Coral Reefs

, Volume 35, Issue 3, pp 909–918 | Cite as

Long-term isolation and local adaptation in Palau’s Nikko Bay help corals thrive in acidic waters

  • Yimnang GolbuuEmail author
  • Marine Gouezo
  • Haruko Kurihara
  • Lincoln Rehm
  • Eric Wolanski


The reefs in Palau’s Nikko Bay live in seawater with low pH that is similar to conditions predicted for 2100 because of ocean acidification. Nevertheless, the reefs at Nikko Bay have high coral cover and high diversity. We hypothesize that the low-pH environment in Nikko Bay is caused by low flushing rates, which causes long-term isolation and local adaptation. To test this hypothesis, we modeled the water circulation in and around Nikko Bay. Model results show that average residence time is 71 d, which is ten times the residence time on fore-reef habitats. The long residence time restricts the exchange of coral larvae in the bay with adjacent reefs, allowing persistent selection for tolerant traits and local adaptation. The corals in Nikko Bay are also more susceptible to local pollution because the waters are poorly flushed. Therefore, local management must focus on minimizing human impacts such as dredging, overfishing and pollution in the bay, which would compromise the condition of the corals that have already adapted to low-pH conditions.


Ocean acidification Coral reefs Flushing Residence time Resilience Adaptation 



Authors would like to thank everyone involved with Palau International Coral Reef Center’s long-term coral reef monitoring program. We thank A. Merep for his assistance in the field. We also thank Y. S. Yuen and T. Kawai for their assistance with the current measurements. We are thankful to C. Doropoulos for reviewing an earlier version of this manuscript. This study was supported by NOAA Coral Reef Conservation Program, NOAA Coastal Oceans Program, Pew Fellowship in Marine Conservation, and JICA-JST.


  1. Barkley HC, Cohen AL, Golbuu Y, Starczak VR, DeCarlo TM, Shamberger KEF (2015) Changes in coral reef communities across a natural gradient in seawater pH. Sci Adv 1:e1500328CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bolin B, Rodhe H (2011) A note on the concepts of age distribution and transit time in natural reservoirs. Tellus 25:58–62CrossRefGoogle Scholar
  3. Cole TG, Ewel KC, Devoe NN (1999) Structure of mangrove trees and forests in Micronesia. For Ecol Manage 117:95–109CrossRefGoogle Scholar
  4. Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2014) Fast coral reef calcifiers are more sensitive to ocean acidification in short-term laboratory incubations. Limnol Oceanogr 59:1081–1091CrossRefGoogle Scholar
  5. Costanza R, de Groot R, Sutton P, van der Ploeg S, Anderson SJ, Kubiszewski I, Farber S, Turner RK (2014) Changes in the global value of ecosystem services. Glob Environ Change 26:152–158CrossRefGoogle Scholar
  6. Deleersnijder E, Tartinville B, Rancher J (1997) A simple model of the tracer flux from the Mururoa lagoon to the Pacific. Appl Math Lett 10:13–17CrossRefGoogle Scholar
  7. Dickinson WR, Athens JS (2007) Holocene paleoshoreline and paleoenvironmental history of Palau: implications for human settlement. Journal of Island and Coastal Archaeology 2:175–196CrossRefGoogle Scholar
  8. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Ann Rev Mar Sci 1:169–192CrossRefPubMedGoogle Scholar
  9. Ellison JC (2009) Geomorphology and sedimentology of mangroves. In: Perillo GM, Wolanski E, Cahoon DR, Brinson MM (eds) Coastal wetlands. An integrated ecosystem approach. Elsevier, Amsterdam, pp 565–592Google Scholar
  10. Enochs IC, Manzello DP, Donham EM, Kolodziej G, Okano R, Johnston L, Young C, Iguel J, Edwards CB, Fox MD, Valentino L, Johnson S, Benavente D, Clark SJ, Carlton R, Burton T, Eynaud Y, Price NN (2015) Shift from coral to macroalgae dominance on a volcanically acidified reef. Nat Clim Chang 5:1083–1088CrossRefGoogle Scholar
  11. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang 1:165–169CrossRefGoogle Scholar
  12. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366CrossRefPubMedGoogle Scholar
  13. Figueiredo J, Baird AH, Harii S, Connolly SR (2014) Increased local retention of reef coral larvae as a result of ocean warming. Nat Clim Chang 4:498–502CrossRefGoogle Scholar
  14. Golbuu Y, Victor S, Penland L, Idip D, Emaurois C, Okaji K, Yukihira H, Iwase A, van Woesik R (2007) Palau’s coral reefs show differential habitat recovery following the 1998 bleaching event. Coral Reefs 26:319–332CrossRefGoogle Scholar
  15. Golbuu Y, Wolanski E, Idechong JW, Victor S, Isechal AL, Oldiais NW, Idip D, Richmond RH, van Woesik R (2012) Predicting coral recruitment in Palau’s complex reef archipelago. PLoS One 7:e50998CrossRefPubMedPubMedCentralGoogle Scholar
  16. Hendriks IE, Duarte CM, Álvarez M (2010) Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuar Coast Shelf Sci 86:157–164CrossRefGoogle Scholar
  17. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528CrossRefPubMedGoogle Scholar
  18. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742CrossRefPubMedGoogle Scholar
  19. Inoue S, Kayanne H, Yamamoto S, Kurihara H (2013) Spatial community shift from hard to soft corals in acidified water. Nat Clim Chang 3:683–687CrossRefGoogle Scholar
  20. IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, New York, p 1535Google Scholar
  21. Kayanne H, Yamano H, Randall RH (2002) Holocene sea-level changes and barrier reef formation on an oceanic island, Palau Islands, western Pacific. Sediment Geol 150:47–60CrossRefGoogle Scholar
  22. Kobayashi K (2000) Horizontally-moving subducted slab may generate enigmatic features of the Palau and Yap Trench-arcs. Proc Jpn Acad Ser B Phys Biol Sci 76:133–138CrossRefGoogle Scholar
  23. Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): a visual basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32:1259–1269CrossRefGoogle Scholar
  24. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434CrossRefPubMedGoogle Scholar
  25. Lewis E, Wallace DWR (1998) CO2SYS program developed for the CO2 system calculations. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak RidgeCrossRefGoogle Scholar
  26. Manzello DP, Kleypas JA, Budd DA, Eakin CM, Glynn PW, Langdon C (2008) Poorly cemented coral reefs of the eastern tropical Pacific: possible insights into reef development in a high-CO2 world. Proc Natl Acad Sci U S A 105:10450–10455CrossRefPubMedPubMedCentralGoogle Scholar
  27. McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2:623–627CrossRefGoogle Scholar
  28. Mehrbach C, Culberson CH, Hawley JE, Pytkowicx RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure 1. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  29. Mucci A (1983) The solubility of calcite and aragonite in seawater at various salinities, temperatures, and one atmosphere total pressure. Am J Sci 283:780–799CrossRefGoogle Scholar
  30. Murray SP, Arief D (1988) Throughflow into the Indian Ocean through the Lombok Strait, January 1958–Janauary 1986. Nature 333:444–447CrossRefGoogle Scholar
  31. Nakamura M, Ohki S, Suzuki A, Sakai K (2011) Coral larvae under ocean acidification: survival, metabolism, and metamorphosis. PLoS One 6:e14521CrossRefPubMedPubMedCentralGoogle Scholar
  32. Nozawa Y, Okubo N (2011) Survival dynamics of reef coral larvae with special consideration of larval size and the genus Acropora. Biol Bull 220:15–22PubMedGoogle Scholar
  33. Okubo A (1971) Oceanic diffusion diagrams. Deep Sea Research and Oceanographic Abstracts 18:789–802CrossRefGoogle Scholar
  34. Okubo A (1973) Effect of shoreline irregularities on streamwise dispersion in estuaries and other embayments. Netherlands Journal of Sea Research 6:213–224CrossRefGoogle Scholar
  35. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422CrossRefPubMedGoogle Scholar
  36. QGIS Development Team (2015) QGIS Geographic Information System. Open Source Geospatial Foundation Project,
  37. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134CrossRefGoogle Scholar
  38. Shamberger KEF, Cohen AL, Golbuu Y, McCorkle DC, Lentz SJ, Barkley HC (2014) Diverse coral communities in naturally acidified waters of a Western Pacific reef: diverse coral reefs in acidified waters. Geophys Res Lett 41:499–504CrossRefGoogle Scholar
  39. van Woesik R, Houk P, Isechal AL, Idechong JW, Victor S, Golbuu Y (2012) Climate-change refugia in the sheltered bays of Palau: analogs of future reefs. Ecol Evol 2:2474–2484CrossRefPubMedPubMedCentralGoogle Scholar
  40. Wisshak M, Schönberg CH, Form A, Freiwald A (2012) Ocean acidification accelerates reef bioerosion. PLoS One 7:e45124CrossRefPubMedPubMedCentralGoogle Scholar
  41. Wolanski E, Brinson MM, Cahoon DR, Perillo GM (2009) Costal wetlands: a synthesis. In: Perillo GM, Wolanski E, Cahoon DR, Brinson MM (eds) Coastal wetlands. An integrated ecosystem approach. Elsevier, Amsterdam, pp 1–62Google Scholar
  42. Wolanski E, Elliott M (2015) Estuarine ecohydrology, 2nd edn. Elsevier, Amsterdam, p 322Google Scholar
  43. Wolanski E, Furukawa K (2007) The oceanography of Palau. In: Kayanne H, Omori M, Fabricius K, Verheij E, Colin P, Golbuu Y, Yukihira H (eds) Coral reefs of Palau. Palau International Coral Reef Center, Palau, pp 59–72Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Yimnang Golbuu
    • 1
    Email author
  • Marine Gouezo
    • 1
  • Haruko Kurihara
    • 2
  • Lincoln Rehm
    • 1
  • Eric Wolanski
    • 3
  1. 1.Palau International Coral Reef CenterKororRepublic of Palau
  2. 2.Biology Program, Faculty of ScienceUniversity of the RyukyusNishiharaJapan
  3. 3.TropWATER and College of Marine and Environmental SciencesJames Cook UniversityTownsvilleAustralia

Personalised recommendations