Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Photobiology of the zoanthid Zoanthus sociatus in intertidal and subtidal habitats

Miguel C. Leal A F , Igor C. S. Cruz B , Carlos R. Mendes C , Ricardo Calado A , Ruy K. P. Kikuchi D , Rui Rosa E , Amadeu M. V. M. Soares A , João Serôdio A and Rui J. M. Rocha A
+ Author Affiliations
- Author Affiliations

A Departamento de Biologia and CESAM, Universidade de Aveiro, Campus Universitário de Santiago, PT-3810-193 Aveiro, Portugal.

B Programa de Pós-Graduação em Ecologia e Evolução, Universidade do Estado do Rio de Janeiro (UERJ), Rio de Janeiro, RJ, Brazil.

C Instituto de Oceanografia, Universidade Federal do Rio Grande (FURG), Avenida Itália, quilômetro 8, Rio Grande, RS, 96203-900, Brazil.

D Departamento de Oceanografia Universidade Federal da Bahia (UFBA) and INCT AmbTropic, Salvador, Brazil.

E MARE – Marine and Environmental Sciences Centre, Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa, Avenida Nossa Senhora do Cabo, 939, PT-2750-374 Cascais, Portugal.

F Corresponding author. Present address: Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, Seestrasse 79, CH-6047 Kastanienbaum, Switzerland. Email: miguelcleal@gmail.com

Marine and Freshwater Research 67(12) 1991-1997 https://doi.org/10.1071/MF15300
Submitted: 14 January 2015  Accepted: 15 September 2015   Published: 10 December 2015

Abstract

Intertidal environments are boundaries between marine and terrestrial ecosystems that are subject to rapid fluctuations across tidal cycles. This study investigates, for the first time, the photobiology of symbiotic zoanthids inhabiting different tidal environments: subtidal, intertidal pools and intertidal areas exposed to air during low tide. More specifically, we assessed the photochemical efficiency, Symbiodinium density and photosynthetic pigments profile of Zoanthus sociatus during low tide. Photochemical efficiency was lower and cell density higher in air exposed zoanthids. The profile of photosynthetic pigments also varied significantly among tidal habitats, particularly photoprotective pigments such as dinoxanthin and diadinoxanthin. Differences were also observed for the pigment content per cell, but the proportion of particular pigments (peridinin/chlorophyll-a and diatoxanthin+diadinoxanthin/chlorophyll-a) remained stable. Results suggest that aerial exposure conditions induce reversible downregulation of photochemical processes but no photophysiological impairment or bleaching. These findings provide a baseline for future studies addressing the prevalence of these overlooked cnidarians in environmentally dynamic reef flats.

Additional keywords: aerial exposure, chlorophyll fluorescence, photosynthetic pigments, Symbiodinium, tidal pool.


References

Bingham, B. L., Freytes, I., Emery, M., Dimond, J., and Muller-Parker, G. (2011). Aerial exposure and body temperature of the intertidal sea anemone Anthopleura elegantissima. Invertebrate Biology 130, 291–301.
Aerial exposure and body temperature of the intertidal sea anemone Anthopleura elegantissima.Crossref | GoogleScholarGoogle Scholar |

Brown, B. E., Dunne, R. P., Scoffin, T. P., and Le Tissier, M. D. A. (1994). Solar damage in intertidal corals. Marine Ecology Progress Series 105, 219–230.
Solar damage in intertidal corals.Crossref | GoogleScholarGoogle Scholar |

Brown, B., Ambarsari, I., Warner, M., Fitt, W., Dunne, R., Gibb, S., and Cummings, D. (1999). Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18, 99–105.
Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection.Crossref | GoogleScholarGoogle Scholar |

Brown, B. E., Downs, C. A., Dunne, R. P., and Gibb, S. W. (2002). Preliminary evidence for tissue retraction as a factor in photoprotection of corals incapable of xanthophyll cycling. Journal of Experimental Marine Biology and Ecology 277, 129–144.
Preliminary evidence for tissue retraction as a factor in photoprotection of corals incapable of xanthophyll cycling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xot1Wht70%3D&md5=6d70bf2495d51c1ddfd4609b84e10a0dCAS |

Clarke, K., and Gorley, R. (2006). ‘PRIMER v6: User Manual/Tutorial.’ (PRIMER-E: Plymouth.)

Cruz, I. C. S., Kikuchi, R. K. P., Longo, L. L., and Creed, J. C. (2015). Evidence of a phase shift to Epizoanthus gabrieli Carlgreen, 1951 (Order Zoanthidea) and loss of coral cover on reefs in the Southwest Atlantic. Marine Ecology 36, 318–325.
Evidence of a phase shift to Epizoanthus gabrieli Carlgreen, 1951 (Order Zoanthidea) and loss of coral cover on reefs in the Southwest Atlantic.Crossref | GoogleScholarGoogle Scholar |

Done, T. J. (1999). Coral community adaptability to environmental change at the scales of regions, reefs and reef zones. American Zoologist 39, 66–79.
Coral community adaptability to environmental change at the scales of regions, reefs and reef zones.Crossref | GoogleScholarGoogle Scholar |

Eakin, C. M., and Glynn, P. W. (1996). Low tidal exposures and reef mortalities in the eastern Pacific. Coral Reefs 15, 120.
Low tidal exposures and reef mortalities in the eastern Pacific.Crossref | GoogleScholarGoogle Scholar |

Fadlallah, Y. H., Allen, K. W., and Estudillo, R. A. (1995). Mortality of shallow reef corals in the western Arabian Gulf following aerial exposure in winter. Coral Reefs 14, 99–107.
Mortality of shallow reef corals in the western Arabian Gulf following aerial exposure in winter.Crossref | GoogleScholarGoogle Scholar |

Fitt, W., Brown, B., Warner, M., and Dunne, R. (2001). Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20, 51–65.
Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals.Crossref | GoogleScholarGoogle Scholar |

Goericke, R., and Welschmeyer, N. (1992). Pigment turnover in the marine diatom Thalassiosira weissflogii: 1. The 14CO2-labelling kinetics of chlorophyll-a. Journal of Phycology 28, 498–507.
Pigment turnover in the marine diatom Thalassiosira weissflogii: 1. The 14CO2-labelling kinetics of chlorophyll-a.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXjsF2ksQ%3D%3D&md5=93283cb240e7eb144d5be34d8003e88cCAS |

Hibino, Y., Todd, P., Ashworth, C. D., Obuchi, M., and Reimer, J. D. (2013). Monitoring colony colour and zooxanthellae (Symbiodinium spp.) condition in the reef zoanthid Palythoa tuberculosain Okinawa, Japan. Marine Biology Research 9, 794–801.
Monitoring colony colour and zooxanthellae (Symbiodinium spp.) condition in the reef zoanthid Palythoa tuberculosain Okinawa, Japan.Crossref | GoogleScholarGoogle Scholar |

Hill, R. (2013). Evidence of light-induced phenotypic plasticity in zoanthids: editorial comment on the feature article by Wei et al. Marine Biology 160, 1051.
Evidence of light-induced phenotypic plasticity in zoanthids: editorial comment on the feature article by Wei et al.Crossref | GoogleScholarGoogle Scholar |

Hoegh-Guldberg, O., and Jones, R. (1999). Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Marine Ecology Progress Series 183, 73–86.
Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals.Crossref | GoogleScholarGoogle Scholar |

Hughes, T. P., Graham, N. A. J., Jackson, J. B. C., Mumby, P. J., and Steneck, R. S. (2010). Rising to the challenge of sustaining coral reef resilience. Trends in Ecology & Evolution 25, 633–642.
Rising to the challenge of sustaining coral reef resilience.Crossref | GoogleScholarGoogle Scholar |

Kaiser, M. J., Attrill, M. J., Jennings, S., Thomas, D. N., Barnes, D. K. A., Brierley, A. S., Hiddink, J. G., Kaartokallio, H., Polunin, N. V. C., and Raffaelli, D. G. (2011). ‘Marine Ecology: Processes, Systems, and Impacts.’ (Oxford University Press: Oxford, UK.)

Kamezaki, M., Higa, M., Hirose, M., Suda, S., and Reimer, J. D. (2013). Different zooxanthellae types in populations of the zoanthid Zoanthus sansibaricus along depth gradients in Okinawa, Japan. Marine Biodiversity 43, 61–70.
Different zooxanthellae types in populations of the zoanthid Zoanthus sansibaricus along depth gradients in Okinawa, Japan.Crossref | GoogleScholarGoogle Scholar |

Karlson, R. H. (1988). Size-dependent growth in two zoanthid species: a contrast in clonal strategies. Ecology 69, 1219–1232.
Size-dependent growth in two zoanthid species: a contrast in clonal strategies.Crossref | GoogleScholarGoogle Scholar |

Kemp, D. W., Cook, C. B., Lajeunesse, T. C., and Brooks, W. R. (2006). A comparison of the thermal bleaching responses of the zoanthid Palythoa caribaeorum from three geographically different regions in south Florida. Journal of Experimental Marine Biology and Ecology 335, 266–276.
A comparison of the thermal bleaching responses of the zoanthid Palythoa caribaeorum from three geographically different regions in south Florida.Crossref | GoogleScholarGoogle Scholar |

Kuguru, B., Achituv, Y., Gruber, D. F., and Tchernov, D. (2010). Photoacclimation mechanisms of corallimorpharians on coral reefs: photosynthetic parameters of zooxanthellae and host cellular responses to variation in irradiance. Journal of Experimental Marine Biology and Ecology 394, 53–62.
Photoacclimation mechanisms of corallimorpharians on coral reefs: photosynthetic parameters of zooxanthellae and host cellular responses to variation in irradiance.Crossref | GoogleScholarGoogle Scholar |

LaJeunesse, T. (2002). Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology 141, 387–400.
Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs.Crossref | GoogleScholarGoogle Scholar |

Leal, M. C., Jesus, B., Ezequiel, J., Calado, R., Rocha, R. J. M., Cartaxana, P., and Serôdio, J. (2015a). Concurrent imaging of chlorophyll fluorescence, chlorophyll-a content and green fluorescent proteins-like proteins of symbiotic cnidarians. Marine Ecology 36, 572–584.
Concurrent imaging of chlorophyll fluorescence, chlorophyll-a content and green fluorescent proteins-like proteins of symbiotic cnidarians.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1yhs7jO&md5=516b94fdb2e1f2866bc1d04809b7e645CAS |

Leal, M. C., Hoadley, K., Pettay, D. T., Grajales, A., Calado, R., and Warner, M. E. (2015b). Symbiont type influences trophic plasticity of a model cnidarian-dinoflagellate symbiosis. The Journal of Experimental Biology 218, 858–863.
Symbiont type influences trophic plasticity of a model cnidarian-dinoflagellate symbiosis.Crossref | GoogleScholarGoogle Scholar | 25617454PubMed |

Leggat, W., Ainsworth, T. D., Dove, S., and Hoegh-Guldberg, O. (2006). Aerial exposure influences bleaching patterns. Coral Reefs 25, 452–452.
Aerial exposure influences bleaching patterns.Crossref | GoogleScholarGoogle Scholar |

Levy, O., Achituv, Y., Yacobi, Y., Stambler, N., and Dubinsky, Z. (2006). The impact of spectral composition and light periodicity on the activity of two antioxidant enzymes (SOD and CAT) in the coral Favia favus. Journal of Experimental Marine Biology and Ecology 328, 35–46.
The impact of spectral composition and light periodicity on the activity of two antioxidant enzymes (SOD and CAT) in the coral Favia favus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCrtrbF&md5=fac5e6b3ce1d195fc44b32bc079c75f5CAS |

Maxwell, K., and Johnson, G. (2000). Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
Chlorophyll fluorescence – a practical guide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2js74%3D&md5=bedb76ad6a6a8a9e8c5f240b7096cb74CAS | 10938857PubMed |

Mendes, C. R., Cartaxana, P., and Brotas, V. (2007). Determination of phytoplankton and microphytobenthos pigments: comparing resolution and sensitivity of a C18 and C8 method. Limnology and Oceanography, Methods 5, 363–370.
Determination of phytoplankton and microphytobenthos pigments: comparing resolution and sensitivity of a C18 and C8 method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtl2rtrjK&md5=627f5c2f886b44c1072fbefb1dd2a694CAS |

Morris, S., and Taylor, A. C. (1983). Diurnal and seasonal variation in physico-chemical conditions within intertidal rock pools. Estuarine, Coastal and Shelf Science 17, 339–355.
Diurnal and seasonal variation in physico-chemical conditions within intertidal rock pools.Crossref | GoogleScholarGoogle Scholar |

Rabelo, E. F., Rocha, L. L., Colares, G. B., Bomfim, T. A., Nogueira, V. L. R., Katzenberger, M., Matthews-Cascon, H., and Melo, V. M. M. (2014). Symbiodinium diversity associated with zoanthids (Cnidaria: Hexacorallia) in Northeastern Brazil. Symbiosis 64, 105–113.
Symbiodinium diversity associated with zoanthids (Cnidaria: Hexacorallia) in Northeastern Brazil.Crossref | GoogleScholarGoogle Scholar |

Rabelo, E. F., Soares, M. O., Bezerra, L. E. A., and Matthews-Cascon, H. (2015). Distribution pattern of zoanthids (Cnidaria: Zoantharia) on a tropical reef. Marine Biology Research 11, 584–592.
Distribution pattern of zoanthids (Cnidaria: Zoantharia) on a tropical reef.Crossref | GoogleScholarGoogle Scholar |

Reimer, J., Takishita, K., and Maruyama, T. (2006). Molecular identification of symbiotic dinoflagellates (Symbiodinium spp.) from Palythoa spp. (Anthozoa: Hexacorallia) in Japan. Coral Reefs 25, 521–527.
Molecular identification of symbiotic dinoflagellates (Symbiodinium spp.) from Palythoa spp. (Anthozoa: Hexacorallia) in Japan.Crossref | GoogleScholarGoogle Scholar |

Reimer, J. D., Ono, S., Tsukahara, J., Takishita, K., and Maruyama, T. (2007). Non-seasonal clade-specificity and subclade microvariation in symbiotic dinoflagellates (Symbiodinium spp.) in Zoanthus sansibaricus (Anthozoa: Hexacorallia) at Kagoshima Bay, Japan. Phycological Research 55, 58–65.
Non-seasonal clade-specificity and subclade microvariation in symbiotic dinoflagellates (Symbiodinium spp.) in Zoanthus sansibaricus (Anthozoa: Hexacorallia) at Kagoshima Bay, Japan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFKktrY%3D&md5=f888817cc5864f387b1080e35f75546bCAS |

Reimer, J. D., Irei, Y., Fujii, T., and Yang, S.-Y. (2013). Molecular analyses of shallow-water zooxanthellate zoanthids (Cnidaria: Hexacorallia) from Taiwan and their Symbiodinium spp. Zoological Studies 52, 38.
Molecular analyses of shallow-water zooxanthellate zoanthids (Cnidaria: Hexacorallia) from Taiwan and their Symbiodinium spp.Crossref | GoogleScholarGoogle Scholar |

Rocha, R. J. M., Calado, R., Cartaxana, P., Furtado, J., and Serôdio, J. (2013a). Photobiology and growth of leather coral Sarcophyton cf. glaucum fragments stocked under low light in a recirculated system. Aquaculture 414–415, 235–242.
Photobiology and growth of leather coral Sarcophyton cf. glaucum fragments stocked under low light in a recirculated system.Crossref | GoogleScholarGoogle Scholar |

Rocha, R. J. M., Serôdio, J., Leal, M. C., Cartaxana, P., and Calado, R. (2013b). Effect of light intensity on post-fragmentation photobiological performance of the soft coral Sinularia flexibilis. Aquaculture 388–391, 24–29.
Effect of light intensity on post-fragmentation photobiological performance of the soft coral Sinularia flexibilis.Crossref | GoogleScholarGoogle Scholar |

Rodríguez, J. J. G., Mirón, A. S., Camacho, F. G., García, M. C. C., Belarbi, E. H., Chisti, Y., and Grima, E. M. (2009). Causes of shear sensitivity of the toxic dinoflagellate Protoceratium reticulatum. Biotechnology Progress 25, 792–800.
Causes of shear sensitivity of the toxic dinoflagellate Protoceratium reticulatum.Crossref | GoogleScholarGoogle Scholar |

Romaine, S., Tambutté, E., Allemand, D., and Gattuso, J.-P. (1997). Photosynthesis, respiration and calcification of a zooxanthellate scleractinian coral under submerged and exposed conditions. Marine Biology 129, 175–182.
Photosynthesis, respiration and calcification of a zooxanthellate scleractinian coral under submerged and exposed conditions.Crossref | GoogleScholarGoogle Scholar |

Schreiber, U., Schliwa, U., and Bilger, W. (1986). Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research 10, 51–62.
Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXktlGrsbY%3D&md5=d133b23b45fec482d112f901c4bb5f7eCAS | 24435276PubMed |

Sebens, K. P. (1982). Intertidal distribution of zoanthids on the Caribbean coast of Panama: effects of predation and desiccation. Bulletin of Marine Science 32, 316–335.

Shick, J. M., and Dykens, J. A. (1984). Photobiology of the symbiotic sea anemone Anthopleura elegantissima: photosynthesis, respiration, and behaviour under intertidal conditions. The Biological Bulletin 166, 608–619.
Photobiology of the symbiotic sea anemone Anthopleura elegantissima: photosynthesis, respiration, and behaviour under intertidal conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlt1Ogs7w%3D&md5=c66145c72560dd82a9bb885c1b7ed022CAS |

Stambler, N., and Dubinsky, Z. (2004). Stress effects on metabolism of hermatypic coral. In ‘Coral Health and Disease’. (Eds E. Rosernberg and Y. Loya.) pp. 195–215. (Springer-Verlag: Berlin.)

Suggett, D. J., Goyen, S., Evenhuis, C., Szabo, M., Pettay, D. T., Warner, M. E., and Ralph, P. J. (2015). Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytologist 208, 370–381.
Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation.Crossref | GoogleScholarGoogle Scholar | 26017701PubMed |

Teixeira, T., Diniz, M. S., Calado, R., and Rosa, R. (2013). Coral physiological adaptations to air exposure: heat shock and oxidative stress responses in Veretillum cynomorium. Journal of Experimental Marine Biology and Ecology 439, 35–41.
Coral physiological adaptations to air exposure: heat shock and oxidative stress responses in Veretillum cynomorium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXisVejsr0%3D&md5=85d07a23fa9fbd5371ad8a070bef9aa3CAS |

Titlyanov, E., and Titlyanova, T. (2002). Reef-building corals – symbiotic autotrophic organisms: 2. Pathways and mechanisms of adaptation to light. Russian Journal of Marine Biology 28, S16–S31.
Reef-building corals – symbiotic autotrophic organisms: 2. Pathways and mechanisms of adaptation to light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt1CntA%3D%3D&md5=b569f3a9b7f31c0db1a6975e6f1b74a6CAS |

Venn, A. A., Wilson, M. A., Trapido-Rosenthal, H. G., Keely, B. J., and Douglas, A. E. (2006). The impact of coral bleaching on the pigment profile of the symbiotic alga, Symbiodinium. Plant, Cell & Environment 29, 2133–2142.
The impact of coral bleaching on the pigment profile of the symbiotic alga, Symbiodinium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVajtw%3D%3D&md5=1c27998c54c0b1e80a2f1ccca112498aCAS |

Venn, A., Loram, J., and Douglas, A. (2008). Photosynthetic symbioses in animals. Journal of Experimental Botany 59, 1069–1080.
Photosynthetic symbioses in animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjs1Khurg%3D&md5=a8fa1d2bebd642e8a26346f4fe1fb91bCAS | 18267943PubMed |

Warner, M., Fitt, W., and Schmidt, G. (1999). Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proceedings of the National Academy of Sciences of the United States of America 96, 8007.
Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVOku7s%3D&md5=a077e5a631a9cf52414648373cba76fdCAS | 10393938PubMed |

Wijgerde, T., Melis, A. V., Silva, C. I. F., Leal, M. C., Vogels, L., Mutter, C., and Osinga, R. (2014). Red light represses the photophysiology of the scleractinian coral Stylophora pistillata. PLoS One 9, e92781.
Red light represses the photophysiology of the scleractinian coral Stylophora pistillata.Crossref | GoogleScholarGoogle Scholar | 24658108PubMed |

Yang, S. Y., Bourgeois, C., Ashworth, C. D., and Reimer, J. D. (2013). Palythoa zoanthid ‘barrens’ in Okinawa: examination of possible environmental cues. Zoological Studies 52, 39.
Palythoa zoanthid ‘barrens’ in Okinawa: examination of possible environmental cues.Crossref | GoogleScholarGoogle Scholar |

Zapata, M., Rodríguez, F., and Garrido, J. L. (2000). Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Marine Ecology Progress Series 195, 29–45.
Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsFChsLs%3D&md5=a859768d9328a8bd41bfc1ac6656a4ebCAS |