Vol. 20 No. 1 (2025)
Articles

Anuran life histories remain consistent across contrasting precipitation regimes in Northeastern Brazilian forests

Francis Luiz Santos Caldas
Instituto Federal de Sergipe, Campus Propriá, CEP 49900-000, Propriá, Brasil
Adrian Antonio Garda
Departamento de Botânica, Ecologia e Zoologia, Universidade Federal do Rio Grande do Norte, CEP 59078-900, Natal, Brasil
Bio
Cássio Rachid Meireles de Almeida Simões
Programa de Pós-Graduação em Biodiversidade e Evolução, Instituto de Biologia, Universidade Federal da Bahia, CEP 40170-115, Salvador, Brasil
Bio
Edinaldo Leite-Filho
Centro de Ciências Agrárias, Laboratório de Microbiologia, Universidade Federal da Paraíba – Campus II, CEP 58397-000, Areia, Brasil
Bio
Renato Gomes Faria
Departamento de Biologia, Laboratório de Répteis e Anfíbios, Universidade Federal de Sergipe, CEP 49100-000, São Cristovão, Brasil
Bio
Daniel Oliveira Mesquita
Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, CEP 58059-900 João Pessoa, Paraíba, Brasil

Published 2025-05-12

Keywords

  • Frogs,
  • local adaptation,
  • abiotic conditions,
  • selective pressures,
  • Ecophysiology,
  • life history,
  • precipitation seasonality
  • ...More
    Less

How to Cite

Francis Luiz Santos Caldas, Antonio Garda, A., Rachid Meireles de Almeida Simões, C., Leite-Filho, E., Gomes Faria, R., & Oliveira Mesquita, D. (2025). Anuran life histories remain consistent across contrasting precipitation regimes in Northeastern Brazilian forests. Acta Herpetologica, 20(1), 49–58. https://doi.org/10.36253/a_h-17047

Abstract

Amphibians are inherently dependent on water, and many species characteristics are influenced by this resource, particularly in ecoregions with contrasting precipitation regimes, such as the dry Caatinga and the moist Atlantic Forests of Northeastern Brazil. We compared these environments and hypothesized that anurans, regardless of the species, would be smaller in the Caatinga due to unpredictable duration of the rainy season, which accelerates metamorphosis, and the resulting fluctuations of resources, which limit energy reserves for growth. Furthermore, we anticipated that female reproductive strategies in the Caatinga would be more focused on quality rather than quantity, with small clutches and large oocytes. To test these hypotheses, we sampled areas of Caatinga and Atlantic Forest (two of each) in northeastern Brazil through 15-day consecutive campaigns conducted during the dry and rainy seasons. We combined active searches and pitfall traps to collect the anurans. We performed intraspecific comparisons using morphometric measurements and number and volume of oocytes. Contrary to our expectations, body size did not differ between forests for either sex. In moist environments, the extended reproductive period and the associated energetic demands may constrain growth, imposing costs similar to those in the semiarid environment, resulting in comparable body sizes. Similarly, few differences were observed in oocyte numbers and volumes. Leptodactylus macrosternum and Rhinella diptycha showed fewer and smaller oocytes, respectively, in the Caatinga. Biological factors such as lifespan and body size, and environmental factors such as the duration of the hydroperiod, predation, and insolation can influence oocyte size and numbers in different conditions. However, they likely interact in minimizing energy expenditure, resulting in similar reproductive strategies in contrasting environments.

References

  1. Ab’Saber, A.N. (1977): Os domínios morfoclimáticos na América do Sul: primeira aproximação. Geomorfologia 52: 1-121.
  2. Ab’Saber, A.N. (1999): Sertões e sertanejos: uma geografia humana sofrida. Estud. Av. 13: 7-59. DOI: https://doi.org/10.1590/S0103-40141999000200002
  3. Afonso, L.G., Eterovick, P.C. (2007): Spatial and temporal distribution of breeding anurans in streams in southeastern Brazil. J. Nat. Hist. 41: 949-963. DOI: https://doi.org/10.1080/00222930701311680
  4. Aguiar, A.J.C., Martins, C.F. (2002): Abelhas e vespas solitárias em ninhos-armadilha na Reserva Biológica Guaribas (Mamanguape, Paraíba, Brasil). Rev. Bras. Zool. 19: 101-116. DOI: https://doi.org/10.1590/S0101-81752002000500005
  5. Andrade-Lima, D. (1981): The caatingas dominium. Rev. Bras. Bot. 4: 149-163.
  6. Arzabe, C., Carvalho, C.X., Costa, M.A.G. (1998): Anuran assemblages in Crasto Forest ponds (Sergipe State, Brazil): comparative structure and calling activity patterns. Herpetol. J. 8: 111-113.
  7. Arzabe, C. (1999): Reproductive activity patterns of anurans in two different altitudinal sites within the Brazilian Caatinga. Rev. Bras. Zool. 16: 851-864. DOI: https://doi.org/10.1590/S0101-81751999000300022
  8. Barbosa, M.R.V., Thomas, W.W., Zárate, E.L.P., Lima, R.B., Agra, M.F., Lima, I.B., Pessoa, M.C.R., Lourenço, A.R.L., Delgado Júnior, G.C., Pontes, R.A., Chagas, E.C.O., Viana, J.L., Neto, P.C.G., Araújo, C.M.L.R., Araújo, A.A.M., Freita, G.B., Lima, J.R., Silva, F.O., Vieira, L.A.F., Pereira, L.A., Costa, R.M.T., Duré, R.C., Sá, M.G.V. (2011): Checklist of the vascular plants of the Guaribas Biological Reserve, Paraíba, Brazil. Rev. Nord. Biol. 20: 79-106.
  9. Bento, D.M., Ferreira, R.L., Prous, X., Souza-Silva, M., Bellini, B.C., Vasconcellos, A. (2016): Seasonal variations in cave invertebrate communities in the semiarid Caatinga, Brazil. J. Cave Karst Stud. 78: 61-71. DOI: https://doi.org/10.4311/2015LSC0111
  10. Blaustein, A.R., Edmond, B., Kiesecker, J.M., Beatty, J.J., Hokit, D.G. (1995): Ambient ultraviolet radiation causes mortality in salamander eggs. Ecol. Appl. 5: 740-743. DOI: https://doi.org/10.2307/1941981
  11. Blaustein, L., Garb, J.E., Shebitz, D., Nevo, E. (1999): Microclimate, developmental plasticity and community structure in artificial temporary pools. Hydrobiologia 392: 187-196. DOI: https://doi.org/10.1023/A:1003559332439
  12. Bradshaw, C.J.A., McMahon, C.R. (2008): Fecundity. In: Encyclopedia of Ecology, pp. 1535-1543. Amsterdam, Elsevier Inc. DOI: https://doi.org/10.1016/B978-008045405-4.00645-5
  13. Brandão, R.A., Fenker, J., Lopes, B.E.P.C., Sena, V.M.A., Vasconcelos, B.D. (2020): Diet of terrestrial anurans in an ephemeral and simplified habitat during the dry season in the Brazilian Cerrado. Ethol. Ecol. Evol. 1: 1-24.
  14. Braun, P.C., Braun, C.A.S. (1977): Nova espécie de Hyla do Estado do Rio Grande do Sul, Brasil (Anura, Hylidae). Rev. Bras. Biol. 37: 853-857.
  15. Caldas, F.L.S., Silva, B.D., Santos, R.A., De-Carvalho, C.B., Santana, D.O., Gomes, F.F.A., Faria, R.G. (2016): Autoecology of Phyllomedusa nordestina (Anura: Hylidae) in areas of the Caatinga and Atlantic Forest in the State of Sergipe, Brazil. North-West. J. Zool. 12: 271-285.
  16. Caldas, F.L.S., Garda, A.A., Cavalcanti, L.B.Q., Leite-Filho, E., Faria, R.G., Mesquita, D.O. (2019): Spatial and trophic structure of anuran assemblages in environments with different seasonal regimes in the Brazilian Northeast Region. Copeia 107: 567-584. DOI: https://doi.org/10.1643/CH-18-109
  17. Cechin, S.Z., Martins, M. (2000): Eficiência de armadilhas de queda (pitfall traps) em amostragens de anfíbios e répteis no Brasil. Rev. Bras. Zool. 17: 729-740. DOI: https://doi.org/10.1590/S0101-81752000000300017
  18. Crump, M.L., Scott, N.J.J. (1994): Measuring and monitoring biological diversity: standard methods for amphibians. In: Standard Techniques for Inventory and Monitoring, pp. 76-141. Heyer, W.R., Donnelly, M.A., Mcdiarmid, R.W., Hayek, L.C., Foster, M.S., Eds., Washington, D.C., Eds, Smithsonian Institution Press.
  19. Dayton, G.H., Fitzgerald, L.A. (2001): Competition, predation, and the distributions of four desert anurans. Oecologia 129: 430-435. DOI: https://doi.org/10.1007/s004420100727
  20. Dayton, G.H., Fitzgerald, L.A. (2006): Habitat suitability models for desert amphibians. Biol. Cons. 132: 40-49. DOI: https://doi.org/10.1016/j.biocon.2006.03.012
  21. Demetrius, L. (2000): Directionality theory and the evolution of body size. Proc. R. Soc. B. 267: 2385-2391. DOI: https://doi.org/10.1098/rspb.2000.1295
  22. Dias, S.C., Candido, D.M., Brescovit, A.D. (2006): Scorpions from Mata do Buraquinho, João Pessoa, Paraíba, Brazil, with ecological notes on a population of Ananteris mauryi Lourenço (Scorpiones, Buthidae). Rev. Bras. Zool. 23: 707-710. DOI: https://doi.org/10.1590/S0101-81752006000300014
  23. Dinerstein, E., Olson, D., Joshi, A., Vynne, C., Burgess, N., Wikramanayake, E., Saleem, M. (2017): Ecoregions 2017. Resolve. https://ecoregions.appspot.com/.
  24. Enge, K.M. (2001): The pitfalls of pitfall traps. J. Herpetol. 35: 467-478. DOI: https://doi.org/10.2307/1565965
  25. Fox, J., Marquez, M.M., Bouchet-Valat, M. (2024). Rcmdr: R Commander. R package version 2.9-5, https://github.com/RCmdr-Project/rcmdr.
  26. García, J., Arizaga, J., Rodríguez, J.I., Alonso, D., Suárez‐Seoane, S. (2021): Morphological differentiation in a migratory bird across geographic gradients in mountains of southern Europe. J. Biogeogr. 48: 2828-2838. DOI: https://doi.org/10.1111/jbi.14242
  27. Heyer, W.R. (1969): The adaptive ecology of the species groups of the genus Leptodactylus (Amphibia, Leptodactylidae). Evolution 23: 421-428. DOI: https://doi.org/10.1111/j.1558-5646.1969.tb03525.x
  28. Horato, M.N., Almeida-Santos, M., Rocha, C.F.D., Sabagh, L.T. (2024): Reproductive ecology of treefrogs: egg size promotes reproductive effort differences between females. Evol. Ecol. 38: 481-493. DOI: https://doi.org/10.1007/s10682-024-10306-3
  29. Howard, R.D. (1981): Sexual dimorphism in bullfrogs. Ecology 62: 303-310. DOI: https://doi.org/10.2307/1936704
  30. INMET (2012): Instituto Nacional de Meteorologia. https://portal.inmet.gov.br.
  31. INMET (2013): Instituto Nacional de Meteorologia. https://portal.inmet.gov.br.
  32. Jared, C., Mailho‐Fontana, P.L., Mendelson, J., Antoniazzi, M.M. (2019): Life history of frogs of the Brazilian semi‐arid (Caatinga), with emphasis in aestivation. Acta Zool. 101: 302-310. DOI: https://doi.org/10.1111/azo.12295
  33. Jolicoeur, P. (1963): The multivariate generalization of the allometry equation. Biometrics 19: 497-499. DOI: https://doi.org/10.2307/2527939
  34. Joly, C.A., Metzger, J.P., Tabarelli, M. (2014): Experiences from the Brazilian Atlantic Forest: ecological findings and conservation initiatives. New Phytol. 204: 459-473. DOI: https://doi.org/10.1111/nph.12989
  35. Kissel, A.M., Palen, W.J., Ryan, M.E., Adams, M.J. (2019): Compounding effects of climate change reduce population viability of a montane amphibian. Ecol. Appl. 29: 1-12. DOI: https://doi.org/10.1002/eap.1832
  36. Li, H., Cui, C., Shen, H., Zhu, Y., Chen, Z., Chen, X. (2023): Morphological variation and its correlation with bioclimatic factors in Odorrana graminea sensu stricto. Front. Ecol. Evol. 11: 1-11. DOI: https://doi.org/10.3389/fevo.2023.1139995
  37. Liao, W.B., Luo, Y., Lou, S.L., Lu, D., Jehle, R. (2016): Geographic variation in life-history traits: growth season affects age structure, egg size and clutch size in Andrew’s toad (Bufo andrewsi). Front. Zool. 13: 1-9. DOI: https://doi.org/10.1186/s12983-016-0138-0
  38. Lima, P.J., Heckendorff, W.D. (1985): Climatologia. In: Atlas Geográfico do Estado da Paraíba, pp. 34-43. UFPB, Ed., João Pessoa, Governo do Estado da Paraíba.
  39. Melchiors, J., Di-Bernardo, M., Pontes, G.M.F., de Oliveira, R.B., Solé, M., Kwet, A. (2004): Reproduction of Pseudis minuta (Anura, Hylidae) in southern Brazil. Phyllomedusa 3: 61-68. DOI: https://doi.org/10.11606/issn.2316-9079.v3i1p61-68
  40. Mesquita, D.O., Costa, G.C., Zatz, M.G. (2004): Ecological aspects of the casque-headed frog Aparasphenodon brunoi (Anura, Hylidae) in a Restinga habitat in southeastern Brazil. Phyllomedusa 3: 51-59. DOI: https://doi.org/10.11606/issn.2316-9079.v3i1p51-59
  41. Moreira, D.C., Carvajalino-Fernández, J.M., Navas, C.A., Carvalho, J.E., Hermes-Lima, M. (2021): Metabolic and redox biomarkers in skeletal muscle underlie physiological adaptations of two estivating anuran species in a South American semi-arid environment. Front. Physiol. 12: 1-13. DOI: https://doi.org/10.3389/fphys.2021.769833
  42. Morrison, C., Hero, J.M. (2003): Geographic variation in life‐history characteristics of amphibians: a review. J. Anim. Ecol. 72: 270-279. DOI: https://doi.org/10.1046/j.1365-2656.2003.00696.x
  43. Napoli, M.F., Pimenta, B.V.S. (2009): A new species of the Bokermannohyla circumdata group (Anura: Hylidae) from the coastal forests of Bahia, Northeastern Brazil. Copeia 2009: 674-683. DOI: https://doi.org/10.1643/CH-08-224
  44. Navas, C.A., Antoniazzi, M.M., Jared, C. (2004): A preliminary assessment of anuran physiological and morphological adaptation to the Caatinga, a Brazilian semi-arid environment. Int. Congr. Ser. 1275: 298-305. DOI: https://doi.org/10.1016/j.ics.2004.08.061
  45. Neckel-Oliveira, S. (2004): Effects of landscape change on clutches of Phyllomedusa tarsius, a neotropical treefrog. Biol. Cons. 118: 109-116. DOI: https://doi.org/10.1016/j.biocon.2003.07.013
  46. Nimer, E. (1979): Climatologia do Brasil. Rio de Janeiro, IBGE.
  47. Nimer, E. (1989): Climatologia da região Nordeste. In: Climatologia do Brasil, p. 315-361. IBGE, DRNEA, Eds., Rio de Janeiro, Fundação Instituto Brasileiro de Geografia e Estatística.
  48. Nunes-de-Almeida, C.H.L., Haddad, C.F.B., Toledo, L.F. (2021): A revised classification of the amphibian reproductive modes. Salamandra, 57: 413-427.
  49. Oliveira-Filho, A., Carvalho, D. (1993): Floristica e fisionomia da vegetação no extremo norte do litoral da Paraíba. Rev. Bras. Bot. 16: 115-130.
  50. Pavón‐Vázquez, C.J., Brennan, I.G., Skeels, A., Keogh, J.S. (2022): Competition and geography underlie speciation and morphological evolution in Indo‐Australasian monitor lizards. Evolution 76: 476-495. DOI: https://doi.org/10.1111/evo.14403
  51. Pfennig, D.W., Murphy, P.J. (2002): How fluctuating competition and phenotypic plasticity mediate species divergence. Evolution 56: 1217-1228. DOI: https://doi.org/10.1111/j.0014-3820.2002.tb01433.x
  52. Pough, F.H., Taigen, T.L., Stewart, M.M., Brussard, P.F. (1983): Behavioral modification of evaporative water loss by a Puerto Rican frog. Ecology 64: 244-252. DOI: https://doi.org/10.2307/1937072
  53. R Development Core Team (2018): R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
  54. Roff, D.A. (1992): Evolution of Life Histories: theory and Analysis. New York, Chapman e Hall.
  55. Roff, D.A. (2002): Life-history Evolution. Sunderland, Sinauer Associates. DOI: https://doi.org/10.1016/B978-0-12-384719-5.00087-3
  56. Rohlf, F.J., Bookstein, F.L. (1987): A comment on shearing as a method for “size correction”. Syst. Biol. 36: 356-367. DOI: https://doi.org/10.2307/2413400
  57. Saenz, D., Fitzgerald, L.A., Baum, K.A., Conner, R.N., Adams, D. (2006): Abiotic correlates of anuran calling phenology: the importance of rain, temperature, and season. Herpetol. Monogr. 20: 64-82. DOI: https://doi.org/10.1655/0733-1347(2007)20[64:ACOACP]2.0.CO;2
  58. Santana, G.G., Vieira, W.L., Pereira-Filho, G.A., Delfim, F.R., Lima, Y.C., Vieira, K.S. (2008): Herpetofauna em um fragmento de Floresta Atlântica no estado da Paraíba, Região Nordeste do Brasil. Biotemas 21: 75-84. DOI: https://doi.org/10.5007/2175-7925.2008v21n1p75
  59. Schäuble, C.S. (2004): Variation in body size and sexual dimorphism across geographical and environmental space in the frogs Limnodynastes tasmaniensis and L. peronii. Biol. J. Linn. Soc. 82: 39-56. DOI: https://doi.org/10.1111/j.1095-8312.2004.00315.x
  60. Schiwitz, N.C., Schalk, C.M., Saenz, D. (2020): Activity level-predation risk tradeoff in a tadpole guild: implications for community organization along the hydroperiod gradient. Am. Midl. Nat. 183: 223-232.
  61. Silva, I.S., Lucena, E.F., Moura, F.M.S., Vasconcellos, A. (2021): Termite flights seasonally promote nutrient pulses in the Caatinga dry forest in northeastern Brazil. Appl. Soil Ecol. 166: 1-6. DOI: https://doi.org/10.1016/j.apsoil.2021.104066
  62. Silva, J.M.C., Barbosa, L.C.F., Leal, I.R., Tabarelli, M. (2017): The Caatinga: understanding the challenges. In: Caatinga: the Largest Tropical Dry Forest Region in South America, pp. 3-19. Silva, J.M.C., Leal, I.R., Tabarelli, M., Eds, Gewerbestrasse, Springer International Publishing. DOI: https://doi.org/10.1007/978-3-319-68339-3_1
  63. Sinsch, U., Pelster, B., Ludwig, G. (2015): Large-scale variation of size- and age-related life-history traits in the common frog: a sensitive test case for macroecological rules. J. Zool. 297: 32-43. DOI: https://doi.org/10.1111/jzo.12243
  64. Somers, K.M. (1986): Multivariate allometry and removal of size with principal components analysis. Syst. Biol. 35: 359-368. DOI: https://doi.org/10.1093/sysbio/35.3.359
  65. Sousa, T.R., Benício, R.A., Fonseca, M.G. (2022): Polimorfismo em Rhinella diptycha (Anura: Bufonidae) em uma área de Caatinga, estado do Piauí, Nordeste do Brasil. Biosphere 1: 16-22.
  66. Stark, G., Meiri, S. (2018): Cold and dark captivity: Drivers of amphibian longevity. Glob. Ecol. Biogeogr. 27: 1384-1397. DOI: https://doi.org/10.1111/geb.12804
  67. Sullivan, B.K., Fernandez, P.J. (1999): Breeding activity, estimated age-structure, and growth in sonoran desert anurans. Herpetologica 55: 334-343.
  68. Tevis Jr, L. (1966): Unsuccessful breeding by desert toads (Bufo punctatus) at the limit of their ecological tolerance. Ecology 47: 766-775. DOI: https://doi.org/10.2307/1934263
  69. Tiar-Saadi, M., Tiar, G., Bouslama, Z., Široký, P. (2022): Mechanisms determining body size and shape difference in Algerian spur-thighed tortoises (Testudo graeca). Animals 12: 1-21. DOI: https://doi.org/10.3390/ani12101330
  70. Tonhasca-Júnior, A. (2005): Ecologia e História Natural da Mata Atlântica. Rio de Janeiro, Interciência.
  71. Varjão, I.C.G., Ribeiro, L.B. (2018): Field record of aestivation with formation of cocoon in the frog Leptodactylus fuscus (Anura: Leptodactylidae) in a semiarid region of northeastern Brazil. Phyllomedusa 17: 135-138. DOI: https://doi.org/10.11606/issn.2316-9079.v17i1p135-138
  72. Velloso, A.L., Sampaio, E.V., Giulietti, A.M., Barbosa, M.R.V., Castro, A.A.J.F., Queiroz, L.P., Fernandes, A., Oren, D.C., Cestaro, L.A., Carvalho, A.J.E. (2002): Ecorregiões Propostas para o Bioma Caatinga. Recife, Flamar Gráfica e Editora.
  73. Vieira, W.L.S., Arzabe, C., Santana, G.G. (2007): Composição e distribuição espaço-temporal de anuros no Cariri paraibano, Nordeste do Brasil. Oecol. Bras. 11: 383-396. DOI: https://doi.org/10.4257/oeco.2007.1103.08
  74. Werner, E.E. (1986): Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Amer. Nat. 128: 319-341. DOI: https://doi.org/10.1086/284565
  75. Wiens, J.J., Pyron, R.A., Moen, D.S. (2011): Phylogenetic origins of local‐scale diversity patterns and the causes of Amazonian megadiversity. Ecol. Lett. 14: 643-652. DOI: https://doi.org/10.1111/j.1461-0248.2011.01625.x
  76. Woodward, B.D. (1983): Predator-prey interactions and breeding-pond use of temporary-pond species in a desert anuran community. Ecology 64: 1549-1555. DOI: https://doi.org/10.2307/1937509