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Feeling the heat: Elevated temperature affects male display activity of a lekking grassland bird


Autoři: Mishal Gudka aff001;  Carlos David Santos aff002;  Paul M. Dolman aff004;  José Mª Abad-Gómez aff005;  João Paulo Silva aff007
Působiště autorů: School of Biological Sciences, University of East Anglia, Norwich, United Kingdom aff001;  Núcleo de Teoria e Pesquisa do Comportamento, Universidade Federal do Pará, Belém, Brazil aff002;  Department of Migration, Max Planck Institute for Animal Behavior, Radolfzell, Germany aff003;  School of Environmental Sciences, University of East Anglia, Norwich, United Kingdom aff004;  Conservation Biology Research Group, Department of Anatomy, Cell Biology and Zoology, Faculty of Sciences, University of Extremadura, Badajoz, Spain aff005;  Servicio de Conservación de la Naturaleza y Áreas Protegidas, Consejería de Medio Ambiente y Rural, Políticas Agrarias y Territorio, Junta de Extremadura, Mérida, Badajoz, Spain aff006;  CIBIO/InBio, Centro de Investigação em Biodiversidade e Recursos Genéticos, Laboratório Associado, Universidade do Porto, Campus Agrário de Vairão, Vairão, Portugal aff007;  CIBIO/InBio, Centro de Investigação em Biodiversidade e Recursos Genéticos, Laboratório Associado, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, Lisbon, Portugal aff008
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0221999

Souhrn

Most species-climate models relate range margins to long-term mean climate but lack mechanistic understanding of the ecological or demographic processes underlying the climate response. We examined the case of a climatically limited edge-of-range population of a medium-sized grassland bird, for which climate responses may involve a behavioural trade-off between temperature stress and reproduction. We hypothesised that temperature will be a limiting factor for the conspicuous, male snort-call display behaviour, and high temperatures would reduce the display activity of male birds.

Using remote tracking technology with tri-axial accelerometers we classified and studied the display behaviour of 17 free-ranging male little bustards, Tetrax tetrax, at 5 sites in the Iberian Peninsula. Display behaviour was related to temperature using two classes of Generalized Additive Mixed Models (GAMMs) at different temporal resolutions. GAMMs showed that temperature, time of the day and Julian date explained variation in display behaviour within the day, with birds snort-calling significantly less during higher temperatures. We also showed that variation in daily snort-call activity was related to average daytime temperatures, with our model predicting an average decrease in daytime snort-call display activity of up to 10.4% for the temperature increases projected by 2100 in this region due to global warming. For lekking birds and mammals undertaking energetically-costly displays in a warming climate, reduced display behaviour could impact inter- and intra-sex mating behaviour interactions through sexual selection and mate choice mechanisms, with possible consequences on mating and reproductive success. The study provides a reproducible example for how accelerometer data can be used to answer research questions with important conservation inferences related to the impacts of climate change on a range of taxonomic groups.

Klíčová slova:

Biology and life sciences – Plant science – Organisms – Eukaryota – Engineering and technology – Psychology – Animals – Social sciences – Medicine and health sciences – Physiology – Vertebrates – Amniotes – Zoology – Behavior – Electronics – Earth sciences – Ecology and environmental sciences – Plant ecology – Ecology – Terrestrial environments – Animal behavior – Atmospheric science – Birds – Biological locomotion – Accelerometers – Animal sexual behavior – Mating behavior – Ornithology – Bird flight – Plant communities – Grasslands – Animal flight – Climatology – Climate change


Zdroje

1. Dawson TP, Jackson ST, House JI, Prentice IC, Mace GM. Beyond Predictions: Biodiversity Conservation in a Changing Climate. Science. 2011;332: 53–58 doi: 10.1126/science.1200303 21454781

2. Urban MC. Accelerating extinction risk from climate change. Science. 2015;348: 571–573. doi: 10.1126/science.aaa4984 25931559

3. Cahill AE, Aiello-Lammens ME, Fisher-Reid MC, Hua X, Karanewsky CJ, Yeong Ryu H, et al. How does climate change cause extinction? Proc R Soc—Biol Sci. 2012;280. doi: 10.1098/rspb.2012.1890 23075836

4. Huey RB, Kearney MR, Krockenberger A, Holtum JAM, Jess M, Williams SE. Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos Trans R Soc B. 2012;367: 1665–79 doi: 10.1098/rstb.2012.0005. doi: 10.1098/rstb.2012.0005 22566674

5. Buckley LB Huey RB. Temperature extremes: geographic patterns, recent changes, and implications for organismal vulnerabilities. Glob Change Biol. 2016;22: 3829–3842.

6. Pearson RG, Dawson TP. Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Glob Ecol Biogeogr. 2003;12: 361–371. doi: 10.1046/j.1466-822X.2003.00042.x

7. Araújo MB, Pearson RG, Thuiller W, Erhard M. Validation of species–climate impact models under climate change. Glob Change Biol. 2005;11: 1504–1513. doi: 10.1111/j.1365-2486.2005.01000.x

8. Mustin K, Sutherland WJ, Gill JA. The complexity of predicting climate-induced ecological impacts. Clim Res. 2007;35: 165–175.

9. Dillon ME, Wang G, Huey RB. Global metabolic impacts of recent climate warming. Nature. 2010;467: 704–706. doi: 10.1038/nature09407 20930843

10. Welbergen JA, Klose SM, Markus N, Eby P. Climate change and the effects of temperature extremes on Australian flying-foxes. Proc Biol Sci. 2008;275: 419–425. doi: 10.1098/rspb.2007.1385 18048286

11. Rastogui SC. Essentials of Animal Physiology, 4th edn. New Age Int New Delhi India. 2007;

12. Boyles JG, Seebacher F, Smit B, McKechnie A.E. Adaptive thermoregulation in endotherms may alter responses to climate change. Integr Comp Biol. 2011;51: 676–690. doi: 10.1093/icb/icr053 21690108

13. Rezende EL, Cortés A, Bacigalupe LD, Nespolo RF, Bozinovic F. Ambient temperature limits above-ground activity of the subterranean rodent Spalacopus cyanus. J Arid Environ. 2003;55: 63–74. doi: 10.1016/S0140-1963(02)00259-8

14. Hill RA. Thermal constraints on activity scheduling and habitat choice in baboons. Am J Phys Anthropol. 2006;129: 242–249. doi: 10.1002/ajpa.20264 16323181

15. Sinervo B, Méndez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans E, Cruz MV-S, et al. Erosion of Lizard Diversity by Climate Change and Altered Thermal Niches. Science. 2010;328: 894–899 doi: 10.1126/science.1184695. 20466932

16. Chown SL, Hoffmann AA, Kristensen TN MJA Jr., Stenseth NChr, Pertoldi C. Adapting to climate change: a perspective from evolutionary physiology. Clim Res. 2010;43: 3–15. doi: 10.3354/cr00879

17. Somero GN. The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers.’ J Exp Biol. 2010;213: 912–920. doi: 10.1242/jeb.037473 20190116

18. Woodin SA, Hilbish TJ, Helmuth B, Jones S, Wethey D. Climate change, species distribution models, and physiological performance metrics: predicting when biogeographic models are likely to fail. Ecol Evol. 2013;3: 3334–3346. doi: 10.1002/ece3.680 24223272

19. Mathewson PD, Moyer-Horner L, Beever EA, Briscoe NJ, Kearney M, Yahn JM, et al. Mechanistic variables can enhance predictive models of endotherm distributions: the American pika under current, past, and future climates. Glob Change Biol. 2016;23: 1048–1064.

20. Alatalo RV, Höglund J, Lundberg AJ. Sutherland W. Evolution of black grouse leks: female preferences benefit males in larger leks. Behav Ecol. 1992;3: 53–59. doi: 10.1093/beheco/3.1.53

21. Loyau A, Lacroix F. Watching sexy displays improves hatching success and offspring growth through maternal allocation. Proc R Soc B. 2010;277: DOI: 10.1098/rspb.2010.0473. doi: 10.1098/rspb.2010.0473 20538650

22. Morales MB, Casas F, Morena EG de la, Ponjoan A, Calabuig G, Martínez-Padilla J, et al. Density dependence and habitat quality modulate the intensity of display territory defence in an exploded lekking species. Behav Ecol Sociobiol. 2014;68: 1493–1504. doi: 10.1007/s00265-014-1758-z

23. Apollonio M, Festa-Bianchet M, Mari F. Correlates of copulatory success in a fallow deer lek. Behav Ecol Sociobiol. 1989;25: 89–97. doi: 10.1007/BF00302925

24. Apollonio M, Festa-Bianchet M, Mari F, Mattioli S, Sarno B. To lek or not to lek: mating strategies of male fallow deer. Behav Ecol. 1992;3: 25–31. doi: 10.1093/beheco/3.1.25

25. McComb KE. Female choice for high roaring rates in red deer, Cervus elaphus. Anim Behav. 1991;41: 79–88. doi: 10.1016/S0003-3472(05)80504-4

26. Isvaran Kavita, Jhala Yadavendradev. Variation in Lekking Costs in Blackbuck (Antilope cervicapra): Relationship to Lek-Territory Location and Female Mating Patterns. Behaviour. 2000;137: 547–563.

27. Jiguet F, Bretagnolle V. Courtship behaviour in a lekking species: individual variations and settlement tactics in male little bustard. Behav Processes. 2001;55: 107–118. doi: 10.1016/S0376-6357(01)00173-5 11470502

28. Chargé R, Saint Jalme M, Lacroix F, Cadet A, Sorci G. Male health status, signalled by courtship display, reveals ejaculate quality and hatching success in a lekking species. J Anim Ecol. 2010;79: 843–850. doi: 10.1111/j.1365-2656.2010.01696.x 20412349

29. Chargé R, Teplitsky C, Hingrat Y, Saint Jalme M, Lacroix F, Sorci G. Quantitative genetics of sexual display, ejaculate quality and size in a lekking species. J Anim Ecol. 2013;82: 399–407. doi: 10.1111/1365-2656.12023 23228188

30. Silva JP, Catry I, Palmeirim JM, Moreira F. Freezing heat: thermally imposed constraints on the daily activity patterns of a free-ranging grassland bird. ECOSPHERE. 2015;6: 1–13.

31. Christensen JH, Kumar K, Aldrian E, An S-I, Cavalcanti IFA, Castro M de, et al. Climate Phenomena and their Relevance for Future Regional Climate Change. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change; 2013 pp. 1217–1308.

32. Jiguet F, Bretagnolle V. Sexy males and choosy females on exploded leks: correlates of male attractiveness in the Little Bustard. Behav Processes. 2014;103: 246–255. doi: 10.1016/j.beproc.2014.01.008 24440985

33. Hebblewhite M, Haydon DT. Distinguishing technology from biology: a critical review of the use of GPS telemetry data in ecology. Philos Trans R Soc B Biol Sci. 2010;365: 2303–2312. doi: 10.1098/rstb.2010.0087 20566506

34. BirdLife I. Species factsheet: Tetrax tetrax. Downloaded from http://www.birdlife.org on 25/02/2017; 2017.

35. Wolff A, Paul J-P, Martin J-L, Bretagnolle V. The benefits of extensive agriculture to birds: the case of the little bustard. J Appl Ecol. 2001;38: 963–975. doi: 10.1046/j.1365-2664.2001.00651.x

36. Delgado MP, Traba J, Morales MB. Climate Niche Constraints in Two Coexisting Steppe Birds: The Little and the Great Bustards. BioOne. 2011;64: 223–238.

37. Morales MB, Traba J, Carriles E, Delgado MP, Garci-a de la Morena EL. Sexual differences in microhabitat selection of breeding little bustards Tetrax tetrax: Ecological segregation based on vegetation structure. Acta Oecologica. 2008;34: 345. doi: 10.1016/j.actao.2008.06.009

38. Ribeiro PF, Santos JL, Bugalho MN, Santana J, Reino L, Beja P, et al. Modelling farming system dynamics in High Nature Value Farmland under policy change. Agr Ecosyst Env. 2014;183: 138–144. doi: 10.1016/j.agee.2013.11.002

39. Iñigo A, Barov B. Action plan for the little bustard Tetrax tetrax in the European Union. SEO|BirdLife and BirdLife International for the European Commission; 2010.

40. Rivas-Martínez S. Climatic Data of Portugal. CIF–Phytosociological Research Center, Madrid.; 2001.

41. Blondel J. The Mediterranean region: biological diversity through time and spaces [Internet]. Oxford University Press; 2010. Available: http://library.wur.nl/WebQuery/clc/1929515

42. Silva J, Estanque B, Moreira F, Palmeirim J. Population density and use of grasslands by female Little Bustards during lek attendance, nesting and brood-rearing. J Ornithol Jan2014. 2014;155: 53. doi: 10.1007/s10336-013-0986-8

43. Silva JP, Moreira F, Palmeirim JM. Spatial and temporal dynamics of lekking behaviour revealed by high-resolution GPS tracking. Anim Behav. 2017;129: 197–204. doi: 10.1016/j.anbehav.2017.05.016

44. Schulz H. Grundlagenforschung zur Biologie der Zwergtrappe Tetrax tetrax. 1985.

45. Caccamise DF, Hedin RS. An Aerodynamic Basis for Selecting Transmitter Loads in Birds. Wilson Bull. 1985;97: 306–318.

46. Wilson RP, Grémillet D, Syder J, Kierspel MAM, Garthe S, Weimerskirch H, et al. Remote-sensing systems and seabirds: their use, abuse and potential for measuring marine environmental variables. Mar Ecol Prog Ser. 2002; 241–261.

47. Barron DG, Brawn JD, Weatherhead PJ. Meta-analysis of transmitter effects on avian behaviour and ecology. Methods Ecol Evol. 2010;1: 180–187. doi: 10.1111/j.2041-210X.2010.00013.x

48. Marcelino J, Moreira F, Mañosa S, Cuscó F, Morales MB, Morena ELGDL, et al. Tracking data of the Little Bustard Tetrax tetrax in Iberia shows high anthropogenic mortality. Bird Conserv Int. 2018;28: 509–520. doi: 10.1017/S095927091700051X

49. Pennycuick CJ, Fast PLF, Ballerstädt N, Rattenborg N. The effect of an external transmitter on the drag coefficient of a bird’s body, and hence on migration range, and energy reserves after migration. J Ornithol. 2012;153: 633–644. doi: 10.1007/s10336-011-0781-3

50. Vandenabeele SP, Grundy E, Friswell MI, Grogan A, Votier SC, Wilson RP. Excess Baggage for Birds: Inappropriate Placement of Tags on Gannets Changes Flight Patterns. PLOS ONE. 2014;9: e92657. doi: 10.1371/journal.pone.0092657 24671007

51. Ponjoan A, Ponjoan A, Bota G, De La Morena ELG, Morales MB, Wolff A, et al. Adverse Effects of Capture and Handling Little Bustard. J Wildl Manag. 2008;72: 315. doi: 10.2193/2006-443

52. Nathan R, Spiegel O, Fortmann-Roe S, Harel R, Wikelski M, Getz WM. Using tri-axial acceleration data to identify behavioral modes of free-ranging animals: general concepts and tools illustrated for griffon vultures. J Exp Biol. 2012;215. doi: 10.1242/jeb.058602 22357592

53. Brown DD, Kays R, Wikelski M, Wilson R, Klimley AP. Observing the unwatchable through acceleration logging of animal behavior. Anim Biotelemetry. 2013;1: 20. doi: 10.1186/2050-3385-1-20

54. Pagano AM, Rode KD, Cutting A, Owen MA, Jensen S, Ware JV, et al. Using tri-axial accelerometers to identify wild polar bear behaviors. Endanger Species Res. 2017;32: 19–33.

55. Studd EK, Landry-Cuerrier M, Menzies AK, Boutin S, McAdam AG, Lane JE, et al. Behavioral classification of low frequency acceleration and temperature data from a free ranging small mammal. Ecol Evol. 2018;9: 619–630. doi: 10.1002/ece3.4786 30680142

56. Resheff YS, Rotics S, Harel R, Spiegel O, Nathan R. AcceleRater: a web application for supervised learning of behavioral modes from acceleration measurements. Mov Ecol. 2014;2: 27. doi: 10.1186/s40462-014-0027-0 25709835

57. Resheff Y. AcceleRater Software Manual. http://accapp.move-ecol-minerva.huji.ac.il/static/pdf/draft.pdf; 2014.

58. Maindonald J. Smoothing Terms in GAM Models [Internet]. 2010.

59. Wood S, Scheipl F. Generalized Additive Mixed Models using “mgcv” and “lme4” [Internet]. 2017. Available: https://cran.r-project.org/web/packages/gamm4/gamm4.pdf

60. Muñoz-Mas R, Costa RMS, Alcaraz-Hernández JD, Martínez-Capel F. Microhabitat competition between Iberian fish species and the endangered Júcar nase (Parachondrostoma arrigonis; Steindachner, 1866). J Ecohydraulics. 2017;2: 3–15.

61. Granadeiro JP, Andrade J, Palmeirim JM. Modelling the distribution of shorebirds in estuarine areas using generalised additive models. J Sea Res. 2004;52: 227–240. doi: 10.1016/j.seares.2004.01.005

62. Geisser S. Predictive Inference [Internet]. Chapman and Hall/CRC; 1993. Available: https://www.crcpress.com/Predictive-Inference/Geisser/p/book/9780412034718

63. IPCC. Fifth Assessment Report, Climate Change 2013: The Physical Science Basis [Internet]. http://www.ipcc.ch/report/ar5/wg1/; 2013. Available: http://www.ipcc.ch/report/ar5/wg1/

64. Ponjoan A, Bota G, Mañosa S. Ranging behaviour of little bustard males, Tetrax tetrax, in the lekking grounds. Behav Processes. 2012;91: 35–40. doi: 10.1016/j.beproc.2012.05.005 22626823

65. Isvaran K. Female Grouping Best Predicts Lekking in Blackbuck (Antilope cervicapra). Behav Ecol Sociobiol. 2005;57: 283–294.

66. Höglund J, Lundberg A. Sexual selection in a monomorphic lek-breeding bird: correlates of male mating success in the great snipe Gallinago media. Behav Ecol Sociobiol. 1987;21: 211–216. doi: 10.1007/BF00292501

67. Morales MB, Alonso J, Martín C et al, Ethol J. Male sexual display and attractiveness in the great bustard Otis tarda: the role of body condition. J Ethol. 2003;21: 51–56. doi: 10.1007/s10164-002-0076-5

68. Alonso JC, Magaña M. Correlates of male mating success in great bustard leks: the effects of age, weight, and display effort. Behav Ecol Sociobiol. 2010;64. doi: 10.1007/s00265-010-0972-6

69. Estrada A, Delgado MP, Arroyo B, Traba J, Morales MB. Forecasting Large-Scale Habitat Suitability of European Bustards under Climate Change: The Role of Environmental and Geographic Variables. PLOS ONE. 2016;11: e0149810. doi: 10.1371/journal.pone.0149810 26939133

70. Terrien J, Perret M, Aujard F. Behavioral thermoregulation in mammals: a review. Front Biosci Landmark Ed. 2011;16: 1428–1444. 21196240


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