Skip to main content

Advertisement

SpringerLink
Log in

Response of a native endangered axolotl, Ambystoma mexicanum (Amphibia), to exotic fish predator

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The axolotl (Ambystoma mexicanum) is a critically endangered and threatened species endemic of the Central Valley of Mexico. The population of this neotenic amphibian has declined in recent years as a result of habitat destruction, polluted waters, and the introduction of exotic species such as tilapia. We evaluated the antipredator response of predator-naïve axolotls to visual and chemical cues of the Nile tilapia (Oreochromis niloticus) and its foraging consequences. Axolotls decreased their activity and increased their use of refuge in the presence of combined chemical and visual cues from the predator. The axolotls seem to use their vision to confirm the level of risk perceived through chemical signals to modulate their antipredator response accordingly. The axolotls engaged in prey capture at a similar rate independent of the type of predator exposure. However, the efficiency of prey capture decreased in axolotls exposed to the chemical and the combined visual and chemical cues from the tilapia. The foraging costs to the axolotls induced by tilapia can ultimately affect their growth rate and size. The axolotls display antipredator behaviours to reduce the risk of predation by tilapia, which is a primary condition of coexistence with this exotic predator.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Álvarez del Villar, J. & L. Navarro, 1957. Los peces del Valle de México. Secretaría de Marina. Instituto Nacional de la Pesca e Industrias Conexas: 3–22.

  • Amo, L., P. López & J. Martín, 2004. Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges. Animal Behaviour 67: 647–653.

    Article  Google Scholar 

  • Anver, M. R. & C. L. Pond, 1984. Biology and diseases of amphibians. In Fox, J. G., B. J. Cohen & F. M. Loew (eds), Laboratory Animal Medicine. Academic Press, New York: 427–447.

    Chapter  Google Scholar 

  • Armstrong, J. B., S. T. Duhon & G. M. Malacinski, 1989. Raising the axolotl in captivity. In Armstrong, J. B. & G. M. Malacinsky (eds), Developmental Biology of the Axolotl. Oxford University Press, New York: 220–227.

    Google Scholar 

  • Blancas-Arroyo, A. G., G. Figueroa-Lucero, I. A. Barriga-Sosa & J. L. Arredondo, 2003. Aportaciones al cultivo controlado del pez blanco, Chirostoma humboldtianum, Valenciennes 1835 (Pisces: Atherinopsidae). In Rojas, C. P. M. & C. D. Fuentes (eds), Historia y Avances del Cultivo de Pescado blanco. Instituto Nacional de la Pesca, SAGARPA, México, D.F. [available on internet at http://www.inapesca.gob.mx/portal/documentos/publicaciones/LIBROS/pescado_blanco.pdf].

  • Chivers, D. P., J. M. Kiesecker, M. T. Anderson, E. L. Wildy & A. R. Blaustein, 1996. Avoidance response of terrestrial salamander (Ambystoma macrodactylum) to chemical alarm cues. Journal of Chemical Ecology 22: 1709–1716.

    Article  CAS  PubMed  Google Scholar 

  • Chivers, D. P. & R. J. F. Smith, 1998. Chemical alarm signalling in aquatic predator/prey systems: a review and prospectus. Ecoscience 5: 338–352.

    Google Scholar 

  • Contreras, V., E. Martínez-Meyer, E. Valiente & L. Zambrano, 2009. Recent decline and potential distribution in the last remnant area of the microendemic Mexican axolotl (Ambystoma mexicanum). Biological Conservation 142: 2881–2885.

    Article  Google Scholar 

  • DOF-Diario Oficial de la Federación, 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, México.

  • Eisthen, H. L. & D. Park, 2005. Chemical signals and vomeronasal system function in axolotl (Ambystoma mexicanum). In Mason, R., M. LeMaster & D. Müller-Schwarze (eds), Chemical Signals in Vertebrates. Springer, New York: 216–227.

    Chapter  Google Scholar 

  • Ferrari, M. C. O., A. Gonzalo, F. Messier & D. P. Chivers, 2007. Generalization of learned predator recognition: an experimental test and framework for future studies. Proceedings of the Royal Society, Biological Sciences 274:1853–1859.

  • Fessehaye, Y., A. Kabir, H. Bovenhuis & H. Komen, 2006. Prediction of cannibalism in juvenile Oreochromis niloticus based on predator to prey weight ratio, and effects of age and stocking density. Aquaculture 255: 314–322.

    Article  Google Scholar 

  • Fitzpatrick, B. M., M. F. Benard & J. A. Fordyce, 2003. Morphology and escape performance of tiger salamander larvae (Ambystoma tigrinum mavortium). Journal of Experimental Zoology 2797A: 147–159.

    Article  Google Scholar 

  • Fitzsimmons, K., 2000. Tilapia aquaculture in Mexico. In Costa-Pierce, B. A. & J. E. Rakocy (eds), Tilapia Aquaculture in the Americas, Vol. 2. The World Aquaculture Society, Baton Rouge: 171–183.

    Google Scholar 

  • Fortes, R. S., F. J. Martínez, M. Villarroel & F. J. Sánchez-Vázquez, 2010. Daily feeding patterns and self-selection of dietary oil in Nile tilapia. Aquaculture Research 42: 157–160.

    Article  Google Scholar 

  • Ghirlanda, S. & M. Enquist, 2003. A century of generalisation. Animal Behavior 66: 15–36.

  • Gonzálo, A., P. López & J. Martín, 2007. Iberian green frog tadpoles may learn to recognize novel predators from chemical alarm cues of conspecifics. Animal Behavior 74: 447–453.

    Article  Google Scholar 

  • Graue, W. V., 1998. Estudio genético y demográfico de la población del anfibio Ambystoma mexicanum (Caudata: Ambystomidae) del Lago de Xochimilco. Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, México.

    Google Scholar 

  • Hartman, E. J. & M. V. Abrahams, 2000. Sensory compensation and the detection of predators: the interaction between chemical and visual information. Proceedings of the Royal Society, Biological Sciences 267: 571–575.

    Article  CAS  Google Scholar 

  • Hickman, C. R., M. D. Stone & A. Mathis, 2004. Priority use of chemical over visual cues for detection of predators by graybelly salamanders Eurycea multiplicata griseogaster. Herpetologica 60: 203–210.

    Article  Google Scholar 

  • IUCN, 2014. The IUCN Red List of Threatened Species [available on internet at http://www.iucnredlist.org].

  • Jara, F. & M. Perotti, 2010. Risk of predation and behavioural response in three anuran species: influence of tadpole size and predator type. Hydrobiologia 644: 313–324.

    Article  Google Scholar 

  • Johnson, E., P. Bierzychudek & H. Whiteman, 2003. Potential of prey size and type to affect foraging asymmetries in tiger salamander (Ambystoma tigrinum nebulosum) larvae. Canadian Journal of Zoology 81: 1726–1735.

    Article  Google Scholar 

  • Kats, L. B. & L. M. Dill, 1998. The scent of death: chemo-sensory assessment of predation risk by prey animals. Ecoscience 5: 361–394.

    Google Scholar 

  • Kats, L. B. & R. P. Ferrer, 2003. Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Diversity and Distribution 9: 99–110.

    Article  Google Scholar 

  • Kelley, J. L. & A. E. Magurran, 2003. Learned predator recognition and antipredator responses in fishes. Fish and Fisheries 4: 216–226.

    Article  Google Scholar 

  • Kerby, J. L., A. J. Hart & A. Storfer, 2011. Combined effect of virus, pesticide, and predator cue on the larval tiger salamander (Ambystoma tigrinum). EcoHealth 8: 46–54.

    Article  PubMed  Google Scholar 

  • Kiesecker, J. M., 2003. Invasive species as a global problem: towards understanding the worldwide decline of amphibians. In Semlitsh, R. D. (ed), Amphibian Conservation. Smithsonian Press, Washington, DC: 113–126.

    Google Scholar 

  • Knapp, R. A. & K. R. Matthews, 2000. Non-native fish introductions and the decline of the mountain yellow-legged frog from within protected areas. Conservation Biology 14: 428–438.

    Article  Google Scholar 

  • Landberg, T. & E. Azizi, 2010. Ontogeny of escape swimming performance in the spotted salamander. Functional Ecology 24: 576–587.

    Article  Google Scholar 

  • Lindquist, S. B. & M. D. Bachmann, 1982. The role of visual and olfactory cues in the prey catching behavior of the tiger salamander, Ambystoma tigrinum. Copeia 1982: 81–90.

  • Mathis, A. & F. Vincent, 2000. Differential use of visual and chemical cues in predator recognition and threat-sensitive predator-avoidance responses by larval newts (Notophthalmus viridescens). Canadian Journal of Zoology 78: 1646–1652.

    Article  CAS  Google Scholar 

  • Milinski, M. & Y. R. Heller, 1978. Influence of a predator on the optimal foraging of sticklebacks (Gasterosteus aculeatus L.). Nature 273: 642–644.

    Article  Google Scholar 

  • Mundy, B., 1997. Simple brine shrimp hatchery. In Duhon, S. T. (ed), Compendium of Axolotl Husbandry Methods. Axolotl Newsletter 25. Indiana University Axolotl Colony, Bloomington.

    Google Scholar 

  • Münz, H. & B. Claas, 1991. Activity of lateral line efferent in the axolotl Ambystoma mexicanum. Journal of Comparative Physiology 169: 461–469.

    Google Scholar 

  • Njiru, M., J. Okeyo-Owuor, J. Muchiri & G. Cowx, 2004. Shifts in the food of Nile tilapia, Oreochromis niloticus (L.) in Lake Victoria, Kenya. African Journal of Ecology 42: 163–170.

    Article  Google Scholar 

  • Nunes, A. L., G. Orizaola, A. Laurila & R. Rebelo, 2014. Rapid evolution of constitutive and inducible defenses against an invasive predator. Ecology 95: 1520–1530.

    Article  PubMed  Google Scholar 

  • Pearson, K. J. & C. P. Goater, 2009. Effects of predaceous and nonpredaceous introduced fish on the survival, growth, and antipredation behaviours of long-toed salamanders. Canadian Journal of Zoology 87: 948–955.

    Article  Google Scholar 

  • Pease, K. M., 2011. Rapid evolution of anti-predator defenses in Pacific tree frog tadpoles exposed to invasive predatory crayfish. Doctoral dissertation. University of California, Los Angeles.

  • Pilliod, D. S., R. S. Arkle & B. A. Maxel, 2013. Persistence and extirpation in invaded landscapes: patch characteristics and connectivity determine effects of non-native predatory fish on native salamanders. Biological Invasions 15: 671–685.

    Article  Google Scholar 

  • Richardson, J. L., 2001. A comparative study of activity levels in larval anurans and response to the presence of different predators. Behavioral Ecology 12: 51–58.

    Article  Google Scholar 

  • Robles, M. M. B., 2011. Ritmo circadiano de actividad locomotriz en el ajolote mexicano juvenil Ambystoma mexicanum: sincronización y libre curso. Thesis, Facultad de Ciencias, Universidad Nacional Autónoma de México.

  • Robles-Mendoza, C., C. E. Basilio & R. C. P. Vanegas, 2009. Maintenance media for the axolotl Ambystoma mexicanum juveniles (Amphibia: Caudata). Hidrobiológica 19: 205–210.

    Google Scholar 

  • Secor, S. M. & M. Boehm, 2006. Specific dynamic action of ambystomatid salamanders and the effects of meal size, meal type, and body temperature. Physiological and Biochemical Zoology 79: 720–735.

    Article  PubMed  Google Scholar 

  • Semlitsch, R. D., 1987. Interactions between fish and salamander larvae. Cost of predator avoidance or competition? Oecologia 72: 481–486.

    Article  Google Scholar 

  • Sih, A., D. I. Bolnick, B. Luttbeg, J. L. Orrock, S. D. Peacor, L. M. Pintor, E. Preisser, J. S. Rehage & J. R. Vonesh, 2010. Predator-prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119: 610–621.

    Article  Google Scholar 

  • Skelly, D. K., 1992. Field evidence for a cost of behavioural antipredator response in a larval amphibian. Ecology 73: 704–708.

    Article  Google Scholar 

  • Skelly, D. K., 1994. Activity level and the susceptibility of anuran larvae to predation. Animal Behaviour 47: 465–468.

    Article  Google Scholar 

  • Stauffer, H. P. & R. D. Semlitsch, 1993. Effects of visual, chemical and tactile cues of fish on the behavioural responses of tadpoles. Animal Behaviour 46: 355–364.

    Article  Google Scholar 

  • Trujillo-Jiménez, P. & E. V. Espinosa de los Monteros, 2006. La ecología alimentaria del pez endémico Girardinichthys multiradiatus (Cyprinidontiformes: Goodeidae) en el Parque Nacional Lagunas de Zempoala, México. Revista de Biología Tropical 54: 1247–1255.

    Article  PubMed  Google Scholar 

  • Valiente, R. E. L, 2006. Efecto de las especies introducidas en Xochimilco para la rehabilitación del hábitat del ajolote (Ambystoma mexicanum). Thesis, Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, México.

  • Vera, L. M., L. Cairns, F. J. Sánchez-Vázquez & H. Migaud, 2009. Circadian rhythms of locomotor activity in the Nile tilapia Oreochromis niloticus. Chronobiology International 26: 666–681.

    Article  PubMed  Google Scholar 

  • Walls, S. C., 1995. Differential vulnerability to predation and refuge use in competing larval salamanders. Oecologia 101: 86–93.

    Article  Google Scholar 

  • Werner, E. & B. Anholt, 1993. Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. American Naturalist 142: 242–272.

    Article  CAS  PubMed  Google Scholar 

  • Ydenberg, R. C. & L. M. Dill, 1986. The economics of fleeing from predators. Advances in the Study of Behavior 16: 229–249.

    Article  Google Scholar 

  • Zambrano, L., V. Contreras, M. Mazari-Hiriart & A. Zarco-Arista, 2009. Spatial heterogeneity of water quality in a highly degraded tropical freshwater ecosystem. Environmental Management 43: 249–263.

    Article  PubMed  Google Scholar 

  • Zambrano, L., E. Valiente & M. J. Zanden, 2010. Food web overlap among native axolotl (Ambystoma mexicanum) and two exotic fishes: carp (Cyprinus carpio) and tilapia (Oreochromis niloticus) in Xochimilco, Mexico City. Biological Invasions 12: 3061–3069.

    Article  Google Scholar 

  • Zerba, K. E. & J. P. Collins, 1992. Spatial heterogeneity and individual variation in diet of an aquatic top predator. Ecology 73: 268–279.

    Article  Google Scholar 

Download references

Acknowledgments

This research was funded by the Facultad de Ciencias, Universidad Nacional Autónoma de México, UNAM. We thank the staff of the vivarium of FES-Iztacala-UNAM for donating the axolotls and Karla Kruesi Cortés for assistance during the experiments.

Author information

Authors and Affiliations

  1. Laboratorio de Ecofisiología, Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, 04510, Mexico, D.F., Mexico

    Guillermina Alcaraz & Xarini López-Portela

  2. Unidad Multidisciplinaria de Docencia e Investigación-Sisal, Facultad de Ciencias, Universidad Nacional Autónoma de México, Puerto de Abrigo s/n, 97356, Sisal, Yucatán, Mexico

    Cecilia Robles-Mendoza

Authors
  1. Guillermina Alcaraz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xarini López-Portela
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cecilia Robles-Mendoza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guillermina Alcaraz.

Additional information

Handling editor: Lee B. Kats

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alcaraz, G., López-Portela, X. & Robles-Mendoza, C. Response of a native endangered axolotl, Ambystoma mexicanum (Amphibia), to exotic fish predator. Hydrobiologia 753, 73–80 (2015). https://doi.org/10.1007/s10750-015-2194-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-015-2194-4

Keywords

Search

Navigation