Vol. 19 No. 2 (2024)
Articles

The effect of climate change on spatio-temporal activity in burrowing frogs of the Smilisca group

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  • Alondra Encarnación-Luévano,
  • J. Jesús Sigala-Rodríguez,
  • Gustavo E. Quintero-Díaz,
  • Marcelo Silva Briano,
  • Octavio Rojas-Soto
Alondra Encarnación-Luévano
Colección Zoológica, Departamento de Biología, Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México
J. Jesús Sigala-Rodríguez
Colección Zoológica, Departamento de Biología, Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México
Gustavo E. Quintero-Díaz
Departamento de Biología, Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México
Marcelo Silva Briano
Laboratorio de Ecología, Departamento de Biología, Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México
Octavio Rojas-Soto
Laboratorio de Bioclimatología, Red de Biología Evolutiva, Instituto de Ecología A. C., Xalapa, Veracruz 91073, México
DOI: https://doi.org/10.36253/a_h-15232

Published 2024-11-16

Keywords

  • ecological niche modeling,
  • seasonal niche,
  • distribution,
  • anurans,
  • estivation,
  • global warming
    • ...More
    Less

How to Cite

Encarnación-Luévano, A., Sigala-Rodríguez, J. J., Quintero-Díaz, G. E., Silva Briano, M., & Rojas-Soto, O. (2024). The effect of climate change on spatio-temporal activity in burrowing frogs of the Smilisca group. Acta Herpetologica, 19(2), 139–153. https://doi.org/10.36253/a_h-15232

Copyright (c) 2024 Alondra Encarnación-Luévano, José Jesús Sigala-Rodríguez, Gustavo E. Quintero-Díaz, Marcelo Silva-Briano, Octavio Rojas-Soto

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This work is licensed under a Creative Commons Attribution 4.0 International License.

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Abstract

Measuring the potential effects of future climate changes on the spatio-temporal variance of optimal conditions for seasonal species is a key conservation issue. This study assesses the impact of climate change on the spatial and temporal patterns of optimal conditions for activity in two burrowing frogs, Smilisca fodiens and S. dentata. Ecological Niche Modeling was used to implement niche seasonality models, with calibration performed during the peak activity (July). These models were then transferred to current and future conditions for the remainder of the year, predicting future scenarios up to 2070 with an intermediate trajectory greenhouse gas concentration of 4.5 W/m2. Climate change transferability was assessed for four potential scenarios: 1) high precipitation and low temperature, 2) high precipitation and high temperature, 3) low precipitation and low temperature, and 4) low precipitation and high temperature. We examined the impact across future projected areas and analyzed geographic change trends based on latitude, longitude, and elevation. For both species, the best scenario would involve increased precipitation in the future. However, the worst-case would be a combination of reduced precipitation and higher temperatures. Due to large area loss, northern populations of S. fodiens may be highly vulnerable. Concerning S. dentata, the outlook is worrisome, with all known populations experiencing losses in most months. Area gains may not help either species since they tend to occur at elevations above their known ranges. Using a seasonal approach in spatio-temporal analysis enhances comprehension of the behavioral adaptations of seasonal species and their vulnerability to current and future climatic variations.

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References

  1. Bachmann, J.C., Van Buskirk, J. (2021): Adaptation to elevation but limited local adaptation in an amphibians. Evolution 75: 956-969. DOI: https://doi.org/10.1111/evo.14109
  2. Barve, N., Barve, V., Jiménez-Valverde, A., Lira-Noriega, A., Maher, S.P., Peterson, A.T., Villalobos, F. (2011): The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecol. Modell. 222: 1810-1819. DOI: https://doi.org/10.1016/j.ecolmodel.2011.02.011
  3. Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W., Courchamp, F. (2012): Impacts of climate change on the future of biodiversity. Ecol. Lett. 15: 365-377. DOI: https://doi.org/10.1111/j.1461-0248.2011.01736.x
  4. Bodensteiner, B.L., Agudelo-Cantero, G.A., Arietta, A.Z.A., Gunderson, A.R., Muñoz, M.M., Refsnider, J.M., Gangloff, E.J. (2021): Thermal adaptation revisited: How conserved are thermal traits of reptiles and amphibians? J. Exp. Zool. 335: 173-194. DOI: https://doi.org/10.1002/jez.2414
  5. Breckenridge, W.J., Tester, J.R. (1961): Growth, local movements and hibernation of the Manitoba toad, Bufo hemiophrys. Ecology 42: 637-646. DOI: https://doi.org/10.2307/1933495
  6. Breiner, F.T., Guisan, A., Bergamini, A., Nobis, M.P. (2015): Overcoming limitations of modelling rare species by using ensembles of small models. Methods Ecol. Evol. 6: 1210-1218. DOI: https://doi.org/10.1111/2041-210X.12403
  7. Clavel, J., Julliard, R., Devictor, V. (2011): Worldwide decline of specialist species: toward a global functional homogenization? Front. Ecol. Environ. 9: 222-228. DOI: https://doi.org/10.1890/080216
  8. Chadwick, E.A., Slater, F.M., Ormerod, S.J. (2006): Inter- and intraspecific differences in climatically mediated phenological change in coexisting Triturus species. Global Chang. Biol. 12: 1069-1078. DOI: https://doi.org/10.1111/j.1365-2486.2006.01156.x
  9. Chandler, H.C., Rypel, A.L., Jiao, Y., Haas, C.A., Gorman, T.A. (2016): Hindcasting historical breeding conditions for an endangered salamander in ephemeral wetlands of the southeastern USA: implications of climate change. PLoS ONE. 11: e0150169. DOI: https://doi.org/10.1371/journal.pone.0150169
  10. Cobos, M.E., Peterson, A.T., Barve, N., Osorio-Olvera, L. (2019): kuenm: an R package for detailed development of ecological niche models using Maxent. PeerJ 7: e6281. DOI: https://doi.org/10.7717/peerj.6281
  11. Cohen, J., Jetz, W. (2023): Diverse strategies for tracking seasonal environmental niches at hemispheric scale. Global Ecol. Biogeog. 32: 1549-1560. DOI: https://doi.org/10.1111/geb.13722
  12. Dawson, T.P., Jackson, S.T., House, I.J., Prentice, I.C., Mace, G.M. (2011): Beyond Forecasts: Conserving Biodiversity Under Climate Change. Science 332: 53-58. DOI: https://doi.org/10.1126/science.1200303
  13. de la Cerda, L.M. (2008): Pastizal. In: La Biodiversidad en Aguascalientes: Estudio de Estado, pp. 92-97. Ávila, H., Melgarejo, E.D., Cruz, A., Eds, CONABIO, IMAE, UAA.
  14. De Mendiburu, F. (2023): agricolae: Statistical procedures for agricultural research. R package version 1.2-6. https://CRAN.R-project.org/package=agricolae.
  15. Duellman, W.E. (2001): The Hylid Frogs of Middle America. Society for the Study of Amphibians and Reptiles Press, Kansas.
  16. Encarnación-Luévano, A., Quintero-Díaz, G.E. (In Press): Contribution to the ecology and natural history of the upland burrowing treefrog Smilisca dentata. J. Herpetol.
  17. Encarnación-Luévano, A., Peterson, A.T., Rojas-Soto, O.R. (2021): Burrowing habit in Smilisca frogs as an adaptive response to ecological niche constraints in seasonally dry environments. Front. Biogeogr. 13: e50517. DOI: https://doi.org/10.21425/F5FBG50517
  18. Encarnación-Luévano, A., Rojas-Soto, O.R., Sigala-Rodríguez, J.J. (2013): Activity response to climate seasonality in species with fossorial habits: a niche modeling approach using the Lowland Burrowing Treefrog (Smilisca fodiens). PLoS ONE. 8: 1-7. DOI: https://doi.org/10.1371/journal.pone.0078290
  19. Esparza-Orozco, A., Lira-Noriega, A., Martínez-Montoya, J.F., Pineda-Martínez, L.F., Méndez-Gallegos, S.J. (2020): Influences of environmental heterogeneity on amphibian composition at breeding sites in a semiarid region of Mexico. J. Arid Enviro. 182: 104259. DOI: https://doi.org/10.1016/j.jaridenv.2020.104259
  20. ESRI 2019. ArcGIS Desktop: Release 10.8. Redlands, CA: Environmental Systems Research Institute.
  21. Fajardo, J., Corcoran, D., Roehrdanz, P.R., Hannah, L., Marquet, P.A. (2020): GCM compareR: A web application to assess differences and assist in the selection of general circulation models for climate change research. Methods Ecol. Evol. 11: 656-663. DOI: https://doi.org/10.1111/2041-210X.13360
  22. Farooqi, T.J., Irfan, M., Protela, R., Zhou, X., Shulin, P., Ali, A. (2022): Global progress in climate change and biodiversity conservation research. Glob. Ecol. Conserv. 38: e02272. DOI: https://doi.org/10.1016/j.gecco.2022.e02272
  23. Gámez-Brunswick, C., Rojas-Soto, O. (2020): The effect of seasonal variation in the activity patterns of the American Black Bear: an ecological niche modelling approach. Mammalia 84: 315-322. DOI: https://doi.org/10.1515/mammalia-2019-0017
  24. Goldberg, S.R. (2019): Notes on Reproduction of Lowland Burrowing Treefrogs, Smilisca fodiens (Anura: Hylidae), from Sinaloa and Sonora, Mexico. Bull. Chic. Herpetol. Soc. 54: 83-84.
  25. Green, T., Das, E., Green, D.M. (2016): Springtime Emergence of Overwintering Toads, Anaxyrus fowleri, in Relation to Environmental Factors. Copeia. 104: 393-401. DOI: https://doi.org/10.1643/CE-15-323
  26. Guevara, L., Gerstner, B.E., Kass, J.M., Anderson, R.P. (2017): Toward ecologically realistic predictions of species distributions: A cross-time example from tropical montane cloud forests. Glob. Chang. Biol. 24: 1511-1522. DOI: https://doi.org/10.1111/gcb.13992
  27. Habibullah, M.S., Din, B.H., Tan, S.H., Zahid, H. (2021): Impact of climate change on biodiversity loss: global evidence. Environ. Sci. Pollut. Res. 29: 1073–1086. DOI: https://doi.org/10.1007/s11356-021-15702-8
  28. Höök, M., Sivertsson, A., Aleklett, K. (2010): Validity of the Fossil Fuel Production Outlooks in the IPCC Emission Scenarios. Nat. Resour. Res. 19: 63-81. DOI: https://doi.org/10.1007/s11053-010-9113-1
  29. IPCC (2014): Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Core Writing Team, Pachauri, R.K., Meyer, L.A. Eds, IPCC, Geneva, Switzerland.
  30. Jaramillo, V.J., García-Oliva, F., Martínez-Yrízar, A. (2010): La selva seca y el disturbio antrópico en un contexto funcional. In: Diversidad, amenazas y áreas prioritarias para la conservación de las selvas secas del Pacífico de México, pp. 235-250. Ceballos, G., Martínez, L., García, A., Espinoza, E., Bezaury-Creel, Dirzo, R., Eds, Fondo de Cultura Económica and CONABIO.
  31. Jimenez-Valverde, A. (2020): Sample size for the evaluation of presence-absence models. Ecol. Indic. 114: 106289. https://doi.org/10.1016/j.ecolind.2020.106289 DOI: https://doi.org/10.1016/j.ecolind.2020.106289
  32. Karger, D.N., Conrad, O., Böhner, J., Kawohl, T., Kreft, H., Soria-Auza, R.W., Zimmermann, N.E., Linder, P., Kessler, M. (2017): Climatologies at high resolution for the Earth land surface areas. Sci. Data 4: 170122. DOI: https://doi.org/10.1038/sdata.2017.122
  33. Martínez-Meyer, E., Peterson, A.T., Navarro-Sigüenza, A. (2004): Evolution of seasonal ecological niches in the Passerina buntings (Aves: Cardinalidae). Proc. Royal Soc. B 271: 1151-1157. DOI: https://doi.org/10.1098/rspb.2003.2564
  34. Nakazawa, Y., Peterson, A.T., Martínez-Meyer, E., Navarro-Sigüenza, A. (2004): Seasonal Niches of Nearctic-Neotropical Migratory Birds: Implications for the Evolution of Migration. The Auk. 121: 610-618. DOI: https://doi.org/10.1093/auk/121.2.610
  35. Navas, C.A., Gomes, F.R., Carvalho, J.E. (2008): Thermal relationships and exercise physiology in anuran amphibians: Integration and evolutionary implications. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 151: 344-362. DOI: https://doi.org/10.1016/j.cbpa.2007.07.003
  36. Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C., D’amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C., Loucks, C.J., Allnutt, T.F., Ricketts, T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P., Kassem, K. (2001): Terrestrial ecoregions of the world: a new map of life on Earth. BioScience 51: 933-938. DOI: https://doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2
  37. Owens, H.L., Campbell, L.P., Dornak, L.L., Saupe, E.E., Barve, N., Soberón, J., Ingenloff, K., Lira-Noriega, A., Hensz, C.M., Myers, C.E., Peterson, A.T. (2013): Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas. Ecol. Modell. 263: 10-18. DOI: https://doi.org/10.1016/j.ecolmodel.2013.04.011
  38. Pacifici, M., Visconti, P., Butchart, S., Watson, J.E.M., Cassola, F.M., Rondinini, C. (2017): Species’ traits influenced their response to recent climate change. Nat. Clim. Change 7: 205-208. DOI: https://doi.org/10.1038/nclimate3223
  39. Parra, J.L., Graham, C.C., Freile, J.F. (2004): Evaluating alternative data sets for ecological niche models of birds in the Andes. Ecography 27: 350-360. DOI: https://doi.org/10.1111/j.0906-7590.2004.03822.x
  40. Pearson, R.G., Raxworthy, C.J., Nakamura, M., Peterson, A.T. (2007): Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J. Biogeogr. 34: 102-117. DOI: https://doi.org/10.1111/j.1365-2699.2006.01594.x
  41. Peterson, A.T., Ortega-Huerta, M.A., Bartley, J., Sánchez-Cordero, V., Soberón, J., Buddemeier, R.H., Stockwell, D.R.B. (2002): Future projections for Mexican faunas under global climate change scenarios. Nature 416: 626-629. DOI: https://doi.org/10.1038/416626a
  42. Peterson, A.T., Papeş, M., Soberón, J. (2008): Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecol. Modell. 213: 63-72. DOI: https://doi.org/10.1016/j.ecolmodel.2007.11.008
  43. Phillips, S.J., Anderson, R.P., Schapire, R.E. (2006): Maximum entropy modeling of species geographic distributions. Ecol. Modell. 190: 231-259. DOI: https://doi.org/10.1016/j.ecolmodel.2005.03.026
  44. Quintero-Díaz, G.E., Vázquez-Díaz, J. (2009): Historia Natural de una Rana muy Mexicana. Municipio de Aguascalientes, SHM, Biodiversidad AC, SEMARNAT, Aguascalientes.
  45. R Core Team. (2020): R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  46. Reading, C.J. (2003): The effects of variation in climatic temperature (1980–2001) on breeding activity and tadpole stage duration in the common toad, Bufo bufo. Sci. Total Environ. 310: 231-236. DOI: https://doi.org/10.1016/S0048-9697(02)00643-5
  47. Rojas-Soto, O., Baldo, D., Lescano, J., Encarnación-Luévano, A., Leynaud, G., Nori, J. (2021): Seasonal Dissociation in Fossorial Activity between the Llanos’ Frog Populations as a Survival Strategy in Arid Subtropical Environments. J. Herpetol. 55: 442-451. DOI: https://doi.org/10.1670/20-096
  48. Ruibal, R., Hillman, S. (1981); Cocoon structure and function in the burrowing hylid frog, Pternohyla fodiens. J. Herpetol. 15: 403-40. DOI: https://doi.org/10.2307/1563529
  49. Scheffers, B.R., Edwards, D.P., Diesmos, A., Williams, S.E., Evans, T.A. (2014): Microhabitats reduce animal’s exposure to climate extremes. Glob Chang Biol. 20: 495-503. DOI: https://doi.org/10.1111/gcb.12439
  50. Shcheglovitova, M., Anderson, R.P. (2013): Estimating optimal complexity for ecological niche models: A jackknife approach for species with small sample sizes. Ecol. Modell. 269: 9-17. DOI: https://doi.org/10.1016/j.ecolmodel.2013.08.011
  51. Sierra-Morales, P., Rojas-Soto, O., Ríos-Muñoz, C.A., Ochoa-Ochoa, L.M., Flores-Rodríguez, P., Almazán-Núñez, R.C. (2021): Climate change projections suggest severe decreases in the geographic ranges of bird species restricted to Mexican humid mountain forests. Glob. Ecol. Conserv. 30: e01794. DOI: https://doi.org/10.1016/j.gecco.2021.e01794
  52. Smith, M.A., Green, D.M. (2005): Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 28: 110-128. DOI: https://doi.org/10.1111/j.0906-7590.2005.04042.x
  53. Soberon, J., Peterson, A.T. (2005): Interpretation of Models of Fundamental Ecological Niches and Species’ Distributional Areas. Biodivers. Inform. 2: 1-10. DOI: https://doi.org/10.17161/bi.v2i0.4
  54. Soto-Sandoval, Y., Suazo-Ortuño, I., Urbina-Cardona, N., Marroquín-Páramo, J., Alvarado-Díaz, J. (2017): Efecto de los estadios sucesionales del bosque tropical seco sobre el microhabitat usado por Agalychnis dacnicolor (Anura: Phyllomedusidae) y Smilisca fodiens (Anura: Hylidae). Rev. Biol. Trop. 65: 777-798. DOI: https://doi.org/10.15517/rbt.v65i2.24706
  55. Sullivan, B.K., Bowker, R.W., Malmos, K.B., Gergus, E.W.A. (1996): Arizona distribution of three Sonoran Desert anurans: Bufo retiformis, Gastrophryne olivacea, and Pternohyla fodiens. Great Basin Nat. 56: 38-47. DOI: https://doi.org/10.5962/bhl.part.4107
  56. Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., Siqueira, M.F., Grainger, A., Hannah, L., Hughes, L., Huntley, B., van Jaarsveld, A.S., Midgley, G.F., Miles, L., Ortega-Huerta, M.A., Peterson, A.T., Phillips, O.L., Williams, S.E. (2004): Extinction risk from climate change. Nature 427: 145-148. DOI: https://doi.org/10.1038/nature02121
  57. Todd, B.D., Scott, D.E., Pechmann, J.H., Gibbons, J.W. (2011): Climate change correlates with rapid delays and advancements in reproductive timing in an amphibian community. Proc. Royal Soc. B. 278: 2191-2197. DOI: https://doi.org/10.1098/rspb.2010.1768
  58. van-Vuuren, D.P., den-Elzen, M.G.J., Lucas, P.L., Eickhout, B., Strengers, B.J., van Ruijven, B., Wonink, S., van Houdt, R. (2007): Stabilizing greenhouse gas concentrations at low levels: an assessment of reduction strategies and costs. Clim. Change 81: 119-159. DOI: https://doi.org/10.1007/s10584-006-9172-9
  59. Weatherhead, P.J., Sperry, J.H., Carfagno, G.L.F., Blouin-Demers, G. (2012): Latitudinal variation in thermal ecology of North American ratsnakes and its implications for the effect of climate warming on snakes. J. Therm. Biol. 37: 273-281. DOI: https://doi.org/10.1016/j.jtherbio.2011.03.008
  60. Wickham, H. (2016): ggplot2: Elegant graphics or data analysis. Springer-Verlag, New York. DOI: https://doi.org/10.1007/978-3-319-24277-4_9