Temporal functional changes in coral and fish communities on subtropical coastal coral reefs
Charlotte G. Clay A * , James Davis Reimer B C , Katie M. Cook A D , Hirotaka Yamagawa B , Ellen Gravener A , Lee Hui Yian Theodora B E and Maria Beger A FA School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds, LS2 9JT, UK.
B Molecular Invertebrate Systematics and Ecology Laboratory, Graduate School of Engineering and Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan.
C Tropical Biosphere Research Center, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan.
D National Institute of Water and Atmospheric Research (NIWA), Hamilton, New Zealand.
E Experimental Marine Ecology Laboratory, Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117558, Singapore.
F Centre for Biodiversity and Conservation Science, School of Biological Sciences, The University of Queensland, Brisbane, Qld 4072, Australia.
Marine and Freshwater Research 74(12) 1081-1094 https://doi.org/10.1071/MF22253
Submitted: 1 April 2022 Accepted: 17 June 2023 Published: 18 July 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Global and local stressors can drive phase shifts from zooxanthellate scleractinian coral communities to macroalgae-dominated ecosystems. However, our understanding of altered ecosystem functioning, productivity and stability remains limited as pre-shift data are typically lacking for degraded coral-reef sites.
Aims: Here, we assessed functional changes in fish communities in Nakagusuku Bay, Okinawa, Japan, over 45 years, by comparing pre-disturbance (1975) to post-disturbance (2018–2020) datasets, and identified possible drivers of changes.
Methods: We analysed data for 393 fish species and 26 coral genera at 13 sites, measured at four-time points (1975, 2018, 2019 and 2020). Analyses were performed using a range of ordination techniques.
Key results: We found reductions in functional richness and trait space contraction over time for fishes. Changes in coral functional groups over time correlated with changes in the functional diversity of reef-fish communities; a reduction in branching corals reduced habitat availability for coral-reliant fishes.
Conclusions: Increasing sedimentation and eutrophication as a result of construction along the Nakagusuku Bay coast likely reduced living coral cover and fish diversity, and thermal stress likely facilitated the simplification and shifts of both coral communities and coral specialist fishes away from shore.
Implications: Both global and local threats need to be considered when assessing functioning of coral-reef ecosystems for coral-reef conservation efforts.
Keywords: coastal urbanisation, functional change, Japan, Okinawa, reef communities, Ryukyu Islands, urban reefs, turbid reefs.
References
Borcard D, Gillet F, Legendre P (2018) ‘Numerical ecology with R.’ (Springer)Botta-Dukát, Z (2005). Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. Journal of Vegetation Science 16, 533–540.
| Rao’s quadratic entropy as a measure of functional diversity based on multiple traits.Crossref | GoogleScholarGoogle Scholar |
Bougeard, S, and Dray, S (2018). Supervised multiblock analysis in R with the ade4 package. Journal of Statistical Software 86, 1–17.
| Supervised multiblock analysis in R with the ade4 package.Crossref | GoogleScholarGoogle Scholar |
Brandl, SJ, Rasher, DB, Côté, IM, Casey, JM, Darling, ES, Lefcheck, JS, and Duffy, JE (2019). Coral reef ecosystem functioning: eight core processes and the role of biodiversity. Frontiers in Ecology and the Environment 17, 445–454.
| Coral reef ecosystem functioning: eight core processes and the role of biodiversity.Crossref | GoogleScholarGoogle Scholar |
Browne, NK, Smithers, SG, and Perry, CT (2012). Coral reefs of the turbid inner-shelf of the Great Barrier Reef, Australia: an environmental and geomorphic perspective on their occurrence, composition and growth. Earth-Science Reviews 115, 1–20.
| Coral reefs of the turbid inner-shelf of the Great Barrier Reef, Australia: an environmental and geomorphic perspective on their occurrence, composition and growth.Crossref | GoogleScholarGoogle Scholar |
Cheal, AJ, MacNeil, MA, Cripps, E, Emslie, MJ, Jonker, M, Schaffelke, B, and Sweatman, H (2010). Coral–macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef. Coral Reefs 29, 1005–1015.
| Coral–macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar |
Chessel, D, Dufour, A, and Thioulouse, J (2004). The ade4 package – I: one-table methods. R News 4, 5–10.
Coll, M (2020). Environmental effects of the COVID-19 pandemic from a (marine) ecological perspective. Ethics in Science and Environmental Politics 20, 41–55.
| Environmental effects of the COVID-19 pandemic from a (marine) ecological perspective.Crossref | GoogleScholarGoogle Scholar |
Cook, KM, Yamagiwa, H, Beger, M, Masucci, GD, Ross, S, Lee, HYT, Stuart-Smith, RD, and Reimer, JD (2022). A community and functional comparison of coral and reef fish assemblages between four decades of coastal urbanisation and thermal stress. Ecology and Evolution 12, e8736.
| A community and functional comparison of coral and reef fish assemblages between four decades of coastal urbanisation and thermal stress.Crossref | GoogleScholarGoogle Scholar |
Cornwell, WK, Schwilk, DW, and Ackerly, DD (2006). A trait-based test for habitat filtering: convex hull volume. Ecology 87, 1465–1471.
| A trait-based test for habitat filtering: convex hull volume.Crossref | GoogleScholarGoogle Scholar |
Cowburn, B, Moritz, C, Birrell, C, Grimsditch, G, and Abdulla, A (2018). Can luxury and environmental sustainability co-exist? Assessing the environmental impact of resort tourism on coral reefs in the Maldives. Ocean & Coastal Management 158, 120–127.
| Can luxury and environmental sustainability co-exist? Assessing the environmental impact of resort tourism on coral reefs in the Maldives.Crossref | GoogleScholarGoogle Scholar |
Cowman, PF, Parravicini, V, Kulbicki, M, and Floeter, SR (2017). The biogeography of tropical reef fishes: endemism and provinciality through time. Biological Reviews 92, 2112–2130.
| The biogeography of tropical reef fishes: endemism and provinciality through time.Crossref | GoogleScholarGoogle Scholar |
Darling, ES, Graham, NAJ, Januchowski-Hartley, FA, Nash, KL, Pratchett, MS, and Wilson, SK (2017). Relationships between structural complexity, coral traits, and reef fish assemblages. Coral Reefs 36, 561–575.
| Relationships between structural complexity, coral traits, and reef fish assemblages.Crossref | GoogleScholarGoogle Scholar |
DiBattista, JD, Reimer, JD, Stat, M, Masucci, GD, Biondi, P, De Brauwer, M, Wilkinson, SP, Chariton, AA, and Bunce, M (2020). Environmental DNA can act as a biodiversity barometer of anthropogenic pressures in coastal ecosystems. Scientific Reports 10, 8365.
| Environmental DNA can act as a biodiversity barometer of anthropogenic pressures in coastal ecosystems.Crossref | GoogleScholarGoogle Scholar |
Dikou, A, and van Woesik, R (2006). Survival under chronic stress from sediment load: spatial patterns of hard coral communities in the southern islands of Singapore. Marine Pollution Bulletin 52, 1340–1354.
| Survival under chronic stress from sediment load: spatial patterns of hard coral communities in the southern islands of Singapore.Crossref | GoogleScholarGoogle Scholar |
Dolédec, S, Chessel, D, ter Braak, CJF, and Champely, S (1996). Matching species traits to environmental variables: a new three-table ordination method. Environmental and Ecological Statistics 3, 143–166.
| Matching species traits to environmental variables: a new three-table ordination method.Crossref | GoogleScholarGoogle Scholar |
Dray, S, and Dufour, A-B (2007). The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22, 1–20.
| The ade4 package: implementing the duality diagram for ecologists.Crossref | GoogleScholarGoogle Scholar |
Dray, S, and Legendre, P (2008). Testing the species traits–environment relationships: the fourth-corner problem revisited. Ecology 89, 3400–3412.
| Testing the species traits–environment relationships: the fourth-corner problem revisited.Crossref | GoogleScholarGoogle Scholar |
Dray, S, Dufour, A, and Chessel, D (2007). The ade4 package – II: two-table and K-table methods. R News 7, 47–52.
Dray, S, Choler, P, Dolédec, S, Peres-Neto, PR, Thuiller, W, Pavoine, S, and ter Braak, CJF (2014). Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation. Ecology 95, 14–21.
| Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation.Crossref | GoogleScholarGoogle Scholar |
Díaz, S, Purvis, A, Cornelissen, JHC, Mace, GM, Donoghue, MJ, Ewers, RM, Jordano, P, and Pearse, WD (2013). Functional traits, the phylogeny of function, and ecosystem service vulnerability. Ecology and Evolution 3, 2958–2975.
| Functional traits, the phylogeny of function, and ecosystem service vulnerability.Crossref | GoogleScholarGoogle Scholar |
Edwards, CB, Friedlander, AM, Green, AG, Hardt, MJ, Sala, E, Sweatman, HP, Williams, ID, Zgliczynski, B, Sandin, SA, and Smith, JE (2014). Global assessment of the status of coral reef herbivorous fishes: evidence for fishing effects. Proceedings of the Royal Society B: Biological Sciences 281, 20131835.
| Global assessment of the status of coral reef herbivorous fishes: evidence for fishing effects.Crossref | GoogleScholarGoogle Scholar |
Floyd, M, Mizuyama, M, Obuchi, M, Sommer, B, Miller, MGR, Kawamura, I, Kise, H, Reimer, JD, and Beger, M (2020). Functional diversity of reef molluscs along a tropical-to-temperate gradient. Coral Reefs 39, 1361–1376.
| Functional diversity of reef molluscs along a tropical-to-temperate gradient.Crossref | GoogleScholarGoogle Scholar |
Fonseca, CR, and Ganade, G (2001). Species functional redundancy, random extinctions and the stability of ecosystems. Journal of Ecology 89, 118–125.
| Species functional redundancy, random extinctions and the stability of ecosystems.Crossref | GoogleScholarGoogle Scholar |
Graham, NAJ, Wilson, SK, Jennings, S, Polunin, NVC, Bijoux, JP, and Robinson, J (2006). Dynamic fragility of oceanic coral reef ecosystems. Proceedings of the National Academy of Sciences 103, 8425–8429.
| Dynamic fragility of oceanic coral reef ecosystems.Crossref | GoogleScholarGoogle Scholar |
Green AL, Bellwood DR (2009) Monitoring functional groups of herbivorous reef fishes as indicators of coral reef resilience: a practical guide for coral reef managers in the Asia Pacific region. IUCN.
Guest, JR, Tun, K, Low, J, Vergés, A, Marzinelli, EM, Campbell, AH, Bauman, AG, Feary, DA, Chou, LM, and Steinberg, PD (2016). 27 years of benthic and coral community dynamics on turbid, highly urbanised reefs off Singapore. Scientific Reports 6, 36260.
| 27 years of benthic and coral community dynamics on turbid, highly urbanised reefs off Singapore.Crossref | GoogleScholarGoogle Scholar |
Hatabu, A, Mao, X, Zhou, Y, Kawashita, N, Wen, Z, Ueda, M, Takagi, T, and Tian, Y-S (2020). Knowledge, attitudes, and practices toward COVID-19 among university students in Japan and associated factors: an online cross-sectional survey. PLoS ONE 15, e0244350.
| Knowledge, attitudes, and practices toward COVID-19 among university students in Japan and associated factors: an online cross-sectional survey.Crossref | GoogleScholarGoogle Scholar |
Heery, EC, Hoeksema, BW, Browne, NK, Reimer, JD, Ang, PO, Huang, D, Friess, DA, Chou, LM, Loke, LHL, Saksena-Taylor, P, Alsagoff, N, Yeemin, T, Sutthacheep, M, Vo, ST, Bos, AR, Gumanao, GS, Syed Hussein, MA, Waheed, Z, Lane, DJW, Johan, O, Kunzmann, A, Jompa, J, Suharsono Taira, D, Bauman, AG, and Todd, PA (2018). Urban coral reefs: degradation and resilience of hard coral assemblages in coastal cities of East and Southeast Asia. Marine Pollution Bulletin 135, 654–681.
| Urban coral reefs: degradation and resilience of hard coral assemblages in coastal cities of East and Southeast Asia.Crossref | GoogleScholarGoogle Scholar |
Hempson, TN, Graham, NAJ, MacNeil, MA, Hoey, AS, and Wilson, SK (2018). Ecosystem regime shifts disrupt trophic structure. Ecological Applications 28, 191–200.
| Ecosystem regime shifts disrupt trophic structure.Crossref | GoogleScholarGoogle Scholar |
Heron, SF, Maynard, JA, van Hooidonk, R, and Eakin, CM (2016). Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Scientific Reports 6, 38402.
| Warming trends and bleaching stress of the world’s coral reefs 1985–2012.Crossref | GoogleScholarGoogle Scholar |
Hongo, C, and Yamano, H (2013). Species-specific responses of corals to bleaching events on anthropogenically turbid reefs on Okinawa Island, Japan, over a 15-year period (1995–2009). PLoS ONE 8, e60952.
| Species-specific responses of corals to bleaching events on anthropogenically turbid reefs on Okinawa Island, Japan, over a 15-year period (1995–2009).Crossref | GoogleScholarGoogle Scholar |
Hooper, DU, Chapin, FS, Ewel, JJ, Hector, A, Inchausti, P, Lavorel, S, Lawton, JH, Lodge, DM, Loreau, M, Naeem, S, Schmid, B, Setälä, H, Symstad, AJ, Vandermeer, J, and Wardle, DA (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75, 3–35.
| Effects of biodiversity on ecosystem functioning: a consensus of current knowledge.Crossref | GoogleScholarGoogle Scholar |
Hughes, TP, Rodrigues, MJ, Bellwood, DR, Ceccarelli, D, Hoegh-Guldberg, O, McCook, L, Moltschaniwskyj, N, Pratchett, MS, Steneck, RS, and Willis, B (2007). Phase shifts, herbivory, and the resilience of coral reefs to climate change. Current Biology 17, 360–365.
| Phase shifts, herbivory, and the resilience of coral reefs to climate change.Crossref | GoogleScholarGoogle Scholar |
Hughes, TP, Kerry, JT, Álvarez-Noriega, M, Álvarez-Romero, JG, Anderson, KD, Baird, AH, Babcock, RC, Beger, M, Bellwood, DR, Berkelmans, R, Bridge, TC, Butler, IR, Byrne, M, Cantin, NE, Comeau, S, Connolly, SR, Cumming, GS, Dalton, SJ, Diaz-Pulido, G, Eakin, CM, Figueira, WF, Gilmour, JP, Harrison, HB, Heron, SF, Hoey, AS, Hobbs, J-PA, Hoogenboom, MO, Kennedy, EV, Kuo, C-Y, Lough, JM, Lowe, RJ, Liu, G, McCulloch, MT, Malcolm, HA, McWilliam, MJ, Pandolfi, JM, Pears, RJ, Pratchett, MS, Schoepf, V, Simpson, T, Skirving, WJ, Sommer, B, Torda, G, Wachenfeld, DR, Willis, BL, and Wilson, SK (2017). Global warming and recurrent mass bleaching of corals. Nature 543, 373–377.
| Global warming and recurrent mass bleaching of corals.Crossref | GoogleScholarGoogle Scholar |
Hughes, TP, Kerry, JT, Baird, AH, Connolly, SR, Dietzel, A, Eakin, CM, Heron, SF, Hoey, AS, Hoogenboom, MO, Liu, G, McWilliam, MJ, Pears, RJ, Pratchett, MS, Skirving, WJ, Stella, JS, and Torda, G (2018). Global warming transforms coral reef assemblages. Nature 556, 492–496.
| Global warming transforms coral reef assemblages.Crossref | GoogleScholarGoogle Scholar |
Israngkura, A (2022). Marine resource recovery in southern Thailand during COVID-19 and policy recommendations. Marine Policy 137, 104972.
| Marine resource recovery in southern Thailand during COVID-19 and policy recommendations.Crossref | GoogleScholarGoogle Scholar |
Jones, GP, McCormick, MI, Srinivasan, M, and Eagle, JV (2004). Coral decline threatens fish biodiversity in marine reserves. Proceedings of the National Academy of Sciences 101, 8251–8253.
| Coral decline threatens fish biodiversity in marine reserves.Crossref | GoogleScholarGoogle Scholar |
Khan, I, Shah, D, and Shah, SS (2021). COVID-19 pandemic and its positive impacts on environment: an updated review. International Journal of Environmental Science and Technology 18, 521–530.
| COVID-19 pandemic and its positive impacts on environment: an updated review.Crossref | GoogleScholarGoogle Scholar |
Kirwan, ML, Murray, AB, Donnelly, JP, and Corbett, DR (2011). Rapid wetland expansion during European settlement and its implication for marsh survival under modern sediment delivery rates. Geology 39, 507–510.
| Rapid wetland expansion during European settlement and its implication for marsh survival under modern sediment delivery rates.Crossref | GoogleScholarGoogle Scholar |
Komyakova, V, Munday, PL, and Jones, GP (2013). Relative importance of coral cover, habitat complexity and diversity in determining the structure of reef fish communities. PLoS ONE 8, e83178.
| Relative importance of coral cover, habitat complexity and diversity in determining the structure of reef fish communities.Crossref | GoogleScholarGoogle Scholar |
Laliberté, E, and Legendre, P (2010). A distance-based framework for measuring functional diversity from multiple traits. Ecology 91, 299–305.
| A distance-based framework for measuring functional diversity from multiple traits.Crossref | GoogleScholarGoogle Scholar |
Laureto, LMO, Cianciaruso, MV, and Samia, DSM (2015). Functional diversity: an overview of its history and applicability. Natureza & Conservação 13, 112–116.
| Functional diversity: an overview of its history and applicability.Crossref | GoogleScholarGoogle Scholar |
Lavorel, S, Storkey, J, Bardgett, RD, De Bello, F, Berg, MP, Le Roux, X, Moretti, M, Mulder, C, Pakeman, RJ, Díaz, S, and Harrington, R (2013). A novel framework for linking functional diversity of plants with other trophic levels for the quantification of ecosystem services. Journal of Vegetation Science 24, 942–948.
| A novel framework for linking functional diversity of plants with other trophic levels for the quantification of ecosystem services.Crossref | GoogleScholarGoogle Scholar |
Legendre P, Legendre L (2012) ‘Numerical ecology.’ (Elsevier)
Legendre, P, Galzin, R, and Harmelin-Vivien, ML (1997). Relating behavior to habitat: solutions to the fourth-corner problem. Ecology 78, 547–562.
| Relating behavior to habitat: solutions to the fourth-corner problem.Crossref | GoogleScholarGoogle Scholar |
Magneville, C, Loiseau, N, Albouy, C, Casajus, N, Claverie, T, Escalas, A, Leprieur, F, Maire, E, Mouillot, D, and Villéger, S (2022). mFD: an R package to compute and illustrate the multiple facets of functional diversity. Ecography 2022, .
| mFD: an R package to compute and illustrate the multiple facets of functional diversity.Crossref | GoogleScholarGoogle Scholar |
Masucci, GD, and Reimer, JD (2019). Expanding walls and shrinking beaches: loss of natural coastline in Okinawa Island, Japan. PeerJ 7, e7520.
| Expanding walls and shrinking beaches: loss of natural coastline in Okinawa Island, Japan.Crossref | GoogleScholarGoogle Scholar |
Masuda, R (2008). Seasonal and interannual variation of subtidal fish assemblages in Wakasa Bay with reference to the warming trend in the Sea of Japan. Environmental Biology of Fishes 82, 387–399.
| Seasonal and interannual variation of subtidal fish assemblages in Wakasa Bay with reference to the warming trend in the Sea of Japan.Crossref | GoogleScholarGoogle Scholar |
McCormack, G (1999). From the sea that divides to the sea that links: contradictions of ecological and economic development in Okinawa. Capitalism Nature Socialism 10, 3–39.
| From the sea that divides to the sea that links: contradictions of ecological and economic development in Okinawa.Crossref | GoogleScholarGoogle Scholar |
McWilliam, M, Hoogenboom, MO, Baird, AH, Kuo, C-Y, Madin, JS, and Hughes, TP (2018). Biogeographical disparity in the functional diversity and redundancy of corals. Proceedings of the National Academy of Sciences 115, 3084–3089.
| Biogeographical disparity in the functional diversity and redundancy of corals.Crossref | GoogleScholarGoogle Scholar |
Micheli, F, Mumby, PJ, Brumbaugh, DR, Broad, K, Dahlgren, CP, Harborne, AR, Holmes, KE, Kappel, CV, Litvin, SY, and Sanchirico, JN (2014). High vulnerability of ecosystem function and services to diversity loss in Caribbean coral reefs. Biological Conservation 171, 186–194.
| High vulnerability of ecosystem function and services to diversity loss in Caribbean coral reefs.Crossref | GoogleScholarGoogle Scholar |
Mouillot, D, Bellwood, DR, Baraloto, C, Chave, J, Galzin, R, Harmelin-Vivien, M, Kulbicki, M, Lavergne, S, Lavorel, S, Mouquet, N, Paine, CET, Renaud, J, and Thuiller, W (2013). Rare species support vulnerable functions in high-diversity ecosystems. PLoS Biology 11, e1001569.
| Rare species support vulnerable functions in high-diversity ecosystems.Crossref | GoogleScholarGoogle Scholar |
Mouillot, D, Villéger, S, Parravicini, V, Kulbicki, M, Arias-González, JE, Bender, M, Chabanet, P, Floeter, SR, Friedlander, A, Vigliola, L, and Bellwood, DR (2014). Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs. Proceedings of the National Academy of Sciences 111, 13757.
| Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs.Crossref | GoogleScholarGoogle Scholar |
Moustaka, M, Langlois, TJ, McLean, D, Bond, T, Fisher, R, Fearns, P, Dorji, P, and Evans, RD (2018). The effects of suspended sediment on coral reef fish assemblages and feeding guilds of north-west Australia. Coral Reefs 37, 659–673.
| The effects of suspended sediment on coral reef fish assemblages and feeding guilds of north-west Australia.Crossref | GoogleScholarGoogle Scholar |
Nakano Y (2004) Direct impacts of coastal development. In ‘Coral Reefs of Japan’. (Eds Ministry of the Environment, Japanese Coral Reef Society) pp. 60–63. (Ministry of the Environment)
Ng, CSL, Toh, TC, and Chou, LM (2016). Coral restoration in Singapore’s sediment-challenged sea. Regional Studies in Marine Science 8, 422–429.
| Coral restoration in Singapore’s sediment-challenged sea.Crossref | GoogleScholarGoogle Scholar |
Nishihira M (2020) ‘Scleractinian corals genus identification practice book.’ (Okinawa Churashima Foundation: Okinawa, Japan)
Omori, M (2011). Degradation and restoration of coral reefs: experience in Okinawa, Japan. Marine Biology Research 7, 3–12.
| Degradation and restoration of coral reefs: experience in Okinawa, Japan.Crossref | GoogleScholarGoogle Scholar |
Patton, WK (1994). Distribution and ecology of animals associated with branching corals (Acropora spp.) from the Great Barrier Reef, Australia. Bulletin of Marine Science 55, 193–211.
Pratchett, MS, Hoey, AS, Wilson, SK, Messmer, V, and Graham, NAJ (2011). Changes in biodiversity and functioning of reef fish assemblages following coral bleaching and coral loss. Diversity 3, 424–452.
| Changes in biodiversity and functioning of reef fish assemblages following coral bleaching and coral loss.Crossref | GoogleScholarGoogle Scholar |
Reimer, JD, Yang, S-Y, White, KN, Asami, R, Fujita, K, Hongo, C, Ito, S, Kawamura, I, Maeda, I, Mizuyama, M, Obuchi, M, Sakamaki, T, Tachihara, K, Tamura, M, Tanahara, A, Yamaguchi, A, and Jenke-Kodama, H (2015). Effects of causeway construction on environment and biota of subtropical tidal flats in Okinawa, Japan. Marine Pollution Bulletin 94, 153–167.
| Effects of causeway construction on environment and biota of subtropical tidal flats in Okinawa, Japan.Crossref | GoogleScholarGoogle Scholar |
Reimer, JD, Biondi, P, Lau, YW, Masucci, GD, Nguyen, XH, Santos, MEA, and Wee, HB (2019). Marine biodiversity research in the Ryukyu Islands, Japan: current status and trends. PeerJ 7, e6532.
| Marine biodiversity research in the Ryukyu Islands, Japan: current status and trends.Crossref | GoogleScholarGoogle Scholar |
Reiss, J, Bridle, JR, Montoya, JM, and Woodward, G (2009). Emerging horizons in biodiversity and ecosystem functioning research. Trends in Ecology & Evolution 24, 505–514.
| Emerging horizons in biodiversity and ecosystem functioning research.Crossref | GoogleScholarGoogle Scholar |
Smith, JE, Hunter, CL, and Smith, CM (2010). The effects of top–down versus bottom-up control on benthic coral reef community structure. Oecologia 163, 497–507.
| The effects of top–down versus bottom-up control on benthic coral reef community structure.Crossref | GoogleScholarGoogle Scholar |
Sully, S, Burkepile, DE, Donovan, MK, Hodgson, G, and van Woesik, R (2019). A global analysis of coral bleaching over the past two decades. Nature Communications 10, 1264.
| A global analysis of coral bleaching over the past two decades.Crossref | GoogleScholarGoogle Scholar |
Taira, D, Poquita-Du, RC, Toh, TC, Toh, KB, Ng, CSL, Afiq-Rosli, L, Chou, LM, and Song, T (2018). Spatial variability of fish communities in a highly urbanised reef system. Urban Ecosystems 21, 85–95.
| Spatial variability of fish communities in a highly urbanised reef system.Crossref | GoogleScholarGoogle Scholar |
Thioulouse J, Dray S, Dufour A-B, Siberchicot A, Jombart T, Pavoine S (2018) ‘Multivariate analysis of ecological data with ade4.’ (Springer)
Verberk, WCEP, van Noordwijk, CGE, and Hildrew, AG (2013). Delivering on a promise: integrating species traits to transform descriptive community ecology into a predictive science. Freshwater Science 32, 531–547.
| Delivering on a promise: integrating species traits to transform descriptive community ecology into a predictive science.Crossref | GoogleScholarGoogle Scholar |
Veron JEN (2000) ‘Corals of the world.’ (Australian Institute of Marine Science: Townsville, Qld, Australia)
Villéger, S, Miranda, JR, Hernández, DF, and Mouillot, D (2010). Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecological Applications 20, 1512–1522.
| Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation.Crossref | GoogleScholarGoogle Scholar |
Violle, C, Navas, M-L, Vile, D, Kazakou, E, Fortunel, C, Hummel, I, and Garnier, E (2007). Let the concept of trait be functional!. Oikos 116, 882–892.
| Let the concept of trait be functional!.Crossref | GoogleScholarGoogle Scholar |
Wear, SL (2016). Missing the boat: critical threats to coral reefs are neglected at global scale. Marine Policy 74, 153–157.
| Missing the boat: critical threats to coral reefs are neglected at global scale.Crossref | GoogleScholarGoogle Scholar |
Weigel, B, Blenckner, T, and Bonsdorff, E (2016). Maintained functional diversity in benthic communities in spite of diverging functional identities. Oikos 125, 1421–1433.
| Maintained functional diversity in benthic communities in spite of diverging functional identities.Crossref | GoogleScholarGoogle Scholar |
Wilson, SK, Graham, NAJ, Pratchett, MS, Jones, GP, and Polunin, NVC (2006). Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Global Change Biology 12, 2220–2234.
| Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient?Crossref | GoogleScholarGoogle Scholar |
Wilson, SK, Burgess, SC, Cheal, AJ, Emslie, M, Fisher, R, Miller, I, Polunin, NVC, and Sweatman, HPA (2008). Habitat utilization by coral reef fish: implications for specialists vs. generalists in a changing environment. Journal of Animal Ecology , 220–228.
| Habitat utilization by coral reef fish: implications for specialists vs. generalists in a changing environment.Crossref | GoogleScholarGoogle Scholar |
Wilson, SK, Dolman, AM, Cheal, AJ, Emslie, MJ, Pratchett, MS, and Sweatman, HPA (2009). Maintenance of fish diversity on disturbed coral reefs. Coral Reefs 28, 3–14.
| Maintenance of fish diversity on disturbed coral reefs.Crossref | GoogleScholarGoogle Scholar |
Wilson, SK, Robinson, JPW, Chong-Seng, K, Robinson, J, and Graham, NAJ (2019). Boom and bust of keystone structure on coral reefs. Coral Reefs 38, 625–635.
| Boom and bust of keystone structure on coral reefs.Crossref | GoogleScholarGoogle Scholar |
Wingfield-Hayes R (2020) Coronavirus: Japan’s mysteriously low virus death rate. In BBC News, 4 July 2020. Available at https://www.bbc.co.uk/news/world-asia-53188847 [Verified 10 March 2021]
Worm, B, Barbier, EB, Beaumont, N, Duffy, JE, Folke, C, Halpern, BS, Jackson, JBC, Lotze, HK, Micheli, F, Palumbi, SR, Sala, E, Selkoe, KA, Stachowicz, JJ, and Watson, R (2006). Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790.
| Impacts of biodiversity loss on ocean ecosystem services.Crossref | GoogleScholarGoogle Scholar |
Yachi, S, and Loreau, M (1999). Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proceedings of the National Academy of Sciences 96, 1463–1468.
| Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis.Crossref | GoogleScholarGoogle Scholar |
Yamagiwa H (2021) Transition of coral communities between 1975–76 and 2018–2021 in Nakagusuku Bay, Okinawa, Japan. MSc thesis, University of the Ryukyus, Japan.
Yamazato K, Nishihara M (1977) 1. Coral reefs of Nakagusuku Bay. In ‘Marine ecological survey of Nakagusuku Bay: field surveys’. (Eds S Nishijima, K Yamazato, M Nishihira, S Arasaki, H Ida) pp. 1–103. (Japan Institute for Environmental Science)