Morphological differentiation of Ambystoma dumerilii populations in captivity and wildlife conditions
DOI:
https://doi.org/10.22201/ib.20078706e.2023.94.4969Keywords:
Ambystoma, Achoque, Allometric patterns, Fluctuating asymmetry, Geometric morphometrics, Habitat perturbationAbstract
Ambystoma dumerilii, known as “achoque”, is a microendemic salamander from Lake Pátzcuaro, considered as a critically endangered species according to the IUCN (2020). The main threats are high levels of water contamination, high levels of eutrophication in addition to the fact that invasive species can be found within the “achoque” habitat. For these reasons, an important conservation effort has been the maintenance of “achoque” in captivity. However, captivity is known to be a stressor derived from non-optimal conditions that can have important physiological consequences that are reflected in body conditions. Therefore, our objective was to evaluate the condition of A. dumerilii individuals through a morphological analysis using different parameters such as morphological character sizes, geometric morphometrics, fluctuating asymmetry and allometry, in individuals from Lake Pátzcuaro and captivity. We found that almost all the traits have a negative allometric relationship with the body size in individuals from both conditions. Our results showed that individuals from the lake presented greater sizes, slimmer bodies and higher levels of fluctuating asymmetry than captive individuals, all results are consistent in the context of performance with greater potential adaptations to increase swimming performance than individuals from captivity.
References
Adams, D. C. (2000). Divergence of trophic morphology and resource use among populations of Plethodon cinereus and P. hoffmani in Pennsylvania - a possible case of character displacement. In R. C. Bruce, R. G. Jaeger, & L. D. Houck (Eds.), Biology of plethodontid salamanders (pp. 383–395). Boston, MA: Springer Science. https://doi.org/10.1007/978-1-4615-4255-1_19
Adams, D. C. (2004). Character displacement via aggressive interference in Appalachian salamanders. Ecology, 85, 2664–2670. https://doi.org/10.1890/04-0648
Adams, D. C., & Rohlf, F. J. (2000). Ecological character displacement in Plethodon: biomechanical differences found from a geometric morphometric study. Proceedings of the National Academy of Sciences, 97, 4106–4111. https://doi.org/10.1073/pnas.97.8.4106
Aguilar-Miguel, X. (2005). Ambystoma dumerilii. Algunas especies de anfibios y reptiles contenidos en el Proyecto de Norma Oficial Mexicana PROY-NOM-059-ECOL-2000. Facultad de Ciencias, Centro de Investigación en Recursos Bióticos, Universidad Autónoma del Estado de México. Bases de datos SNIBCONABIO. Proyecto W035. México. D.F. Disponible en: http://www.conabio.gob.mx/conocimiento/ise/fichasnom/Ambystomadumerilii00.pdf
Aguilar-Miguel, X., & Casas Andreu, G. (2005). Ficha técnica de Ambystoma dumerilii. In Aguilar-Miguel, X. Algunas especies de anfibios y reptiles contenidos en el Proyecto de Norma Oficial Mexicana PROY-NOM-059-ECOL-2000. Facultad de Ciencias, Centro de Investigación en Recursos Bióticos, Universidad Autónoma del Estado de México. Bases de datos SNIB-CONABIO. Proyecto No. W035. México, D.F. Retrieved on November 28th, 2021 from: https://www.naturalista.mx/taxa/26782-Ambystoma-dumerilii
Alarcón‐Ríos, L., Velo‐Antón, G., & Kaliontzopoulou, A. (2017). A non‐invasive geometric morphometrics method for exploring variation in dorsal head shape in urodeles: sexual dimorphism and geographic variation in Salamandra salamandra. Journal of Morphology, 278, 475–485. https://doi.org/10.1002/jmor.20643
Altwegg, R., & Reyer, H. U. (2003). Patterns of natural selection on size at metamorphosis in water frogs. Evolution, 57, 872–882. https://doi.org//10.1111/j.0014-3820.2003.tb00298.x
Álvarez, D., & Nicieza, A. G. (2002). Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion. Oecologia, 131, 186–195. https://doi.org//10.1007/s00442-002-0876-x
Anderson, J. D., & Worthington, R. D. (1971). The life history of the Mexican salamander Ambystoma ordinarium Taylor. Herpetologica, 27, 165–176.
Assis, V. R., Titon, S. C. M., Barsotti, A. M. G., Titon, B. Jr., & Gomes, F. R. (2015). Effects of acute restraint stress, prolonged captivity stress and transdermal corticosterone application on immunocompetence and plasma levels of corticosterone on the cururu toad (Rhinella icterica). Plos One, 10, e0121005. https://doi.org/10.1371/journal.pone.0121005
Aubret, F., & R. Shine. (2008). The origin of evolutionary innovations: locomotor consequences of tail shape in aquatic snakes. Functional Ecology, 22, 312–322. https://doi.org/10.1111/j.1365-2435.2007.01359.x
Azizi, E., & Horton, J. M. (2004). Pattern of axial and appendicular movements during aquatic walking in the salamander Siren lacertina. Zoology, 107, 111–120. https://doi.org/10.1016/j.zool.2004.03.002
Bookstein, F. L. (1997). Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Medical Image Analysis, 1, 225–243. https://doi.org/10.1016/S1361-8415(97)85012-8
Brunson, K. L., Avishai-Eliner, S., Hatalski, C. G., & Baram, T. Z. (2001). Neurobiology of the stress response early in life: evolution of a concept and the role of corticotropin releasing hormone. Molecular Psychiatry, 6, 647–656. https://doi.org/10.1038/sj.mp.4000942
Calisi, R. M., & Bentley, G. E. (2009). Lab and field experiments: are they the same animal? Hormones and Behavior, 56, 1–10. https://doi.org/10.1016/j.yhbeh.2009.02.010
Casas-Andreu, G., Cruz-Aviña, R., & Aguilar-Miguel, X. (2004). Un regalo poco conocido de México al mundo: el ajolote o axolotl (Ambystoma: Caudata: Amphibia). Con algunas notas sobre la crítica situación de sus poblaciones. Ciencia Ergo Sum, 10, 304–308.
Cayuela, H., Quay, L., Dumet, A., Léna, J. P., Miaud, C., & Rivière, V. (2017). Intensive vehicle traffic impacts morphology and endocrine stress response in a threatened amphibian. Oryx, 51, 182–188. https://doi.org/10.1017/S0030605315000812
Cuevas-Reyes, P., Canché-Delgado, A., Maldonado-López, Y., Fernandes, G. W., Oyama, K., & González-Rodríguez, A. (2018). Patterns of herbivory and leaf morphology in two Mexican hybrid oak complexes: importance of fluctuating asymmetry as indicator of environmental stress in hybrid plants. Ecological Indicators, 90, 164–170. https://doi.org/10.1016/j.ecolind.2018.03.009
Davis, A. K., & Maerz, J. C. (2010). Effects of exogenous corticosterone on circulating leukocytes of a salamander (Ambystoma talpoideum) with unusually abundant eosinophils. International Journal of Zoology, 2010, 735937. https://doi.org/10.1371/journal.pone.0163736
Davis, A. K., & Maerz, J. C. (2011). Assessing stress levels of captive-reared amphibians with hematological data: implications for conservation. Initiatives Journal of Herpetology, 45, 40–44. https://doi.org/10.1670/10-180.1
Davis, A. K., & Maney, D. L. (2018). The use of glucocorticoid hormones or leucocyte profiles to measure stress in vertebrates: What's the difference? Methods in Ecology and Evolution, 9, 1556–1568. https://doi.org/10.1111/2041-210X.13020
Davis, D. R., Ferguson, K. J., Schwarz, M. S., & Kerby, J. L. (2020). Effects of agricultural pollutants on stress hormones and viral infection in larval salamanders. Wetlands, 40, 577–586. https://doi.org/10.1007/s13157-019-01207-1
de Vosjoli, P. (1999). Designing environments for captive amphibians and reptiles. Veterinary clinics of North America: Exotic Animal Practice, 2, 43–68.
Deban, S. M., & Schilling, N. (2009). Activity of trunk muscles during aquatic and terrestrial locomotion in Ambystoma maculatum. Journal of Experimental Biology, 212, 2949–2959. https://doi.org/10.1242/jeb.032961
Delgado-Acevedo, J., & Restrepo, C. (2008). The contribution of habitat loss to changes in body size, allometry, and bilateral asymmetry in two Eleutherodactylus frogs from Puerto Rico. Conservation Biology, 22, 773–782. https://doi.org/10.1111/j.1523-1739.2008.00930.x
Denver, R. J. (1997). Environmental stress as a developmental cue: corticotropin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis. Hormones and Behavior, 31, 169–179. https://doi.org/10.1006/hbeh.1997.1383
Denver, R. J. (2009). Stress hormones mediate environment-genotype interactions during amphibian development. General and Comparative Endocrinology, 164, 20–31. https://doi.org/10.1016/j.ygcen.2009.04.016
Denver, R. J., Mirhadi, N., & Phillips, M. (1998). Adaptive plasticity in amphibian metamorphosis: response of Scaphiopus hammondii tadpoles to habitat desiccation. Ecology, 79, 1859–1872. https://doi.org/10.2307/176694
Des Roches, S., Post, D. M., Turley, N. E., Bailey, J. K., Hendry, A. P., Kinnison, M. T. et al. (2018). The ecological importance of intraspecific variation. Nature Ecology & Evolution, 2, 57–64. https://doi.org/10.1038/s41559-017-0402-5
Duellman, W. E., & Trueb, L. (1986). Biology of amphibians. McGraw-Hill Book Co., New York. https://doi.org/10.2307/1445022
Duellman, W. E., & Trueb, L. (1994). Biology of amphibians. The Johns Hopkins University Press, Baltimore.
Essner, Jr., R. L., & Suffian, D. J. (2010). Captive husbandry in the Rocky Mountain Tailed Frog, Ascaphus montanus. Herpetological Review, 41, 181–184. https://doi.org/10.1126/sciadv.abn1104
Fairbairn, D. J. (1997). Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics, 28, 659–687. https://doi.org/10.1146/annurev.ecolsys.28.1.659
Fitzpatrick, B. M., Benard, M. F., & Fordyce, J. A. (2003). Morphology and escape performance of tiger salamander larvae (Ambystoma tigrinum mavortium). Journal of Experimental Zoology, 297A, 147–159. https://doi.org/10.1002/JEZ.A.10254
Fox, G. A., Cooper, A. M., & Hayes, W. K. (2015). The dilemma of choosing a reference character for measuring sexual size dimorphism, sexual body component dimorphism, and character scaling: cryptic dimorphism and allometry in the scorpion Hadrurus arizonensis. Plos One, 10, e0120392. https://doi.org/10.1371/journal.pone.0120392
Frolich, L. M., & Biewener, A. A. (1992). Analysis of the functional role of the body axis during terrestrial and aquatic locomotion in the salamander Ambystoma tigrinum. Journal of Experimental Biology, 162, 107–130. https://doi.org/10.1242/jeb.162.1.107
Gangenova, E., Giombini, M. I., Zurita, G. A., & Marangoni, F. (2020). Morphological responses of three persistent native anuran species after forest conversion into monoculture pine plantations: tolerance or prosperity? Integrative Zoology, 15, 428–440. https://doi.org/10.1111/1749-4877.12440
Gray, M. J., & L. M. Smith. (2005). Influence of land use on postmetamorphic body size of playa lake amphibians. Journal of Wildlife Management, 69, 515–524.
Hoff, K., Huq, N., King, V. A., & Wassersug, R. J. (1989). The kinematics of larval salamander swimming. Canadian Journal of Zoology, 67, 2756–2761. https://doi.org/10.1139/z89-391
Hu, F., Crespi, E. J., & Denver, R. J. (2008). Programming neuroendocrine stress axis activity by exposure to glucocorticoids during postembryonic development of the frog Xenopus laevis. Endocrinology, 149, 5470–5481. https://doi.org/10.1210/en.2008-0767
Huacuz-Elías, D. C. (2002). Programa de conservación y manejo de Ambystoma dumerilii: el A. dumerilii del Lago de Pátzcuaro. Morelia, Mich: UMSNH.
Huacuz-Elías, D. C. (2008). Biología y conservación del género Ambystoma en Michoacán, México (Ph.D. Thesis). Universidad de Salamanca, Salamanca, España.
Huerto-Delgadillo, R. I., Vargas-Velázquez, S., & Ortiz-Paniagua, C. F. (2011). Estudio ecosistémico del lago de Pátzcuaro: aportes en gestión ambiental para el fomento del desarrollo sustentable. Jiutepec, Morelos: Instituto Mexicano de Tecnología del Agua.
Iglesias-Carrasco, M., Martín, J., & Cabido, C. (2017). Urban habitats can affect body size and body condition but not immune response in amphibians. Urban Ecosystems, 20, 1331–1338. https://doi.org/10.1007/s11252-017-0685-y
Ijspeert, A. J., & Cabelguen, J. M. (2006). Gait transition from swimming to walking: investigation of salamander locomotion control using nonlinear oscillators. In H. Kimura, K. Tsuchiya, A. Ishiguro, & H. Witte (Eds.), Adaptive motion of animals and machines (pp. 177–188). Tokio, Japan: Springer. https://doi.org/10.1007/4-431-31381-8_16
Irschick, D. J., & Garland, T. J. (2001). Integrating function and ecology in studies of adaptation: investigations of locomotor capacity as a model system. Annual Review of Ecology and Systematics, 32, 367–396. https://doi.org/10.1146/annurev.ecolsys.32.081501.114048
IUCN (International Union for Conservation of Nature) SSC (Species Survival Commission) Amphibian Specialist Group. (2020). Ambystoma dumerilii. The IUCN Red List of Threatened Species: e.T59055A53973725. Retrieved on November 28th 2020, from: https://dx.doi.org/10.2305/IUCN.UK.2020-1.RLTS.T59055A53973725.en.
Jessop, T. M., Madsen, T., Sumner, J., Rudiharto, H., Phillips, J. A., & Ciofi, C. (2006). Maximum body Size among insular Komodo dragon populations covaries with large prey density. Oikos, 112, 422–429. https://doi.org/10.1111/j.0030-1299.2006.14371.x
Johansson, F., Lederer, B., & Lind, M. I. (2010). Trait performance correlations across life stages under environmental stress conditions in the common frog, Rana temporaria. Plos One, 5, e11680. https://doi.org/10.1371/journal.pone.0011680
Klingenberg, C. P. (2003). Developmental instability as a research tool: using patterns of fluctuating asymmetry to infer the developmental origins of morphological integration. In M. Polak (Ed.), Developmental instability: causes and consequences (pp.427–442). New York: Oxford University Press.
Klingenberg, C. P. (2011). MorphoJ: an integrated software pack-age for geometric morphometrics. Molecular Ecology Resources, 11, 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
Lempa, K., Martel, J., Koricheva, J., Haukioja, K., Ossipov, V., Ossipova, S. et al. (2000). Covariation of fluctuating asymmetry, herbivory and chemistry during birch leaf expansion. Oecologia, 122, 354–360. https://doi.org/10.1007/s004420050041
Lens, L., von Dongen, S., & Matthysen, E. (2002). Fluctuating asymmetry as an early warning system in the critically endangered Taita Thrush. Conservation Biology, 16, 479–487. https://doi.org/10.1046/j.1523-1739.2002.00516.x
Lleonart, J., Salat, J., & Torres, G. J. (2000). Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology, 205, 85–93. https://doi.org/10.1006/jtbi.2000.2043
Lomolino, M. V., Channell, R., Perault, D. R., & Smith, G. A. (2001). Down- sizing nature: anthropogenic dwarfing of species and ecosystems. In J. L. Lockwood, & M. L. McKinney (Eds.), Biotic homogenization (pp. 223–243). New York: Kluwer Academic/ Plenum. https://doi.org/10.1007/978-1-4615-1261-5_11
Lowe, W. H., Likens, G. E., & Cosentino, B. J. (2006). Self-organization in streams: the relationship between movement behaviour and body condition in a headwater salamander. Freshwater Biology, 51, 2052–2062. https://doi.org/10.1111/j.1365-2427.2006.01635.x
Martel, J., Lempa, K., & Haukioja, E. (1999). Effect of stress and rapid growth on fluctuating asymmetry and insect damage in birch leaves. Oikos, 86, 208–216. https://doi.org/10.2307/3546439
Matthews, S. G. (2002). Early programming of the hypothalamo–pituitary–adrenal axis. Trends in Endocrinology and Metabolism, 13, 373–380. https://doi.org/10.1016/s1043-2760(02)00690-2
Michaels, C. J., Gini, B., & Preziosi, R. F. (2014). The importance of natural history and species-specific approaches in amphibian ex-situ conservation. The Herpetological Journal, 24, 135–145.
Milligan, J. R., Krebs, R. A., & Mal, T. K. (2008). Separating developmental and environmental effects on fluctuating asymmetry in Lythrum salicaria and Penthorum sedoides. International Journal of Plant Sciences, 169, 625–630. https://doi.org/10.1086/533600
Møller, P. A., & Manning, J. (2003). Growth and developmental instability. The Veterinary Journal, 166, 19–27. https://doi.org/10.1016/s1090-0233(02)00262-9
Montes-Calderón, M. A., Alvarado-Díaz, J., & Suazo-Ortuño, I. (2011). Abundancia, actividad espacial y crecimiento de Ambystoma ordinarium Taylor 1940 (Caudata: Ambysto-matidae) en Michoacán, México. Biológicas, 13, 50–53.
Morrison, C., Hero, J. M., & Browning, J. (2004). Altitudinal variation in the age at maturity, longevity, and reproductive lifespan of anuran in subtropical Queensland. Herpetologica, 60, 34–44. https://doi.org/10.1655/02-68
Murta-Fonseca, R. A., Folly, M., Carmo, L. F., & Martins, A. (2020). Growing towards disparity: geometric morphometrics reveals sexual and allometric differences in Aparasphenodon brunoi (Anura: Hylidae: Lophyohylinae) head shape. Cuadernos de Herpetología, 34, 1–11. https://doi.org/10.31017/CdH.2020.(2019-032)
Ortega, A. J. (1999). El ajolote. Elementos: Ciencia y Cultura, 036, 55-57.
Palmer, A. R., & Strobeck, C. (1986). Fluctuating asymmetry: measurement, analysis, patterns. Annual Review of Ecology Systematics, 17, 391–421. https://doi.org/10.1146/ANNUREV.ES.17.110186.002135
Phillips, B. L., Brown, G. P., Webb, J. K., & Shine, R. (2006). Invasion and the evolution of speed in toads. Nature, 439, 803. https://doi.org/10.1038/439803a
Ramírez-Hernández, G., Suazo-Ortuño, I., Alvarado-Díaz, J., Escalera-Vázquez, L. H., Maldonado-López, Y., & Tafolla-Venegas, D. (2019). Effects of habitat disturbance on parasite infection and stress of the endangered Mexican stream salamander Ambystoma ordinarium. Salamandra, 55, 160–172.
Ramírez-Herrejón, J. P., Zambrano, L., Mercado-Silva, N., Torres-Téllez, A., Pineda-García, F., Caraveo-Patiño, J. et al. (2014). Long term changes in the fish fauna of Lago de Pátzcuaro in Central México. Latin American Journal of Aquatic Research, 42, 137–149. https://doi.org/10.3856/vol42-issue1-fulltext-11
Relyea, R. A. (2001). Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology, 82, 523–540. https://doi.org/10.2307/2679877
Relyea, R. A., & Hoverman, J. T. (2003). The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs. Oecologia, 134, 596–604. https://doi.org/10.1007/s00442-002-1161-8
Riva-Tonini, J. F., Provete, D. B., Maciel, N. M., Morais, A. R., Goutte, S., Toledo, L. F. et al. (2020). Allometric escape from acoustic constraints is rare for frog calls. Ecology and Evolution, 10, 3686–3695. https://doi.org/10.1002/ece3.6155
Rohlf, F. J. (2015). The tps series of software. Hystrix the Italian Journal of Mammalogy, 26, 9–12. https://doi.org/10.4404/hystrix-26.1-11264
Semarnat (Secretaría del Medio Ambiente y Recursos Naturales). (2010). Norma Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental - Especies nativas de México de flora y fauna silvestres - Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio - Lista de especies en riesgo. Diario Oficial de la Federación. 30 de diciembre de 2010, Segunda Sección, México.
Semarnat (Secretaría de Medio Ambiente y Recursos Naturales) (2018). Programa de Acción para la Conservación de las Especies Ambystoma spp. Ciudad de México: Semarnat/ Conanp.
Shaffer, H. B. (1984). Evolution in a paedomorphic lineage. II. Allometry and form in the Mexican ambystomatid salamanders. Evolution, 38, 1207–1218. https://doi.org/10.2307/2408629
Shaffery, H. M., & Relyea, R. A. (2015). Predator-induced defenses in five species of larval Ambystoma. Copeia, 103, 552–562. https://doi.org/10.1643/CE-14-043
Shi, Y., Puzianowska-Kuznicka, M., & Stolow, M. A. (1996). Tadpole competence and tissue-specific temporal regulation of amphibian metamorphosis: roles of thryoid hormone and its receptors. Bioessays, 18, 391–399. https://doi.org/10.1002/bies.950180509
Sibly, R., & Calow, P. (1984). Direct and absorption costing in the evolution of life cycles. Journal of Theoretical Biology, 111, 463–473. https://doi.org/10.1016/S0022-5193(84)80234-9
Slight, D. J., Nichols, H. J., & Arbuckle, K. (2015). Are mixed diets beneficial for the welfare of captive axolotls (Ambystoma mexicanum)? Effects of feeding regimes on growth and behavior. Journal of Veterinary Behavior, 10, 185–190. https://doi.org/10.1016/j.jveb.2014.09.004
Soto-Rojas, C., Suazo-Ortuño, I., Montoya-Laos, J. A., & Alvarado-Díaz, J. (2017). Habitat quality affects the incidence of morphological abnormalities in the endangered salamander Ambystoma ordinarium. Plos One, 12, e0183573. https://doi.org/10.1371/journal.pone.0183573
Steinicke, H., Gruber, B., Grimm, A., Grosse, W. R., & Henle, K. (2015). Morphological shifts in populations of generalist and specialist amphibians in response to fragmentation of the Brazilian Atlantic forests. Nature Conservation, 13, 47–59. https://doi.org/10.3897/natureconservation.13.7428
Stoler, A. B., & Relyea, R. A. (2013). Leaf litter quality induces morphological and developmental changes in larval amphibians. Ecology, 94, 1594–1603. https://doi.org/10.1890/12-2087.1
Tejedo, M., Marangoni, F., Pertoldi, C., Richter‐Boix, A., Laurila, A., Orizaola, G. et al. (2010). Contrasting effects of environmental factors during larval stage on morphological plasticity in post-metamorphic frogs. Climate Research, 43, 31–39. https://doi.org/10.3354/cr00878
Titon, S. C. M., Assis, V. R., Titon, Jr. B., Cassettari, B. O., Fernandes, P. A. C. M., & Gomes, F. R. (2017). Captivity effects on immune response and steroid plasma levels of a Brazilian toad (Rhinella schneideri). Journal of Experimental Zoology A, 327, 127–138. https://doi.org/10.1002/jez.2078
Tomasini-Ortiz, C., Bravo-Inclán, L., Sánchez-Chávez, J., & Moeller-Chávez, G. (2016). Monitoreo de descargas de aguas residuales y su impacto en el lago de Pátzcuaro, México (2006-2011). Revista AIDIS de Ingeniería y Ciencias Ambientales: Investigación, Desarrollo y Práctica, 9, 61–74. Retrieved from https://revistas.unam.mx/index.php/aidis/article/view/50113
Urban, M. C. (2010). Microgeographic adaptations of spotted salamander morphological defenses in response to a predaceous salamander and beetle. Oikos, 119, 646–658. https://doi.org/10.1111/j.1600-0706.2009.17970.x
Van Buskirk, J. (2011). Amphibian phenotypic variation along a gradient in canopy cover: species differences and plasticity. Oikos, 120, 906–914. https://doi.org/10.1111/j.1600-0706.2010.18845.x
Van Buskirk, J., & McCollum, S. A. (2000). Functional mechanisms of an inducible defence in tadpoles: morphology and behaviour influence mortality risk from predation. Journal of Evolutionary Biology, 13, 336–347. https://doi.org/10.1046/j.1420-9101.2000.00173.x
Van Buskirk, J., & Schmidt, B. R. (2000). Predator-induced phenotypic plasticity in larval newts: trade-offs, selection, and variation in nature. Ecology, 81, 3009–3028. https://doi.org/10.2307/177397
Vega-Trejo, R., Zúñiga-Vega, J. J., & Langerhans, R. B. (2014). Morphological differentiation among populations of Rhinella marina (Amphibia: Anura) in western Mexico. Evolutionary Ecology, 28, 69–88. https://doi.org/10.1007/s10682-013-9667-6
Velarde-Mendoza, T. (2012). Importancia ecológica y cultural de una especie endémica de ajolote (Ambystoma dumerilii) del lago de Pátzcuaro, Michoacán. Etnobiología, 10, 40–49.
Velickovic, M., & Perisic, S. (2006). Leaf fluctuating asymmetry of common plantain as an indicator of habitat quality. Plant Biosystems, 140, 138–145. https://doi.org/10.1080/11263500600756322
Vorndran, I. C., Reichwaldt, E., & Nürnberger, B. (2002). Does differential susceptibility to predation in tadpoles stabilize the Bombina hybrid zone? Ecology, 83, 1648–1659. https://doi.org/10.2307/3071985
Wright, A. N., & Zamudio, K. R. (2002). Color pattern asymmetry as a correlate of habitat disturbance in spotted salamanders (Ambystoma maculatum). Journal of Herpetology, 36, 129–133. https://doi.org/10.1670/0022-1511(2002)036[0129:CPAAAC]2.0.CO;2
Wu, Z., Li, Y., & Murray, B. R. (2006). Insular shifts in body size of rice frogs in the Zhoushan archipelago, China. Journal of Animal Ecology, 75, 1071–1080. https://doi.org/10.1111/j.1365-2656.2006.01126.x
Zambrano, L., Cordoval-Tapia, F., Ramírez-Herrejón, J. P., Mar-Silva, V., Bustamante, L., Camargo, T. et al. (2011). Las especies exóticas en el lago de Pátzcuaro, Michoacán, México. In R. Huerto-Delgadillo, S. Vargas-Velázquez, & C. Ortiz-Paniagua, (Eds.). Estudio ecosistémico del lago de Pátzcuaro. Jiutepec, Morelos: Instituto Mexicano de Tecnología del Agua. https://doi.org/10.13140/RG.2.1.3619.0242
Zhelev, Z. M., Popgeorgiev, G. S., & Georgieva, Z. K. (2014). Fluctuating asymmetry in the populations of Pelophylax ridibundus and Pseudepidalea viridis (Amphibia: Anura) in the region of the lead and zinc plant “Kardzhali” (South Bulgaria). Acta Zoologica Bulgarica, 66, 83–87.
Zhelev, Z. M., Popgeorgiev, G. S., Arnaudov, A. D., Georgieva, K. N., & Mehterov, N. H. (2015). Fluctuating asymmetry in Pelophylax ridibundus (Amphibia: Ranidae) as a response to anthropogenic pollution in south Bulgaria. Archives of Biological Sciences, 67, 1009–1023. https://doi.org/10.2298/ABS141210064Z
Zhelev, Z. M., Tsonev, S. V., & Angelov, M. V. (2019). Fluctuating asymmetry in Pelophylax ridibundus meristic morphological traits and their importance in assessing environmental health. Ecological Indicators, 107, 105589. https://doi.org/10.1016/j.ecolind.2019.105589
