Faithful fathers and crooked cannibals: the adaptive significance of parental care in the bush frog Raorchestes chalazodes, Western Ghats, India
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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.
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.
KeywordsReproductive ecology Parental care Predation Cannibalism Evolution The Western Ghats
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.
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.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national (WL5(a) 19456), and/or institutional guidelines (B136072 and M140424) for the care and use of animals were followed.
- 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 40–61Google Scholar
- 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 CrossRefGoogle Scholar
- 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.
- Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, PrincetonGoogle Scholar
- Crump ML (1995) Parental care. In: Heatwole H, Sullivan BK (eds) Amphibian Biology, Vol. 2. Surrey Beatty & Sons, Chipping Norton, NSW, pp 518–567Google Scholar
- Duellman WE, Trueb L (1994) Biology of amphibians. Johns Hopkins University Press, BaltimoreGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 71:379–391Google Scholar
- Gururaja KV (2012) Pictorial guide to frogs and toads of the Western Ghats. Gubbi Labs LLP, GubbiGoogle Scholar
- Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:4Google Scholar
- Heyer R, Donnelly MA, Foster M, Mcdiarmid R (1994) Measuring and monitoring biological diversity: standard methods for amphibians. Smithsonian Institution Press, WashingtonGoogle Scholar
- Johnsingh AJT (2001) The Kalakad–Mundanthurai tiger reserve: a global heritage of biological diversity. Curr Sci 80:378–388Google Scholar
- 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 160:1–170Google Scholar
- 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 CrossRefGoogle Scholar
- 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 343–386Google Scholar
- 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 CrossRefGoogle Scholar
- 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 127–147Google Scholar
- 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 CrossRefGoogle Scholar
- RStudio Team (2015) RStudio: integrated development for R. RStudio Inc., Boston, MAGoogle Scholar
- 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 CrossRefGoogle Scholar
- Therneau T (2009) Package ‘coxme’. Mixed Effects Cox Models. Available: http://r-forge.r-project.org
- Townsend DS (1989) The consequences of microhabitat choice for male reproductive success in a tropical frog (Eleutherodactylus coqui). Herpetologica 45:451–458Google Scholar
- Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179Google Scholar
- 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 184–197Google Scholar
- Wells KD (2007) The ecology and behavior of amphibians. Univ Chicago Press, Chicago, IL. https://doi.org/10.7208/chicago/9780226893334.001.0001 CrossRefGoogle Scholar
- Wilson EO (1975) Sociobiology: the new synthesis. Cambridge University Press, Cambridge, MAGoogle Scholar
- 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 CrossRefGoogle Scholar