Skip to main content
SpringerLink
Log in

Parents adjust care in response to weather conditions and egg dehydration in a Neotropical glassfrog

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Parental hydration of terrestrially developing eggs has evolved repeatedly among frogs and is thought to buffer embryos from environmental variation. While many anurans offer relevant opportunities to study parental care, research on how parents respond to environmental variation and offspring conditions are lacking. In this study, we investigated the interrelationships of weather, embryo hydration demands, and parental provisioning in a wild population of the glassfrog Hyalinobatrachium (‘Centrolenella’) fleischmanni in Oaxaca, Mexico. We determined whether males modify parental behavior in response to changes in weather conditions that effect embryo dehydration, how variation in both weather and parental hydration affect egg water balance and embryonic mortality, and whether parental provisioning is related to the hydration levels of egg clutches. We found that male H. fleischmanni compensate for environmental variation in offspring conditions by adjusting the frequency of parental care in response to both weather and egg dehydration. Using a male removal experiment, we examined the function of paternal care and made comparisons with previous research, finding that both the adaptive value of parental care and flexibility in parental behavior are impacted by spatial and temporal conditions. We present observations that indicate a direct conflict between providing parental care and multiple matings. In summary, this research demonstrates that the variable frequency of paternal care in H. fleischmanni is a response to the fluctuating nature of the climate and resulting hydration requirements of embryos in combination with the allocation of effort to parental care versus mating activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alrashidi M, Kosztolányi A, Küpper C, Cuthill IC, Javed S, Székely T (2010) The influence of a hot environment on parental cooperation of a ground-nesting shorebird, the Kentish plover Charadrius alexandrinus. Front Zool 7:1

    Article  PubMed  Google Scholar 

  • Altig R, McDiarmid RW (2007) Morphological diversity and evolution of egg and clutch structure in amphibians. Herpetol Monogr 21:1–32

    Article  Google Scholar 

  • Baeza JA, Fernández M (2002) Active brood care in Cancer setosus (Crustacea: Decapoda): the relationship between female behaviour, embryo oxygen consumption and the cost of brooding. Funct Ecol 16:241–251

    Article  Google Scholar 

  • Bickford DP (2004) Differential parental care behaviors of arboreal and terrestrial microhylid frogs from Papua New Guinea. Behav Ecol Sociobiol 55:402–409

    Article  Google Scholar 

  • Brown JL, Twomey E, Morales V, Summers K (2008) Phytotelm size in relation to parental care and mating strategies in two species of Peruvian poison frogs. Behaviour 145:1139–1165

    Article  Google Scholar 

  • Brown JL, Morales V, Summers K (2010) A key ecological trait drove the evolution of biparental care and monogamy in an amphibian. Am Nat 175:436–446

    Article  PubMed  Google Scholar 

  • Buckley CR, Michael SF, Irschick DJ (2005) Early hatching decreases jumping performance in a direct-developing frog, Eleutherodactylus coqui. Funct Ecol 19:67–72

    Article  Google Scholar 

  • Caldwell JP (1973) Tropical tree frog communities: patterns of reproduction, size, and utilization of structural habitat. PhD dissertation, University of Kansas, Lawrence

  • Carlisle TR (1982) Brood success in variable environments: implications for parental care allocation. Anim Behav 30:824–836

    Article  Google Scholar 

  • Clutton-Brock T (1991) The evolution of parental care. Princeton University Press, Princeton

    Google Scholar 

  • Conway CJ, Martin TE (2000) Effects of ambient temperature on avian incubation behavior. Behav Ecol 11:178–188

    Article  Google Scholar 

  • Crump ML (1996) Parental care among the amphibia. Adv Stud Behav 25:109–144

    Article  Google Scholar 

  • Dautel N, Salgado Maldonado AL, Abuza R, Imba H, Griffin K, Guayasamin JM (2011) Advertisement and combat calls of the glass frog Centrolene lynchi (Anura: Centrolenidae), with notes on combat and reproductive behaviors. Phyllomedusa 10:31–43

    Google Scholar 

  • Delia J, Cisneros-Heredia DF, Whitney J, Murrieta-Galindo R (2010) Observations on the reproductive behavior of a Neotropical glassfrog Hyalinobatrachium fleischmanni (Anura: Centrolenidae). S Am J Herpetol 5:1–12

    Article  Google Scholar 

  • Dick JTA, Faloon SE, Elwood RW (1998) Active brood care in an amphipod: influences of embryonic development, temperature and oxygen. Anim Behav 56:663–672

    Article  PubMed  Google Scholar 

  • Gomez-Mestre I, Pyron RA, Wiens JJ (2012) Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs. Evolution 66:3687–3700

    Article  PubMed  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes indentification. Herpetologica 16:183–190

    Google Scholar 

  • Green BS, McCormick MI (2005) O2 replenishment to fish nests: males adjust brood care to ambient conditions and brood development. Behav Ecol 16:389–397

    Article  Google Scholar 

  • Grimaldi D (1994) Description and immature stages of Hirtodrosophila batrachida sp. n. (Diptera, Drosophilidae), a predator of frog embryos. Entomol Scand 25:129–136

    Article  Google Scholar 

  • Hawley TJ (2006) Embryonic development and mortality in Hyalinobatrachium pulveratum (Anura: Centrolenidae) of south-western Costa Rica. J Trop Ecol 22:731

    Article  Google Scholar 

  • Hayes MP (1983) A technique for partitioning hatching and mortality estimates in leaf-breeding frogs. Herpetol Rev 14:115–116

    Google Scholar 

  • Hayes MP (1991) A study of clutch attendance in the Neotropical frog Centrolenella fleischmanni (Anura: Centrolenidae). PhD dissertation, University of Miami, Coral Gabes, FL

  • Horton NJ, Bebchuk JD, Jones CL, Lipsitz SR, Catalano PJ, Zahner GEP, Fitzmaurice GM (1999) Goodness of fit for GEE: an example with mental health service utilization. Stat Med 18:213–222

    Article  PubMed  CAS  Google Scholar 

  • Ishimatsu A, Yoshida Y, Itoki N, Takeda T, Lee HJ, Graham JB (2007) Mudskippers brood their eggs in air but submerge them for hatching. J Exp Biol 210:3946–3954

    Article  PubMed  Google Scholar 

  • Jacobson SK (1985) Reproductive behavior and male mating success in two species of glass frogs (Centrolenidae). Herpetologica 41:396–404

    Google Scholar 

  • Jones JC, Reynolds JD (1999) Costs of egg ventilation for male common gobies breeding in conditions of low dissolved oxygen. Anim Behav 57:181–188

    Article  PubMed  Google Scholar 

  • Kam YC, Yen CF, Hsu CL (1998) Water balance, growth, development, and survival of arboreal frog eggs (Chirixalus eiffingeri, Rhacophoridae): importance of egg distribution in bamboo stumps. Physiol Zool 71:534–540

    PubMed  CAS  Google Scholar 

  • Kubicki B (2007) Ranas de Vidrio de Costa Rica/Glass frogs of Costa Rica. Instituto Nacional de Biodiversidad (INBio), Heredoa

    Google Scholar 

  • Lips KR, Mendelson JR, Muñoz-Alonso A, Canseco-Márquez L, Mulcahy DG (2004) Amphibian population declines in montane southern Mexico: resurveys of historical localities. Biol Conserv 119:555–564

    Article  Google Scholar 

  • Lynch JD, Ruiz PM, Vincente Rueda J (1983) Notes on the distribution and reproductive biology of Centrolene geckoideum Jimenez de la Espada in Colombia and Ecuador (Amphibia: Centrolenidae). Stud Neotropical Fauna Environ 18:239–243

    Article  Google Scholar 

  • Martin AA, Cooper AK (1972) The ecology of terrestrial anuran eggs, genus Crinia (Leptodactylidae). Copeia 1972:163–168

    Article  Google Scholar 

  • McDiarmid RW (1978) Evolution of parental care in frogs. In: Burghardt GM, Bekoff M (eds) The development of behavior: comparative and evolutionary aspects. Garland, New York, pp 127–147

    Google Scholar 

  • McDiarmid RW, Alder K (1974) Notes on territorial and vocal behavior of Neotropical frogs of the genus Centrolenella. Herpetologica 30:75–78

    Google Scholar 

  • NOAA National Climatic Data Center (2010) State of the climate: global analysis for March 2010. http://www/ncdc.noaa.gov/sotc/global/. Accessed April 20, 2012

  • Roff DA (1992) The evolution of life histories. Chapman & Hall, New York

    Google Scholar 

  • Salthe SN, Mecham JS (1974) Reproductive and courtship patterns. In: Lofts B (ed) Physiology of the amphibia 2. Academic, New York, pp 309–521

    Chapter  Google Scholar 

  • Savage JM (2002) The amphibians and reptiles of Costa Rica: a herpetofuana between two continents, between two seas. University of Chicago Press, Chicago

    Google Scholar 

  • Shine R, Madsen TRL, Elphick MJ, Harlow PS (1997) The influence of nest temperatures and maternal brooding on hatchling phenotypes in water phythons. Ecology 78:1713–1721

    Article  Google Scholar 

  • Somma LA, Fawcett JD (1989) Brooding behavior of the prairie skink, Eumeces septentrionalis, and its relationship to the hydric environment of the nest. Zool J Linn Soc 95:245–256

    Article  Google Scholar 

  • Stahlschmidt Z, DeNardo DF (2010) Parental behavior in pythons is responsive to both the hydric and thermal dynamics of the nest. J Exp Biol 213:1691–1696

    Article  PubMed  Google Scholar 

  • Taigen TL, Pough FH, Stewart MM (1984) Water balance of terrestrial Anuran (Eleutherodactylus coqui) eggs: importance of parental care. Ecology 65:248–255

    Article  Google Scholar 

  • Touchon JC, Warkentin KM (2009) Negative synergism of rainfall patterns and predators affects frog egg survival. J Anim Ecol 78:715–723

    Article  PubMed  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179

    Google Scholar 

  • Tulp I, Schekkerman H, Bruinzeel LW, Jukema J, Visser GH, Piersma T (2009) Energetic demands during incubation and chick rearing in a uniparental and a biparental shorebird breeding in the high Arctic. Auk 126:155–164

    Article  Google Scholar 

  • Valencia-Aguliar A, Castro-Herrera F, Ramírez-Pinilla MP (2012) Microhabitats for oviposition and male clutch attendance in Hyalinobatrachium aureoguttatum (Anura: Centrolendiae). Copiea 2012:722–731

    Article  Google Scholar 

  • Vargas-Salinas F, Lopez-A FB, Muñoz-G NJ (2007) Cochranella savagei (Savage’s glass frog). Reproduction. Herpetol Rev 38:436–437

    Google Scholar 

  • Villa J (1984) Biology of a Neotropical glass frog, Centrolenella fleischmanni (Boettger), with special reference to its frogfly associates. Milwaukee Pub Mus Contrib Biol Geol 55:1–60

    Google Scholar 

  • Vockenhuber EA, Hödl W, Karpfen U (2008) Reproductive behavior of the glass frog Hyalinobatrachium valerioi (Anura: Centrolenidae) at the tropical stream Quebrada Negra (La Gamba, Costa Rica). Stapfia 88:335–348

    Google Scholar 

  • Vockenhuber EA, Hödl W, Amézquita A (2009) Glassy fathers do matter: egg attendance enhances embryonic survivorship in the glass frog Hyalinobatrachium valerioi. J Herpetol 43:340–344

    Article  Google Scholar 

  • Warkentin KM (2000) Wasp predation and wasp-induced hatching of red-eyed treefrog eggs. Anim Behav 60:503–510

    Article  PubMed  Google Scholar 

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

    Book  Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York

    Google Scholar 

Download references

Acknowledgments

We are forever indebted to the family of Rogelio Cortéz-Rojas and Eloisa Escobar-Cortéz, and the people of San Gabriel Mixtepec for opening up their community, providing access to field sites, friendship, and chelas while working in the Mexican Sierra. We sincerely acknowledge all the thoughtful comments, suggestions, and critical review of methods, analyses, and/ or versions of this manuscript by R.W. McDiarmid, D.R. Chalcraft, T. Lamb, K.M. Warkentin, E. Twomey, M.P. Hayes, J.C. Touchon, P. Buston, K.L. Cohen, J. Majoris, and two anonymous reviewers. Funding was provided by Grant-In-Aid of Research from the National Academy of Science administered by Sigma Xi (The Scientific Research Society), the American Society of Ichthyologists and Herpetologists Gaige Fund Award, and the Next-Step Scholarship (East Carolina University). Permits were provided by the Secretaria de Medio Ambiente y Recursos Naturals (SEMERNAT).

Ethical standards

This research was conducted in compliance with current laws and protocols of the United Mexican States. Research was approved and permits were provided by the Secretaria de Medio Ambiente y Recursos Naturals (SEMERNAT permit numbers: 01903, 01902, 09280).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Author notes

  1. Jesse R. J. Delia

    Present address: Department of Biology, Boston University, Boston, MA, 02215, USA

Authors and Affiliations

  1. Biology Department, East Carolina University, Greenville, NC, 27858, USA

    Jesse R. J. Delia & Kyle Summers

  2. Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, A. P. 1-69 Plaza Juárez, C.P. 42001, Pachuca, Hidalgo, Mexico

    Aurelio Ramírez-Bautista

Authors
  1. Jesse R. J. Delia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aurelio Ramírez-Bautista
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kyle Summers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jesse R. J. Delia.

Additional information

Communicated by J. Christensen-Dalsgaard

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(XLSX 12.0 kb)

ESM 2

(XLSX 9.96 kb)

ESM 3

(DOCX 16.6 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Delia, J.R.J., Ramírez-Bautista, A. & Summers, K. Parents adjust care in response to weather conditions and egg dehydration in a Neotropical glassfrog. Behav Ecol Sociobiol 67, 557–569 (2013). https://doi.org/10.1007/s00265-013-1475-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-013-1475-z

Keywords

Search

Navigation