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Sponges frequently produce toxic secondary metabolites, especially in tropical coral reefs. These metabolites are thought to have evolved as a chemically mediated defence mechanism and are highly effective against potential predators (Proksch 1994). Nudibranchs of the family Phyllidiidae feed on sponges of the order Halichondrida and exploit this adaptation: they selectively sequester the toxins and employ them for their own protection (Ritson-Williams and Paul 2007; Cimino and Ghiselin 2009). Other than most dorid nudibranchs, phyllidiids lack radulae and jaws. Rather, they are specialized in suctorial feeding. Their feeding apparatus consists of a small mouth followed by an inflated part of the pharynx known as the pharyngeal bulb, which contains secretory glands and can be everted (Fig. 1b, d), presumably for external digestion (Brunckhorst 1993).
During a biodiversity survey off West Halmahera (northern Moluccas) in 2009, we recorded seven phyllidiid species on six halichondrid species. Sponges were identified by the second author (NJdV). Vouchers are deposited in NCB Naturalis. Phyllidia varicosa, Phyllidiella pustulosa, and Phyllidiella nigra fed almost exclusively on the same sponge host, Axinyssa aff. variabilis (Fig. 1a), however, using different feeding techniques. P. varicosa feeds superficially, consuming little more than its host’s skin, often leaving a pattern of multiple discoloured, rosette-shaped marks (Fig. 1c). In contrast, P. pustulosa inserts its exceptionally large pharyngeal bulb deep into the host sponge, frequently creating a narrow hole as deep as half its own length (Fig. 1d). Finally, P. nigra, which has a pharyngeal bulb similar to that of P. pustulosa, yet not quite as large, appears to consume consecutive chunks of tissue from the host’s surface; in one instance, little of the exposed surface was left untouched (Fig. 1e). Dissection of two specimens of each species revealed a significant amount of whole spicules belonging to Axinyssa aff. variabilis in the digestive tracts of P. nigra and P. pustulosa, but not in P. varicosa.
In conclusion, P. varicosa, P. pustulosa, and P. nigra differ in the way they exploit their mutual host, and this difference may facilitate their coexistence in species-rich coral reefs.
References
Brunckhorst DJ (1993) The systematics and phylogeny of phyllidiid nudibranchs (Doridoidea). Rec Aust Mus Suppl 16:1–107
Cimino G, Ghiselin MT (2009) Chemical defense and the evolution of opisthobranch gastropods. Proc Calif Acad Sci 60:175–422
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Ritson-Williams R, Paul VJ (2007) Marine benthic invertebrates use multimodal cues for defense against reef fish. Mar Ecol Prog Ser 340:29–39
Acknowledgments
The survey was sponsored by the Research Centre for Oceanography, Indonesian Institute of Sciences (PPO-LIPI), and funded by the J. J. ter Pelkwijk Fund, the Martin Foundation, and the A.M. Buitendijk Fund. The research permit was issued by the Indonesian State Ministry of Research and Technology (RISTEK).
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Open Access This is an open access article distributed under the terms of the Creative Commons Attribution Noncommercial License (https://creativecommons.org/licenses/by-nc/2.0), which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
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van Alphen, J., de Voogd, N.J. & Hoeksema, B.W. Differential feeding strategies in phyllidiid nudibranchs on coral reefs at Halmahera, northern Moluccas. Coral Reefs 30, 59 (2011). https://doi.org/10.1007/s00338-010-0698-y
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DOI: https://doi.org/10.1007/s00338-010-0698-y