Abstract
Parental care has evolved many times in multiple taxa and, by definition, enhances offspring survivorship. Anurans exhibit a diverse array of parental care behaviors, but studies examining their adaptive significance in an evolutionary context are limited. The critically endangered bush frog, Raorchestes chalazodes (Rhacophoridae), only breeds inside hollow internodes of the endemic bamboo (Ochlandra travancorica) in the southern Western Ghats of India from June through October. From systematic surveys, we established that adult males are sole caregivers exhibiting egg attendance and egg guarding behavior. Predation was the main cause of egg mortality in the absence of an attending male; the majority of predation events were caused by conspecific males. The results highlight the role of regional and microhabitat-specific selection pressures such as strong seasonality, limited resources, and competition for oviposition sites. Oviposition sites are in high demand, but in short supply and by consuming unattended eggs, the conspecific male may benefit from nutritional gains as well as mating opportunities at the oviposition site. Our work lays foundations for further examination of social and reproductive behaviors of anurans not only in the Western Ghats but also in South and Southeast Asia.
Significance statement
The bamboo-breeding frog R. chalazodes is one among 62 arboreal frogs of the genus Raorchestes found in the Western Ghats of India. It was presumed extinct until its rediscovery in 2011 from within bamboo internodes endemic to the region. Adult males of this species care for direct developing eggs, laid exclusively inside of hollow bamboo internodes. Conspecific males cannibalized unattended egg clutches when the caregiving adult male was experimentally removed from the oviposition site. Eggs were also eaten by ants, parasitized by flies, and died from fungal infections or drowned. Male parental care in the form of egg attendance and egg guarding prevents predation of eggs and increases offspring survivorship. Parental care behavior is common among several taxa with external fertilization. Integrating natural history with in situ experiments may reveal novel insights into the adaptive nature of parental care behavior.
This is a preview of subscription content, access via your institution.
References
Alonso-Alvarez C, Velando A (2012) Benefits and costs of parental care. In: Smiseth PT, Kölliker M (eds) Royle NJ. Oxford University Press, Oxford, pp 40–61
Alonzo SH (2012) Sexual selection favours male parental care, when females can choose. Proc R Soc Lond B 279(1734):1784–1790. https://doi.org/10.1098/rspb.2011.2237
Anderson DB (1936) Relative humidity or vapor pressure deficit. Ecology 17(2):277–282. https://doi.org/10.2307/1931468
Balshine S (2012) Patterns of parental care in vertebrates. In: Royle NJ, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 62–80. https://doi.org/10.1093/acprof:oso/9780199692576.003.0004
Bee MA, Schwartz JJ, Summers K (2013) All’s well that begins wells: celebrating 60 years of animal behaviour and 36 years of research on anuran social behaviour. Anim Behav 85(1):5–18. https://doi.org/10.1016/j.anbehav.2012.10.031
Bickford D (2004) Differential parental care behaviors of arboreal and terrestrial microhylid frogs from Papua New Guinea. Behav Ecol Sociobiol 55(4):402–409. https://doi.org/10.1007/s00265-003-0717-x
Biju SD, Dutta SK, Vasudevan K, Vijayakumar SP, Srinivasulu C (2004) Raorchestes chalazodes. The IUCN Red List of Threatened Species 2004: e.T58829A11847257.http://dx.doi.org/10.2305/IUCN.UK.2004.RLTS.T58829A11847257.en.
Boos S, Meunier J, Pichon S, Kölliker M (2014) Maternal care provides antifungal protection to eggs in the European earwig. Behav Ecol 25(4):754–761. https://doi.org/10.1093/beheco/aru046
Brown JL, Morales V, Summers K (2010) A key ecological trait drove the evolution of biparental care and monogamy in an amphibian. Am Nat 175(4):436–446. https://doi.org/10.1086/650727
Brown JL, Twomey E, Summers K, Morales V (2008) Phytotelm size in relation to parental care and mating strategies in two species of Peruvian poison frogs. Behaviour 145(9):1139–1165. https://doi.org/10.1163/156853908785387647
Claessen D, de Roos AM, Persson L (2000) Dwarfs and giants: cannibalism and competition in size-structured populations. Am Nat 155(2):219–237. https://doi.org/10.1086/303315
Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton
Consolmagno RC, Requena GS, Machado G, Brasileiro CA (2016) Costs and benefits of temporary egg desertion in a rocky shore frog with male-only care. Behav Ecol Sociobiol 70(5):785–795. https://doi.org/10.1007/s00265-016-2102-6
Crump ML (1995) Parental care. In: Heatwole H, Sullivan BK (eds) Amphibian Biology, Vol. 2. Surrey Beatty & Sons, Chipping Norton, NSW, pp 518–567
Crump ML (1996) Parental care among the amphibia. Adv Stud Behav 25:109–144. https://doi.org/10.1016/S0065-3454(08)60331-9
Crump ML (2015) Anuran reproductive modes: evolving perspectives. J Herpetol 49(1):1–16. https://doi.org/10.1670/14-097
Delia JRJ, Bravo-Valencia L, Warkentin KM (2017) Patterns of parental care in Neotropical glassfrogs: fieldwork alters hypotheses of sex-role evolution. J Evol Biol 30(5):898–914. https://doi.org/10.1111/jeb.13059
Delia JRJ, Ramírez-Bautista A, Summers K (2013) Parents adjust care in response to weather conditions and egg dehydration in a Neotropical glassfrog. Behav Ecol Sociobiol 67(4):557–569. https://doi.org/10.1007/s00265-013-1475-z
Denoël M, Demars B (2008) The benefits of heterospecific oophagy in a top predator. Acta Oecol 34(1):74–79. https://doi.org/10.1016/j.actao.2008.03.004
Devy MS, Davidar P (2003) Pollination systems of trees in Kakachi, a mid-elevation wet evergreen forest in Western Ghats, India. Am J Bot 90(4):650–657. https://doi.org/10.3732/ajb.90.4.650
Duellman WE, Trueb L (1994) Biology of amphibians. Johns Hopkins University Press, Baltimore
Dugas MB, Wamelink CN, Killius AM, Richards-Zawacki CL (2016) Parental care is beneficial for offspring, costly for mothers, and limited by family size in an egg-feeding frog. Behav Ecol 27(2):476–483. https://doi.org/10.1093/beheco/arv173
Fox LR (1975) Cannibalism in natural populations. Annu Rev Ecol Syst 6(1):87–106. https://doi.org/10.1146/annurev.es.06.110175.000511
Ganesh T, Ganesan R, Devy MS, Davidar P, Bawa KS (1996) Assessment of plant biodiversity at a mid-elevation evergreen forest of Kalakad-Mundanthurai Tiger Reserve, Western Ghats, India. Curr Sci 71:379–391
Gravel M-A, Cooke SJ (2009) Influence of inter-lake variation in natural nest predation pressure on the parental care behaviour of smallmouth bass (Micropterus dolomieu). Ethology 115(6):608–616. https://doi.org/10.1111/j.1439-0310.2009.01641.x
Gururaja KV (2012) Pictorial guide to frogs and toads of the Western Ghats. Gubbi Labs LLP, Gubbi
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:4
Heyer R, Donnelly MA, Foster M, Mcdiarmid R (1994) Measuring and monitoring biological diversity: standard methods for amphibians. Smithsonian Institution Press, Washington
Johnsingh AJT (2001) The Kalakad–Mundanthurai tiger reserve: a global heritage of biological diversity. Curr Sci 80:378–388
Juncá FA (1996) Parental care and egg mortality in Colostethus stepheni. J Herpetol 30(2):292–294. https://doi.org/10.2307/1565530
Kam Y-C, Chuang Z-S, Yen C-F (1996) Reproduction, oviposition-site selection, and tadpole oophagy of an arboreal nester, Chirixalus eiffingeri (Rhacophoridae), from Taiwan. J Herpetol 30(1):52–59. https://doi.org/10.2307/1564706
Kluge AG (1981) The life history, social organization, and parental behavior of Hyla rosenbergi Boulenger, a nest-building gladiator frog. Misc Publ Mus Zool Univ Michigan 160:1–170
Kokko H, Jennions MD (2012) Sex differences in parental care. In: Royle NJ, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 101–116. https://doi.org/10.1093/acprof:oso/9780199692576.003.0006
Lehtinen RM, Nussbaum RA (2003) Parental care: a phylogenetic perspective. In: Jamieson BGM (ed) Reproductive biology and phylogeny of Anura. Science Publishers Inc, Enfield, NH, pp 343–386
Marconato A, Bisazza A (1988) Mate choice, egg cannibalism and reproductive success in the river bullhead, Cottus gobio L. J Fish Biol 33(6):905–916. https://doi.org/10.1111/j.1095-8649.1988.tb05539.x
McDiarmid R (1978) Evolution of parental care in frogs. In: Burghardt GM, Bekoff M (eds) The development of behavior: comparative and evolutionary aspects. Garland STPM Press, New York, pp 127–147
Michaud J, Grant A (2004) Adaptive significance of sibling egg cannibalism in Coccinellidae: comparative evidence from three species. Ann Entomol Soc Am 97(4):710–719. https://doi.org/10.1603/0013-8746(2004)097[0710:ASOSEC]2.0.CO;2
Owens IPF, Bennett PM (1994) Mortality costs of parental care and sexual dimorphism in birds. Proc R Soc Lond B 257(1348):1–8. https://doi.org/10.1098/rspb.1994.0086
Parsons W, Zhong W, Rudolf VHW (2013) Mating status and kin recognition influence the strength of cannibalism. Anim Behav 85(2):365–369. https://doi.org/10.1016/j.anbehav.2012.11.006
Pizzari T, Bonduriansky R (2010) Sexual behaviour: conflict, cooperation and co-evolution. In: Székely T, Moore AJ, Komdeur J (eds) Social behaviour: genes, ecology and evolution. Cambridge University Press, Cambridge, pp 230–266. https://doi.org/10.1017/CBO9780511781360.021
Poo S, Bickford DP (2013) The adaptive significance of egg attendance in a south-east asian tree frog. Ethology 119(8):671–679. https://doi.org/10.1111/eth.12108
Poo S, Evans TA, Tan MK, Bickford DP (2016) Dynamic switching in predator attack and maternal defence of prey. Biol J Linn Soc 118(4):901–910. https://doi.org/10.1111/bij.12786
Porter B, Fiumera A, Avise J (2002) Egg mimicry and allopaternal care: two mate-attracting tactics by which nesting striped darter (Etheostoma virgatum) males enhance reproductive success. Behav Ecol Sociobiol 51(4):350–359. https://doi.org/10.1007/s00265-002-0456-4
Reguera P, Gomendio M (1999) Predation costs associated with parental care in the golden egg bug Phyllomorpha laciniata (Heteroptera: Coreidae). Behav Ecol 10(5):541–544. https://doi.org/10.1093/beheco/10.5.541
Ridley M (1978) Paternal care. Anim Behav 26:904–932. https://doi.org/10.1016/0003-3472(78)90156-2
Ringler E, Barbara Beck K, Weinlein S, Huber L, Ringler M (2017) Adopt, ignore, or kill? Male poison frogs adjust parental decisions according to their territorial status. Sci Rep 7:43544. https://doi.org/10.1038/srep43544
Royle NJ, Russell AF, Wilson AJ (2014) The evolution of flexible parenting. Science 345(6198):776–781. https://doi.org/10.1126/science.1253294
RStudio Team (2015) RStudio: integrated development for R. RStudio Inc., Boston, MA
Schradin C, Anzenberger G (2001) Costs of infant carrying in common marmosets, Callithrix jacchus: an experimental analysis. Anim Behav 62(2):289–295. https://doi.org/10.1006/anbe.2001.1767
Seshadri KS (2014) Effects of historical selective logging on anuran communities in a wet evergreen forest, South India. Biotropica 46(5):615–623. https://doi.org/10.1111/btp.12141
Seshadri KS, Gururaja KV, Bickford DP (2015) Breeding in bamboo: a novel anuran reproductive strategy discovered in Rhacophorid frogs of the Western Ghats, India. Biol J Linn Soc 114(1):1–11. https://doi.org/10.1111/bij.12388
SijiMol K, Dev SA, Sreekumar VB (2016) A review of the ecological functions of reed bamboo, genus Ochlandra in the Western Ghats of India: implications for sustainable conservation. Trop Conserv Sci 9(1):389–407. https://doi.org/10.1177/194008291600900121
Simon MP (1983) The ecology of parental care in a terrestrial breeding frog from New Guinea. Behav Ecol Sociobiol 14(1):61–67. https://doi.org/10.1007/BF00366657
Smiseth PT, Kölliker M, Royle NJ (2012) What is parental care? In: Royle NJ, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 1–17. https://doi.org/10.1093/acprof:oso/9780199692576.003.0001
Smith C, Wootton RJ (1995) The costs of parental care in teleost fishes. Rev Fish Biol Fisher 5(1):7–22. https://doi.org/10.1007/BF01103363
Summers K, McKeon CS, Heying H (2006) The evolution of parental care and egg size: a comparative analysis in frogs. Proc R Soc Lond B 273(1587):687–692. https://doi.org/10.1098/rspb.2005.3368
Summers K, McKeon CS, Heying H, Hall J, Patrick W (2007) Social and environmental influences on egg size evolution in frogs. J Zool 271(2):225–232. https://doi.org/10.1111/j.1469-7998.2006.00213.x
Taigen TL, Pough FH, Stewart MM (1984) Water balance of terrestrial anuran (Eleutherodactylus coqui) eggs: importance of parental care. Ecology 65(1):248–255. https://doi.org/10.2307/1939477
Therneau T (2009) Package ‘coxme’. Mixed Effects Cox Models. Available: http://r-forge.r-project.org
Tilley SG (1972) Aspects of parental care and embryonic development in Desmognathus ochrophaeus. Copeia 1972:32–40
Toledo LF, Sazima I, Haddad CFB (2011) Behavioural defences of anurans: an overview. Ethol Ecol Evol 23(1):1–25. https://doi.org/10.1080/03949370.2010.534321
Townsend DS (1989) The consequences of microhabitat choice for male reproductive success in a tropical frog (Eleutherodactylus coqui). Herpetologica 45:451–458
Townsend DS, Stewart MM, Pough FH (1984) Male parental care and its adaptive significance in a neotropical frog. Anim Behav 32(2):421–431. https://doi.org/10.1016/S0003-3472(84)80278-X
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179
Vijayakumar SP, Dinesh KP, Prabhu MV, Shanker K (2014) Lineage delimitation and description of nine new species of bush frogs (Anura: Raorchestes, Rhacophoridae) from the Western Ghats Escarpment. Zootaxa 3893(4):451–488. https://doi.org/10.11646/zootaxa.3893.4.1
Villa J (1979) Two fungi lethal to frog eggs in Central America. Copeia 1979(4):650–655. https://doi.org/10.2307/1443873
Villa J, Townsend DS (1983) Viable frog eggs eaten by phorid fly larvae. J Herpetol 17(3):278–281. https://doi.org/10.2307/1563832
Vockenhuber EA, Hödl W, Amézquita A (2009) Glassy fathers do matter: egg attendance enhances embryonic survivorship in the glass frog Hyalinobatrachium valerioi. J Herpetol 43(2):340–344. https://doi.org/10.1670/08-092R1.1
von May R, Medina-Müller M, Donnelly MA, Summers K (2009) Breeding-site selection by the poison frog Ranitomeya biolat in Amazonian bamboo forests: an experimental approach. Can J Zool 87:453–464
Wells KD (1977) Territoriality and male mating success in the green frog (Rana clamitans). Ecology 58(4):750–762. https://doi.org/10.2307/1936211
Wells KD (1978) Territoriality in the green frog (Rana clamitans): vocalizations and agonistic behaviour. Anim Behav 26:1051–1063. https://doi.org/10.1016/0003-3472(78)90094-5
Wells KD (1981) Parental behavior of male and female frogs. In: Alexander RD, Tinkle D (eds) Natural selection and social behavior. Chiron Press, New York, pp 184–197
Wells KD (2007) The ecology and behavior of amphibians. Univ Chicago Press, Chicago, IL. https://doi.org/10.7208/chicago/9780226893334.001.0001
Weygoldt P (1980) Complex brood care and reproductive behavior in captive poison-arrow frogs, Dendrobates pumilio O. Schmidt. Behav Ecol Sociobiol 74:329–332
Whittingham LA, Robertson RJ (1994) Food availability, parental care and male mating success in red-winged blackbirds (Agelaius phoeniceus). J Anim Ecol 63(1):139–150. https://doi.org/10.2307/5590
Wilson EO (1975) Sociobiology: the new synthesis. Cambridge University Press, Cambridge, MA
Windsor DM, Choe JC (1994) Origins of parental care in chrysomelid beetles. In: Jolivet PH, Cox ML, Petitpierre E (eds) Novel aspects of the biology of Chrysomelidae. Series Entomologica. Kluwer Academic Publishers, Dordrecht, pp 111–117. https://doi.org/10.1007/978-94-011-1781-4_4
Wynne-Edwards KE (1998) Evolution of parental care in Phodopus: conflict between adaptations for survival and adaptations for rapid reproduction. Am Zool 38(1):238–250. https://doi.org/10.1093/icb/38.1.238
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed EffectsModels and extensions in ecology with R. Springer, New York. https://doi.org/10.1007/978-0-387-87458-6
Acknowledgments
The Tamil Nadu Forest Department provided permits, and their staff provided logistical support. Drs M. D. Soubadra, T. Ganesh, and R. Ganesan permitted the use of facilities of the Agastyamalai Community-based Conservation Centre, and M. Mathivanan, A. Saravanan, and the staff provided logistics. Dr. T. Ganesh, Dr. K.V. Gururaja, S. Johnson, A. Sachin, A. Saravanan, S. Tamizalagan, Vidisha Kulkarni, and Vignesh Kamath assisted KSS in data collection. KSS was supported the Navjot Sodhi Conservation Biology scholarship from the National University of Singapore. Field research was supported by The Mohamed bin Zayed Species Conservation Fund and Chicago Zoological Society-Endangered Species Fund. Dr. K.V. Gururaja provided critical inputs to KSS during fieldwork and when writing the manuscript. K. Vidisha prepared the illustration. This manuscript is also an outcome of the Science Writing workshop conducted by the Conservation Leadership Program in 2017, Bengaluru, India, and benefitted immensely from the inputs of Dr. Martin Fisher and Ms. Laura Owens. Dr. Frank Rheindt commented on the manuscript. Comments from Catharina Karlsson, Dr. Eva Ringler, and another anonymous reviewer improved the quality of this paper. We thank them all.
Funding
This research was supported by grants from the Mohamed bin Zayed Species Conservation Fund (14258557), Chicago Zoological Trust, and a travel award by the Conservation Leadership Program.
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 applicable international, national (WL5(a) 19456), and/or institutional guidelines (B136072 and M140424) for the care and use of animals were followed.
Additional information
Communicated by K. Summers
Rights and permissions
About this article
Cite this article
Seshadri, K.S., Bickford, D.P. Faithful fathers and crooked cannibals: the adaptive significance of parental care in the bush frog Raorchestes chalazodes, Western Ghats, India. Behav Ecol Sociobiol 72, 4 (2018). https://doi.org/10.1007/s00265-017-2420-3
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-017-2420-3
Keywords
- Reproductive ecology
- Parental care
- Predation
- Cannibalism
- Evolution
- The Western Ghats