Sex-Biased Predation on Newts of the Genus Taricha by a Novel Predator and Its Relationship with Tetrodotoxin Toxicity
Stokes, Amber N., Cook, David G., Hanifin, Charles T., Brodie, Edmund D., The American Midland Naturalist
Newts of the genus Taricha have long been studied in regards to their skin toxin, tetrodotoxin (TTX). It has been shown that the TTX levels across populations of Taricha are highly variable, and this has been mostly attributed to the interaction between Taricha and their only documented predators, garter snakes of the genus Thamnophis. Here we show that predators other than Thamnophis prey extensively on some newt populations. Ledson Marsh in Annadel State Park in Santa Rosa, CA is a breeding ground for both the California newt (Taricha torosa) and the rough-skinned newt (Taricha granulosa). Predation on these newts was tracked from 1998-2009 and was most often in the form of evisceration and significantly male-biased. As TTX seems to have been developed as an antipredator defense in Taricha, we used Fluorometric High Phase Liquid Chromatography (HPLC) analysis to quantify TTX levels in the skin often male and ten female newts of each species to determine the influence that TTX levels may have on sex-biased predation in this population. We found Taricha females were not significantly more toxic than males. Also, we found that T. torosa were significantly more toxic than T. granulosa, which is in contrast with other newt toxicity studies.
Unlike many prey species, adult Taricha are highly toxic (Mosher et al, 1964; Wakely et al, 1966; Brodie, 1968; Brodie et al, 1974; Daly et al, 1987; Hanifin et al, 1999, 2002). Early studies of Taricha granulosa (Brodie, 1968) showed that virtually all potential predators were susceptible to tetrodotoxin (TTX), the deadly neurotoxin found in the newts' skin. Tetrodotoxin acts by blocking sodium channels (Narahashi et al, 1967) and death from exposure is usually the result of respiratory failure (Brodie, 1968). The only known predators that do not die from ingesting adult Taricha were garter snakes of the genus Thamnophis (Brodie and Brodie, 1990, 1991). Garter snakes have varying levels of resistance to TTX that apparently coevolved with newt toxicity (Brodie et al, 2002; Hanifin et al, 2008).
Hanifin et al (2008) have shown that there is great geographic variation in the toxicity of newts throughout their range. Populations of newts throughout the Pacific coast of the United States and Canada have an average range of whole skin toxicity from 0.000 mg TTX to 4.695 mg TTX. These results suggest that predation on Taricha in some localities along their range is possible, although successful predation has almost never been documented by predators other than Thamnophis. Anecdotal accounts of predation attempts on Taricha by various birds usually report the subsequent death of the predator (McAllister et al, 1997; Mobley and Stidham, 2000). However, recently, successful predation on Taricha, whereby the enure newt was consumed whole with no apparent ill effects by great blue herons (Fellers el al, 2008) and bullfrogs (Rana catesbeiana; Jennings and Cook, 1998), has been reported, although other studies found both species susceptible to TTX (Brodie, 1968). The reports of predation by great blue herons and bullfrogs are from areas where newts have very little or no TTX (Hanifin et al, 2008). Additionally, predation attempts on Taricha by a skunk have been observed, but the fate of the skunk is unknown (M. Edgehouse, pers. comm.). The outcome of these individual predator-prey interactions may be highly influenced by variations in newt toxicity.
Not only is there variation in toxicity geographically, but there is variation within a population and between the sexes (Hanifin et al, 2002). Female Taricha have been found to be more toxic in some populations than male Taricha, likely as a maternal investment to protect eggs. This type of investment could lead to phenomena such as sex-biased predation where a predator selectively preys on the sex with lower toxicity. Sex-biased predation is common in predator/prey systems; however, the causes of such sex differences in predation as well as the direction of bias (i. …