Distance interaction between marine cave-dwelling sponges and crustaceans
Sponges are benthic organisms that are dominant in several ecosystems and known to produce a huge chemical diversity. The putative release of some specialized metabolites in the surrounding seawater is still a matter of debate, but the presence of such compounds in the environment of sponges is thought to influence the behaviour of various mobile organisms and may, thus, contribute to benthic ecosystem structuring and functioning. Underwater Mediterranean caves are characterized by stable environmental conditions and sessile species assemblages dominated by sponges. A two-choice test system was developed to assess the response of two cave-dwelling crustaceans (Hemimysis margalefi and Palaemon serratus) and two other species living in shallow water environments (Leptomysis sp. and Palaemon elegans) to various seawater treatments: control− seawater from an exposed coastline, control+ seawater coming from an underwater cave, and seawater conditioned with four Mediterranean sponges commonly found at the entrance of underwater caves (Aplysina cavernicola, Haliclona fulva, Oscarella tuberculata and Spongia officinalis) or their chemical extracts. We tested the swimming behaviour of these crustacean species in three complementary experiments: (1) control seawater vs. cave seawater; (2) control seawater vs. seawater conditioned with the sponge community, (3) control seawater vs. seawater containing chemical extracts of the same sponge community. Both cave-dwelling crustaceans were attracted by the seawater conditioned with the sponge community, while Leptomysis sp. spent more time in the control seawater and P. elegans exhibited indifferent responses. All four crustacean species avoided the seawater containing the sponge extracts. Interestingly, the response shown by the crustaceans was affected by the time of day. A comparative and untargeted metabolomic approach was applied to the surrounding seawater to identify putative chemomarkers that could explain the crustaceans’ behaviours. Among other compounds found in the seawater, a family of metabolites with molecular formulae in accordance with those of oxylipin derivatives is released by sponges and may, therefore, serve as chemical cues acting as kairomones in the homing behaviour of cave-dwelling crustaceans.
The authors are grateful to the TOTAL Foundation for funding our research programme. This work was performed in the framework of the French-Brazilian International Associated Laboratory “LIA MARRIO” of the CNRS, and received the support of the MALLABAR metabolomics plateau funded by the CNRS, the PACA Region and ANR. We warmly thank Pierre Chevaldonné, Cesar Ruiz and Laurent Vanbostal for collecting H. margalefi and Leptomysis sp. individuals. We are also grateful to Philippe Aublanc of the Paul Ricard Oceanography Institute for providing P. serratus and P. elegans individuals, to Eva Ternon for her assistance to the seawater processing prior to metabolomics, to Jean Charles Martin for his contribution to the development of bioinformatics tools, and to Rachel Mackie for her reviewing of the English.
MS and TP designed the experiments. MS and MLC performed the experiments. MS, SG, MLC and OPT analysed the data. MS, SG, MLC, OPT and TP wrote the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
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