Evidence against mutualism in an aeolid nudibranch associated with Symbiodiniaceae dinoflagellates

Abstract

The symbiotic association with Symbiodiniaceae dinoflagellates has been more investigated for reef-building corals than for other metazoan taxa. Nudibranchs are relevant hosts as they present a wide variety of relationships with Symbiodiniaceae that range from predation to mutualistic association. The aeolid Berghia stephanieae is perhaps the best model for ecological studies in the mollusk-dinoflagellate association due to its hardiness, short life cycle and simple aquaculture protocols. However, it remains untested if B. stephanieae and Symbiodiniaceae actually engage in mutualism. Therefore, this study experimentally investigated the following aspects pertaining to the relationship between the two organisms: (i) Symbiodiniaceae retention time in the host tissue, (ii) effect of Symbodiniaceae presence in the prey item on host growth, and (iii) host capability to obtain free-living Symbiodiniaceae. Three experiments were performed: (i) monitoring of Symbiodiniaceae concentration in the cerata of starved B. stephanieae, (ii) offer of different-sized prey with and without symbionts and measuring B. stephanieae growth, and (iii) offer of free-living Symbiodiniaceae to B. stephanieae. Results show that the retention time (3–5 days) is much shorter than for many symbiont-associated nudibranchs. Berghia stephanieae growth is influenced by prey size, and apparently not affected by symbiont presence. Finally, this species is unable to obtain free-living Symbiodiniaceae. These results indicate that B. stephanieae does not meet criteria for a mutualistic relationship with Symbiodiniaceae, such as long-term retention and metabolite or favor exchange. This relationship may be in an evolutionary transitional stage, unlike the fully functional mutualism found in other organisms such as reef-building corals.