Local environmental conditions affecting anuran tadpoles’ microhabitat choice and morphological adaptation
N. C. S. Marques
A B E , L. Rattis B C and F. Nomura D
+ Author Affiliations
- Author Affiliations
A PósGraduação em Ecologia e Evolução, Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Goiânia, Goiás 74001970, Brazil.
B Instituto de Pesquisa Ambiental da Amazônia, Setor de Habitações Individuais Norte Centro de Atividades 5, Bloco J2, Sala 309, Lago Norte, Brasília, Distrito Federal 71503-505, Brazil.
C The Woods Hole Research Center, 149 Woods Hole Road, Falmouth, MA 02540, USA.
D Departamento de Ecologia, Universidade Federal de Goiás, Rodovia Nerópolis Goiânia quilômetro 5 Campus II, Samambaia CP 131, Goiânia, Goiás 74001970, Brazil.
E Corresponding author. Email: marques.ncs@gmail.com
Marine and Freshwater Research 70(3) 395-401 https://doi.org/10.1071/MF18106
Submitted: 6 March 2018 Accepted: 13 July 2018 Published: 4 October 2018
Abstract
In this study, we investigated the environmental variables that best explained tadpole occurrence, as well as associations between environmental variables and the morphological traits of tadpoles. We modelled the occurrence of tadpoles to evaluate the significance of trait–environment relationships by sampling in 86 ponds, measuring a set of environmental descriptors of these ponds, determining the tadpoles’ external-morphology changes and using a generalised linear mixed model approach. The best fitting model predicting tadpole occurrence included all the environmental variables measured (pond dimensions, pond margin type, pond bottom substrate, vegetation type inside the pond, vegetation type in the pond margins, landscape descriptors) and seven morphology–environment interactions. Tadpoles are capable of fine-tuning their morphology according to the environmental traits of the pond and land use changes around the pond. Vegetation heterogeneity of ponds interacts with tadpole morphology primarily on tail size and deviations in the mean position of the eye, nostril and mouth. Moreover, there are increases in body size and tail length in smaller ponds, as well as in ponds surrounded vegetation changes from forest to pasture or short crops. Changes in environmental variables as a result of land use change can affect the dispersion of adult frogs and, consequently, the occurrence of and morphological variations in tadpoles. Local environmental variables play important roles driving tadpoles’ microhabitat choice; once tadpoles cannot select the site of their developmental, they need to compensate for any mismatching by induced morphological adaptations.
Additional keywords: abiotic factors, amphibians, Brazilian Cerrado, ecomorphology, geometric morphometrics.
References
Altig, R., and Johnston, G. F. (1989). Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetological Monograph 3, 81–109.| Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats.Crossref | GoogleScholarGoogle Scholar |
Altig, R., and McDiarmid, R. W. (1999a). Diversity: familial and generic characterizations. In ‘Tadpoles: The Biology of Anuran Larvae’. (Eds R. Altig and R. W. McDiarmid.) pp. 295–337. (The University of Chicago Press: Chicago, IL, USA.)
Altig, R., and McDiarmid, R. W. (1999b). Body plan: development and morphology. In ‘Tadpoles: The Biology of Anuran Larvae’. (Eds R. Altig and R. W. McDiarmid.) pp. 24–51. (The University of Chicago Press: Chicago, IL, USA.)
Altwegg, R., and Reyer, H. U. (2003). Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57, 872–882.
| Patterns of natural selection on size at metamorphosis in water frogs.Crossref | GoogleScholarGoogle Scholar |
Azevedo-Ramos, C., Magnusson, W. E., and Bayliss, P. (1999). Predation as the key factor structuring tadpole assemblages in a savanna area in central Amazonia. Copeia 1999, 22–33.
| Predation as the key factor structuring tadpole assemblages in a savanna area in central Amazonia.Crossref | GoogleScholarGoogle Scholar |
Costa, R. N., and Nomura, F. (2016). Measuring the impacts of Roundup Original on fluctuating asymmetry and mortality in a neotropical tadpole. Hydrobiologia 765, 85–96.
| Measuring the impacts of Roundup Original on fluctuating asymmetry and mortality in a neotropical tadpole.Crossref | GoogleScholarGoogle Scholar |
Costa, R. N., Solé, M., and Nomura, F. (2017). Agropastoral activities increase fluctuating asymmetry in tadpoles of two neotropical anuran species. Austral Ecology 42, 801–809.
| Agropastoral activities increase fluctuating asymmetry in tadpoles of two neotropical anuran species.Crossref | GoogleScholarGoogle Scholar |
de Souza Queiroz, C., da Silva, F. R., and de Rossa-Feres, D. C. C. (2015). The relationship between pond habitat depth and functional tadpole diversity in an agricultural landscape. Royal Society Open Science 2, 150–165.
| The relationship between pond habitat depth and functional tadpole diversity in an agricultural landscape.Crossref | GoogleScholarGoogle Scholar |
Dolédec, S., Chessel, D., Ter Braak, C. J. F., and Champely, S. (1996). Matching species traits to environmental variables: a new three-table ordination method. Environmental and Ecological Statistics 3, 143–166.
| Matching species traits to environmental variables: a new three-table ordination method.Crossref | GoogleScholarGoogle Scholar |
Eterovick, P. C. (2003). Distribution of anuran species among montane streams in southeastern Brazil. Journal of Tropical Ecology 19, 219–228.
| Distribution of anuran species among montane streams in southeastern Brazil.Crossref | GoogleScholarGoogle Scholar |
Eterovick, P. C., and Barata, I. M. (2006). Distribution of tadpoles within and among Brazilian streams: the influence of predators, habitat size and heterogeneity. Herpetologica 62, 365–377.
| Distribution of tadpoles within and among Brazilian streams: the influence of predators, habitat size and heterogeneity.Crossref | GoogleScholarGoogle Scholar |
Gianoli, E., and Valladares, F. (2012). Studying phenotypic plasticity: the advantages of a broad approach. Biological Journal of Linnean Society 105, 1–7.
| Studying phenotypic plasticity: the advantages of a broad approach.Crossref | GoogleScholarGoogle Scholar |
Goldsborough, L. G., and Beck, A. E. (1989). Rapid dissipation of glyphosate in small forest ponds. Archives of Environmental Contamination and Toxicology 18, 537–544.
| Rapid dissipation of glyphosate in small forest ponds.Crossref | GoogleScholarGoogle Scholar |
Grözinger, F., Wertz, A., Thein, J., Feldhaar, H., and Rödel, M. O. (2012). Environmental factors fail to explain oviposition site use in the European common frog. Journal of Zoology 288, 103–111.
| Environmental factors fail to explain oviposition site use in the European common frog.Crossref | GoogleScholarGoogle Scholar |
Inger, R. F., Voris, H. K., and Frogner, K. J. (1986). Organization of a community of tadpoles in rain forest streams in Borneo. Journal of Tropical Ecology 2, 193–205.
| Organization of a community of tadpoles in rain forest streams in Borneo.Crossref | GoogleScholarGoogle Scholar |
Jamil, T., Opdekamp, W., van Diggelen, R., and ter Braak, C. J. (2012). Trait–environment relationships and tiered forward model selection in linear mixed models. International Journal of Ecology 2012, 1–12.
| Trait–environment relationships and tiered forward model selection in linear mixed models.Crossref | GoogleScholarGoogle Scholar |
Jamil, T., Ozinga, W. A., Kleyer, M., and ter Braak, C. J. (2013). Selecting traits that explain species–environment relationships: a generalized linear mixed model approach. Journal of Vegetation Science 24, 988–1000.
| Selecting traits that explain species–environment relationships: a generalized linear mixed model approach.Crossref | GoogleScholarGoogle Scholar |
Kopp, K., Wachlevski, M., and Eterovick, P. C. (2006). Environmental complexity reduces tadpole predation by water bugs. Canadian Journal of Zoology 84, 136–140.
| Environmental complexity reduces tadpole predation by water bugs.Crossref | GoogleScholarGoogle Scholar |
Langerhans, R. B., Chapman, L. J., and DeWitt, T. J. (2007). Complex phenotype–environment associations revealed in an East African cyprinid. Journal of Evolutionary Biology 20, 1171–1181.
| Complex phenotype–environment associations revealed in an East African cyprinid.Crossref | GoogleScholarGoogle Scholar |
Legendre, P., Galzin, R., and Harmelin-Vivien, M. L. (1997). Relating behavior to habitat: solutions to the fourth‐corner problem. Ecology 78, 547–562.
Marques, N. C. S. (2016). Padrões de ocorrência e composição de girinos do Cerrado: importância da interação fenótipo-ambiente e do espaço. Ph.D. Thesis, Universidade de Goiás, Goiânia, Brazil.
Marques, N. S., and Nomura, F. (2015). Where to live? How morphology and evolutionary history predict microhabitat choice by tropical tadpoles. Biotropica 47, 227–235.
| Where to live? How morphology and evolutionary history predict microhabitat choice by tropical tadpoles.Crossref | GoogleScholarGoogle Scholar |
Michel, M. J. (2011). Spatial dependence of phenotypeenvironment associations for tadpoles in natural ponds. Evolutionary Ecology 25, 915–932.
| Spatial dependence of phenotypeenvironment associations for tadpoles in natural ponds.Crossref | GoogleScholarGoogle Scholar |
Miner, B. G., Sultan, S. E., Morgan, S. G., Padilla, D. K., and Relyea, R. A. (2005). Ecological consequences of phenotypic plasticity. Trends in Ecology & Evolution 20, 685–692.
| Ecological consequences of phenotypic plasticity.Crossref | GoogleScholarGoogle Scholar |
Mittermeier, R. A., Gil, P. R., Hoffmann, M., Pilgrim, J., Brooks, C. M., Lamoreux, J., Mittermeier, C. G., da Fonseca, G. A. B., and Seligmann, P. A. (2004). ‘Hotspots Revisited: Earth’s Biologically Wealthiest and Most Threatened Ecosystems.’ (CEMEX: Mexico City, Mexico.)
Nessimian, J. L., Venticinque, E. M., Zuanon, J., De Marco, P., Gordo, M., Fidelis, L., Batista, J. D., and Juen, L. (2008). Land use, habitat integrity, and aquatic insect assemblages in central Amazonian streams. Hydrobiologia 614, 117–131.
| Land use, habitat integrity, and aquatic insect assemblages in central Amazonian streams.Crossref | GoogleScholarGoogle Scholar |
Nogueira, C., Colli, G. R., and Martins, M. (2009). Local richness and distribution of the lizard fauna in natural habitat mosaics of the Brazilian Cerrado. Austral Ecology 34, 83–96.
| Local richness and distribution of the lizard fauna in natural habitat mosaics of the Brazilian Cerrado.Crossref | GoogleScholarGoogle Scholar |
Noland, R., and Ultsch, G. R. (1981). The roles of temperature and dissolved oxygen in microhabitat selection by the tadpoles of a frog Rana pipiens and a toad Bufo terrestris. Copeia 1981, 645–652.
| The roles of temperature and dissolved oxygen in microhabitat selection by the tadpoles of a frog Rana pipiens and a toad Bufo terrestris.Crossref | GoogleScholarGoogle Scholar |
Nomura, F., do Prado, V. H. M., da Silva, F. R., Borges, R. E., Dias, N. Y. N., and Rossa‐Feres, D. D. C. (2011). Are you experienced? Predator type and predator experience trade‐offs in relation to tadpole mortality rates. Journal of Zoology 284, 144–150.
| Are you experienced? Predator type and predator experience trade‐offs in relation to tadpole mortality rates.Crossref | GoogleScholarGoogle Scholar |
Orton, G. L. (1953). The systematics of vertebrate larvae. Systematic Zoology 2, 63–75.
| The systematics of vertebrate larvae.Crossref | GoogleScholarGoogle Scholar |
Orton, G. L. (1957). Larval evolution and frog classification. Systematic Zoology 6, 79–86.
| Larval evolution and frog classification.Crossref | GoogleScholarGoogle Scholar |
Pfennig, D. (1990). The adaptive significance of an environmentally cued developmental switch in an anuran tadpole. Oecologia 85, 101–107.
| The adaptive significance of an environmentally cued developmental switch in an anuran tadpole.Crossref | GoogleScholarGoogle Scholar |
Queiroz, G. M. P., Silva, M. R., Bianco, R. J. F., Pinheiro, A., and Kaufman, V. (2011). Transporte de glifosato pelo escoamento superficial e por lixiviação em um solo agrícola. Quimica Nova 34, 190–195.
| Transporte de glifosato pelo escoamento superficial e por lixiviação em um solo agrícola.Crossref | GoogleScholarGoogle Scholar |
Relyea, R. A. (2002). Competitorinduced plasticity in tadpoles: consequences, cues, and connections to predatorinduced plasticity. Ecological Monographs 72, 523–540.
| Competitorinduced plasticity in tadpoles: consequences, cues, and connections to predatorinduced plasticity.Crossref | GoogleScholarGoogle Scholar |
Relyea, R. A. (2005). The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecological Applications 15, 618–627.
| The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities.Crossref | GoogleScholarGoogle Scholar |
Resetarits, W., Binckley, C. A., and Chalcraft, D. R. (2005). Habitat selection, species interactions, and processes of community assembly in complex landscapes. In ‘Metacommunities: Spatial Dynamics and Ecological Communities’. (Eds M. Holyoak, M. A. Leibold, and R. D. Holt.) pp. 374–398. (University of Chicago Press: Chicago, IL, USA.)
Ribeiro, J. F., and Walter, B. M. T. (2008). As principais fitofisionomias do Bioma Cerrado. In ‘Cerrado: Ecologia e Flora’. (Eds S. M. Sano, S. P. Almeida, and J. F. Ribeiro.) pp. 151–212. (Embrapa Cerrados: Planaltina, Brazil.)
Rohlf, J. F. (1990). Morphometrics. Annual Review of Ecology and Systematics 21, 299–316.
| Morphometrics.Crossref | GoogleScholarGoogle Scholar |
Rossa-Feres, D. C., and Nomura, F. (2006). Characterization and taxonomic key for tadpoles Amphibia, Anura from the northwestern region of São Paulo State, Brazil. Biota Neotropica 6, 1–26.
| Characterization and taxonomic key for tadpoles Amphibia, Anura from the northwestern region of São Paulo State, Brazil.Crossref | GoogleScholarGoogle Scholar |
Rozas, L. P., and Odum, W. E. (1988). Occupation of submerged aquatic vegetation by fishes: testing the roles of food and refuge. Oecologia 77, 101–106.
| Occupation of submerged aquatic vegetation by fishes: testing the roles of food and refuge.Crossref | GoogleScholarGoogle Scholar |
Scheiner, S. M. (1993). Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24, 35–68.
| Genetics and evolution of phenotypic plasticity.Crossref | GoogleScholarGoogle Scholar |
Sneath, P. H., and Sokal, R. R. (1973). ‘Numerical Taxonomy.’ (Freeman: San Francisco, CA, USA.)
Spera, S. A., Galford, G. L., Coe, M. T., Macedo, M. N., and Mustard, J. F. (2016). Land‐use change affects water recycling in Brazil’s last agricultural frontier. Global Change Biology 22, 3405–3413.
| Land‐use change affects water recycling in Brazil’s last agricultural frontier.Crossref | GoogleScholarGoogle Scholar |
Stearns, S. C. (1989). The evolutionary significance of phenotypic plasticity. Bioscience 39, 436–445.
| The evolutionary significance of phenotypic plasticity.Crossref | GoogleScholarGoogle Scholar |
Stein, M., and Blaustein, L. (2015). Larval performance and oviposition habitat selection of the tree frog, Hyla savignyi, in response to conspecific larval density. Israel Journal of Ecology & Evolution 61, 61–66.
| Larval performance and oviposition habitat selection of the tree frog, Hyla savignyi, in response to conspecific larval density.Crossref | GoogleScholarGoogle Scholar |
Teplitsky, C., Piha, H., Laurila, A., and Merilä, J. (2005). Common pesticide increases costs of antipredator defenses in Rana temporaria tadpoles. Environmental Science & Technology 39, 6079–6085.
| Common pesticide increases costs of antipredator defenses in Rana temporaria tadpoles.Crossref | GoogleScholarGoogle Scholar |
Ultsch, G. R., Bradford, D. F., and Freda, J. (1999). Physiology: coping with the environment. In ‘Tadpoles: The Biology of Anuran Larvae’. (Eds R. W. McDiarmid and R. Altig.) pp. 189–214. (The University of Chicago Press: Chicago, IL, USA.)
Valdujo, P. H., Silvano, D. L., Colli, G., and Martins, M. (2012). Anuran species composition and distribution patterns in Brazilian Cerrado, a Neotropical Hotspot. South American Journal of Herpetology 7, 63–78.
| Anuran species composition and distribution patterns in Brazilian Cerrado, a Neotropical Hotspot.Crossref | GoogleScholarGoogle Scholar |
Van Buskirk, J. (2002). A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. American Naturalist 160, 87–102.
| A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae.Crossref | GoogleScholarGoogle Scholar |
Van Buskirk, J. (2005). Local and landscape influence on amphibian occurrence and abundance. Ecology 86, 1936–1947.
| Local and landscape influence on amphibian occurrence and abundance.Crossref | GoogleScholarGoogle Scholar |
Van Buskirk, J. (2009). Getting in shape: adaptation and phylogenetic inertia in morphology of Australian anuran larvae. Journal of Evolutionary Biology 22, 1326–1337.
| Getting in shape: adaptation and phylogenetic inertia in morphology of Australian anuran larvae.Crossref | GoogleScholarGoogle Scholar |
Van Buskirk, J., and Relyea, R. A. (1998). Natural selection for phenotypic plasticity: predator-induced morphological responses in tadpoles. Biological Journal of the Linnean Society. Linnean Society of London 65, 301–328.
| Natural selection for phenotypic plasticity: predator-induced morphological responses in tadpoles.Crossref | GoogleScholarGoogle Scholar |
Van Buskirk, J., McCollum, S. A., and Werner, E. E. (1997). Natural selection for environmentally induced phenotypes in tadpoles. Evolution 51, 1983–1992.
| Natural selection for environmentally induced phenotypes in tadpoles.Crossref | GoogleScholarGoogle Scholar |
Wells, K. D. (2007). ‘The Ecology and Behavior of Amphibians.’ (University of Chicago Press: Chicago, IL, USA.)
Zelditch, M. L., Swiderski, D. L., and Sheets, H. D. (2012). ‘Geometric Morphometrics for Biologists: a Primer.’ (Academic Press, Elsevier: London, UK.)
