The interaction between herbivores, algae, and corals is a key to understand coral reef resilience. However, most previous studies have focused on herbivorous fishes and have conducted in the Caribbean and the Great Barrier Reef. Therefore, information on other herbivores and/or outside the regions is scarce, causing a serious information deficiency.
In this PhD study, we examined the interaction between herbivores, algae, and corals in southern Taiwan through field surveys and an in situ cage experiment. In the first study (Chapter 2), we examined herbivore assemblages in southern Taiwan and determinants of juvenile coral abundance (proxy of coral recovery) thereby considering eight factors. We found that diadematid sea urchins were dominant herbivores in many reef sites, compared with herbivorous fishes and gastropods, and diadematid abundance was the best (positive) predictor of juvenile coral abundance in generalized linear mixed models (GLMMs).
In the second study (Chapter 3), we conducted an in situ cage experiment using three density conditions (0, 8, 16 indiv./m2) of the locally dominant diadematid, Diadema savignyi. Results demonstrated a strong algal control by D. savignyi: algal cover (biomass) declined rapidly from 95% (1.5 g/100cm2) in 0 indiv./m2 to 47% (0.5) in 8 indiv./m2 and 5–16% (0.02) in 16 indiv./m2. On the other hand, coral recruitment process, examined in coral recruit density and growth/survival of small coral fragments (proxy of coral juveniles) significantly declined in 16 indiv./m2, whereas those were similar between 0 and 8 indiv./m2.
In the third study (Chapter 4), we examined the assemblage structure and determinants of abundance in diadematid sea urchins in southern Taiwan, as their ecological information was virtually lacking. We identified five species and one species complex from two genera based on morphology and colour patterns: Diadema savignyi, D. paucispinum, D. setosum, Diadema spp., Echinothrix calamaris, and E. diadema. Of these, D. savignyi was the dominant species (32.1% of total), and D. savignyi, Diadema spp., E. calamaris, and E. diadema were commonly observed at most study sites. Among seven factors considered, macroalgal cover was the only significant (positive) predictor of diadematid abundance in the GLMM.
Results of this PhD study elucidated the increasingly important role of diadematid sea urchins in coral recovery, via controlling algae and enhancing coral recruitment process. This phenomenon is most likely occurred by a probable shift in dominant herbivores from herbivorous fishes to non-fishery species, diadematid sea urchins under chronic overfishing in southern Taiwan. We suggest to consider the remnant, but often ignored herbivores, diadematid sea urchins in management and conservation planning of coral reefs, along with recovery efforts for other key macro-herbivores, herbivorous fishes and gastropods.

References
Adam, T. C., Burkepile, D. E., Ruttenberg, B. I., & Paddack, M. J. (2015). Managing herbivores for their impacts on Caribbean coral reef ecosystems: A summary report for managers and practitioners. PRBD-2015-1. US National Marine Fisheries Service.
Anthony, K. R., Marshall, P. A., Abdulla, A., Beeden, R., Bergh, C., Black, R., . . . Graham, N. A. (2015). Operationalizing resilience for adaptive coral reef management under global environmental change. Global Change Biology, 21(1), 48-61.
Bak, R. P., & van Eys, G. (1975). Predation of the sea urchin Diadema antillarum Philippi on living coral. Oecologia, 20(2), 111-115.
Bellwood, D. R., Hughes, T. P., Folke, C., & Nystrom, M. (2004). Confronting the coral reef crisis. Nature, 429(6994), 827-833.
Bellwood, D. R., Hughes, T. P., & Hoey, A. S. (2006). Sleeping functional group drives coral-reef recovery. Current Biology, 16(24), 2434-2439.
Birkeland, C. (1977). The importance of rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits. Paper presented at the Proc. 3rd Int. Coral Reef Symp.
Bruno, J. F., & Selig, E. R. (2007). Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS ONE, 2(8), e711.
Burkepile, D. E., & Hay, M. E. (2008). Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proceedings of the National Academy of Sciences, 105(42), 16201-16206.
Carpenter, R. C. (1981). Grazing by Diadema antillarum (Philippi) and its effects on the benthic algal community. Journal of Marine Research, 39, 749-765.
Carpenter, R. C. (1986). Partitioning Herbivory and Its Effects on Coral Reef Algal Communities. Ecological Monographs, 56(4), 345-364. doi:10.2307/1942551
Carpenter, R. C., & Edmunds, P. J. (2006). Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecol Lett, 9(3), 271-280.
Coppard, S. E., & Campbell, A. C. (2007). Grazing preferences of diadematid echinoids in Fiji. Aquatic botany, 86(3), 204-212.
Dumont, C. P., Lau, D. C., Astudillo, J. C., Fong, K. F., Chak, S. T., & Qiu, J.-W. (2013). Coral bioerosion by the sea urchin Diadema setosum in Hong Kong: Susceptibility of different coral species. Journal of Experimental Marine Biology and Ecology, 441, 71-79.
Edmunds, P. J., & Carpenter, R. C. (2001). Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. Proceedings of the National Academy of Sciences, 98(9), 5067-5071.
Fabricius, K. E. (2011). Factors determining the resilience of coral reefs to eutrophication: a review and conceptual model. Coral reefs: an ecosystem in transition (pp. 493-505): Springer.
Furman, B., & Heck, K. L. (2009). Differential impacts of echinoid grazers on coral recruitment. Bulletin of Marine Science, 85(2), 121-132.
Gardner, T. A., Côté, I. M., Gill, J. A., Grant, A., & Watkinson, A. R. (2003). Long-term region-wide declines in Caribbean corals. Science, 301(5635), 958-960.
Graham, N. A., Bellwood, D. R., Cinner, J. E., Hughes, T. P., Norström, A. V., & Nyström, M. (2013). Managing resilience to reverse phase shifts in coral reefs. Frontiers in Ecology and the Environment, 11(10), 541-548.
Hay, M. E. (1984). Patterns of fish and urchin grazing on Caribbean coral reefs: are previous results typical? Ecology, 65(2), 446-454.
Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., . . . Caldeira, K. (2007). Coral reefs under rapid climate change and ocean acidification. Science, 318(5857), 1737-1742.
Holling, C. S. (1973). Resilience and stability of ecological systems. Annual Review of Ecology and Systematics, 4(1), 1-23.
Hughes, Baird, A. H., Dinsdale, E. A., Moltschaniwskyj, N. A., Pratchett, M. S., Tanner, J. E., & Willis, B. L. (1999). Patterns of recruitment and abundance of corals along the Great Barrier Reef. Nature, 397(6714), 59-63.
Hughes, T. P. (1994). Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science, 265(5178), 1547-1551.
Hughes, T. P., Anderson, K. D., Connolly, S. R., Heron, S. F., Kerry, J. T., Lough, J. M., . . . Bridge, T. C. (2018). Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science, 359(6371), 80-83.
Hughes, T. P., Kerry, J. T., Baird, A. H., Connolly, S. R., Dietzel, A., Eakin, C. M., . . . Torda, G. (2018). Global warming transforms coral reef assemblages. Nature. doi:10.1038/s41586-018-0041-2
Hughes, T. P., Rodrigues, M. J., Bellwood, D. R., Ceccarelli, D., Hoegh-Guldberg, O., McCook, L., . . . Willis, B. (2007). Phase Shifts, Herbivory, and the Resilience of Coral Reefs to Climate Change. Current Biology, 17(4), 360-365. doi:https://doi.org/10.1016/j.cub.2006.12.049
Idjadi, J., Haring, R., & Precht, W. (2010). Recovery of the sea urchin Diadema antillarum promotes scleractinian coral growth and survivorship on shallow Jamaican reefs. Mar Ecol Prog Ser, 403, 91-100.
Keck, M., & Sakdapolrak, P. (2013). What is social resilience? Lessons learned and ways forward. Erdkunde, 5-19.
Knowlton, N. (2001). Sea urchin recovery from mass mortality: New hope for Caribbean coral reefs? Proceedings of the National Academy of Sciences, 98(9), 4822-4824.
Lam, K., Shin, P., & Hodgson, P. (2007). Severe bioerosion caused by an outbreak of corallivorous Drupella and Diadema at Hoi Ha Wan Marine Park, Hong Kong. Coral Reefs, 26(4), 893-893.
Lapointe, B. E. (1999). Simultaneous top-down and bottom-up forces control macroalgal blooms on coral reefs (Reply to the comment by Hughes et al.). Limnology and Oceanography, 44(6), 1586-1592.
Lessios, H. (1988). Mass mortality of Diadema antillarum in the Caribbean: what have we learned? Annual Review of Ecology and Systematics, 19(1), 371-393.
Lessios, H., Kessing, B., & Pearse, J. S. (2001). Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution, 55(5), 955-975.
Lewis, J. B. (1966). Growth and breeding in the tropical echinoid Diadema antillarum Philippi. Bulletin of Marine Science, 16(1), 151-158.
Ling, S., Johnson, C., Frusher, S., & Ridgway, K. (2009). Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proceedings of the National Academy of Sciences, 106(52), 22341-22345.
Lirman, D. (2001). Competition between macroalgae and corals: effects of herbivore exclusion and increased algal biomass on coral survivorship and growth. Coral Reefs, 19(4), 392-399.
McClanahan, T. (1988). Coexistence in a sea urchin guild and its implications to coral reef diversity and degradation. Oecologia, 77(2), 210-218.
McClanahan, T., Cokos, B., & Sala, E. (2002). Algal growth and species composition under experimental control of herbivory, phosphorus and coral abundance in Glovers Reef, Belize. Marine Pollution Bulletin, 44(6), 441-451.
McClanahan, T., Muthiga, N., Kamukuru, A., Machano, H., & Kiambo, R. (1999). The effects of marine parks and fishing on coral reefs of northern Tanzania. Biological Conservation, 89(2), 161-182.
McCook, L. (1999). Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs, 18(4), 357-367.
Mcleod, E., Anthony, K. R., Mumby, P. J., Maynard, J., Beeden, R., Graham, N. A., . . . MacGowan, P. (2019). The future of resilience-based management in coral reef ecosystems. Journal of environmental management, 233, 291-301.
Miller, M., Hay, M., Miller, S., Malone, D., Sotka, E., & Szmant, A. (1999). Effects of nutrients versus herbivores on reef algae: a new method for manipulating nutrients on coral reefs. Limnology and Oceanography, 44(8), 1847-1861.
Mortensen, T. (1940). A Monograph of the Echinoidea, Vol. III. 1: Aulodonta with additions to Vol. II (Lepidocentroida and Stirodonta). Atlas: CA Reitzel.
Mumby, P. J. (2006). The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecological Applications, 16(2), 747-769.
Mumby, P. J., Harborne, A. R., Williams, J., Kappel, C. V., Brumbaugh, D. R., Micheli, F., . . . Blackwell, P. G. (2007). Trophic cascade facilitates coral recruitment in a marine reserve. Proceedings of the National Academy of Sciences, 104(20), 8362-8367.
Mumby, P. J., & Steneck, R. S. (2008). Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends in ecology & evolution, 23(10), 555-563.
Muthiga, N., & McClanahan, T. (2007). Chapter 11 Ecology of Diadema (Vol. 37).
Myhre, S., & Acevedo-Gutiérrez, A. (2007). Recovery of sea urchin Diadema antillarum populations is correlated to increased coral and reduced macroalgal cover. Marine Ecology Progress Series, 329, 205-210.
Neilson, B. J., Wall, C. B., Mancini, F. T., & Gewecke, C. A. (2018). Herbivore biocontrol and manual removal successfully reduce invasive macroalgae on coral reefs. PeerJ, 6, e5332.
Nozawa, Y., Lin, C.-H., & Meng, P.-J. (2020). Sea urchins (diadematids) promote coral recovery via recruitment on Taiwanese reefs. Coral Reefs. doi:10.1007/s00338-020-01955-1
O’Leary, J., Potts, D., Schoenrock, K., & McClahanan, T. (2013). Fish and sea urchin grazing opens settlement space equally but urchins reduce survival of coral recruits. Marine Ecology Progress Series, 493, 165-177.
Ogden, J. C., & Lobel, P. S. (1978). The role of herbivorous fishes and urchins in coral reef communities. Environmental Biology of Fishes, 3(1), 49-63.
Pandolfi, J. M., Bradbury, R. H., Sala, E., Hughes, T. P., Bjorndal, K. A., Cooke, R. G., . . . Paredes, G. (2003). Global trajectories of the long-term decline of coral reef ecosystems. Science, 301(5635), 955-958.
Pearse, J. (1998). Distribution of Diadema savignyi and D. setosum in the tropical Pacific. Echinoderms: San Francisco. AA Balkema, Rotterdam, 777-782.
Randall, J., Schroeder, R., & Starck, W. (1964). Notes on the biology of the echinoid Diadema antillarum. Caribb. J. Sci, 4(2-3), 421-433.
Ruengsawang, N., & Yeemin, T. (2000). Bioerosion caused by grazing activities on coral communities in the Gulf of Thailand. Proc. 9th Int. Coral Reef Symp, 1, 289-294.

Sammarco, P. W. (1980). Diadema and its relationship to coral spat mortality: grazing, competition, and biological disturbance. Journal of Experimental Marine Biology and Ecology, 45(2), 245-272.
Sammarco, P. W. (1982a). Echinoid grazing as a structuring force in coral communities: whole reef manipulations. Journal of Experimental Marine Biology and Ecology, 61(1), 31-55.
Sammarco, P. W. (1982b). Effects of grazing by Diadema antillarum Philippi (Echinodermata: Echinoidea) on algal diversity and community structure. Journal of Experimental Marine Biology and Ecology, 65(1), 83-105.
Sammarco, P. W., Levinton, J., & Ogden, J. (1974). Grazing and control of coral-reef community structure by Diadema antillarum Philippi (Echinodermata-Echinoidea)-preliminary study. Journal of Marine Research, 32(1), 47-53.
Solandt, J., & Campbell, A. C. (2001). Macroalgal feeding characteristics of the sea urchin Diadema antillarum Philippi at Discovery Bay, Jamaica. Caribbean Journal of Science, 37(3/4), 227-238.
Steneck, R. S., & Dethier, M. N. (1994). A functional group approach to the structure of algal-dominated communities. Oikos, 69(3), 476-498.
Tuya, F., Haroun, R. J., Boyra, A., & Sanchez-Jerez, P. (2005). Sea urchin Diadema antillarum: different functions in the structure and dynamics of reefs on both sides of the Atlantic. Marine Ecology Progress Series, 302, 307-310.
Tuya, F., Martin, J., Reuss, G., & Luque, A. (2001). Food preferences of the sea urchin Diadema antillarum in Gran Canaria Island (Central-East Atlantic Ocean). J Mar Biol Assoc UK, 81, 1-5.
Uy, F., Bongalo, J., & Dy, D. T. (2001). Bioerosion potential of three species of sea urchins commonly found in the reef flats of eastern Mactan Island, Cebu, Philippines. Philippine Scientist (Philippines).
Williams, I. D., Kindinger, T. L., Couch, C. S., Walsh, W. J., Minton, D., & Oliver, T. A. (2019). Can Herbivore Management Increase the Persistence of Indo-Pacific Coral Reefs? Frontiers in Marine Science, 6(557). doi:10.3389/fmars.2019.00557