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.
Similar content being viewed by others
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
Bennet-Clark HC, Daws AG (1999) Transduction of mechanical energy into sound energy in the cicada Cyclochila australasiae. J Exp Biol 202:1803–1817
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
Bonnet X, Bradshaw D, Shine R (1998) Capital versus income breeding: an ectothermic perspective. Oikos 83:333–342
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
Brown JH, Gillooly JF, Allen AP et al (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789
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
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
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
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
Clark CW, Mangel M (2000) Dynamic state variable models in ecology: methods and applications. Oxford University Press, New York
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
Drewry GE, Heyer WR, Rand AS (1982) A functional analysis of the complex call of the frog Physalaemus pustulosus. Copeia 1982:636–645
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
Fletcher NH (2004) A simple frequency-scaling rule for animal communication. J Acoust Soc Am 115:2334–2338
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
Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press, Chicago
Gillooly JF, Ophir AG (2010) The energetic basis of acoustic communication. Proc R Soc B Biol Sci 277:1325–1331
Gillooly JF, Brown JH, West GB et al (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251
Ginzburg L, Damuth J (2008) The space-lifetime hypothesis: viewing organisms in four dimensions, literally. Am Nat 171:125–131
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
Glazier DS (2009) Activity affects intraspecific body-size scaling of metabolic rate in ectothermic animals. J Comp Physiol B 179:821–828
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
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
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
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
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
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
Houston A, McNamara JM (1999) Models of Adaptive Behaviour. Cambridge University Press, Cambridge
Humfeld SC (2013) Condition-dependent signaling and adoption of mating tactics in an amphibian with energetic displays. Behav Ecol 24:859–870
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
Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67
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
Judge KA, Ting JJ, Gwynne DT (2008) Condition dependence of male life span and calling effort in a field cricket. Evolution 62:868–878
Karasov WH (1986) Energetics, physiology and vertebrate ecology. Trends Ecol Evol 1:101–104
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
Kokko H, Brooks R, McNamara JM, Houston AI (2002) The sexual selection continuum. Proc R Soc Lond B Biol Sci 269:1331–1340
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
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
Marquet PA, Allen AP, Brown JH et al (2014) On theory in ecology. Bioscience 64:701–710
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
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
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
McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Comstock, Cornell University Press, Ithaca
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
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
Moore IT, Hopkins WA (2009) Interactions and trade-offs among physiological determinants of performance and reproductive success. Integr Comp Biol 49:441–451
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
Narins PM, Feng AS, Fay RR, Popper AN (eds) (2007) Hearing and sound communication in amphibians. Springer, New York
Navas CA (1996) Thermal dependency of field locomotor and vocal performance of high-elevation anurans in the tropical Andes. J Herpetol 30:478–487
Nee S, Read AF, Greenwood JJD, Harvey PH (1991) The relationship between abundance and body size in British birds. Nature 351:312–313
Ophir AG, Schrader SB, Gillooly JF (2010) Energetic cost of calling: general constraints and species-specific differences. J Evol Biol 23:1564–1569
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
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
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
Prestwich KN (1994) The energetics of acoustic signaling in anurans and insects. Am Zool 34:625–643
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
Price CA, Weitz JS, Savage VM et al (2012) Testing the metabolic theory of ecology. Ecol Lett 15:1465–1474
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
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
Ryan MJ (1988) Energy, calling, and selection. Am Zool 28:885–898
Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163
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
Sibly RM, Brown JH, Kodric-Brown A (2012) Metabolic ecology: a scaling approach. Wiley-Blackwell, Oxford
Sullivan BK (1989) Interpopulational variation in vocalizations of Bufo woodhousii. J Herpetol 23:368–373
Sullivan BK, Hinshaw SH (1992) Female choice and selection on male calling behaviour in the grey treefrog Hyla versicolor. Anim Behav 44:733–744
Underwood AJ (1997) Ecological experiments: their logical design and interpretation using analysis of variance. Cambridge University Press, Melbourne
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
Weiner J (1992) Physiological limits to sustainable energy budgets in birds and mammals: ecological implications. Trends Ecol Evol 7:384–388
Wells KD (1977) The social behaviour of anuran amphibians. Anim Behav 25:666–693
Wells KD (2001) The energetics of calling in frogs. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington, DC, pp 45–60
Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chicago
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
West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126
White CR, Phillips NF, Seymour RS (2006) The scaling and temperature dependence of vertebrate metabolism. Biol Lett 2:125–127
White CR, Cassey P, Blackburn TM (2007) Allometric exponents do not support a universal metabolic allometry. Ecology 88:315–323
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
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
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.
Additional information
Communicated by Jean-François Le Galliard.
Student statement
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.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-015-3499-8