Crinoid anthraquinones as kairomones allowing host selection for the symbiotic snapping shrimp Synalpheus stimpsonii

Abstract

Quinones are one of the major pigment groups that provide such bright colors to feather stars (Echinodermata, Crinoidea). These secondary metabolites also act as defensive molecules rendering crinoids unpalatable and repellent to other organisms. However, feather stars are usually associated with numerous symbiotic organisms, amongst which the ectocommensal snapping shrimp Synalpheus stimpsonii. We investigated the chemical stimulus allowing host selection in S. stimpsonii through the combination of behavioral tests, chemical extractions, and mass spectrometry analyses. The individuals of S. stimpsonii used in the experiments were sampled around the Great Reef of Toliara (Madagascar) where they are found in association with two crinoid species: Comanthus wahlbergii and Phanogenia distincta. The chemical attractiveness of the two crinoid hosts and a non-host species, Cenometra bella, was tested in an olfactometer. The three crinoids produced attractive kairomones allowing the snapping shrimp to recognize them. Mass spectrometry analyses on purified extracts of P. distincta revealed the presence of three different anthraquinones (rhodoptilometrin, comantherin, and a new crinoid anthraquinone). Compared to the existing literature, this anthraquinonic cocktail is specific to P. distincta. When these extracts were injected in the olfactometer, they triggered similar attracting behavior suggesting that crinoid anthraquinones are kairomones allowing host selection for S. stimpsonii. This hypothesis is also supported by the fact that shrimps were chemically attracted by pure commercial anthraquinones. In addition to their traditional defensive role (allomones), anthraquinones would, therefore, also function as kairomones, maintaining the symbiosis between S. stimpsonii and its crinoid hosts.