Build me up to break me down: frothed spawn in the sandpaper frog, Lechriodus fletcheri, is formed by female parents and later broken down by their offspring
John Gould
+ Author Affiliations
- Author Affiliations
School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW 2308, Australia. Email: john.gould@uon.edu.au
Australian Journal of Zoology 67(3) 153-161 https://doi.org/10.1071/ZO20038
Submitted: 31 May 2020 Accepted: 7 July 2020 Published: 14 July 2020
Abstract
Several genera of anuran amphibians deposit their eggs within mucous secretions that have been aerated by the parents to produce a foam or bubble spawn body. This is a dynamic medium for embryo development given that it gradually breaks down over time, and one that has been hypothesised to serve a variety of purposes including protecting embryos from external stresses, such as suboptimal temperatures, desiccation and predation. In this study, I provide additional details of bubble spawn production in the sandpaper frog, Lechriodus fletcheri. Field and laboratory observations showed that females aerate spawn while in inguinal amplexus, using flanged fingers to transport air bubbles into the mucous. While the frothed spawn is initially resistant to breakdown, it gradually loses bubbles and flattens out into a film. This temporal shift in structure is likely to be adaptive, as the resultant increase in surface area allows embryos to come in direct contact with the open water, which may accommodate their increased oxygen demands or ease extrication from the mass. I provide evidence that this process is controlled by the residing embryos, given that spawn in the absence of embryos does not break down, highlighting the ability of offspring to modify their immediate environment even before hatching occurs to ensure conditions remain suitable for their changing needs.
References
Altig, R., and McDiarmid, R. W. (2007). Morphological diversity and evolution of egg and clutch structure in amphibians. Herpetological Monograph 21, 1–32.| Morphological diversity and evolution of egg and clutch structure in amphibians.Crossref | GoogleScholarGoogle Scholar |
Anstis, M. (2017). ‘Tadpoles and Frogs of Australia.’ (New Holland Publishers Pty Limited: Sydney.)
Bastos, R. P., Haddad, C. F., and Pombal, J. P. (2010). Foam nest in Scinax rizibilis (Amphibia: Anura: Hylidae). Zoologia (Curitiba) 27, 881–886.
| Foam nest in Scinax rizibilis (Amphibia: Anura: Hylidae).Crossref | GoogleScholarGoogle Scholar |
Bokermann, W. (1962). Observações biológicas sobre Physalaemus cuvieri Fitz, 1826 (Amphibia, Salientia). Revista Brasileira de Biologia 22, 391–399.
Brizzi, R., Delfino, G., and Jantra, S. (2003). An overview of breeding glands. In ‘Reproductive Biology and Phylogeny of Anura’. (Ed. B. Jamieson.) pp. 253–317. (Science Publishers Inc.: Sydney.)
Buzatto, B. A., Thyer, E. M., Roberts, J. D., and Simmons, L. W. (2017). Sperm competition and the evolution of precopulatory weapons: testis size and amplexus position, but not arm strength, affect fertilization success in a chorusing frog. Evolution 71, 329–341.
| Sperm competition and the evolution of precopulatory weapons: testis size and amplexus position, but not arm strength, affect fertilization success in a chorusing frog.Crossref | GoogleScholarGoogle Scholar | 27911018PubMed |
Cockran, C., and Thoms, C. (1996). ‘Amphibians of Oregon, Washington, and British Columbia: A Field Identification Guide.’ (Lone Pine Publishing: Vancouver.)
Coe, M. (1974). Observations on the ecology and breeding biology of the genus Chiromantis (Amphibia: Rhacophoridae). Journal of Zoology 172, 13–34.
| Observations on the ecology and breeding biology of the genus Chiromantis (Amphibia: Rhacophoridae).Crossref | GoogleScholarGoogle Scholar |
Cooper, A., Kennedy, M. W., Fleming, R. I., Wilson, E. H., Videler, H., Wokosin, D. L., Su, T. J., Green, R. J., and Lu, J. R. (2005). Adsorption of frog foam nest proteins at the air–water interface. Biophysical Journal 88, 2114–2125.
| Adsorption of frog foam nest proteins at the air–water interface.Crossref | GoogleScholarGoogle Scholar | 15626715PubMed |
Dobkin, D. S., and Gettinger, R. D. (1985). Thermal aspects of anuran foam nests. Journal of Herpetology 19, 271–275.
| Thermal aspects of anuran foam nests.Crossref | GoogleScholarGoogle Scholar |
Downie, J., and Nokhbatolfoghahai, M. (2006). Presence and absence of the cement gland in foamnesting leptodactylids (Anura: Leptodactylidae): implications for the transition to terrestrial development. The Herpetological Journal 16, 77–81.
Duellman, W., and Trueb, L. (1986). ‘Biology of Amphibians.’ (McGraw-Hill: New York.)
Fleming, R. I., Mackenzie, C. D., Cooper, A., and Kennedy, M. W. (2009). Foam nest components of the tungara frog: a cocktail of proteins conferring physical and biological resilience. Proceedings. Biological Sciences 276, 1787–1795.
| Foam nest components of the tungara frog: a cocktail of proteins conferring physical and biological resilience.Crossref | GoogleScholarGoogle Scholar | 19324764PubMed |
Frost, D. R. (1985). ‘Amphibian Species of the World. A Taxonomic and Geographical Reference.’ (Association of Systematics Collections and Allen Press: Kansas.)
Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190.
Gould, J., Clulow, J., and Clulow, S. (2019). Food, not friend: tadpoles of the sandpaper frog (Lechriodus fletcheri) cannibalise conspecific eggs as a food resource in ephemeral pools. Ethology 126, 486–491.
Haddad, C. F., and Hödl, W. (1997). New reproductive mode in anurans: bubble nest in Chiasmocleis leucosticta (Microhylidae). Copeia 1997, 585–588.
| New reproductive mode in anurans: bubble nest in Chiasmocleis leucosticta (Microhylidae).Crossref | GoogleScholarGoogle Scholar |
Haddad, C. F., and Pombal, J. P. (1998). Redescription of Physalaemus spiniger (Anura: Leptodactylidae) and description of two new reproductive modes. Journal of Herpetology 32, 557–565.
| Redescription of Physalaemus spiniger (Anura: Leptodactylidae) and description of two new reproductive modes.Crossref | GoogleScholarGoogle Scholar |
Heyer, W. R. (1969). The adaptive ecology of the species groups of the genus Leptodactylus (Amphibia, Leptodactylidae). Evolution 23, 421–428.
| The adaptive ecology of the species groups of the genus Leptodactylus (Amphibia, Leptodactylidae).Crossref | GoogleScholarGoogle Scholar | 28562917PubMed |
Heyer, W. R., and Rand, A. S. (1977). Foam nest construction in the leptodactylid frogs Leptodactylus pentadactylus and Physalaemus pustulosus (Amphibia, Anura, Leptodactylidae). Journal of Herpetology 11, 225–228.
| Foam nest construction in the leptodactylid frogs Leptodactylus pentadactylus and Physalaemus pustulosus (Amphibia, Anura, Leptodactylidae).Crossref | GoogleScholarGoogle Scholar |
Hödl, W. (1986). Foam nest construction in South American leptodactylid frogs. In ‘Studies in Herpetology’. (Ed Z. Rocek.) pp. 565–570. (Charles University: Prague.)
Hödl, W. (1990). An analysis of foam nest construction in the Neotropical frog Physalaemus ephippifer (Leptodactylidae). Copeia 1990, 547–554.
| An analysis of foam nest construction in the Neotropical frog Physalaemus ephippifer (Leptodactylidae).Crossref | GoogleScholarGoogle Scholar |
Hödl, W. (1992). Reproductive behaviour in the neotropical foam-nesting frog Pleurodema diplolistris (Leptodactylidae). Amphibia-Reptilia 13, 263–274.
| Reproductive behaviour in the neotropical foam-nesting frog Pleurodema diplolistris (Leptodactylidae).Crossref | GoogleScholarGoogle Scholar |
Kabisch, K., Herrmann, H. J., Klossek, P., Luppa, H., and Brauer, K. (1998). Foam gland and chemical analysis of the foam of Polypedates leucomystax (Gravenhorst 1829) (Anura: Rhacophoridae). Russian Journal of Herpetology 5, 10–14.
Liu, C. C. (1950). Amphibians of western China. Fieldiana. Zoology Memoirs 2, 1–400.
| Amphibians of western China.Crossref | GoogleScholarGoogle Scholar |
Luna, M. C., Mcdiarmid, R. W., and Faivovich, J. (2018). From erotic excrescences to pheromone shots: structure and diversity of nuptial pads in anurans. Biological Journal of the Linnean Society 124, 403–446.
| From erotic excrescences to pheromone shots: structure and diversity of nuptial pads in anurans.Crossref | GoogleScholarGoogle Scholar |
Martin, A. (1970). Parallel evolution in the adaptive ecology of leptodactylid frogs of South America and Australia. Evolution 24, 643–644.
| Parallel evolution in the adaptive ecology of leptodactylid frogs of South America and Australia.Crossref | GoogleScholarGoogle Scholar | 28562999PubMed |
Méndez-Narváez, J., Flechas, S., and Amézquita, A. (2015). Foam nests provide context-dependent thermal insulation to embryos of three leptodactylid frogs. Physiological and Biochemical Zoology 88, 246–253.
| Foam nests provide context-dependent thermal insulation to embryos of three leptodactylid frogs.Crossref | GoogleScholarGoogle Scholar | 25860824PubMed |
Orizaola, G., and Brana, F. (2003). Oviposition behaviour and vulnerability of eggs to predation in four newt species (genus Triturus). The Herpetological Journal 13, 121–124.
Rivero, J. A. (1969). Observations on the agonistic and breeding behavior of Leptodactylus pentadactylus and other amphibian species in Venezuela. Breviora 321, 1–14.
Ryan, M. J. (1985). ‘The Túngara Frog: a Study in Sexual Selection and Communication.’ (University of Chicago Press: Chicago.)
Salthe, S. N. (1965). Increase in volume of the perivitelline chamber during development of Rana pipiens Schreber. Physiological Zoology 38, 80–98.
| Increase in volume of the perivitelline chamber during development of Rana pipiens Schreber.Crossref | GoogleScholarGoogle Scholar |
Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 22930834PubMed |
Seymour, R. S. (1994). Oxygen diffusion through the jelly capsules of amphibian eggs. Israel Journal of Zoology 40, 493–506.
Seymour, R. S. (1999). Respiration of aquatic and terrestrial amphibian embryos. American Zoologist 39, 261–270.
| Respiration of aquatic and terrestrial amphibian embryos.Crossref | GoogleScholarGoogle Scholar |
Seymour, R. S., and Bradford, D. F. (1995). Respiration of amphibian eggs. Physiological Zoology 68, 1–25.
| Respiration of amphibian eggs.Crossref | GoogleScholarGoogle Scholar |
Seymour, R. S., and Roberts, J. D. (1991). Embryonic respiration and oxygen distribution in foamy and nonfoamy egg masses of the frog Limnodynastes tasmaniensis. Physiological Zoology 64, 1322–1340.
| Embryonic respiration and oxygen distribution in foamy and nonfoamy egg masses of the frog Limnodynastes tasmaniensis.Crossref | GoogleScholarGoogle Scholar |
Stamp, N. E. (1980). Egg deposition patterns in butterflies: why do some species cluster their eggs rather than deposit them singly? American Naturalist 115, 367–380.
| Egg deposition patterns in butterflies: why do some species cluster their eggs rather than deposit them singly?Crossref | GoogleScholarGoogle Scholar |
Stebbins, R. C. (2003). ‘A Field Guide to Western Reptiles and Amphibians.’ (Houghton Mifflin Harcourt: Boston.)
Tyler, M. (1989). ‘Australian Frogs.’ (Viking O’Neil: Melbourne.)
Tyler, M. J., and Crook, G. A. (1983). Reproductive biology of the frogs of the Magela Creek system, Northern Territory. Records of the South Australian Museum 18, 415–440.
Tyler, M. J., and Davies, M. (1979). Foam nest construction by Australian leptodactylid frogs (Amphibia, Anura, Leptodactylidae). Journal of Herpetology 13, 509–510.
| Foam nest construction by Australian leptodactylid frogs (Amphibia, Anura, Leptodactylidae).Crossref | GoogleScholarGoogle Scholar |
Urch, U. A., and Hedrick, J. L. (1981). The hatching enzyme from Xenopus laevis: limited proteolysis of the fertilization envelope. Journal of Supramolecular Structure and Cellular Biochemistry 15, 111–117.
| The hatching enzyme from Xenopus laevis: limited proteolysis of the fertilization envelope.Crossref | GoogleScholarGoogle Scholar | 6965088PubMed |
Wells, K. D. (1977). The social behaviour of anuran amphibians. Animal Behaviour 25, 666–693.
| The social behaviour of anuran amphibians.Crossref | GoogleScholarGoogle Scholar |
Wells, K. (2007). ‘The Ecology and Behavior of Amphibians.’ (The University of Chicago Press: Chicago.)
Yamasaki, H., Katagiri, C., and Yoshizaki, N. (1990). Selective degradation of specific components of fertilization coat and differentiation of hatching gland cells during the two phase hatching of Bufo japonicus embryos. Development, Growth & Differentiation 32, 65–72.
| Selective degradation of specific components of fertilization coat and differentiation of hatching gland cells during the two phase hatching of Bufo japonicus embryos.Crossref | GoogleScholarGoogle Scholar |
Yoshizaki, N., and Katagiri, C. (1975). Cellular basis for the production and secretion of the hatching enzyme by frog embryos. The Journal of Experimental Zoology 192, 203–212.
| Cellular basis for the production and secretion of the hatching enzyme by frog embryos.Crossref | GoogleScholarGoogle Scholar |
Zina, J. (2006). Communal nests in Physalaemus pustulosus (Amphibia: Leptodactylidae): experimental evidence for female oviposition preferences and protection against desiccation. Amphibia-Reptilia 27, 148–150.
| Communal nests in Physalaemus pustulosus (Amphibia: Leptodactylidae): experimental evidence for female oviposition preferences and protection against desiccation.Crossref | GoogleScholarGoogle Scholar |
