[en] Scrutinizing the traits of octocorals that could affect their physiological performance becomes increasingly important as several of these species are observed to become dominant on reefs pressured by the Anthropocene. In the present study, we compare the organismal traits of two branching octocorals Litophyton sp. and Stereonephthya sp. commonly populating in sympatry the high-latitude coral communities of northern Taiwan. Using 13 traits, we describe and compare performance traits in these two symbiotic species that we discuss in light of the association they maintain with their algal partners. Litophyton sp. and Stereonephthya sp. hosted Durusdinium and Gerakladium, respectively. Both genera represent singular associations, with the latter further establishing the first solid report of Gerakladium in octocorals. Traits distinguished two groups explained by the two partnerships considered. Litophyton sp. associated with Durusdinium had significantly higher organic matter, chlorophyll (chl) a, total lipid and lower chl c/chl a ratio than Stereonephthya sp. associated with Gerakladium. The δ15N in the host and algae, as well as δ13C in the host were also higher in Litophyton species. Although no significant difference was observed in the δ13C of the algae, Litophyton sp. presented a significantly higher variance for this trait and for chl a content than Stereonephthya species. Altogether, the traits examined suggested contrasting performances among the two octocorals. Both octocoral species clearly deviate from an autotrophic diet. Litophyton sp. appears to complement its heterotrophic diet with photosynthetically acquired energy, while Stereonephthya sp. tends to be more specialized and benefits relatively little from its symbiotic relationship. Our study calls for greater consideration of the individual variation in octocoral physiology and in the definition of their ecological strategies.
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Aharonovich D., Benayahu Y., (2012). Microstructure of octocoral sclerites for diagnosis of taxonomic features. Mar. Biodivers. 42 173–177. 10.1007/s12526-011-0102-103
Aurelle D., Pivotto I. D., Malfant M., Topçu N. E., Masmoudi M. B., Chaoui L., et al. (2017). Fuzzy species limits in Mediterranean gorgonians (Cnidaria, Octocorallia): inferences on speciation processes. Zool. Scripta 46 767–778. 10.1111/zsc.12245
Baker D. M., Freeman C. J., Knowlton N., Thacker R. W., Kim K., Fogel M. L., (2015). Productivity links morphology, symbiont specificity and bleaching in the evolution of Caribbean octocoral symbioses. ISME J. 9 2620–2629. 10.1038/ismej.2015.71 25989369
Baker D. M., Webster K. L., Kim K., (2010). Caribbean octocorals record changing carbon and nitrogen sources from 1862 to 2005. Global Change Biol. 16 2701–2710. 10.1111/j.1365-2486.2010.02167.x
Bănaru D., Carlotti F., Barani A., Grégori G., Neffati N., Harmelin-Vivien M., (2013). Seasonal variation of stable isotope ratios of size-fractionated zooplankton in the Bay of Marseille (NW Mediterranean Sea). J. Plankton Res. 36 145–156. 10.1093/plankt/fbt083 32665766
Barneah O., Weis V. M., Perez S., Benayahu Y., (2004). Diversity of dinoflagellate symbionts in red sea soft corals: mode of symbiont acquisition matters. Mar. Ecol. Prog. Ser. 275 89–95. 10.3354/meps275089
Bednarz V. N., Cardini U., van Hoytema N., Al-Rshaidat M. M. D., Wild C., (2015). Seasonal variation in dinitrogen fixation and oxygen fluxes associated with two dominant zooxanthellate soft corals from the northern Red Sea. Mar. Ecol. Prog. Ser. 519 141–152. 10.3354/meps11091
Bellwood D. R., Streit R. P., Brandl S. J., Tebbett S. B., (2018). The meaning of the term ‘function’ in ecology: a coral reef perspective. Funct. Ecol. 33 948–961. 10.1111/1365-2435.13265
Ben-David-Zaslow R., Benayahu Y., (1999). Temporal variation in lipid, protein and carbohydrate content in the Red Sea soft coral Heteroxenia fuscescens. J. Mar. Biol. Assoc. U K. 79 1001–1006. 10.1017/s002531549900123x
Berner T., Achituv Y., Dubinsky Z., Benayahu Y., (1987). Pattern of distribution and adaptation to different irradiance levels of zooxanthellae in the soft coral Litophyton arboreum (Octocorallia, Alcyonacea). Symbiosis 3 23–39.
Bo M., Baker A. C., Gaino E., Wirshing H. H., Scoccia F., Bavestrello G., (2011). First description of algal mutualistic endosymbiosis in a black coral (Anthozoa: Antipatharia). Mar. Ecol. Prog. Ser. 435 1–11. 10.3354/meps09228
Bodin N., Le Loc’h F., Hily C., (2007). Effect of lipid removal on carbon and nitrogen stable isotope ratios in crustacean tissues. J. Exp. Mar. Biol. Ecol. 341 168–175. 10.1016/j.jembe.2006.09.008
Cocito S., Ferrier-Pagès C., Cupido R., Rottier C., Meier-Augenstein W., Kemp H., et al. (2013). Nutrient acquisition in four Mediterranean gorgonian species. Mar. Ecol. Prog. Ser. 473 179–188. 10.3354/meps10037
Coma R., Llorente-Llurba E., Serrano E., Gili J.-M., Ribes M., (2015). Natural heterotrophic feeding by a temperate octocoral with symbiotic zooxanthellae: a contribution to understanding the mechanisms of die-off events. Coral Reefs 34 549–560. 10.1007/s00338-015-1281-1283
Coma R., Ribes M., Gili J.-M., Zabala M., (1998). An energetic approach to the study of life-history traits of two modular colonial benthic invertebrates. Mar. Ecol. Prog. Ser. 162 89–103. 10.3354/meps162089
Coplen T. B., (2011). Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun. Mass. Spectrom 25 2538–2560. 10.1002/rcm.5129 21910288
Coppari M., Zanella C., Rossi S., (2019). The importance of coastal gorgonians in the blue carbon budget. Sci. Rep. 9:13550. 10.1038/s41598-019-49797-49794
Courtial L., Planas Bielsa V., Houlbreque F., Ferrier-Pages C., (2018). Effects of ultraviolet radiation and nutrient level on the physiological response and organic matter release of the scleractinian coral Pocillopora damicornis following thermal stress. PLoS One 13:e0205261. 10.1371/journal.pone.0205261 30356284
Denis V., Soto D., De Palmas S., Lin Y. T. V., Benayahu Y., Huang Y. M., et al. (2019). “Taiwan,” in Mesophotic Coral Ecosystems, eds Loya Y., Puglise K. A., Bridge T. C. L., (Cham: Springer International Publishing), 249–264. 10.1007/978-3-319-92735-0_14
Dubinsky Z., Falkowski P. G., Porter J. W., Muscatine L., Smith D. C., (1984). Absorption and utilization of radiant energy by light- and shade-adapted colonies of the hermatypic coral Stylophora pistillata. Proc. Royal Soc. Lond. Ser. B. Biol. Sci. 222 203–214. 10.1098/rspb.1984.0059
Etnoyer P., Warrenchuk J., (2007). A catshark nursery in a deep gorgonian field in the Mississippi Canyon, Gulf of Mexico. Bull. Mar. Sci. 81 553–559.
Ezzat L., Fine M., Maguer J.-F., Grover R., Ferrier-Pagès C., (2017). Carbon and nitrogen acquisition in shallow and deep holobionts of the scleractinian coral S. pistillata. Front. Mar. Sci. 4:102. 10.3389/fmars.2017.00102
Fabricius K., Alderslade P., (2001). Soft Corals and Sea Fans: A Comprehensive Guide to the Tropical Shallow Water Genera of the Central-west Pacific, the Indian Ocean and the Red Sea. Townsville, TSV: AIMS.
Falkowski P. G., Dubinsky Z., (1981). Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289 172–174. 10.1038/289172a0
Ferrier-Pagès C., Peirano A., Abbate M., Cocito S., Negri A., Rottier C., et al. (2011). Summer autotrophy and winter heterotrophy in the temperate symbiotic coral Cladocora caespitosa. Limnol. Oceanog. 56 1429–1438. 10.4319/lo.2011.56.4.1429
Folch J., Lees M., Sloane Stanley G. H., (1957). A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226 497–509.
Fox M. D., Williams G. J., Johnson M. D., Radice V. Z., Zgliczynski B. J., Kelly E. L. A., et al. (2018). Gradients in primary production predict trophic strategies of Mixotrophic corals across spatial scales. Curr. Biol. 28 3355–3363.e4. 10.1016/j.cub.2018.08.057 30344114
Gerhart D. J., (1990). Fouling and gastropod predation: consequences of grazing for a tropical octocoral. Mar. Ecol. Prog. Ser. 62 103–108. 10.3354/meps062103
Gerz M., Guillermo Bueno C., Ozinga W. A., Zobel M., Moora M., van der Heijden M., (2018). Niche differentiation and expansion of plant species are associated with mycorrhizal symbiosis. J. Ecol. 106 254–264. 10.1111/1365-2745.12873
Gori A., Viladrich N., Gili J. M., Kotta M., Cucio C., Magni L., et al. (2012). Reproductive cycle and trophic ecology in deep versus shallow populations of the Mediterranean gorgonian Eunicella singularis (Cap de Creus, northwestern Mediterranean Sea). Coral Reefs 31 823–837. 10.1007/s00338-012-0904-901
Hill M., Allenby A., Ramsby B., Schonberg C., Hill A., (2011). Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: evidence of heteroplasmy and putative host-specific symbiont lineages. Mol. Phylogenet. Evol. 59 81–88. 10.1016/j.ympev.2011.01.006 21256238
Hughes T. P., Kerry J. T., Baird A. H., Connolly S. R., Dietzel A., Eakin C. M., et al. (2018). Global warming transforms coral reef assemblages. Nature 556 492–496. 10.1038/s41586-018-0041-42
Jeffrey S. W., Humphrey G. F., (1975). New spectrophotometric equations for determining chlorophyll a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochemie und Physiol. der Pflanzen 167 191–194. 10.1016/s0015-3796(17)30778-3
Jeng M. S., Huang H. D., Dai C. F., Hsiao Y. C., Benayahu Y., (2011). Sclerite calcification and reef-building in the fleshy octocoral genus Sinularia (Octocorallia: Alcyonacea). Coral Reefs 30 925–933. 10.1007/s00338-011-0765-z
Kaiser P., Schlichter D., Fricke H. W., (1993). Influence of light on algal symbionts of the deep water coral Leptoseris fragilis. Mar. Biol. 117 45–52. 10.1007/BF00346424
Kearney M., Simpson S. J., Raubenheimer D., Helmuth B., (2010). Modelling the ecological niche from functional traits. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365 3469–3483. 10.1098/rstb.2010.0034 20921046
Khalesi M. K., Beeftink H. H., Wijffels R. H., (2009). Light-dependency of growth and secondary metabolite production in the captive zooxanthellate soft coral Sinularia flexibilis. Mar. Biotechnol. (NY) 11 488–494. 10.1007/s10126-008-9164-z 19048343
LaJeunesse T. C., Parkinson J. E., Gabrielson P. W., Jeong H. J., Reimer J. D., Voolstra C. R., et al. (2018). Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28 2570–2580. 10.1016/j.cub.2018.07.008 30100341
Lesser M. P., Stat M., Gates R. D., (2013). The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs 32 603–611. 10.1007/s00338-013-1051-z
Lin Y. T. V., Denis V., (2019). Acknowledging differences: number, characteristics, and distribution of marine benthic communities along Taiwan coast. Ecosphere 10:e02803. 10.1002/ecs2.2803
Mass T., Kline D. I., Roopin M., Veal C. J., Cohen S., Iluz D., et al. (2010). The spectral quality of light is a key driver of photosynthesis and photoadaptation in Stylophora pistillata colonies from different depths in the Red Sea. J. Exp. Biol. 213 4084–4091. 10.1242/jeb.039891 21075950
McFadden C. S., Benayahu Y., Pante E., Thoma J. N., Nevarez P. A., France S. C., (2011). Limitations of mitochondrial gene barcoding in Octocorallia. Mol. Ecol. Resour. 11 19–31. 10.1111/j.1755-0998.2010.02875.x 21429097
McFadden C. S., France S. C., Sanchez J. A., Alderslade P., (2006). A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Mol. Phylogenet. Evol. 41 513–527. 10.1016/j.ympev.2006.06.010 16876445
McWilliam M., Hoogenboom M. O., Baird A. H., Kuo C. Y., Madin J. S., Hughes T. P., (2018). Biogeographical disparity in the functional diversity and redundancy of corals. Proc. Natl. Acad. Sci. U S A. 115 3084–3089. 10.1073/pnas.1716643115 29507193
Muscatine L., Porter J. W., Kaplan I. R., (1989). Resource partitioning by reef corals as determined from stable isotope composition. I. δ13C of zooxanthellae and animal tissue vs depth. Mar. Biol. 100 185–193. 10.1007/Bf00391957
Nir O., Gruber D. F., Einbinder S., Kark S., Tchernov D., (2011). Changes in scleractinian coral Seriatopora hystrix morphology and its endocellular Symbiodinium characteristics along a bathymetric gradient from shallow to mesophotic reef. Coral Reefs 30 1089–1100. 10.1007/s00338-011-0801-z
Noda H., Parkinson J. E., Yang S. Y., Reimer J. D., (2017). A preliminary survey of zoantharian endosymbionts shows high genetic variation over small geographic scales on Okinawa-jima Island, Japan. PeerJ 5:e3740. 10.7717/peerj.3740 29018596
O’Neal W., Pawlik J. R., (2002). A reappraisal of the chemical and physical defenses of Caribbean gorgonian corals against predatory fishes. Mar. Ecol. Prog. Ser. 240 117–126. 10.3354/meps240117
Pochon X., Pawlowski J., Zaninetti L., Rowan R., (2001). High genetic diversity and relative specificity among symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar. Biol. 139 1069–1078. 10.1007/s002270100674
Pupier C. A., Bednarz V. N., Ferrier-Pagès C., (2018). Studies with soft corals – recommendations on sample processing and normalization metrics. Front. Mar. Sci. 5:348. 10.3389/fmars.2018.00348
Pupier C. A., Fine M., Bednarz V. N., Rottier C., Grover R., Ferrier-Pages C., (2019). Productivity and carbon fluxes depend on species and symbiont density in soft coral symbioses. Sci. Rep. 9:17819. 10.1038/s41598-019-54209-54208
R Core Team (2019). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
Ramsby B. D., Shirur K. P., Iglesias-Prieto R., Goulet T. L., (2014). Symbiodinium photosynthesis in Caribbean octocorals. PLoS One 9:e106419. 10.1371/journal.pone.0106419 25192405
Reijnen B. T., van der Meij S. E., van Ofwegen L. P., (2011). Fish, fans and hydroids: host species of pygmy seahorses. Zookeys 103 1–26. 10.3897/zookeys.103.953 21747677
Reynolds J. M., Bruns B. U., Fitt W. K., Schmidt G. W., (2008). Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc. Natl. Acad. Sci. U S A. 105 13674–13678. 10.1073/pnas.0805187105 18757737
Ribes M., Coma R., Gili J.-M., (1998). Heterotrophic feeding by gorgonian corals with symbiotic zooxanthella. Limnol. Oceanog. 43 1170–1179. 10.4319/lo.1998.43.6.1170
Rossi S., Coppari M., Viladrich N., (2017). “Benthic-Pelagic coupling: new perspectives in the animal forests,” in Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots, eds Rossi S., Bramanti L., Gori A., Orejas C., (Cham: Springer International Publishing), 855–885. 10.1007/978-3-319-21012-4_23
Rossi S., Gili J.-M., Coma R., Linares C., Gori A., Vert N., (2006). Temporal variation in protein, carbohydrate, and lipid concentrations in Paramuricea clavata (Anthozoa, Octocorallia): evidence for summer–autumn feeding constraints. Mar. Biol. 149 643–651. 10.1007/s00227-005-0229-225
Rossi S., Schubert N., Brown D., Gonzalez-Posada A., Soares M. O., (2020). Trophic ecology of Caribbean octocorals: autotrophic and heterotrophic seasonal trends. Coral Reefs 39 433–449. 10.1007/s00338-020-01906-w
Rossi S., Schubert N., Brown D., Soares M. O., Grosso V., Rangel-Huerta E., et al. (2018). Linking host morphology and symbiont performance in octocorals. Sci. Rep. 8:12823. 10.1038/s41598-018-31262-31263
Sánchez J. A., (2016). “Diversity and evolution of octocoral animal forests at both sides of tropical America,” in Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots, eds Rossi S., Bramanti L., Gori A., Orejas C., (Cham: Springer International Publishing), 1–33. 10.1007/978-3-319-17001-5_39-1 33311142
Scheufen T., Kramer W. E., Iglesias-Prieto R., Enriquez S., (2017). Seasonal variation modulates coral sensibility to heat-stress and explains annual changes in coral productivity. Sci. Rep. 7:4937. 10.1038/s41598-017-04927-4928
Schlichter D., Svoboda A., Kremer B. P., (1983). Functional autotrophy of Heteroxenia fuscescens (Anthozoa: Alcyonaria): carbon assimilation and translocation of photosynthates from symbionts to host. Mar. Biol. 78 29–38. 10.1007/BF00392968
Schubert N., Brown D., Rossi S., (2017). “Symbiotic versus non-symbiotic octocorals: physiological and ecological implications,” in Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots, eds Rossi S., Bramanti L., Gori A., Orejas C., (Cham: Springer International Publishing), 887–918. 10.1007/978-3-319-21012-4_54
Slattery M., Pankey M. S., Lesser M. P., (2019). Annual thermal stress increases a soft coral’s susceptibility to bleaching. Sci. Rep. 9:8064. 10.1038/s41598-019-44566-44569
Sorokin Y., (1991). Biomass, metabolic rates and feeding of some common reef zoantharians and octocorals. Aus. J. Mar. Freshwater Res. 42 729–741. 10.1071/MF9910729
Sturaro N., Hsieh Y. E., Chen Q., Wang P. L., Denis V., (2020). Toward a standardised protocol for the stable isotope analysis of scleractinian corals. Rapid Commun. Mass Spectrom. 34:e8663. 10.1002/rcm.8663 31802564
van Ofwegen L., (2016). The genus litophyton forskål, 1775 (Octocorallia, Alcyonacea, Nephtheidae) in the Red Sea and the western Indian Ocean. ZooKeys 567 1–128. 10.3897/zookeys.567.7212 27103869
Van Oppen M. J., Mieog J. C., Sanchez C. A., Fabricius K. E., (2005). Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol. Ecol. 14 2403–2417. 10.1111/j.1365-294X.2005.02545.x 15969723
Vercelloni J., Liquet B., Kennedy E. V., Gonzalez-Rivero M., Caley M. J., Peterson E. E., et al. (2020). Forecasting intensifying disturbance effects on coral reefs. Glob. Chang Biol. 26 2785–2797. 10.1111/gcb.15059 32115808
Violle C., Enquist B. J., McGill B. J., Jiang L., Albert C. H., Hulshof C., et al. (2012). The return of the variance: intraspecific variability in community ecology. Trends Ecol. Evol. 27 244–252. 10.1016/j.tree.2011.11.014 22244797
Violle C., Navas M.-L., Vile D., Kazakou E., Fortunel C., Hummel I., et al. (2007). Let the concept of trait be functional! Oikos. Oikos 116 882–892. 10.1111/j.0030-1299.2007.15559.x
Wheeler D. A., Srinivasan M., Egholm M., Shen Y., Chen L., McGuire A., et al. (2008). The complete genome of an individual by massively parallel DNA sequencing. Nature 452 872–876. 10.1038/nature06884 18421352
Williams G., Delbeek J., Shepherd B., Wolters S., (2010). Zooxanthellae in Ellisellid gorgonians of the philippines. Proc. Calif. Acad. Sci. 61 647–648.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.
