BULLETIN OF MARINE SCIENCE. 87(4):767–794. 2011 CORAL REEF PAPER http://dx.doi.org/10.5343/bms.2010.1025 IN TANDEM REEF CORAL AND CRYPtic METAZOAN DECLINES AND EXtiNctiONS Peter W Glynn ABSTRACT Coral reef degradation and loss have been extensively documented worldwide dur- ing the last few decades. While much attention has been directed toward the mor- tality of reef-building corals vis-à-vis various observed disturbances (e.g., bleaching, diseases, overfishing, nutrification), the fate of other reef-associated metazoans, es- pecially invertebrates, has not received sufficient attention. Living and dead cor- als, reef frameworks, and carbonate sediments provide essential habitat niches for a multitude of symbiotic and cryptic species. Thirty-one animal phyla contain species that inhabit coral reefs with known global species richness estimated at 93,000. Pos- sibly as many as 1,000,000 reef-associated metazoans occur globally. Many of these species are undiscovered because of their cryptic or sibling nature. Metazoan reef associates have important functional roles on reefs, e.g., increasing survivorship of coral hosts, aiding in reef framework construction (calcification, consolidation), providing trophic resources, affecting coral mortality (corallivores) and erosion (bioerosion). Despite widespread bleaching and mortality, no reef-building corals (Scleractinia) have yet to become globally extinct. Three populations of Millepora spp. (Hydroida) were severely impacted in Pacific Panama during the 1982–83 El Niño–Southern Oscillation event. Present status indicates recovery of Millepora in- tricata Milne-Edwards and Haime, 1860 to shallow reef zones from relatively deep (10–15 m) refugia. Furthermore, two hydrocoral species have suffered regional ex- tinctions in the eastern Pacific with populations still present in the Indo-Pacific (Millepora platyphylla Hemprich and Ehrenberg, 1834) and eastern Indian Ocean (Millepora boschmai de Weerdt and Glynn, 1991). Considering the large numbers of obligate symbionts and other coral reef metazoan associates, there is a strong likeli- hood of large-scale extinctions following the loss of reef-building corals. Modern coral reefs were perhaps the first reported marine ecosystems to experience region-wide impacts from present-day climate change, principally from sea warming episodes (Glynn 1984, Brown 1987). Several other kinds of disturbances, acting alone or in combination with elevated temperature, have resulted in unprecedented global declines in coral reefs during the past few decades. Documented examples of local to regional-scale damage have been reported for cyclones and related disturbances (Woodley et al. 1981, Knowlton et al. 1990, Hughes and Connell 1999), diseases, including coral and sea urchin epizootics (Lessios et al. 1984, Hughes 1994, Aronson and Precht 1997, Harvell et al. 1999), coastal development and nutrient loading (Wilkinson 2008), and overfishing and the loss of herbivores (Jackson et al. 2001, Pandolfi et al. 2003). Additionally, recent studies have shown that calcification rates in corals and coralline algae are declining due to increasing CO2 levels and associated ocean acidification L( angdon and Atkinson 2005, Kuffner et al. 2008). Critically, most reef-building or zooxanthellate corals, i.e., those engaged in an obligate symbiotic relationship with photoautotrophic dinoflagellates Symbiodinium( spp.), live perilously close to their upper thermal (Glynn and D’Croz 1990, Brown Bulletin of Marine Science 767 OA © 2011 Rosenstiel School of Marine and Atmospheric Science of the University of Miami Open access content 768 BULLETIN OF MARINE SCIENCE. VOL 87, NO 4. 2011 1997, Coles and Brown 2003) and irradiance (Shick et al. 1996, Wellington and Fitt 2003) tolerance limits. If the holobiont (coral host and algal endosymbionts or zooxanthellae) is unduly stressed, the symbiotic association is disrupted, leading to a loss of algae with visible coral bleaching and possible coral death. In the context of contemporary climate change, my aim here is three-fold, namely, to (a) compile evidence of the vulnerability of coral reefs to changing environmental conditions, (b) examine the habitat niches and roles of coral reef invertebrates with special reference to assessing their species richness and potentially destructive ac- tivities, and (c) offer some projections on the fate of coral reefs and how declines in coral hosts and reef habitat structures could impact associated biotas. In contrast to the loss of rain forests, which has resulted mainly from direct over-exploitation by humankind, coral reef loss is largely an indirect result of climate change, i.e., an un- precedented rapid warming of the world’s oceans due to the retention of anthropo- genically-produced greenhouse gases. However, in certain areas (Caribbean), coral mortality has been due primarily to diseases (e.g., Aronson and Precht 2001a, Weil et al. 2006), although elevated sea temperatures may also lower some coral’s resistance to disease (Lesser et al. 2007). Of the various kinds of disturbances, I will focus on increasing seawater tem- perature because of its demonstrated severe global impact to coral reef ecosystems. When first reported in the 1980s, region-wide coral bleaching/mortality events were regarded as acute disturbances, but because of their subsequent frequent occurrences, they are now considered to be chronic (Hoegh-Guldberg 1999, Baker et al. 2008, Fenner and Heron 2009). Even if CO2 emissions can be stopped, modeling results indicate that residual levels of greenhouse gases will allow for continued atmospheric warming for at least 1000 yrs into the future (Solomon et al. 2009). Vulnerability of Reef-Building Corals Reef-building corals live close to their upper temperature tolerance limits, thus contributing to their vulnerability during periods of elevated thermal stress (Hoegh- Guldberg 1999, Baker et al. 2008). This susceptibility to thermal stress was evident in the Florida Keys during the warmest summer months of 1997, 1998, and 2005 when sea surface temperature anomalies reached 0.5–1.0 °C and resulted in widespread coral reef bleaching and mortality (Fig. 1). Recent laboratory and field studies also suggest an interactive effect of elevated pCO2 and temperature that together depress coral calcification (Reynaud et al. 2003, De’ath et al. 2009, Tanzil et al. 2009). Thus, with increasing temperature stress and a declining aragonitic saturation state, coral health and skeletal growth could become rapidly compromised. Anomalously elevated temperatures also interact synergistically with high irradi- ance levels, including ultraviolet radiation, that cause coral bleaching (Gleason and Wellington 1993, Dunne and Brown 1996). Reduced salinity, generally more influ- ential locally, also has been identified as a stressor causing coral bleaching (Brown 1997). Finally, disease prevalence has been shown to increase at higher temperatures as well (Brandt and McManus 2009). Whether bacterial infections during periods of high temperature stress can initiate mass bleaching events (Kushmaro et al. 1998, Ben-Haim Rozenblat and Rosenberg 2003) or are the result of weakened corals offer- ing an increased opportunity for microbial invasions (Mydlarz et al. 2006, Lesser et al. 2007, Ainsworth et al. 2008) remains to be determined. GLYnn: coral REEF metaZoan EXtinctions 769 Figure 1. Time series plots of monthly mean sea surface temperature anomalies at five Florida Keys coral reef sites during the warmest seasonal period (July–September). Each bar represents 1 mo, white bars identify bleaching years. Modified after Manzello et al. (2007). According to Wilkinson’s (2008) assessment of the condition of global coral reefs during the past few decades, 19% have been effectively destroyed, and 35% are under threat of loss in 20–40 yrs. Jackson’s (2008) assessment of reef coral decline is even higher, with an overall 61% loss of coral cover globally. Coral cover losses at 263 monitored Caribbean reef sites demonstrated a mean decline of from ~54% to 9% over a three decade period (Gardner et al. 2003). In 2005, the northern hemisphere experienced the highest mean temperature since reliable records began in 1880. At that time, much of the eastern Caribbean experienced record high coral mortality. Coral reefs in the US Virgin Islands, the heaviest impacted area, suffered 51.5% coral mortality overall (Wilkinson and Souter 2008). In terms of species’ vulnerabilities, a comprehensive analysis concluded that one-third of all known reef-building corals (~231 of 704 species that could be assigned conservation status) are at an elevated risk of extinction from climate change and local impacts (Carpenter et al. 2008). These recent assessments indicate that coral losses and reef degradation have been substantial on a global scale. Because in recent years some coral reefs have shown significant recovery of live coral cover (e.g., Connell 1997, Coles and Brown 2003, Guzman and Cortés 2007, Wellington and Glynn 2007), it could be argued that perhaps these ecosystems pos- sess an inherent resilience with a capacity for continued existence, albeit in some altered state. An analysis of recovery after major bleaching events has shown that the majority of disturbed reefs in the Indian and Central/West Pacific Oceans have 770 BULLETIN OF MARINE SCIENCE. VOL 87, NO 4. 2011 revealed increases in live coral cover (Baker et al. 2008). Whether this recovery will continue at the present increasing pace of ocean warming, disease outbreaks,