Home Linking macroalgal δ15N-values to nitrogen sources and effects of nutrient stress on coral condition in an upwelling region
Article
Licensed
Unlicensed Requires Authentication

Linking macroalgal δ15N-values to nitrogen sources and effects of nutrient stress on coral condition in an upwelling region

  • Hui Huang , Xiu Bao Li EMAIL logo , Eduard A. Titlyanov , Cheng Ye , Tamara V. Titlyanova , Ya Ping Guo and Jing Zhang
Published/Copyright: September 6, 2013
Botanica Marina
From the journal Botanica Marina Volume 56 Issue 5-6

Abstract

Land-based sewage pollution is a major threat to the health of near-shore coral reefs. Macroalgal δ15N-values are useful indicators for tracking nitrogen sources and sewage input; however, the direct link between δ15N-values of macroalgae and the coral condition, including live coral cover, species richness, and juvenile coral density, is unclear. Macroalgal δ15N-values of two species, Lobophora variegata and Tricleocarpa oblongata, were measured in Wenchang (northeast Hainan Island, South China Sea) in both the dry and wet seasons, to assess the influence of nitrogen sources and nutrient stress resulting from sewage input or upwelling on the condition of corals. Macroalgal δ15N-values showed that shallow stations between the reef and the coast were severely affected by sewage input (e.g., river discharges and aquaculture ponds), whereas deep stations on the outside of the reef were influenced by upwelling-based nutrients. Correlation and redundancy analysis demonstrated that δ15N-values of L. variegata had a stronger relation with coral condition than any other environmental parameter (e.g., water quality index, turbidity, and dissolved nutrients), with significant negative correlations in both the dry and wet seasons. Thus, macroalgal δ15N-values can be used to determine where nutrient stress is negatively affecting corals, highlighting the links of human activities and coastal upwelling with marine ecosystems.

Keywords: coral condition; macroalgae; nitrogen sources; nutrient stress; stable isotope; upwelling
Corresponding author: Xiu Bao Li, CAS Key Laboratory of Tropical Marine Bioresources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China, e-mail:

This work was supported by the National Natural Science Foundation of China (40830850, 41106141, 40931160437, and 41106107), the National Key Technology R and D Program (2009BAB44B01), the Open Research Fund of State Key Laboratory of Estuarine and Coastal Research (SKLEC-KF201307), and the Ocean Public Welfare Scientific Research Project (201005012-6 and 201105012-2).

References

Cooper, T.F., J.P. Gilmour and K.E. Fabricius. 2009. Bio-indicators of changes in water quality on coral reefs: review and recommendations for monitoring programmes. Coral Reefs 28: 589–606.10.1007/s00338-009-0512-xSearch in Google Scholar

Cooper, T.F., R. Berkelmans, K.E. Ulstrup, S. Weeks, B. Radford, A.M. Jones, J. Doyle, M. Canto, R.A. O’Leary and M.J.H. van Oppen. 2011. Environmental factors controlling the distribution of symbiodinium harboured by the coral Acropora millepora on the Great Barrier Reef. PLOS One 6: e25536. DOI:10.1371/journal.pone.0025536.10.1371/journal.pone.0025536Search in Google Scholar

Costanzo, S.D., M.J. O’Donohue, W.C. Dennison, N.R. Loneragan and M. Thomas. 2001. A new approach for detecting and mapping sewage impacts. Mar. Pollut. Bull. 42: 149–156.10.1016/S0025-326X(00)00125-9Search in Google Scholar

Costanzo, S.D., M.J. O’Donohue and W.C. Dennison. 2004. Assessing the influence and distribution of shrimp pond effluent in a tidal mangrove creek in north-east Australia. Mar. Pollut. Bull. 48: 514–525.10.1016/j.marpolbul.2003.09.006Search in Google Scholar

Diaz-Pulido, G. and J. Garzon-Ferreira. 2002. Seasonality in algal assemblages on upwelling-influenced coral reefs in the Colombian Caribbean. Bot. Mar. 45: 284–292.10.1515/BOT.2002.028Search in Google Scholar

Edmunds, P.J., R.B. Aronson, D.W. Swanson, D.R. Levitan and W.F. Precht. 1998. Photographic versus visual census techniques for the quantification of juvenile corals. Bull. Mar. Sci. 62: 937–946.Search in Google Scholar

Fabricius, K.E. 2011. Factors determining the resilience of coral reefs to eutrophication: a review and conceptual model. In: (Z. Dubinsky and N. Stambler, eds.) Coral reefs: an ecosystem in transition. Springer Press, Dordrecht. pp. 493–505.Search in Google Scholar

Fabricius, K., G. De’ath, L. McCook, E. Turak and D.M. Williams. 2005. Changes in algal, coral and fish assemblages along water quality gradients on the inshore Great Barrier Reef. Mar. Pollut. Bull. 51: 384–398.Search in Google Scholar

Fabricius, K.E., T.F. Cooper, C. Humphrey, S. Uthicke, G. De’ath, J. Davidson, H. LeGrand, A. Thompson and B. Schaffelke. 2012. A bio-indicator system for water quality on inshore coral reefs of the Great Barrier Reef. Mar. Pollut. Bull. 65: 320–332.10.1016/j.marpolbul.2011.09.004Search in Google Scholar

Firstater, F.N., F.J. Hidalgo, B.J. Lomovasky, J. Tarazona, G. Flores and O.O. Iribarne. 2010. Coastal upwelling may overwhelm the effect of sewage discharges in rocky intertidal communities of the Peruvian coast. Mar. Freshwater Res. 61: 309–319.10.1071/MF09102Search in Google Scholar

Foster, N.L., S.J. Box and P.J. Mumby. 2008. Competitive effects of macroalgae on the fecundity of the reef-building coral Montastraea annularis. Mar. Ecol. Prog. Ser. 367: 143–152.10.3354/meps07594Search in Google Scholar

Fourqurean, J.W., T.O. Moore, B. Fry and J.T. Hollibaugh. 1997. Spatial and temporal variation in C:N:P ratios, δ15N and δ13C of eelgrass Zostera marina as indicators of ecosystem processes, Tomales Bay, California, USA. Mar. Ecol. Prog. Ser. 157: 147–157.Search in Google Scholar

Garcia-Sanz, T., J.M. Ruiz-Fernandez, M. Ruiz, R. Garcia, M.N. Gonzalez and M. Perez. 2010. An evaluation of a macroalgal bioassay tool for assessing the spatial extent of nutrient release from offshore fish farms. Mar. Environ. Res. 70: 189–200.10.1016/j.marenvres.2010.05.001Search in Google Scholar

Han, W.Y., M.B. Wang and K.B. Ma. 1990. The lowest surface water temperature area of China Sea in summer-the upwelling along the east coast of Hainan Island (in Chinese). Oceanol. Limnol. Sin. 21: 167–275.Search in Google Scholar

Heaton, T.H.E. 1986. Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere – a review. Chem. Geol. 59: 87–102.10.1016/0168-9622(86)90059-XSearch in Google Scholar

Herbeck, L.S., D. Unger, U. Krumme, S.M. Liu and T.C. Jennerjahn. 2011. Typhoon-induced precipitation impact on nutrient and suspended matter dynamics of a tropical estuary affected by human activities in Hainan, China. Estuar. Coast. Shelf S. 93: 375–388.10.1016/j.ecss.2011.05.004Search in Google Scholar

Herbeck, L.S., D. Unger, Y. Wu and T.C. Jennerjahn. 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: 92–104.10.1016/j.csr.2012.05.006Search in Google Scholar

Jing, Z.Y., Y.Q. Qi, Z.L. Hua and H. Zhang. 2009. Numerical study on the summer upwelling system in the northern continental shelf of the South China Sea. Cont. Shelf Res. 29: 467–478.10.1016/j.csr.2008.11.008Search in Google Scholar

Jompa, J. and L.J. McCook. 2002. The effects of nutrients and herbivory on competition between a hard coral (Porites cylindrica) and a brown alga (Lobophora variegata). Limnol. Oceanogr. 47: 527–534.10.4319/lo.2002.47.2.0527Search in Google Scholar

Jones, A.B., M.J. O’Donohue, J. Udy and W.C. Dennison. 2001. Assessing ecological impacts of shrimp and sewage effluent: biological indicators with standard water quality analyses. Estuar. Coast. Shelf S. 52: 91–109.10.1006/ecss.2000.0729Search in Google Scholar

Kuffner, I.B., L.J. Walters, M.A. Becerro, V.J. Paul, R. Ritson-William and K.S. Beach. 2006. Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar. Ecol. Prog. Ser. 323: 107–117.10.3354/meps323107Search in Google Scholar

Lapointe, B.E., P.J. Barile, M.M. Littler and D.S. Littler. 2005. Macroalgal blooms on southeast Florida coral reefs II. Cross-shelf discrimination of nitrogen sources indicates widespread assimilation of sewage nitrogen. Harmful Algae 4: 1106–1122.10.1016/j.hal.2005.06.002Search in Google Scholar

Li, X.B. 2011. Identification of major factors influencing the composition, spatial and temporal variation of scleractinian coral community in Sanya, China (in Chinese). PhD thesis. Chinese Academy of Sciences, Beijing. pp. 1–107.Search in Google Scholar

Li, X.B., H. Huang, J.S. Lian, J.H. Yang, C. Ye, Y.Q. Chen and L.M. Huang. 2013. Coral community changes in response to a high sedimentation event: a case study in a turbid bay of south Hainan Island, China. Chin. Sci. Bull. 58: 1028–1037.10.1007/s11434-012-5601-5Search in Google Scholar

Lin, H.J., C.Y. Wu, S.J. Kao, W.Y. Kao and P.J. Meng. 2007. Mapping anthropogenic nitrogen through point sources in coral reefs using δ15N in macroalgae. Mar. Ecol. Prog. Ser. 335: 95–109.10.3354/meps335095Search in Google Scholar

Liu, S.M., R.H. Li, G.L. Zhang, D.R. Wang, J.Z. Du, L.S. Herbeck, J. Zhang and J.L. Ren. 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: 49–68.10.1016/j.marchem.2011.02.003Search in Google Scholar

Nadon, M.O. and G. Stirling. 2006. Field and simulation analyses of visual methods for sampling coral cover. Coral Reefs 25: 177–185.10.1007/s00338-005-0074-5Search in Google Scholar

Parsons, M.L., W.J. Walsh, C.J. Settlemier, D.J. White, J.M. Ballauer, P.M. Ayotte, K.M. Osada and B. Carman. 2008. A multivariate assessment of the coral ecosystem health of two embayments on the lee of the island of Hawaii. Mar. Pollut. Bull. 56: 1138–1149.10.1016/j.marpolbul.2008.03.004Search in Google Scholar PubMed

Pastorok, R.A. and G.R. Bilyard. 1985. Effects of sewage pollution on coral reef communities. Mar. Ecol. Prog. Ser. 21: 175–189.10.3354/meps021175Search in Google Scholar

Rakocinski, C.F., J. Lyczkowski-Shultz and S.L. Richardson. 1996. Ichthyoplankton assemblage structure in Mississippi sound as revealed by canonical correspondence analysis. Estuar. Coast. Shelf S. 43: 237–257.10.1006/ecss.1996.0067Search in Google Scholar

Reopanichkul, P., T.A. Schlacher, R.W. Carter and S. Worachananant. 2009. Sewage impacts coral reefs at multiple levels of ecological organization. Mar. Pollut. Bull. 58: 1356–1362.10.1016/j.marpolbul.2009.04.024Search in Google Scholar PubMed

Risk, M.J., B.E. Lapointe, O.A. Sherwood and B.J. Bedford. 2009. The use of δ15N in assessing sewage stress on coral reefs. Mar. Pollut. Bull. 58: 793–802.10.1016/j.marpolbul.2009.02.008Search in Google Scholar PubMed

Smith, J.E., J.W. Runcie and C.M. Smith. 2005. Characterization of a large-scale ephemeral bloom of the green alga Cladophora sericea on the coral reefs of West Maui, Hawaii. Mar. Ecol. Prog. Ser. 302: 77–91.10.3354/meps302077Search in Google Scholar

Su, N., J.Z. Du, W.S. Moore, S.M. Liu and J. Zhang. 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.Search in Google Scholar

ter Braak, C.J. 1995. Oraination. In: (R.H. Jongman, C.J. ter Braak and O.F. van Tongeren, eds) Data analysis in community and landscape ecology. Cambridge University Press, Cambridge. pp. 91–173.Search in Google Scholar

Thornber, C.S., P. DiMilla, S.W. Nixon and R.A. McKinney. 2008. Natural and anthropogenic nitrogen uptake by bloom-forming macroalgae. Mar. Pollut. Bull. 56: 261–269.10.1016/j.marpolbul.2007.10.031Search in Google Scholar PubMed

Titlyanov, E.A., S.I. Kiyashko, T.V. Titlyanova, P.V. Huyen and I.M. Yakovleva. 2011. Identifying nitrogen sources for macroalgal growth in variously polluted coastal areas of southern Vietnam. Bot. Mar. 54: 367–376.10.1515/bot.2011.041Search in Google Scholar

Umezawa, Y., T. Miyajima, M. Yamamuro, H. Kayanne and I. Koike. 2002. Fine-scale mapping of land-derived nitrogen in coral reefs by δ15N in macroalgae. Limnol. Oceanogr. 47: 1405–1416.10.4319/lo.2002.47.5.1405Search in Google Scholar

Wong, G.T.F., S.W. Chung, F.K. Shiah, C.C. Chen, L.S. Wen and K.K. Liu. 2002. Nitrate anomaly in the upper nutricline in the northern South China Sea – evidence for nitrogen fixation. Geophys. Res. Lett. 29: doi:10.1029/2002GL015796.10.1029/2002GL015796Search in Google Scholar

Yoshida, N., H. Morimoto, M. Hirano, I. Koike, S. Matsuo, E. Wada, T. Saino and A. Hattori. 1989. Nitrification rates and δ15N abundances of N2O and NO3- in the Western North Pacific. Nature 342: 895–897.10.1038/342895a0Search in Google Scholar

Yoshikawa, C., Y. Yamanaka and T. Nakatsuka. 2006. Nitrate-nitrogen isotopic patterns in surface waters of the western and central equatorial Pacific. J. Oceanogr. 62: 511–525.10.1007/s10872-006-0072-4Search in Google Scholar

Zhou, G.W., H. Huang, J.S. Lian, C.L. Zhang and X.B. Li. 2011. Habitat correlation of Symbiodinium diversity in two reef-building coral species in an upwelling region, eastern Hainan Island, China. J. Mar. Biol. Assoc. UK 92: 1–8.Search in Google Scholar

Received: 2012-11-13
Accepted: 2013-8-15
Published Online: 2013-09-06
Published in Print: 2013-12-01

©2013 by Walter de Gruyter Berlin Boston

Articles in the same Issue

  1. Masthead
  2. Masthead
  3. Research articles
  4. Ecological dynamics of Zostera marina (eelgrass) in three adjacent bays in Atlantic Canada
  5. Historical and present distribution of Zostera marina in the high north (Troms County, northern Norway) – a decline over the last century
  6. Tolerance to air exposure: a feature driving the latitudinal distribution of two sibling kelp species
  7. Colpomenia bullosa crust (Phaeophyceae) stressed less by grazing than by abiotic factors in high intertidal rockpools in southeast Australia
  8. Assessment of Fucus virsoides distribution in the Gulf of Trieste (Adriatic Sea) and its relation to environmental variables
  9. Long-term changes in sublittoral macroalgal assemblages related to water quality improvement
  10. Linking macroalgal δ15N-values to nitrogen sources and effects of nutrient stress on coral condition in an upwelling region
  11. Non-coralline crustose algae associated with maerl beds in Portugal: a reappraisal of their diversity in the Atlantic Iberian beds
  12. Hydrolithon abyssophila sp. nov. (Hydrolithoideae, Corallinales), a bisporic coralline from the insular shelf edge of Puerto Rico and the Virgin Islands (US)
  13. The first record of Grateloupia subpectinata from the New Zealand region and comparison with G. prolifera, a species endemic to the Chatham Islands
  14. Neosiphonia baliana sp. nov. and N. silvae sp. nov. (Rhodomelaceae, Rhodophyta) from Bali, Indonesia
  15. Effects of density and substrate type on recruitment and growth of Pyropia torta (Rhodophyta) gametophytes
  16. Morphology and life stages of the potentially pinnatoxin-producing thecate dinoflagellate Vulcanodinium rugosum from the tropical Mexican Pacific
  17. Short communication
  18. Fungal endophytes of the seagrasses Halodule wrightii and Thalassia testudinum in the north-central Gulf of Mexico
https://doi.org/10.1515/bot-2012-0223
Keywords for this article
coral condition; macroalgae; nitrogen sources; nutrient stress; stable isotope; upwelling

Articles in the same Issue

  1. Masthead
  2. Masthead
  3. Research articles
  4. Ecological dynamics of Zostera marina (eelgrass) in three adjacent bays in Atlantic Canada
  5. Historical and present distribution of Zostera marina in the high north (Troms County, northern Norway) – a decline over the last century
  6. Tolerance to air exposure: a feature driving the latitudinal distribution of two sibling kelp species
  7. Colpomenia bullosa crust (Phaeophyceae) stressed less by grazing than by abiotic factors in high intertidal rockpools in southeast Australia
  8. Assessment of Fucus virsoides distribution in the Gulf of Trieste (Adriatic Sea) and its relation to environmental variables
  9. Long-term changes in sublittoral macroalgal assemblages related to water quality improvement
  10. Linking macroalgal δ15N-values to nitrogen sources and effects of nutrient stress on coral condition in an upwelling region
  11. Non-coralline crustose algae associated with maerl beds in Portugal: a reappraisal of their diversity in the Atlantic Iberian beds
  12. Hydrolithon abyssophila sp. nov. (Hydrolithoideae, Corallinales), a bisporic coralline from the insular shelf edge of Puerto Rico and the Virgin Islands (US)
  13. The first record of Grateloupia subpectinata from the New Zealand region and comparison with G. prolifera, a species endemic to the Chatham Islands
  14. Neosiphonia baliana sp. nov. and N. silvae sp. nov. (Rhodomelaceae, Rhodophyta) from Bali, Indonesia
  15. Effects of density and substrate type on recruitment and growth of Pyropia torta (Rhodophyta) gametophytes
  16. Morphology and life stages of the potentially pinnatoxin-producing thecate dinoflagellate Vulcanodinium rugosum from the tropical Mexican Pacific
  17. Short communication
  18. Fungal endophytes of the seagrasses Halodule wrightii and Thalassia testudinum in the north-central Gulf of Mexico
Sign up now to receive a 20% welcome discount
Institutional Access
How does access work?
Have an idea on how to improve our website?
Please write us.
© 2025 De Gruyter Brill
Downloaded on 26.10.2025 from https://www.degruyterbrill.com/document/doi/10.1515/bot-2012-0223/html
Scroll to top button