Abstract
In this study, we examined two non-scleractinian taxa, the rare nudibranch Phyllodesmium lizardensis and Bayerxenia sp., the octocoral on which the nudibranch lives and feeds, to investigate the effect of experimental heat stress on their symbioses with Symbiodinium. Bleaching has not been studied in nudibranchs. Bayerxenia sp. belongs to the alcyonacea family Xeniidae, members of which are known to be heat sensitive, but the genus has never been subject to heat stress experiments or bleaching observations. While qPCR did not reveal any changes to the symbiont community composition, the two host species responded differently to increased temperature. There were changes in the relative proportion of tissue types in Bayerxenia sp., but these were not attributable to the temperature treatment. Bayerxenia sp. exhibited no changes in cellular structure (apoptosis or cell necrosis), or symbiont functioning, cell size, density, or cladal community structure. On the other hand, the host, P. lizardensis, experienced tissue loss and symbiont densities decreased significantly with the majority of the remaining symbiont cells significantly degenerated after the heat stress. This decrease did not influence symbiont community composition, symbiont cell size, or photosynthetic efficiency. While the bleaching process in nudibranchs was demonstrated for the first time, the physiological and molecular pathways leading to this response still require attention.
References
Abrego D, Ulstrup KE, Willis BL, van Oppen MJH (2008) Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc Lond B Biol Sci 275:2273–2282
Addessi L (2001) Giant clam bleaching in the lagoon of Takapoto atoll (French Polynesia). Coral Reefs 19:220-220
Ainsworth TD, Hoegh-Guldberg O, Heron SF, Skirving WJ, Leggat W (2008) Early cellular changes are indicators of pre-bleaching thermal stress in the coral host. J Exp Mar Bio Ecol 364:63–71
Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand
Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc Lond B Biol Sci 273:2305–2312
Buck BH, Rosenthal H, Saint-Paul U (2002) Effect of increased irradiance and thermal stress on the symbiosis of Symbiodinium microadriaticum and Tridacna gigas. Aquat Living Resour 15:107–117
Burghardt I, Schrödl M, Wagele H (2008a) Three new solar-powered species of the genus Phyllodesmium Ehrenberg, 1831 (Mollusca : Nudibranchia : Aeolidioidea) from the tropical Indo-Pacific, with analysis of their photosynthetic activity and notes on biology. J Molluscan Stud 74:277–292
Burghardt I, Stemmer K, Wagele H (2008b) Symbiosis between Symbiodinium (Dinophyceae) and various taxa of Nudibranchia (Mollusca : Gastropoda), with analyses of long-term retention. Org Divers Evol 8:66–76
Castillo KD, Helmuth BST (2005) Influence of thermal history on the response of Montastraea annularis to short-term temperature exposure. Mar Biol 148:261–270
Clarke K, Gorley R (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, UK
Drohan AF, Thoney DA, Baker AC (2005) Synergistic effect of high temperature and ultraviolet-B radiation on the gorgonian Eunicea tourneforti (Octocorallia : Alcyonacea : Plexauridae). Bull Mar Sci 77:257–266
Dunn SR, Thomason JC, Le Tissier MDA, Bythell JC (2004) Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell Death Differ 11:1213–1222
Dunn SR, Bythell JC, Le Tissier MDA, Burnett WJ, Thomason JC (2002) Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J Exp Mar Bio Ecol 272:29–53
Elias H, Hyde DM (1980) An elementary introduction to stereology (quantitative microscopy). Am J Anat 159:411–446
Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65
FitzPatrick S, Liberatore K, Garcia J, Burghardt I, Colman D, Moquin S, Takacs-Vesbach C, Shepherd U (2012) Symbiodinium diversity in the soft coral Heteroxenia sp. and its nudibranch predator Phyllodesmium lizardensis. Coral Reefs 31:895–905
Fromont J, Garson M (1999) Sponge bleaching on the West and East coasts of Australia. Coral Reefs 18:340-340
Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biol Bull 182:324–332
Gilbert JA, Hill R, Doblin MA, Ralph PJ (2012) Microbial consortia increase thermal tolerance of corals. Mar Biol 159:1763–1771
Glynn PW (1996) Coral reef bleaching: Facts, hypotheses and implications. Glob Chang Biol 2:495–509
Goulet TL, Coffroth MA (2003) Stability of an octocoral-algal symbiosis over time and space. Mar Ecol Prog Ser 250:117–124
Goulet TL, Cook CB, Goulet D (2005) Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallida/ Symbiodinium symbiosis. Limnol Oceanogr 50:1490–1498
Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89:10302–10305
Jimenez IM, Kuhl M, Larkum AWD, Ralph PJ (2011) Effects of flow and colony morphology on the thermal boundary layer of corals. J R Soc Interface 8:1785–1795
Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32:1259–1269
Kuguru B, Winters G, Beer S, Santos SR, Chadwick NE (2007) Adaptation strategies of the corallimorpharian Rhodactis rhodostoma to irradiance and temperature. Mar Biol 151:1287–1298
LaJeunesse TC (2001) Investigating the biodiversity, ecology and phylogeny of endosymbiontic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880
LaJeunesse TC, Smith R, Walther M, Pinzon J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magana AL, Perez AL, Reyes-Bonilla H, Warner ME (2010) Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc R Soc Lond B Biol Sci 277:2925–2934
Loram JE, Boonham N, O’Toole P, Trapido-Rosenthal HG, Douglas AE (2007) Molecular quantification of symbiotic dinoflagellate algae of the genus Symbiodinium. Biol Bull 212:259–268
Magalon H, Flot JF, Baudry E (2007) Molecular identification of symbiotic dinoflagellates in Pacific corals in the genus Pocillopora. Coral Reefs 26:551–558
Mayfield AB, Hirst MB, Gates RD (2009) Gene expression normalization in a dual-compartment system: a real-time quantitative polymerase chain reaction protocol for symbiotic anthozoans. Mol Ecol Resour 9:462–470
Mieog JC, van Oppen MJH, Cantin NE, Stam WT, Olsen JL (2007) Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs 26:449–457
Mouillot D, Bellwood DR, Baraloto C, Chave J, Galzin R, Harmelin-Vivien M, Kulbicki M, Lavergne S, Lavorel S, Mouquet N, Paine CET, Renaud J, Thuiller W (2013) Rare Species Support Vulnerable Functions in High-Diversity Ecosystems. PLoS Biol 11:e1001569
Muller-Parker G, Pierce-Cravens J, Bingham BL (2007) Broad thermal tolerance of the symbiotic dinoflagellate Symbiodinium muscatinei (Dinophyta) in the sea anemone Anthopleura elegantissima (Cnidaria) from northern latitudes. J Phycol 43:25–31
Oliver TA, Palumbi SR (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440
Palmer CV, Bythell JC, Willis BL (2012) Enzyme activity demonstrates multiple pathways of innate immunity in Indo-Pacific anthozoans. Proc R Soc Lond B Biol Sci 279:3879–3887
Reinicke GB (1995) Xeniidae des Roten Meeres (Octocorallia, Alcyonacea)—Beiträge zur Systematik und Ökologie. Essener Ökologische Schriften 6:1–168
Rowan R (2004) Coral bleaching - thermal adaptation in reef coral symbionts. Nature 430:742-742
Sabourault C, Ganot P, Moya A, Furla P (2012) Endosymbiosis drives transcriptomic adjustments and genomic adaptations in cnidarians. Proc 12th Int Coral Reef Symp 7A_1
Santos SR, Taylor DJ, Kinzie RA, Hidaka M, Sakai K, Coffroth MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–111
Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts - symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8:23–43
Stimson J, Sakai K, Sembali H (2002) Interspecific comparison of the symbiotic relationship in corals with high and low rates of bleaching-induced mortality. Coral Reefs 21:409–421
Strychar KB, Coates M, Sammarco PW, Piva TJ, Scott PT (2005) Loss of Symbiodinium from bleached soft corals Sarcophyton ehrenbergi, Sinularia sp. and Xenia sp. J Exp Mar Bio Ecol 320:159–177
Thornhill D, LaJeunesse TC, Santos CR (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 16:5326–5340
Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722
Uthicke S, Vogel N, Doyle J, Schmidt C, Humphrey C (2012) Interactive effects of climate change and eutrophication on the dinoflagellate-bearing benthic foraminifer Marginopora vertebralis. Coral Reefs 31:401–414
van Oppen MJH, Mieog JC, Sanchez CA, Fabricus KE (2005) Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol Ecol 14:2403–3484
Vicente VP (1990) Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral Reefs 8:199–202
Waegele H, Vonnemann V, Waegele JW (2003) Towards a phylogeny of the Opisthobranchia. In: Lydeard C, Lindberg D (eds) Molecular systematics and phylogeography of mollusks. Smithsonian Institution Press, Washington, DC, pp 185–228
Ziegler M, Uthicke S (2011) Photosynthetic plasticity of endosymbionts in larger benthic coral reef Foraminifera. J Exp Mar Bio Ecol 407:70–80
Acknowledgments
We wish to thank S. Perry, J. Schmieder (Bonn) for support with histological analyses and T. Alpermann (Frankfurt) for advice on interpretation of qPCR data. We are grateful to Lizard Island Research Station staff and for assistance with field work by C. Carrasco and S. Moquin. The trip to Lizard Island was funded by the German National Academic Foundation (M.Z.). The molecular work was funded by a NSF Grant (ID0436605), a NIH Post-Baccalaureate Research Education Grant (K.L.L.) (R25GM075149), a UNM Research Allocations grant, an anonymous donation to the UNM Biology Department, and NIH Grant 1P20RR18754 to UNM’s Molecular Biology Facility. We thank the editor and anonymous reviewers for their thoughtful comments that helped to improve the manuscript.
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Ziegler, M., FitzPatrick, S.K., Burghardt, I. et al. Thermal stress response in a dinoflagellate-bearing nudibranch and the octocoral on which it feeds. Coral Reefs 33, 1085–1099 (2014). https://doi.org/10.1007/s00338-014-1204-8
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DOI: https://doi.org/10.1007/s00338-014-1204-8