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Reproductive ecology and territorial behavior of Boana goiana (Anura: Hylidae), a gladiator frog from the Brazilian Cerrado

ABSTRACT

Anuran males and females adopt different reproductive and behavioral strategies in different contexts. We investigated the reproductive ecology and territorial behavior of the treefrog Boana goiana (B. Lutz, 1968) from the Brazilian Cerrado. We hypothesized that competitor density/proximity would increase the behavioral responses of B. goiana males, and that mating would be assortative. We also tested if the number of eggs correlates with female size and if there is a trade-off between clutch size and egg size. We conducted two territoriality experiments to test the effects of male size, competitor proximity and competitor density. Larger males called more in the presence of a second male. In the second experiment, the largest males emitted more calls and the distance to the nearest male increased as resident males called more. In both experiments, the number of calls was influenced by either male size or spacing between males. Some males behaved as satellites, probably to avoid fights. Our analyses indicate that females choose males with similar sizes to their own, corroborating our hypothesis of size-assortative mating. We found no relationships between female size and clutch size/volume, and between egg size and number of eggs per clutch. We also report multiple spawning for this species. The low incidence of physical combats and the spacing pattern indicate that this species relies almost solely on calls to resolve contests, which could be explained by low motivation, or simply because males avoid combats to decrease injury risks. Thus, acoustic or even multimodal communication seems crucial for social interactions of B. goiana.

KEY WORDS:
Clutch size; acoustic communication; assortative mating; male competition; aggressive interactions; arrival dynamics

INTRODUCTION

In the classic Darwinian definition of sexual selection, in animals that reproduce sexually, males and females will adopt different strategies to ensure their reproductive success (Andersson 1994Andersson MB (1994) Sexual Selection, Princeton University Press, New Jersey, 624 pp., Candolin 2019Candolin U (2019) Sexual selection and sexual conflict. In: Taft G, Nicholls M, Willis M (Eds) Encyclopedia of Ecology. Elsevier, 2nd ed., vol. 1, 310-318. https://doi.org/10.1016/B978-0-12-409548-9.10886-3
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). Because their reproduction is limited in time and space (Haddad and Prado 2005Haddad CFB, Prado CPA (2005) Reproductive modes in frogs and their unexpected diversity in the Atlantic Forest of Brazil. BioScience 55(3): 207-217., Wells 2007Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chigago, 1148 pp. https://doi.org/10.7208/chicago/9780226893334.001.0001
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), anuran amphibians are good model organisms to investigate factors related to mating and reproductive success, with males and females adopting markedly different strategies (Cayuela et al. 2017Cayuela H, Lengagne T, Joly P, Léna JP (2017) Females trade off the uncertainty of breeding resource suitability with male quality during mate choice in an anuran. Animal Behaviour 123: 179-185. https://doi.org/10.1016/j.anbehav.2016.11.002
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, Valencia-Aguilar et al. 2020Valencia-Aguilar A, Zamudio KR, Haddad CFB, Bogdanowicz SM, Prado CPA (2020) Show me you care: female mate choice based on egg attendance rather than male or territorial traits. Behavioral Ecology 31: 1054-1064. https://doi.org/10.1093/beheco/araa051
https://doi.org/10.1093/beheco/araa051...
). In general terms, the reproductive success of males of many animal species can be defined by a variety of factors, including body size, territory quality, displays, and built structures (e.g. fish: McKaye et al. 1990McKaye KR, Louda SM, Stauffer-Jr JR (1990) Bower size and male reproductive success in a cichlid fish lek. The American Naturalist 135(5): 597-613. https://doi.org/10.1086/285064
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, frogs: Olsson and Shine 1996Olsson M, Shine R (1996) Does reproductive success increase with age or with size in species with indeterminate growth? A case study using sand lizards (Lacerta agilis). Oecologia 105: 175-178. https://doi.org/10.1007/BF00328543
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, crabs: Murai and Backwell 2006Murai M, Backwell PRY (2006) A conspicuous courtship signal in the fiddler crab Uca perplexa: female choice based on display structure. Behavioral Ecology and Sociobiology 60: 736-741. https://doi.org/10.1007/s00265-006-0217-x
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). Specifically for male anurans, arrival at the reproductive area is often associated with mating success, and males that arrive early may increase their chances of mating (Lodé et al. 2005Lodé T, Holveck M, Lesbarrères D (2005) Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina. Biological Journal of the Linnean Society 86(2): 191-200. https://doi.org/10.1111/j.1095-8312.2005.00521.x
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, Dias et al. 2017Dias TM, Prado CPA, Bastos RP (2017) Nightly calling patterns in a Neotropical gladiator frog. Acta Ethologica 20(3): 207-214. https://doi.org/10.1007/s10211-017-0263-6
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). The establishment and maintenance of a territory can also be essential for the reproductive success of anuran males (Wells 1977aWells KD (1977a) The social behaviour of anuran amphibians. Animal Behaviour 25(3): 666-693. https://doi.org/10.1016/0003-3472(77)90118-X
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). Regarding the ability to establish and maintain territories by males, acoustic signaling is an essential component of anuran social behavior (Wells 2007Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chigago, 1148 pp. https://doi.org/10.7208/chicago/9780226893334.001.0001
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). Male anurans use calls to establish territories, interact aggressively with other males, maintain the spacing among calling neighbors and - most importantly - to attract females (Bastos et al. 2011Bastos RP, Alcantra MB, Morais AR, Lignau R, Signorelli L (2011) Vocal behaviour and conspecific call response in Scinax centralis (Anura: Hylidae). Herpetolological Journal 21(1): 43-50. https://www.ingentaconnect.com/contentone/bhs/thj/2011/00000021/00000001/art00006
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, Lemes et al. 2012Lemes P, Tessarolo G, Morais AR, Bastos RP (2012) Acoustic repertoire of Barycholos ternetzi (Anura: Strabomantidae) in central Brazil. South American Journal of Herpetology 7(2): 157-164. https://doi.org/10.2994/057.007.0205
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). The calling activity of neighbors may influence the resident males’ behavior, changing their acoustic behavior and sometimes leading to physical combats (Wells 1977aWells KD (1977a) The social behaviour of anuran amphibians. Animal Behaviour 25(3): 666-693. https://doi.org/10.1016/0003-3472(77)90118-X
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, Bastos et al. 2011Bastos RP, Alcantra MB, Morais AR, Lignau R, Signorelli L (2011) Vocal behaviour and conspecific call response in Scinax centralis (Anura: Hylidae). Herpetolological Journal 21(1): 43-50. https://www.ingentaconnect.com/contentone/bhs/thj/2011/00000021/00000001/art00006
https://www.ingentaconnect.com/contenton...
, Lemes et al. 2012Lemes P, Tessarolo G, Morais AR, Bastos RP (2012) Acoustic repertoire of Barycholos ternetzi (Anura: Strabomantidae) in central Brazil. South American Journal of Herpetology 7(2): 157-164. https://doi.org/10.2994/057.007.0205
https://doi.org/10.2994/057.007.0205...
). Males can also assess the size of rival males by evaluating call parameters, thus avoiding a conflict with a larger opponent (Bee and Perrill 1996Bee MA, Perril SA (1996) Responses to conspecific advertisement calls in the green frog (Rana clamitans) and their role in male-male communication. Behaviour 133(3/4): 283-301. https://doi.org/10.1163/156853996X00152
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, Bee et al. 1999Bee MA, Perril SA, Owen PC (1999) Size assessment in simulated territorial encounters between male green frogs (Rana clamitans). Behavioral Ecology and Sociobiology 45: 177-184. https://doi.org/10.1007/s002650050551
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, Nali and Prado 2014Nali RC, Prado CPA (2014) Complex call with different messages in Bokermannohyla ibitiguara (Anura, Hylidae), a gladiator frog of the Brazilian Cerrado. Journal of Herpetology 48(3): 407-414. https://doi.org/10.1670/13-090
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). Furthermore, the establishment of a territory by one of the males can affect the outcome of the contest by increasing motivation to defend its territory (Owen and Gordon 2005Owen PC, Gordon NM (2005) The effect of perceived intruder proximity and resident body size on the aggressive responses of male green frogs, Rana clamitans (Anura: Ranidae). Behavioral Ecology and Sociobiology 58: 446-455. https://doi.org/10.1007/s00265-005-0961-3
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).

Meanwhile, the reproductive success of females is usually affected by mate choice and their capacity to produce oocytes, which generally correlates with body size (e.g. lizards and snakes: Shine 1992Shine R (1992) Relative clutch mass and body shape in lizards and snakes: is reproductive investment constrained or optimized? Evolution 46: 828-833. https://doi.org/10.1111/j.1558-5646.1992.tb02088.x
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, frogs: Pettitt et al. 2013Pettitt BA, Bourne GR, Bee MA (2013) Advertisement call variation in the golden rocket frog (Anomaloglossus beebei): Evidence for individual distinctiveness. Ethology 119(3): 244-256. https://doi.org/10.1111/eth.12058
https://doi.org/10.1111/eth.12058...
). In anurans, the reproductive effort of females usually fits one of three patterns: clutches with a few large eggs, clutches with many small eggs, or variable egg sizes within the same clutch (Crump 1984Crump ML (1984) Intraclutch egg size variability in Hyla crucifer (Anura: Hylidae). Copeia 1984(2): 302-308. https://www.jstor.org/stable/1445185?seq=1
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, Dziminski et al. 2009Dziminski MA, Vercoe PE, Roberts JD (2009) Variable offspring provisioning and fitness: a direct test in the field. Functional Ecology 23(1): 164-171. https://doi.org/10.1111/j.1365-2435.2008.01480.x
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, Pupin et al. 2018Pupin NC, Haddad CFB, Prado CPA (2018) Maternal provisioning by foam-nesting frogs of the genus Physalaemus (Anura, Leptodactylidae) in contrasting environments. Amphibia-Reptilia 39(1): 120-125. https://doi.org/10.1163/15685381-00003146
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). Additionally, large females can produce more eggs than small females, and this positive relationship between clutch size and female size is known for several anuran species (e.g. Kusano and Hayashi 2002Kusano T, Hayashi T (2002) Female size-specific clutch parameters of two closely related stream-breeding frogs, Rana sakuraii and R. tagoi tagoi: female size-independent and size-dependent egg sizes. Current Herpetology 21(2): 75-86. https://doi.org/10.5358/hsj.21.75
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, Wogel et al. 2002Wogel H, Abrunhosa PA, Pombal-Jr JP (2002) Atividade reprodutiva de Physalaemus signifer (Anura, Leptodactylidae) em ambiente temporário. Iheringia , Série Zoologia, 92(2): 57-70. https://doi.org/10.1590/S0073-47212002000200006
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, Dziminski and Alford 2005Dziminski MA, Alford RA (2005) Patterns and fitness consequences of intraclutch variation in egg provisioning in tropical Australian frogs. Oecologia 146: 98-109. https://doi.org/10.1007/s00442-005-0177-2
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). In this context, the reproductive strategies of females may vary depending on the environmental conditions (Crump 1984Crump ML (1984) Intraclutch egg size variability in Hyla crucifer (Anura: Hylidae). Copeia 1984(2): 302-308. https://www.jstor.org/stable/1445185?seq=1
https://www.jstor.org/stable/1445185?seq...
, Pupin et al. 2018Pupin NC, Haddad CFB, Prado CPA (2018) Maternal provisioning by foam-nesting frogs of the genus Physalaemus (Anura, Leptodactylidae) in contrasting environments. Amphibia-Reptilia 39(1): 120-125. https://doi.org/10.1163/15685381-00003146
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). Another important aspect is mate choice and anuran females often choose their mates (Morris 1989Morris MR (1989) Female choice of large males in the treefrog Hyla chrysoscelis: the importance of identifying the scale of choice. Behavioral Ecology and Sociobiology 25: 275-281. https://doi.org/10.1007/BF00300054
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), favoring males that may confer them the greatest reproductive success, but strategies may vary among species (Pfennig 2000Pfennig KS (2000) Female spadefoot toads compromise on mate quality to ensure conspecific matings. Behavioral Ecology 11(2): 220-227. https://doi.org/10.1093/beheco/11.2.220
https://doi.org/10.1093/beheco/11.2.220...
, Pettitt et al. 2013Pettitt BA, Bourne GR, Bee MA (2013) Advertisement call variation in the golden rocket frog (Anomaloglossus beebei): Evidence for individual distinctiveness. Ethology 119(3): 244-256. https://doi.org/10.1111/eth.12058
https://doi.org/10.1111/eth.12058...
, Valencia-Aguilar et al. 2020Valencia-Aguilar A, Zamudio KR, Haddad CFB, Bogdanowicz SM, Prado CPA (2020) Show me you care: female mate choice based on egg attendance rather than male or territorial traits. Behavioral Ecology 31: 1054-1064. https://doi.org/10.1093/beheco/araa051
https://doi.org/10.1093/beheco/araa051...
). Within the broader framework of sexual selection, some species may exhibit assortative mating. In such cases, females may choose males with traits similar to their own, such as those with aposematic color patterns (Reynolds and Fitzpatrick 2007Reynolds RG, Fitzpatrick BM (2007) Assortative mating in poison dart frogs based on an ecologically important trait. Evolution 61(9): 2253-2259. https://doi.org/10.1111/j.1558-5646.2007.00174.x
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) or males of similar body sizes, which allows for a closer juxtaposition of the cloa cae during mating, increasing fertilization rates (Licht 1976Licht LE (1976) Sexual selection in toads (Bufo americanus). Canadian Journal of Zoology 54(8): 1277-1284. https://doi.org/10.1139/z76-145
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, Bastos and Haddad 1996Bastos RP, Haddad CFB (1996) Breeding activity of neotropical treefrog Hyla elegans (Anura: Hylidae). Journal of Herpetolology 30(3): 355-360. https://www.jstor.org/stable/1565172?seq=1
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).

Although anuran territorial behavior is well studied (Fellers 1979Fellers GM (1979) Aggression, territoriality, and mating behaviour in North American treefrogs. Animal Behaviour 27(1): 107-119. https://doi.org/10.1016/0003-3472(79)90131-3
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, Bee 2016Bee MA (2016) Social recognition in anurans. In: Bee MA, Miller CT (Eds) Psychological mechanisms in animal communication. Animal Signals and Communication. Springer, Cham, vol. 5, 169-221. https://doi.org/10.1007/978-3-319-48690-1_7
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), the vast majority of the knowledge regarding this issue comes from direct natural history observations (e.g. Oliveira et al. 2011Oliveira FFR, Nogueira PAG, Eterovick PC (2011) Natural history of Phyllomedusa megacephala (Miranda-Ribeiro, 1926) (Anura: Hylidae) in southeastern Brazil, with descriptions of its breeding biology and male territorial behaviour. Journal of Natural History 46(1-2): 117-129. https://doi.org/10.1080/00222933.2011.626127
https://doi.org/10.1080/00222933.2011.62...
) or experiments using playbacks (e.g. Amézquita et al. 2005Amézquita A, Castellanos L, Hödl W (2005) Auditory matching of male Epipedobates femoralis (Anura: Dendrobatidae) under field conditions. Animal Behaviour 70(6): 1377-1386. https://doi.org/10.1016/j.anbehav.2005.03.012
https://doi.org/10.1016/j.anbehav.2005.0...
). Regardless of being well established in herpetology, these approaches have some limitations: naturalistic observations depend on chance to describe some behaviors and are purely descriptive, while playback experiments are unable to address multimodal communication. In contrast, in situ experiments investigating interactions between two or more individuals are rare (e.g. Hagen et al. 2016Hagen L, Rodríguez A, Menke N, Göcking C, Bisping M, Frommolt K, Ziegler T, Bonkowski M, Vences M (2016) Vocalizations in juvenile anurans: common spadefoot toads (Pelobates fuscus) regularly emit calls before sexual maturity. The Science of Nature 103: 75. https://doi.org/10.1007/s00114-016-1401-0
https://doi.org/10.1007/s00114-016-1401-...
), however, they allow for a factorial design and can be more informative than the aforementioned approaches. This becomes more important when we consider that multimodal signaling seems to be more common and important for anuran social behavior than previously thought (Hartmann et al. 2004Hartmann MT, Hartmann PA, Haddad CFB (2004) Visual signaling and reproductive biology in a nocturnal treefrog, genus Hyla (Anura: Hylidae). Amphibia-Reptilia 25(4): 395-406. https://doi.org/10.1163/1568538042788933
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, Richardson et al. 2010Richardson C, Gomez D, Durieux P, Théry M, Joly P, Léna J, Plénet S, Lengagne T (2010) Hearing is not necessarily believing in nocturnal anurans. Biology Letters 6(5): 633-635. https://doi.org/10.1098/rsbl.2010.0038
https://doi.org/10.1098/rsbl.2010.0038...
, Starnberger et al. 2014Starnberger I, Preininger D, Hödl W (2014) From uni to multimodality: towards an integrative view on anuran communication. Journal of Comparative Physiology A 200: 777-787. https://doi.org/10.1007/s00359-014-0923-1
https://doi.org/10.1007/s00359-014-0923-...
).

Boana goiana (B. Lutz, 1968) is an interesting model orga nism to study aspects of the reproductive biology of both male and female anurans. The species is a gladiator frog distributed in the central Brazilian states of Goiás, Minas Gerais and in the Distrito Federal (Frost 2020Frost DR (2020) Amphibian species of the world: an online reference. American Museum of Natural History, version 6.1. http://research.amnh.org/herpetology/amphibia/index.php [Acessed: 27/07/2020]
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). In the rainy season, males of this species call perched on the vegetation surrounding water bodies (Menin et al. 2004Menin M, Silva RA, Giaretta AA (2004) Reproductive biology of Hyla goiana (Anura, Hylidae). Iheringia, Série Zoologia, 94(1): 49-52. https://doi.org/10.1590/S0073-47212004000100008
https://doi.org/10.1590/S0073-4721200400...
). Furthermore, males of B. goiana are known to display territorial behavior and to be faithful to calling sites (Menin et al. 2004Menin M, Silva RA, Giaretta AA (2004) Reproductive biology of Hyla goiana (Anura, Hylidae). Iheringia, Série Zoologia, 94(1): 49-52. https://doi.org/10.1590/S0073-47212004000100008
https://doi.org/10.1590/S0073-4721200400...
, Dias et al. 2017Dias TM, Prado CPA, Bastos RP (2017) Nightly calling patterns in a Neotropical gladiator frog. Acta Ethologica 20(3): 207-214. https://doi.org/10.1007/s10211-017-0263-6
https://doi.org/10.1007/s10211-017-0263-...
). Although some studies on the species’ biology have already been published (Bastos et al. 2003Bastos RP, Bueno MAF, Dutra SL, Lima LP (2003) Padrões de vocalização de anúncio em cinco espécies de Hylidae (Amphibia: Anura) do Brasil Central. Comunicações do Museu de Ciências de Tecnologia da PUCRS, Série Zoologia, 16(1): 39-51., Menin et al. 2004Menin M, Silva RA, Giaretta AA (2004) Reproductive biology of Hyla goiana (Anura, Hylidae). Iheringia, Série Zoologia, 94(1): 49-52. https://doi.org/10.1590/S0073-47212004000100008
https://doi.org/10.1590/S0073-4721200400...
, Morais et al. 2016Morais AR, Siqueira MN, Márquez R, Bastos RP (2016) Males of Hypsiboas goianus (Anura; Hylidae) do not assess neighbor fighting ability through acoustic interactions. Acta Ethologica 19(1): 43-50. https://doi.org/10.1007/s10211-015-0221-0
https://doi.org/10.1007/s10211-015-0221-...
, Dias et al. 2017Dias TM, Prado CPA, Bastos RP (2017) Nightly calling patterns in a Neotropical gladiator frog. Acta Ethologica 20(3): 207-214. https://doi.org/10.1007/s10211-017-0263-6
https://doi.org/10.1007/s10211-017-0263-...
), little is known about the reproductive ecology and dynamics of male territoriality. Because of their territorial behavior and the presence of weaponry in males, B. goiana is particularly suitable to investigate the effect of competitor density on the reproductive and territorial behavior of hylids. Competitor density is known to affect territorial and reproductive behavior in many animal groups, such as teleost fishes (e.g. Kaspersson et al. 2010Kaspersson R, Höjesjö J, Pedersen S (2010) Effects of density on foraging success and aggression in age-structured groups of brown trout. Animal Behaviour 79: 709-715. https://doi.org/10.1016/j.anbehav.2009.12.025
https://doi.org/10.1016/j.anbehav.2009.1...
, Magellan et al. 2011Magellan K, Richardson T, Filmalter JD, Forget F, Midgley C, Kaiser H (2011) Competitor density influences resource defence in a Poeciliid fish. Journal of Applied Icthyology 27: 912-915. https://doi.org/10.1111/j.1439-0426.2010.01577.x.
https://doi.org/10.1111/j.1439-0426.2010...
), spiders (e.g. Ritschoff 2010Rittschoff CC (2010) Male density affects large-male advantage in the golden silk spider, Nephila clavipes. Behavioral Ecology 21(5): 979-985. https://doi.org/10.1093/beheco/arq099
https://doi.org/10.1093/beheco/arq099...
) and passerine birds (e.g. Foltz et al. 2015Foltz SL, Ross AE, Laing BT, Rock RP, Battle KE, Moore IT (2015) Get off my lawn: increased aggression in urban song sparrows is related to resource availability. Behavioral Ecology 26(6): 1548-1557. https://doi.org/10.1093/beheco/arv111
https://doi.org/10.1093/beheco/arv111...
). Investigations regarding the effect of competitor density in the social behavior of amphibians, conversely, focus mostly on issues such as mating success and amplexus duration (e.g. Chuang et al. 2013Chuang M, Bee MA, Kam Y (2013). Short amplexus duration in a territorial anuran: a possible adaptation in response to male-male competition. PLoS One 8(12): e83116. https://doi.org/10.1371/journal.pone.0083116
https://doi.org/10.1371/journal.pone.008...
), with territoriality being a neglected aspect. The concept of economic defendability predicts that male competition will increase with density if the resource value outweighs the cost of defense (Grant 1993Grant JWA (1993) Whether or not to defend? The influence of resource distribution. Marine and Freshwater Behaviour and Physiology 23: 137-153. https://doi.org/10.1080/10236249309378862
https://doi.org/10.1080/1023624930937886...
). This prediction can be applied to B. goiana: mating is restricted to the reproductive season, meaning that female availability is restricted in time, and males occupy and defend spatially limited calling perches (Dias et al. 2017Dias TM, Prado CPA, Bastos RP (2017) Nightly calling patterns in a Neotropical gladiator frog. Acta Ethologica 20(3): 207-214. https://doi.org/10.1007/s10211-017-0263-6
https://doi.org/10.1007/s10211-017-0263-...
). In this context, competitor density and prior establishment of territories, i.e. the resident effect (Baugh and Forester 1994Baugh JR, Forester DC (1994) Prior residence effect in the dart-poison frog, Dendrobates pumilio. Behaviour 131(3/4): 207-224. https://doi.org/10.1163/156853994X00442
https://doi.org/10.1163/156853994X00442...
), likely affect the social behavior of B. goiana. Lastly, studies that provide basic information of a species’ life history, ecology and behavior are important because not only they provide basic information for conservation purposes, but they also provide background knowledge for testing more elaborated hypotheses, and B. goiana is a potentially interesting organism to provide such information.

In the present study, we investigated the reproductive ecology and the dynamics of the territorial behavior of B. goiana, combining in-situ experiments with natural history observations. We hypothesized that: 1) because size is related to success in contests, large males will be more aggressive and will dominate interactions without a prior resident, and these contests will escalate with time; 2) because resources are restricted across time and space, an increase in competitor density will increase the intensity of aggressive behaviors displayed by resident males towards intruders; and 3) because similar body sizes facilitate cloacal juxtaposition, females will display size-assortative mate choice. We also tried to answer the following questions: a) Do large males arrive at the reproductive area early in the reproductive season? b) Is there a positive relationship between female size and clutch size? c) Is there a trade-off between egg size and number of eggs per clutch?

MATERIAL AND METHODS

The study was conducted at the Floresta Nacional de Silvânia (FNS; 16°39’32”S, 48°36’29” W, elevation ca. 900 m), municipality of Silvânia, state of Goiás, central-western Brazil. The FNS is located in the Cerrado domain and includes many vegetation types, one of which is the gallery forest, where we conducted this study (sensu Oliveira-Filho and Ratter 2002Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomies and wood flora of the Cerrado biome. In: Oliveira PS, Marquis RJ (Eds) The Cerrado of Brazil. Columbia University Press, New York, 91-120.). According to Koppen’s classification (Peel et al. 2007Peel MC, Finlayson BL, Mcmahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences Discussions, European Geosciences Union 4(2): 439-473. https://hal.archives-ouvertes.fr/hal-00298818/document
https://hal.archives-ouvertes.fr/hal-002...
), the study area is characterized by a tropical savanna climate (Aw), with two well-defined seasons, a rainy season from October to March and a dry season from April to September.

Data collection

Territoriality

During the reproductive seasons of 2012-13 and 2013-14, we conducted territoriality experiments in the field. We placed B. goiana males 100 cm above the ground because this height is the most commonly observed in nature (Menin et al. 2004Menin M, Silva RA, Giaretta AA (2004) Reproductive biology of Hyla goiana (Anura, Hylidae). Iheringia, Série Zoologia, 94(1): 49-52. https://doi.org/10.1590/S0073-47212004000100008
https://doi.org/10.1590/S0073-4721200400...
). The usual distance between males in natural environments is around 200 cm, and distances smaller than 100 cm are rare (Menin et al. 2004). Thus, we placed males 50 cm apart to maximize their behavioral response in the establishment and defense of the territory.

To test our first two hypotheses, we designed two territoriality experiments. In the first experiment we tested if male size related to calling behavior and social status in a contest without prior residence - since resident males may be more likely to win due to different motivation rates (Baugh and Forester 1994Baugh JR, Forester DC (1994) Prior residence effect in the dart-poison frog, Dendrobates pumilio. Behaviour 131(3/4): 207-224. https://doi.org/10.1163/156853994X00442
https://doi.org/10.1163/156853994X00442...
). For that, we chose two males in calling activity that were at approximately 2 m from each other. Next, the two males were taken to another place within the reproductive area. There, the males were placed on a small tree 100 cm above the ground and were initially 50 cm apart. We waited until one of them started calling and counted the number of advertisement calls and aggressive calls emitted by both males during two minutes. The counting of the calls was repeated 15 and 30 minutes later, totaling three counting periods (initial, 15, 30 min). We also determined the distance between the males with a measuring tape in each counting period. After the third counting period, the experiment was terminated and males were measured with a digital caliper (0.01 mm). We replicated this experiment 15 times with different males at each trial. For each two-minute counting period performed, the behavioral responses of males were also recorded using the focal animal method (Altman 1974Altman J (1974) Observational study of behaviour: sampling methods. Behaviour 49(3/4): 227-265. Stable URL: https://www.jstor.org/stable/4533591?seq = 1
https://www.jstor.org/stable/4533591?seq...
).

To test our second hypothesis, we designed a second experiment, in which we arrived at the reproductive area and searched for two males that were up to 400 cm apart, so that we could see both simultaneously. These males were considered resident males. During two minutes we counted the number of advertisement calls and aggressive calls emitted by them. Following this, we increased male density by searching for a third male (first intruder), which was placed between the resident males. We waited until the intruder male started to call and once again counted the number of advertisement and aggressive calls emitted by the resident males, during two minutes. We also used a measuring tape to measure the distance between all males. This procedure was repeated until a second and then a third intruder was placed in the area. After counting the calls and measuring the distance between the males, the experiment was terminated. A total of four counting periods were performed, including: 1) two resident males; 2) adding one intruder male; 3) adding a second intruder; 4) adding a third intruder. We replicated this experiment six times, with different males used at each trial. Males were also measured as described above. For each two-minute counting period performed, the behavioral responses of males were also recorded employing the focal animal method (Altman 1974Altman J (1974) Observational study of behaviour: sampling methods. Behaviour 49(3/4): 227-265. Stable URL: https://www.jstor.org/stable/4533591?seq = 1
https://www.jstor.org/stable/4533591?seq...
).

Reproductive ecology

We visited the reproductive area during the 1996-97, 1997-98, 2005-06, 2006-07, 2012-13 and 2013-14 rainy seasons. Data obtained before 2012 were used only to verify size-assortative mating and test our third hypothesis. Data for the remaining exploratory objectives were obtained exclusively from 2012 onwards. We searched for pairs in amplexus after sunset (around 07:00 p.m.) and, when captured, placed them in plastic bags containing water and waited for them to spawn; after which we returned the pair and the clutch to the sample site. Amplectant pairs were collected because the reproductive site (a stream) used by B. goiana prevented us from sampling eggs spawned directly in the field - some eggs could be carried away by the water flow and/or remain hidden in detritus, resulting in unreliable data. For each clutch we counted the number of eggs and collected 10 eggs to be measured. The eggs were fixed in 10% formalin and deposited at the Coleção Zoológica da Universidade Federal de Goiás (ZUFG). We measured egg diameter in the laboratory using a Zeiss stereomicroscope with a scaled background, to the nearest 0.01 mm, and calculated clutch volume according to Guimarães et al. (2011Guimarães TCS, de Figueiredo GB, Mesquita DO, Vasconcellos MM (2011) Ecology of Hypsiboas albopunctatus (Anura: Hylidae) in a Neotropical Savanna. Journal of Herpetology 45(2): 244-250. https://doi.org/10.1670/09-255.1
https://doi.org/10.1670/09-255.1...
). We also measured the snout-vent length (SVL) and mass of all males and females with a digital caliper (0.01 mm) and a digital scale (0.01 g), respectively. Lastly, we also marked the individuals with subcutaneous implants (alphanumeric fluorescent tags visible under ultraviolet light, Northwest Marine Technology, Inc.) to avoid pseudoreplication.

Data analyses

Before performing the analyses, all variables were log-transformed and tested for normal distribution (Zar 1999Zar JH (1999) Biostatistical Analysis. Prentice Hall, New Jersey, 663 pp.). A ln(x+1) transformation was adopted if the data matrix included zeroes, whilst a ln(x) transformation was adopted for the remaining variables. All tests were performed in the R software (R Development Core Team 2013R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.Rproject.org
http://www.Rproject.org...
).

Territoriality

For each replicate of the first experiment, we labelled the male who emitted more calls as the alpha, and the other was considered the beta. To determine the establishment of dominance between the males and the validity of our alpha-beta classification, we tested if the supposed alphas and betas differed in the number of calls emitted during the experiment using a paired t-test. Since the difference was statistically significant (t[14] = 6.35, p < 0.001), i.e., alpha males emitted more calls, we considered our classification as valid.

To test whether alpha males were larger than betas, we compared their SVL with a paired t-test. For the experiments, we considered the variable “male size” as a composite measure obtained by using the scaled mass index, an allometric index that accounts for the different scaling rates of body length and mass (Peig and Green 2009Peig 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. https://doi.org/10.1111/j.1600-0706.2009.17643.x
https://doi.org/10.1111/j.1600-0706.2009...
). To investigate if male behavior escalated through time, we tested whether number of calls emitted by males varied among the counting periods (initial, 15 min, and 30 min later) performing two repeated-measure ANCOVAs (one test for the advertisement calls and another for the aggressive calls). We used the distance between males and male size as covariates. For these tests, only one randomly chosen male (either the alpha or the beta male) was included in the analyses. Thus, while there was only one distance value possible, the variable “male size” always corresponded to the male that was chosen.

In the second experiment, to evaluate if an increase in the number of nearby males affected the number of calls emitted by the resident males, we compared these variables among the counting periods. For that, we performed two repeated-measure ANCOVAs (one test for the advertisement calls and another for the aggressive calls), using the distance to the nearest male and male size as covariates. The variable “male size” was determined as described for the first experiment. For these tests, only one randomly chosen resident male was included in the analyses. Thus, both “distance to the nearest male” and “male size” referred specifically to the male that was chosen.

Reproductive ecology

To analyze if mating was assortative regarding body size, we performed a Pearson’s Correlation test between the SVLs of males and females in amplexus. To increase the robustness of this analysis, we included previously obtained data from the 1996-97, 1997-98, 2005-06 and 2006-07 reproductive seasons, as well as the data obtained from 2012-2013 onwards. To examine if clutch size (number of eggs per clutch) and clutch volume (number of eggs per clutch*egg volume) were correlated with female SVL, and whether egg size was correlated with the number of eggs per clutch, we performed simple linear regressions. To examine the body size profile (and, therefore, the age) of males of the studied population, we performed a one-way ANOVA to test if SVL of males differed among the months of the reproductive season.

Ethical and legal standards

We performed the procedures and experiments detailed in this study in strict accordance to the Brazilian federal and state laws regulating the sampling of animal species, their welfare and their use for research purposes. Sampling and handling of animals were authorized under ICMBio permit #40668-1.

RESULTS

Territoriality

In the first experiment, alpha males were significantly larger than beta males (SVL, t[14] = 2.37, p = 0.03) (Fig. 1). The SVL of alpha males ranged from 31.03 to 34.33 mm (average = 33.10 ± 0.94, n = 15) and body mass from 1.14 to 1.61 g (average = 1.41 ± 0.13, n = 15); while the SVL of beta males varied from 28.80 to 33.60 mm (average = 31.94 ± 1.42, n = 15) and body mass from 1.01 to 1.59 g (average = 1.33 ± 0.15, n = 15). The number of advertisement and aggressive calls emitted by males did not significantly differ among periods (i.e. behaviors did not escalate), and the number of advertisement calls was positively influenced by male body size, while the number of aggressive calls was positively influenced by the distance between males (Table 1).

Figure 1
Body size (SVL) of the alpha and beta males of Boana goiana sampled in the first territoriality experiment, in Silvânia, Goiás, Brazil; bar height represents the range between the first and third quartiles, whiskers represent maximum and minimum values, horizontal bars represent the median, gray bar represents alpha males, white bar represents beta males, (*) indicates statistically significant differences.

Table 1
Results for the first and second territoriality experiments: the repeated measures ANCOVAs for the effect of the period, distance between the males and male size on the variation of the number of calls emitted by males of Boana goiana are shown for both experiments. Distance and size were used as covariates. Statistically significant values of “p” are shown in bold.

Of a total of 15 replicates in the first experiment, the frequencies of the observed behavioral responses were as follows: (a) males only walked away from each other (n = 3); (b) males only approached each other (n = 2); (c) males walked away and then approached each other (n = 2); (d) males approached and then walked away from each other (n = 6); (e) one male amplected a female that approached him during the experiment (n = 1); (f) one male approached the other, initiated physical contact and caused both males to fall to the ground (n = 1).

In the second experiment, the number of aggressive calls emitted by resident males increased with male size and with the distance between males (Table 1). The number of advertisement calls was not influenced by any of the tested variables (Table 1). Frequencies of the observed behavioral responses, of a total of six replicates, were as follows: a) the introduced male behaved as satellite male (n = 2); b) one resident male and one introduced male behaved as satellite males (n = 1); c) one resident male walked away (n = 1); d) the introduced male walked away (n = 2); e) one resident male engaged in physical combat with one introduced male, both fell to the ground and resumed calling activity after a few minutes (n = 1).

To further explore how the co-variables influenced calling behavior in the territoriality experiments, we ran a series of a posteriori tests. For the first experiment, we performed two random-effects GLMs, one for each type of call. We used a Poisson distribution model with a log link, and the repeated-measures (i.e. individuals across time) as the random effect. To fit these models, instead of an ln+1 transformation, we used raw data scaled within the model. The results showed that the number of advertisement calls was positively related to both male size and distance between the males, while the number of aggressive calls was positively related only to the distance between males (Table 2). The same approach was chosen for the second experiment, with one random-effect GLM for each type of call, using the same parameters described above. No effects were reported for the advertisement calls, while aggressive calls were positively influenced by both male size and distance to the nearest male (Table 2, Figs 2, 3). Because the ANCOVAs showed the effect of time to be non-significant (Table 1), we dismissed it as a variable in the GLMs. We performed these analyses in the R software using the “nlme4” package.

Figures 2-3
Relationship between the number of aggressive calls emitted by the resident male and (2) the distance to the nearest male, and (3) male size of Boana goiana in the second territoriality experiment, in Silvânia, Goiás, Brazil; (*) predictor variables were scaled to fit the model.

Figure 4
Body size (SVL) of males of Boana goiana along the months of the reproductive season 2013/2014, in Silvânia, Goiás, Brazil. Black circles indicate the means, whiskers indicate the standard deviation.

Table 2
Results of the random-effect GLMs performed as a posteriori analyses for the two territoriality experiments; number of advertisement and aggressive calls were used as response-variables; predictor variables were distance between males and male size for the first experiment, and distance to the nearest male and male size for the second experiment; statistically significant values of “p” are shown in bold.

Reproductive ecology

The clutches contained on average 164.88 ± 30.18 eggs (range = 105 - 207 eggs; n = 9) and the average diameter of eggs was 1.68 ± 0.16 mm (range = 1.39 - 1.96 mm; n = 90 eggs from 9 clutches). As we marked and recaptured individuals (Table 3), we were able to observe that from the nine clutches we sampled, two were fertilized by the same male (176 and 150 eggs, with a 24 h interval between them) and two were laid by the same female (151 and 207 eggs, with a 33-day interval between them).

Table 3
Captures and recaptures of males of Boana goiana in Silvânia, Goiás, Brazil. First season: January 2013 to May 2013; Second season: October 2013 to May 2014.

Male SVL ranged from 28.53 to 37.48 mm (average = 32.55 ± 1.46 mm, n = 217) and male mass from 1.01 to 1.61 g (average = 1.34 ± 0.13, n = 57). Female SVL ranged from 34.40 to 37.48 mm (average = 35.84 ± 0.10, n = 8) and female mass from 1.39 to 1.92 g (average = 1.72 ± 0.19, n = 8). We did not find any relationship between female SVL and the number of eggs per clutch, between female SVL and clutch volume, nor between egg size and the number of eggs per clutch (F[1,7] = 1.32, r²adj = 0.04, p = 0.28; F[1,7] = 1.39, r²adj = 0.04, p = 0.27; F[1,7] = 0.43, r²adj = -0.076, p = 0.53; n = 8, respectively). Body size (SVL) of males and females in amplexus were positively correlated (r = 0.65, p < 0.001, n = 14). Male to female SVL ratio averaged 0.911 ± 0.03 (range = 0.86-0.97 mm). Male SVL varied among months, i.e., in the last months of the reproductive season (March, April and May), males were smaller compared to males of all other months (F[5,211] = 4.59, p < 0.001). Mean SVL of males from December to February was 32.75 ± 1.57 mm (range = 28.58-37.48 mm; n = 107) and from March to May it was 32.34 ± 1.31 mm (range = 28.53-35.23 mm; n = 110) (Fig. 4).

In the 2012-13 reproductive season, we marked 108 individuals (4 females and 104 males), and in the reproductive season of 2013-14 we marked 128 individuals (5 females and 123 males). However, no individual marked in the first season was recaptured in the second reproductive season. The total number of individuals captured and recaptured is shown in Table 3. Recapture intervals ranged from 1 to 84 days.

DISCUSSION

Male anurans emit advertisement calls to attract females and announce their position to nearby males competing for the same territories and/or females (Wells 1977aWells KD (1977a) The social behaviour of anuran amphibians. Animal Behaviour 25(3): 666-693. https://doi.org/10.1016/0003-3472(77)90118-X
https://doi.org/10.1016/0003-3472(77)901...
). In many species, males can recognize the size and, consequently, the condition of their opponents evaluating the characteristics of the advertisement calls, which allows males to avoid fights they have low probabilities to win (Wells 1978Wells KD (1978) Territoriality in the green frog (Rana clamitans): vocalizations and agonistic interactions. Animal Behaviour 26(4): 1051-1063. https://doi.org/10.1016/0003-3472(78)90094-5
https://doi.org/10.1016/0003-3472(78)900...
, Robertson 1986Robertson JGM (1986) Male territoriality, fighting and assessment of fighting ability in the Australian frog Uperoleia rugosa. Animal Behaviour 34: 763-772. https://doi.org/10.1016/S0003-3472(86)80060-4
https://doi.org/10.1016/S0003-3472(86)80...
, Bee and Perril 1996Bee MA, Perril SA (1996) Responses to conspecific advertisement calls in the green frog (Rana clamitans) and their role in male-male communication. Behaviour 133(3/4): 283-301. https://doi.org/10.1163/156853996X00152
https://doi.org/10.1163/156853996X00152...
, Nali and Prado 2014Nali RC, Prado CPA (2014) Complex call with different messages in Bokermannohyla ibitiguara (Anura, Hylidae), a gladiator frog of the Brazilian Cerrado. Journal of Herpetology 48(3): 407-414. https://doi.org/10.1670/13-090
https://doi.org/10.1670/13-090...
). Thus, when body condition asymmetries between males are large and more easily assessed, less intense encounters are expected, because weaker individuals will probably give up earlier (Bee 2002Bee MA (2002) Territorial male bullfrogs (Rana catesbeiana) do not assess fighting ability based on size related variation in acoustic signals. Behavioral Ecology 13(1): 109-124. https://doi.org/10.1093/beheco/13.1.109
https://doi.org/10.1093/beheco/13.1.109...
). In our first experiment, the alpha males were larger than the betas, and the number of advertisement calls was positively correlated with male condition. This partially corroborates our first hypothesis, and suggests that males of B. goiana may be assessing the condition of their opponents through their calls, and thus avoiding costly conflicts with large males. However, a recent study on the acoustic behavior of B. goiana showed that males did not alter their vocal activity in response to playbacks simulating a larger opponent (Morais et al. 2016Morais AR, Siqueira MN, Márquez R, Bastos RP (2016) Males of Hypsiboas goianus (Anura; Hylidae) do not assess neighbor fighting ability through acoustic interactions. Acta Ethologica 19(1): 43-50. https://doi.org/10.1007/s10211-015-0221-0
https://doi.org/10.1007/s10211-015-0221-...
), suggesting that males may not be able to assess their opponents’ size solely through their calls.

If B. goiana males do not assess the condition of their opponents via their calls to avoid unnecessary fights, what could explain the low prevalence of physical contact during contests? We suggest two non-exclusive explanations. The first relates to fighting motivation: if males had already mated before the experiments, this should decrease their motivation to engage in costly contest behaviors (Brown et al. 2007Brown WD, Chimenti AJ, Siebert JR (2007) The payoff of fighting in house crickets: motivational asymmetry increases male aggression and mating success. Ethology 113(5): 457-465. https://doi.org/10.1111/j.1439-0310.2007.01357.x
https://doi.org/10.1111/j.1439-0310.2007...
). In anurans, energetic depletion, and the resulting decrease in motivation, may occur before any measurable decrease in body condition (e.g. bullfrogs, Hettyey et al. 2009Hettyey A, Vági B, Hévizi G, Török J (2009) Changes in sperm stores, ejaculate size, fertilization success, and sexual motivation over repeated matings in the common toad, Bufo bufo (Anura: Bufonidae). Biological Journal of the Linnean Society 96(2): 361-371. https://doi.org/10.1111/j.1095-8312.2008.01126.x
https://doi.org/10.1111/j.1095-8312.2008...
). Because we performed most of our experiments in the middle-late reproductive season (January-May), and given the constraints of in-situ experimental designs, if some males had previously mated, they are less likely to engage in costly confrontations with other males. The second explanation deals with the low frequency of scars in males: very few males used in the experiments had scars, contrasting to species such as Boana curupi (Garcia, Faivovich & Haddad, 2007), in which 90% of the males exhibited fighting scars (Candaten et al. 2020Candaten A, Possenti AG, Mainardi AA, Rocha MC, Palaoro AV (2020) Fighting scars: Heavier Gladiator frogs bear more injuries than lighter frogs. Acta Ethologica 23: 39-44. https://doi.org/10.1007/s10211-019-00333-7
https://doi.org/10.1007/s10211-019-00333...
). This could mean that either B. goiana is inherently less aggressive than other gladiator frogs or, alternatively, that resources were not limited enough to motivate aggression (Arnott and Elwood 2008Arnott G, Elwood RW (2008) Information gathering and decision making about resource value in animal contests. Animal Behaviour 76(3): 529-542. https://doi.10.1016/j.anbehav.2008.04.019
https://doi.10.1016/j.anbehav.2008.04.01...
). For example, males of B. curupi fight to monopolize a few oviposition sites along a stream, while oviposition in B. goiana occurred along the entire stream area (Dias et al. 2017Dias TM, Prado CPA, Bastos RP (2017) Nightly calling patterns in a Neotropical gladiator frog. Acta Ethologica 20(3): 207-214. https://doi.org/10.1007/s10211-017-0263-6
https://doi.org/10.1007/s10211-017-0263-...
, Candaten et al. 2020Candaten A, Possenti AG, Mainardi AA, Rocha MC, Palaoro AV (2020) Fighting scars: Heavier Gladiator frogs bear more injuries than lighter frogs. Acta Ethologica 23: 39-44. https://doi.org/10.1007/s10211-019-00333-7
https://doi.org/10.1007/s10211-019-00333...
). However, to further test these hypotheses, comparisons among different populations and experiments controlling for previous matings are necessary. Nonetheless, it is important to highlight that the argument that B. goiana males do not evaluate their opponent’s size via their calls comes from an experiment using playback (Morais et al. 2016Morais AR, Siqueira MN, Márquez R, Bastos RP (2016) Males of Hypsiboas goianus (Anura; Hylidae) do not assess neighbor fighting ability through acoustic interactions. Acta Ethologica 19(1): 43-50. https://doi.org/10.1007/s10211-015-0221-0
https://doi.org/10.1007/s10211-015-0221-...
). Thus, another possibility is that males of this species employ a multimodal communication, assessing their opponents using more than one type of signal, such as visual ones (Starnberger et al. 2014Starnberger I, Preininger D, Hödl W (2014) From uni to multimodality: towards an integrative view on anuran communication. Journal of Comparative Physiology A 200: 777-787. https://doi.org/10.1007/s00359-014-0923-1
https://doi.org/10.1007/s00359-014-0923-...
). Combination of acoustic and visual signals have been reported for several anuran species, including hylids closely related to B. goiana, such as Boana albomarginata (Spix, 1824) and Boana albopunctata (Spix, 1824) (Giasson and Haddad 2006Giasson LOM, Haddad CFB (2006) Social interactions in Hypsiboas albomarginatus (Anura: Hylidae) and the significance of acoustic and visual signals. Journal of Herpetology 40(2): 171-180. https://doi.org/10.1670/205-05A.1
https://doi.org/10.1670/205-05A.1...
, Toledo et al. 2007Toledo LF, Araújo OGS, Guimarães LD, Lignau R, Haddad CFB (2007) Visual and acoustic signaling in three species of Brazilian nocturnal tree frogs (Anura, Hylidae). Phyllomedusa 6(1): 61-68. http://www.phyllomedusa.esalq.usp.br/articles/volume6/number1/616168.pdf
http://www.phyllomedusa.esalq.usp.br/art...
). These visual signals occur even in nocturnal species (Hartmann et al. 2004Hartmann MT, Hartmann PA, Haddad CFB (2004) Visual signaling and reproductive biology in a nocturnal treefrog, genus Hyla (Anura: Hylidae). Amphibia-Reptilia 25(4): 395-406. https://doi.org/10.1163/1568538042788933
https://doi.org/10.1163/1568538042788933...
) and may be very subtle, such as opening the mouth or inflating the vocal sac without calling (Lipinski et al. 2012Lipinski VM, Caldart VM, Iop S (2012) Visual communication in Hypsiboas curupi (Anura: Hylidae) at Parque Estadual do Turvo, southern Brazil. Phyllomedusa 11(1): 71-74. http://www.phyllomedusa.esalq.usp.br/articles/volume11/number1/1117174.pdf
http://www.phyllomedusa.esalq.usp.br/art...
), behaviors that were observed in B. goiana during our experiments (T.M. Dias, pers. obs.). Thus, a possibility remains that physical combats were rare during our study because males were able to use more than one source of information to assess their opponents’ size to avoid unnecessary conflicts, though this hypothesis needs further testing and does not exclude other possible explanations mentioned above.

The aggressive calls of B. goiana probably have the role of maintaining a spatial separation between calling males, and thus may serve as a warning to intruders (Wells 1977aWells KD (1977a) The social behaviour of anuran amphibians. Animal Behaviour 25(3): 666-693. https://doi.org/10.1016/0003-3472(77)90118-X
https://doi.org/10.1016/0003-3472(77)901...
, Dyson and Passmore 1992Dyson ML, Passmore NI (1992) Inter-male spacing and aggression in African painted reed frogs, Hyperolius marmoratus. Ethology 91(3): 237-247. https://doi.org/10.1111/j.1439-0310.1992.tb00865.x
https://doi.org/10.1111/j.1439-0310.1992...
). The reduction of the acoustic interference, achieved through the maintenance of spacing between males, may be more important for male reproductive success than the possession of a particular calling site (Whitney and Krebs 1975Whitney CL, Krebs JR (1975) Spacing and calling in Pacific Tree Frogs, Hyla regilla. Canadian Journal of Zoology 53(11): 1519-1527. https://doi.org/10.1139/z75-187
https://doi.org/10.1139/z75-187...
, Wells 1977aWells KD (1977a) The social behaviour of anuran amphibians. Animal Behaviour 25(3): 666-693. https://doi.org/10.1016/0003-3472(77)90118-X
https://doi.org/10.1016/0003-3472(77)901...
, Nali and Prado 2014Nali RC, Prado CPA (2014) Complex call with different messages in Bokermannohyla ibitiguara (Anura, Hylidae), a gladiator frog of the Brazilian Cerrado. Journal of Herpetology 48(3): 407-414. https://doi.org/10.1670/13-090
https://doi.org/10.1670/13-090...
). Resident males are also more likely to win territorial disputes, because the cost of losing a territory is higher for a resident (Wells 1978, Bee et al. 1999Bee MA, Perril SA, Owen PC (1999) Size assessment in simulated territorial encounters between male green frogs (Rana clamitans). Behavioral Ecology and Sociobiology 45: 177-184. https://doi.org/10.1007/s002650050551
https://doi.org/10.1007/s002650050551...
, Owen and Gordon 2005Owen PC, Gordon NM (2005) The effect of perceived intruder proximity and resident body size on the aggressive responses of male green frogs, Rana clamitans (Anura: Ranidae). Behavioral Ecology and Sociobiology 58: 446-455. https://doi.org/10.1007/s00265-005-0961-3
https://doi.org/10.1007/s00265-005-0961-...
). Additionally, large males usually win contests against small males (Howard 1978Howard RD (1978) The evolution of mating strategies in bullfrogs, Rana catesbeiana. Evolution 32: 850-871. https://doi.org/10.2307/2407499
https://doi.org/10.2307/2407499...
, Wells 1978Wells KD (1978) Territoriality in the green frog (Rana clamitans): vocalizations and agonistic interactions. Animal Behaviour 26(4): 1051-1063. https://doi.org/10.1016/0003-3472(78)90094-5
https://doi.org/10.1016/0003-3472(78)900...
). In our second experiment, large males emitted more aggressive calls and the more males in the chorus, the larger was the distance adopted by the nearest male. This suggests that males of B. goiana can detect the spatial position of other males and that intruder males can adjust their behavior according to the social context (Wells 1977bWells KD (1977b) Territoriality and male mating success in the green frog (Rana clamitans). Ecology 58(4): 750-762. https://doi.org/10.2307/1936211
https://doi.org/10.2307/1936211...
). Thus, maintaining a suitable distance from the resident male or avoiding areas where they are calling may be strategies adopted by intruder males of B. goiana to avoid undesired physi cal combats and/or acoustic interference. Similar behaviors were described for another species of gladiator frog, Bokermannohyla ibitiguara (Cardoso, 1983) (Nali and Prado 2012Nali RC, Prado CPA (2012) Habitat use, reproductive traits and social interactions in stream-dweller treefrog endemic to the Brazilian Cerrado. Amphibia-Reptilia 33(3/4): 337-347. https://doi.org/10.1163/15685381-00002836
https://doi.org/10.1163/15685381-0000283...
, 2014Nali RC, Prado CPA (2014) Complex call with different messages in Bokermannohyla ibitiguara (Anura, Hylidae), a gladiator frog of the Brazilian Cerrado. Journal of Herpetology 48(3): 407-414. https://doi.org/10.1670/13-090
https://doi.org/10.1670/13-090...
).

Interestingly, the increase in male density did not lead to an increase in aggression levels or any other change in calling behaviors (Table 1), dismissing our second hypothesis. General theory predicts that competition should become more intense the more valuable (or scarce) a resource is (Grant 1993Grant JWA (1993) Whether or not to defend? The influence of resource distribution. Marine and Freshwater Behaviour and Physiology 23: 137-153. https://doi.org/10.1080/10236249309378862
https://doi.org/10.1080/1023624930937886...
, Arnott and Elwood 2008Arnott G, Elwood RW (2008) Information gathering and decision making about resource value in animal contests. Animal Behaviour 76(3): 529-542. https://doi.10.1016/j.anbehav.2008.04.019
https://doi.10.1016/j.anbehav.2008.04.01...
). Since it does not seem to be the case for B. goiana, two explanations are possible. The first is a scenario where there are too many competitors, meaning that the costs of defense are high and any potential benefit does not pay off (Grant 1993Grant JWA (1993) Whether or not to defend? The influence of resource distribution. Marine and Freshwater Behaviour and Physiology 23: 137-153. https://doi.org/10.1080/10236249309378862
https://doi.org/10.1080/1023624930937886...
). This does not seem to be the case, because even though aggression levels were low, there was a clear establishment and defense of territories, with only two males adopting alternative strategies such as satellite behavior. The second explanation could be that resource value does not increase enough to motivate an increase in aggressive behavior. This makes sense when we consider that, in our case, the resource is a mating opportunity. Although we predicted such opportunities are restricted across both time (the reproductive season) and space (the reproductive site), the results showed that this may not be the case - there is evidence that females of B. goiana mate more than once in the same reproductive season (discussed in more details below, and see Results). If mating opportunities are not as restricted as previously thought, investing in increased aggression may not be an adaptive strategy because such behavior is costly and risky (Briffa and Sneddon 2007Briffa M, Sneddon LU (2007) Physiological constraints on contest behavior. Functional Ecology 21: 627-637. https://doi.org/10.1111/j.1365-2435.2006.01188.x
https://doi.org/10.1111/j.1365-2435.2006...
), and maintaining the spacing between calling males in a chorus seems to be a more cost-effective strategy, as indicated by our results discussed above (Tables 1 and 2, Figs 2, 3).

Although most males were territorial, some males behaved as satellite males (sensu Wells 2007Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chigago, 1148 pp. https://doi.org/10.7208/chicago/9780226893334.001.0001
https://doi.org/10.7208/chicago/97802268...
) during the territorial experi ments and this strategy was already observed for many anuran species (e.g. Toledo and Haddad 2005Toledo LF, Haddad CFB (2005) Reproductive biology of Scinax fuscomarginatus (Anura, Hylidae) in south-eastern Brazil. Journal of Natural History 39(32): 3029-3037. https://doi.org/10.1080/00222930500221403
https://doi.org/10.1080/0022293050022140...
, Leary et al. 2005Leary CJ, Fox DJ, Shepard DB, Garcia AM (2005) Body size, age, growth and alternative mating tactics in toads: satellite males are smaller but not younger than calling males. Animal Behaviour 70(3): 663-671. https://doi.org/10.1016/j.anbehav.2004.12.013
https://doi.org/10.1016/j.anbehav.2004.1...
, Nali and Prado 2012Nali RC, Prado CPA (2012) Habitat use, reproductive traits and social interactions in stream-dweller treefrog endemic to the Brazilian Cerrado. Amphibia-Reptilia 33(3/4): 337-347. https://doi.org/10.1163/15685381-00002836
https://doi.org/10.1163/15685381-0000283...
). This alternative strategy has been suggested to represent an attempt of males to intercept females approaching calling males or obtain a vacant territory (Wells 1977bRobertson JGM (1986) Male territoriality, fighting and assessment of fighting ability in the Australian frog Uperoleia rugosa. Animal Behaviour 34: 763-772. https://doi.org/10.1016/S0003-3472(86)80060-4
https://doi.org/10.1016/S0003-3472(86)80...
, Haddad 1991Haddad CFB (1991) Satellite behavior in the Neotropical treefrog Hyla minuta. Journal of Herpetology 25(2): 226-229. https://www.jstor.org/stable/1564657?seq=1
https://www.jstor.org/stable/1564657?seq...
). Another strategy would be engaging in a fight in order to obtain the resident’s territory. However, physical combats were rare during both experiments and never exceeded 5 s (T.M. Dias, pers. obs.). Aggressive behaviors can include both aggressive calls and physical combats (Wogel et al. 2002Wogel H, Abrunhosa PA, Pombal-Jr JP (2002) Atividade reprodutiva de Physalaemus signifer (Anura, Leptodactylidae) em ambiente temporário. Iheringia , Série Zoologia, 92(2): 57-70. https://doi.org/10.1590/S0073-47212002000200006
https://doi.org/10.1590/S0073-4721200200...
, Costa et al. 2010Costa TB, Guimarães LD, Bastos RP (2010) Comportamento territorial e de acasalamento de Phyllomedusa azurea (Anura, Hylidae) em uma lagoa temporária do centro-oeste do Brasil. Phyllomedusa 9(2): 99-108. https://doi.org/10.11606/issn.2316-9079.v9i2p99-108
https://doi.org/10.11606/issn.2316-9079....
Lemes et al. 2012Lemes P, Tessarolo G, Morais AR, Bastos RP (2012) Acoustic repertoire of Barycholos ternetzi (Anura: Strabomantidae) in central Brazil. South American Journal of Herpetology 7(2): 157-164. https://doi.org/10.2994/057.007.0205
https://doi.org/10.2994/057.007.0205...
). However, as costs of physical combats can be high, males of B. goiana may be investing more in aggressive calls and, sometimes, adopting a satellite posture, which may be important to decrease energy expenditure and avoid injuries that could be caused by fights (Kluge 1981Kluge AG (1981) The life history, social organization, and parental behavior of Hyla rosenbergi Boulenger a nest-building gladiator frog. Miscellaneous Publications Museum of Zoology University of Michigan 160: 1-170., Nali and Prado 2012Nali RC, Prado CPA (2012) Habitat use, reproductive traits and social interactions in stream-dweller treefrog endemic to the Brazilian Cerrado. Amphibia-Reptilia 33(3/4): 337-347. https://doi.org/10.1163/15685381-00002836
https://doi.org/10.1163/15685381-0000283...
). However, because satellite behavior only occurred in 2 of the 30 males used in the second experiment, the establishment of territories and maintenance of spacing between males mostly via calling behavior seems to be the norm for this population of B. goiana.

There was a positive relationship between the body size of males and females of B. goiana in amplexus, which indicates size-assortative mating and corroborates our third hypothesis. In some anuran species, females are able to assess male traits and choose those that might increase their fitness (Robertson 1990Robertson JGM (1990) Female choice increases fertilization success in the Australian frog, Uperoleia laevigata. Animal Behaviour 39: 639-645. https://doi.org/10.1016/S0003-3472(05)80374-4
https://doi.org/10.1016/S0003-3472(05)80...
, Reynolds and Fitzpatrick 2007Reynolds RG, Fitzpatrick BM (2007) Assortative mating in poison dart frogs based on an ecologically important trait. Evolution 61(9): 2253-2259. https://doi.org/10.1111/j.1558-5646.2007.00174.x
https://doi.org/10.1111/j.1558-5646.2007...
, Valencia-Aguilar et al. 2020Valencia-Aguilar A, Zamudio KR, Haddad CFB, Bogdanowicz SM, Prado CPA (2020) Show me you care: female mate choice based on egg attendance rather than male or territorial traits. Behavioral Ecology 31: 1054-1064. https://doi.org/10.1093/beheco/araa051
https://doi.org/10.1093/beheco/araa051...
). Size-assortative mating has been reported for some anurans and is suggested to favor a close juxtaposition of cloacae (Licht 1976Licht LE (1976) Sexual selection in toads (Bufo americanus). Canadian Journal of Zoology 54(8): 1277-1284. https://doi.org/10.1139/z76-145
https://doi.org/10.1139/z76-145...
, Morris 1989Morris MR (1989) Female choice of large males in the treefrog Hyla chrysoscelis: the importance of identifying the scale of choice. Behavioral Ecology and Sociobiology 25: 275-281. https://doi.org/10.1007/BF00300054
https://doi.org/10.1007/BF00300054...
, Bastos and Haddad 1996Bastos RP, Haddad CFB (1996) Breeding activity of neotropical treefrog Hyla elegans (Anura: Hylidae). Journal of Herpetolology 30(3): 355-360. https://www.jstor.org/stable/1565172?seq=1
https://www.jstor.org/stable/1565172?seq...
, but see Green 2019Green DM (2019) Rarity of size-assortative mating in animals: assessing the evidence with anuran amphibians. The American Naturalist 193: 279-295. https://doi.org/10.1086/701124
https://doi.org/10.1086/701124...
). As most anurans exhibit external fertilization, better cloacae juxtaposition can maximize egg fertilization, potentially increasing the reproductive success of individuals in amplexus (Licht 1976Licht LE (1976) Sexual selection in toads (Bufo americanus). Canadian Journal of Zoology 54(8): 1277-1284. https://doi.org/10.1139/z76-145
https://doi.org/10.1139/z76-145...
, Robertson 1990Robertson JGM (1990) Female choice increases fertilization success in the Australian frog, Uperoleia laevigata. Animal Behaviour 39: 639-645. https://doi.org/10.1016/S0003-3472(05)80374-4
https://doi.org/10.1016/S0003-3472(05)80...
, Bourne 1993Bourne GR (1993) Proximate costs and benefits of mate acquisition at leks of the frog Ololygon rubra. Animal Behaviour 45: 1051-1059. https://doi.org/10.1006/anbe.1993.1131
https://doi.org/10.1006/anbe.1993.1131...
, Bastos and Haddad 1996Bastos RP, Haddad CFB (1996) Breeding activity of neotropical treefrog Hyla elegans (Anura: Hylidae). Journal of Herpetolology 30(3): 355-360. https://www.jstor.org/stable/1565172?seq=1
https://www.jstor.org/stable/1565172?seq...
). In this context, it is likely that B. goiana females are choosing males with similar body sizes, though how females are evaluating the males (e.g. using acoustic signals, visual signals, or both) remains unanswered (see previous discussion regarding the males, and also Starnberger et al. 2014Starnberger I, Preininger D, Hödl W (2014) From uni to multimodality: towards an integrative view on anuran communication. Journal of Comparative Physiology A 200: 777-787. https://doi.org/10.1007/s00359-014-0923-1
https://doi.org/10.1007/s00359-014-0923-...
).

Most studies on anurans report a positive relationship between female size and clutch size/volume (e.g. Wogel et al. 2002Wogel H, Abrunhosa PA, Pombal-Jr JP (2002) Atividade reprodutiva de Physalaemus signifer (Anura, Leptodactylidae) em ambiente temporário. Iheringia , Série Zoologia, 92(2): 57-70. https://doi.org/10.1590/S0073-47212002000200006
https://doi.org/10.1590/S0073-4721200200...
, Dziminski and Alford 2005Dziminski MA, Alford RA (2005) Patterns and fitness consequences of intraclutch variation in egg provisioning in tropical Australian frogs. Oecologia 146: 98-109. https://doi.org/10.1007/s00442-005-0177-2
https://doi.org/10.1007/s00442-005-0177-...
, Pupin et al. 2010Pupin NC, Gasparini JL, Bastos RP, Haddad CFB, Prado CPA (2010) Reproductive biology of an endemic Physalaemus of the Brazilian Atlantic forest, and the trade-off between clutch and egg size in terrestrial breeders of the P. signifer group. Herpetological Journal 20(3): 147-156. https://www.ingentaconnect.com/contentone/bhs/thj/2010/00000020/00000003/art00005
https://www.ingentaconnect.com/contenton...
, Guimarães et al. 2011Guimarães TCS, de Figueiredo GB, Mesquita DO, Vasconcellos MM (2011) Ecology of Hypsiboas albopunctatus (Anura: Hylidae) in a Neotropical Savanna. Journal of Herpetology 45(2): 244-250. https://doi.org/10.1670/09-255.1
https://doi.org/10.1670/09-255.1...
). However, we did not find this relationship for B. goiana, and this same result was already observed for other hylid species (Lips 2001Lips KR (2001) Reproductive trade-offs and bet-hedging in Hyla calypsa, a Neotropical treefrog. Oecologia 128(4): 509-518. https://doi.org/10.1007/s004420100687
https://doi.org/10.1007/s004420100687...
, Hartmann et al. 2004Hartmann MT, Hartmann PA, Haddad CFB (2004) Visual signaling and reproductive biology in a nocturnal treefrog, genus Hyla (Anura: Hylidae). Amphibia-Reptilia 25(4): 395-406. https://doi.org/10.1163/1568538042788933
https://doi.org/10.1163/1568538042788933...
). We found that at least one female mated and spawned two times in the same reproductive season. In another occasion, after a female had spawned, we observed through the transparent skin of its abdomen that the female still carried several oocytes. These are evidences that B. goiana females may spawn more than once during each reproductive season, as observed for other anuran species (Rafínska 1991Rafínska A (1991) Reproductive biology of the fire-bellied toads, Bornbina bornbina and B. variegata (Anura: Discoglossidae): egg size, clutch size and larval period length differences. Biological Journal of Linnean Society 43(3): 197-210. https://doi.org/10.1111/j.1095-8312.1991.tb00593.x
https://doi.org/10.1111/j.1095-8312.1991...
, Bastos and Haddad 1996Bastos RP, Haddad CFB (1996) Breeding activity of neotropical treefrog Hyla elegans (Anura: Hylidae). Journal of Herpetolology 30(3): 355-360. https://www.jstor.org/stable/1565172?seq=1
https://www.jstor.org/stable/1565172?seq...
, Vaira 2001Vaira M (2001) Breeding biology of leaf frog Phyllomedusa boliviana (Anura, Hylidae). Amphibia-Reptilia 22(4): 421-429. https://doi.org/10.1163/15685380152770381
https://doi.org/10.1163/1568538015277038...
). For species with multiple spawns, it has been suggested that the correlation between female size and size of clutches and eggs might be weak because clutches will differ in size between the beginning and the end of the breeding season (Parker and Begon 1986Parker GA, Begon M (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. The American Naturalist 128(4): 573-592. https://www.jstor.org/stable/2461339?seq=1
https://www.jstor.org/stable/2461339?seq...
, Kusano and Hayashi 2002Kusano T, Hayashi T (2002) Female size-specific clutch parameters of two closely related stream-breeding frogs, Rana sakuraii and R. tagoi tagoi: female size-independent and size-dependent egg sizes. Current Herpetology 21(2): 75-86. https://doi.org/10.5358/hsj.21.75
https://doi.org/10.5358/hsj.21.75...
, Prado and Haddad 2005Prado CPA, Haddad CFB (2005) Size-fecundity relationships and reproductive investment in female frogs in the Pantanal, South-Western Brazil. Herpetological Journal 15(3): 181-189. https://www.ingentaconnect.com/contentone/bhs/thj/2005/00000015/00000003/art00007
https://www.ingentaconnect.com/contenton...
). Considering that egg size may represent a similar energetic cost for the female as the number of eggs per clutch, the same explanation could be applied for the absence of relationship between clutch size versus female size and between egg size versus eggs per clutch in this multiple-clutch species (Prado and Haddad 2005Prado CPA, Haddad CFB (2005) Size-fecundity relationships and reproductive investment in female frogs in the Pantanal, South-Western Brazil. Herpetological Journal 15(3): 181-189. https://www.ingentaconnect.com/contentone/bhs/thj/2005/00000015/00000003/art00007
https://www.ingentaconnect.com/contenton...
). Alternatively, the placement of the amplectant pairs in plastic bags to spawn may have affected their behavior. However, we think this is unlikely, because once ovulation begins the female is unable to prevent spawning. Thus, the observation of remaining oocytes in the abdomen of females and the lack of correlation between female size and clutch size/volume indicate that females of B. goiana spawn more than once during the reproductive season.

Our results differ in some aspects from what was previously known for B. goiana. For the population of B. goiana studied in Minas Gerais state, the mean number of eggs per clutch was higher and the mean egg size was smaller compared to our results (Menin et al. 2004Menin M, Silva RA, Giaretta AA (2004) Reproductive biology of Hyla goiana (Anura, Hylidae). Iheringia, Série Zoologia, 94(1): 49-52. https://doi.org/10.1590/S0073-47212004000100008
https://doi.org/10.1590/S0073-4721200400...
). The average female SVL from the Minas Gerais population was larger than what we report here, which could explain the larger clutches found in that population (Menin et al. 2004Menin M, Silva RA, Giaretta AA (2004) Reproductive biology of Hyla goiana (Anura, Hylidae). Iheringia, Série Zoologia, 94(1): 49-52. https://doi.org/10.1590/S0073-47212004000100008
https://doi.org/10.1590/S0073-4721200400...
). Furthermore, our sample size is larger and thus less likely to be affected by extreme values within the population that could affect the average values. Additionally, depending on the environmental conditions of the reproductive areas (e.g. competition, predation, food resources, unpredictability of water bodies), females may differ in the reproductive investment (e,g. fewer and larger eggs, many smaller eggs, eggs variable in size) (Crump 1984Crump ML (1984) Intraclutch egg size variability in Hyla crucifer (Anura: Hylidae). Copeia 1984(2): 302-308. https://www.jstor.org/stable/1445185?seq=1
https://www.jstor.org/stable/1445185?seq...
, Dziminski et al. 2009Dziminski MA, Vercoe PE, Roberts JD (2009) Variable offspring provisioning and fitness: a direct test in the field. Functional Ecology 23(1): 164-171. https://doi.org/10.1111/j.1365-2435.2008.01480.x
https://doi.org/10.1111/j.1365-2435.2008...
, Pupin et al. 2018Pupin NC, Haddad CFB, Prado CPA (2018) Maternal provisioning by foam-nesting frogs of the genus Physalaemus (Anura, Leptodactylidae) in contrasting environments. Amphibia-Reptilia 39(1): 120-125. https://doi.org/10.1163/15685381-00003146
https://doi.org/10.1163/15685381-0000314...
). Considering the evidence for multiple spawning in B. goiana, this plastic response to dynamic environmental conditions seems plausible. Unfortunately, the available information does not allow us to infer the specific reasons for these reported differences.

We found that males were larger at the beginning of the reproductive season at our study site. Differences in the timing of male arrival may affect mating success, especially when the majority of the females arrive at the beginning of the reproductive season (Lodé et al. 2005Lodé T, Holveck M, Lesbarrères D (2005) Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina. Biological Journal of the Linnean Society 86(2): 191-200. https://doi.org/10.1111/j.1095-8312.2005.00521.x
https://doi.org/10.1111/j.1095-8312.2005...
, Wells 2007Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chigago, 1148 pp. https://doi.org/10.7208/chicago/9780226893334.001.0001
https://doi.org/10.7208/chicago/97802268...
). Following this, large males arrive earlier than small males, although the reason for this is unclear (Salvador and Carrascal 1990Salvador A, Carrascal LM (1990) Reproductive phenology and temporal patterns of mate access in Mediterranean anurans. Journal of Herpetology 24(4): 438-441. https://doi.org/10.2307/1565070
https://doi.org/10.2307/1565070...
, Lodé et al. 2005Lodé T, Holveck M, Lesbarrères D (2005) Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina. Biological Journal of the Linnean Society 86(2): 191-200. https://doi.org/10.1111/j.1095-8312.2005.00521.x
https://doi.org/10.1111/j.1095-8312.2005...
). One explanation could be that large males are older and more experienced, and thus know the reproductive area better and are able to arrive first (Reading 2001Reading CJ (2001) Non-random pairing with respect to past breeding experience in the common toad (Bufo bufo). Journal of Zoology 255(4): 511-518. https://doi.org/10.1017/S0952836901001595
https://doi.org/10.1017/S095283690100159...
). However, this may not apply for B. goiana because no individual captured in the first season was recaptured in the second, suggesting that they may not live for more than one year. An alternative explanation could be that large males of B. goiana may simply have better physical conditions, arriving earlier at the area, and establishing territories first, as observed for Rana dalmatina Fitzinger, 1839 (Ranidae) (Lodé et al. 2005Lodé T, Holveck M, Lesbarrères D (2005) Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina. Biological Journal of the Linnean Society 86(2): 191-200. https://doi.org/10.1111/j.1095-8312.2005.00521.x
https://doi.org/10.1111/j.1095-8312.2005...
). A third explanation would be that the smaller size/condition of the males at the end of the reproductive season could reflect recruitment, as observed for Boana albopunctata (Spix, 1824) (de Sá et al. 2014De Sá FP, Zina J, Haddad CFB (2014) Reproductive dynamics of the Neotropical treefrog Hypsiboas albopunctatus (Anura, Hylidae). Journal of Herpetology 48(2): 181-185. https://doi.org/10.1670/12-193
https://doi.org/10.1670/12-193...
). The reproductive season of B. goiana starts in October, and one possibility is that males born at the beginning of the season may already be sexually mature around May. If this is true, the entrance of these young, small males into the breeding active population may lower the average size of the males, thus explaining our results. Lastly, because resident males tend to lose weight throughout the reproductive season due to calling activity and territorial defense (Wells 1978Wells KD (1978) Territoriality in the green frog (Rana clamitans): vocalizations and agonistic interactions. Animal Behaviour 26(4): 1051-1063. https://doi.org/10.1016/0003-3472(78)90094-5
https://doi.org/10.1016/0003-3472(78)900...
, Robertson 1986Robertson JGM (1986) Male territoriality, fighting and assessment of fighting ability in the Australian frog Uperoleia rugosa. Animal Behaviour 34: 763-772. https://doi.org/10.1016/S0003-3472(86)80060-4
https://doi.org/10.1016/S0003-3472(86)80...
), and may be dependent on sperm stored before the reproductive season (Hettyey et al. 2009Hettyey A, Vági B, Hévizi G, Török J (2009) Changes in sperm stores, ejaculate size, fertilization success, and sexual motivation over repeated matings in the common toad, Bufo bufo (Anura: Bufonidae). Biological Journal of the Linnean Society 96(2): 361-371. https://doi.org/10.1111/j.1095-8312.2008.01126.x
https://doi.org/10.1111/j.1095-8312.2008...
), they may leave the chorus before the end of the breeding season. This could allow small males to enter the chorus and obtain a chance of reproducing in the late breeding season. An interesting technique that could help to discern between these explanations is to mark the tadpoles and keep track of them until maturity (e.g. Martin 2011Martin RA (2011) Evaluating a novel technique for individual identification of anuran tadpoles using coded wire tags. Herpetological Conservation and Biology 6(1): 155-160. http://www.herpconbio.org/Volume_6/Issue_1/Martin_2011.pdf
http://www.herpconbio.org/Volume_6/Issue...
, Courtois et al. 2013Courtois EA, Lelong C, Calvez O, Loyau A, Schmeller DS (2013) The use of visible implant Alpha tags for anuran tadpoles. Herpetological Review 44(2): 230-233. https://ssarherps.org/herpetological-review-pdfs
https://ssarherps.org/herpetological-rev...
).

Males and females of B. goiana appear to be capable of adopting different reproductive strategies according to environmental conditions and social contexts. Females of this species much likely spawn multiple clutches, which can vary regarding the number of eggs and egg size. It would be particularly interesting to follow females throughout an entire reproductive season, so that we could investigate trade-offs between egg size, egg number and female investment in different environmental conditions. Females might be obtaining information about calling males, and thus selecting those with similar body sizes, as evidenced by the size-assortative mating, which could increase their fitness via increased fertilization rates. Males of B. goiana seem to avoid fights in which individuals have low probabilities to win, because physical combats were rare. This is corroborated by the distance between calling males, which increased with the number of aggressive calls of the resident male. Alternatively, low aggression levels can be the result of low motivation or even an inherent trait of B. goiana, but these hypotheses require further investigation. The possibility that this species employs multimodal communication could also explain some inconsistencies with published data, although this also requires further evaluation. Acoustic communication seems to be extremely important for B. goiana in many social contexts and future studies should investigate which information, if any, are being assessed by individuals, as well as how this information could be conveyed.

ACKNOWLEDGEMENTS

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Finance Code 001), and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, #476800/2011-0). We are grateful to ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) for providing the collection permits. R.P. Bastos (#304363/2010-3) and C.P.A. Prado are grateful to CNPq (#301125/2013-9), and T.M. Dias to CAPES, for fellowships. C.P.A. Prado acknowledges the Fundação de Amparo à Pesquisa do Estado de São Paulo for financial support (FAPESP #2009/12013-4). We thank P. de Marco Jr and A.V. Palaoro for the help with the statistical analyses. We are also grateful to P. Nobre, A.R. Morais, M.N. Siqueira, I. Carvalho, P.G. Gambale, and J.M. Ribeiro for help in the fieldwork; and to M.M. Dalosto for reading and commenting the manuscript, and for the help in the statistical analyses. We specially thank V.T.T. de Sousa for help in the fieldwork, statistical analyses, and for valuable insights and comments on the manuscript. The authors are also grateful to two anonymous reviewers and the editor for valuable suggestions and criticisms that greatly improved the manuscript. We dedicate this study to Marcelo Menin (in memoriam), who was a great herpetologist and a pioneer in the study of the biology of Boana goiana.

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    » https://doi.org/10.1590/S0073-47212002000200006
  • Zar JH (1999) Biostatistical Analysis. Prentice Hall, New Jersey, 663 pp.

Publication Notes

  • Available online:

    April 16, 2021
  • Zoobank Register:

    http://zoobank.org/14A5783A-AF14-435C-911C-CDB5A4F03122
  • Publisher:

    © 2021 Sociedade Brasileira de Zoologia. Published by Pensoft Publishers at https://zoologia.pensoft.net

Edited by

Editorial responsibility:

Fabricius M.C.B. Domingos

Data availability

Data citations

Frost DR (2020) Amphibian species of the world: an online reference. American Museum of Natural History, version 6.1. http://research.amnh.org/herpetology/amphibia/index.php [Acessed: 27/07/2020]

Publication Dates

  • Publication in this collection
    30 Apr 2021
  • Date of issue
    2021

History

  • Received
    13 Apr 2020
  • Accepted
    16 Mar 2021
  • Published
    16 Apr 2021
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