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

Abstract

Worms and other marine invertebrates living in soft sediments commonly produce brominated natural products that have been hypothesized to function as defenses against consumers, but this hypothesis has not been tested directly. When 16 species of worms from a Georgia mud flat were fed to two sympatric fishes (Fundulus heteroclitus, Leiostomus xanthurus) and a crab (Callinectes similis), 15 species (94%) were palatable to all three predators. Only the hemichordate Saccoglossus kowalevskii was unpalatable to both fishes, but even it was readily consumed by the crab. Bioassay-guided chemical investigations demonstrated that Saccoglossus kowalevskii was rejected by fishes because it contained 2,3,4-tribromopyrrole at 0.2% of worm dry mass. This is the first direct test of brominated worm metabolites as defenses against sympatric consumers. The deterrence of 2,3,4-tribromopyrrole in S. kowalevskii may explain why densities of this worm increase 40-fold during seasons when predation is high and densities of palatable worms decline sharply. To more broadly examine the effects of brominated metabolites on worm palatability, we collected from North Carolina, Georgia, and Florida 14 species reported to produce brominated metabolites. These species were fed to sympatric consumers to assess palatability and also analyzed for brominated metabolites by gas chromatography mass spectrometry (GC/MS). Nine of the fourteen species contained brominated metabolites, but only two were unpalatable. In a final test, five additional brominated metabolites produced by marine worms were added to palatable foods at natural concentrations and at up to 20ϫ natural concentrations. None deterred feeding at natural concentrations, one was deterrent at 5-15ϫ natural concentration, and four had no effect at even 20ϫ natural concentration. Thus, while one worm was defended by a brominated compound, most worms containing brominated metabolites were palatable, and brominated natural products seldom functioned as chemical defenses against consumers.

Chemical defense of a soft-sediment dwelling phoronid against local epibenthic predators

“…Each compound was tested in separate feeding assays with seaperch by adding it to squid paste at concentrations that reflect whole phoronid and phoronid lophophore concentrations, where these could be detected by the GC/ TOF-MS, and at a range of higher concentrations. When the bromophenol compound was not detectable by GC/TOF-MS, it was offered to Embiotoca lateralis at concentrations found in other infaunal species as reported in the literature and at higher concentrations: 2, 6-dibromophenol is found at 2.84 × 10 -6 g ml -1 in acorn worms Balanoglossus aurantiacus (Kicklighter et al 2004b), and 2, 4, 6-tribromophenol is found at a concentration of 1.118 × 10 -5 g ml -1 in B. carnosus (Higa et al 1980). Feeding assays for the extracts and fractions were conducted using the standard palatability procedures described.…”

“…We also tested the deterrent properties of 3 specific brominated phenolic compounds -2, 4-dibromophenol, 2, 6-dibromophenol, and 2, 4, 6-tribromophenol -as these compounds have been previously suggested to be biologically active (Kicklighter et al 2004b) and two have been reported from Phoronopsis viridis (Sheikh & Djerassi 1975). We measured the concentration of these compounds in phoronids from Bodega Harbor using the following procedure.…”

“…bromo-and chlorophenols) have been isolated from a number of common soft-sediment infaunal polychaetes (Woodin 1985, Steward et al 1996, Fielman et al 1999, Kicklighter et al 2003, 2004a, hemichordates (King 1986, King et al 1995, Steward et al 1996, Giray & King 1997, Fielman et al 1999, Cowart et al 2000, and at least 1 mollusk (Fielman et al 1999), evidence for their effectiveness as antipredator defenses is equivocal at best (Giray & King 1997, Kicklighter et al 2004b). Still, chemical deterrents against generalist predators have been demonstrated for a few soft-sediment invertebrates (Kicklighter et al 2003(Kicklighter et al , 2004b.…”

Natural 14C in Saccoglossus bromophenolosus compared to 14C in surrounding sediments

“…Marine organisms synthesize thousands of halogenated organic compounds (HOCs) and use these secondary metabolites to deter feeding, hinder or inhibit settlement of competitors, and perhaps regulate internal salt or hydrogen peroxide levels (Gribble 2000, 2003, Winterton 2000, Kicklighter et al 2004). Generally, these compounds, with levels approaching as much as several percent of the total body mass, have been identified from analysis of grab samples of individual species.…”

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

“…However, because feeding preferences of bluehead wrasse commonly parallel preferences of other generalist consumers (see Lindquist & Hay 1996, McClintock et al 1996, Bullard & Hay 2002a, Burns et al 2003, and because this wrasse has commonly been used as a model, generalist consumer in other investigations of invertebrate chemical defenses (e.g. Pawlik et al 1995, Lindquist & Hay 1996, Kubanek et al 2002, Pisut & Pawlik 2002, we used this species for our bioassays of palatability.…”