Skip to main content

Advertisement

SpringerLink
Log in

Microhabitat selection of axolotls, Ambystoma mexicanum, in artificial and natural aquatic systems

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

Abstract

Studies of habitat selection are crucial for the conservation of threatened amphibians. Wild salamanders are often distributed near rocks or vegetation, which provide shelter. However, nothing is known about habitat selection of the Mexican axolotl (Ambystoma mexicanum), an endangered salamander of great cultural and ecological value. This study aims to test the relationship between vegetation presence and the distribution of captive-raised axolotls in two systems: a closed canal in their native ecosystem (n = 10) and an artificial canal within a zoological park (n = 6). We used radio-telemetry to analyse the hourly distribution and movement patterns of axolotls in each study site during 72-h observational periods. We found that movement patterns and microhabitat selection were related to vegetation coverage and diurnal and nocturnal periods. Sex and age had no effect in habitat selection. Axolotls in both study sites preferred vegetated microhabitats, but in Xochimilco this preference was only significant during daytime when they were less active. These habitat-specific patterns of spatial distribution may represent behavioural strategies for reducing predation. The first approach of behavioural insights from this study will inform the construction of refuges to reduce the alarming depletion of axolotls in the wild.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arlt, D. & T. Pärt, 2007. Nonideal breeding habitat selection: a mismatch between preferences and fitness. Ecology 88: 792–801.

    Article  Google Scholar 

  • Armillas, P., 2017. Gardens on Swamp. Science 174: 653–661.

    Article  Google Scholar 

  • Bojórquez, L. & F. Villa, 1997. La zona lacustre de Xochimilco: Reconstrucciones hipotéticas. In Stephan-Otto, E. (ed.), Primer Seminario Internacional de Investigadores de Xochimilco. Asociación internacional de investigadores de Xochimilco A.C, México: 468–493.

    Google Scholar 

  • Brown, R., S. Cooke, G. Anderson & S. McKinley, 1999. Evidence to challenge the “2% rule” for biotelemetry. North American Journal of Fisheries Managment 19: 867–871.

    Article  Google Scholar 

  • Capers, R. S., R. Selky & G. J. Bugbee, 2010. The relative importance of local condition and regional preocesses in structuring aquatic plant communities. Freshwater Biology 55: 952–966.

    Article  Google Scholar 

  • Chalmers, R. J. & C. S. Loftin, 2006. Wetland and microhabitat use by nesting four-toed salamanders in maine. Journal of Herpetology 40: 478–485.

    Article  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 

  • Crump, M. & N. Scott, 1994. Visual encounters survey. In Heyer, W., M. A. Donelly, R. McDlarmld, L. Hayec & M. Foster (eds), Measuring and monitoring biological diversity Standard methods for amphibians. Smithsonian Institution Press, Washington D.C: 94–112.

    Google Scholar 

  • Davic, R. D. & L. P. Orr, 1987. The relationship between rock density and salamander density in a mountain stream. Herpetologica 43: 357–361.

    Google Scholar 

  • Denoël, M. & F. Andreone, 2003. Trophic habits and aquatic microhabitat use in gilled immature, paedomorphic and metamorphic alpine newts (Triturus alpestris apuanus) in a pond in central Italy. Belgian Journal of Zoology 133: 95–102.

    Google Scholar 

  • Duarte, C. M., J. Kañff & R. H. Paters, 1986. Patterns in biomass and cover aquatic macrophyres in lakes. Canadian Journal of Fisheries and Aquatic Science 43: 1900–1908.

    Article  Google Scholar 

  • Faccio, S., 2003. Postbreeding emigration and habitat use by Jefferson and spotted salamander in Vermont. Journal of Herpetology 37: 479–489.

    Article  Google Scholar 

  • Ferreira, N., C. Ramirez, G. Urbina & J. Cruz, 1993. Resultados preliminares de la reproducción del ajolote de Xochimilco Ambystoma mexicanum para el establecimiento de una colonia. In Xochimilco, U. A. M. (ed), Primer seminario internacional de investigadores de Xochimilco. Tomo II. Universidad Autónoma Metrolpolitana, Mexico, D.F.: 250

    Google Scholar 

  • Ficetola, G. F., C. Rondinini, A. Bonardi, D. Baisero & E. Padoa-Schioppa, 2015. Habitat availability for amphibians and extinction threat: a global analysis. Diversity and Distributions 21: 302–311.

    Article  Google Scholar 

  • Foster, R. L., A. M. McMillan & K. J. Roblee, 2009. Population status of hellbender salamanders (Cryptobranchus alleganiensis) in the Allegheny River Drainage of New York State. Journal of Herpetology 43: 579–588.

    Article  Google Scholar 

  • Grant, E. H. C., D. A. W. Miller, B. R. Schmidt, M. J. Adams, S. M. Amburgey, T. Chambert, S. S. Cruickshank, R. N. Fisher, D. M. Green, B. R. Hossack, P. T. J. Johnson, M. B. Joseph, T. A. G. Rittenhouse, M. E. Ryan, J. H. Waddle, S. C. Walls, L. L. Bailey, G. M. Fellers, T. A. Gorman, A. M. Ray, D. S. Pilliod, S. J. Price, D. Saenz, W. Sadinski & E. Muths, 2016. Quantitative evidence for the effects of multiple drivers on continental-scale amphibian declines. Scientific Reports 6: 25625.

    Article  CAS  Google Scholar 

  • Gustafson, D. H., C. J. Pettersson & J. C. Malmgren, 2006. Great crested newts (Triturus cristatus) as indicators of aquatic plant diversity. The Herpetological Journal 16: 347–352.

    Google Scholar 

  • Hamer, A. J. & M. J. McDonnell, 2008. Amphibian ecology and conservation in the urbanising world: a review. Biological conservation 141(10): 2432–2449.

    Article  Google Scholar 

  • Hartel, T., S. Nemes, D. Cogǎlniceanu, K. Öllerer, O. Schweiger, C. I. Moga & L. Demeter, 2007. The effect of fish and aquatic habitat complexity on amphibians. Hydrobiologia 583: 173–182.

    Article  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 

  • Hill, M. O., 1974. Correspondence analysis: a neglected multi- variate method. Applied Statistics 3: 340–354.

    Article  Google Scholar 

  • Hinojosa, D. & L. Zambrano, 2004. Interactions of common carp (Cyprinus carpio) with benthic crayfish decapods in shallow ponds. Hydrobiologia 515: 115–122.

    Article  Google Scholar 

  • Hoffman, R., G. Larson & B. Samora, 2004. Responses of Ambystoma gracile to the removal of introduced nonnative fish from a mountain lake. Journal of Herpetology 38: 578–585.

    Article  Google Scholar 

  • Holomuski, J. R., 1986. Intraespecific predation and habitat use by tiger salamanders (Ambystoma tigrinum nebulosum). Journal of Herpetology 20: 439–441.

    Article  Google Scholar 

  • Janowsky-Bell, M. & N. Horner, 1999. Landscape structure, habitat fragmentation, and the ecology of insects. Agricultural and Forest Entomology 27: 503–512.

    Google Scholar 

  • Keen, W. H., 1984. Influence of moisture on activity of plethodontid salamander. Copeia 3: 684–688.

    Article  Google Scholar 

  • Kelley, J. & C. Macías-Garcia, 2010. Ontogenetic effects of captive breeding. In Breed, M. D. & J. Moore (eds), Encyclopedia of Animal Behavior 2. Academic Press, San Diego: 589–595.

    Chapter  Google Scholar 

  • La Toya, T. K., D. L. Jacob, M. A. Hanson, B. R. Herwing, S. E. Bowe & M. L. Otte, 2013. Macrophytes in shallow lakes: relationship with water, sediment and watershed characteristics. Aquatic Botany 109: 39–48.

    Article  Google Scholar 

  • Lecis, R., R. Lecis & K. Norris, 2004. Habitat correlates of distribution and local population decline of the endemic Sardinian newt Euproctus platycephalus. Biological Conservation 115: 303–317.

    Article  Google Scholar 

  • Lehtiniemi, M., J. Engström-Öst & M. Viitasalo, 2005. Turbidity decreases anti-preadtor bahaviour in pike larvae, Esox lucius. Environmental Biology of Fishes 73: 1–8.

    Article  Google Scholar 

  • López, S., 2012. Detección química y visual de la presencia de un depredador (Oreochromis niloticus) en Ambystoma mexicanum. UNAM.

  • Madison, D. M., 1998. Habitat-contingent reproductive behaviour in radio-implanted salamanders: a model and test. Animal Behaviour 55: 1203–1210.

    Article  CAS  Google Scholar 

  • Marco, A., M. Lizana, A. Alvarez & A. R. Blaustein, 2001. Egg-wrapping behaviour protects newt embryos from UV radiation. Animal Behaviour 61: 639–644.

    Article  Google Scholar 

  • Marín, A. I., 2007. Preferencia de plantas para la ovoposición del ajolote Ambystoma mexicanum en condiciones de laboratorio. B.Sc. Dissertation, Universidad Nacional Autónoma de México, México

  • Mayor, S. J., D. C. Schneider, J. A. Schaefer & S. P. Mahoney, 2009. Habitat selection at multiple scales. Écoscience 16: 238–247.

    Article  Google Scholar 

  • Mena, H. & L. Zambrano, 2016. A surgical procedure for implanting radio transmitters in axolotls (Ambystoma mexicanum). Herpetological Review 47: 34–38.

    Google Scholar 

  • Miaud, C., 1993. Predation on newt eggs (Triturus alpestris and T. helveticus): identification of predators and protective role of oviposition behaviour. Journal of Zoology 231: 575–581.

    Article  Google Scholar 

  • O’Hare, M. T., I. D. M. Gunn, D. S. Chapman, B. J. Dudley & B. V. Purse, 2012. Impact of space, local environmental and habitat connectivity on macrophyte communities in conservation lakes. Diversity and Distributions 18: 603–614.

    Article  Google Scholar 

  • Orser, P. N. & D. J. Shure, 1975. Population cycles and activity pattern of the dusky salamnder, Demohnathus fuscus fuscus. The American Midland Naturalist 93: 403–410.

    Article  Google Scholar 

  • Petranka, J., 1998. Salamanders of the United States and Canada. Smithsonian Institution Press, Washington D. C.

    Google Scholar 

  • Petranka, J. W., J. J. Just & E. C. Crawford, 1982. Hatching of amphibian embryos: the physiological trigger. Science 217: 257–259.

    Article  CAS  Google Scholar 

  • Ricciardi, A. & J. B. Rasmussen, 1999. Extinction rates of North American freshwater fauna. Conservation Biology 13: 1220–1222.

    Article  Google Scholar 

  • Rodriguez-Lara, V., E. Peña-Mirabal, R. Baez-Saldaña, A. L. Esparza-Silva, E. García-Zepeda, M. A. C. Cervantes & T. I. Fortoul, 2014. Estrogen receptor beta and CXCR4/CXCL12 expression: differences by sex and hormonal status in lung adenocarcinoma. Archives of Medical Research 45(2): 158–169.

    Article  CAS  Google Scholar 

  • Salthe, S. N., 1969. Reproductive modes and the number and size of ova in the urodels. The American Midland Naturalist 81: 467–490.

    Article  Google Scholar 

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

    Google Scholar 

  • Simonetti, J. A., 1989. Microhabitat use by small mammals in central Chile. Oikos 56: 309–318.

    Article  Google Scholar 

  • Taylor, J., 1983. Orientation and flight behavior of a neotenic salamander (Ambystoma gracile) in Oregon. American Midland Naturalist 109: 40–49.

    Article  Google Scholar 

  • Valiente, E., A. H. Tovar, D. Eslava-andoval & L. Zambrano, 2010. Creating refuges for the axolotl (Ambystoma mexicanum). Ecological Restoration 8: 257–265.

    Article  Google Scholar 

  • Voss, S., M. Woodcock & L. Zambrano, 2015. A tale of two axolotls. BioScience 65: 1134–1140.

    Google Scholar 

  • Ward, J. V., 1992. Aquatic insects ecology: biology and habitat. Wiley, New York: 438.

    Google Scholar 

  • Whitham, J. & A. Mathis, 2000. Effects of hunger and predation risk on foraging behavior of graybelly salamanders, Eurycea multiplicata. Journal of Chemical Ecology 26: 1659–1665.

    Article  CAS  Google Scholar 

  • Wise, S. & B. Buchanan, 2006. Influence of artificiall ilumination on the nocturnal behavior and physiology of salamanders. In Rich, C. & J. E. Longcore (eds), Ecological consequences of artificial lighting. Island Press, Washington D.C.: 221–251.

    Google Scholar 

  • Wisenden, B. D., 2000. Olfactory assessment of predation risk in the aquatic environment. Philosophical Transactions of the Royal Society B: Biological Sciences 355: 1205–1208.

    Article  CAS  Google Scholar 

  • Zambrano, L. & M. Mazari, 2011. Programa de análisis de restauración del sistema lacustre de Xochimilco y del Ajolote. Mexico, D.F

  • Zambrano, L., E. Valiente & M. J. Vander 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 

  • Zambrano, L., H. Cortes & A. Merlo-Galeazzi, 2015. Eat and be eaten: reciprocal predation between axolotls (Ambystoma mexicanum) and crayfish (Cambarellus montezumae) as they grow in size. Marine and Freshwater Behaviour and Physiology 48: 13–23.

    Article  CAS  Google Scholar 

  • Zermeño, V., C. Ximénez, P. Morán, A. Valadez, O. Valenzuela, E. Rascón & R. Cerritos, 2013. Worldwide genealogy of Entamoeba histolytica: an overview to understand haplotype distribution and infection outcome. Infection, Genetics and Evolution 17: 243–252.

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to the Zoológico de Chapultepec for allowing us to use their facilities, Adriana Fernández Ortega for providing us with useful information, and Gustavo Cabrera and Ruben Rojas in CORENA for partly supporting the project. Horacio Mena carried out the microchip implants and followed the health of the animals during the whole experiment. This work was part of CA’s thesis at the Posgrado de Ciencias Biológicas. AGR received a postdoctoral research Grant from PAPIIT IV200117 and IV210117.

Author information

Authors and Affiliations

  1. Departamento de Zoología, Instituto de Biología, Universidad Nacional Autonoma de Mexico, Circuito exterior sin número, Copilco, Coyoacan, 04510, Mexico City, DF, Mexico

    Cristina Ayala, Alejandra G. Ramos, Ángel Merlo & Luis Zambrano

Authors
  1. Cristina Ayala
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alejandra G. Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ángel Merlo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luis Zambrano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luis Zambrano.

Additional information

Handling editor: Vasilis Valavanis

Electronic supplementary material

Below is the link to the electronic supplementary material.

10750_2018_3792_MOESM1_ESM.png

Supplementary material 1 (PNG 6035 kb). Photographs showing the natural canal in Xochimilco (A) and the artificial canal in the Zoológico de Chapultepec (B)

10750_2018_3792_MOESM2_ESM.jpg

Supplementary material 2 (JPEG 6024 kb). Figures showing the spatial locations of individual axolotls (Ambystoma mexicanum) within the zoo (n = 6) and Xochimilco canals (March, n = 5; June, n = 5), each map represents one unique animal. The 72 points observed within quadrats, represent the hourly positions of each individual axolotl. Appendix 2A represents the zoo experiment, appendix 2B represents XochM, which was the first experiment in Xochimilco, and appendix 2C is XochJ, which was the second experiment in Xochimilco

Supplementary material 3 (JPEG 3955 kb)

Supplementary material 4 (JPEG 3960 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ayala, C., Ramos, A.G., Merlo, Á. et al. Microhabitat selection of axolotls, Ambystoma mexicanum, in artificial and natural aquatic systems. Hydrobiologia 828, 11–20 (2019). https://doi.org/10.1007/s10750-018-3792-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3792-8

Keywords

Search

Navigation