Opportunistic consumption of coral spawn by the ruby brittle star (Ophioderma rubicundum)

Abstract Many reef invertebrates reproduce through simultaneous broadcast spawning, with an apparent advantage of overwhelming potential predators and maximizing propagule survival. Although reef fish have been observed to consume coral gamete bundles during spawning events, there are few records of such predation by benthic invertebrates. Here, we document several instances of the ruby brittle star, Ophioderma rubicundum, capturing and consuming egg‐sperm bundles of the mountainous star coral, Orbicella faveolata, and the symmetrical brain coral, Pseudodiploria strigosa, during spawning events in the Cayman Islands in 2012 and the Florida Keys in 2022. These observations are widely separated in space and time (>600 km, 10 years), suggesting that this behavior may be prevalent on western Atlantic reefs. Since O. rubicundum spawns on the same or subsequent nights as these coral species, we hypothesize that this opportunistic feeding behavior takes advantage of lipid‐rich coral gamete bundles to recover energy reserves expended by the brittle star during gametogenesis. The consumption of coral gametes by adult brittle stars suggests an underexplored trophic link between reef invertebrates and also provides evidence that ophiuroid–coral symbioses may oscillate between commensalism and parasitism depending on the ontogeny and reproductive status of both animals. Our observations provide insights into the nuanced, dynamic associations between coral reef invertebrates and may have implications for coral reproductive success and resilience.

[1]  Esmeralda Pérez-Cervantes,et al.  Differences in the progression rate of SCTLD in Pseudodiploria strigosa are related to colony size and morphology , 2022, Frontiers in Marine Science.

[2]  Tom Shlesinger,et al.  Breakdown in spawning synchrony: A silent threat to coral persistence , 2019, Science.

[3]  D. Petersen,et al.  The reproductive biology and early life ecology of a common Caribbean brain coral, Diploria labyrinthiformis (Scleractinia: Faviinae) , 2017, Coral Reefs.

[4]  Joshua S Madin,et al.  Fecundity and the demographic strategies of coral morphologies. , 2016, Ecology.

[5]  M. Berumen,et al.  Spawning of coral reef invertebrates and a second spawning season for scleractinian corals in the central Red Sea , 2016 .

[6]  J. Pawlik,et al.  Cleaning mutualist or parasite? Classifying the association between the brittlestar Ophiothrix lineata and the Caribbean reef sponge Callyspongia vaginalis , 2014 .

[7]  John W M Bush,et al.  The fine art of surfacing: its efficacy in broadcast spawning. , 2012, Journal of theoretical biology.

[8]  A. Baird,et al.  Ontogenetic change in the lipid and fatty acid composition of scleractinian coral larvae , 2012, Coral Reefs.

[9]  M. Vermeij,et al.  Day time spawning of a Caribbean coral , 2011, Coral Reefs.

[10]  N. Knowlton,et al.  GENETIC, SPATIAL, AND TEMPORAL COMPONENTS OF PRECISE SPAWNING SYNCHRONY IN REEF BUILDING CORALS OF THE MONTASTRAEA ANNULARIS SPECIES COMPLEX , 2011, Evolution; international journal of organic evolution.

[11]  O. Hoegh‐Guldberg,et al.  The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals , 2010 .

[12]  S. Lewis,et al.  Predators selectively graze reproductive structures in a clonal marine organism , 2009 .

[13]  B. Willis,et al.  Systematic and Biogeographical Patterns in the Reproductive Biology of Scleractinian Corals , 2009 .

[14]  K. Nadaoka,et al.  Temporal changes in settlement, lipid content and lipid composition of larvae of the spawning hermatypic coral Acropora tenuis , 2007 .

[15]  A. Grant,et al.  Long-Term Region-Wide Declines in Caribbean Corals , 2003, Science.

[16]  B. Willis,et al.  Reproductive energy investment in corals: scaling with module size , 2003, Oecologia.

[17]  M. McCormick Consumption of coral propagules after mass spawning enhances larval quality of damselfish through maternal effects , 2003, Oecologia.

[18]  R. Raff,et al.  CONVERGENT MATERNAL PROVISIONING AND LIFE‐HISTORY EVOLUTION IN ECHINODERMS , 2002, Evolution; international journal of organic evolution.

[19]  A. Baird,et al.  Variable palatability of coral eggs to a planktivorous fish , 2001 .

[20]  M. Pratchett,et al.  Consumption of coral propagules represents a significant trophic link between corals and reef fish , 2001, Coral Reefs.

[21]  E. Dinsdale,et al.  Supply-side ecology works both ways: The link between benthic adults, fecundity, and larval recruits , 2000 .

[22]  T. Hughes,et al.  RECRUITMENT FAILURE, LIFE HISTORIES, AND LONG‐TERM DECLINE OF CARIBBEAN CORALS , 2000 .

[23]  J. Mckenzie Sea Stars, Sea Urchins and Allies: Echinoderms of Florida and the Caribbean , 1997 .

[24]  T. Hughes,et al.  Reproductive Strategies of Modular Organisms: Comparative Studies of Reef‐ Building Corals , 1996 .

[25]  P. Taylor Evolutionary palaeoecology of symbioses between bryozoans and hermit crabs , 1994 .

[26]  T. Maruyama,et al.  Lipid composition of positively buoyant eggs of reef building corals , 1993, Coral Reefs.

[27]  R. Babcock,et al.  Aspects of the Fertilization Ecology of Broadcast Spawning Corals: Sperm Dilution Effects and in situ Measurements of Fertilization. , 1992, The Biological bulletin.

[28]  S. C. Wyers,et al.  Spawning of hermatypic corals in Bermuda: a pilot study , 1991, Hydrobiologia.

[29]  G. Hendler,et al.  The ploys of sex: relationships among the mode of reproduction, body size and habitats of coral-reef brittlestars , 1986, Coral Reefs.

[30]  A. Szmant Reproductive ecology of Caribbean reef corals , 1986, Coral Reefs.

[31]  B. Willis,et al.  Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef , 1986 .

[32]  B. Willis,et al.  Mass Spawning in Tropical Reef Corals , 1984, Science.

[33]  G. Hendler The Association of Ophiothrix lineata and Callyspongia vaginalis: A Brittlestar‐Sponge Cleaning Symbiosis? , 1984 .

[34]  J. B. Lewis,et al.  Community structure of ophiuroids (Echinodermata) from three different habitats on a coral reef in Barbados, West Indies , 1983 .

[35]  John B. Lewis,et al.  Feeding mechanisms and feeding strategies of Atlantic reef corals , 1975 .

[36]  A. A. Reimer,et al.  Chemical control of feeding in four species of tropical ophiuroids of the genus Ophioderma. , 1975, Comparative biochemistry and physiology. A, Comparative physiology.

[37]  M. Yamaguchi Growth of Juvenile Acanthaster planci (L.) in the Laboratory , 1974 .

[38]  J. Nevenzel Occurrence, function and biosynthesis of wax esters in marine organisms , 1970, Lipids.

[39]  A. C. Giese Lipids in the economy of marine invertebrates. , 1966, Physiological reviews.

[40]  A. C. Giese,et al.  Cyclic biochemical changes in several echinoderms , 1958 .

[41]  R. Bidigare,et al.  Are all eggs created equal? A case study from the Hawaiian reef-building coral Montipora capitata , 2012, Coral Reefs.

[42]  G. Schmahl,et al.  Biology and Ecology of Coral Reefs and Coral Communities in the Flower Garden Banks Region, Northwestern Gulf of Mexico , 2008 .

[43]  P. D. Vize,et al.  Tight Temporal Consistency of Coral Mass Spawning at the Flower Garden Banks, Gulf of Mexico, from 1997-2003 , 2005 .

[44]  M. Westneat,et al.  Predation on coral spawn by planktivorous fish , 2004, Coral Reefs.

[45]  S. Ward,et al.  Two patterns of energy allocation for growth, reproduction and lipid storage in the scleractinian coral Pocillopora damicornis , 2004, Coral Reefs.

[46]  P. D. Vize,et al.  Mass spawning by two brittle star species, Ophioderma rubicundumand O. squamosissimum (Echinodermata: Ophiuroidea), at the Flower Garden Banks, Gulf of Mexico , 2003 .

[47]  D. Pawson,et al.  Echinoderms of the Rhomboidal cays, Belize: Biodiversity, distribution, and ecology , 2000 .

[48]  J. Videler,et al.  Observations on spawning of scleractinian corals and other invertebrates on the reefs of Bonaire (Netherlands Antilles, Caribbean) , 1999 .

[49]  O. L. Arenas,et al.  Synchronous mass spawning of Montastraea annularis (Ellis & Solander) and Montastraea faveolata (Ell , 1999 .

[50]  K. Deslarzes,et al.  Timing, Species Participation, and Environmental Factors Influencing Annual Mass Spawning at the Flower Garden Banks (Northwest Gulf of Mexico) , 1998 .

[51]  M. V. Veghel Multiple species spawning on Curaçao Reefs , 1993 .

[52]  C. Mundy,et al.  Predictable and unpredictable spawning events: in situ behavioural data from free-spawning coral reef invertebrates , 1992 .

[53]  P. Aliño,et al.  Observations of the synchronized mass spawning and postsettlement activity of octocorals on the Great Barrier Reef, Australia: biological aspects , 1989 .

[54]  B. Kensley,et al.  The Atlantic Barrier Reef ecosystem at Carrie Bow Cay, Belize , 1982 .

[55]  J. Binyon Physiology of echinoderms , 1972 .