Palatability and defense of some tropical infaunal worms: alkylpyrrole sulfamates as deterrents to fish feeding

Abstract

Numerous studies have investigated chemical defenses among sessile species growing on hard substrates, but few have addressed this for mobile species in soft-sediment communities. We investigated the palatability and potential chemical defenses of 11 worm species from soft-sediment systems in southern Florida, USA. Three species were unpalatable to the bluehead wrasse Thalassoma bifasciatum. The polychaete Cirriformia tentaculata and the hemichordate Ptychodera bahamensis were uniformly unpalatable. For the polychaete Eupolymnia crassicornis, the exposed tentacles were unpalatable, but the body, which remains protected in a deeply buried tube, was palatable. These unpalatable worms were chemically defended; extracts of C. tentaculata, P. bahamensis, and the tentacles of E. crassicornis deterred fish feeding. For C. tentaculata, bioassay-guided fractionation demonstrated that a mixture of 3 closely related alkylpyrrole sulfamates deterred fish at naturally occurring concentrations (2-n-hexylpyrrole sulfamate [1.6% of worm dry mass], 2-n-heptylpyrrole sulfamate [3.1% dry mass], and 2-n-octylpyrrole sulfamate [0.8% dry mass]). This appears to be the first documentation of characterized natural products defending a marine worm from consumers. For P. bahamensis and the tentacles of E. crassicornis, deterrent effects of crude extracts decomposed before specific compounds could be identified.

Do brominated natural products defend marine worms from consumers? Some do, most don’t

“…2, 3); P. bahamensis was also defended chemically (based on bioassays like those shown in Fig. 2), but the deterrent metabolites were not determined (Kicklighter et al 2003).…”

“…Crabs were usually offered whole worms, but whole worms of some species were often too big for our small fishes to eat. Our previous experience with fish and crab feeding (Kicklighter 2003) suggested that consumers fed similarly on either whole worms or worm portions and that the release of body fluids from worm portions did not stimulate feeding on species that would have been avoided otherwise. As examples, for worms small enough for our fishes to handle (e.g., Spiochaetopterus oculatus, Streblospio benedicti, Tharyx marioni), consumption of whole worms or worm portions was always equivalent, and in assays with larger fishes and worms from other habitats, worms that were rejected when offered entire in the field were also rejected when segments were offered in the lab (Kicklighter and Hay pers.…”

“…1; Table 1). C. tentaculata was also unpalatable, but it did not contain brominated metabolites; this species was defended by a family of nonbrominated pyrroles, (Kicklighter et al 2003). For P. bahamensis, crude extracts and further fractions were unpalatable to the bluehead wrasse, but it is unknown whether brominated metabolites were responsible, since the activity was lost with further purifications (Kicklighter et al 2003).…”

Chemical mediation of interactions among marine organisms

“…325 ' 326 Bioassay-guided isolation of C. tentaculata extracts led to the isolation of predator deterrent 2-alkylpyrrole sulfamates 93-95. 325 ' 327 In a second survey of 16 species of worms collected from a Georgia mud-flat, only one species, Saccoglossus kowalevskii, was unpalatable to two sympatric fish, Fundulus heteroclitus and Leisostomus xanthurus. 12% Bioassayguided fractionation yielded 2,3,4-tribromopyrrole 96 as the active constituent in S. kowalevskii.…”

Chemical Mediation of Interactions Among Marine Organisms

“…tentacles) of the animal was unpalatable to fish and crabs. 325 ' 326 Bioassay-guided isolation of C. tentaculata extracts led to the isolation of predator deterrent 2-alkylpyrrole sulfamates 93-95. 325 ' 327 In a second survey of 16 species of worms collected from a Georgia mud-flat, only one species, Saccoglossus kowalevskii, was unpalatable to two sympatric fish, Fundulus heteroclitus and Leisostomus xanthurus.…”