The scent of danger: arginine as an olfactory cue of reduced predation risk

Abstract

SUMMARY Animal perception of chemosensory cues is a function of ecological context. Larvae of the California newt (Taricha torosa), for example, exhibit predator-avoidance behavior in response to a chemical from cannibalistic adults. The poison tetrodotoxin (TTX), well known as an adult chemical defense, stimulates larval escape to refuges. Although they are cannibals,adult newts feed preferentially on worms (Eisenia rosea) over conspecific young. Hence, larval avoidance reactions to TTX are suppressed in the presence of odor from these alternative prey. The free amino acid,arginine, is abundant in fluids emitted by injured worms. Here, we demonstrate that arginine is a natural suppressant of TTX-stimulated larval escape behavior. Compared to a tapwater control, larvae initiated vigorous swimming in response to 10–7 mol l–1 TTX. This excitatory response was eliminated when larval nasal cavities were blocked with an inert gel, but not when gel was placed on the forehead (control). In additional trials, a binary mixture of arginine and 10–7 mol l–1 TTX failed to induce larval swimming. The inhibitory effect of arginine was, however, dose dependent. An arginine concentration as low as 0.3-times that of TTX was significantly suppressant. Further analysis showed that suppression by arginine of TTX-stimulated behavior was eliminated by altering the positively-charged guanidinium moiety, but not by modifying the carbon chain, carboxyl group, or amine group. These results are best explained by a mechanism of competitive inhibition between arginine and TTX for common, olfactory receptor binding sites. Although arginine alone has no impact on larval behavior, it nevertheless signals active adult predation on alternative prey, and hence, reduced cannibalism risk.

Chemosensory reception, behavioral expression, and ecological interactions at multiple trophic levels

“…Arg, arginine; TTX, tetrodotoxin. This graphic summarizes combined results from eight published investigations (Elliot et al, 1993;McAllister et al, 1997;Kerby and Kats, 1998;Mobley and Stidham, 2000;Brodie et al, 2005;Zimmer et al, 2006;Ferrer and Zimmer, 2007) (present study).…”

“…For a common suite of analogs, the magnitudes of adult attraction and larval suppression were not positively correlated (Kendall's Tau: R. P. d.f.=5,P=0.57). In fact, suppression of TTX-induced behaviors in larvae was tolerant of most structural modifications (Ferrer and Zimmer, 2007). Changes in the carboxyl terminus and carbon side chain had no effect on response to arginine.…”

“…and behavior The dissolved free-amino acid (DFAA), arginine, has opposing behavioral effects and contrasting ecological consequences on two life history stages of the same newt species (Ferrer and Zimmer, 2007) (current study). It stimulates (adult) predatory search in one case and inhibits (larval) cannibal-avoidance in the other.…”

“…In this case, larval hiding behavior is suppressed by the stream-borne presence of the free-amino acid, L-arginine (Ferrer and Zimmer, 2007). Arginine is abundant in the body fluids of worms, and released upon injury into stream water (see 'Amino acid composition of worm body fluids' in the Results).…”

“…The present paper is written from the perspective of an adult predator, with comparisons to the larval stage. By contrast, the accompanying paper is written from the perspective of the larval prey (Ferrer and Zimmer, 2007).…”