Primacy of bottom-up effects on a butterflyfish assemblage
Susannah M. Leahy A B E , Garry R. Russ B C and Rene A. Abesamis B D
+ Author Affiliations
- Author Affiliations
A College of Marine and Environmental Sciences, and Centre for Tropical Environmental and Sustainability Sciences, James Cook University, Cairns, Qld 4878, Australia.
B ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Qld 4811, Australia.
C College of Marine and Environmental Sciences, James Cook University, Townsville, Qld 4811, Australia.
D Silliman University – Angelo King Center for Research and Environmental Management (SUAKCREM), 6200 Dumaguete City, Negros Oriental, Philippines.
E Corresponding author. Email: susannah.leahy@gmail.com
Marine and Freshwater Research 67(8) 1175-1185 https://doi.org/10.1071/MF15012
Submitted: 13 January 2015 Accepted: 11 April 2015 Published: 1 September 2015
Abstract
The question of whether biological systems are maintained by top-down versus bottom-up drivers is a recurring one in ecology. It is a particularly important question to address in the management of coral reefs, which are at risk from a variety of anthropogenic stressors. Here, we explicitly test whether the abundance of different feeding guilds of coral-associated Chaetodon butterflyfishes are controlled by top-down or bottom-up drivers, and we assess the relative influence of all statistically significant drivers. We find that the abundance and species richness of Chaetodon butterflyfishes are predominately determined by bottom-up drivers. The abundance of corallivores is primarily driven by availability of branching and tabular live corals, whereas the abundance of generalists is most strongly influenced by a negative association with macroalgal cover. We also find evidence of weak top-down control on the abundance of corallivorous butterflyfish by gape-limited mesopredators, but no such effects on generalist butterflyfish. Our findings indicate that conservation of coral reefs for Chaetodon butterflyfishes must include management at a larger spatial scale in order to reduce the effect of coral reef stressors such as declining water quality and climate change, but should also include implementation of fisheries management tools in order to increase local herbivory.
Additional keywords: boosted regression trees, butterflyfish, Chaetodon, Coral Triangle, macroalgae, mesopredator.
References
Almany, G. R. (2004). Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141, 105–113.| Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes.Crossref | GoogleScholarGoogle Scholar | 15197644PubMed |
Almany, G. R., and Webster, M. S. (2006). The predation gauntlet: early post-settlement mortality in reef fishes. Coral Reefs 25, 19–22.
| The predation gauntlet: early post-settlement mortality in reef fishes.Crossref | GoogleScholarGoogle Scholar |
Armsworth, P. R. (2002). Recruitment limitation, population regulation, and larval connectivity in reef fish metapopulations. Ecology 83, 1092–1104.
| Recruitment limitation, population regulation, and larval connectivity in reef fish metapopulations.Crossref | GoogleScholarGoogle Scholar |
Baum, J. K., and Worm, B. (2009). Cascading top-down effects of changing oceanic predator abundances. Journal of Animal Ecology 78, 699–714.
| Cascading top-down effects of changing oceanic predator abundances.Crossref | GoogleScholarGoogle Scholar | 19298616PubMed |
Bellwood, D. R., Hughes, T. P., and Hoey, A. S. (2006). Sleeping functional group drives coral-reef recovery. Current Biology 16, 2434–2439.
| Sleeping functional group drives coral-reef recovery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlalsLrO&md5=88788c6e6c56f300e273d328d1c3d65fCAS | 17174918PubMed |
Berumen, M. L., Almany, G. R., Planes, S., Jones, G. P., Saenz-Agudelo, P., and Thorrold, S. R. (2012). Persistence of self-recruitment and patterns of larval connectivity in a marine protected area network. Ecology and Evolution 2, 444–452.
| Persistence of self-recruitment and patterns of larval connectivity in a marine protected area network.Crossref | GoogleScholarGoogle Scholar | 22423335PubMed |
Bozec, Y. M., Doledec, S., and Kulbicki, M. (2005). An analysis of fish-habitat associations on disturbed coral reefs: chaetodontid fishes in New Caledonia. Journal of Fish Biology 66, 966–982.
| An analysis of fish-habitat associations on disturbed coral reefs: chaetodontid fishes in New Caledonia.Crossref | GoogleScholarGoogle Scholar |
Brett, M. T., and Goldman, C. R. (1997). Consumer versus resource control in freshwater pelagic food webs. Science 275, 384–386.
| Consumer versus resource control in freshwater pelagic food webs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtlKqtA%3D%3D&md5=bbfc97ed0fde0923926095b92cc5d2cbCAS | 8994034PubMed |
Brodie, J. E., Kroon, F. J., Schaffelke, B., Wolanski, E. C., Lewis, S. E., Devlin, M. J., Bohnet, I. C., Bainbridge, Z. T., Waterhouse, J., and Davis, A. M. (2012). Terrestrial pollutant runoff to the Great Barrier Reef: an update of issues, priorities and management responses. Marine Pollution Bulletin 65, 81–100.
| Terrestrial pollutant runoff to the Great Barrier Reef: an update of issues, priorities and management responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotlOgt7s%3D&md5=bdc0e75b4d0fe7b4e7952b745305ec70CAS | 22257553PubMed |
Burke, L., Reytar, K., Spalding, M., and Perry, A. (2012) ‘Reefs at Risk Revisited in the Coral Triangle.’ (World Resources Institute: Washington, DC.)
Cheal, A. J., Wilson, S. K., Emslie, M. J., Dolman, A. M., and Sweatman, H. (2008). Responses of reef fish communities to coral declines on the Great Barrier Reef. Marine Ecology Progress Series 372, 211–223.
| Responses of reef fish communities to coral declines on the Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar |
Cinner, J. E., McClanahan, T. R., Graham, N. A. J., Pratchett, M. S., Wilson, S. K., and Raina, J.-B. (2009). Gear-based fisheries management as a potential adaptive response to climate change and coral mortality. Journal of Applied Ecology 46, 724–732.
| Gear-based fisheries management as a potential adaptive response to climate change and coral mortality.Crossref | GoogleScholarGoogle Scholar |
Clark, N. J., and Russ, G. R. (2012). Ontogenetic shifts in the habitat associations of butterflyfishes (F. Chaetodontidae). Environmental Biology of Fishes 94, 579–590.
| Ontogenetic shifts in the habitat associations of butterflyfishes (F. Chaetodontidae).Crossref | GoogleScholarGoogle Scholar |
Cole, A. J., Pratchett, M. S., and Jones, G. P. (2008). Diversity and functional importance of coral-feeding fishes on tropical coral reefs. Fish and Fisheries 9, 286–307.
| Diversity and functional importance of coral-feeding fishes on tropical coral reefs.Crossref | GoogleScholarGoogle Scholar |
Coppock, A. G., Gardiner, N. M., and Jones, G. P. (2013). Olfactory discrimination in juvenile coral reef fishes: response to conspecifics and corals. Journal of Experimental Marine Biology and Ecology 443, 21–26.
| Olfactory discrimination in juvenile coral reef fishes: response to conspecifics and corals.Crossref | GoogleScholarGoogle Scholar |
Crosby, M. P., and Reese, E. S. (2005). Relationship of habitat stability and intra-specific population dynamics of an obligate corallivore butterflyfish. Aquatic Conservation: Marine and Freshwater Ecosystems 15, S13–S25.
| Relationship of habitat stability and intra-specific population dynamics of an obligate corallivore butterflyfish.Crossref | GoogleScholarGoogle Scholar |
Cury, P., Bakun, A., Crawford, R. J. M., Jarre, A., Quinones, R. A., Shannon, L. J., and Verheye, H. M. (2000). Small pelagics in upwelling systems: patterns of interaction and structural changes in ‘wasp-waist’ ecosystems. ICES Journal of Marine Science 57, 603–618.
| Small pelagics in upwelling systems: patterns of interaction and structural changes in ‘wasp-waist’ ecosystems.Crossref | GoogleScholarGoogle Scholar |
Dahlgren, C. P., and Eggleston, D. B. (2000). Ecological processes underlying ontogenetic habitat shifts in a coral reef fish. Ecology 81, 2227–2240.
| Ecological processes underlying ontogenetic habitat shifts in a coral reef fish.Crossref | GoogleScholarGoogle Scholar |
De’ath, G. (2007). Boosted trees for ecological modeling and prediction. Ecology 88, 243–251.
| Boosted trees for ecological modeling and prediction.Crossref | GoogleScholarGoogle Scholar | 17489472PubMed |
DeVantier, L., Alcala, A., and Wilkinson, C. (2004). The Sulu-Sulawesi Sea: environmental and socioeconomic status, future prognosis and ameliorative policy options. AMBIO: A Journal of the Human Environment 33, 88–97.
| The Sulu-Sulawesi Sea: environmental and socioeconomic status, future prognosis and ameliorative policy options.Crossref | GoogleScholarGoogle Scholar |
Dixson, D. L., Jones, G. P., Munday, P. L., Planes, S., Pratchett, M. S., Srinivasan, M., Syms, C., and Thorrold, S. R. (2008). Coral reef fish smell leaves to find island homes. Proceedings of the Royal Society of London – B. Biological Sciences 275, 2831–2839.
| Coral reef fish smell leaves to find island homes.Crossref | GoogleScholarGoogle Scholar |
Doherty, P. J., and Williams, D. M. (1988). The replenishment of coral reef fish populations. Oceanography and Marine Biology – an Annual Review 26, 487–551.
Doherty, P. J., Dufour, V., Galzin, R., Hixon, M. A., Meekan, M. G., and Planes, S. (2004). High mortality during settlement is a population bottleneck for a tropical surgeonfish. Ecology 85, 2422–2428.
| High mortality during settlement is a population bottleneck for a tropical surgeonfish.Crossref | GoogleScholarGoogle Scholar |
Done, T. J. (1992). Phase-shifts in coral reef communities and their ecological significance. Hydrobiologia 247, 121–132.
| Phase-shifts in coral reef communities and their ecological significance.Crossref | GoogleScholarGoogle Scholar |
Elith, J., Leathwick, J. R., and Hastie, T. (2008). A working guide to boosted regression trees. Journal of Animal Ecology 77, 802–813.
| A working guide to boosted regression trees.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cvgsFOqsQ%3D%3D&md5=6bf5cbdc5da9857e868eaf296231d27dCAS | 18397250PubMed |
Emslie, M., Cheal, A., Sweatman, H., and Delean, S. (2008). Recovery from disturbance of coral and reef fish communities on the Great Barrier Reef, Australia. Marine Ecology Progress Series 371, 177–190.
| Recovery from disturbance of coral and reef fish communities on the Great Barrier Reef, Australia.Crossref | GoogleScholarGoogle Scholar |
Emslie, M. J., Pratchett, M. S., and Cheal, A. J. (2011). Effects of different disturbance types on butterflyfish communities of Australia’s Great Barrier Reef. Coral Reefs 30, 461–471.
| Effects of different disturbance types on butterflyfish communities of Australia’s Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar |
Emslie, M. J., Cheal, A. J., and Johns, K. A. (2014). Retention of habitat complexity minimizes disassembly of reef fish communities following disturbance: a large-scale natural experiment. PLoS One 9, e105384.
| Retention of habitat complexity minimizes disassembly of reef fish communities following disturbance: a large-scale natural experiment.Crossref | GoogleScholarGoogle Scholar | 25140801PubMed |
English, S. S., Wilkinson, C. C., and Baker, V. V. (1994) ‘Survey Manual for Tropical Marine Resources.’ (Australian Institute of Marine Science: Townsville, Qld, Australia.)
Estes, J. A., Tinker, M. T., Williams, T. M., and Doak, D. F. (1998). Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282, 473–476.
| Killer whale predation on sea otters linking oceanic and nearshore ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmslejurY%3D&md5=7fd41ee16205507e06ac0018fbe19defCAS | 9774274PubMed |
Fabricius, K. E. (2005). Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Marine Pollution Bulletin 50, 125–146.
| Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitVahsbk%3D&md5=724e50926a3f71b9ab97850898b13ad3CAS | 15737355PubMed |
Feeney, W. E., Lönnstedt, O. M., Bosiger, Y., Martin, J., Jones, G. P., Rowe, R. J., and McCormick, M. I. (2012). High rate of prey consumption in a small predatory fish on coral reefs. Coral Reefs 31, 909–918.
| High rate of prey consumption in a small predatory fish on coral reefs.Crossref | GoogleScholarGoogle Scholar |
Ferretti, F., Worm, B., Britten, G. L., Heithaus, M. R., and Lotze, H. K. (2010). Patterns and ecosystem consequences of shark declines in the ocean. Ecology Letters 13, 1055–1071.
| 20528897PubMed |
Findley, J. S., and Findley, M. T. (2001). Global, regional, and local patterns in species richness and abundance of butterflyfishes. Ecological Monographs 71, 69–91.
| Global, regional, and local patterns in species richness and abundance of butterflyfishes.Crossref | GoogleScholarGoogle Scholar |
Foale, S., Adhuri, D., Alino, P., Allison, E. H., Andrew, N., Cohen, P., Evans, L., Fabinyi, M., Fidelman, P., Gregory, C., Stacey, N., Tanzer, J., and Weeratunge, N. (2013). Food security and the Coral Triangle Initiative. Marine Policy 38, 174.
| Food security and the Coral Triangle Initiative.Crossref | GoogleScholarGoogle Scholar |
Frank, D. A. (2008). Evidence for top predator control of a grazing ecosystem. Oikos 117, 1718–1724.
| Evidence for top predator control of a grazing ecosystem.Crossref | GoogleScholarGoogle Scholar |
Gomez, E. D., Aliño, P. M., Yap, H. T., and Licuanan, W. Y. (1994). A review of the status of Philippine reefs. Marine Pollution Bulletin 29, 62–68.
| A review of the status of Philippine reefs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtFWjsbg%3D&md5=b5da7aca59cdcfd98717861880474225CAS |
Graham, N. A. J. (2007). Ecological versatility and the decline of coral feeding fishes following climate driven coral mortality. Marine Biology 153, 119–127.
| Ecological versatility and the decline of coral feeding fishes following climate driven coral mortality.Crossref | GoogleScholarGoogle Scholar |
Graham, N. A. J., Wilson, S. K., Pratchett, M. S., Polunin, N. V. C., and Spalding, M. D. (2009). Coral mortality versus structural collapse as drivers of corallivorous butterflyfish decline. Biodiversity and Conservation 18, 3325–3336.
| Coral mortality versus structural collapse as drivers of corallivorous butterflyfish decline.Crossref | GoogleScholarGoogle Scholar |
Groves, C., Game, E., Anderson, M., Cross, M., Enquist, C., Ferdaña, Z., Girvetz, E., Gondor, A., Hall, K., Higgins, J., Marshall, R., Popper, K., Schill, S., and Shafer, S. (2012). Incorporating climate change into systematic conservation planning. Biodiversity and Conservation 21, 1651–1671.
| Incorporating climate change into systematic conservation planning.Crossref | GoogleScholarGoogle Scholar |
Halford, A., Cheal, A. J., Ryan, D., and Williams, D. M. (2004). Resilience to large-scale disturbance in coral and fish assemblages on the Great Barrier Reef. Ecology 85, 1892–1905.
| Resilience to large-scale disturbance in coral and fish assemblages on the Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar |
Harborne, A. R., Jelks, H. L., Smith-Vaniz, W. F., and Rocha, L. A. (2012). Abiotic and biotic controls of cryptobenthic fish assemblages across a Caribbean seascape. Coral Reefs 31, 977–990.
| Abiotic and biotic controls of cryptobenthic fish assemblages across a Caribbean seascape.Crossref | GoogleScholarGoogle Scholar |
Harmelin-Vivien, M. L. (1994). The effects of storms and cyclones on coral reefs: a review. Journal of Coastal Research 12, 211–231.
Harrison, H., Williamson, D., Evans, R., Almany, G., Thorrold, S., Russ, G., Feldheim, K., van Herwerden, L., Planes, S., Srinivasan, M., Berumen, M., and Jones, G. (2012). Larval export from marine reserves and the recruitment benefit for fish and fisheries. Current Biology 22, 1023–1028.
| Larval export from marine reserves and the recruitment benefit for fish and fisheries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnslSntLs%3D&md5=4ce8760e99da48daec6b8517b233c023CAS | 22633811PubMed |
Hixon, M. A. (1991) Chapter 17 – Predation as a Process Structuring Coral Reef Fish Communities. In ‘The Ecology of Fishes on Coral Reefs’. (Ed. P. F. Sale.) pp. 475–508. (Academic Press: San Diego, CA, USA.)
Hoegh-Guldberg, O. (2011). Coral reef ecosystems and anthropogenic climate change. Regional Environmental Change 11, 215–227.
| Coral reef ecosystems and anthropogenic climate change.Crossref | GoogleScholarGoogle Scholar |
Hoegh-Guldberg, O., Hoegh-Guldberg, H., Veron, J. E. N., Green, A., Gomez, E. D., Lough, J., King, M. Ambariyanto, Hansen, L., Cinner, J., Dews, G., Russ, G., Schuttenberg, H. Z., Peñaflor, E. L., Eakin, C. M., Christensen, T. R. L., Abbey, M., Areki, F., Kosaka, R. A., Tewfik, A., and Oliver, J. (2009) ‘The Coral Triangle and Climate Change: Ecosystems, People and Societies at Risk.’ (WWF Australia: Brisbane, Qld, Australia.)
Holmes, T. H., and McCormick, M. I. (2010). Size-selectivity of predatory reef fish on juvenile prey. Marine Ecology Progress Series 399, 273–283.
| Size-selectivity of predatory reef fish on juvenile prey.Crossref | GoogleScholarGoogle Scholar |
Hourigan, T. (1989). Environmental determinants of butterflyfish social systems. Environmental Biology of Fishes 25, 61–78.
| Environmental determinants of butterflyfish social systems.Crossref | GoogleScholarGoogle Scholar |
Hughes, T. P. (1994). Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265, 1547–1551.
| Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvjs1OjsA%3D%3D&md5=ad1e26560cdf06fbca397f94f654224eCAS | 17801530PubMed |
Hughes, T. P., and Connell, J. H. (1999). Multiple stressors on coral reefs: a long-term perspective. Limnology and Oceanography 44, 932–940.
| Multiple stressors on coral reefs: a long-term perspective.Crossref | GoogleScholarGoogle Scholar |
Hughes, T. P., Baird, A. H., Bellwood, D. R., Card, M., Connolly, S. R., Folke, C., Grosberg, R., Hoegh-Guldberg, O., Jackson, J. B. C., Kleypas, J., Lough, J. M., Marshall, P., Nyström, M., Palumbi, S. R., Pandolfi, J. M., Rosen, B., and Roughgarden, J. (2003). Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933.
| Climate change, human impacts, and the resilience of coral reefs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1elsb4%3D&md5=49096c324f4ef3066d55b164ac2e9913CAS | 12920289PubMed |
Hughes, T. P., Rodrigues, M. J., Bellwood, D. R., Ceccarelli, D., Hoegh-Guldberg, O., McCook, L., Moltschaniwskyj, N., Pratchett, M. S., Steneck, R. S., 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 | 1:CAS:528:DC%2BD2sXhvVyjur0%3D&md5=8de3503313175d380c6bb6b7633b15c1CAS | 17291763PubMed |
Jones, G. P., and McCormick, M. I. (2002) Chapter 10 – Numerical and energetic processes in the ecology of coral reef fishes. In ‘Coral Reef Fishes’. (Ed. P. F. Sale.) pp. 221–238. (Academic Press: San Diego, CA, USA.)
Jones, G., Almany, G. R., Russ, G. R., Sale, P., Steneck, R., van Oppen, M., and Willis, B. L. (2009). Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28, 307–325.
| Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges.Crossref | GoogleScholarGoogle Scholar |
Kingsford, M. J., Leis, J. M., Shanks, A., Lindeman, K. C., Morgan, S. G., and Pineda, J. (2002). Sensory environments, larval abilities and local self-recruitment. Bulletin of Marine Science 70, 309–340.
Knowlton, N., and Jackson, J. B. C. (2008). Shifting baselines, local impacts, and global change on coral reefs. PLOS Biology 6, e54.
| Shifting baselines, local impacts, and global change on coral reefs.Crossref | GoogleScholarGoogle Scholar | 18303956PubMed |
Komyakova, V., Munday, P. L., and Jones, G. P. (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 | 24349455PubMed |
Lecchini, D., and Galzin, R. (2005). Spatial repartition and ontogenetic shifts in habitat use by coral reef fishes (Moorea, French Polynesia). Marine Biology 147, 47–58.
| Spatial repartition and ontogenetic shifts in habitat use by coral reef fishes (Moorea, French Polynesia).Crossref | GoogleScholarGoogle Scholar |
Lecchini, D., Waqalevu, V., Parmentier, E., Radford, C., and Banaigs, B. (2013). Fish larvae prefer coral over algal water cues: implications of coral reef degradation. Marine Ecology Progress Series 475, 303–307.
| Fish larvae prefer coral over algal water cues: implications of coral reef degradation.Crossref | GoogleScholarGoogle Scholar |
McClanahan, T. R., Ateweberhan, M., Muhando, C. A., Maina, J., and Mohammed, M. S. (2007). Effects of climate and seawater temperature variation on coral bleaching and mortality. Ecological Monographs 77, 503–525.
| Effects of climate and seawater temperature variation on coral bleaching and mortality.Crossref | GoogleScholarGoogle Scholar |
McCook, L. J. (1999). Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18, 357–367.
| Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar |
McLeod, E., Moffitt, R., Timmermann, A., Salm, R., Menviel, L., Palmer, M. J., Selig, E. R., Casey, K. S., and Bruno, J. F. (2010). Warming seas in the coral triangle: coral reef vulnerability and management implications. Coastal Management 38, 518–539.
| Warming seas in the coral triangle: coral reef vulnerability and management implications.Crossref | GoogleScholarGoogle Scholar |
Menge, B. A. (2000). Top-down and bottom-up community regulation in marine rocky intertidal habitats. Journal of Experimental Marine Biology and Ecology 250, 257–289.
| Top-down and bottom-up community regulation in marine rocky intertidal habitats.Crossref | GoogleScholarGoogle Scholar | 10969172PubMed |
Mumby, P. J., Dahlgren, C. P., Harborne, A. R., Kappel, C. V., Micheli, F., Brumbaugh, D. R., Holmes, K. E., Mendes, J. M., Broad, K., Sanchirico, J. N., Buch, K., Box, S., Stoffle, R. W., and Gill, A. B. (2006). Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311, 98–101.
| Fishing, trophic cascades, and the process of grazing on coral reefs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1egtQ%3D%3D&md5=45e5fd0e2ced9ef339bdce294744602bCAS | 16400152PubMed |
Mumby, P. J., Harborne, A. R., Williams, J., Kappel, C. V., Brumbaugh, D. R., Micheli, F., Holmes, K. E., Dahlgren, C. P., Paris, C. B., and Blackwell, P. G. (2007). Trophic cascade facilitates coral recruitment in a marine reserve. Proceedings of the National Academy of Sciences of the United States of America 104, 8362–8367.
| Trophic cascade facilitates coral recruitment in a marine reserve.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtVertbg%3D&md5=5fc719ed87177a2bcb68c6933f2907f2CAS | 17488824PubMed |
Munday, P., Jones, G., and Caley, M. (1997). Habitat specialisation and the distribution and abundance of coral-dwelling gobies. Marine Ecology Progress Series 152, 227–239.
| Habitat specialisation and the distribution and abundance of coral-dwelling gobies.Crossref | GoogleScholarGoogle Scholar |
Myers, R. A., Baum, J. K., Shepherd, T. D., Powers, S. P., and Peterson, C. H. (2007). Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850.
| Cascading effects of the loss of apex predatory sharks from a coastal ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsFSitrw%3D&md5=46fc872a3098aa00922b3337e654d3f0CAS | 17395829PubMed |
Neudecker, S. (1989). Eye camouflage and false eyespots: chaetodontid responses to predators. Environmental Biology of Fishes 25, 143–157.
| Eye camouflage and false eyespots: chaetodontid responses to predators.Crossref | GoogleScholarGoogle Scholar |
Nyström, M., Folke, C., and Moberg, F. (2000). Coral reef disturbance and resilience in a human-dominated environment. Trends in Ecology & Evolution 15, 413–417.
| Coral reef disturbance and resilience in a human-dominated environment.Crossref | GoogleScholarGoogle Scholar |
O’Leary, J. K., Potts, D. C., Braga, J. C., and McClanahan, T. R. (2012). Indirect consequences of fishing: reduction of coralline algae suppresses juvenile coral abundance. Coral Reefs 31, 547–559.
| Indirect consequences of fishing: reduction of coralline algae suppresses juvenile coral abundance.Crossref | GoogleScholarGoogle Scholar |
Pace, M. L., Cole, J. J., Carpenter, S. R., and Kitchell, J. F. (1999). Trophic cascades revealed in diverse ecosystems. Trends in Ecology & Evolution 14, 483–488.
| Trophic cascades revealed in diverse ecosystems.Crossref | GoogleScholarGoogle Scholar |
Pandolfi, J. M., Jackson, J. B. C., Baron, N., Bradbury, R. H., Guzman, H. M., Hughes, T. P., Kappel, C. V., Micheli, F., Ogden, J. C., Possingham, H. P., and Sala, E. (2005). Are US coral reefs on the slippery slope to slime? Science 307, 1725–1726.
| Are US coral reefs on the slippery slope to slime?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisVyrsL0%3D&md5=c57ccf44fb9148659fca0dcffcbc6777CAS | 15774744PubMed |
Power, M. E. (1992). Top-down and bottom-up forces in food webs: do plants have primacy. Ecology 73, 733–746.
| Top-down and bottom-up forces in food webs: do plants have primacy.Crossref | GoogleScholarGoogle Scholar |
Pratchett, M. S., and Berumen, M. L. (2008). Interspecific variation in distributions and diets of coral reef butterflyfishes (Teleostei: Chaetodontidae). Journal of Fish Biology 73, 1730–1747.
| Interspecific variation in distributions and diets of coral reef butterflyfishes (Teleostei: Chaetodontidae).Crossref | GoogleScholarGoogle Scholar |
Pratchett, M. S., Wilson, S. K., and Baird, A. H. (2006). Declines in the abundance of Chaetodon butterflyfishes following extensive coral depletion. Journal of Fish Biology 69, 1269–1280.
| Declines in the abundance of Chaetodon butterflyfishes following extensive coral depletion.Crossref | GoogleScholarGoogle Scholar |
Pratchett, M. S., Berumen, M. L., Marnane, M. J., Eagle, J. V., and Pratchett, D. J. (2008). Habitat associations of juvenile versus adult butterflyfishes. Coral Reefs 27, 541–551.
| Habitat associations of juvenile versus adult butterflyfishes.Crossref | GoogleScholarGoogle Scholar |
Prugh, L. R., Stoner, C. J., Epps, C. W., Bean, W. T., Ripple, W. J., Laliberte, A. S., and Brashares, J. S. (2009). The rise of the mesopredator. Bioscience 59, 779–791.
| The rise of the mesopredator.Crossref | GoogleScholarGoogle Scholar |
Rasquinho, O., Liu, J., and Leong, D. (2013). Assessment on disaster risk reduction of Tropical Storm Washi. Tropical Cyclone Research and Review 2, 169–175.
Richardson, A. J., and Schoeman, D. S. (2004). Climate impact on plankton ecosystems in the Northeast Atlantic. Science 305, 1609–1612.
| Climate impact on plankton ecosystems in the Northeast Atlantic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntlGrsr4%3D&md5=f8c061b46616bce5f059c7fa1259c9d7CAS | 15361622PubMed |
Ridgeway, G. (2007) Generalized Boosted Models: a guide to the gmb package. Available at http://www.saedsayad.com/docs/gbm2.pdf [Verified 14 August 2014].
Rizzari, J. R., Frisch, A. J., Hoey, A. S., and McCormick, M. I. (2014). Not worth the risk: apex predators suppress herbivory on coral reefs. Oikos 123, 829–836.
| Not worth the risk: apex predators suppress herbivory on coral reefs.Crossref | GoogleScholarGoogle Scholar |
Russ, G. R., Stockwell, B., and Alcala, A. C. (2005). Inferring versus measuring rates of recovery in no-take marine reserves. Marine Ecology Progress Series 292, 1–12.
| Inferring versus measuring rates of recovery in no-take marine reserves.Crossref | GoogleScholarGoogle Scholar |
Sale, P. F. (2004). Connectivity, recruitment variation, and the structure of reef fish communities. Integrative and Comparative Biology 44, 390–399.
| Connectivity, recruitment variation, and the structure of reef fish communities.Crossref | GoogleScholarGoogle Scholar | 21676724PubMed |
Stella, J. S., Pratchett, M. S., Hutchings, P. A., and Jones, G. P. (2011) ‘Coral-associated Invertebrates: Diversity, Ecological Importance and Vulnerability to Disturbance.’ pp. 43–104. (CRC Press: Boca Raton, FL, USA.)
Tkachenko, K. S., and Soong, K. (2010). Protection of habitat types: a case study of the effectiveness of a small marine reserve and impacts of different habitats on the diversity and abundance of coral reef fishes. Zoological Studies (Taipei, Taiwan) 49, 195–210.
United States Naval Research Laboratory Marine Meteorology Division (2011) Washi TrackFile. (United States Naval Research Laboratory Marine Meteorology Division: Monterey, CA, USA.)
Veron, J. E. N., Hoegh-Guldberg, O., Lenton, T. M., Lough, J. M., Obura, D. O., Pearce-Kelly, P., Sheppard, C. R. C., Spalding, M., Stafford-Smith, M. G., and Rogers, A. D. (2009). The coral reef crisis: the critical importance of <350 ppm CO2. Marine Pollution Bulletin 58, 1428–1436.
| The coral reef crisis: the critical importance of <350 ppm CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFygs7zJ&md5=92e0f8c7aa51a2d182f0ea29e6e38999CAS |
Ware, D. M., and Thomson, R. E. (2005). Bottom-up ecosystem trophic dynamics determine fish production in the northeast pacific. Science 308, 1280–1284.
| Bottom-up ecosystem trophic dynamics determine fish production in the northeast pacific.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1CiurY%3D&md5=7b8868a83e6971091d19fc69eeba3e0dCAS | 15845876PubMed |
Webster, M. (2002). Role of predators in the early post-settlement demography of coral-reef fishes. Oecologia 131, 52–60.
| Role of predators in the early post-settlement demography of coral-reef fishes.Crossref | GoogleScholarGoogle Scholar |
Williams, D. M., English, S., and Milicich, M. J. (1994). Annual recruitment surveys of coral reef fishes are good indicators of patterns of settlement. Bulletin of Marine Science 54, 314–331.
Wilson, S. K., Fisher, R., Pratchett, M. S., Graham, N. A. J., Dulvy, N. K., Turner, R. A., Cakacaka, A., Polunin, N. V. C., and Rushton, S. P. (2008). Exploitation and habitat degradation as agents of change within coral reef fish communities. Global Change Biology 14, 2796–2809.
| Exploitation and habitat degradation as agents of change within coral reef fish communities.Crossref | GoogleScholarGoogle Scholar |
Yambao, A. C., White, A. T., Ablong, W. E., and Alcala, M. R. (2001) ‘Coastal Environmental Profile of Negros Oriental.’ Philippines Department of Environment and Natural Resources, number 9719229020. (Philippines Department of Environment and Natural Resources: Cebu City, Philippines.)
