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Environmental and social determinants of anuran lekking behavior: intraspecific variation in populations at thermal extremes

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Abstract

Environmental and social factors are critical to determine the timing and duration of lekking behavior since they provide species with signs to maximize benefits over costs in sexual displays. However, these factors have rarely been studied under different environmental conditions, and thus, it remains unclear whether exogenous factors affecting group displays show a general species-specific pattern or whether they are population-specific. Using audio-trapping techniques, we compared factors influencing the daily occurrence and duration of lekking behavior in two populations of Hyla molleri and two populations of Hyla meridionalis located at the thermal extremes (coldest vs. hottest) of their Iberian distribution range. From 12,240 hourly recordings over one season, multimodel inference revealed that the major determinants of chorus occurrence were similar between populations and species (i.e., chorus size the previous day, daytime air temperature, relative humidity, and barometric pressure), and accounted for 51–79 % of its deviance. In contrast, the major determinants of chorus duration differed between populations and species (i.e., chorus size, number of day, and air temperature and relative humidity at the onset of the chorus), and accounted for 38–69 % of its variance. Our findings suggest that the decision making related to lek attendance is environment-dependent, takes place at time between lekking events, and is associated with exogenous factors that may be both stable across species ranges and population-specific when populations are under different climatic conditions. This intraspecific variation might be underlain by plasticity mechanisms providing tree frogs with means to cope with changing environments. Moreover, social facilitation related to male-male acoustic competition seems to play a relevant role on the daily time invested by males in lek attendance.

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References

  • Acevedo MA, Villanueva-Rivera LJ (2006) Using automated digital recording systems as effective tools for the monitoring of birds and amphibians. Wildlife Soc B 34:211–214

    Article  Google Scholar 

  • AEMET (2008) Resumen anual climatológico 2007. Agencia Estatal de Meteorología. Ministerio de Medio Ambiente y Medio Rural y Marino, Madrid

    Google Scholar 

  • Alexander RD (1961) Aggressiveness, territoriality, and sexual behavior in field crickets (Orthoptera: Gryllidae). Behaviour 17:130–223

    Article  Google Scholar 

  • Baines D (1996) Seasonal variation in lek attendance and lekking behaviour by male Black Grouse Tetrao tetrix. Ibis 138:177–180

    Article  Google Scholar 

  • Barbadillo LJ, Lapena M (2003) Hibridación natural de Hyla arborea (Linnaeus, 1758) e Hyla meridionalis (Boettger, 1874) en la Península Ibérica. Munibe 16:140–145

    Google Scholar 

  • Beebee TJC (1995) Amphibian breeding and climate. Nature 374:219–220

    Article  CAS  Google Scholar 

  • Berg KS, Brumfield RT, Apanius V (2006) Phylogenetic and ecological determinants of the neotropical dawn chorus. Proc R Soc Lond B 273:999–1005

    Article  CAS  Google Scholar 

  • Blair WF (1961) Calling and spawning seasons in a mixed population of anurans. Ecology 42:99–110

    Article  Google Scholar 

  • Blankenhorn HJ (1972) Meteorological variables affecting onset and duration of calling in Hyla arborea L. and Bufo calamita calamita Laur. Oecologia 9:223–234

    Article  Google Scholar 

  • Blaustein AR, Belden LK, Olson DH, Green DM, Root TL, Kiesecker JM (2001) Amphibian breeding and climate change. Conserv Biol 15:1804–1809

    Article  Google Scholar 

  • Bosch J, Márquez R (2001) Call timing in male-male acoustical interactions and female choice in the midwife toad Alytes obstetricans. Copeia 2001:169–177

    Article  Google Scholar 

  • Bradbury JW (1981) The evolution of leks. In: Alexander RD, Tinkle DW (eds) Natural selection and social behavior. Chiron, New York, pp 138–169

    Google Scholar 

  • Bridges AS, Dorcas ME (2000) Temporal variation in anuran calling behavior: implications for surveys and monitoring programs. Copeia 2000:587–592

    Article  Google Scholar 

  • Brooke PN, Alford RA, Schwarzkopf L (2000) Environmental and social factors influence chorusing behaviour in a tropical frog: examining various temporal and spatial scales. Behav Ecol Sociobiol 49:79–87

    Article  Google Scholar 

  • Broquet T, Jaquiéry J, Perrin N (2009) Opportunity for sexual selection and effective population size in the lek-breeding European treefrog (Hyla arborea). Evolution 63:674–683

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Burnham KP, Anderson DR (2004) Multimodel inference. Understanding AIC and BIC in model selection. Sociol Meth Res 33:261–304

    Article  Google Scholar 

  • Cambron ME, Bowker RG (2006) An automated digital sound recording system: the Amphibulator. Proceeding of the Eighth IEEE International Symposium on Multimedia, San Diego, pp 592–600

    Google Scholar 

  • Capranica RR (1966) Vocal response of the bullfrog to natural and synthetic mating calls. J Acoust Soc Am 40:1131–1139

    Article  Google Scholar 

  • Castellano S, Zanollo V, Marconi V, Berto G (2009) The mechanisms of sexual selection in a lek-breeding anuran, Hyla intermedia. Anim Behav 77:213–224

    Article  Google Scholar 

  • Chatfield C (2003) The analysis of time series: an introduction, 6th edn. Chapman & Hall, London

    Google Scholar 

  • Clutton-Brock TH, Deutsch JC, Nefdt RJC (1993) The evolution of ungulate leks. Anim Behav 46:1121–1138

    Article  Google Scholar 

  • Cramer JS (1999) Predictive performance of the binary logit model in unbalanced samples. J R Stat Soc 48:85–89

    Article  Google Scholar 

  • Cree A (1989) Relationship between environmental conditions and nocturnal activity of the terrestrial frog, Leiopelma archeyi. J Herpetol 23:61–68

    Article  Google Scholar 

  • Crespo EG, Oliveira ME, Rosa HD, Paillette M (1989) Mating calls of the Iberian midwife toads Alytes obstetricans boscai and Alytes cisternasii. Bioacoustics 2:1–9

    Article  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. ISBN: 3-900051-07-0

  • Dorcas ME, Price SJ, Walls SC, Barichivich WJ (2009) Auditory monitoring of anuran populations. In: Dodd CK (ed) Amphibian ecology and conservation. A handbook of techniques. Oxford University Press, Oxford, pp 281–298

    Google Scholar 

  • Downes JA (1969) The swarming and mating flight of Diptera. Annu Rev Entomol 14:271–298

    Article  Google Scholar 

  • Emerson SB (2001) Male advertisement calls: behavioural variation and physiological processes. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington, pp 36–44

    Google Scholar 

  • Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49

    Article  Google Scholar 

  • FitzGerald GJ, Bider JR (1974) Seasonal activity of the toad Bufo americanus in southern Quebec as revealed by a sand-transect technique. Can J Zool 52:1–5

    Article  Google Scholar 

  • Friedl TWP, Klump GM (2005) Sexual selection in the lek-breeding European treefrog: body size, chorus attendance, random mating and good genes. Anim Behav 70:1141–1154

    Article  Google Scholar 

  • Fritzsch B, Ryan MJ, Wilczynski W, Hetherington TE, Walkowiak W (1988) The evolution of the amphibian auditory system. Wiley, New York

    Google Scholar 

  • Frommolt KH, Bardeli R, Clausen M (2008) Computational bioacoustics for assessing biodiversity. BfN-Skripten, Vol. 234, Bonn

  • Fukuyama K, Kusano T (1992) Factors affecting breeding activity in a stream-breeding frog, Buergeria buergeri. J Herpetol 26:88–91

    Article  Google Scholar 

  • García-París M, Montori A, Herrero P (2004) Fauna Ibérica, vol 24., Amphibia, Lissamphibia. Museo Nacional de Ciencias Naturales-CSIC, Madrid

    Google Scholar 

  • Gelman A (2005) Analysis of variance? Why it is more important than ever. Ann Stat 33:1–53

    Article  Google Scholar 

  • Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans. The University of Chicago Press, Chicago

    Google Scholar 

  • Gerhardt HC, Schneider H (1980) Mating call discrimination by females of the treefrog Hyla meridionalis on Tenerife. Behav Process 5:143–149

    Article  Google Scholar 

  • Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Global Planet Change 63:90–104

    Article  Google Scholar 

  • Grafe TU (1997) Costs and benefits of mate choice in the lek-breeding reed frog, Hyperolius marmoratus. Anim Behav 53:1103–1117

    Article  Google Scholar 

  • Grafe TU, Meuche I (2005) Chorus tenure and estimates of population size of male European tree frogs Hyla arborea: implications for conservation. Amphibia-Reptilia 26:437–444

    Article  Google Scholar 

  • Grafe TU, Thein J (2001) Energetics of calling and metabolic substrate use during prolonged exercise in the European treefrog Hyla arborea. J Comp Physiol B 171:69–76

    Article  PubMed  CAS  Google Scholar 

  • Grant RA, Chadwick EA, Halliday T (2009) The lunar cycle: a cue for amphibian reproductive phenology? Anim Behav 78:349–357

    Article  Google Scholar 

  • Han EN, Gatehouse AG (1991) Effect of temperature and photoperiod on the calling behaviour of a migratory insect, the oriental armyworm Mythimna separata. Physiol Entomol 16:419–427

    Article  Google Scholar 

  • Hatano FH, Rocha CFD, Sluys MV (2002) Environmental factors affecting calling activity of a tropical diurnal frog (Hylodes phyllodes: Leptodactylidae). J Herpetol 36:314–318

    Google Scholar 

  • Heinzmann U (1970) Untersuchungen zur bio-akustik und ökologie der geburtshelferkröte, Alytes o. obstertricans (Laur.). Oecologia 5:19–55

    Article  Google Scholar 

  • Henzi SP, Dyson ML, Piper SE, Passmore NE, Bishop P (1995) Chorus attendance by male and female painted reed frogs (Hyperolius marmoratus): environmental factors and selection pressures. Funct Ecol 9:485–491

    Article  Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Höglund J, Alatalo RV (1995) Leks. Princeton University Press, Princeton

    Google Scholar 

  • Hosmer DW, Lemeshow S (1989) Applied logistic regression. Wiley, New York

    Google Scholar 

  • Jaquiéry J, Broquet T, Aguilar C, Evanno G, Perrin N (2009) Good genes drive female choice for mating partners in the lek-breeding European treefrog. Evolution 64:108–115

    Article  PubMed  Google Scholar 

  • Jehle R, Arak A (1998) Graded call variation in male Asian cricket frogs (Rana nicobariensis). Bioacoustics 9:35–48

    Article  Google Scholar 

  • Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    Article  PubMed  Google Scholar 

  • Knopp T, Heimovirta M, Kokko H, Merilä J (2008) Do male moor frogs (Rana arvalis) lek with kin? Mol Ecol 17:2522–2530

    Article  PubMed  CAS  Google Scholar 

  • Kokko H, Sutherland WJ, Lindstöm J, Reynolds JD, Mackenzie A (1998) Individual mating success, lek stability, and the neglected limitations of statistical power. Anim Behav 56:755–762

    Article  PubMed  Google Scholar 

  • Lloyd L (1867) The game birds and wild fowl of Sweden and Norway. Frederick Warne, London

    Book  Google Scholar 

  • Llusia D, Márquez R, Bowker RG (2011) Terrestrial sound monitoring systems, a methodology for quantitative calibration. Bioacoustics 20:277–286

    Article  Google Scholar 

  • Lopez PT, Narins PM, Lewis ER, Moore SW (1988) Acoustically induced call modification in the white-lipped frog, Leptodactylus albilabris. Anim Behav 36:1295–1308

    Article  Google Scholar 

  • Lott DF (1991) Intraspecific variation in the social systems of wild vertebrates. Cambridge University Press, Cambridge

    Google Scholar 

  • Loureiro A, Ferrand de Almeida N, Carretero MA, Paulo OS (2008) Atlas dos anfíbios e répteis de Portugal. Instituto da Conservação da Natureza e da Biodiversidade, Lisboa

    Google Scholar 

  • Mackenzie A, Reyolds JD, Brown VJ, Sutherland WJ (1995) Variation in male mating success on leks. Am Nat 145:633–652

    Article  Google Scholar 

  • Manel S, Williams HC, Ormerod SJ (2001) Evaluating presence-absence models in ecology: the need to account for prevalence. J Appl Ecol 38:921–931

    Article  Google Scholar 

  • Márquez R, Tejedo M (1990) Size-based mating pattern in the tree frog Hyla arborea. Herpetologica 46:176–182

    Google Scholar 

  • Márquez R, Moreira C, Do Amaral JPS, Pargana JM, Crespo EG (2005) Sound pressure level of advertisement calls of Hyla meridionalis and Hyla arborea. Amphibia-Reptilia 26:391–395

    Article  Google Scholar 

  • Montgomery DC (2001) Design and analysis of experiments, 5th edn. Wiley, New York

    Google Scholar 

  • Montgomery DC, Peck EA (1992) Introduction to linear regression analysis. Wiley, New York

    Google Scholar 

  • Moreira G, Barreto L (1997) Seasonal variation in nocturnal calling activity of a savanna anuran community in central Brazil. Amphibia-Reptilia 18:49–57

    Article  Google Scholar 

  • Murphy CG (1994) Determinants of chorus tenure in barking treefrogs (Hyla gratiosa). Behav Ecol Sociobiol 34:285–294

    Article  Google Scholar 

  • Murphy CG (1999) Nightly timing of chorusing by male barking treefrogs (Hyla gratiosa): the influence of female arrival and energy. Copeia 1999:333–347

    Article  Google Scholar 

  • Murphy CG (2003) The cause of correlations between nightly numbers of male and female barking treefrogs (Hyla gratiosa) attending choruses. Behav Ecol 14:274–281

    Article  Google Scholar 

  • Narins PM (2001) Ectothermy's last stand. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington, pp 61–70

    Google Scholar 

  • Narins PM, Feng AS, Fay RR, Popper AN (2007) Hearing and sound communication in amphibians. Springer, New York

    Google Scholar 

  • Navas CA (1996) The effect of temperature on the vocal activity of tropical anurans: a comparison of high and low-elevation species. J Herpetol 30:488–497

    Article  Google Scholar 

  • Navas CA, Bevier CR (2001) Thermal dependency of calling performance in the eurythermic frog Colostethus subpunctatus. Herpetologica 57:384–395

    Google Scholar 

  • Neter J, Kutner MH, Nachtsheim C, Wasserman W (1996) Applied linear statistical models, 3rd edn. Irwin, Chicago

    Google Scholar 

  • Obert HJ (1975) The dependence of calling activity in Rana esculenta Linné 1758 and Rana ridibunda Pallas 1771 upon exogenous factors (Ranidae, Anura). Oecologia 18:317–328

    Article  Google Scholar 

  • Obrist MK, Pavan G, Sueur J, Riede K, Llusia D, Márquez R (2010) Bioacoustics approaches in biodiversity inventories. Abc Taxa 8:68–99

    Google Scholar 

  • Oliveira ME, Paillette M, Rosa HD, Crespo EG (1991) A natural hybrid between Hyla arborea and Hyla meridionalis detected by mating calls. Amphibia-Reptilia 12:15–20

    Article  Google Scholar 

  • Oseen KL, Wassersug RJ (2002) Environmental factors influencing calling in sympatric anurans. Oecologia 133:616–625

    Article  Google Scholar 

  • Paillette M (1967) Rhythm of acoustic activity of Hyla arborea (Linné) and Hyla meridionalis Boettger anourous amphibians. CR Soc Biol 161:986–992

    CAS  Google Scholar 

  • Paredes D, Trigo RM, Garcia-Herrera R, Trigo IF (2006) Understanding precipitation changes in Iberia in early spring: weather typing and storm-tracking approaches. J Hydrometeorol 7:101–113

    Article  Google Scholar 

  • Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sc 11:1633–1644

    Article  Google Scholar 

  • Pemberton JM, Balmford AP (1987) Lekking in fallow deer. J Zool 213:762–765

    Article  Google Scholar 

  • Peterson CR, Dorcas ME (1994) Automated data acquisition. In: Heyer WR, Donnelly MA, McDiarmid RW, Hayek LC, Foster MS (eds) Measuring and monitoring biological diversity: standard methods for amphibians. Smithsonian Institution Press, Washington, pp 47–57

    Google Scholar 

  • Pleguezuelos JM, Márquez R, Lizana M (2002) Atlas y Libro Rojo de los anfibios y reptiles de España. Dirección General de Conservación de la Naturaleza-Asociación Herpetológica. Española, Madrid

    Google Scholar 

  • Prestwich KN (1994) The energetics of acoustic signalling in anuran and insects. Am Zool 34:625–643

    Google Scholar 

  • Richards SA, Whittingham MJ, Stephens PA (2011) Model selection and model averaging in behavioural ecology: the utility of the IT-AIC framework. Behav Ecol Sociobiol 65:77–89

    Article  Google Scholar 

  • Ritke ME, Babb JG, Ritke MK (1992) Temporal patterns of reproductive activity in the gray treefrog (Hyla chrysoscelis). J Herpetol 26:107–111

    Article  Google Scholar 

  • Rome LC, Stevens ED, John-Alder HB (1992) The influence of temperature and thermal acclimation on physiological function. In: Feder ME, Burggren WW (eds) Environmental physiology of the amphibians. The University of Chicago Press, Chicago, pp 183–205

    Google Scholar 

  • Rosa HD, Oliveira ME (1994) Genetic differentiation of the Iberian tree frogs Hyla arborea molleri and Hyla meridionalis (Amphibia, Anura). J Zool Syst Evol Res 32:117–128

    Article  Google Scholar 

  • Ryan MJ (2001) Anuran communication. Smithsonian Institution Press, Washington

    Google Scholar 

  • Ryan MJ, Rand AS (1998) Evoked vocal response in male Tungara frogs: pre-existing biases in male responses? Anim Behav 56:1509–1516

    Article  PubMed  Google Scholar 

  • Ryan MJ, Tuttle MD, Taft LK (1981) The costs and benefits of frog chorusing behaviour. Behav Ecol Sociobiol 8:273–278

    Article  Google Scholar 

  • Salvador A, Carrascal LM (1990) Reproductive phenology and temporal patterns of mate access in Mediterranean anurans. J Herpetol 24:438–441

    Article  Google Scholar 

  • Schneider H (1971) Die steuerung des täglichen rufbeginns beim Laubfrosch, Hyla arborea arborea (L.). Oecologia 8:310–320

    Google Scholar 

  • Schneider H (1974) Structure of the mating calls and relationships of the European tree frogs (Hylidae, Anura). Oecologia 14:99–110

    Article  Google Scholar 

  • Schneider H (1982) Phonotaxis bei weibchen des kanarischen Laubfrosches, Hyla meridionalis. Zool Anz 208:161–174

    Google Scholar 

  • Schneider H, Eichelberg H (1974) The mating call of hybrids of the fire-bellied toad and yellow-bellied toad (Bombina bombina (L.), Bombina v. variegata (L.), Discoglossidae, Anura). Oecologia 16:61–71

    Article  Google Scholar 

  • Schwartz JJ, Ressel SJ, Bevier CR (1995) Carbohydrate and calling: depletion of muscle glycogen and the chorusing dynamics of the neotropical treefrog Hyla microcephala. Behav Ecol Sociobiol 37:125–135

    Article  Google Scholar 

  • Schwenk K, Padilla DK, Bakken GS, Full RJ (2009) Grand challenges in organismal biology. Integr Comp Biol 49:7–14

    Article  PubMed  Google Scholar 

  • Shirose LJ, Bishop CA, Green DM, MacDonald CJ, Brooks RJ, Helferty NJ (1997) Validation tests of an amphibian call count survey technique in Ontario, Canada. Herpetologica 53:312–320

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freedman, New York

    Google Scholar 

  • Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (2007) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

    Google Scholar 

  • Steelman CK, Dorcas ME (2010) Anuran calling survey optimization: developing and testing predictive models of anuran calling activity. J Herpetol 44:61–68

    Article  Google Scholar 

  • Stöck M, Dubey S, Klütsch C, Litvinchuk SN, Scheidt U, Perrin N (2008) Mitochondrial and nuclear phylogeny of circum-Mediterranean tree frogs from the Hyla arborea group. Mol Phylogenet Evol 49:1019–1024

    Article  PubMed  CAS  Google Scholar 

  • Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behav Ecol Sociobiol 65:13–21

    Article  Google Scholar 

  • Taigen TL, Wells KD (1985) Energetics of vocalization by an anuran amphibian (Hyla versicolor). J Comp Physiol B 155:163–170

    Article  Google Scholar 

  • Trigo RM, Palutikof JP (2001) Precipitation scenarios over Iberia: a comparison between direct GCM output and different downscaling techniques. J Climate 14:4422–4446

    Article  Google Scholar 

  • Tryjanowski P, Mariusz R, Sparks TH (2003) Changes in spawning dates of common frogs and common toads in western Poland in 1978–2002. Ann Zool Fenn 40:459–464

    Google Scholar 

  • Tuttle MD, Ryan MJ (1981) Bat predation and the evolution of frog vocalizations in the Neotropics. Science 214:677–678

    Article  PubMed  CAS  Google Scholar 

  • Walkowiak W (2007) Call production and neural basis of vocalization. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 87–112

    Google Scholar 

  • Weary DM, Lambrechts MM, Krebs JR (1991) Does singing exhaust male great tits? Anim Behav 41:540–542

    Article  Google Scholar 

  • Weir LA, Mossman MJ (2005) North American amphibian monitoring program (NAAMP). In: Lannoo M (ed) Amphibian declines: the conservation status of United States species. University of California Press, Berkeley, pp 307–313

    Google Scholar 

  • Wells KD (1977) The social behaviour of anuran amphibians. Anim Behav 25:666–693

    Article  Google Scholar 

  • Wells KD (2007) The ecology and behavior of amphibians. The University of Chicago Press, Chicago

    Google Scholar 

  • Wells KD, Taigen TL (1986) The effect of social interactions on calling energetics in the gray treefrog (Hyla versicolor). Behav Ecol Sociobiol 19:9–18

    Article  Google Scholar 

  • Widemo F, Owens IPF (1995) Lek size, male mating skew and the evolution of lekking. Nature 373:148–151

    Article  CAS  Google Scholar 

  • Wilczynski W, Chu J (2001) Acoustic communication, endocrine control, and the neurochemical systems of the brain. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington, pp 23–35

    Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Meth Ecol Evol 1:3–14

    Article  Google Scholar 

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Acknowledgments

We want to thank José Manuel Mendes for granting us access to the pond in his property in Castelo de Vide. Permits to work and use of facilities in protected areas were granted by Somiedo Natural Park (Principado de Asturias), ICTS Doñana (CSIC), and Consejerías de Medio Ambiente (Principado de Asturias and Andalucía). We are also grateful to Richard G. Bowker and Mark E. Cambron of Western Kentucky University for designing and building the Amphibulator (timer-controller for ARS). Meteorological data were kindly provided by AEMET (Agencia Estatal de Meteorología. Ministerio de Medio Ambiente y Medio Rural y Marino) and Guillermo Ballester (OGIMET Weather Information Service). David Sánchez provided information about bioclimatic variables for the Iberian distribution range of tree frogs. Xavier Eekhout and Antón Arias helped in the field and with the data processing. José Miguel Oliveira, Maribel Benítez, Manolo Chirosa, and Hélder Duarte also helped in the field. We appreciate suggestions from anonymous reviewers that greatly improved this research report. The first author was supported by an FPI predoctoral grant from Ministerio de Ciencia e Innovación (BES-2006-13104, Spain). The last author was in receipt of a fellowship from the Fundação para a Ciência e a Tecnologia (SFRH/BPD/3514/2000, Portugal) and a SYNTHESYS project (ES-TAF-1251, Spain). Research was funded by projects TEMPURA (CGL2005-00092/BOS), ACOURA (CGL2008-04814-C02), and project TATANKA (CGL2011-25062), Ministerio de Ciencia e Innovación, Spain (PI. R. Márquez).

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Llusia, D., Márquez, R., Beltrán, J.F. et al. Environmental and social determinants of anuran lekking behavior: intraspecific variation in populations at thermal extremes. Behav Ecol Sociobiol 67, 493–511 (2013). https://doi.org/10.1007/s00265-012-1469-2

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