Modeling patterns of coral bleaching at a remote Central Pacific atoll

Abstract

A mild bleaching event (9.2% prevalence) at Palmyra Atoll occurred in response to the 2009 ENSO, when mean water temperature reached 29.8–30.1 °C. Prevalence among both abundant and sparse taxa varied with no clear pattern in susceptibility relating to coral morphology. Seven taxon-specific models showed that turbidity exacerbated while prior exposure to higher background temperatures alleviated bleaching, with these predictors explaining an average 16.3% and 11.5% variation in prevalence patterns, respectively. Positive associations occurred between bleaching prevalence and both immediate temperature during the bleaching event (average 8.4% variation explained) and increased sand cover (average 3.7%). Despite these associations, mean unexplained variation in prevalence equalled 59%. Lower bleaching prevalence in areas experiencing higher background temperatures suggests acclimation to temperature stress among several coral genera, while WWII modifications may still be impacting the reefs via shoreline sediment re-distribution and increased turbidity, exacerbating coral bleaching susceptibility during periods of high temperature stress.

Introduction

Coral bleaching is among a myriad of threats to coral reef survival worldwide, including human overexploitation, ocean acidification, declining water quality, and disease outbreaks (Hoegh-Guldberg, 1999, Harvell et al., 2002, Hughes et al., 2003, Bellwood et al., 2004, Hoegh-Guldberg et al., 2007, De’ath et al., 2009). Bleaching occurs in response to environmental stress (Weis, 2008) and the pale appearance results from the breakdown of the association between the coral host and its symbionts (unicellular photosynthetic dinoflagellates, commonly known as zooxanthellae). This breakdown is manifested as a loss of the symbiotic dinoflagellates or their photosynthetic pigments. Dysfunction of the coral-dinoflagellate symbiosis can lead to coral mortality (Brown and Suharsono,, 1990, Gleason, 1993, Sheppard, 2003, McClanahan, 2004, McClanahan et al., 2004, McClanahan et al., 2007b), decreased coral reproduction (Szmant and Gassman, 1990), reduced reef productivity and growth (Goreau and Macfarlane, 1990, Glynn, 1993, Meesters and Bak, 1993), coral disease outbreaks (Whelan et al., 2007), community shifts towards dominance by smaller, less fecund coral populations (Done, 1999) or larger coral colonies (Edmunds, 2005), and invasion and overgrowth of weakened or dead corals by algae (Diaz-Pulido and McCook, 2002). Extreme bleaching events can even lead to phase shifts resulting in reefs dominated by other benthic organisms such as algae (McClanahan et al., 2001) and sponges (Aronson et al., 2002). Because corals act as facilitators for other reef invertebrates (Idjadi and Edmunds, 2006) and fish (Jones et al., 2004), their loss or resultant community shifts threaten reef biodiversity and functioning.

Coral bleaching events are primarily triggered by extreme seawater temperature anomalies often associated with disturbances to the El Niño-Southern Oscillation (ENSO) (Hoegh-Guldberg, 1999, Hughes et al., 2003, Sheppard, 2003). In 1997–1998, an unprecedented mass bleaching event occurred that affected coral reefs across the globe (Hoegh-Guldberg, 1999, Wilkinson, 1999) and coincided with the strongest ENSO disturbance on record (Kerr, 1999). Bleaching events vary spatially and temporally (West and Salm, 2003, Berkelmans et al., 2004, Obura, 2005), and although extreme temperature anomalies are often the initiating factor (Glynn, 1993, Brown, 1997, Hoegh-Guldberg, 1999, Yee and Barron, 2010), interacting environmental and biological factors are most likely responsible for local prevalence patterns (Fitt et al., 2001, Douglas, 2003, Maina et al., 2008, Yee et al., 2008, Yee and Barron, 2010). Environmental factors include temperature variability (Maina et al., 2008), depth (Marshall and Baird, 2000, Yee et al., 2008), irradiance (Lesser et al., 1990, Iglesias-Prieto et al., 1992, Mumby et al., 2001, Lesser and Farrell, 2004, Gill et al., 2006, Yee et al., 2008), sedimentation (Philipp and Fabricius, 2003), turbidity (Goreau et al., 2000, Otis et al., 2004, Yee et al., 2008), salinity (Glynn, 1993, Meehan and Ostrander, 1997), inorganic nutrients (McClanahan et al., 2003), water flow and mixing rates (Nakamura and van Woesik, 2001, McClanahan et al., 2005, McClanahan et al., 2007b, Yee and Barron, 2010), cool water flushing (Riegl and Piller, 2003), wind speed (Maina et al., 2008, Yee and Barron, 2010) and substrate composition (Ortiz et al., 2009). Biological factors also influence bleaching patterns, including the susceptibility of different coral genera to stress (Marshall and Baird, 2000, McClanahan et al., 2005, McClanahan et al., 2007a, Yee et al., 2008, Brandt, 2009), genotypic variation of the corals and their algal symbionts (Rowan et al., 1997, Smith-Keune and van Oppen, 2006, Sampayo et al., 2008, Suwa et al., 2008, Oliver and Palumbi, 2009), pathogenic infection of corals (Kushmaro et al., 1996, Ben-Haim et al., 2003, Rosenberg et al., 2007), acclimation and adaptation resulting from exposure to past environmental stress and bleaching events (Brown et al., 2002, McClanahan and Maina, 2003, Baker et al., 2004, McClanahan et al., 2005, McClanahan et al., 2007c, Berkelmans and van Oppen, 2006), coral colony size (Bak and Meesters, 1998, Bak and Meesters, 1999, Mumby, 1999, Shenkar et al., 2005, Brandt, 2009), and colony growth form (Hoegh-Guldberg and Salvat, 1995, Marshall and Baird, 2000, Loya et al., 2001, Ortiz et al., 2009). All of these factors, in conjunction with the influence of local anthropogenic stressors (Carilli et al., 2009, Carilli et al., 2010), can interact to mitigate or exacerbate bleaching, with the interactions often being taxon-specific (Anthony and Connolly, 2004, Yee et al., 2008). With future climate change, and expected increases in the frequency and severity of coral bleaching events (Donner et al., 2005), understanding the links between bleaching spatial patterns and environmental conditions will improve future bleaching predictions and help to identify those reefs requiring conservation priority (McClanahan et al., 2007a, McClanahan et al., 2007b). Isolated systems may be amongst the most vulnerable to bleaching-associated impacts due to low levels of biological (larval) connectivity, resulting in reduced genetic diversity and potential for selective resistance and recovery (Graham et al., 2006). These isolated systems offer an insight into bleaching dynamics under reduced levels of reef connectivity (Halford and Caley, 2009); a likely consequence of the predicted global decline of coral reefs.

A mild bleaching event took place at Palmyra Atoll in 2009, a physically isolated reef system in the Central Pacific Ocean. The bleaching event coincided with the strengthening of the 2009 ENSO, when temperature anomalies increased across the eastern and central equatorial Pacific Ocean (NOAA, 2010a). Bleaching warnings were first issued in October 2009, with Palmyra reaching a NOAA bleaching alert level 2 (⩾8 degree heating weeks) by late November 2009 (NOAA, 2010b). We took this opportunity to advance our understanding of the environmental conditions that influence local bleaching prevalence and severity patterns on an isolated reef. Our specific aims were to determine: (1) the environmental associations of variations in bleaching prevalence and severity during a mild bleaching event at Palmyra and (2) the influence of prior exposure to environmental stress (specifically temperature) on patterns of bleaching susceptibility.