Assessing trophic relationships between shallow-water black corals (Antipatharia) and their symbionts using stable isotopes

Authors

  • Lucas Terrana Biology of Marine Organisms and Biomimetics, University of Mons, 7000 Mons
  • Gilles Lepoint Laboratory of Oceanology-MARE Centre, University of Liège, 4000 Liège
  • Igor Eeckhaut Biology of Marine Organisms and Biomimetics, University of Mons, 7000 Mons

DOI:

https://doi.org/10.26496/bjz.2019.33

Keywords:

Antipatharians, Black corals, Symbioses, Stable Isotopes, Madagascar

Abstract

Shallow-water antipatharians host many symbiotic species, which spend their adult life with their host and/or use them to have access to food. Here we determine the trophic relationships between four common macrosymbionts observed on/in Cirripathes anguina, Cirrhipathes densiflora and Stichopathes maldivensis in SW Madagascar. These include the myzostomid Eenymeenymyzostoma nigrocorallium, the gobiid fish Bryaninops yongei, and two palaemonid shrimps, Pontonides unciger and Periclimenes sp. The first is an endosymbiont living in the digestive tract, while the others are ectosymbionts. The analyses show that most likely (i) none of the symbionts uses the host as a main food source, (ii) nocturnal plankton represents a main part of the diet of antipatharians while the symbionts feed preferentially on diurnal plankton, (iii) the myzostomid has the narrowest trophic niche, (iv) the two shrimps have distinct trophic niches and feed at lower trophic level than do the other symbionts. Concerning the myzostomids, they had the same δ13C values but had significantly higher δ15N values than the hosts. TEFs (Trophic Enrichment Factors) recorded were Δ13C = 0.28 ± 0.25 ‰ and Δ15N = 0.51 ± 0.37 ‰, but these were not high enough to explain a predator-prey relationship. These worms rely on the coral diet but may also ingest host fluids explaining the slight enrichment in heavier nitrogen isotopes. On the other hand, the ectosymbionts use the coral as a pathway to have access to food from the midwater: they feed from the water passing nearby the black corals, but a kleptoparasitic behaviour cannot be excluded.

References

Baillon S., Hamel J.F. & Mercier A. (2014). Diversity, distribution and nature of faunal associations with deep-sea pennatulacean corals in the Northwest Atlantic. PloS ONE 9 (11): e111519. https://doi.org/10.1371/journal.pone.0111519

Bearhop S., Adams C.E., Waldron S., Fuller R.A. & MacLeod H. (2004). Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 73 (5): 1007–1012. https://doi.org/10.1111/j.0021-8790.2004.00861.x

Becker E.L., Cordes E.E., Macko S.A., Lee R.W. & Fisher C.R. (2013). Using stable isotope compositions of animal tissues to infer trophic interactions in Gulf of Mexico lower slope seep communities. PloS ONE 8 (12): e74459. https://doi.org/10.1371/journal.pone.0074459

Bo M., Rouse G., Martin D. & Bavestrello G. (2014). A myzostomid endoparasitic in black corals. Coral Reefs 33 (1): 273–273.

Boag B., Neilson R., Robinson D., Scrimgeour C.M. & Handley L.L. (1998). Wild rabbit host and some parasites show trophic-level relationships for δ13C and δ15N: a first report. Isotopes in Environmental and Health Studies 34 (1–2): 81–85. https://doi.org/10.1080/10256019708036335

Boland R.C. & Parrish F.A. (2005). A description of fish assemblages in the black coral beds off Lahaina, Maui, Hawai‘i. Pacific Science 59: 411–420. https://doi.org/10.1353/psc.2005.0032

Bruce A.J. (1978). A report on a collection of pontoniine shrimps from Madagascar and adjacent seas. Zoological Journal of the Linnean Society 62: 205–290. https://doi.org/10.1111/j.1096-3642.1978.tb01039.x

Bruce A.J. (2005). Pontoniine shrimps from the 2003 NORFANZ Expedition, 10 May–16 June (Crustacea: Decapoda:Palaemonidae). Zootaxa 981: 1–20. https://doi.org/10.11646/zootaxa.981.1.1

Buhl-Mortensen L. & Mortensen P.B. (2004). Symbiosis in deep-water corals. Symbiosis 37: 33–61

Caulier G., Lepoint G., Van Nedervelde F. & Eeckhaut I. (2014). The diet of the Harlequin crab Lissocarcinus orbicularis, an obligate symbiont of sea cucumbers (holothuroids) belonging to the genera Thelenota, Bohadschia and Holothuria. Symbiosis 62: 91–99. https://doi.org/10.1007/s13199-014-0274-2

Criales M.M. (1980). Commensal caridean shrimps of Octocorallia and Antipatharia in Curaçao and Bonaire with description of a new species of Neopontonides. Studies on the Fauna of Curaçao and other Caribbean Islands 61 (1): 68–85.

Darimont C.T., Paquet P.C. & Reimchen T.E. (2009). Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate. Journal of Animal Ecology 78 (1): 126–133. https://doi.org/10.1111/j.1365-2656.2008.01473.x

Davis W.P. & Cohen D.M. (1968). A gobiid fish and a palaemonid shrimp living on an antipatharian sea whip in the tropical pacific. Bulletin of Marine Science 18 (4): 749–761.

DeNiro M.J. & Epstein S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45: 341–351. https://doi.org/10.1016/0016-7037(81)90244-1

De Ridder C. & Holthuis L.B. (1979). Pontonides sympathes, a new species of commensal shrimp (Crustacea, Decapoda, Pontoniinae) from Antipatharia in the Galapagos Islands. Zoologische Mededelingen 54 (7): 101–110.

Deudero S., Pinnegar J.K. & Polunin N.V. (2002). Insights into fish host-parasite trophic relationships revealed by stable isotope analysis. Diseases of Aquatic Organisms 52 (1): 77–86. https://doi.org/10.3354/dao052077

Doucett R.R., Giberson D.J. & Power G. (1999). Parasitic association of Nanocladius (Diptera:Chironomidae) and Pteronarcys biloba (Plecoptera:Pteronarcyidae): insights from stable-isotope analysis. Journal of the North American Benthological Society 18: 514–523.

Eeckhaut I. & Lanterbecq D. (2005). Myzostomida: a review of the phylogeny and ultrastructure. Hydrobiologia 535 (1): 253–275. https://doi.org/10.1007/s10750-004-5636-y

Fleming N.E.C., Harrod C., Griffin D.C., Newton J. & Houghton J.D.R (2014). Scyphozoan jellyfish provide short-term reproductive habitat for hyperiid amphipods in a temperate near-shore environment. Marine Ecology Progress Series 510: 229–240. https://doi.org/10.3354/meps10896

Frédérich B., Michel L.N., Zaeytydt E., Bolaya R.L., Lavitra T., Parmentier E. & Lepoint G. (2017) Comparative feeding ecology of cardinalfishes (Apogonidae) at Toliara Reef, Madagascar. Zoological Studies 56: 10. https://doi.org/10.6620/ZS.2017.56-10

Goenaga C. (1977). Two New Species of Stichopathes (Zoantharia; Antipatharia) with Observations on Aspects of Their Biology. Unpublished MS Thesis, University of Puerto Rico, Puerto Rico.

Herler J. (2007). Microhabitats and ecomorphology of coral- and coral rock-associated gobiid fish (Teleostei: Gobiidae) in the northern Red Sea. Marine Ecology 28: 82–94. https://doi.org/10.1111/j.1439-0485.2007.00165.x

Iken K., Brey T., Wand U., Voigt J. & Junghans P. (2001). Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Progress in Oceanography 50 (1–4): 383─405. https://doi.org/10.1016/s0079-6611(01)00062-3

Jackson A.L., Inger R., Parnell A.C. & Bearhop S. (2011). Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses. Journal of Animal Ecology 3: 595─602. https://doi.org/10.1111/j.1365-2656.2011.01806.x

Kirkendale L. & Messing C.G. (2003). An annotated checklist and key to the Crinoidea of Guam and the Commonwealth of the Northern Marianas Islands. Micronesica 3536: 523–546.

Larson H. (1985). A revision of the gobiid genus Bryaninops (Pisces), with a description of six new species. Beagle, Records of the Museums and Art Galleries of the Northern Territory 2 (1): 57–93. Available from https://biodiversitylibrary.org/page/55710181 [accessed 24 Oct. 2019].

Love M.S., Yoklavich M.M., Black B.A. & Andrews A.H. (2007). Age of black coral (Antipathes dendrochristos) colonies, with notes on associated invertebrate species. Bulletin of Marine Science 80 (2): 391–399.

Marin I. (2007). The coral-associated shrimp genus Pontonides (Caridea, Palaemonidae, Pontoniinae) in Nhatrang Bay, Vietnam, with description of two new species. Zootaxa 1635: 1–21. https://doi.org/10.5281/zenodo.179514

McCutchan J.H., Lewis W.M., Kendall C. & McGrath C.C. (2003). Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102: 378–390. https://doi.org/10.1034/j.1600-0706.2003.12098.x

Molodtsova T.N. & Budaeva N. (2007). Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469–479

Munday P.L., Pierce S.J., Jones G.P. & Larson H.K. (2002). Habitat use, social organization and reproductive biology of the seawhip goby, Bryaninops yongei. Marine Freshwater Research 53: 769–775. https://doi.org/10.1071/mf01205

Neilson R. & Brown D.J. (1999). Feeding on different host plants alters the natural abundances of δ13C and δ15N in Longidoridae (Nemata). Journal of Nematology 31 (1): 20.

Parmentier E. & Das K. (2004). Commensal vs. parasitic relationship between Carapini fish and their hosts: some further insight through δ13C and δ15N measurements. Journal of Experimental Marine Biology and Ecology 310 (1): 47–58. https://doi.org/10.1016/j.jembe.2004.03.019

Parmentier E. & Michel L. (2013). Boundary lines in symbiosis forms. Symbiosis 60: 1–5. https://doi.org/10.1007/s13199-013-0236-0

Parnell A., Inger R., Bearhop S. & Jackson A.L. (2008). SIAR: Stable isotope analysis in R. Available from https://rdrr.io/cran/siar/ [accessed 24 Oct. 2019].

Phillips D.L. & Koch P.L. (2002). Incorporating concentration dependence in stable isotope mixing models. Oecologia 130 (1): 114–125.

Phillips D.L., Inger R., Bearhop S., Jackson A.L., Moore J.W., Parnell A.C., Semmens B.X. & Ward E.J. (2014). Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology 92 (10): 823–835. https://doi.org/10.1139/cjz-2014-0127

Pinnegar J.K., Campbell N. & Polunin N.V.C. (2001). Unusual stable isotope fractionation patterns observed for fish host—parasite trophic relationships. Journal of Fish Biology 59 (3): 494–503. https://doi.org/10.1111/j.1095-8649.2001.tb02355.x

Post D.M. (2002). Using stable isotope to estimate trophic position: models, methods, and assumptions. Ecology 83: 703–718. https://doi.org/10.2307/3071875

Power M. & Klein G.M. (2004). Fish host–cestode parasite stable isotope enrichment patterns in marine, estuarine and freshwater fishes from northern Canada. Isotopes in Environmental and Health Studies 40 (4): 257–266. https://doi.org/10.1080/10256010410001678062

R Development Core Team. (2015). R: A Language and Environment for Statistical Computing. Vienna, Austria. Available from http://www.R-project.org [accessed 24 Oct. 2019].

Raffel T.R., Martin L.B. & Rohr J.R. (2008). Parasites as predators: unifying natural enemy ecology. Trends in Ecology & Evolution 23 (11): 610–618. https://doi.org/10.1016/j.tree.2008.06.015

Richoux N.B. & Ndhlovu R.T. (2015). Temporal variability in the isotopic niches of rocky shore grazers and suspension feeders. Marine Ecology 36 (4): 1045–1059. https://doi.org/10.1111/maec.12200

Semmens B.X., Ward E.J., Moore J.W., Darimont C.T. (2009). Quantifying inter- and intra-population niche variability using hierarchical Bayesian stable isotope mixing models. PLoS ONE 4: e6187. https://doi.org/10.1371/journal.pone.0006187

Sih J. & Chouw J. (2009). Fish and whips: Use of gorgonians as a habitat by the large whipcoral goby, Bryaninops amplus (Larson). Raffles Bulletin of Zoology 22: 145–157.

Soule D.F. & Soule J.D. (1972). Ancestrulae and body wall morphogenesis of some Hawaiian and eastern Pacific Smittinidae (Bryozoa). Transactions of the American Microscopical Society 91: 251–260. https://doi.org/10.2307/3224873

Syväranta J., Lensu A., Markomäki T.J., Oksanen S. & Jones R.I. (2013). An empirical evaluation of the utility of convex hull and standard ellipse areas for assessing population niche widths from stable isotope data. PLoS ONE 8: 1–8. https://doi.org/10.1371/journal.pone.0056094

Terrana L. & Eeckhaut I. (2017). Taxonomic description and 3D modelling of a new species of myzostomid (Annelida, Myzostomida) associated with black corals from Madagascar. Zootaxa 4244 (2):277–295. https://doi.org/10.11646/zootaxa.4244.2.9

Terrana L., Caulier G., Todinanahary G., Lepoint G. & Eeckhaut I. (2016). Characteristics of the infestation of Seriatopora corals by the coral gall crab Hapalocarcinus marsupialis Stimpson, 1859 on the great reef of Toliara, Madagascar. Symbiosis 69 (2): 113–122. https://doi.org/10.1007%2Fs13199-016-0391-1

Vega R., Vega R. & Luque A.A. (2002). Coralliophila kaofitorum, a new species (Gastropoda: Coralliophilidae) from the Canary Islands living on Antipathes wollastoni (Cnidaria: Anthozoa: Antipatharia). Nautilus 116: 50–55.

Wagner D., Luck D.G. & Toonen R.J. (2012). The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63: 67–132. https://doi.org/10.1016/b978-0-12-394282-1.00002-8

Wirtz P. & d’Udekem-d’Acoz C. (2001). Decapoda from Antipatharia, Gorgonaria and Bivalvia at the Cape Verde Islands. Helgoland Marine Research 55: 112–115. https://doi.org/10.1007/s101520100073

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Published

2019-11-28

How to Cite

Terrana, L., Lepoint, G., & Eeckhaut, I. (2019). Assessing trophic relationships between shallow-water black corals (Antipatharia) and their symbionts using stable isotopes. Belgian Journal of Zoology, 149. https://doi.org/10.26496/bjz.2019.33

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