Macroalgal assemblage changes on coral reefs along a natural gradient from fish farms in southern Hainan Island

Authors

  • Xiubao Li State Key Laboratory of Estuarine and Coastal Research, East China Normal University, Shanghai 200062, China
  • Eduard A. Titlyanov A. V. Zhirmunsky Institute of Marine Biology, Far Eastern Branch of the Russian Academy of Sciences, Palchevskogo 17, Vladivostok 690059, Russia
  • Jing Zhang State Key Laboratory of Estuarine and Coastal Research, East China Normal University, Shanghai 200062, China
  • Tamara V. Titlyanova A. V. Zhirmunsky Institute of Marine Biology, Far Eastern Branch of the Russian Academy of Sciences, Palchevskogo 17, Vladivostok 690059, Russia
  • Guosen Zhang State Key Laboratory of Estuarine and Coastal Research, East China Normal University, Shanghai 200062, China
  • Hui Huang Key Laboratory of Tropical Marine Bio-Resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China

Keywords:

species richness, algal blooms, aquaculture effluents, South China Sea

Abstract

Degradation processes on coral reefs are associated with changes in macroalgal assemblages. In this study, a floristic study of the macrophyte species on coral reefs along a pollution gradient at 3 transects in southern Hainan Island, China, was conducted in April 2014. A total of 73 benthic macroalgal taxa were collected, of which 58% were reds, 23% browns and 19% greens. Along with the distance away from the outlet of fish farms, macroalgal species richness increased significantly from 40 species to 71 species. However, macroalgal biomass decreased from 1.58 kg m−2 to 1.1 kg m−2. Brown blooms of Chnoospora implexa, Padina australis, Sargassum polycystum and S. sanyaense changed to green blooms of Ulva lactuca and Caulerpa racemosa from moderately polluted sites to severely polluted sites close to the outlet. This study supports the results that severe pollution can lead not only to a significant decline of macroalgal species richness and changes in macroalgal assemblages, but also to the occurrence of green blooms. This study will hopefully provide more accurate cases to link nutrient pollution to changes in benthic organisms on coral reefs.

References

Arévalo, A., Pinedo, S., Ballesteros, E., 2007. Changes in the composition and structure of Mediterranean rocky-shore communities following a gradient of nutrient enrichment: descriptive study and test of proposed methods to assess water quality regarding macroalgae. Mar. Pollut. Bull. 55, 04–113.

Cardoso, P. G., Pardal, M. A., Lillebo, A. I., Ferreira, S. M., Raffaelli, D., Marques, J. C., 2004. Dynamic changes in seagrass assemblages under eutrophication and implications for recovery. J. Exp. Mar. Biol. Ecol. 302, 233–248.

Clarke, K. R., Gorley, R. N., 2006. PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth.

Costanzo, S. D., O'Donohue, M. J., Dennison, W. C., Loneragan, N. R., Thomas, M., 2001. A new approach for detecting and mapping sewage impacts. Mar. Pollut. Bull. 42, 149–156.

DeGeorges, A., Goreau, T. J., Reilly, B., 2010. Land-sourced pollution with an emphasis on domestic sewage: lessons from the Caribbean and implications for coastal development on Indian Ocean and Pacific coral reefs. Sustainability 2, 2919–2949.

Diaz-Pulido, G., McCook, L. J., 2002. The fate of bleached corals: patterns and dynamics of algal recruitment. Mar. Ecol. Prog. Ser. 232, 115–128.

Guinda, X., Juanes, J. A., Puente, A., Revilla, J. A., 2008. Comparison of two methods for quality assessment of macroalgae assemblages, under different pollution types. Ecol. Indic. 8, 743–753.

Guiry, M. D., Guiry, G. M., 2015. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org (accessed January 2015).

Heaton, T. H. E., 1986. Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere - a review. Chem. Geol. 59, 87–102.

Herbeck, L. S., Unger, D., 2013. Pond aquaculture effluents traced along back-reef waters by standard water quality parameters, delta N-15 in suspended matter and phytoplankton bioassays. Mar. Ecol. Prog. Ser. 478, 71–86.

Herbeck, L. S., Unger, D., Wu, Y., Jennerjahn, T. C., 2013. Effluent, nutrient and organic matter export from shrimp and fish ponds causing eutrophication in coastal and back-reef waters of NE Hainan, tropical China. Cont. Shelf. Res. 57, 92–104.

Huang, H., Li, X. B., Titlyanov, E. A., Ye, C., Titlyanova, T. V., Guo, Y. P., Zhang, J., 2013. Linking macroalgal delta N-15-values to nitrogen sources and effects of nutrient stress on coral condition in an upwelling region. Bot. Mar. 56, 471–480.

Hughes, T. P., Huang, H., Young, M. A. L., 2013. The wicked problem of China's disappearing coral reefs. Conserv. Biol. 27, 261–269.

Kleypas, J. A., McManus, J. W., Menez, L. A. B., 1999. Environmental limits to coral reef development: Where do we draw the line? Am. Zool. 39, 146–159.

Lapointe, B. E., 1997. Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol. Oceanogr. 42, 1119–1131.

Lapointe, B. E., Clark, M. W., 1992. Nutrient inputs from the watershed and coastal eutrophication in the Florida Keys. Estuaries 15, 465–476.

Largo, D. B., Sembrano, J., Hiraoka, M., Ohno, M., 2004. Taxonomic and ecological profile of ‘green tide’ species of Ulva (Ulvales, Chlorophyta) in central Philippines. Hydrobiologia 512, 247–253.

Li, X. B., Huang, H., Lian, J. S., Yang, J. H., Ye, C., Chen, Y. Q., Huang, L. M., 2013. Coral community changes in response to a high sedimentation event: A case study in southern Hainan Island. Chin. Sci. Bull. 58, 1028–1037.

Li, X. B., Liu, S., Huang, H., Huang, L. M., Jing, Z. Y., Zhang, C. L., 2012. Coral bleaching caused by an abnormal water temperature rise at Luhuitou fringing reef, Sanya Bay, China. Aquat. Ecosyst. Health Mgmt. 15(2), 227–233.

Li, X. B., Wang, D. R., Huang, H., Zhang, J., Lian, J. S., Yuan, X. C., Yang, J. H., Zhang, G. S., 2015. Linking benthic community structure to terrestrial runoff and upwelling in the coral reefs of northeastern Hainan Island. Estuarine, Coastal and Shelf Science 156, 92–102.

Liu, J. Y., 2008. Checklist of marine biota of China Seas. Scientific Book Service Company, Beijing.

Liu, S. M., Li, R. H., Zhang, G. L., Wang, D. R., Du, J. Z., Herbeck, L. S., Zhang, J., Ren, J. L., 2011. The impact of anthropogenic: activities on nutrient dynamics in the tropical Wenchanghe and Wenjiaohe Estuary and Lagoon system in East Hainan, China. Mar. Chem. 125, 49–68.

Nelson, T. A., Nelson, A. V., Tjoelker, M., 2003. Seasonal and spatial patterns of “Green tides” (Ulvoid algal blooms) and related water quality parameters in the coastal waters of Washington state, USA. Bot. Mar. 46, 263–275.

Saunders, G. W., Hommersand, M. H., 2004. Assessing red algal supraordinal diversity and taxonomy in the context of contemporary systematic data. American Journal of Botany 91, 1494–1507.

Su, N., Du, J. Z., Moore, W. S., Liu, S. M., Zhang, J., 2011. An examination of groundwater discharge and the associated nutrient fluxes into the estuaries of eastern Hainan Island, China using Ra-226. Sci. Total Environ. 409, 3909–3918.

Thornber, C. S., DiMilla, P., Nixon, S. W., McKinney, R. A., 2008. Natural and anthropogenic nitrogen uptake by bloom-forming macroalgae. Mar. Pollut. Bull. 56, 261–269.

Titlyanov, E. A., Titlyanova, T. V., 2008. Coral-algal competition on damaged reefs. Russ. J. Mar. Biol. 34, 199–219.

Titlyanov, E. A., Kiyashko, S. I., Titlyanova, T. V., Yakovleva, I. M., Li, X. B., Huang, H., 2011a. Nitrogen sources to macroalgal growth in Sanya Bay (Hainan Island, China). Current Development in Oceanography 2, 65–84.

Titlyanov, E. A., Titlyanova, T. V., Xia, B. M., Bartsch, I., 2011b. Checklist of marine benthic green algae (Chlorophyta) on Hainan, a subtropical island off the coast of China: comparisons between the 1930s and 1990–2009 reveal environmental changes. Bot. Mar. 54, 523–535.

Titlyanova, T. V., Titlyanov, E. A., Xia, B. M., Bartsch, I.. 2012. New records of benthic marine green algae (Chlorophyta) for the island of Hainan (China). Nova Hedwigia 94, 441–470.

Titlyanov, E. A., Titlyanova, T. V., Huang, H., Li, X. B., 2014a. Seasonal changes in benthic algal communities of the upper subtidal zone in Sanya Bay (Hainan Island, China). J. Mar. Biol. Assoc. Uk. 94, 51–64.

Titlyanova, T. V., Titlyanov, E. A., Kalita, T. L., 2014b. Marine algal flora of Hainan Island: a comprehensive synthesis. Coastal Ecosystems 1, 28–53.

Titlyanov, E. A., Titlyanova, T. V., Li, X. B., Kalita, T. L., Huang, H., 2014c. Recent (2008–2012) seaweed flora of Hainan Island, South China Sea. Marine Biology Research. http://dx.doi.org/10.1080/17451000.2014.955803.

Tsiamis, K., Panayotidis, P., Salomidi, M., Pavlidou, A., Kleinteich, J., Balanika, K., Kupper, F. C., 2013. Macroalgal community response to re-oligotrophication in Saronikos Gulf. Mar. Ecol. Prog. Ser. 472, 73–85.

Tsuda, R. T., 2003. Checklist and bibliography of the marine benthic algae from the Mariana Islands (Guam and CNMI). University of Guam. Technical Report 107, 1–37.

Wang, D. R., Wang, H. J., Li, Y. C., Yang, Y., Liang, W., 2011. Preliminary study of coral larvae supplementary source around Leizhou Peninsula. Journal of Trophical Oceanography 30, 26–32 (in Chinese).

Wu, Y., Bao, H. Y., Unger, D., Herbeck, L. S., Zhu, Z. Y., Zhang, J., Jennerjahn, T. C., 2013. Biogeochemical behavior of organic carbon in a small tropical river and estuary, Hainan, China. Cont. Shelf Res. 57, 32–43.

Zhang, Q. M., Shi. Q., Chen, G., Fong, T. C. W., Wong, D. C. C., Huang, H., Wang, H. K., Zhao, M. X., 2006. Status monitoring and health assessment of Luhuitou fringing reef of Sanya, Hainan, China. Chin. Sci. Bull. 51, 81–88.

Zhou, Z. G., 2004. Status and protecton strategies on coral reefs in Hannan Island. Ocean Development and Management 6, 48–51 (in Chinese).

Published

2016-01-02

Issue

Section

Research article