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Lethal Effects of Water Quality on Threatened California Salamanders but Not on Co-Occurring Hybrid Salamanders

Authors

  • MAUREEN E. RYAN,

    Corresponding author
    • Department of Evolution and Ecology, and Center for Population Biology, University of California, Davis, CA, U.S.A
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  • JARRETT R. JOHNSON,

    1. Department of Biology, Western Kentucky University, Bowling Green, KY, U.S.A
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  • BENJAMIN M. FITZPATRICK,

    1. Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, U.S.A
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  • LINDA J. LOWENSTINE,

    1. Department of Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California, Davis, CA, U.S.A
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  • ANGELA M. PICCO,

    1. United States Fish and Wildlife Service, Pacific Southwest Regional Office, Sacramento, CA, U.S.A
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  • H. BRADLEY SHAFFER

    1. Department of Ecology and Evolutionary Biology, 621 Charles E. Young Drive South, Room LS5120, Box 951606, Los Angeles, CA 90095 & La Kretz Center for California Conservation Science, Institute of the Environment and Sustainability, La Kretz Hall, Suite 300, Box 951496, 619 Charles E. Young Drive East, University of California, Los Angeles, CA, U.S.A
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Current address: Department of Civil & Environmental Engineering, University of Washington, 201 More Hall, Box 352700, Seattle, WA 98195, U.S.A. emails moryan@u.washington.edu, ambystomo@gmail.com

Abstract

Biological invasions and habitat alteration are often detrimental to native species, but their interactions are difficult to predict. Interbreeding between native and introduced species generates novel genotypes and phenotypes, and human land use alters habitat structure and chemistry. Both invasions and habitat alteration create new biological challenges and opportunities. In the intensively farmed Salinas Valley, California (U.S.A.), threatened California tiger salamanders (Ambystoma californiense) have been replaced by hybrids between California tiger salamander and introduced barred tiger salamanders (Ambystoma tigrinum mavortium). We conducted an enclosure experiment to examine the effects habitat modification and relative frequency of hybrid and native California tiger salamanders have on recruitment of salamanders and their prey, Pacific chorus frogs (Pseudacris regilla). We tested whether recruitment differed among genetic classes of tiger salamanders (hybrid or native) and pond hydroperiod (seasonal or perennial). Roughly 6 weeks into the experiment, 70% (of 378 total) of salamander larvae died in 4 out of 6 ponds. Native salamanders survived (n = 12) in these ponds only if they had metamorphosed prior to the die-offs. During die-offs, all larvae of native salamanders died, whereas 56% of hybrid larvae died. We necropsied native and hybrid salamanders, tested water quality, and queried the California Department of Pesticide Regulation database to investigate possible causes of the die-offs. Salamander die-offs, changes in the abundance of other community members (invertebrates, algae, and cyanobacteria), shifts in salamander sex ratio, and patterns of pesticide application in adjacent fields suggest that pesticide use may have contributed to die-offs. That all survivors were hybrids suggests that environmental stress may promote rapid displacement of native genotypes.

Efectos Letales de la Calidad del Agua sobre Salamandras de California Amenazadas pero no sobre Salamandras Híbridas Concurrentes

Resumen

Las invasiones biológicas y la alteración del hábitat a menudo son perjudiciales para las especies nativas, pero es difícil predecir sus interacciones. El entrecruzamiento de especies nativas e introducidas genera genotipos y fenotipos nuevos, y el uso de tierras por humanos altera la estructura y química del hábitat. Tanto las invasiones como la alteración del hábitat crean nuevos retos y oportunidades biológicas. En el intensivamente cultivado Valle Salinas, California (E.U.A.), la salamandra de California amenazada (Ambystoma californiense) ha sido reemplazada por híbridos de A. californiense y la salamandra introducida (Ambystoma tigrinum mavortium). Realizamos un experimento con encierros para examinar los efectos de la modificación del hábitat y de la frecuencia relativa de salamandras híbridas y nativas sobre el reclutamiento de salamandras y su presa, ranas (Pseudacris regilla). Probamos si el reclutamiento difirió entre clases genéticas de salamandras (híbridas o nativas) y el hidroperíodo del cuerpo de agua (temporal o perenne). A seis semanas de iniciado el experimento, 70% (de un total de 378) de las larvas de salamandra murieron en 4 de 6 cuerpos de agua. Las salamandras nativas sobrevivieron (n = 12) en estos cuerpos de agua solo si habían metamorfoseado antes de las declinaciones. Durante las declinaciones, murieron todas las larvas de salamandras nativas, mientras que 56% de las larvas híbridas murieron. Realizamos necropsias a las salamandras nativas e híbridas, probamos la calidad del agua y revisamos la base de datos del Departamento de Regulación de Pesticidas de California para investigar posibles causas de las declinaciones. Las declinaciones de salamandras, cambios en la abundancia de otros miembros de la comunidad (invertebrados, algas y cianobacterias), cambios en la proporción de sexos de las salamandras y patrones de aplicación de pesticidas en campos adyacentes sugieren que el uso de pesticidas pudo haber contribuido a las declinaciones. El hecho de que todos los sobrevivientes son híbridos sugiere que el estrés ambiental puede promover un rápido desplazamiento de los genotipos nativos.

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