Ecological functions of tetrodotoxin in a deadly polyclad flatworm

Abstract

The deadly neurotoxin tetrodotoxin (TTX) is found in a variety of animal phyla and, because of its toxicity, is most often assumed to deter predation. On the tropical Pacific island of Guam, we found an undescribed flatworm (planocerid sp. 1) that contains high levels of TTX and its analogs. Through ecological experiments, we show that TTXs do not protect these flatworms from some predators but instead are used to capture mobile prey. TTX is known to have multiple ecological functions, which has probably led to its widespread presence among prokaryotes and at least 10 metazoan phyla.prey-capture ͉ chemical ecology T he ecological functions of tetrodotoxin (TTX, Fig. 1a) and its analogs have rarely been tested even though it has been isolated and characterized since 1965 (1; reviewed in ref.2). The cellular mechanism of TTX paralysis is well understood (blocking sodium ion channels that control nerve impulses; ref.3) but its functions for organisms are just beginning to be understood. Because of the potent toxicity of TTX, it is often assumed to protect marine and terrestrial organisms from predators (4-6). In terrestrial amphibians [Taricha granulosa (7) and Atelopus spp. (8)], and marine pufferfish (Takifugu spp.; ref. 9) TTX is found in the skin, where it could be tasted by potential predators. The ecological significance of TTX as a defensive compound was recently shown in the evolutionary ecology of newts (Taricha granulosa) and their snake predators (Thamnophis sirtalis) (10, 11). Alternative ecological functions of TTX are known from pufferfish, which use TTX as a pheromone to attract males to gravid females (12), and in the blue-ringed octopus Hapalochlaena maculosa and six species of arrowworms, all of which contain TTX in their venom glands (13-16).On the tropical Pacific island of Guam, we found a flatworm (undescribed, but vouchered as planocerid sp. 1; ref. 17 and Fig. 1b) that eats gastropods. Flatworms in Planoceridae are poorly studied, and fundamental questions such as what and how they eat remain unknown for most species. The flatworm Planocera multitentaculata contains TTX (18), but its ecological role in this flatworm was never tested. In this study, we describe the feeding ecology of planocerid sp. 1, and through ecological experiments, test whether TTX is used for defense or prey capture.

Chemical defense in pelagic octopus paralarvae: Tetrodotoxin alone does not protect individual paralarvae of the greater blue-ringed octopus (Hapalochlaena lunulata) from common reef predators

“…Noguchi and Arakawa 2008), and some freshwater fish gustatory neurons respond to TTX (Yamamori et al 1987), empirical data on the realized anitpredator efficacy is lacking. Conversely, although originally thought to be a defense (Miyazawa et al 1987), TTX is used as venom in a polyclad worm (Ritson-Williams et al 2006). Here we test whether the pelagic paralarvae of H. lunulata contain TTX and, if so, whether TTX protects the paralarvae from predation by common reef predators.…”

Adaptive evolution of voltage-gated sodium channels: The first 800 million years

“…A number of animals use the neurotoxin tetrodotoxin (TTX), mainly for protection against predators (49) but in a few cases as a weapon to subdue prey (50). Animals associated with TTX span the animal kingdom.…”

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

“…For a biodiverse assemblage of animal and microbial species, TTX serves as a chemical defense or venom (Kim et al, 1975;Sheumack et al, 1978;Miyazawa et al, 1986;Thuesen et al, 1988;Ritson-Williams et al, 2006). It acts as a potent neurotoxin by binding to and blocking voltage-gated sodium channels on nerve and muscle cell membranes (Hille, 2001).…”