Surface sequestration of chemical feeding deterrents in the Antarctic sponge Latrunculia apicalis as an optimal defense against sea star spongivory

Abstract

Latrunculia apicalis is a spherically shaped demosponge that previous investigations have shown is rarely preyed upon by sea stars which are the dominant spongivores in antarctic benthic communities. Prior studies have also demonstrated that L. apicalis produces organic compounds that elicit a tube foot retraction response in the keystone spongivorous sea star Perknaster fuscus that can be used as a reliable assay for feeding deterrence. L. apicalis is known to contain discorhabdin alkaloids which serve, among other roles, as the source of its green coloration. To assess the defensive nature of the discorhabdin alkaloids toward P. fuscus, we have determined discorhabdin G concentrations in discrete sponge layers and evaluated those concentrations in the P. fuscus bioassay. In discorhabdin G-bearing sponges, we found a gradient of discorhabdin G that falls off rapidly toward the center of the sponge. On average, 52% of total discorhabdin G in a given sponge was found within 2 mm of the sponge surface. Tube foot retraction responses to extracts from the surface tissues (0–2 mm depth) of L. apicalis were compared to those of an inner layer (8–10 mm depth) and to a sample comprised of the same inner layer spiked with discorhabdin G at a concentration equivalent to that of the surface tissues. Tube foot retraction response times to extracts of the surface layers and the spiked inner layers were not statistically different, but were significantly greater than responses to the unaltered inner layer and controls. These results support the predictions of the optimal defense theory as L. apicalis sequesters its defensive chemistry (discorhabdin G) in its most vulnerable surface tissues, where the likelihood of predation from sea stars is highest. As antarctic sponges are generally preyed upon by extraoral feeding sea stars rather than deeper biting predators such as fish, surface sequestration may be uniquely adaptive in sessile macroinvertebrates occurring in antarctic marine benthic environments.