Volume 42 Issue 6
Jun.  2023
Turn off MathJax
Article Contents
Linbin Zhou, Yehui Tan, Liangmin Huang. Coral reef ecological pump for gathering and retaining nutrients and exporting carbon: a review and perspectives[J]. Acta Oceanologica Sinica, 2023, 42(6): 1-15. doi: 10.1007/s13131-022-2130-1
Citation: Linbin Zhou, Yehui Tan, Liangmin Huang. Coral reef ecological pump for gathering and retaining nutrients and exporting carbon: a review and perspectives[J]. Acta Oceanologica Sinica, 2023, 42(6): 1-15. doi: 10.1007/s13131-022-2130-1

Coral reef ecological pump for gathering and retaining nutrients and exporting carbon: a review and perspectives

doi: 10.1007/s13131-022-2130-1
Funds:  The Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) under contract No. GML2019ZD0405; the National Natural Science Foundation of China under contract Nos 41506150 and 41130855; the Guangdong Basic and Applied Basic Research Foundation under contract No. 2019A1515011645; the National Science and Technology Basic Work Program of the Ministry of Science and Technology of China under contract No. 2015FY110600; the Science and Technology Planning Project of Guangdong Province, China under contract No. 2020B1212060058; the Development Fund of South China Sea Institute of Oceanology of the Chinese Academy of Sciences under contract No. SCSIO202204.
More Information
  • Corresponding author: tanyh@scsio.ac.cnhlm@scsio.ac.cn
  • Received Date: 2022-08-20
  • Accepted Date: 2022-10-21
  • Available Online: 2023-06-26
  • Publish Date: 2023-06-25
  • How coral reefs with high productivity and biodiversity can flourish in oligotrophic tropical oceans has inspired substantial research on coral reef ecosystems. Increasing evidence shows that similar to water in an oasis in the desert, there are stable nutrient supplies to coral reefs in oligotrophic oceans. Here, with emphasis on the fluxes of organic matter, we summarize at the ecosystem level (1) the multiple input pathways of external nutrients, (2) the storage of nutrients in reef organisms, (3) the efficient retaining and recycling of dissolved and particulate organic matter within coral reef ecosystems, (4) the distinctly high phytoplankton productivity and biomass inside and near oceanic coral reefs, and (5) the export of reef-related organic carbon to adjacent open oceans. These properties enable coral reefs to function as ecological “pumps” for gathering nutrients across ecosystems and space, retaining and recycling nutrients within the ecosystem, supporting high phytoplankton productivity, and exporting organic carbon to adjacent open oceans. Particularly, the high phytoplankton productivity and biomass make waters around coral reefs potential hotspots of carbon export to ocean depths via the biological pump. We demonstrate that organic carbon influx is vital for coral reef ecosystems’ carbon budget and carbon export. The concept of the coral reef ecological pump provides a framework to improve the understanding of the functioning of the coral reef ecosystem and its responses to disturbance. Prospects of the coral reef ecological pump in coral reef studies are discussed in changing oceans driven by human activities and global change in the Anthropocene.
  • loading
  • Albuquerque T, Loiola M, de Anchieta C C Nunes J, et al. 2015. In situ effects of human disturbances on coral reef-fish assemblage structure: temporary and persisting changes are reflected as a result of intensive tourism. Marine and Freshwater Research, 66(1): 23–32. doi: 10.1071/MF13185
    Alldredge A L, Carlson C A, Carpenter R C. 2013. Sources of organic carbon to coral reef flats. Oceanography, 26(3): 108–113. doi: 10.5670/oceanog.2013.52
    Allgeier J E, Burkepile D E, Layman C A. 2017. Animal pee in the sea: consumer-mediated nutrient dynamics in the world’s changing oceans. Global Change Biology, 23(6): 2166–2178. doi: 10.1111/gcb.13625
    Allgeier J E, Layman C A, Mumby P J, et al. 2014. Consistent nutrient storage and supply mediated by diverse fish communities in coral reef ecosystems. Global Change Biology, 20(8): 2459–2472. doi: 10.1111/gcb.12566
    Allgeier J E, Speare K E, Burkepile D E. 2018. Estimates of fish and coral larvae as nutrient subsidies to coral reef ecosystems. Ecosphere, 9(6): e02216
    Allgeier J E, Valdivia A, Cox C, et al. 2016. Fishing down nutrients on coral reefs. Nature Communications, 7: 12461. doi: 10.1038/ncomms12461
    Andradi-Brown D A, Banaszak A T, Frazer T K, et al. 2020. Editorial: coral reefs in the anthropocene—Reflecting on 20 years of reef conservation UK. Frontiers in Marine Science, 7: 364. doi: 10.3389/fmars.2020.00364
    Apprill A. 2020. The role of symbioses in the adaptation and stress responses of marine organisms. Annual Review of Marine Science, 12: 291–314. doi: 10.1146/annurev-marine-010419-010641
    Atkinson M J. 1987. Rates of phosphate uptake by coral reef flat communities. Limnology and Oceanography, 32(2): 426–435. doi: 10.4319/lo.1987.32.2.0426
    Atkinson M J. 1992. Productivity of Enewetak Atoll reef flats predicted from mass transfer relationships. Continental Shelf Research, 12(7–8): 799–807
    Atkinson M J. 2011. Biogeochemistry of nutrients. In: Dubinsky Z, Stambler N, eds. Coral Reefs: An Ecosystem in Transition. Dordrecht: Springer, 199–206
    Atkinson M J, Falter J L. 2003. Coral reefs. In: Black K D, Shimmield G B, eds. Biogeochemistry of Marine Systems. Oxford: Blackwell Publishing, 40–64
    Azam F, Fenchel T, Field J G, et al. 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series, 10: 257–263. doi: 10.3354/meps010257
    Baquiran J I P, Conaco C. 2018. Sponge-microbe partnerships are stable under eutrophication pressure from mariculture. Marine Pollution Bulletin, 136: 125–134. doi: 10.1016/j.marpolbul.2018.09.011
    Bates N R. 2002. Seasonal variability of the effect of coral reefs on seawater CO2 and air-sea CO2 exchange. Limnology and Oceanography, 47(1): 43–52. doi: 10.4319/lo.2002.47.1.0043
    Benavides M, Houlbrèque F, Camps M, et al. 2016. Diazotrophs: a non-negligible source of nitrogen for the tropical coral Stylophora pistillata. Journal of Experimental Biology, 219(17): 2608–2612
    Benkwitt C E, Wilson S K, Graham N A J. 2020. Biodiversity increases ecosystem functions despite multiple stressors on coral reefs. Nature Ecology & Evolution, 4(7): 919–926
    Berkström C, Eggertsen L, Goodell W, et al. 2020. Thresholds in seascape connectivity: the spatial arrangement of nursery habitats structure fish communities on nearby reefs. Ecography, 43(6): 882–896. doi: 10.1111/ecog.04868
    Biegala I C, Raimbault P. 2008. High abundance of diazotrophic picocyanobacteria (<3 µm) in a Southwest Pacific coral lagoon. Aquatic Microbial Ecology, 51: 45–53. doi: 10.3354/ame01185
    Bonnin L, Robbins W D, Boussarie G, et al. 2019. Repeated long-range migrations of adult males in a common Indo-Pacific reef shark. Coral Reefs, 38(6): 1121–1132. doi: 10.1007/s00338-019-01858-w
    Borsa P, Richer De Forges B, Baudat-Franceschi J. 2018. Keep cruises off remote coral reefs. Nature, 558: 372-372
    Bouillon S, Connolly R M. 2009. Carbon exchange among tropical coastal ecosystems. In: Nagelkerken I, ed. Ecological Connectivity among Tropical Coastal Ecosystems. Dordrecht: Springer, 45–70
    Brandl S J, Tornabene L, Goatley C H R, et al. 2019. Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science, 364(6446): 1189–1192. doi: 10.1126/science.aav3384
    Brocke H J, Piltz B, Herz N, et al. 2018. Nitrogen fixation and diversity of benthic cyanobacterial mats on coral reefs in Curaçao. Coral Reefs, 37(3): 861–874. doi: 10.1007/s00338-018-1713-y
    Brocke H J, Wenzhoefer F, de Beer D, et al. 2015. High dissolved organic carbon release by benthic cyanobacterial mats in a Caribbean reef ecosystem. Scientific Reports, 5: 8852. doi: 10.1038/srep08852
    Burkepile D E, Allgeier J E, Shantz A A, et al. 2013. Nutrient supply from fishes facilitates macroalgae and suppresses corals in a Caribbean coral reef ecosystem. Scientific Reports, 3: 1493. doi: 10.1038/srep01493
    Callaghan D P, Nielsen P, Cartwright N, et al. 2006. Atoll lagoon flushing forced by waves. Coastal Engineering, 53: 691–704
    Carballo J L, Cruz-Barraza J A, Vega C, et al. 2019. Sponge diversity in Eastern Tropical Pacific coral reefs: an interoceanic comparison. Scientific Reports, 9(1): 9409. doi: 10.1038/s41598-019-45834-4
    Cardini U, Bednarz V N, van Hoytema N, et al. 2016. Budget of primary production and dinitrogen fixation in a highly seasonal Red Sea coral reef. Ecosystems, 19(5): 771–785. doi: 10.1007/s10021-016-9966-1
    Charpy L, Dufour P, Garcia N. 1997. Particulate organic matter in sixteen Tuamotu atoll lagoons (French Polynesia). Marine Ecology Progress Series, 151: 55–65. doi: 10.3354/meps151055
    Chen Xiaoyan, Yu Kefu, Huang Xueyong, et al. 2019. Atmospheric nitrogen deposition increases the possibility of macroalgal dominance on remote coral reefs. Journal of Geophysical Research: Biogeosciences, 124(5): 1355–1369. doi: 10.1029/2019JG005074
    Costa M B, Macedo E C, Valle-Levinson A, et al. 2017. Wave and tidal flushing in a near-equatorial mesotidal atoll. Coral Reefs, 36(1): 277–291. doi: 10.1007/s00338-016-1525-x
    Crossland C J, Hatcher B G, Smith S V. 1991. Role of coral reefs in global ocean production. Coral Reefs, 10(2): 55–64. doi: 10.1007/BF00571824
    Cuet P, Atkinson M J, Blanchot J, et al. 2011. CNP budgets of a coral-dominated fringing reef at La Réunion, France: coupling of oceanic phosphate and groundwater nitrate. Coral Reefs, 30(1): 45–55
    Darwin C R. 1842. The structure and distribution of coral reefs. Being the first part of the geology of the voyage of the Beagle, under the command of Capt. In: Fitzroy R N, ed. During the Years 1832 to 1836. London: Smith Elder and Co.
    Davis S E, Lirman D, Wozniak J R. 2009. Nitrogen and phosphorus exchange among tropical coastal ecosystems. In: Nagelkerken I, ed. Ecological Connectivity Among Tropical Coastal Ecosystems. Dordrecht: Springer, 9–44
    de Goeij J M, van Oevelen D, Vermeij M J A, et al. 2013. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science, 342(6154): 108–110. doi: 10.1126/science.1241981
    de Paula Y C, Schiavetti A, Sampaio C L S, et al. 2018. The effects of fish feeding by visitors on reef fish in a Marine Protected Area open to tourism. Biota Neotropica, 18(3): e20170339
    Delesalle B, Buscail R, Carbonne J, et al. 1998. Direct measurements of carbon and carbonate export from a coral reef ecosystem (Moorea Island, French Polynesia). Coral Reefs, 17(2): 121–132. doi: 10.1007/s003380050106
    den Haan J, Visser P M, Ganase A E, et al. 2014. Nitrogen fixation rates in algal turf communities of a degraded versus less degraded coral reef. Coral Reefs, 33(4): 1003–1015. doi: 10.1007/s00338-014-1207-5
    Derville S, Torres L G, Dodémont R, et al. 2019. From land and sea, long-term data reveal persistent humpback whale (Megaptera novaeangliae) breeding habitat in New Caledonia. Aquatic Conservation: Marine and Freshwater Ecosystems, 29(10): 1697–1711. doi: 10.1002/aqc.3127
    Diaz-Pulido G, Barrón C. 2020. CO2 enrichment stimulates dissolved organic carbon release in coral reef macroalgae. Journal of Phycology, 56(4): 1039–1052. doi: 10.1111/jpy.13002
    Doty M S, Oguri M. 1956. The island mass effect. ICES Journal of Marine Science, 22(1): 33–37. doi: 10.1093/icesjms/22.1.33
    Du Jianguo, Xie Meiling, Wang Yuyu, et al. 2020. Connectivity of fish assemblages along the mangrove-seagrass-coral reef continuum in Wenchang, China. Acta Oceanologica Sinica, 39(8): 43–52. doi: 10.1007/s13131-019-1490-7
    Dudgeon S, Kübler J E. 2020. A multistressor model of carbon acquisition regulation for macroalgae in a changing climate. Limnology and Oceanography, 65(10): 2541–2555. doi: 10.1002/lno.11470
    Duran A, Collado-Vides L, Burkepile D E. 2016. Seasonal regulation of herbivory and nutrient effects on macroalgal recruitment and succession in a Florida coral reef. PeerJ, 4: e2643. doi: 10.7717/peerj.2643
    Edgar G J, Stuart-Smith R D. 2014. Systematic global assessment of reef fish communities by the Reef Life Survey program. Scientific Data, 1: 140007. doi: 10.1038/sdata.2014.7
    Elsner J B, Kossin J P, Jagger T H. 2008. The increasing intensity of the strongest tropical cyclones. Nature, 455: 92–95
    Erler D V, Santos I R, Eyre B D. 2014. Inorganic nitrogen transformations within permeable carbonate sands. Continental Shelf Research, 77: 69–80. doi: 10.1016/j.csr.2014.02.002
    Eyre B D, Glud R N, Patten N. 2008. Mass coral spawning: a natural large-scale nutrient addition experiment. Limnology and Oceanography, 53: 997–1013
    Fabricius K E. 2005. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Marine Pollution Bulletin, 50(2): 125–146. doi: 10.1016/j.marpolbul.2004.11.028
    Ferrier-Pagès C, Gattuso J P, Cauwet G, et al. 1998. Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis. Marine Ecology Progress Series, 172: 265–274. doi: 10.3354/meps172265
    Ferrier-Pagès C, Leclercq N, Jaubert J, et al. 2000. Enhancement of pico- and nanoplankton growth by coral exudates. Aquatic Microbial Ecology, 21: 203–209. doi: 10.3354/ame021203
    Ferrier-Pagès C, Sauzéat L, Balter V. 2018. Coral bleaching is linked to the capacity of the animal host to supply essential metals to the symbionts. Global Change Biology, 24: 3145–3157
    Fiore C L, Jarett J K, Olson N D, et al. 2010. Nitrogen fixation and nitrogen transformations in marine symbioses. Trends in Microbiology, 18(10): 455–463. doi: 10.1016/j.tim.2010.07.001
    Fitt W K, McFarland F K, Warner M E, et al. 2000. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnology and Oceanography, 45(3): 677–685. doi: 10.4319/lo.2000.45.3.0677
    Ford A K, Van Hoytema N, Moore B R, et al. 2017. High sedimentary oxygen consumption indicates that sewage input from small islands drives benthic community shifts on overfished reefs. Environmental Conservation, 44(4): 405–411. doi: 10.1017/S0376892917000054
    Fox M D, Elliott Smith E A, Smith J E, et al. 2019. Trophic plasticity in a common reef-building coral: insights from δ13C analysis of essential amino acids. Functional Ecology, 33(11): 2203–2214. doi: 10.1111/1365-2435.13441
    Francis F T, Cȏté I M. 2018. Fish movement drives spatial and temporal patterns of nutrient provisioning on coral reef patches. Ecosphere, 9(5): e02225
    Friedlander A M, Obura D, Aumeeruddy R, et al. 2014. Coexistence of low coral cover and high fish biomass at Farquhar Atoll, Seychelles. PLoS ONE, 9(1): e87359. doi: 10.1371/journal.pone.0087359
    Furnas M J, Mitchell A W, Skuza M. 1995. Nitrogen and Phosphorus Budgets for the Central Great Barrier Reef Shelf. Towmsville Queensland: Great Barrier Reef Marine Park Authority
    Gattuso J P, Frankignoulle M, Smith S V. 1999. Measurement of community metabolism and significance in the coral reef CO2 source-sink debate. Proceedings of the National Academy of Sciences of the United States of America, 96(23): 13017–13022. doi: 10.1073/pnas.96.23.13017
    Geesey G G, Alexander G V, Bray R N, et al. 1984. Fish fecal pellets are a source of minerals for inshore reef communities. Marine Ecology Progress Series, 15: 19–25. doi: 10.3354/meps015019
    Genin A, Monismith S G, Reidenbach M A, et al. 2009. Intense benthic grazing of phytoplankton in a coral reef. Limnology and Oceanography, 54(3): 938–951. doi: 10.4319/lo.2009.54.3.0938
    Goatley C H R, Bellwood D R. 2016. Body size and mortality rates in coral reef fishes: a three-phase relationship. Proceedings of the Royal Society B: Biological Sciences, 283(1841): 20161858. doi: 10.1098/rspb.2016.1858
    Godinot C, Gaysinski M, Thomas O P, et al. 2016. On the use of 31P NMR for the quantification of hydrosoluble phosphorus-containing compounds in coral host tissues and cultured zooxanthellae. Scientific Reports, 6: 21760. doi: 10.1038/srep21760
    González-Dávila M, Casiano J M S, Machín F. 2017. Changes in the partial pressure of carbon dioxide in the Mauritanian-Cap Vert upwelling region between 2005 and 2012. Biogeosciences, 14(17): 3859–3871. doi: 10.5194/bg-14-3859-2017
    Gove J M, McManus M A, Neuheimer A B, et al. 2016. Near-island biological hotspots in barren ocean basins. Nature Communications, 7: 10581. doi: 10.1038/ncomms10581
    Graham N A J, Nash K L. 2013. The importance of structural complexity in coral reef ecosystems. Coral Reefs, 32(2): 315–326. doi: 10.1007/s00338-012-0984-y
    Graham N A J, Wilson S K, Carr P, et al. 2018. Seabirds enhance coral reef productivity and functioning in the absence of invasive rats. Nature, 559(7713): 250–253. doi: 10.1038/s41586-018-0202-3
    Gray S E C, DeGrandpre M D, Langdon C, et al. 2012. Short-term and seasonal pH, pCO2 and saturation state variability in a coral-reef ecosystem. Global Biogeochemical Cycles, 26(3): GB3012
    Green R H, Jones N L, Rayson M D, et al. 2019. Nutrient fluxes into an isolated coral reef atoll by tidally driven internal bores. Limnology and Oceanography, 64(2): 461–473. doi: 10.1002/lno.11051
    Green A L, Maypa A P, Almany G R, et al. 2015. Larval dispersal and movement patterns of coral reef fishes, and implications for marine reserve network design. Biological Reviews, 90(4): 1215–1247. doi: 10.1111/brv.12155
    Grover R, Ferrier-Pagès C, Maguer J F, et al. 2014. Nitrogen fixation in the mucus of Red Sea corals. Journal of Experimental Biology, 217(22): 3962–3963
    Gruber R K, Lowe R J, Falter J L. 2018. Benthic uptake of phytoplankton and ocean-reef exchange of particulate nutrients on a tide-dominated reef. Limnology and Oceanography, 63(4): 1545–1561. doi: 10.1002/lno.10790
    Haas A F, Fairoz M F M, Kelly L W, et al. 2016. Global microbialization of coral reefs. Nature Microbiology, 1: 16042
    Hadaidi G, Gegner H M, Ziegler M, et al. 2019. Carbohydrate composition of mucus from scleractinian corals from the central Red Sea. Coral Reefs, 38(1): 21–27. doi: 10.1007/s00338-018-01758-5
    Hamner W M, Colin P L, Hamner P P. 2007. Export-import dynamics of zooplankton on a coral reef in Palau. Marine Ecology Progress Series, 334: 83–92
    Hamner W M, Jones M S, Carleton J H, et al. 1988. Zooplankton, planktivorous fish, and water currents on a windward reef face: Great Barrier Reef, Australia. Bulletin of Marine Science, 42(3): 459–479
    Hata H, Kudo S, Yamano H, et al. 2002. Organic carbon flux in Shiraho coral reef (Ishigaki Island, Japan). Marine Ecology Progress Series, 232: 129–140. doi: 10.3354/meps232129
    Hata H, Suzuki A, Maruyama T, et al. 1998. Carbon flux by suspended and sinking particles around the barrier reef of Palau, western Pacific. Limnology and Oceanography, 43(8): 1883–1893. doi: 10.4319/lo.1998.43.8.1883
    Hatcher B G. 1988. Coral reef primary productivity: a beggar’s banquet. Trends in Ecology & Evolution, 3(5): 106–111
    Hatcher B G. 1997. Coral reef ecosystems: how much greater is the whole than the sum of the parts?. Coral Reefs, 16: S77–S91
    Hernández-León S. 1991. Accumulation of mesozooplankton in a wake area as a causative mechanism of the “island-mass effect”. Marine Biology, 109(1): 141–147. doi: 10.1007/BF01320241
    Heupel M R, Papastamatiou Y P, Espinoza M, et al. 2019. Reef shark science—key questions and future directions. Frontiers in Marine Science, 6: 12. doi: 10.3389/fmars.2019.00012
    Hoer D R, Gibson P J, Tommerdahl J P, et al. 2018. Consumption of dissolved organic carbon by Caribbean reef sponges. Limnology and Oceanography, 63(1): 337–351. doi: 10.1002/lno.10634
    Honig S E, Mahoney B. 2016. Evidence of seabird guano enrichment on a coral reef in Oahu, Hawaii. Marine Biology, 163(2): 22. doi: 10.1007/s00227-015-2808-4
    Houlbrèque F, Ferrier-Pagès C. 2009. Heterotrophy in tropical scleractinian corals. Biological Reviews, 84(1): 1–17. doi: 10.1111/j.1469-185X.2008.00058.x
    Huang Liangmin. 1991. Characteristics of photosynthetic pigments and primary productivity distribution in the waters around Nansha Islands (In Chinese with English abstract). In: Chen Q, Ed. Mutidisciplinary Expedition to Nansha Islands Chinese Academy of Sciences, eds. Proceedings of Studies on Marine Organisms in Nansha Islands and Adjacent Waters II. Beijing: China Ocean Press, 34–49
    Huang Liangmin. 1997. A Study on Ecological Processes of Nansha Islands Sea Area I (in Chinese). Beijing: Science Press
    Huang Liangmin, Tan Yehui, Song Xingyu, et al. 2020. A Study on Ecological Processes of Nansha Islands Sea Area (in Chinese). Beijing: Science Press
    Ikawa H, Faloona I, Kochendorfer J, et al. 2013. Air-sea exchange of CO2 at a Northern California coastal site along the California Current upwelling system. Biogeosciences, 10(7): 4419–4432. doi: 10.5194/bg-10-4419-2013
    James A K, Washburn L, Gotschalk C, et al. 2020. An island mass effect resolved near Mo’orea, French Polynesia. Frontiers in Marine Science, 7: 16. doi: 10.3389/fmars.2020.00016
    Jantzen C, Wild C, Rasheed M, et al. 2010. Enhanced pore-water nutrient fluxes by the upside-down jellyfish Cassiopea sp. in a Red Sea coral reef. Marine Ecology Progress Series, 411: 117–125. doi: 10.3354/meps08623
    Jiang Wei, Yang Haodan, Wu Xingyuan, et al. 2020. Research progress of environmental influence and coral record of submarine groundwater discharge in coral reefs. Haiyang Xuebao (In Chinese with English Abstract), 42(11): 1–11. doi: 10.3969/j.issn.0253-4193.2020.11.001
    Johannes R E, Alberts J, D’Elia C, et al. 1972. The metabolism of some coral reef communities: a team study of nutrient and energy flux at Eniwetok. BioScience, 22(9): 541–543. doi: 10.2307/1296314
    Johannes R E, Coles S L, Kuenzel N T. 1970. The role of zooplankton in the nutrition of some scleractinian corals. Limnology and Oceanography, 15(4): 579–586. doi: 10.4319/lo.1970.15.4.0579
    Karcher D B, Roth F, Carvalho S, et al. 2020. Nitrogen eutrophication particularly promotes turf algae in coral reefs of the central Red Sea. PeerJ, 8: e8737. doi: 10.7717/peerj.8737
    Karnauskas K B, Cohen A L. 2012. Equatorial refuge amid tropical warming. Nature Climate Change, 2: 530–534
    Kayanne H, Suzuki A, Saito H. 1995. Diurnal changes in the partial pressure of carbon dioxide in coral reef water. Science, 269(5221): 214–216. doi: 10.1126/science.269.5221.214
    Ke Zhixin, Tan Yehui, Huang Liangmin, et al. 2018. Spatial distribution patterns of phytoplankton biomass and primary productivity in six coral atolls in the central South China Sea. Coral Reefs, 37(3): 919–927. doi: 10.1007/s00338-018-1717-7
    Kealoha A K, Shamberger K E F, Reid E C, et al. 2019. Heterotrophy of oceanic particulate organic matter elevates net ecosystem calcification. Geophysical Research Letters, 46(16): 9851–9860. doi: 10.1029/2019GL083726
    Khan J A, Goatley C H R, Brandl S J, et al. 2017. Shelter use by large reef fishes: long-term occupancy and the impacts of disturbance. Coral Reefs, 36(4): 1123–1132. doi: 10.1007/s00338-017-1604-7
    Kinsey D W, Hopley D. 1991. The significance of coral reefs as global carbon sinks—response to Greenhouse. Global and Planetary Change, 3(4): 363–377. doi: 10.1016/0921-8181(91)90117-F
    Kossin J P, Knapp K R, Olander T L, et al. 2020. Global increase in major tropical cyclone exceedance probability over the past four decades. Proceedings of the National Academy of Sciences of the United States of America, 117(22): 11975–11980. doi: 10.1073/pnas.1920849117
    Kötter I. 2003. Feeding ecology of coral reef sponges [dissertation]. Bremen: University Bremen, 77
    Kumagai N H, Molinos J G, Yamano H, et al. 2018. Ocean currents and herbivory drive macroalgae-to-coral community shift under climate warming. Proceedings of the National Academy of Sciences of the United States of America, 115(36): 8990–8995. doi: 10.1073/pnas.1716826115
    Larkum A W D, Kennedy I R, Muller W J. 1988. Nitrogen fixation on a coral reef. Marine Biology, 98(1): 143–155. doi: 10.1007/BF00392669
    Lee S, Ford A K, Mangubhai S, et al. 2018. Effects of sandfish (Holothuria scabra) removal on shallow-water sediments in Fiji. PeerJ, 6: e4773. doi: 10.7717/peerj.4773
    Leichter J J, Stewart H L, Miller S L. 2003. Episodic nutrient transport to Florida coral reefs. Limnology and Oceanography, 48: 1394–1407
    Lesser M P, Morrow K M, Pankey S M, et al. 2018. Diazotroph diversity and nitrogen fixation in the coral Stylophora pistillata from the Great Barrier Reef. The ISME Journal, 12(3): 813–824. doi: 10.1038/s41396-017-0008-6
    Leys S P, Yahel G, Reidenbach M A, et al. 2011. The sponge pump: the role of current induced flow in the design of the sponge body plan. PLoS ONE, 6(12): e27787. doi: 10.1371/journal.pone.0027787
    Liberman T, Genin A, Loya Y. 1995. Effects on growth and reproduction of the coral Stylophora pistillata by the mutualistic damselfish Dascyllus marginatus. Marine Biology, 121(4): 741–746. doi: 10.1007/BF00349310
    Liu Qingxia, Zhou Linbin, Wu Yun, et al. 2022. Quantification of the carbon released by a marine fish using a carbon release model and radiocarbon. Marine Pollution Bulletin, 181: 113908. doi: 10.1016/j.marpolbul.2022.113908
    Lønborg C, Calleja M L, Fabricius K E, et al. 2019. The Great Barrier Reef: a source of CO2 to the atmosphere. Marine Chemistry, 210: 24–33. doi: 10.1016/j.marchem.2019.02.003
    Lønborg C, Doyle J, Furnas M, et al. 2017. Seasonal organic matter dynamics in the Great Barrier Reef lagoon: contribution of carbohydrates and proteins. Continental Shelf Research, 138: 95–105. doi: 10.1016/j.csr.2017.01.010
    Lorrain A, Houlbrèque F, Benzoni F, et al. 2017. Seabirds supply nitrogen to reef-building corals on remote Pacific islets. Scientific Reports, 7(1): 3721. doi: 10.1038/s41598-017-03781-y
    Martínez-Moreno J, Hogg A M, England M H, et al. 2021. Global changes in oceanic mesoscale currents over the satellite altimetry record. Nature Climate Change, 11(5): 397–403. doi: 10.1038/s41558-021-01006-9
    Massaro R F S, De Carlo E H, Drupp P S, et al. 2012. Multiple factors driving variability of CO2 exchange between the ocean and atmosphere in a tropical coral reef environment. Aquatic Geochemistry, 18(4): 357–386. doi: 10.1007/s10498-012-9170-7
    McMahon A, Santos I R. 2017. Nitrogen enrichment and speciation in a coral reef lagoon driven by groundwater inputs of bird guano. Journal of Geophysical Research: Oceans, 122(9): 7218–7236. doi: 10.1002/2017JC012929
    McManus M A, Benoit-Bird K J, Brock Woodson C. 2008. Behavior exceeds physical forcing in the diel horizontal migration of the midwater sound-scattering layer in Hawaiian waters. Marine Ecology Progress Series, 365: 91–101. doi: 10.3354/meps07491
    McMurray S E, Stubler A D, Erwin P M, et al. 2018. A test of the sponge-loop hypothesis for emergent Caribbean reef sponges. Marine Ecology Progress Series, 588: 1–14. doi: 10.3354/meps12466
    Meunier V, Bonnet S, Pernice M, et al. 2019. Bleaching forces coral’s heterotrophy on diazotrophs and Synechococcus. The ISME Journal, 13(11): 2882–2886. doi: 10.1038/s41396-019-0456-2
    Meyer J L, Schultz E T. 1985. Tissue condition and growth rate of corals associated with schooling fish. Limnology and Oceanography, 30(1): 157–166. doi: 10.4319/lo.1985.30.1.0157
    Meyer J L, Schultz E T, Helfman G S. 1983. Fish schools: an asset to corals. Science, 220(4601): 1047–1049. doi: 10.1126/science.220.4601.1047
    Mueller B, den Haan J, Visser P M, et al. 2016. Effect of light and nutrient availability on the release of dissolved organic carbon (DOC) by Caribbean turf algae. Scientific Reports, 6: 23248. doi: 10.1038/srep23248
    Nagelkerken I. 2009. Ecological Connectivity Among Tropical Coastal Ecosystems. Dordrecht: Springer
    Nelson C E, Alldredge A L, McCliment E A, et al. 2011. Depleted dissolved organic carbon and distinct bacterial communities in the water column of a rapid-flushing coral reef ecosystem. The ISME Journal, 5(8): 1374–1387. doi: 10.1038/ismej.2011.12
    Newman M J H, Paredes G A, Sala E, et al. 2006. Structure of Caribbean coral reef communities across a large gradient of fish biomass. Ecology Letters, 9(11): 1216–1227. doi: 10.1111/j.1461-0248.2006.00976.x
    Ning Zhiming, Yu Kefu, Wang Yinghui, et al. 2019. Carbon and nutrient dynamics of permeable carbonate and silicate sands adjacent to coral reefs around Weizhou Island in the northern South China Sea. Estuarine, Coastal and Shelf Science, 225: 106229
    Odum E P, Barrett G W. 2005. Fundamentals of Ecology. 5th ed. Belmont: Thomson Brooks/Cole
    Odum H T, Odum E P. 1955. Trophic structure and productivity of a windward coral reef community on Eniwetok atoll. Ecological Monographs, 25(3): 291–320. doi: 10.2307/1943285
    Palacios D M. 2002. Factors influencing the island-mass effect of the Galápagos Archipelago. Geophysical Research Letters, 29(23): 2134
    Patten N L, Wyatt A S J, Lowe R J, et al. 2011. Uptake of picophytoplankton, bacterioplankton and virioplankton by a fringing coral reef community (Ningaloo Reef, Australia). Coral Reefs, 30(3): 555–567. doi: 10.1007/s00338-011-0777-8
    Pawlik J R, Loh T L, McMurray S E. 2018. A review of bottom-up vs. top-down control of sponges on Caribbean fore-reefs: what’s old, what’s new, and future directions. PeerJ, 6: e4343. doi: 10.7717/peerj.4343
    Pawlik J R, McMurray S E. 2020. The emerging ecological and biogeochemical importance of sponges on coral reefs. Annual Review of Marine Science, 12: 315–337
    Peel L R, Daly R, Daly C A K, et al. 2019. Stable isotope analyses reveal unique trophic role of reef manta rays (Mobula alfredi) at a remote coral reef. Royal Society Open Science, 6(9): 190599. doi: 10.1098/rsos.190599
    Peirano A, Morri C, Bianchi C N, et al. 2001. Biomass, carbonate standing stock and production of the Mediterranean coral Cladocora caespitosa (L. ). Facies, 44(1): 75–80. doi: 10.1007/BF02668168
    Pinnegar J K, Polunin N V C. 2006. Planktivorous damselfish support significant nitrogen and phosphorus fluxes to Mediterranean reefs. Marine Biology, 148(5): 1089–1099. doi: 10.1007/s00227-005-0141-z
    Polovina J J. 1984. Model of a coral reef ecosystem I. The ECOPATH model and its application to French Frigate Shoals. Coral Reefs, 3(1): 1–11. doi: 10.1007/BF00306135
    Pupier C A, Bednarz V N, Grover R, et al. 2019. Divergent capacity of scleractinian and soft corals to assimilate and transfer diazotrophically derived nitrogen to the reef environment. Frontiers in Microbiology, 10: 1860. doi: 10.3389/fmicb.2019.01860
    Purcell S W, Conand C, Uthicke S, et al. 2016. Ecological roles of exploited sea cucumbers. In: Hughes R N, Hughes D J, Smith I P, et al., eds. Oceanography and Marine Biology: An Annual Review, Vol. 54. Boca Raton: CRC Press, 367–386
    Qiu Dajun, Huang Liangmin, Huang Hui, et al. 2010. Two functionally distinct ciliates dwelling in Acropora corals in the South China Sea near Sanya, Hainan Province, China. Applied and Environmental Microbiology, 76(16): 5639–5643. doi: 10.1128/AEM.03009-09
    Rädecker N, Pogoreutz C, Voolstra C R, et al. 2015. Nitrogen cycling in corals: the key to understanding holobiont functioning?. Trends in Microbiology, 23(8): 490–497
    Radice V Z, Hoegh-Guldberg O, Fry B, et al. 2019. Upwelling as the major source of nitrogen for shallow and deep reef-building corals across an oceanic atoll system. Functional Ecology, 33(6): 1120–1134. doi: 10.1111/1365-2435.13314
    Reid S B, Hirota J, Young R E, et al. 1991. Mesopelagic-boundary community in Hawaii: micronekton at the interface between neritic and oceanic ecosystems. Marine Biology, 109(3): 427–440. doi: 10.1007/BF01313508
    Ribes M, Coma R, Atkinson M J, et al. 2005. Sponges and ascidians control removal of particulate organic nitrogen from coral reef water. Limnology and Oceanography, 50(5): 1480–1489. doi: 10.4319/lo.2005.50.5.1480
    Rice M M, Maher R L, Vega Thurber R, et al. 2019. Different nitrogen sources speed recovery from corallivory and uniquely alter the microbiome of a reef-building coral. PeerJ, 7: e8056
    Richardson T L. 2019. Mechanisms and pathways of small-phytoplankton export from the surface ocean. Annual Review of Marine Science, 11: 57–74. doi: 10.1146/annurev-marine-121916-063627
    Richardson T L, Jackson G A. 2007. Small phytoplankton and carbon export from the surface ocean. Science, 315(5813): 838–840. doi: 10.1126/science.1133471
    Richter C, Wunsch M, Rasheed M, et al. 2001. Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges. Nature, 413(6857): 726–730. doi: 10.1038/35099547
    Rix L, de Goeij J M, van Oevelen D, et al. 2017. Differential recycling of coral and algal dissolved organic matter via the sponge loop. Functional Ecology, 31(3): 778–789. doi: 10.1111/1365-2435.12758
    Rix L, de Goeij J M, van Oevelen D, et al. 2018. Reef sponges facilitate the transfer of coral-derived organic matter to their associated fauna via the sponge loop. Marine Ecology Progress Series, 589: 85–96. doi: 10.3354/meps12443
    Roopin M, Henry R P, Chadwick N E. 2008. Nutrient transfer in a marine mutualism: patterns of ammonia excretion by anemonefish and uptake by giant sea anemones. Marine Biology, 154(3): 547–556. doi: 10.1007/s00227-008-0948-5
    Ruiz Sebastián C, McClanahan T R. 2013. Description and validation of production processes in the coral reef ecosystem model CAFFEE (Coral–Algae–Fish-Fisheries Ecosystem Energetics) with a fisheries closure and climatic disturbance. Ecological Modelling, 263: 326–348. doi: 10.1016/j.ecolmodel.2013.05.012
    Sambrook K, Bonin M C, Bradley M, et al. 2020. Broadening our horizons: seascape use by coral reef-associated fishes in Kavieng, Papua New Guinea, is common and diverse. Coral Reefs, 39(4): 1187–1197. doi: 10.1007/s00338-020-01954-2
    Sandin S A, Smith J E, Demartini E E, et al. 2008. Baselines and degradation of coral reefs in the northern Line Islands. PLoS ONE, 3(2): e1548. doi: 10.1371/journal.pone.0001548
    Savage C. 2019. Seabird nutrients are assimilated by corals and enhance coral growth rates. Scientific Reports, 9(1): 4284. doi: 10.1038/s41598-019-41030-6
    Schöttner S, Pfitzner B, Grünke S, et al. 2011. Drivers of bacterial diversity dynamics in permeable carbonate and silicate coral reef sands from the Red Sea. Environmental Microbiology, 13(7): 1815–1826. doi: 10.1111/j.1462-2920.2011.02494.x
    Sebens K P, Vandersall K S, Savina L A, et al. 1996. Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Marine Biology, 127(2): 303–317. doi: 10.1007/BF00942116
    Shantz A A, Ladd M C, Schrack E, et al. 2015. Fish-derived nutrient hotspots shape coral reef benthic communities. Ecological Applications, 25(8): 2142–2152. doi: 10.1890/14-2209.1
    Sheng Huaxia, Wan X S, Zou Bobo, et al. 2023. An efficient diazotroph-derived nitrogen transfer pathway in coral reef system. Limnology and Oceanography, 68: 963–981
    Shiozaki T, Kodama T, Furuya K. 2014. Large-scale impact of the island mass effect through nitrogen fixation in the western South Pacific Ocean. Geophysical Research Letters, 41(8): 2907–2913. doi: 10.1002/2014GL059835
    Silveira C B, Silva-Lima A W, Francini-Filho R B, et al. 2015. Microbial and sponge loops modify fish production in phase-shifting coral reefs. Environmental Microbiology, 17(10): 3832–3846. doi: 10.1111/1462-2920.12851
    Starke C, Ekau W, Moosdorf N. 2020. Enhanced productivity and fish abundance at a submarine spring in a coastal lagoon on Tahiti, French Polynesia. Frontiers in Marine Science, 6: 809. doi: 10.3389/fmars.2019.00809
    Staunton Smith J, Johnson C R. 1995. Nutrient inputs from seabirds and humans on a populated coral cay. Marine Ecology Progress Series, 124: 189–200. doi: 10.3354/meps124189
    Suzuki A, Kawahata H. 2003. Carbon budget of coral reef systems: an overview of observations in fringing reefs, barrier reefs and atolls in the Indo-Pacific regions. Tellus B: Chemical and Physical Meteorology, 55(2): 428–444. doi: 10.3402/tellusb.v55i2.16761
    Suzuki A, Kawahata H, Ayukai T, et al. 2001. The oceanic CO2 system and carbon budget in the Great Barrier Reef, Australia. Geophysical Research Letters, 28(7): 1243–1246. doi: 10.1029/2000GL011875
    Tait D R, Erler D V, Santos I R, et al. 2014. The influence of groundwater inputs and age on nutrient dynamics in a coral reef lagoon. Marine Chemistry, 166: 36–47. doi: 10.1016/j.marchem.2014.08.004
    Tanaka Y, Miyajima T, Koike I, et al. 2008. Production of dissolved and particulate organic matter by the reef-building corals Porites cylindrica and Acropora pulchra. Bulletin of Marine Science, 82(2): 237–245
    Tanaka Y, Miyajima T, Watanabe A, et al. 2011a. Distribution of dissolved organic carbon and nitrogen in a coral reef. Coral Reefs, 30(2): 533–541. doi: 10.1007/s00338-011-0735-5
    Tanaka Y, Ogawa H, Miyajima T. 2011b. Production and bacterial decomposition of dissolved organic matter in a fringing coral reef. Journal of Oceanography, 67(4): 427–437. doi: 10.1007/s10872-011-0046-z
    Thornhill D J, Rotjan R D, Todd B D, et al. 2011. A connection between colony biomass and death in Caribbean reef-building corals. PLoS ONE, 6(12): e29535. doi: 10.1371/journal.pone.0029535
    Tilstra A, van Hoytema N, Cardini U, et al. 2018. Effects of water column mixing and stratification on planktonic primary production and dinitrogen fixation on a northern Red Sea coral reef. Frontiers in Microbiology, 9: 2351. doi: 10.3389/fmicb.2018.02351
    Torréton J P, Dufour P. 1996. Temporal and spatial stability of bacterioplankton biomass and productivity in an atoll lagoon. Aquatic Microbial Ecology, 11: 251–261. doi: 10.3354/ame011251
    Torréton J P, Pagès J, Talbot V. 2002. Relationships between bacterioplankton and phytoplankton biomass, production and turnover rate in Tuamotu atoll lagoons. Aquatic Microbial Ecology, 28: 267–277. doi: 10.3354/ame028267
    Turk-Kubo K A, Frank I E, Hogan M E, et al. 2015. Diazotroph community succession during the VAHINE mesocosm experiment (New Caledonia lagoon). Biogeosciences, 12(24): 7435–7452. doi: 10.5194/bg-12-7435-2015
    Uthicke S. 2001a. Interactions between sediment-feeders and microalgae on coral reefs: grazing losses versus production enhancement. Marine Ecology Progress Series, 210: 125–138. doi: 10.3354/meps210125
    Uthicke S. 2001b. Nutrient regeneration by abundant coral reef holothurians. Journal of Experimental Marine Biology and Ecology, 265(2): 153–170. doi: 10.1016/S0022-0981(01)00329-X
    Vega Thurber R L, Burkepile D E, Fuchs C, et al. 2014. Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Global Change Biology, 20: 544–554
    Venn A A, Loram J E, Douglas A E. 2008. Photosynthetic symbioses in animals. Journal of Experimental Botany, 59(5): 1069–1080. doi: 10.1093/jxb/erm328
    Ware J R, Smith S V, Reaka-Kudla M L. 1992. Coral reefs: sources or sinks of atmospheric CO2?. Coral Reefs, 11(3): 127–130
    Weber L, Gonzalez-Díaz P, Armenteros M, et al. 2019. The coral ecosphere: a unique coral reef habitat that fosters coral–microbial interactions. Limnology and Oceanography, 64(6): 2373–2388. doi: 10.1002/lno.11190
    Wiebe W J, Johannes R E, Webb K L. 1975. Nitrogen fixation in a coral reef community. Science, 188(4185): 257–259. doi: 10.1126/science.188.4185.257
    Wild C, Huettel M, Klueter A, et al. 2004a. Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature, 428(6978): 66–70. doi: 10.1038/nature02344
    Wild C, Niggl W, Naumann M S, et al. 2010. Organic matter release by Red Sea coral reef organisms—potential effects on microbial activity and in situ O2 availability. Marine Ecology Progress Series, 411: 61–71. doi: 10.3354/meps08653
    Wild C, Rasheed M, Werner U, et al. 2004b. Degradation and mineralization of coral mucus in reef environments. Marine Ecology Progress Series, 267: 159–171. doi: 10.3354/meps267159
    Wilkinson C R, Fay P. 1979. Nitrogen fixation in coral reef sponges with symbiotic cyanobacteria. Nature, 279(5713): 527–529. doi: 10.1038/279527a0
    Williams I D, Baum J K, Heenan A, et al. 2015. Human, oceanographic and habitat drivers of central and western Pacific coral reef fish assemblages. PLoS ONE, 10(4): e0120516. doi: 10.1371/journal.pone.0120516
    Williams J J, Papastamatiou Y P, Caselle J E, et al. 2018. Mobile marine predators: an understudied source of nutrients to coral reefs in an unfished atoll. Proceedings of the Royal Society B: Biological Sciences, 285(1875): 20172456. doi: 10.1098/rspb.2017.2456
    Wu Chengye, Zhang Jianlin, Huang Liangmin. 2001. Primary productivity in some coral reef lagoons and their adjacent sea areas of Nansha Islands in spring. Journal of Tropical Oceanography (in Chinese), 20(3): 59–67
    Wyatt A S J, Falter J L, Lowe R J, et al. 2012. Oceanographic forcing of nutrient uptake and release over a fringing coral reef. Limnology and Oceanography, 57(2): 401–419. doi: 10.4319/lo.2012.57.2.0401
    Wyatt A S J, Leichter J J, Toth L T, et al. 2020. Heat accumulation on coral reefs mitigated by internal waves. Nature Geoscience, 13(1): 28–34. doi: 10.1038/s41561-019-0486-4
    Wyatt A S J, Lowe R J, Humphries S, et al. 2010. Particulate nutrient fluxes over a fringing coral reef: relevant scales of phytoplankton production and mechanisms of supply. Marine Ecology Progress Series, 405: 113–130. doi: 10.3354/meps08508
    Wyatt A S J, Lowe R J, Humphries S, et al. 2013. Particulate nutrient fluxes over a fringing coral reef: Source-sink dynamics inferred from carbon to nitrogen ratios and stable isotopes. Limnology and Oceanography, 58(1): 409–427. doi: 10.4319/lo.2013.58.1.0409
    Xu Shendong, Zhang Zhinan, Yu Kefu, et al. 2021. Spatial variations in the trophic status of Favia palauensis corals in the South China Sea: insights into their different adaptabilities under contrasting environmental conditions. Science China: Earth Sciences, 64(6): 839–852. doi: 10.1007/s11430-020-9774-0
    Yahel G, Post A F, Fabricius K, et al. 1998. Phytoplankton distribution and grazing near coral reefs. Limnology and Oceanography, 43(4): 551–563. doi: 10.4319/lo.1998.43.4.0551
    Yamaguchi R, Suga T. 2019. Trend and variability in global upper-ocean stratification since the 1960s. Journal of Geophysical Research: Oceans, 124(12): 8933–8948. doi: 10.1029/2019JC015439
    Yan Hongqiang, Yu Kefu, Shi Qi, et al. 2016. Seasonal variations of seawater pCO2 and sea-air CO2 fluxes in a fringing coral reef, northern South China Sea. Journal of Geophysical Research: Oceans, 121(1): 998–1008. doi: 10.1002/2015JC011484
    Zaneveld J R, Burkepile D E, Shantz A A, et al. 2016. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nature Communications, 7: 11833
    Zhang Fan, Blasiak L C, Karolin J O, et al. 2015. Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges. Proceedings of the National Academy of Sciences of the United States of America, 112(14): 4381–4386. doi: 10.1073/pnas.1423768112
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索


    Article Metrics

    Article views (659) PDF downloads(73) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint