Coral lipids are an important energy source when their symbiotic zooxanthellae density decreases

Men Zheng; Chen Hanji; Xu Shendong; Yu Kefu; Mo Hongyan

doi:10.12284/hyxb2023022

Volume 45 Issue 1

Jan. 2023

Turn off MathJax

Article Contents

Article Navigation > Haiyang Xuebao > 2023 > 45(1): 71-79

Men Zheng，Chen Hanji，Xu Shendong, et al. Coral lipids are an important energy source when their symbiotic zooxanthellae density decreases[J]. Haiyang Xuebao，2023, 45(1)：71–79 doi: 10.12284/hyxb2023022

Citation:

PDF( 1355 KB)

Coral lipids are an important energy source when their symbiotic zooxanthellae density decreases

doi: 10.12284/hyxb2023022

Men Zheng^1
,,
Chen Hanji¹,
Xu Shendong^{1, 2, 3
,
,},
Yu Kefu^{1, 3},
Mo Hongyan¹

1.
Guangxi Laboratory on the Study of Coral Reefs in the South China Sea, School of Marine Sciences, Guangxi University, Nanning 530004, China
2.
Key Laboratory of Coastal Zone Environmental Processes and Ecological Remediation, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai 264003, China
3.
Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai 519082, China

Received Date: 2022-05-20
Rev Recd Date: 2022-09-05

Available Online: 2022-09-09

Publish Date: 2023-01-09

Abstract

Abstract

Coral bleaching has become increasingly severe in recent years. Bleaching means a decrease in the symbiotic zooxanthellae density in corals. However, the significance of lipids in corals to maintain the stability of energy supply when the zooxanthellae density decreases remains unclear. Favia palauensis and Porites lutea samples collected in the Xisha Islands in March and June 2020 as materials were used in this study. By combining physiological parameters (zooxanthellae density and lipid content) with geochemical indexes (stable nitrogen isotope δ¹⁵N_z value of zooxanthellae), the response of coral lipids to the changes in zooxanthellae density and photosynthetic intensity was investigated. The results showed that the zooxanthellae density and δ¹⁵N_z value of two genera of corals decreased significantly in summer, implying that the decrease in zooxanthellae density in summer resulted in a decrease in their photosynthetic intensity. At the same time, the lipid content of the two genera of corals also decreased significantly, and the lipid content was positively correlated with zooxanthellae density and δ¹⁵N_z value, indicating that there was a coupling relationship between the coral lipid content and the changes of the photosynthetic intensity of zooxanthellae. When photosynthesis intensity decreases, coral can better maintain the stability of energy supply by consuming their own stored lipids, which is of great significance to improve their adaptability to environmental stress and bleaching resilience.
- coral,
- energy supply,
- zooxanthellae,
- lipids,
- nitrogen isotopes

FullText(HTML)

References(50)

References

[1]	Baumann J, Grottoli A G, Hughes A D, et al. Photoautotrophic and heterotrophic carbon in bleached and non-bleached coral lipid acquisition and storage[J]. Journal of Experimental Marine Biology and Ecology, 2014, 461: 469−478. doi: 10.1016/j.jembe.2014.09.017
[2]	Baker A C, Glynn P W, Riegl B. Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook[J]. Estuarine, Coastal and Shelf Science, 2008, 80(4): 435−471. doi: 10.1016/j.ecss.2008.09.003
[3]	吴钟解, 王道儒, 涂志刚, 等. 西沙生态监控区造礁石珊瑚退化原因分析[J]. 海洋学报, 2011, 33(4): 140−146. Wu Zhongjie, Wang Daoru, Tu Zhigang, et al. The analysis on the reason of hermatypic coral degradation in Xisha[J]. Haiyang Xuebao, 2011, 33(4): 140−146.
[4]	Warner M, Chilcoat G, McFarland F, et al. Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastraea[J]. Marine Biology, 2002, 141(1): 31−38. doi: 10.1007/s00227-002-0807-8
[5]	梁甲元, 邓传奇, 许勇前, 等. 一种环境敏感型造礁石珊瑚Pocillopora sp. 共生虫黄藻和细菌的生态特征[J]. 海洋学报, 2022, 44(2): 102−112. Liang Jiayuan, Deng Chuanqi, Xu Yongqian, et al. Ecological characteristics of symbiotic Symbiodiniaceae and bacteria in an environmentally sensitive reef-building coral Pocillopora sp.[J]. Haiyang Xuebao, 2022, 44(2): 102−112.
[6]	Yamashiro H, Oku H, Onaga K. Effect of bleaching on lipid content and composition of Okinawan corals[J]. Fisheries Science, 2005, 71(2): 448−453. doi: 10.1111/j.1444-2906.2005.00983.x
[7]	Pengsakun S, Yeemin T, Sutthacheep M, et al. Monitoring of coral communities in the inner Gulf of Thailand influenced by the elevated seawater temperature and flooding[J]. Acta Oceanologica Sinica, 2019, 38(1): 102−111. doi: 10.1007/s13131-019-1376-8
[8]	Fitt W K, McFarland F K, Warner M E, et al. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching[J]. Limnology and Oceanography, 2000, 45(3): 677−685. doi: 10.4319/lo.2000.45.3.0677
[9]	Porter J W, Fitt W K, Spero H J, et al. Bleaching in reef corals: physiological and stable isotopic responses[J]. Proceedings of the National Academy of Sciences of the United States of America, 1989, 86(23): 9342−9346. doi: 10.1073/pnas.86.23.9342
[10]	Rodrigues L J, Grottoli A G. Energy reserves and metabolism as indicators of coral recovery from bleaching[J]. Limnology and Oceanography, 2007, 52(5): 1874−1882. doi: 10.4319/lo.2007.52.5.1874
[11]	Bessell-Browne P, Stat M, Thomson D, et al. Coscinaraea marshae corals that have survived prolonged bleaching exhibit signs of increased heterotrophic feeding[J]. Coral Reefs, 2014, 33(3): 795−804. doi: 10.1007/s00338-014-1156-z
[12]	Grottoli A G, Rodrigues L J, Palardy J E. Heterotrophic plasticity and resilience in bleached corals[J]. Nature, 2006, 440(7088): 1186−1189. doi: 10.1038/nature04565
[13]	许慎栋, 张志楠, 余克服, 等. 南海造礁珊瑚Favia palauensis营养方式的空间差异及其对环境适应性的影响[J]. 中国科学: 地球科学, 2021, 64(6): 839−852. doi: 10.1007/s11430-020-9774-0 Xu Shendong, Zhang Zhinan, Yu Kefu, et al. Spatial variations in the trophic status of Favia palauensis corals in the South China Sea: insights into their different adaptabilities under contrasting environmental conditions[J]. Science China: Earth Sciences, 2021, 64(6): 839−852. doi: 10.1007/s11430-020-9774-0
[14]	Muscatine L. Glycerol excretion by symbiotic algae from corals and Tridacna and its control by the host[J]. Science, 1967, 156(3774): 516−519. doi: 10.1126/science.156.3774.516
[15]	Patton J S, Battey J F, Rigler M W, et al. A comparison of the metabolism of bicarbonate ¹⁴C and acetate 1-¹⁴C and the variability of species lipid compositions in reef corals[J]. Marine Biology, 1983, 75(2): 121−130.
[16]	Crossland C J, Barnes D J, Borowitzka M A. Diurnal lipid and mucus production in the staghorn coral Acropora acuminata[J]. Marine Biology, 1980, 60(2): 81−90.
[17]	Patton J S, Abraham S, Benson A A. Lipogenesis in the intact coral Pocillopora capitata and its isolated zooxanthellae: evidence for a light-driven carbon cycle between symbiont and host[J]. Marine Biology, 1977, 44(3): 235−247. doi: 10.1007/BF00387705
[18]	Imbs A B, Latyshev N A, Dautova T N, et al. Distribution of lipids and fatty acids in corals by their taxonomic position and presence of zooxanthellae[J]. Marine Ecology Progress Series, 2010, 409: 65−75. doi: 10.3354/meps08622
[19]	Yamashiro H, Oku H, Higa H, et al. Composition of lipids, fatty acids and sterols in Okinawan corals[J]. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 1999, 122(4): 397−407. doi: 10.1016/S0305-0491(99)00014-0
[20]	Harland A D, Navarro J C, Davies P S, et al. Lipids of some Caribbean and Red Sea corals: total lipid, wax esters, triglycerides and fatty acids[J]. Marine Biology, 1993, 117(1): 113−117. doi: 10.1007/BF00346432
[21]	Grottoli A G, Rodrigues L J, Juarez C. Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event[J]. Marine Biology, 2004, 145(3): 621−631.
[22]	Stimson J. The annual cycle of density of zooxanthellae in the tissues of field and laboratory-held Pocillopora damicornis (Linnaeus)[J]. Journal of Experimental Marine Biology and Ecology, 1997, 214(1/2): 35−48.
[23]	李淑, 余克服, 施祺, 等. 南海北部珊瑚共生虫黄藻密度的种间与空间差异及其对珊瑚礁白化的影响[J]. 科学通报, 2008, 53(2): 295−303. doi: 10.1007/s11434-007-0514-4 Li Shu, Yu Kefu, Shi Qi, et al. Interspecies and spatial diversity in the symbiotic zooxanthellae density in corals from northern South China Sea and its relationship to coral reef bleaching[J]. Chinese Science Bulletin, 2008, 53(2): 295−303. doi: 10.1007/s11434-007-0514-4
[24]	Grottoli A G, Rodrigues L J. Bleached Porites compressa and Montipora capitata corals catabolize δ¹³C-enriched lipids[J]. Coral Reefs, 2011, 30(3): 687−692. doi: 10.1007/s00338-011-0756-0
[25]	Oku H, Yamashiro H, Onaga K. Lipid biosynthesis from [¹⁴C]-glucose in the coral Montipora digitata[J]. Fisheries Science, 2003, 69(3): 625−631. doi: 10.1046/j.1444-2906.2003.00665.x
[26]	Heikoop J M, Risk M J, Lazier A V, et al. Nitrogen-15 signals of anthropogenic nutrient loading in reef corals[J]. Marine Pollution Bulletin, 2000, 40(7): 628−636. doi: 10.1016/S0025-326X(00)00006-0
[27]	Muscatine L, Kaplan I R. Resource partitioning by reef corals as determined from stable isotope composition II. δ¹⁵N of zooxanthellae and animal tissue versus depth[J]. Pacific Science, 1994, 48(3): 304−312.
[28]	Ferrier-Pagès C, Peirano A, Abbate M, et al. Summer autotrophy and winter heterotrophy in the temperate symbiotic coral Cladocora caespitosa[J]. Limnology and Oceanography, 2011, 56(4): 1429−1438. doi: 10.4319/lo.2011.56.4.1429
[29]	Heikoop J M, Dunn J J, Risk M J, et al. Relationship between light and the δ¹⁵N of coral tissue: examples from Jamaica and Zanzibar[J]. Limnology and Oceanography, 1998, 43(5): 909−920. doi: 10.4319/lo.1998.43.5.0909
[30]	Djeghri N, Stibor H, Lebeau O, et al. δ¹³C, δ¹⁵N, and C∶N ratios as nutrition indicators of zooxanthellate jellyfishes: insights from an experimental approach[J]. Journal of Experimental Marine Biology and Ecology, 2020, 522: 151257. doi: 10.1016/j.jembe.2019.151257
[31]	Qin Zhenjun, Yu Kefu, Wang Yinghui, et al. Spatial and intergeneric variation in physiological indicators of corals in the South China Sea: insights into their current state and their adaptability to environmental stress[J]. Journal of Geophysical Research: Oceans, 2019, 124(5): 3317−3332. doi: 10.1029/2018JC014648
[32]	李颖虹, 黄小平, 岳维忠. 西沙永兴岛环境质量状况及管理对策[J]. 海洋环境科学, 2004, 23(1): 50−53. doi: 10.3969/j.issn.1007-6336.2004.01.015 Li Yinghong, Huang Xiaoping, Yue Weizhong. Environmental quality and management measures in Yongxing Island of Xisha, South China Sea[J]. Marine Environmental Science, 2004, 23(1): 50−53. doi: 10.3969/j.issn.1007-6336.2004.01.015
[33]	Fagoonee I, Wilson H B, Hassell M P, et al. The dynamics of zooxanthellae populations: a long-term study in the field[J]. Science, 1999, 283(5403): 843−845. doi: 10.1126/science.283.5403.843
[34]	Seemann J. The use of ¹³C and ¹⁵N isotope labeling techniques to assess heterotrophy of corals[J]. Journal of Experimental Marine Biology and Ecology, 2013, 442: 88−95. doi: 10.1016/j.jembe.2013.01.004
[35]	Stimson J S. Location, quantity and rate of change in quantity of lipids in tissue of Hawaiian Hermatypic corals[J]. Bulletin of Marine Science, 1987, 41(3): 889−904.
[36]	Rodrigues L J, Grottoli A G. Calcification rate and the stable carbon, oxygen, and nitrogen isotopes in the skeleton, host tissue, and zooxanthellae of bleached and recovering Hawaiian corals[J]. Geochimica et Cosmochimica Acta, 2006, 70(11): 2781−2789. doi: 10.1016/j.gca.2006.02.014
[37]	Glynn P W, D'Croz L. Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality[J]. Coral Reefs, 1990, 8(4): 181−191. doi: 10.1007/BF00265009
[38]	Fujise L, Yamashita H, Suzuki G, et al. Moderate thermal stress causes active and immediate expulsion of photosynthetically damaged zooxanthellae (Symbiodinium) from corals[J]. PLoS One, 2014, 9(12): e114321. doi: 10.1371/journal.pone.0114321
[39]	Gates R D, Baghdasarian G, Muscatine L. Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching[J]. The Biological Bulletin, 1992, 182(3): 324−332. doi: 10.2307/1542252
[40]	Lesser M P. Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in ymbiotic dinoflagellates[J]. Limnology and Oceanography, 1996, 41(2): 271−283. doi: 10.4319/lo.1996.41.2.0271
[41]	Kuguru B, Winters G, Beer S, et al. Adaptation strategies of the corallimorpharian Rhodactis rhodostoma to irradiance and temperature[J]. Marine Biology, 2007, 151(4): 1287−1298. doi: 10.1007/s00227-006-0589-5
[42]	Salih A, Larkum A, Cox G, et al. Fluorescent pigments in corals are photoprotective[J]. Nature, 2000, 408(6814): 850−853. doi: 10.1038/35048564
[43]	Brown B E, Downs C A, Dunne R P, et al. Exploring the basis of thermotolerance in the reef coral Goniastrea aspera[J]. Marine Ecology Progress Series, 2002, 242: 119−129. doi: 10.3354/meps242119
[44]	Muscatine L, Cernichiari E. Assimilation of photosynthetic products of zooxanthellae by a reef coral[J]. The Biological Bulletin, 1969, 137(3): 506−523. doi: 10.2307/1540172
[45]	Davies P S. Effect of daylight variations on the energy budgets of shallow-water corals[J]. Marine Biology, 1991, 108(1): 137−144. doi: 10.1007/BF01313481
[46]	Lesser M P. Using energetic budgets to assess the effects of environmental stress on corals: are we measuring the right things?[J]. Coral Reefs, 2013, 32(1): 25−33. doi: 10.1007/s00338-012-0993-x
[47]	Kellogg R B, Patton J S. Lipid droplets, medium of energy exchange in the symbiotic anemone Condylactis gigantea: a model coral polyp[J]. Marine Biology, 1983, 75(2): 137−149.
[48]	Anthony K R N, Connolly S R, Willis B L. Comparative analysis of energy allocation to tissue and skeletal growth in corals[J]. Limnology and Oceanography, 2002, 47(5): 1417−1429. doi: 10.4319/lo.2002.47.5.1417
[49]	Gnaiger E, Bitterlich G. Proximate biochemical composition and caloric content calculated from elemental CHN analysis: a stoichiometric concept[J]. Oecologia, 1984, 62(3): 289−298. doi: 10.1007/BF00384259
[50]	Anthony K R N, Hoogenboom M O, Maynard J A, et al. Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching[J]. Functional Ecology, 2009, 23(3): 539−550. doi: 10.1111/j.1365-2435.2008.01531.x