Climate change impedes scleractinian corals as primary reef ecosystem engineers

Coral reefs are among themost diverse and productive ecosystems on our planet. Scleractinian corals function as the primary reef ecosystem engineers, constructing the framework that serves as a habitat for all other coral reefassociated organisms. However, the coral’s engineering role is particularly susceptible to global climate change. Ocean warming can cause extensive mass coral bleaching, which triggers dysfunction of major engineering processes. Sub-lethal bleaching results in the reduction of both primary productivity and coral calcification. This may lead to changes in the release of organic and inorganic products, thereby altering critical biogeochemical and recycling processes in reef ecosystems. Thermal stress-induced bleaching and subsequent coral mortality, along with ocean acidification, further lead to long-term shifts in benthic community structure, changes in topographic reef complexity, and the modification of reef functioning. Such shifts may cause negative feedback loops and further modification of coral-derived inorganic and organic products. This review emphasises the critical role of scleractinian corals as reef ecosystem engineers and highlights the control of corals over key reef ecosystem goods and services, including high biodiversity, coastal protection, fishing, and tourism. Thus, climate change by impeding coral ecosystem engineers will impair the ecosystem functioning of entire reefs. Additional keywords: bleaching, ecosystem goods and services, ocean warming and acidification. Scleractinian corals as reef ecosystem engineers Ecosystem engineers are organisms that modulate the availability of resources to other species by causing physical state changes in biotic or abiotic materials (Jones et al. 1994, 1997). Scleractinian corals act as key reef ecosystem engineers in two main ways: first, they are autogenic engineers, because through their calcification and ensuing reef accretion, they change the physical, chemical, and biological environment and thereby provide habitats for associated reef organisms. The generation of complex, hard, and stable substrates by scleractinian corals underpins the high biodiversity characteristic of tropical coralreef ecosystems (Bellwood and Hughes 2001). Second, corals also act as allogenic ecosystem engineers because they intensively generate and transform inorganic and organic materials. Coral-derived inorganic calcareous skeletons are transformed into calcareous reef sands by reefassociated bio-eroding organisms (such as molluscs, echinoderms, and sponges) and by other biological, physical, and CSIRO PUBLISHING www.publish.csiro.au/journals/mfr Marine and Freshwater Research, 2011, 62, 205–215 CSIRO 2011 Open Access 10.1071/MF10254 1323-1650/11/020205 chemical erosion processes (Glynn 1997; Hallock 1997), so that corals, through the production of inorganic materials, control adjacent sediments. These highly permeable biogenic sediments with generally large grain sizes allow intense advective coupling between the water column and the seafloor (Huettel et al. 2003; Rasheed et al. 2003; Wild et al. 2005a). Calcareous reef sands support abundant associated heterotrophic microbes (Wild et al. 2006). Coral-generated calcareous sediments thereby act as biocatalytic filter systems that facilitate rapid processing and recycling of organic matter (Wild et al. 2004a, 2005a, 2005b, 2008). Corals also continuously release large amounts of dissolved and particulate organic materials, which may function as energy carriers and particle traps (Wild et al. 2004a; Huettel et al. 2006; Naumann et al. 2009). This release of organic material promotes the formation ofmucus–particle aggregations in the water column that increase the sedimentation and recycling rates by which essential elements are retained (Wild et al. 2004b, 2005b; Huettel et al. 2006). Consequently, a wide range of biogeochemical processes, important in coral reef functioning, are directly controlled by scleractinian corals acting as the principal ecosystem engineers. This review sets out to expand our understanding of the impacts of global climate change on coral reef ecosystems owing to the direct impediment of the reef’s primary ecosystem engineer – the scleractinian corals. Rather than focusing on the plight of corals per se, we chose to explore how the impacts of oceanwarming and acidificationmay affect the corals’ ability to act as engineers within this complex ecosystem. We discuss the impact of climate change on scleractinian corals at the organism level and how this translates into responses at the reef ecosystem level. The impact of global climate change on the coral engineer As stenothermic and calcifying organisms, corals are particularly sensitive to both ocean acidification and warming. There are several indications that carbon pollution-induced increases in ocean acidity and temperature are impacting the metabolism and growth of reef-building corals (Langdon and Atkinson 2005; De’ath et al. 2009; Tanzil et al. 2009; Manzello 2010). Ocean acidification and coral calcification Increasing acidity of oceanic waters represents a direct threat to reef-building scleractinian corals, with various implications for their role as ecosystem engineers. Ocean acidification is the consequence of global oceanic uptake of increasing anthropogenic atmospheric CO2 (e.g. Kleypas et al. 1999). Such uptake increases CO2 partial pressure (pCO2) in the water column, decreases seawater pH, increases concentrations of total dissolved CO2 ([CO2] and [HCO3]), and reduces concentrations of [CO3 2 ] in seawater (Caldeira and Wickett 2003; Feely et al. 2004). Physiological processes (e.g. calcification) in corals may respond to these changes in ocean chemistry (Langdon and Atkinson 2005). The reduction in [CO3 2 ], at constant seawater calcium concentration [Ca2þ], consequently results in the decrease of the saturation state of aragonite (Oarag), the polymorph of CaCO3 produced by coral calcification. Presently, tropical surface waters, with the exception of the eastern Pacific Ocean, are about 4-fold supersaturated with respect to aragonite (Hoegh-Guldberg et al. 2007). However, Oarag is expected to significantly decrease to levels of 2.5–3.0 by the year 2100 (Feely et al. 2009). Scleractinian corals generally require seawater that is super-saturated in aragonite for efficient aragonite accretion. In acidified seawater, lowered externalOarag impedes the essential increase of Oarag within the internal calcifying fluid, and causes a corresponding decrease in calcification rate (reviewed in Cohen and Holcomb 2009). This decrease in skeletal growth performance, caused by ocean acidification, directly translates to a decline in the engineering capacity of scleractinian corals to construct essential reef habitats. Various studies have documented the negative effect of ocean acidification and the consequential reduction in seawater Oarag on coral calcification in both the laboratory (e.g. Anthony et al. 2008; Jokiel et al. 2008) and the field (Bak et al. 2009; De’ath et al. 2009; Tanzil et al. 2009). However, a very recent study (Jury et al., in press) presents significant differences in calcification rates at equal [CO3 2 ] and further suggests [HCO3 ] as a potentially more important driver for coral calcification, thereby questioning the reliability of Oarag or [CO3 2 ] as sole predictors of the effect of ocean acidification on coral calcification. Another recent study argues that deleterious effects caused by elevated [CO2], as a result of ocean acidification, may be ameliorated by inorganic nutrient enrichment (Holcomb et al. 2010). These authors conclude that naturally elevated inorganic nutrient levels may thus support increased primary and secondary production, consequently facilitating coral calcification in environmenst with naturally high concentrations of CO2. However, species-specific differences in sensitivity to ocean acidification and thermal stress may occur (Manzello 2010). This could have tremendous effects on the structure of communities in future coral reefs (Loya et al. 2001). Ocean acidification can also affect coral reproduction by reducing sperm motility (Morita et al. 2009) or settlement and post-settlement development of planula larvae and coral recruits (Albright et al. 2008; Cohen et al. 2009). At experimentally reduced aragonite saturation states (Oarag), the early skeleton of coral recruits showed progressive changes in aragonite crystal morphology and a decline in crystal growth rate (Cohen et al. 2009). This implies that ocean acidification may significantly affect recruitment rates and the competitive capacity of coral populations, and may consequently lead to a shift in coral community structure. In addition, a recent study showed that spawning female corals of the temperate species Astrangia poculata are more susceptible to the negative effects of ocean acidification than spawning male corals (Holcomb et al., in press). This gender discrimination may be a result of the energetically expensive egg production process, leaving only limited resources to compensate for the effects of acidification on calcification. On a longer time-scale, this lack of energy and growth may reduce recruitment success for gonochoricspawning coral species. Finally, and possibly most alarmingly, ocean acidification has been identified as a potential trigger for coral bleaching (Anthony et al. 2008). According to this study, branching and massive coral species experience an increase in bleaching with decreasing seawater pH (8.4–7.6) at low (25–268C) and high 206 Marine and Freshwater Research C. Wild et al.