, 165–170 (1988).
33
B. I. Tieleman, J. B. Williams, F. LaCroix, P. Paillat, Physiological responses of Houbara bustards to high ambient temperatures. J. Exp. Biol. 205, 503–511 (2002).
34
A. E. McKechnie, B. O. Wolf, Partitioning of evaporative water loss in white-winged doves: Plasticity in response to short-term thermal acclimation. J. Exp. Biol. 207, 203–210 (2004).
35
M. J. Noakes, B. O. Wolf, A. E. McKechnie, Seasonal and geographical variation in heat tolerance and evaporative cooling capacity in a passerine bird. J. Exp. Biol. 219, 859–869 (2016).
36
M. M. Mariette, K. L. Buchanan, Prenatal acoustic communication programs offspring for high posthatching temperatures in a songbird. Science 353, 812–814 (2016).
37
T. Piersma, J. Drent, Phenotypic flexibility and the evolution of organismal design. Trends Ecol. Evol. 18, 228–233 (2003).
38
A. E. McKechnie et al., Avian thermoregulation in the heat: Evaporative cooling capacity in an archetypal desert specialist, Burchell’s sandgrouse (Pterocles burchelli). J. Exp. Biol. 219, 2137–2144 (2016).
39
R. S. O’Connor, B. O. Wolf, R. M. Brigham, A. E. McKechnie, Avian thermoregulation in the heat: Efficient evaporative cooling in two southern african nightjars. J. Comp. Physiol. B 187, 477–491 (2017).
40
W. A. Talbot, T. J. McWhorter, A. R. Gerson, A. E. McKechnie, B. O. Wolf, Avian thermoregulation in the heat: Evaporative cooling capacity of arid-zone caprimulgiformes from two continents. J. Exp. Biol. 220, 3488–3498 (2017).
41
T. J. McWhorter et al., Avian thermoregulation in the heat: Evaporative cooling capacity and thermal tolerance in two Australian parrots. J. Exp. Biol. 221, jeb168930 (2018).
42
B. Smit et al., Avian thermoregulation in the heat: Phylogenetic variation among avian orders in evaporative cooling capacity and heat tolerance. J. Exp. Biol. 221, jeb174870 (2018).
43
W. W. Weathers, Energetics and thermoregulation by small passerines of the humid, lowland tropics. Auk 114, 341–353 (1997).
44
E. K. Smith, J. J. O’Neill, A. R. Gerson, A. E. McKechnie, B. O. Wolf, Avian thermoregulation in the heat: Resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert songbirds. J. Exp. Biol. 220, 3290–3300 (2017).
45
A. Muñoz-Garcia, R. M. Cox, J. B. Williams, Phenotypic flexibility in cutaneous water loss and lipids of the stratum corneum in house sparrows (Passer domesticus) following acclimation to high and low humidity. Physiol. Biochem. Zool. 81, 87–96 (2008).
46
T. C. M. Hoffman, G. E. Walsberg, Inhibiting ventilatory evaporation produces an adaptive increase in cutaneous evaporation in mourning doves Zenaida macroura. J. Exp. Biol. 202, 3021–3028 (1999).
47
P. Lloyd, Rainfall as a breeding stimulus and clutch size determinant in South African arid‐zone birds. Ibis 141, 637–643 (1999).
48
N. J. van Wilgen, V. Goodall, S. Holness, S. L. Chown, M. A. McGeoch, Rising temperatures and changing rainfall patterns in South Africa’s national parks. Int. J. Climatol. 36, 706–721 (2016).
49
H. Q. Crick, The impact of climate change on birds. Ibis 146, 48–56 (2004).
50
R. Olinger, “How does temperature affect Fork-tailed Drongo, Dicrurus adsimilis, foraging effort, nestling provisioning and growth rates?” MSc thesis, University of Cape Town, Cape Town, South Africa (2017).
51
N. B. Pattinson, B. Smit, Seasonal behavioral responses of an arid-zone passerine in a hot environment. Physiol. Behav. 179, 268–275 (2017).
52
A. E. McKechnie, P. A. R. Hockey, B. O. Wolf, Feeling the heat: Australian landbirds and climate change. Emu 112, i–vii (2012).
53
J. M. Carroll, C. A. Davis, R. D. Elmore, S. D. Fuhlendorf, E. T. Thacker, Thermal patterns constrain diurnal behavior of a ground‐dwelling bird. Ecosphere 6, 1–15 (2015).
54
E. K. Edwards, N. J. Mitchell, A. R. Ridley, The impact of high temperatures on foraging behaviour and body condition in the Western Australian Magpie Cracticus tibicen dorsalis. Ostrich 86, 137–144 (2015).
55
A. J. Bladon et al., Behavioural thermoregulation and climatic range restriction in the globally threatened Ethiopian Bush‐crow Zavattariornis stresemanni. Ibis, (2018).
56
C. Salaberria, P. Celis, I. López‐Rull, D. Gil, Effects of temperature and nest heat exposure on nestling growth, dehydration and survival in a Mediterranean hole‐nesting passerine. Ibis 156, 265–275 (2014).
57
L. Clark, Thermal constraints on foraging in adult European starlings. Oecologia 71, 233–238 (1987).
58
S. A. Oswald, S. Bearhop, R. W. Furness, B. Huntley, K. C. Hamer, Heat stress in a high-latitude seabird: Effects of temperature and food supply on bathing and nest attendance of great skuas Catharacta skua. J. Avian Biol. 39, 163–169 (2008).
59
B. G. Lovegrove, The Living Deserts of Southern Africa (Fernwood Press, Vlaeberg, South Africa, 1993).
60
A. Moise, D. Hudson, Probabilistic predictions of climate change for Australia and southern Africa using the reliability ensemble average of IPCC CMIP3 model simulations. J. Geophys. Res. D Atmospheres 113, D15113 (2008).
61
G. Flato, et al. “Evaluation of climate models” in Climate Change 2013–The Physical Science Basis Working Group I Contribution to Fifth Assessment Report Intergovernmental Panel on Climate Change T. F. Stocker et al., Eds. (Cambridge Univ Press, Cambridge, 2013), pp. 741–866.
62
IPCC, Climate Change 2014 Synthesis Report. Contribution of working groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (IPCC, Geneva, Switzerland, 2014).
63
F. Brient, T. Schneider, Constraints on climate sensitivity from space-based measurements of low-cloud reflection. J. Clim. 29, 5821–5835 (2016).
64
P. T. Brown, K. Caldeira, Greater future global warming inferred from Earth’s recent energy budget. Nature 552, 45–50 (2017).
65
C. Zhai, J. H. Jiang, H. Su, Long‐term cloud change imprinted in seasonal cloud variation: More evidence of high climate sensitivity. Geophys. Res. Lett. 42, 8729–8737 (2015).
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Cover image: Pictured is the head of the tsetse fly Glossina morsitans, which transmits trypanosomiasis to humans and livestock in sub-Saharan Africa. Neeraj Soni et al. characterized the physiological responses of 7 classes of olfactory sensilla in the antenna of G. morsitans, which relies on olfactory cues to find hosts. The findings may help devise tsetse fly control measures. See the article by Soni et al. on pages 14300–14308. Image courtesy of J. Sebastian Chahda.
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© 2019. Published under the PNAS license.
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Published online: June 24, 2019
Published in issue: July 9, 2019
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Acknowledgments
We thank two anonymous reviewers whose comments improved the quality of the manuscript. This work is based on research supported by the National Research Foundation of South Africa Grant 110506 (to A.E.M.) and the DST-NRF Centre of Excellence at the FitzPatrick Institute. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Research Foundation.
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This article is a PNAS Direct Submission.
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The authors declare no conflict of interest.
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