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

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farmed Salinas Valley, California (U.S.A.), threatened California tiger salamanders (Ambystoma californiense) have been replaced by hybrids between California tiger salamander and introduced barred tiger salamanders (Ambystoma tigrinum mavortium).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.

Invasion Complexities: The Diverse Impacts of Nonnative Species on Amphibians

“…Their results demonstrate how the displacement of native genotypes can potentially compromise ecosystems by generating novel genotypes and phenotypes. Ryan et al (2013) also found that salamanders with hybrid genotypes were able to survive major environmental stress while native genotypes could not. All native genotype salamanders died off unless they had already metamorphosed prior to die-off events.…”

Amphibian molecular ecology and how it has informed conservation

“…It breeds primarily in vernal pools and faces threats from extensive habitat conversion to agricultural lands (Davidson et al 2002), pesticide usage (Ryan et al 2012) and hybridization with the invasive barred tiger salamander [Ambystoma (tigrinum) mavortium, BTS], which was introduced to California in the 1950s (Riley et al 2003). Our laboratory has been working on this system for the past 20 years, and we have, along with others, learned a great deal about tiger salamanders in California by studying their molecular ecology.…”

“…Hybridization with the invasive BTS is among the greatest threats facing CTS. Hybrid animals are more robust and have increased survival rates compared to pure native CTS, leading to concerns that hybrids will be strongly favoured by natural selection and replace pure CTS (Fitzpatrick & Shaffer 2007b;Ryan et al 2012). Additionally, the presence of CTS/BTS hybrids has been found to negatively impact other amphibians breeding in the same ponds Searcy et al 2015).…”

Conservation Genetics and Genomics of Amphibians and Reptiles

“…In a series of papers, our laboratory has demonstrated that nonnative A. t. mavortium introduced into central California in the 1950s led to the formation of a hybrid swarm in approximately 25% of the range of the federally and state-protected California tiger salamander (A. californiense); another 25% has been invaded by a smaller set (3/68 marker loci) of superinvasive genes that are spreading more rapidly (46,59,60). At both the phenotypic and genetic levels, these hybrids generally have higher fitness than pure native salamanders, raising serious conservation concerns for the endangered A. californiense (61)(62)(63)(64).…”