Can Small Rare Prey be Chemically Defended? The Case for Marine Larvae

Marine larvae are consumed by a wide variety of generalist fishes and particle-feeding invertebrates, but larvae of any particular species probably constitute a small and variable portion of the diet for these consumers. Because virtually all consumers can ingest small quantities of noxious compounds with minimal detrimental effects, it is uncertain that toxic chemicals in larvae could be consumed in quantities sufficient to select for predator recognition and avoidance. Despite this, chemically defended larvae do occur. We show that, at low doses, secondary metabolites (the didemnins) from adults and larvae of the Caribbean tunicate Trididemnum solidum induced vomiting in fish, resulting in rapid learned aversion to the didemnin-defended food. The particle-feeding anemone Aiptasia pallida did not learn to avoid the chemically defended food. When anemones ingested the chemical equivalent of 15 larvae/d, representing <2% of the mass of their total daily diet, the didemnins in the larvae significantly reduced: (1) growth of adults by 82%, (2) combined growth of adults and daughter clones by 76%, (3) production of daughter clones by 44%, and (4) average mass of individual daughter clones by 41%. At higher water temperatures, anemones cloned more rapidly, but the negative effects of consuming didemnins also occurred more rapidly. Significant differences in the number of daughter clones produced between treatment and control anemones occurred after only 4 d at seawater temperatures of 27°-29°C vs. 32 d at seawater temperatures of 18°-21°C. Thus consumption of even very small quantities of secondary metabolites can decrease consumer fitness substantially and select for predators that recognize and avoid chemically defended larvae, as do many consumers that co-occur with Trididemnum solidum larvae. This is the first rigorous demonstration that consumption of marine secondary metabolites can decrease consumer fitness when ingested at ecologically realistic doses.