Vol. 489: 125–141, 2013 MARINE ECOLOGY PROGRESS SERIES Published August 28 doi: 10.3354/meps10427 Mar Ecol Prog Ser OPENPEN ACCESSCCESS Temporal changes in benthic assemblages on Florida Keys reefs 11 years after the 1997/1998 El Niño R. R. Ruzicka1,*, M. A. Colella1, J. W. Porter2, J. M. Morrison3, J. A. Kidney1, V. Brinkhuis1, K. S. Lunz1, K. A. Macaulay1, L. A. Bartlett1, M. K. Meyers2, J. Colee4 1Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, 100 8th Avenue SE, Saint Petersburg, Florida 33701, USA 2Odum School of Ecology, University of Georgia, 140 East Green Street, Athens, Georgia 30602, USA 3US Geological Survey, St. Petersburg Coastal and Marine Science Center, 600 4th Street S, Saint Petersburg, Florida 33701, USA 4Institute of Food and Agricultural Services, University of Florida, 406 McCarty Hall C, PO Box 110339, Gainesville, Florida 32611, USA ABSTRACT: Disturbances that result in the mass mortality of reef-building corals are changing the appearance of reefs worldwide. Many reefs are transitioning away from scleractinian-coral- dominated assemblages to benthic communities composed primarily of non-scleractinian taxa. This study evaluated recovery patterns of reef communities in the Florida Keys following the mortality associated with the 1997/1998 El Niño. We examined temporal trends among the 5 most spatially abundant reef taxa and stony coral species from 1999 to 2009 at 3 spatial scales, and applied a Principal Coordinate Analysis (PCoA) to determine whether changes in their cover resulted in a shift in community structure. Trends of decreasing stony coral cover were not identi- fied Keys-wide between 1999 and 2009, but 2 of the 3 habitats examined—shallow and deep for- ereefs—did show a significant decline in cover. Concomitantly, octocoral cover significantly increased Keys-wide and in all 3 habitats. The transition to octocorals was most evident on shallow forereefs, where octocoral cover significantly increased at 9 of 12 reefs and overwhelmingly influ- enced the PCoA. On deep forereefs, octocoral and sponge cover did significantly increase, but did not impart a clearly defined shift in community structure like that observed on shallow forereefs. Community composition at patch reefs was relatively consistent during the study, but the increase in octocoral cover may accelerate further following a cold-water mortality event in 2010. These results demonstrate that octocorals are emerging as the predominant benthic taxa in the Florida Keys. Although the transition to octocorals may have started long ago, their apparent resilience to present-day stressors will likely allow this shift to continue into the foreseeable future. KEY WORDS: Coral reefs · Stony corals · Octocorals · Macroalgae · Phase shifts · Principal Coordinate Analysis INTRODUCTION atures and seawater acidity, habitat loss stemming from destructive fishing practices, food web imbal- Modern coral reefs are endangered due to a myr- ances facilitated by overfishing, sedimentation asso- iad of natural and anthropogenic stressors. Numer- ciated with agricultural and construction activities, ous global and local threats to reef-building corals and eutrophication and pathogen introduction due to have been documented. These include reduced watershed pollution and contamination (Hughes et growth and survival due to increasing ocean temper- al. 2003, Burke et al. 2011). Many of these stressors © The authors and Fish & Wildlife Research, Florida, Fish & Wildlife Conservation Commission 2013. Open Access under Creative Com- *Email: [email protected] mons by Attribution Licence. Use, distribution and reproduction are un restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 126 Mar Ecol Prog Ser 489: 125–141, 2013 (e.g. overfishing and coastal development) have long macroalgae). Frequently, these studies are limited in historical precedents leading to chronic, systemic spatial and temporal resolution (e.g. have only a few repercussions (Jackson et al. 2001, Pandolfi et al. study sites or a few years of data). Such limitations 2003). Others have arisen and intensified more often result in misleading characterizations of the recently (e.g. mass stony coral bleaching events and status of reefs (e.g. Pawlik 2011) because succes- disease outbreaks) and pose direct threats to stony sional states can persist for prolonged periods and corals (Harvell et al. 1999, Bruno et al. 2007, Hoegh- natural population fluctuations, irrespective of the Guldberg et al. 2007). The cumulative effect of these larger reef community, can appear as phase shifts stressors has been a worldwide degradation of coral (Connell & Slatyer 1977, Dudgeon et al. 2010). reefs, with some reported to have lost more than half Coral reefs of the Florida Keys are widely consid- their scleractinian cover (Gardner et al. 2003, De’ath ered to be among the most heavily exploited in the et al. 2012). There are instances of degraded reefs world (Kruczynski & McManus 1999, Johns et al. returning to a stony-coral-dominated state, but most 2001), and provide a compelling environment to are confined to the Indo-Pacific region (Connell 1997, study changes in reef community structure. In the Diaz-Pulido et al. 2009, Osborne et al. 2011). In the last 100 yr, serial overfishing has led to the collapse of Caribbean, there is growing evidence that reefs are once-prolific fisheries, including those of queen transitioning from benthic assemblages composed conchs, sponges, turtles, sharks, and groupers (Pan- primarily of stony corals to assemblages dominated dolfi et al. 2005, McClenachan 2009), and the urban- by non-scleractinian taxa (Norström et al. 2009, Roff ization of South Florida has disrupted natural water & Mumby 2012). flow, increased pollution and terrestrial runoff, and One of the most commonly accepted paradigms in intensified the recreational use of reefs by an order of coral reef ecology is that disturbances involving magnitude (Lapointe & Matzie 1996, Johns et al. widespread stony coral mortality lead to ‘phase 2001, Lipp et al. 2002). Reefs in the Florida Keys are shifts’ in community structure (Done 1992, Hughes also vulnerable to emerging threats associated with 1994). Generally, in the immediate aftermath of the climate change, evident in the increasing regularity disturbance, faster-growing, weedier species with of warm-water-induced mass bleaching events in the high reproductive output colonize the space vacated past 30 yr (Causey 2001, Wagner et al. 2010), and to by the long-lived, slow-growing, reef-building the regional spread of marine pandemics, including corals. The weedier species may become well-estab- the mass mortalities of the echinoid Diadema antil- lished and persist indefinitely, preventing a return to larum and the framework-building corals Acropora the original community state (Hughes 1994, Jackson palmata and A. cervicornis (Lessios et al. 1984, Aron- et al. 2001, Rogers & Miller 2006). The most fre- son & Precht 2001). Although the Florida Keys have quently cited example for the Caribbean is the endured a long history of exploitation and pervasive replacement of stony corals by fleshy macroalgae as environmental change, conservation actions have the dominant taxa (Bruno et al. 2009, Dudgeon et al. been implemented over the past 2 decades in an 2010). However, other examples of weedy takeovers attempt to reverse the detrimental effects of overfish- include small, encrusting sponges (Aronson et al. ing and impaired water quality. 2002) and smaller brooding corals like Porites The primary goal of this study was to evaluate the astreoides (Green et al. 2008) and Agaricia tenuifolia response of benthic communities in the Florida Keys (Aronson & Precht 1997, Aronson et al. 2004). The in the 11 yr period following the 1997/1998 El Niño- term ‘phase shift’ implies a switch in the dominant Southern Oscillation, a climatic pattern that induced organisms of a community (Petraitis & Dudgeon extensive ocean warming and was responsible for 2004), but this term has not been well articulated mass scleractinian mortality worldwide during that because ‘dominance’ has often been poorly defined period (Wilkinson 2000, Glynn & Colley 2001). In the (Bruno et al. 2009). This misunderstanding has led to Florida Keys, coral bleaching and increased disease liberal use of ‘phase shifts’ to describe general prevalence associated with this event reduced stony decreases in stony coral cover and relative increases coral cover by ~40% between 1996 and 1999 (Porter in the abundance of other taxa (Rogers & Miller 2006, et al. 2001, Somerfield et al. 2008, Ruzicka et al. Bruno et al. 2009). In addition, many analyses do not 2010). Other benthic groups were affected, with octo- quantify changes in the population structure of the coral cover decreasing ~25% and sponge cover entire community, instead focusing on a single taxo- decreasing ~38% (Harvell et al. 2001, Ruzicka et al. nomic group (e.g. sponges or stony corals) or, at most, 2010). While a leading objective of this study was to a pair of benthic constituents (e.g. stony corals and determine whether stony corals demonstrated any Ruzicka et al.: Changes in Florida Keys benthic assemblages after El Niño 127 Fig. 1. The Florida Keys, showing the location of coral reef evaluation and monitoring project (CREMP) survey sites along the Florida Reef Tract. Shallow and deep forereef sites are paired except for Grecian Rocks, where only the shallow forereef is surveyed