Vol. 367: 73–91, 2008 MARINE ECOLOGY PROGRESS SERIES Published September 11 doi: 10.3354/meps07531 Mar Ecol Prog Ser Impact of coral predators on tropical reefs Randi D. Rotjan1, 2,*, Sara M. Lewis1 1Department of Biology, Tufts University, Medford, Massachusetts 02155, USA 2Present address: Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA ABSTRACT: It is well known that herbivores have numerous and diverse impacts on plant and algal fitness, community structure and ecosystem function. The importance of corallivory as a selective force, however, has been underestimated. Corallivores, or consumers of live coral tissue, employ a wide variety of feeding strategies and can be obligate or facultative coral feeders. Our literature review reveals a complex array of corallivores across the globe, represented by 11 families of fishes and 5 invertebrate phyla and totaling over 160 species known to consume scleractinian corals world- wide. Importantly, although these corallivores span a wide taxonomic range, we found that they have been reported to feed on relatively few genera of hard corals, specifically, on only 28 scleractinian genera worldwide. Damage by corallivores ranges from minor to lethal, but there is a growing body of evidence to support that even limited removal of tissue or skeletal structures has growth and/or fit- ness consequences for a scleractinian coral colony. In light of increasing reef stressors and diminish- ing coral populations, we suggest that the role of corallivores in reef trophodynamics is more complex than appreciated previously. KEY WORDS: Coral reef resilience · Herbivory · Trophodynamics Resale or republication not permitted without written consent of the publisher INTRODUCTION attention has been paid to the role corallivores might play in maintaining or conserving coral reef ecosys- Coral reefs are among the most diverse ecosystems tems. on earth, rivaled only by tropical rainforests in species Judging the impact of corallivory on tropical reefs diversity and abundance (reviewed by Reaka-Kudla has been controversial because many corallivores 1997). Scleractinian corals are the major architects of cause little apparent damage to corals, although a tropical reefs, acting as ecosystem engineers (sensu few species are known to cause severe damage. A Jones et al. 1994) and providing the structural frame- variety of organisms consumes living coral, including work for a highly diverse assemblage of marine organ- fishes, annelids, crustaceans, echinoderms, and mol- isms. It is well established that corals worldwide are lusks. Previous reviews on corallivory by Carpenter increasingly threatened by abiotic stressors, including (1997), Glynn (1990b), and Robertson (1970) have changes in seawater temperatures (Jokiel & Coles focused mainly on invertebrates. Robertson (1970) 1977, 1990) and storms (Knowlton et al. 1990, Bythell et provides an excellent description of corallivorous al. 1993, Alvarez-Filip & Gil 2006). Likewise, much prosobranch gastropods. Hixon (1997) reviewed both attention has been given to other stressors, including direct and indirect effects of fishes on corals, includ- overfishing (Myers & Worm 2003) and disease (Suther- ing corallivorous butterflyfish, whose feeding habits land et al. 2004), which can be caused by biotic or abi- have been well described (e.g. Harmelin-Vivien otic factors and also contribute to coral reef decline. 1989). Even though most general discussions of reef Direct consumption of live coral, or corallivory, repre- trophic interactions have ignored the importance of sents another biotic stressor that can adversely affect corallivory, the identities and impacts of corallivores coral fitness and accelerate rates of coral decline have been carefully investigated for a few specific (Knowlton et al. 1990, Rotjan et al. 2006), yet little locations, such as in the Galapagos (Glynn et al. *Email: [email protected] © Inter-Research 2008 · www.int-res.com 74 Mar Ecol Prog Ser 367: 73–91, 2008 1983) and Panama (Glynn et al. 1972, Glynn 2004). MAJOR VERTEBRATE CORALLIVORES However, because no comprehensive review of the impact of corallivores on tropical reefs exists, the The first evidence of vertebrate corallivory was pro- importance of corallivory as a selective force has vided by Darwin (1842) from the HMS ‘Beagle’ in the likely been underestimated. Indian Ocean, where he recovered live coral from the In this review, we provide a comprehensive descrip- stomachs of two Scarus parrotfish species. However, tion of known vertebrate and invertebrate corallivores, vertebrate corallivory received little attention until their foraging modes, and their rates of coral consump- Cousteau (1952) made detailed behavioral observa- tion. Since scleractinian corals are considered to be the tions of parrotfish feeding on live corals. Since then, major reef-builders, we focus exclusively on sclerac- accumulated studies have reported 114 species of tinian corallivores. We describe major shifts in the rel- vertebrates, representing 11 families of osteichthyan ative importance of different corallivore groups across fishes, known to at least occasionally consume live biogeographic regions. We provide a categorization of corals (Appendix 1). The corals most commonly grazed major predators as obligate versus facultative coral by fishes include the genera Acropora, Pocillopora, feeders, and examine whether they specialize on par- Montipora, and Porites. Interestingly, we found that ticular scleractinian coral genera. We review evidence only 18 of the 111 known coral genera (listed in Veron concerning the impact of corallivory on the growth and 2000), a mere 16.2%, have been reported to be even fitness of reef-building corals. We conclude by dis- occasionally consumed by corallivorous fishes (Appen- cussing critical areas for future research necessary dix 1). This suggests that either observational data are for an understanding of the changing role of coralli- incomplete, or that many coral genera have evolved vores and corallivory in reef trophodynamics and reef effective means of deterring predation. resilience. Vertebrate corallivores use each of the coral feeding strategies described above (see also Appendix 1). Ap- proximately half of the 114 corallivorous fishes are CLASSIFICATION OF CORALLIVORE FEEDING butterflyfishes (Chaetodontidae), browsers that re- STRATEGIES move individual coral polyps with long, fleshy lips (Motta 1988, 1989) without damaging the underlying Corallivores differ in their feeding strategies, with skeleton. In contrast, all other piscine corallivores such different consequences for coral prey. ‘Mucus-feeders’ as parrotfish, puffers, triggerfish, filefish, wrasses, and consume only coral mucus without removing any other damselfish have the ability to remove skeletal material live coral tissue or underlying skeleton. Corallivores along with coral tissue, and thus are either excavators that remove coral tissue without damaging the under- or scrapers. The feeding habits of Indo-Pacific parrot- lying calcium carbonate skeleton are known as fishes have been relatively well studied (Bellwood ‘browsers’ (Hiatt & Strasburg 1960). Bellwood & Choat & Choat 1990), and corallivory is restricted to a few (1990) distinguished two feeding modes for parrotfish large excavating species that possess jaw structures that we apply here to all corallivores: ‘excavators’, capable of exerting large forces on their cutting edge. which feed by removing live coral tissue with major Caribbean parrotfish use two distinct grazing behav- portions of the underlying skeleton, and ‘scrapers’ , iors called focused biting and spot-biting (Bruckner which remove live coral tissue while taking only little et al. 2000): in the former, individual fish repeatedly of the accompanying skeleton. These four categories bite a single area, resulting in extensive coral tissue can be used to classify the feeding strategies used by a and skeletal loss (Fig. 1A), whereas in the latter, wide variety of invertebrates and fish corallivores. feeding consists of shallow bites that are widely scat- Some corallivores may also act as bioeroders (con- tered over the colony surface (Fig. 1B). Identifying sumers of dead coral substrate), and these terms are grazing scars can be difficult; both focused and spot- sometimes used interchangably. However, this distinc- biting scars have been mistaken for disease lesions tion is important because corallivores directly affect (Bruckner & Bruckner 1998a,b, 2000). Although live coral and so are likely to have stronger effects on focused biting (Fig. 1C) on live coral has been impli- coral fitness. Bioeroders are known to play an impor- cated in territorial marking by adult terminal phase tant role in coral reef dynamics, re-shaping reef topog- males of the stoplight parrotfish Sparisoma viride raphy by eroding dead skeletons of mound-building (Bruggemann et al. 1994, van Rooij et al. 1995), spot- corals, and weakening colony structure of live branch- biting does not appear to be associated with territorial- ing corals (reviewed by Hutchings 1986, Sammarco ity (Bruckner et al. 2000). Parrotfish grazing behavior 1996). However, because bioeroders do not consume may differ geographically, since focused biting is com- live coral tissue, they are not considered further in this mon in some Caribbean locations, e.g. Puerto Rico review. (Bruckner & Bruckner 1998c), but comparatively rare Rotjan & Lewis: Corallivory across the globe 75 Fig. 1. Grazing