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Intraspecific scaling in frog calls: the interplay of temperature, body size and metabolic condition

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Abstract

Understanding physiological and environmental determinants of strategies of reproductive allocation is a pivotal aim in biology. Because of their high metabolic cost, properties of sexual acoustic signals may correlate with body size, temperature, and an individual’s energetic state. A quantitative theory of acoustic communication, based on the metabolic scaling with temperature and mass, was recently proposed, adding to the well-reported empirical patterns. It provides quantitative predictions for frequencies, call rate, and durations. Here, we analysed the mass, temperature, and body condition scaling of spectral and temporal attributes of the advertisement call of the treefrog Hypsiboas pulchellus. Mass dependence of call frequency followed metabolic expectations (f~M −0.25, where f is frequency and M is mass) although non-metabolic allometry could also account for the observed pattern. Temporal variables scaled inversely with mass contradicting metabolic expectations (d~M 0.25, where d is duration), supporting instead empirical patterns reported to date. Temperature was positively associated with call rate and negatively with temporal variables, which is congruent with metabolic predictions. We found no significant association between temperature and frequencies, adding to the bulk of empirical evidence. Finally, a result of particular relevance was that body condition consistently determined call characteristics, in interaction with temperature or mass. Our intraspecific study highlights that even if proximate determinants of call variability are rather well understood, the mechanisms through which they operate are proving to be more complex than previously thought. The determinants of call characteristics emerge as a key topic of research in behavioural and physiological biology, with several clear points under debate which need to be analysed on theoretical and empirical grounds.

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References

  • Amorim MCP, McCracken ML, Fine ML (2002) Metabolic costs of sound production in the oyster toadfish, Opsanus tau. Can J Zool 80:830–838

    Article  Google Scholar 

  • Bennet-Clark HC, Daws AG (1999) Transduction of mechanical energy into sound energy in the cicada Cyclochila australasiae. J Exp Biol 202:1803–1817

    PubMed  Google Scholar 

  • Bertram SM, Thomson IR, Auguste B et al (2011) Variation in cricket acoustic mate attraction signalling explained by body morphology and metabolic differences. Anim Behav 82:1255–1261

    Article  Google Scholar 

  • Bonnet X, Bradshaw D, Shine R (1998) Capital versus income breeding: an ectothermic perspective. Oikos 83:333–342

    Article  Google Scholar 

  • Brepson L, Voituron Y, Lengagne T (2013) Condition-dependent ways to manage acoustic signals under energetic constraint in a tree frog. Behav Ecol 24:488–496

    Article  Google Scholar 

  • Brown JH, Gillooly JF, Allen AP et al (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  • Canavero A, Arim M, Naya DE et al (2008) Calling activity patterns in an anuran assemblage: the role of seasonal trends and weather determinants. North-West J Zool 4:29–41

    Google Scholar 

  • Candolin U (1999) The relationship between signal quality and physical condition: is sexual signalling honest in the three-spined stickleback? Anim Behav 58:1261–1267

    Article  PubMed  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 

  • Charlton BD, Ellis WA, McKinnon AJ et al (2011) Cues to body size in the formant spacing of male koala (Phascolarctos cinereus) bellows: honesty in an exaggerated trait. J Exp Biol 214:3414–3422

    Article  PubMed  Google Scholar 

  • Clark CW, Mangel M (2000) Dynamic state variable models in ecology: methods and applications. Oxford University Press, New York

    Google Scholar 

  • Dell AI, Pawar S, Savage VM (2011) Systematic variation in the temperature dependence of physiological and ecological traits. Proc Natl Acad Sci 108:10591–10596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drewry GE, Heyer WR, Rand AS (1982) A functional analysis of the complex call of the frog Physalaemus pustulosus. Copeia 1982:636–645

    Article  Google Scholar 

  • Fitch WT (2000) Skull dimensions in relation to body size in nonhuman mammals: the causal bases for acoustic allometry. Zool-Anal Complex Syst 103:40–58

    Google Scholar 

  • Fletcher NH (2004) A simple frequency-scaling rule for animal communication. J Acoust Soc Am 115:2334–2338

    Article  PubMed  Google Scholar 

  • Gerhardt HC, Bee MA (2007) Recognition and localization of acoustic signals. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 113–146

    Google Scholar 

  • Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press, Chicago

    Google Scholar 

  • Gillooly JF, Ophir AG (2010) The energetic basis of acoustic communication. Proc R Soc B Biol Sci 277:1325–1331

    Article  Google Scholar 

  • Gillooly JF, Brown JH, West GB et al (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251

    Article  CAS  PubMed  Google Scholar 

  • Ginzburg L, Damuth J (2008) The space-lifetime hypothesis: viewing organisms in four dimensions, literally. Am Nat 171:125–131

    Article  PubMed  Google Scholar 

  • Glazier DS (2005) Beyond the “3/4-power law”: variation in the intra-and interspecific scaling of metabolic rate in animals. Biol Rev 80:611–662

    Article  PubMed  Google Scholar 

  • Glazier DS (2009) Activity affects intraspecific body-size scaling of metabolic rate in ectothermic animals. J Comp Physiol B 179:821–828

    Article  PubMed  Google Scholar 

  • Gomes FR, Chauí-Berlinck JG, Bicudo JEP, Navas CA (2004) Intraspecific relationships between resting and activity metabolism in anuran amphibians: influence of ecology and behavior. Physiol Biochem Zool 77:197–208

    Article  PubMed  Google Scholar 

  • Green AJ (1990) Determinants of chorus participation and the effects of size, weight and competition on advertisement calling in the tungara frog, Physalaemus pustulosus (Leptodactylidae). Anim Behav 39:620–638. doi:10.1016/S0003-3472(05)80373-2

    Article  Google Scholar 

  • Hall ML, Molles LE, Illes AE, Vehrencamp SL (2009) Singing in the face of death: male banded wrens Thryophilus pleurostictus sing more to playback in their last breeding season. J Avian Biol 40:217–224

    Article  Google Scholar 

  • Hall ML, Kingma SA, Peters A (2013) Male songbird indicates body size with low-pitched advertising songs. PLoS One 8:e56717. doi:10.1371/journal.pone.0056717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison SJ, Thomson IR, Grant CM, Bertram SM (2013) Calling, courtship, and condition in the fall field cricket, Gryllus pennsylvanicus. PloS One 8:e60356. doi:10.1371/journal.pone.0060356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayward A, Gillooly JF, Kodric-Brown A (2012) Behavior. In: Sibly RM, Brown JH, Kodric-Brown A (eds) Metabolic ecology: a scaling approach, pp 67–76

  • Hempleman SC, Kilgore DL, Colby C et al (2005) Spike firing allometry in avian intrapulmonary chemoreceptors: matching neural code to body size. J Exp Biol 208:3065–3073

    Article  CAS  PubMed  Google Scholar 

  • Houston A, McNamara JM (1999) Models of Adaptive Behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • Humfeld SC (2013) Condition-dependent signaling and adoption of mating tactics in an amphibian with energetic displays. Behav Ecol 24:859–870

    Article  Google Scholar 

  • Irlich UM, Terblanche JS, Blackburn TM, Chown SL (2009) Insect rate-temperature relationships: environmental variation and the metabolic theory of ecology. Am Nat 174:819–835

    Article  PubMed  Google Scholar 

  • Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67

    Article  Google Scholar 

  • Jönsson KI, Herczeg G, O’Hara RB et al (2009) Sexual patterns of prebreeding energy reserves in the common frog Rana temporaria along a latitudinal gradient. Ecography 32:831–839

    Article  Google Scholar 

  • Judge KA, Ting JJ, Gwynne DT (2008) Condition dependence of male life span and calling effort in a field cricket. Evolution 62:868–878

    Article  PubMed  Google Scholar 

  • Karasov WH (1986) Energetics, physiology and vertebrate ecology. Trends Ecol Evol 1:101–104

    Article  CAS  PubMed  Google Scholar 

  • Killen SS, Atkinson D, Glazier DS (2010) The intraspecific scaling of metabolic rate with body mass in fishes depends on lifestyle and temperature. Ecol Lett 13:184–193

    Article  PubMed  Google Scholar 

  • Kokko H, Brooks R, McNamara JM, Houston AI (2002) The sexual selection continuum. Proc R Soc Lond B Biol Sci 269:1331–1340

    Article  Google Scholar 

  • Lingnau R, Bastos RP (2007) Vocalizations of the Brazilian torrent frog Hylodes heyeri (Anura: Hylodidae): repertoire and influence of air temperature on advertisement call variation. J Nat Hist 41:1227–1235

    Article  Google Scholar 

  • Luo L-G, Ding G-H, Ji X (2010) Income breeding and temperature-induced plasticity in reproductive traits in lizards. J Exp Biol 213:2073–2078. doi:10.1242/jeb.041137

    Article  PubMed  Google Scholar 

  • Marquet PA, Allen AP, Brown JH et al (2014) On theory in ecology. Bioscience 64:701–710

    Article  Google Scholar 

  • McCauley SJ, Bouchard SS, Farina BJ et al (2000) Energetic dynamics and anuran breeding phenology: insights from a dynamic game. Behav Ecol 11:429–436

    Article  Google Scholar 

  • McClelland BE, Wilczynski W, Ryan MJ (1996) Correlations between call characteristics and morphology in male cricket frogs (Acris crepitans). J Exp Biol 199:1907–1919

    CAS  PubMed  Google Scholar 

  • McLeod AI, Xu C (2011) bestglm: best subset GLM. R package

  • McLister JD (2001) Physical factors affecting the cost and efficiency of sound production in the treefrog Hyla versicolor. J Exp Biol 204:69–80

    CAS  PubMed  Google Scholar 

  • McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Comstock, Cornell University Press, Ithaca

    Google Scholar 

  • McNamara JM, Houston AI (2008) Optimal annual routines: behaviour in the context of physiology and ecology. Philos Trans R Soc B Biol Sci 363:301–319

    Article  Google Scholar 

  • Mitchell NJ (2001) Males call more from wetter nests: effects of substrate water potential on reproductive behaviours of terrestrial toadlets. Proc R Soc Lond B 268:87–93. doi:10.1098/rspb.2000.1334

    Article  CAS  Google Scholar 

  • Moore IT, Hopkins WA (2009) Interactions and trade-offs among physiological determinants of performance and reproductive success. Integr Comp Biol 49:441–451

    Article  PubMed  Google Scholar 

  • Morrison C, Hero J-M, Smith WP (2001) Mate selection in Litoria chloris and Litoria xanthomera: females prefer smaller males. Austral Ecol 26:223–232

    Article  Google Scholar 

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

    Google Scholar 

  • Navas CA (1996) Thermal dependency of field locomotor and vocal performance of high-elevation anurans in the tropical Andes. J Herpetol 30:478–487

    Article  Google Scholar 

  • Nee S, Read AF, Greenwood JJD, Harvey PH (1991) The relationship between abundance and body size in British birds. Nature 351:312–313

    Article  Google Scholar 

  • Ophir AG, Schrader SB, Gillooly JF (2010) Energetic cost of calling: general constraints and species-specific differences. J Evol Biol 23:1564–1569

    Article  CAS  PubMed  Google Scholar 

  • Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891

    Article  Google Scholar 

  • Peig J, Green AJ (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct Ecol 24:1323–1332

    Article  Google Scholar 

  • Pough FH, Magnusson WE, Ryan MJ et al (1992) Behavioral energetics. In: Feder ME, Burggren WW (eds) Environmental physiology of the amphibians. University of Chicago Press, Chicago, pp 395–436

    Google Scholar 

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

    Article  Google Scholar 

  • Prestwich KN, Brugger KE, Topping M (1989) Energy and communication in three species of hylid frogs: power input, power output and efficiency. J Exp Biol 144:53–80

    Google Scholar 

  • Price CA, Weitz JS, Savage VM et al (2012) Testing the metabolic theory of ecology. Ecol Lett 15:1465–1474

    Article  PubMed  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed 22 Sept 2014

  • Robertson JG (1986) Male territoriality, fighting and assessment of fighting ability in the Australian frog Uperoleia rugosa. Anim Behav 34:763–772

    Article  Google Scholar 

  • Ryan MJ (1988) Energy, calling, and selection. Am Zool 28:885–898

    Article  Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163

    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 

  • Sibly RM, Brown JH, Kodric-Brown A (2012) Metabolic ecology: a scaling approach. Wiley-Blackwell, Oxford

    Book  Google Scholar 

  • Sullivan BK (1989) Interpopulational variation in vocalizations of Bufo woodhousii. J Herpetol 23:368–373

    Article  Google Scholar 

  • Sullivan BK, Hinshaw SH (1992) Female choice and selection on male calling behaviour in the grey treefrog Hyla versicolor. Anim Behav 44:733–744

    Article  Google Scholar 

  • Underwood AJ (1997) Ecological experiments: their logical design and interpretation using analysis of variance. Cambridge University Press, Melbourne

    Google Scholar 

  • Voituron Y, Brepson L, Richardson C et al (2012) Energetics of calling in the male treefrog Hyla arborea: when being large means being sexy at low cost. Behaviour 149:775–793

    Article  Google Scholar 

  • Weiner J (1992) Physiological limits to sustainable energy budgets in birds and mammals: ecological implications. Trends Ecol Evol 7:384–388

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Wells KD (2001) The energetics of calling in frogs. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington, DC, pp 45–60

    Google Scholar 

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

    Book  Google Scholar 

  • Wells KD, Taigen TL (1984) Reproductive behavior and aerobic capacities of male American toads (Bufo americanus): is behavior constrained by physiology? Herpetologica 40:292–298

    Google Scholar 

  • West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126

    Article  CAS  PubMed  Google Scholar 

  • White CR, Phillips NF, Seymour RS (2006) The scaling and temperature dependence of vertebrate metabolism. Biol Lett 2:125–127

    Article  PubMed  Google Scholar 

  • White CR, Cassey P, Blackburn TM (2007) Allometric exponents do not support a universal metabolic allometry. Ecology 88:315–323

    Article  PubMed  Google Scholar 

  • Ziegler L, Arim M, Narins PM (2011) Linking amphibian call structure to the environment: the interplay between phenotypic flexibility and individual attributes. Behav Ecol 22:520–526. doi:10.1093/beheco/arr011

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors would like to express their gratitude to Gabriel Laufer and Indigena Private Wildlife Reserve for allowing this study on their land, and for lending their facilities during fieldwork. Laura Montes de Oca lent her car and gave assistance during field trips, and Mauro Berazategui helped us during fieldwork. The contributions by three anonymous reviewers helped to substantially improve this manuscript. This work was funded by Agencia Nacional de Investigación e Innovación of Uruguay through a studentship to L. Z. (BE_POS_2010_2502), and received support from PEDECIBA Biología (L. Z.; Doctoral Programme, Uruguay). M. A. was funded by a Fondo Clemente Estable grant (FCE_2_2011_1_7117).

Author contribution statement

L. Z., M. A. and F. B. formulated the original idea; M. A. and L. Z. developed the methodology; L. Z. conducted the fieldwork; M. A. and L. Z. performed the statistical analyses; L. Z., M. A. and F. B. wrote the manuscript.

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Correspondence to Lucia Ziegler.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. All applicable institutional and/or national guidelines for the care and use of animals were followed.

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Communicated by Jean-François Le Galliard.

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The present work addresses the energetics of anuran advertisement calls from a novel perspective, integrating empirical patters with more recent metabolic ecology theory. We examined the effect of three call determinants that are also linked to metabolic capacity: mass, temperature and body condition. Additive to the main role of these variables on the call structure in anurans, the significance and pervasiveness of interactions between them appears as a potential determinant of individuals’ allocation to reproduction and the display of different tactics.

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Ziegler, L., Arim, M. & Bozinovic, F. Intraspecific scaling in frog calls: the interplay of temperature, body size and metabolic condition. Oecologia 181, 673–681 (2016). https://doi.org/10.1007/s00442-015-3499-8

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