Noxious newts and their natural enemies: Experimental effects of tetrodotoxin exposure on trematode parasites and aquatic macroinvertebrates

Abstract

The dermal glands of many amphibian species secrete toxins or other noxious substances as a defense strategy against natural enemies. Newts in particular possess the potent neurotoxin tetrodotoxin (TTX), for which the highest concentrations are found in species within the genus Taricha. Adult Taricha are hypothesized to use TTX as a chemical defense against vertebrate predators such as garter snakes (Thamnophis spp.). However, less is known about how TTX functions to defend aquatic-developing newt larvae against natural enemies, including trematode parasites and aquatic macroinvertebrates. Here we experimentally investigated the effects of exogenous TTX exposure on survivorship of the infectious stages (cercariae) of five species of trematode parasites that infect larval amphibians. Specifically, we used dose-response curves to test the sensitivity of trematode cercariae to progressively increasing concentrations of TTX (0.0 [control], 0.63, 3.13, 6.26, 31.32, and 62.64 nmol L−1) and how this differed among parasite species. We further compared these results to the effects of TTX exposure (0 and 1,000 nmolL−1) over 24 hr on seven macroinvertebrate taxa commonly found in aquatic habitats with newt larvae. TTX significantly reduced the survivorship of trematode cercariae for all species, but the magnitude of such effects varied among species. Ribeiroia ondatrae – which causes mortality and limb malformations in amphibians – was the least sensitive to TTX, whereas the kidney-encysting Echinostoma trivolvis was the most sensitive. Among the macroinvertebrate taxa, only mayflies (Ephemeroptera) showed a significant increase in mortality following exogenous TTX exposure, despite the use of a concentration 16x higher than the maximum used for trematodes. Our results suggest that maternal investment of TTX into larval newts may provide protection against certain trematode infections and highlight the importance of future work assessing the effects of newt toxicity on both parasite infection success and the palatability of larval newts to invertebrate predators.

Of poisons and parasites—the defensive role of tetrodotoxin against infections in newts

“…Consistent with these field‐based observations, Calhoun, Bucciarelli, Kats, Zimmer, and Johnson () recently showed that five species of trematodes exhibited dose‐dependent increases in mortality with exposure to TTX. By comparision, aquatic macroinvertebrates that frequently co‐occur wiht newts showed little response to exogenous TTX over the same time peroid (Calhoun et al, ). However, whether such effects extend to other parasite taxa, including nematodes, fungi and viruses, is unknown.…”

“…For instance, larval trematodes such as R. ondatrae that encyst in the skin were encountered in <2% of hosts, despite being common among larval newts and other amphibians that develop in these ponds (Johnson & Wilber, 2017). Consistent with these field-based observations, Calhoun, Bucciarelli, Kats, Zimmer, and Johnson (2017) recently showed that five species of trematodes exhibited dose-dependent increases in mortality with exposure to TTX.…”

“…By comparision, aquatic macroinvertebrates that frequently cooccur wiht newts showed little response to exogenous TTX over the same time peroid (Calhoun et al, 2017 Kotaki & Shimizu, 1993;Lehman & Brodie, 2004), it is difficult to differentiate among these possibilities, particularly in the absence of experimental data.…”

Effects of road salt on a free-living trematode infectious stage

“…To the best of our knowledge, the period of maximum infectivity for Cephalogonimus sp. cercariae is unknown; however, their lifespan is generally >14 h (Calhoun et al ., 2017). Diplostomum spathaceum and Schistosoma mansoni both belong to the order Strigeatida, as does the unidentified strigeid-type cercaria used here, showing declines in infectivity after 6 and 5 h post-emergence, respectively (Olivier, 1966; Karvonen et al ., 2003).…”

The influence of landscape and environmental factors on ranavirus epidemiology in a California amphibian assemblage

“…At each pond, we randomly selected about 10 individuals per species for ranavirus screening (mean = 20 total amphibians per site, range = 1–84). We sampled metamorphic anurans (Gosner stage 25–32; Gosner, ) and late‐stage larval newts (2–4 T; Calhoun, Bucciarelli, Kats, Zimmer, & Johnson, ) to maintain similarity in life stages among species because we were unable to collect metamorphic newts. Therefore, we controlled for differences among life stages in our sampling and did not hypothesise these differences would influence our observed patterns.…”