scent of danger: tetrodotoxin (TTX) as an olfactory cue of predation risk

• Published in: Ecological monographs 2006-11, Vol.76 (4), p.585-600
• Main Authors: Zimmer, Richard K., Schar, Daniel W., Ferrer, Ryan P., Krug, Patrick J., Kats, Lee B., Michel, William C.
• Format: Article
• Language: English
• Subjects: adults; adult–larval interaction; Amphibia. Reptilia; amphibian; Animal and plant ecology; animal behavior; Animal, plant and microbial ecology; avoidance conditioning; Biological and medical sciences; cannibalism; chemical compounds; Chemical ecology; Ecological genetics; Fundamental and applied biological sciences. Psychology; Gels; General aspects; Insect larvae; larva; Larvae; Marine ecology; newt; Newts; odors; olfactometry; Predation; predator; predator avoidance; predator avoidance behavior; Predators; prey; Reptiles & amphibians; salamanders and newts; Salamandridae; Tap water; Taricha torosa; Tetrodotoxin; Toxins; TTX; Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution; Zoology
• ISSN: 0012-9615; 1557-7015
• DOI: 10.1890/0012-9615(2006)076[0585:TSODTT]2.0.CO;2

Larvae of the California newt (Taricha torosa) exhibit striking predator-avoidance behavior, escaping to refuges in response to a chemical cue from cannibalistic adults. In laboratory flow-tank experiments, stream water collected near free-ranging adults induced hiding responses in 100% of the larvae tested. Solutions prepared by bathing adults (in field and laboratory) also evoked strong hiding behaviors. Insensitive to adult feeding status (fed or starved), and clearly not an excretory product, the chemical cue was released from adult skin (i.e., in swabs of adult backs, sides, and bellies). Tetrodotoxin (TTX) was found in skin swabs of adults and in bathwater at 1 × 10-7 mol/L using reversed-phase high-pressure liquid chromatography (HPLC). Concentrations of 1 × 10-7 to 1 × 10-9 mol/L TTX standard, and equivalent dilutions of bathwater, triggered hiding behaviors in larvae, with no subsequent sublethal toxicity. The presence of TTX-sensitive cells within larval olfactory epithelium was confirmed by behavioral experiments and electrophysiological recordings. In contrast, larvae did not hide in response to two other, structurally mimetic compounds (saxitoxin and μ-conotoxin GIIIB). Ontogenetically, larval behavioral responses to TTX and bathwater were strongest during weeks 3—5, diminishing to nil during week 7. No longer susceptible to adult cannibalism, larval indifference to the cue coincided with their ability to climb out of water and onto land. Thus, newt larvae escape cannibalism by detecting a poison (TTX) well known as a chemical defense for conspecific adults. Eliciting a behavioral response in one case and inhibiting neural activity in the other, this compound results in opposing physiological effects, with avoiding predation as the common goal. Accordingly, TTX joins a select group of keystone molecules, each having critical, but different, ecological consequences at multiple trophic levels. The unique combination of bioactive properties makes a compelling case for asymmetrical selection as a force driving the evolution of adult—larval trophic interactions.