Climate change impacts on coral reefs: Synergies with local effects, possibilities for acclimation,...

Marine Pollution Bulletin xxx (2013) xxx–xxx

Contents lists available at SciVerse ScienceDirect

Marine Pollution Bulletin

journal homepage: www.elsevier .com/locate /marpolbul

Climate change impacts on coral reefs: Synergies with local effects,possibilities for acclimation, and management implications

0025-326X/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.marpolbul.2013.06.011

⇑ Corresponding author.E-mail address: [email protected] (M. Ateweberhan).

Please cite this article in press as: Ateweberhan, M., et al. Climate change impacts on coral reefs: Synergies with local effects, possibilities for acclimand management implications. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.06.011

Mebrahtu Ateweberhan a,⇑, David A. Feary b, Shashank Keshavmurthy c, Allen Chen c, Michael H. Schleyer d,Charles R.C. Sheppard a

a Department of Life Science, University of Warwick, CV4 7AL Coventry, United Kingdomb School of the Environment, University of Technology, Sydney, PO Box 123, Broadway, NSW 2007, Australiac Biodiversity Research Centre, Academia Sinica, 128 Academia Road, Nankang, Taipei 115, Taiwand Oceanographic Research Institute, Durban, South Africa

a r t i c l e i n f o
a b s t r a c t
Most reviews concerning the impact of climate change on coral reefs discuss independent effects ofwarming or ocean acidification. However, the interactions between these, and between these and directlocal stressors are less well addressed. This review underlines that coral bleaching, acidification, and dis-eases are expected to interact synergistically, and will negatively influence survival, growth, reproduc-tion, larval development, settlement, and post-settlement development of corals. Interactions withlocal stress factors such as pollution, sedimentation, and overfishing are further expected to compoundeffects of climate change.

Reduced coral cover and species composition following coral bleaching events affect coral reef fishcommunity structure, with variable outcomes depending on their habitat dependence and trophic spe-cialisation. Ocean acidification itself impacts fish mainly indirectly through disruption of predation-and habitat-associated behavior changes.

Zooxanthellate octocorals on reefs are often overlooked but are substantial occupiers of space; thesealso are highly susceptible to bleaching but because they tend to be more heterotrophic, climate changeimpacts mainly manifest in terms of changes in species composition and population structure. Non-cal-cifying macroalgae are expected to respond positively to ocean acidification and promote microbe-induced coral mortality via the release of dissolved compounds, thus intensifying phase-shifts from coralto macroalgal domination.

Adaptation of corals to these consequences of CO2 rise through increased tolerance of corals and suc-cessful mutualistic associations between corals and zooxanthellae is likely to be insufficient to match therate and frequency of the projected changes.

Impacts are interactive and magnified, and because there is a limited capacity for corals to adapt to cli-mate change, global targets of carbon emission reductions are insufficient for coral reefs, so lower targetsshould be pursued. Alleviation of most local stress factors such as nutrient discharges, sedimentation, andoverfishing is also imperative if sufficient overall resilience of reefs to climate change is to be achieved.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

Many excellent reviews exist concerning the impact of climatechange on coral reefs, although most discuss one or a few aspectswith less attention to interactions (Baker et al., 2008; Eakin et al.,2008; Hoegh-Guldberg et al., 2007; Hughes et al., 2003; Mundayet al., 2008). This review combines current understanding of thetwo most important climate change features affecting coral reefs- ocean warming and ocean acidification, and, where possible,how these interact with local factors of pollution and other ecosys-tem-distorting effects such as overfishing and shoreline alterations

(Burke et al., 2011; McClanahan et al., 2012). Further, some previ-ous reviews have considered a ‘general’ coral reef in understandingclimate change impacts, but today it is well understood that, whilemany general principles apply, various factors and impacts may as-sume different degrees of relative importance in different places.For example, coral reefs within a wealthy country may suffer pri-marily from coastal development, whereas those in an adjacentpoor country may be affected more from chemical or sewage dis-charge, bringing both nutrients and pathogens (Burke et al.,2011; McClanahan et al., 2012). Neither location may show mucheffect from global climate change so far, as those effects could bedwarfed by the more local direct impacts. In contrast, an uninhab-ited and large no-take marine reserve may suffer none of the abovelocal impacts so that consequences of climate change may be the

ation,

http://dx.doi.org/10.1016/j.marpolbul.2013.06.011

mailto:[email protected]


http://www.sciencedirect.com/science/journal/0025326X

http://www.elsevier.com/locate/marpolbul


2 M. Ateweberhan et al. / Marine Pollution Bulletin xxx (2013) xxx–xxx

main effects observed there. In addition, much has been writtenabout the relative importance of ‘competing’ top-down vs. bot-tom-up effects, the former being perhaps fishing of high trophic le-vel animals and an example of the latter being fertilisation effectsfrom unconstrained sewage discharges, but either may be para-mount in different locations.

Fig. 1. Current levels of threats from local stress factors in major coral regions of the

1.1. The two main climate change factors

Scientific evidence on potential risks from CO2 rise is over-whelming, causing both warming and reduction of seawater pH(Trenberth et al., 2007; Arndt et al., 2010). If global greenhousegas (GHG) emissions are not curbed, further increases in globaltemperatures and acidification are expected, beyond levels tolera-ble to corals and calcifying algae - the main reef builders (e.g. Ver-on et al., 2009). Combined with rising seas and shifting weatherpatterns, warming and acidification will have significant impactson global biodiversity, ecological functioning and on people (Bind-off et al., 2007; Hansen et al., 2007, 2008). Much attention has beenplaced on coral reefs because they are one of the most vulnerableecosystems to climate change impacts and because a substantialnumber of the world’s poorest people depend directly on them(Hoegh-Guldberg et al., 2007; Burke et al., 2011). The issue of foodsecurity is paramount in many world forums, and the loss of reef-supplied food in particular is generating considerable concern.

Concentration of CO2e1 in the atmosphere has now reached400 ppm (http://www.co2now.org), rising at about 2.5 ppm CO2eper annum; this rate is expected to accelerate (Meehl et al., 2007).This 40% rise in CO2 levels since the industrial revolution (http://www.esrl.noaa.gov/gmd/ccgg/trends; Orr et al., 2005), means thatCO2 levels are now far exceeding those seen in the past >1 millionyears (Feely et al., 2004; Tripati et al., 2009). At current rates, theaverage rise per annum will reach 3–4 ppm CO2e by the end of thecentury, equivalent to a 50% likelihood of global mean temperatureexceeding the pre-industrial level by 5 �C (Meinshausen et al.,2009). Aside from a warming global climate, this increase in CO2 isalso resulting in reduced ocean pH, carbonate ion concentrationand calcium carbonate saturation state, leading to increased carbon-ate dissolution in the world’s oceans (Feely et al., 2004; Orr et al.,2005).

world. (A) Local threat represents cumulative effects of overfishing and destructivefishing, marine-based pollution and damage, coastal development, watershed-based pollution. (B) Proportion of ‘very threatened’ reefs representing threat levelsof medium to very high’. (Modified from Burke et al. (2011)).

1.2. The main local factors

For many years the main causes of deterioration of coral reefswere from industrial pollution, nutrient pollution from sewageand land run off, and from direct disturbances such as dredging,which liberates vast pulses of pollutants and sediments, as wellas overfishing and destructive fishing. In many areas, these con-cerns have in no way diminished (Fig. 1). For example, in the Ara-bian Gulf all these activities are increasingly present and causingextensive harm to reef systems (Feary et al., 2012; Riegl and Purkis,2012), and even in relatively well-managed seas, such as easternAustralia, nutrient run-off is considered a major problem (Leonand Warnken, 2008). Similarly, overfishing continues to be a majorproblem in many places (Jackson et al., 2001; Hughes et al., 2007)and marine diseases are increasing in extent in many locations(Harvell et al., 2002). All these impacts on coral reefs are associateddirectly with proximity to human activities (Lirman and Fong,2007). In fact, until immediately before the 1998 global warmingevent, ‘risk’ to reefs had a marked correlation with distance to hu-man habitation, with remote reef systems presumed to be less atrisk (Bryant et al., 1998).

1 CO2e refers to all green house gases by converting concentrations of other greenhouse gases into CO2 equivalents.

Please cite this article in press as: Ateweberhan, M., et al. Climate change impaand management implications. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1

1.3. Climate change and local factors

Warming events changed the perception of where future prob-lems might come from. For example, reefs in the Indian Ocean,considered to be at ‘least risk’, turned out to be those most sub-stantially impacted by the 1998 global warming event (Wilkinsonet al., 1999; Sheppard, 2006), but at the same time, some of thosemost remote reefs, also seen as being at ‘least risk’ showed muchfaster subsequent recovery (Sheppard et al., 2008; Ateweberhanet al., 2011). The rise in global temperatures started in the 1970s(e.g. Rayner et al., 2003; Reid and Beaugrand, 2012), a trend scar-cely noticed until much later (Sheppard, 2006). Increasingly, riskfrom warmer water was deemed as being of paramount impor-tance, soon to be followed with increased emphasis on decreasingseawater pH, to the extent that local pollution events were some-times thought to be less important (Bongiorni et al., 2003; Szmant,2002). Globally this may be the case, but local effects and distur-bances remain critical (Fig. 1). Over recent years, climate changeand local stressors have both come to be seen as important butto differing degrees in different places. Some may be easily fixed

cts on coral reefs: Synergies with local effects, possibilities for acclimation,016/j.marpolbul.2013.06.011

http://www.co2now.org

http://www.esrl.noaa.gov/gmd/ccgg/trends

http://www.esrl.noaa.gov/gmd/ccgg/trends


M. Ateweberhan et al. / Marine Pollution Bulletin xxx (2013) xxx–xxx 3

locally, at least in principle (although too rarely is this achieved),while climate effects appear much more intractable. Local factorsare also expected to interact with climate change and amplify theireffects (Knowlton and Jackson, 2008; Wiedenmann et al., 2012).Here, aspects of possible increased resistance and tolerance to ef-fects of climate change are examined, before some managementimplications are addressed.

2. Direct impacts of climate change on corals

2.1. Warming effects of increased global CO2 levels on corals

Coral bleaching follows anomalously high seawater tempera-tures, usually interacting with high levels of irradiation (Brown,1997; Glynn, 1996; Hoegh-Guldberg, 1999). Such episodes have in-creased steadily over the last three decades in both frequency andintensity (Hoegh-Guldberg, 1999; Sheppard, 2003). Recurrences ofextreme thermal events are predicted to increase further (Shepp-ard, 2003) and to become more frequent (Donner et al., 2005;van Hooidonk et al., 2013).

There are numerous examples of extreme bleaching eventscausing widespread coral mortality, declines in coral cover, andchanges in benthic and coral community structure and function(Gardner et al., 2003; Bruno and Selig, 2007; McClanahan et al.,2007c; Schutte et al., 2010; Ateweberhan et al., 2011; Wild et al.,2011). However, patterns of change in coral reefs following bleach-ing events differ considerably depending on location and the struc-ture of the coral and benthic community. For example, severitymay vary markedly with depth (Sheppard, 2006), resulting in ‘refu-gia’ coral populations within deeper reef sections or within lagoons(Feary et al., 2012). In addition, some coral growth forms (e.g. mas-sive and sub-massive forms) can be relatively more resistant tobleaching effects than others (e.g. branching corals). Recovery frombleaching effects, in terms of cover at least, may then differ mark-edly depending on local environmental conditions and communitystructure (McClanahan et al., 2007a,c; Ateweberhan and McClana-han, 2010). Recovery may be severely retarded where there areadditional stressors and may take less time where direct impactsare absent (Sheppard et al., 2008). Nearly a decade has beenneeded for the recovery of coral cover in the Chagos Archipelago(Sheppard et al., 2013) while it has not occurred at all in someother areas of the Indian Ocean (Figs. 2 and 3). However, even

Fig. 2. Comparison of hard coral cover between Chagos and Seychelles, central-western Indian Ocean. Both set of islands are situated in similar latitude-ranges andsuffered similar effects during the 1998 thermal stress event. (Data from Grahamet al. (2008), Ateweberhan et al. (2011), Wilson et al. (2012) and Sheppard et al.(2013)).


when coral cover recovers there may be a shift in the kinds of cor-als that dominate different zones on a reef. This is seen par excel-lence in the Arabian Gulf, for example, where the formerdominance of branching Acropora has changed over large areas todominance by faviids and Porites (Sheppard and Loughland,2002; Purkis and Riegl, 2005). Ecological consequences of thischange in coral community structure have barely been examined(but see Riegl and Purkis (2012).

2.2. Acidification and warming effects on corals

Reduced pH caused by higher CO2 concentrations occurs along-side increased concentration of total dissolved CO2 ([CO2 and[HCO3

-]), which in turn reduces carbonate concentration ([CO2�3 ])

and aragonite saturation (Xarag) in seawater. Ocean acidificationrepresents a direct threat to corals and other calcified reeforganisms as they require aragonite supersaturated waters for cal-cification, and increased bi-carbonate ([HCO�3 ]) drastically reducescalcification (Andersson and Mackenzie, 2011). Dissolution of calci-fied matter will also increase with increased acidification (Kleypaset al., 2006). On average, global oceans now have seawater carbon-ate ion concentrations 30 lmol kg�1 seawater lower than duringpre-industrial levels, and are more acidic by 0.1 pH unit (Bindoffet al., 2007; Dore et al., 2007). This reduction in pH is expected toreach 0.4, or a 2.5–3.0 times increase in [H+] by 2100 (Feely et al.,2009). At a 2 �C rise (caused by 450 ppm CO2e), coral reef organ-isms will exhibit very low calcification rates and will cease to grow,and may start to dissolve at 560 ppm CO2e (�3 �C), (Silvermanet al., 2009). These values are larger than previous estimations of40% reduction in calcification at 560 ppm CO2e (Kleypas et al.,2006). The estimates of Silverman et al. (2009) were based on a lin-ear relationship between calcification and Xarag (Langdon andAtkinson, 2005). However, the process of calcification in coralstakes place inside the animal in isolation from the external envi-ronment and the direct link between calcification and Xarag hasbeen questioned; [HCO�3 ] is believed to influence calcification morethan Xarag (Herfort et al., 2008; Jury et al., 2010). Thus coral speciesmay be better able to control pH and cope better with ocean acid-ification than has been predicted by previous models.

The response of corals and other organisms to ocean acidificat-ion varies with other environmental factors, temperature in partic-ular, in non-linear ways, and is possibly synergistic (Langdon andAtkinson, 2005). Most observations suggest that ocean acidificat-ion reduces calcification rate independently of temperature andbleaching, and calcification reduces with increasing temperatures.Calcification, like many other biological processes, has a thermaloptimum which is exceeded during summer or extreme warmevents (Marshall and Clode, 2004). Thus, while some reports (seebelow) have shown that calcification has increased with tempera-ture in some areas, for corals the increase only occurs within thenarrow range up to the lethal limit for the organism, which maybe only a couple of degrees above their ‘normal’ exposure. Forexample, increasing calcification rates are reported with risingsea surface temperatures (SST) in Moorea (French Polynesia)where coral skeletal extension has been investigated for almost200 years; there skeletal extension increased by 4.5% for each1 �C increase in SST (Bessat and Buigues, 2001). Likewise, in Wes-tern Australia increases in calcification were reported, especiallyin high latitude locations, such that temperature appeared moreimportant than acidification (Cooper et al., 2012). However, in gen-eral, a further rise in SST is likely then to lead to increased stressand potential death of the coral, with obvious cessation of calcifi-cation. For example, corals within the Great Barrier Reef have de-clined by about 14.2% since as recently as 1990 (seen as reducedskeletal extension), which is unprecedented for the last 4 centuriesand is linearly correlated with SST increases (De’ath et al., 2009).



Fig. 3. Reefs of Chagos and Seychelles showing different trajectories of recovery. Top left: Dead table corals in Chagos in 2001, where mortality was very high especially inshallow water and in mid depths. Top right: A shallow Seychelles reef in 2004 where corals are still all dead: the reefs around several of these granitic island had shown norecovery and were disintegrating. Bottom: By that date, table corals were recovering throughout Chagos (photo February 2005).


Lastly, coral growth has decreased by almost 11%, associated withincreased ocean acidification, during the last >30 years within theCaribbean, despite high calcification rates observed in summermonths (Bak et al., 2009).

3. Interactive effects

Mediated by temperature and other environmental factors, theabove consequences of climate change may act independently butalso may interact with each other synergistically to amplify effects(Table 1). They may also interact equally with local stressors thatoccur in each different location (Table 2).

3.1. Acidification and coral bleaching

Ocean acidification has been identified as a potential trigger forcoral bleaching (Anthony et al., 2008; Thompson and Dolman,2010) and may also slow down post-bleaching recovery (Loganet al., 2010) and reduce calcification. Lowered pH could directly in-duce stress and make corals susceptible to bleaching by influencingseveral key physiological functions, such as photosynthesis, respi-ration, calcification rates, and the rate of nitrogen-fixation (Eakinet al., 2008; Crawley et al., 2010). Interaction with other stressfactors, such as temperature and disease, will produce muchlarger impacts. For example, following coral bleaching, calcificationrates can be reduced to 37% of mean annual calcification(Rodriguez-Román et al., 2006).

Ocean acidification can also affect different life-history pro-cesses within corals, including reproduction, larval development,settlement and post-settlement development (Kroeker et al.,


2010; Suwa et al., 2010; Albright and Langdon, 2011; Nakamuraet al., 2011). Similarly, early life-history stages (larvae and juve-niles) are thought to be more vulnerable to the effects of bleaching(Edmunds, 2007; Pörtner, 2008). This implies that both acidificat-ion and bleaching can negatively affect recruitment and the com-petitive ability of corals, potentially facilitating a shift in benthiccommunity structure toward a dominance of fleshy algae and few-er calcifying invertebrate forms (Perry and Hepburn, 2008; Nors-tröm et al., 2009). Impacts of acidification and high temperatureson reproductive and development processes also imply that evena non-lethal disturbance event may have long-term impacts, withre-establishment after a major disturbance potentially taking sev-eral years to decades to occur (Wild et al., 2011).

3.2. Climate change and coral diseases

It is sometimes unclear whether the causes of the increasingincidence of coral disease are because of an increased input ofpathogens (e.g. from increasing sewage) or to greater susceptibilitycaused by, for example, raised seawater temperature, or other fac-tors (Table 1). The fact that coral disease prevalence is associatedwith poor environmental conditions resulting from sedimentation,turbidity, nutrients, and algal overgrowth (Aeby and Santavy,2006; Bruckner and Bruckner, 1997; Bruno et al., 2003; Nugueset al., 2004; Voss and Richardson, 2006; Williams et al., 2010) sug-gests these local factors play a significant role. For example, in theLine Islands, proximity to habitation strongly controlled the abun-dance of bacteria and virus-like particles, and this was associatedwith lower coral cover and higher coral disease (Dinsdale et al.,2008).



Table 2Interactive effects of local stress factors on climate change factors and marine diseases.

Climate change factor Relationship with climate change factors Reference

Coral bleaching Sedimentation and turbidity: increase coral susceptibility tobleaching; decrease post bleaching recovery by smothering coralsand limiting settlement of coral larvae

(Fabricius, 2005; Carilli et al., 2009, 2010; Gilmour, 1999; Rogers,1990; Crabbe and Smith, 2005; Nugues and Roberts, 2003a;Nugues and Roberts, 2003b; Wolanski et al., 2004; Wooldridge,2009)

Nutrients: increase coral susceptibility to bleaching throughimbalance of nutrients in surrounding water that inducesbiochemical changes in cells; decreases post bleaching recoverythrough reduced reproductive output and by promoting growth ofcompetitive algae, coral disease and increase of bioerosion andbreakage

(Koop et al., 2001; Fabricius, 2005; Carilli et al., 2009; Nordemaret al., 2003; Nyström et al., 2008; Wiedenmann et al., 2012;Wooldridge, 2009; Wooldridge and Done, 2009)

Overfishing: resistance to bleaching may decrease due to reductionin biomass and functional diversity in reef fishes; post bleachingrecovery by promoting overdominance of fleshy macroalgae andsoft-bodied reef invertebrates, and loss of hard substrates due tointensified bioerosion and expansion of ‘urchin barrens’ associatedwith loss of keystone predators

(Bellwood et al., 2004; Tanner, 1995; Burkepile and Hay, 2008;Burkepile and Hay, 2010; Foster et al., 2008; McClanahan, 2000;Nyström, 2006; Nyström et al., 2008)

Destructive practices: physical destruction may result in partialmortality and weakening, increasing susceptibility to bleaching;reduces post bleaching recovery through reduced reproductivepotential, development and recruit survival

(Caras and Pasternak, 2009; Chabanet et al., 2005; Fox et al., 2005;Davenport and Davenport, 2006 and references therein; Henry andHart, 2005; McManus et al., 1997; Mumby, 1999; Rogers and Cox,2003; Ward, 1995; Zakai and Chadwick-Furman, 2002)

Sedimentation and turbidity: sedimentation stressed corals aremore likely to have reduced calcification

Ocean acidification andreduced carbonate andaragonite concentration

Nutrients: both positive and negative effects of elevated nutrientlevels are reported, however most studies suggest negative effectson calcification, skeletal extension and density and even directmortality; promotes overgrowth of fleshy macroalgae, thus,reduces competitive capacity of corals

(Fabricius et al., 2005; Gilmour, 1999; Nugues and Roberts, 2003a;Nugues and Roberts, 2003b; Rogers, 1983, 1990; Wolanski et al.,2004; Wooldridge, 2009; Wooldridge and Done, 2009)

(Anthony et al., 2011; Chauvin et al., 2011; Dunn et al., 2012;Holcomb et al., 2010; Langdon and Atkinson, 2005; Marubini andDavies, 1996; Renegar and Riegl, 2005)

Overfishing: promotes overgrowth of fleshy macroalgae andbioeroders that could induce stress and diseases and therebylowered calcification

(Bellwood et al., 2004; Jackson et al., 2001; Hughes, 1994; Mumbyet al., 2006)

Destructive practices: physically damaged corals have lowerskeletal growth

(Bak and Steward-Van Es, 1980; Henry and Hart, 2005; Meesterset al., 1997)

Coral diseases Sedimentation and turbidity: increase coral susceptibility todiseases; promote growth of disease causing micro-organisms anddisease inducing fleshy macroalgae

(Bruckner and Bruckner, 1997; Nugues and Roberts, 2003a, 2003b;Nugues et al., 2004; Voss and Richardson, 2006; Williams et al.,2010)

Nutrients: induce proliferation of disease causing microorganismsand bioeroders; intensify growth of fleshy macroalgae that inducecoral diseases

(Bruno et al., 2003; Dinsdale et al., 2008; Kuta and Richardson,2002; Kuntz et al., 2005; Nugues et al., 2004; Voss and Richardson,2006; Williams et al., 2010)

Overfishing: reduction of keystone predatory fishes promotespopulation explosion of prey organisms that become vulnerable tomarine diseases; reduction of herbivorous organisms promotesovergrowth of fleshy macroalgae that induce coral diseases

(Bellwood et al., 2004; Carpenter, 1990; Edmunds and Carpenter,2001; Hughes et al., 2003; McClanahan, 2000; McClanahan et al.,2002b; Jackson et al., 2001)

Destructive practices: corals suffering from mechanical damage aremore sensitive to diseases; damaged corals may have low capacityof post disturbance recovery due to reduced reproductive potentialas a result of trade-off between recovery and reproduction

(Aeby and Santavy, 2006; Henry and Hart, 2005; Page and Willis,2006; Oren et al., 2001; Rinkevich, 1996; Winkler et al., 2004)

Table 1Interactive effects among the main climate change factors of warming and ocean acidification and coral diseases.

Climate change factor Interactive effect References

Warming Induces coral bleaching; bleached corals are more sensitive todiseases and have lowered calcification rates; affects post-disturbance recovery through negative impacts on reproduction,development and recruitment

(Bourne et al., 2009; Crawley et al., 2010; Eakin et al., 2008;Edmunds, 2007; Mydlarz et al., 2009; Pörtner, 2008; Rodriguez-Román et al., 2006; Rodrigues and Grottoli, 2006; Ward et al.,2007)

Extreme temperatures will reduce calcification (Bak et al., 2009; De’ath et al., 2009; Marshall and Clode, 2004)Induces coral disease; disease stressed corals are more sensitive tobleaching and have reduced calcification rates; affects post-disturbance recovery through negative impacts on reproduction,development and recruitment and expending of resources tocombat infection

(Bruno et al., 2007; Gil-Agudelo et al., 2004; Kuta and Richardson,2002; Miller et al., 2009; Patterson et al., 2002; Rosenberg and Ben-Haim, 2002; Zvuloni et al., 2009; Harvell et al., 2007)

Ocean acidification andreduced carbonate andaragonite concentration

Results in reduced calcification; corals with reduced calcificationare more sensitive to bleaching and diseases; affects post-disturbance recovery through negative impacts on reproduction,development and recruitment

(Albright and Langdon, 2011; Anthony et al., 2008; Kroeker et al.,2010; Logan et al., 2010; Nakamura et al., 2011; Silverman et al.,2009; Suwa et al., 2010; Thompson and Dolman, 2010)

Results in dissolution of aragonite and calcite skeleton; weakenedskeleton is more sensitive to the impact of bioeroders and storms

(Carricart-Ganivet, 2007; Gardner et al., 2005; Kleypas et al., 2006;Sokolow, 2009; Tribollet et al., 2002; Sheppard et al., 2006).


Please cite this article in press as: Ateweberhan, M., et al. Climate change impacts on coral reefs: Synergies with local effects, possibilities for acclimation,and management implications. Mar. Pollut. Bull. (2013), http://dx.doi.org/10.1016/j.marpolbul.2013.06.011



Infectious diseases in reef-building corals have been a majorcause of the recent increase in global coral reef degradation (Harv-ell et al., 1999; Rosenberg and Ben-Haim, 2002; Bruno et al., 2007).Diseases have increased in number of occurrences and severity, inthe number of coral species infected, and the geographical extentof outbreaks (Harvell et al., 2004; Sutherland et al., 2004).

The first major noted coral disease impacts were in the Carib-bean, where the huge, shallow stands of Acropora palmata were al-most totally removed in most places by ‘white band disease’(Garrett and Ducklow, 1975; Bourne et al., 2009). Affected areassometimes covered a quarter or a third of the entire planar coralreef area (Sheppard et al., 1995; Sheppard and Rioja-Nieto, 2005).The ecological effect of this was great, because these corals pro-duced extensive ‘forests’ of 3-dimensional habitat which werestrongly wave resistant and provided the main ‘breakwater’ effectin this region.

The outbreak of many other coral diseases, such as black band(Kuta and Richardson, 2002; Zvuloni et al., 2009), white pox (Patt-erson et al., 2002), dark spots and yellow band (Gil-Agudelo et al.,2004), are positively associated with increased seawater tempera-ture (Fig. 4). It is thought that elevated seawater temperature mayaffect basic physiological responses of corals to these pathogens(Rosenberg and Ben-Haim, 2002), such that many opportunistand ‘normally’ harmless coral pathogens become virulent duringhigh SST periods. Such effects may be associated with a concomi-tant weakening of the coral host with warming waters (Harvellet al., 2007), making corals more susceptible to infection. Highersusceptibility may then increase the rate of disease-transmissionswithin and between coral communities, leading to increased epi-demic potential (Zvuloni et al., 2009). In this way a small increasein temperature might be enough to switch diseases to an epidemicphase in tropical waters (Lafferty and Holt, 2003; Zvuloni et al.,2009). Furthermore, warming may influence the seasonality of dis-eases, interfering with disease suppression which may otherwiseoccur in the cold season (Zvuloni et al., 2009) (Fig. 4). With the lat-ter hypothesis, interestingly, an elevation of cool winter tempera-tures could also play a role in disease dynamics.

As with bleaching, increased disease prevalence may be linkedto compromised immunity resulting from starvation conditions(Wild et al., 2011). Additionally, incidence of coral diseases may in-crease following coral bleaching events (Bruno et al., 2007; Harvellet al., 2007; Miller et al., 2009). If bleached corals have reducedimmunity they may simply become too weak to respond to infec-tion and injury (Bourne et al., 2009; Mydlarz et al., 2009). Coralsmay also lose other essential microbial components that interactwith coral hosts and zooxanthellae to form an integral system

Fig. 4. Linear relationship between number of black band disease (BBD) infectionsand seawater temperature. 21.6 �C is a temperature threshold for the appearance ofBBD infections. (Data from Zvuloni et al. (2009))


(holobiont) so that they lose the ability to fight invasion by otherpathogenic microbes (Mullen et al., 2004; Bourne et al., 2009). A re-cent modeling study found a temperature-dependent disease inci-dence for white band disease, the main coral disease in theCaribbean (Yee et al., 2011), which suggests that disease andbleaching may not be independent but rather responses to stressrelated to elevated SSTs and other interacting factors. These predic-tions contrast with expectations of increased disease infection fol-lowing bleaching and seem to support Rosenberg and Ben-Haim’s(2002) suggestion of pathogens as a cause of coral bleaching.

The effect of ocean acidification on coral diseases is relativelyless known but it is expected to play a major role in coral reef com-munity development by enhancing coral stress through interac-tions with other stress factors (Sokolow, 2009). Considering thehigh diversity of coral pathogens and their differing growth ratesin different pH conditions, varying outcomes of ocean acidificationand its interaction with other factors could be expected dependingon how much the growth of pathogenic bacteria is enhanced orprohibited by reduced pH (Williams et al., 2010). Similarly, effectof disease on calcification is less investigated, but corals stressedand weakened by disease could have reduced calcification rates.We hypothesise that disease dynamics are crucially influenced byclimate change, linked both to warming and pollution but couldalso interact with coral bleaching and acidification with synergisticinteractions resulting in amplified effects.

4. Impacts of climate change on soft corals

Octocorals are a major component of shallow reefs and, in theIndo-Pacific especially, most are zooxanthellate and so haveproved to be as susceptible as stony corals to warming and subse-quent mortality. They are not reef builders and so are not depen-dent upon aragonite saturation for calcification as are the moretropical hermatypic Scleractinia although basal sclerites in thegenus Sinularia can be cemented together (Schulunacher, 1997).They are thus more adaptable, diverse and widely distributed thanthe Scleractinia (Fabricius and Alderslade, 2001). Their abundancein the tropics varies and, like stony corals, zooxanthelate generaare generally restricted to warm waters . Most shallow-water,tropical zooxanthellate octocorals are bleaching-susceptible andsimilarly affected by rising SSTs (Fabricius and Klumpp, 1995; Fab-ricius and Alderslade, 2001; Celliers and Schleyer, 2002). Sub-lethal effects of bleaching mediated by climate change have alsobeen recorded and include impaired reproduction and recruitment(Michalek-Wagner and Willis, 2001). On the other hand, bleachingitself creates opportunities for fast-growing fugitive species to‘‘swarm’’ over newly-created open reef space providing a measureof reef stabilization. Phase shifts from scleractinian to soft coraldominance can thus occur. Reefs at Aldabra in the western IndianOcean, for example, underwent a partial replacement of hard coralswith soft corals following the 1998 bleaching event, the genus Rhy-tisma attaining a cover of 28% (Norström et al., 2009). A similar ef-fect involving Cespitularia has been observed on bleached reefs innorthern Mozambique (Schleyer, pers. obs). Once established, alle-lopathy assists in maintaining such persistence (Sammarco, 1996).This causes soft corals to become persistent along a climate gradi-ent (Hughes et al., 2012). In areas such as Chagos vast expanses ofshallow reefs were almost completely denuded of both soft andstony corals following the 1998 bleaching event. In some areaswhere soft corals had formerly dominated, and because soft coralsleft no skeletons, and perhaps because there were limited nutrientinputs and no fishing on these atolls, and hence abundant herbi-vores, there was no subsequent algal domination. Thus, these reefsatypically became devoid of significant attached macro-biota for aperiod of two to three years (Sheppard et al., 2008).




Because of their greater plasticity and wider distribution andrange shifts, soft corals are expected to continue thriving with cli-mate change, especially on high-latitude reefs. South African high-latitude reefs, which are well-endowed with soft corals, have beenmonitored since 1993 (Schleyer et al., 2008). About �6% reductionin 10 years was observed and correlated with increasing SST duringthe monitoring period. This reduction was accompanied by a slightincrease in hard coral cover (>1% in 10 years), possibly caused bygreater accretive competition associated with increasing SST(Schleyer and Cellieris, 2003). Recent monitoring also indicatedthat certain soft coral species that were previously prevalent fur-ther south have vanished from the area (Schleyer, pers. obs.).Pre- and post-1998 ENSO, comparison of principal octocorals col-lected in the Chagos Archipelago shared many common taxa(Schleyer and Benayahu, 2010), but a few discontinuities in theirdiversity revealed subtle changes in more persistent genera(Lobophytum, Sarcophyton); some fast-growing ‘fugitive’ genera(e.g. Cespitularia, Efflatounaria, Heteroxenia) disappeared after theENSO-related 1998 coral bleaching. Such transient fugitives mightthus be eliminated from soft coral communities on isolated reefsystems in the long term where there are repeat ENSO events.The appearance of Carijoa riseii, a species often considered foulingand invasive, was a further indication of reef degradation duringthe ENSO event in Chagos.

Some soft corals appear resilient to bleaching. The Caribbeangorgonian Plexaura kuna, for example, is relatively unaffected bybleaching and this may be true of other zooxanthellate gorgoniansin that region (Lasker, 2003). This may be because soft corals areless dependent on zooxanthellar photosynthesis and more on het-erotrophy (Fabricius and Klumpp, 1995) than Scleractinia. As withstony corals, some soft corals are more bleaching resistant thanothers.

Ocean acidification effects on soft corals are little studied, inpart because soft corals are not as reliant upon their sclerites forsupport, as are the Scleractinia. One experimental study that com-pared important biological traits of soft corals between acidic andnormal conditions found no statistically significant differences(Gabay et al., 2012).

Extreme weather events are a companion to climate change,affecting turbulence, turbidity and sedimentation (IPCC, 2007), fac-tors limiting the distribution of fragile zooxanthellate soft corals(Fabricius and De’ath, 2001; Fabricius and McCorry, 2006). Simul-taneously, increased turbulence and sediment movement couldwell promote the growth of slower-growing, persistent, more sed-iment-tolerant soft corals (Schleyer and Celliers, 2003). Overall,therefore, these important occupiers of reef space may exhibit ef-fects of climate change through changes in species compositionand population structure related to variations in susceptibility towarming and local stress factors.

5. Ocean acidification effects on non-calcifying macroalgae

Generally non-calcifying coral-reef autotrophs such as macroal-gae (Hofmann et al., 2010; Anthony et al., 2011) and adjacent hab-itats such as seagrass (Zimmerman, 2008; Hendriks et al., 2010) areexpected to respond positively to ocean acidification. This suggeststhat dominance by macroalgae could further intensify under oceanacidification scenarios. In model simulations that included temper-ature, bleaching, water chemistry and herbivory, Anthony et al.(2011) demonstrated that under IPCC’s fossil-fuel intensive sce-nario, severe warming and acidification alone could reduce resil-ience of reefs, even under high grazing and low nutrientconditions. Reefs already stressed from overfishing and nutrientpollution would become more susceptible to effects of ocean


acidification. This implies that comprehensive management thatreduces algal growth and promotes coral growth becomes critical.

Macroalgae are further believed to mediate microbe-inducedcoral mortality via the release of dissolved compounds (Smithet al., 2006; Rasher and Hay, 2010; Rasher et al., 2011). Coral stressincreases with proximity to algae, and presence of a positive feed-back loop is expected whereby compounds released by algae en-hance microbial activity on live coral surface, causing mortalityand further algal growth. In less fished reefs, intensive herbivoryon fleshy macroalgae could reduce disease prevalence by breakingthe feedback loop.

6. Climate change effects on reef fish

6.1. Direct effects of CO2 on coral reef fish

Direct effects of ocean acidification on coral reef fish are as-sumed to be negligible at present, as fishes have evolved efficientacid–base mechanisms to overcome increased metabolic CO2

(Melzner et al., 2009). Any direct effects of ocean acidification areexpected to be within internal calcifying elements, especially oto-liths (earbones), because they are aragonite structures. Althoughthere is still little work looking at the direct effects of CO2 on coralreef fishes, Munday et al. (2009a) found little change in embryonicduration, egg survival and size at hatching in eggs and larvae ofAmphiprion percula reared in different CO2 concentrations. Mundayet al. (2010, 2011) also found that the development of otolithswere relatively stable in high CO2 (1050 latm CO2) except in ex-treme CO2 treatments (1721 latm CO2). However, such CO2 valueswere more relevant within an extreme ocean acidification scenarioin a business-as-usual trajectory (encapsulating years 2100 and2200–2300) (Munday et al., 2011).

6.2. Ocean acidification and reef fish behavior

One major effect of increased CO2 on reef fishes will be changesin the success of olfactory cues, especially associated with preda-tor–prey responses. For example, planktivorous damselfish(Amphiprion percula) reared in high CO2 levels (1000 ppm CO2) be-came attracted to water containing the smell of a coral reef fishpredator, as they lost their ability to discriminate between waterpreviously holding predators and non-predators (Dixson et al.,2010; Munday et al., 2010; Ferrari et al., 2011). Similarly, highCO2 can also result in reduced coral-reef fish predator feedingactivity, because of reductions in the ability of these predators todetect coral-reef fish prey (Cripps et al., 2011). The underlyingmechanism for the reduction in olfactory response is poorly under-stood, but may be associated with changes in neurotransmitterfunctions (Nilsson et al., 2012) since these behavioral changescould be successfully reversed by treatment with an antagonistof the GABA-A receptor; thus high CO2 might effectively interferewith neurotransmitter function.

6.3. Habitat change and coral reef fish communities

Although effects of habitat disturbance are clearly significant instructuring benthic tropical communities (Hughes et al., 2003,2012; Pandolfi et al., 2005; Pandolfi and Jackson, 2006; Grahamet al., 2011), reef fish fauna can also exhibit dramatic changes instructure and loss of biodiversity in relation to declining coral cov-er and this has been widely studied (Jones and Syms, 1998; Halfordet al., 2004; Jones et al., 2004; Graham et al., 2006; Wilson et al.,2006; Feary, 2007; Munday et al., 2008; Pratchett et al., 2008;Hixon, 2011;). Known changes in coral reef fish communities inresponse to live coral loss (Jones et al., 2004; Garpe et al., 2006;




Graham et al., 2006, 2009) suggest a widespread reliance on under-lying reef habitat.

Tropical reef fishes have very different degrees of coral depen-dency, from extreme coral specialists (Munday et al., 1997) tothose with highly flexible resource requirements (Guzman andRobertson, 1989). Thus, responses to reductions in the structureof benthic reef communities may be species-specific (Jones andSyms, 1998; Wilson et al., 2006; Feary et al., 2007; Coker et al.,2012). Those which are obligate associates of coral at any stagein their life cycle are expected to decline most where there is re-duced live coral cover (Bell and Galzin, 1984; Williams, 1986;Pratchett et al., 2006; Feary et al., 2007; Bonin et al., 2009, 2011).This may lead to an increase in species that do not have strongassociations with coral, or which exploit habitats that may becomemore common as coral cover declines e.g. rubble, soft corals (Symsand Jones, 2000; Feary et al., 2007; Wilson et al., 2006, 2008a,2009, 2010). Where rapid growth of algae ensues (Hughes, 1994;McClanahan et al., 2002a; McManus and Polsenberg, 2004), abun-dances of herbivores, detritivores and invertivores may increase(Jones et al., 2004; Bellwood et al., 2006a; Wilson et al., 2009,2010).

6.4. Potential for synergistic effects of stressors on tropical fishcommunities

Although there is a wealth of information on the role of partic-ular stressors in structuring tropical fish communities, few, if anystressors occur in isolation. This has produced a range of workexamining the importance of multiplicative stresses, where thesum of two (or more) stresses exceeds the threshold that a singlestress would reach alone (McClanahan et al., 2002b). We can pre-dict from this work that the response of tropical fish communitiesto both abiotic (ocean acidification) and biotic stresses (habitatchange) will vary with other environmental factors, temperaturein particular, in non-linear ways, and is possibly synergistic (Mun-day et al., 2008; Munday et al., 2012). The dramatic effect that ele-vated CO2 can have on a wide range of behaviors and sensoryresponses of tropical reef fishes (Munday et al., 2011; Mundayet al., 2012), suggest that interactive effects will have a much moresubstantial impact on the demography of tropical fish communi-ties than has been observed to date (Munday et al., 2011). One ofthe most pervasive effects of such multiplicative stresses is ex-pected to be on the success and survival of new settlers. The supplyof larvae and differential early post-settlement mortality are keyprocesses structuring adult coral reef fish assemblages (Doherty& Fowler, 1994). Patterns established at settlement may be rein-forced or markedly altered by habitat availability, with both thephysical and biotic structure of coral habitat being vital in deter-mining settlement and survival of tropical fishes (McCormick andHoey, 2004; Feary et al., 2007).

There is increasing understanding of the importance of macro-algae in shaping settlement patterns and early post-settlementsurvival of coral reef fishes (Feary et al., 2007). Juveniles of somereef fish species display a close association with macroalgal standson coral reefs (Wilson et al., 2010). In particular, high densities ofjuvenile herbivorous fishes have been associated with macroalgalstands in the absence of predators (Hughes et al., 2007). It can thenbe predicted that the multiplicative effects of climate warming andelevated CO2 may result in a substantial shift in the functionalcomposition of tropical fish communities, with assemblage struc-ture becoming more likely dominated by fishes associated withmacroalgal resources.

Recent work has shown that the synergistic effects of elevatedCO2 and increasing water temperatures may have substantial neg-ative effects on the aerobic capacity of tropical fishes, with O2 con-sumption increasing in relation to increase in temperature and CO2


acidification (Munday et al., 2009b). Although sensitivity to ele-vated CO2 is expected to vary greatly among fish species, such re-sults show that with increasing oxygen limitation resulting fromrising water temperatures in tropical regions (Pörtner and Knust,2007; Nilsson et al., 2008), rising CO2 levels may compound thisproblem, and lead to considerable range contractions and popula-tion declines in tropical fish communities (Munday et al., 2012).

6.5. Can acclimation and adaptation mechanisms of coral-zooxanthellae catch up with the fast changing environmentalconditions?

Stressful conditions on corals associated with climate changeand localized stress factors are manifested as specific physiologicalresponses involving the coral host and Symbiodinium, or a combi-nation of both, collectively known as the ’holobiont’. A key ques-tion is whether this symbiotic association can adapt to changesin the environment, how this might happen, and whether it canhappen quickly enough to match demonstrated and predictedchanges in climate. Research on coral-zooxanthellae acclimation/adaptation to climate change has focused almost exclusively onthe impact of warming. Responses to ocean acidification and itsinteractive effects are less understood. With regards to bleaching,the questions asked include: how many host and Symbiodiniumassociations can acclimate? Which partner of the symbiosis willbe more effective in acclimating, or will it be a collective effort ofboth the coral host and Symbiodinium?

It has been recognized that the Symbiodinium partner is themain player in resistance mechanisms to thermal stress, however,any success of the holobiont will depend on its ability to adapteither with respect to its genetic make-up or association betweenhost and Symbiodinium over time, or acclimatise by physiologicalprocesses and/or shuffling between Symbiodinium clades and/ortypes (Bellantuono et al., 2012; Haslun et al., 2011; Wicks et al.,2010). Thus, it has become increasingly important to identify holo-biont systems that will or could have the ability to adapt (Laskerand Coffroth, 1999; Middlebrrok et al., 2008; Weis, 2010) and accli-matise (Gates and Edmunds, 1999). The response of holobionts toongoing global changes is largely dependent on whether coral-al-gal symbioses can adjust to decadal rather than millennial ratesof climate change (Hoegh-Guldberg et al., 2002). Climate changeassociated environmental change could lead to increase in the fre-quency of occurrence of different kinds of zooxanthellae and, at thesame time, to more diverse radiations of Symbiodinium types (Ba-ker et al., 2004). Responses to increasing episodic mass bleachingand mortality events however, indicate that such adaptation hasnot happened fast enough in the last 30 years to match the rateand frequency of warming events (Sheppard, 2003; Baskett et al.,2009). Considering the interactive effects of warming and oceanacidification and their subsequent interactions with local stressfactors, acclimation and adaptation mechanisms of the coral holo-biont will not be sufficient and fast enough for coping with the pro-jected environmental change.

7. Management implications

It is widely recognized that the coupling of strong natural dis-turbances with chronic anthropogenic disturbances has lead tothe degradation of many coral reefs globally (Hughes et al., 2003;Hoegh-Guldberg et al., 2007). In many coral reefs the benthic struc-ture is now characterized by low coral cover and diversity, anddominance of seaweeds and soft bodied invertebrates (McClana-han et al., 2002b; Hughes et al., 2003; Norström et al., 2009). Manycurrent management actions are intended to reduce local effectsrelated to resource extraction, pollution, and development




activities, but whether these localized actions are enough to pro-mote ecosystem resilience to global change such as effects of coralbleaching, acidification and diseases is less certain (Coelho andManfrino, 2007; Côté and Darling, 2010). However, given the com-pounding, often synergistic effects of the different impacts affect-ing reefs, alleviation of most of the local, direct stressors such asnutrient discharges and overfishing is imperative if sufficient over-all recovery of reefs is to be achieved. While in principle alleviationof a local stressor might be a more simply achievable goal thanalleviation of the global stressors, these have not been addressedfor several reasons. Although it may seem futile to a local managerto arrest problems of e.g. sewage, dredging or overfishing whenCO2 rise appears inexorable, in fact it may be as important in theshort term. In some areas, such as the uninhabited Chagos atolls,we can see that recovery can occur from high temperatures wherethere are no additional stressors, whereas in many Seychelles reefs,which suffer from additional stressors, there has been, in manycases, very low or no recovery from the collapse of 1998 (Grahamet al., 2008; Wilson et al., 2012) (Figs. 2 and 3b). In healthy reefsrecovery, at least in terms of coral cover, appears to take about adecade at best, in the absence of any local stressors, but in mostcases, it takes much longer or has not happened at all to date(Sheppard et al., 2012). The apparent inability of societies to re-dress the various local impacts in many areas (Riegl and Purkis,2012; Sheppard et al., 2010, 2012), means that much hope and reli-ance is being placed on the ability of corals and their symbionts toacclimate sufficiently quickly to climate change, but, as discussedabove, this hope might be misplaced.

7.1. Unrealistic global targets of carbon emission reduction

Despite the recognized need to reduce CO2 levels, achievementsin this respect remain elusive. Most countries have in principle en-dorsed the goal of limiting global temperatures rises below 2 �C(relative to pre-industrial time) with poignant exceptions fromthe most vulnerable small island state nations that have urgedlower levels (Meinshausen et al., 2009). This temperature rise(equivalent to a maximum of 450 ppm CO2) is considered as al-ready dangerous (Hansen et al., 2008). According to (Hansenet al., 2008), global SSTs higher than 1 �C relative to SSTs in 2000(equivalent to 1.7 �C relative to pre-industrial time) would causeirreversible ice sheet melting and biodiversity loss. Evidence frompaleoclimatic data indicates that average SST rise below 1 �C(350 ppm CO2e) is critical for sustaining population function andfor coral reefs to avoid extreme effects of ocean acidification andrepeat bleaching events (Hansen et al., 2008; Veron et al., 2009).The problem is magnified as there is a lag of several decades be-tween atmospheric CO2 and CO2 dissolved in the world’s oceans(Veron et al., 2009) and this lag creates a ‘legacy’ which is not evi-dent to most policy-makers.

To constrain average global temperature within 2 �C, industrialcountries have pledged to cut emissions to 30% below the 1990levels by 2020 and to 50–80% by 2050 (Rogelj et al., 2010). Rogeljet al. (2010) concluded that the 25–40% reductions by industria-lised countries by 2020 still has a high probability of exceedingthe recommended 2 �C levels. Even a 70% reduction in global greenhouse gas emissions by 2050 from the 2000 levels has a 25% prob-ability of exceeding the 2 �C limit. The Copenhagen negotiations in2009 targeted 30% reductions by 2020, which would also have ahigher than 50% probability of exceeding 2 �C (Rogelj et al.,2010). Some socio-economic evaluations have indicated that thecost of reducing emissions at the 2 �C level globally (450 CO2eppm) would be difficult to bear, so have pushed for stabilizationlevels of up to 650 ppm CO2e (Meinshausen et al., 2009). Such eco-nomic ‘compromises’ would be fatal to reefs as this is equivalent to3.68 �C rise in temperature.


Among calcifying coral-reef organisms, corals and calcifying al-gae will be the most affected by ocean acidification (Kroeker et al.,2010). Corals control the state of the reef through their influenceon important processes, such as productivity, bioerosion and recy-cling of essential elements, making them critical in their contribu-tion to reef functioning and services (Wild et al., 2011). Corallinealgae are also crucial, e.g. on reef crests, cementing calcified matterto form reef framework and as settlement substrata for planulae.These algae are especially sensitive to pH change, and increasedSSTs and ocean acidification may result in net carbonate dissolu-tion exceeding net calcification and ultimately in reduced growthand cover (Jokiel et al., 2008).

7.2. Fisheries closures

Fisheries closures are seen as an effective management tool asthey increase the biomass of herbivore fish populations that couldrestore ecosystem structure and function by reversing fleshy algaldominance (Mumby, 2006; Burkepile and Hay, 2008; Smith et al.,2009). However, increased herbivory associated with long-termclosures may also result in dominance of fast-growing coral taxathat are more susceptible to bleaching (Loya et al., 2001) so thatherbivory may not always confer resistance to the coral reef eco-system (Côté and Darling, 2010). Marine protected areas (MPAs)can even suffer higher bleaching impacts (McClanahan et al.,2001; Graham et al., 2008;Ateweberhan et al., 2011) and may havelower post-bleaching recovery (Graham et al., 2008). In the wes-tern Indian Ocean, the few sites where strong post-bleachingrecovery has been observed are those in locations remote from hu-man settlements with minimal or no fishing pressure and almostno pressure from other stress factors (Sheppard et al., 2008). Thereis also a possible relationship between species dominance and cor-al disease incidence associated with increased disease transmis-sion in high coral cover reefs (Bruno et al., 2007) as fast growingacroporids tend to be more susceptible to disease (Green andBruckner, 2000; Miller et al., 2009; Page and Willis, 2006; Patter-son et al., 2002; Williams et al., 2010). The reduced coral cover inshallow Caribbean reefs is associated with the demise of the twodominant Acropora sp. from white-band disease infection (Schutteet al., 2010). Whether effects of ocean acidification may be medi-ated by fisheries closures is less examined. However, consideringthat fast growing branching corals are more sensitive to the effectsof ocean acidification than massive and sub-massive ones, closuresmight even be more impacted by ocean acidification.

Fisheries closures by themselves may not be enough to promotecoral reef resilience to climate change induced disturbances. Whileoverfishing is a strongly ecosystem distorting activity, the capacityof the reef system to recover from disturbance is probably shapedat least as much by physiological responses (McClanahan et al.,2007a,b; Obura, 2005), by community structure (McClanahanet al., 2007c; Obura, 2001) and by disturbance history (Berkelmanset al., 2004; Brown et al., 2002; Maynard et al., 2008). Thus, inter-active processes including site-specific environmental resistancerelated to local and regional hydrodynamics (Maina et al., 2008;McClanahan et al., 2007a; Obura, 2005), resistance and toleranceto bleaching resulting from coral and zooxanthellae communitystructure (Baker et al., 2004; Loya et al., 2001; Marshall and Baird,2000; McClanahan et al., 2007c) and local stress factors, such asoverfishing and pollution (Bellwood et al., 2006b, 2004; Hugheset al., 2003; Lapointe et al., 2004; Mumby et al., 2006) all becomecritical. Of likely importance too, but less researched, are the dy-namic ecological linkages between reefs and adjacent ecosystemssuch as seagrass beds and mangrove forests, and interactions withother catchment areas and land use systems (Hughes et al., 2003;Mumby et al., 2004; Hoegh-Guldberg et al., 2007; Hughes et al.,2007; Mumby and Steneck, 2008).




7.3. Reef erosion

While many consequences remain unseen by policy-makers,one set of synergistic effects that can be seen by all is the increas-ing erosion of coral shores, a consequence of immense importanceto many countries and island communities. Sea level rise, anotherclimate change consequence but a complex issue not discussedhere, is one such concern, but from the point of view of coral reefsis probably not, by itself, of as much importance as are its interac-tive effects with other interrelated factors.

One consequence of reduction in calcification rates is the forma-tion of less dense skeletons in corals, making them more suscepti-ble to rapid physico-chemical and biological erosion (Tribolletet al., 2002; Carricart-Ganivet, 2007; Sokolow, 2009). Corals weak-ened by acidification and diseases are more vulnerable to bothbioerosion (Sokolow, 2009) and the increasing destructivenessassociated with tropical storms (Gardner et al., 2005). However,we can expect that variation in coral calcification will be relatedto species-specific physiological, accretion rates and calcificationthresholds (Doney et al., 2009). There will also be marked varia-tions in response associated with coral morphology and form(Guinotte and Fabry, 2008; Loya et al., 2001).

At a macro level, coral mortality and subsequent bioerosionmay have marked consequences to shorelines, with huge economicconsequences to those countries affected. In Chagos, where thereare no ‘local’ effects, the 1998 warming caused almost total re-moval of the shallowest ‘forest’ of 1.5 m tall Acropora palifera,which may be responsible for much of the increasingly observedshoreline erosion in those atolls (Sheppard, 2006). One study inthe Seychelles (Sheppard et al., 2005) showed that seaward zonesof fringing reefs – the natural breakwaters in these sites - were lar-gely killed by warming in 1998, resulting in large expanses of deadcoral skeletons which then commenced disintegrating; some sub-sequent modest recovery by new coral recruitment was then setback by further mortalities during minor bleaching events in2002 and 2004. From this, a model of wave energy reaching shore-lines protected by coral reefs was developed, which estimated thedrop in reef height as erosion progressed, leading to a consequent‘pseudo-sea level rise’ of increased depth between the remainingreef surface and water surface as coral colonies disintegrated(Sheppard et al., 2005). The increased wave energy reaching theshores resulting from this explained the observations of erosion;whereas energy reaching shores before mortality had averaged7% of the offshore wave energy, it had risen to about 12% in2004, threatening infrastructure on shore. It is predicted to riseto 18% of the offshore wave energy given continued disintegrationof the dead corals and poor recovery from new recruitment(Sheppard et al., 2005).

8. Conclusions

There is no single ‘most important’ stressor affecting coral reefsin the immediate term, rather different factors assume dominancein different areas and times. Continuing over-use or abuse of reefsystems has already led to the demise of an unacceptably high pro-portion of reefs in all ocean basins, and reduction of many of thelocal stressors in most reef areas is clearly urgently needed. Whileit is common to refer to a certain percentage of the world’s or re-gion’s reefs having suffered ‘degradation’ or similar, such state-ments, common in policy documents for example, appear togloss over the fact that many reefs are already dead and probablyan irrecoverable state. Thus, comments like a certain region has‘suffered a 30% decline in reefs’ may mean that 30% are dead andirrecoverable, not that conditions on all of them have declined by30%. The difference is critical. While CO2 rise is over-arching, it


may be of little consequence to one of the approximately 25% ofreefs that are already dead from other factors, the reefs havingfailed to ‘adapt’ to the stressors existing at those particular sites.

Without coordinated action at local, regional and global levelsto reduce local stress factors and combat climate change, there willbe continued decline of reefs, and of their ability to support humancommunities. Present rates of deterioration, if continued, meanthat most reefs will be lost as effective systems in a few decades.However, even if the local stressors can be averted, reduction ofCO2 levels remains of paramount importance for their long termsurvival. The current global targets of carbon emission reductions,including the targeted limit of a 2 �C rise (450 ppm), are unrealisticand definitely not enough for coral reefs to survive, and lower tar-gets should be pursued. Without such action then entirely new andradical conservation strategies may be required to protect remain-ing coral reefs (e.g. Rau et al., 2012), although in such a scenariosurvival of these ecosystems is likely to be confined to a few inten-sively-managed localities. A huge loss in biodiversity, and produc-tivity which is of value to people, is inevitable in such a high CO2

world.

Acknowledgements

This is a contribution arising out of two meetings organised bythe International Programme on the State of the Ocean (IPSO) andheld at Somerville College, University of Oxford. These were theInternational Earth System Expert Workshop on Ocean Stressesand Impacts held on the, 11th–13th April, 2011 and the Interna-tional Earth System Expert Workshop on Integrated Solutions forSynergistic Ocean Stresses and Impacts, 2nd–4th April, 2012. Thesemeetings were funded by the Kaplan Foundation and the PewCharitable Trusts.

References

Aeby, G.S., Santavy, D.L., 2006. Factors affecting susceptibility of the coralMontastraea faveolata to black-band disease. Mar. Ecol. Prog. Ser. 318, 103–110.

Albright, R., Langdon, C., 2011. Ocean acidification impacts multiple early lifehistory processes of the Caribbean coral Porites astreoides. Glob. Change Biol. 17,2478–2487.

Andersson, A.J., Mackenzie, F.T., 2011. Ocean acidification: setting the recordstraight. Biogeosciences Discussions 8, 6161–6190.

Anthony, K.R.N., Kline, D.I., Diaz-Pulido, G., Dove, S., Hoegh-Guldberg, O., 2008.Ocean acidification causes bleaching and productivity loss in coral reef builders.Proc. Nat. Acad. Sci. 105, 17442–17446.

Anthony, K.R.N., Maynard, J.A., Diaz-Pulido, G., et al., 2011. Ocean acidification andwarming will lower coral reef resilience. Glob. Change Biol. 17, 1798–1808.

Arndt, D.S., Baringer, M.O., Johnson, M.R., 2010. State of the climate in 2009. Bull.Am. Meteorol. Soc. 91, s1–s222.

Ateweberhan, M., McClanahan, T.R., 2010. Relationship between historical sea-surface temperature variability and climate change-induced coral mortality inthe western Indian Ocean. Mar. Pollut. Bull. 60, 964–970.

Ateweberhan, M., McClanahan, T.R., Graham, N.A.J., Sheppard, C.R.C., 2011. Episodicheterogeneous decline and recovery of coral cover in the Western Indian Ocean.Coral Reefs 30, 739–752.

Bak, R.P.M., Steward-Van Es, Y., 1980. Regeneration of superficial damage in thescleractinian corals Agaricia agaricites f. purpurea and Porites astreoides. Bull.Mar. Sci. 30, 883–887.

Bak, R.P.M., Nieuwland, G., Meesters, E.H., 2009. Coral growth rates revisited after31 years: what is causing lower extension rates in Acropora palmata? Bull. Mar.Sci. 84, 287–294.

Baker, A.C., Starger, C.J., McClanahan, T.R., Glynn, P.W., 2004. Corals’ adaptiveresponse to climate change. Nature 430, 741.

Baker, A.C., Glynn, P.W., Riegl, B., 2008. Climate change and coral reef bleaching: anecological assessment of the long-term impacts, recovery trends and futureoutlooks. Estuar. Coast. Shelf Sci. 80, 435–471.

Baskett, M.L., Gaines, S.D., Nisbet, R.M., 2009. Symbiont diversity may help coralreefs survive moderate climate change. Ecol. Appl. 19, 3–17.

Bell, J.D., Galzin, R., 1984. Influence of live coral cover on coral-reef fishcommunities. Mar. Ecol. Prog. Ser. 15, 265–274.

Bellantuono, A.J., Hoegh-Guldberg, O., Rodriguez-Lanetty, M., 2012. Resistance tothermal stress in corals without changes in symbiont composition. Proc. Roy.Soc. B: Biol. Sci. 279, 1100–1107.

Bellwood, D.R., Hughes, T.P., Folke, C., Nystrom, M., 2004. Confronting the coral reefcrisis. Nature 429, 827–832.


http://refhub.elsevier.com/S0025-326X(13)00302-0/h0010










































Bellwood, D.R., Hoey, A.S., Ackerman, J.L., Depczynski, M., 2006a. Coral bleaching,reef fish community phase shifts and the resilience of coral reefs. Glob. ChangeBiol. 12, 1587–1594.

Bellwood, D.R., Hughes, R.H., Hoey, A.S., 2006b. Sleeping functional group drivescoral-reef recovery. Curr. Biol. 16, 2434–2439.

Berkelmans, R., De’ath, G., Kininmonth, S., Skirving, W.J., 2004. A comparison of the1998 and 2002 coral bleaching events on the Great Barrier Reef: spatialcorrelation, patterns, and predictions. Coral Reefs 23, 74–83.

Bessat, F., Buigues, D., 2001. Two centuries of variation in coral growth in a massivePorites colony from Moorea (French Polynesia): a response of ocean-atmosphere variability from south central Pacific. Palaeogeogr. Palaeoclimatol.Palaeoecol. 175, 381–392.

Bindoff, N.L., Willebrand, J., Artale, V., et al., 2007. Observations: oceanic climatechange and sea level. In: Solomon, S., Qin, D., Manning, M., et al. (Eds.), ClimateChange 2007: The Physical Science Basis. Contribution of Working Group I.Cambridge University Press, Cambridge, pp. 385–428.

Bongiorni, L., Shafir, S., Angel, D., Rinkevich, B., 2003. Survival, growth and gonaddevelopment of two hermatypic corals subjected to in situ fish-farm nutrientenrichment. Mar. Ecol. Prog. Ser. 253, 137–144.

Bonin, M.C., Munday, P.L., McCormick, M.I., et al., 2009. Coral-dwelling fishesresistant to bleaching but not to mortality of host corals. Mar. Ecol. Prog. Ser.394, 215–222.

Bonin, M.C., Almany, G.R., Jones, G.P., 2011. Contrasting effects of habitat loss andfragmentation on coral-associated reef fishes. Ecology 92, 1503–1512.

Bourne, D.G., Garren, M., Work, T.M., et al., 2009. Microbial disease and the coralholobiont. Trends Microbiol. 17, 554–562.

Brown, B.E., 1997. Coral bleaching: causes and consequences. Coral Reefs 16, 129–138.

Brown, B.E., Dunne, R.P., Goodson, M.S., Douglas, A.E., 2002. Experience shapes thesusceptibility of a reef coral to bleaching. Coral Reefs 21, 119–126.

Bruckner, A.W., Bruckner, R.J., 1997. Outbreak of coral disease in Puerto Rico. CoralReefs 16, 260.

Bruno, J.F., Selig, E.R., 2007. Regional decline of coral cover in the Indo-Pacific:timing, extent and subregional comparisons. PLoS ONE 2, e711. http://dx.doi.org/10.1371/journal.pone.0000711.

Bruno, J.F., Petes, L.E., Drew Harvell, C., Hettinger, A., 2003. Nutrient enrichment canincrease the severity of coral diseases. Ecol. Lett. 6, 1056–1061.

Bruno, J.F., Selig, E.R., Casey, K.S., et al., 2007. Thermal stress and coral cover asdrivers of coral disease outbreaks. PLoS Biol. 5, e124. http://dx.doi.org/10.1371/journal.pbio.0050124.

Bryant, D., Burke, L., McManus, J.W., Spalding, M., 1998. Reefs at Risk: A Map-basedIndicator of Threats to the World’s Coral Reefs.. World Resources Institute,Washington, DC, USA, 56pp.

Burke, L., Reytar, K., Spalding, M., Perry, A., 2011. Reefs at Risk Revisited. WorldResources Institute, Washington, DC, 114pp.

Burkepile, D.E., Hay, M.E., 2008. Herbivore species richness and feedingcomplementarity affect community structure and function on a coral reef.Proc. Nat. Acad. Sci. 105, 16201.

Burkepile, D.E., Hay, M.E., 2010. Impact of herbivore identity on algal succession andcoral growth on a Caribbean reef. PLoS ONE 5, e8963. http://dx.doi.org/10.1371/journal.pone.0008963.

Caras, T., Pasternak, Z., 2009. Long-term environmental impact of coral mining atthe Wakatobi marine park, Indonesia. Ocean Coast. Manag. 52, 539–544.

Carilli, J.E., Norris, R.D., Black, B.A., et al., 2009. Local stressors reduce coral resilienceto bleaching. PLoS ONE 4, e6324. http://dx.doi.org/10.1371/journal.pone.0006324.

Carilli, J.E., Norris, R.D., Black, B., Walsh, S.M., McField, M., 2010. Century-scalerecords of coral growth rates indicate that local stressors reduce coral thermalstress tolerance threshold. Glob. Change Biol. 16, 1247–1257.

Carpenter, R.C., 1990. Mass mortality of Diadema antillarum. I. Long-term effects onsea urchin population-dynamics and coral reef algal communities. Mar. Biol.104, 67–77.

Carricart-Ganivet, J.P., 2007. Annual density banding in massive coral skeletons:result of growth strategies to inhabit reefs with high microborers’ activity? Mar.Biol. 153, 1–5.

Celliers, L., Schleyer, M.H., 2002. Coral bleaching on high-latitude marginal reefs atSodwana Bay, South Africa. Mar. Pollut. Bull. 44, 1380–1387.

Chabanet, P., Adjeroud, M., Andréfouët, S., et al., 2005. Human-induced physicaldisturbances and their indicators on coral reef habitats: a multi-scale approach.Aquat. Living Resour. 18, 215–230.

Chauvin, A., Denis, V., Cuet, P., 2011. Is the response of coral calcification toseawater acidification related to nutrient loading? Coral Reefs 30, 911–923.

Coelho, V.R., Manfrino, C., 2007. Coral community decline at a remote Caribbeanisland: marine no-take reserves are not enough. Aquat. Conserv.: Mar. Freshw.Ecosyst. 17, 666–685.

Coker, D.J., Pratchett, M.S., Munday, P.L., 2012. Influence of coral bleaching, coralmortality and conspecific aggression on movement and distribution of coral-dwelling fish. J. Exp. Mar. Biol. Ecol. 414, 62–68.

Cooper, T.F., O’Leary, R.A., Lough, J.M., 2012. Growth of Western Australian corals inthe anthropocene. Science 335, 593–596.

Côté, I.M., Darling, E.S., 2010. Rethinking ecosystem resilience in the face of climatechange. PLoS Biol. 8, e1000438. http://dx.doi.org/10.1371/journal.pbio.1000438.

Crabbe, M.J.C., Smith, D.J., 2005. Sediment impacts on growth rates of Acropora andPorites corals from fringing reefs of Sulawesi, Indonesia. Coral Reefs 24, 437–441.


Crawley, A., Kline, D.I., Dunn, S., et al., 2010. The effect of ocean acidification onsymbiont photorespiration and productivity in Acropora formosa. Glob. ChangeBiol. 16, 851–863.

Cripps, I.L., Munday, P.L., McCormick, M.I., 2011. Ocean acidification affects preydetection by a predatory reef fish. PLoS ONE 6, e22736. http://dx.doi.org/10.1371/journal.pone.0022736.

Davenport, J., Davenport, J.L., 2006. The impact of tourism and personal leisuretransport on coastal environments: a review. Estuar. Coast. Shelf Sci. 67, 280–292.

De’ath, G., Lough, J.M., Fabricius, K.E., 2009. Declining coral calcification on theGreat Barrier Reef. Science 323, 116–119.

Dinsdale, E.A., Pantos, O., Smriga, S., et al., 2008. Microbial ecology of four coralatolls in the Northern Line Islands. PLoS ONE 3, e1584. http://dx.doi.org/10.1371/journal.pone.0001584.

Dixson, D.L., Munday, P.L., Jones, G.P., 2010. Ocean acidification disrupts the innateability of fish to detect predator olfactory cues. Ecol. Lett. 13, 68–75.

Doherty, P. Fowler, T. 1994. An empirical test of recruitment limitation in a coralreef fish. Science, 935–939.

Doney, S.C., Fabry, V.J., Feely, R.A., Kleypas, J.A., 2009. Ocean acidification: the otherCO2 problem. Ann. Rev. Mar. Sci. 1, 169–192.

Donner, S.D., Skirving, W.J., Little, C.M., et al., 2005. Global assessment of coralbleaching and required rates of adaptation under climate change. Glob. ChangeBiol. 11, 1–15.

Dore, A.J., Vieno, M., Tang, Y.S., et al., 2007. Modelling the atmospheric transport anddeposition of sulphur and nitrogen over the United Kingdom and assessment ofthe influence of SO2 emissions from international shipping. Atmos. Environ. 41,2355–2367.

Dunn, J.G., Sammarco, P.W., LaFleur, G., 2012. Effects of phosphate on growth andskeletal density in the scleractinian coral Acropora muricata: a controlledexperimental approach. J. Exp. Mar. Biol. Ecol. 411, 34–44.

Eakin, C.M., Kleypas, J., Hoegh-Guldberg, O., 2008. Global climate change and coralreefs: rising temperatures, acidification and the need for resilient reefs. Science318, 1737–1742.

Edmunds, P.J., 2007. Evidence for a decadal-scale decline in the growth rates ofjuvenile scleractinian corals. Mar. Ecol. Prog. Ser. 341, 1–13.

Edmunds, P.J., Carpenter, R.C., 2001. Recovery of Diadema antillarum reducesmacroalgal cover and increases abundance of juvenile corals on a Caribbeanreef. Proc. Nat. Acad. Sci. U.S.A. 98, 5067–5071.

Fabricius, K.E., 2005. Effects of terrestrial runoff on the ecology of corals and coralreefs: review and synthesis. Mar. Pollut. Bull. 50, 125–146.

Fabricius, K.E., Alderslade, P., 2001. Soft Corals and Sea Fans: A ComprehensiveGuide to the Tropical Shallow Water Genera of the Central-west Pacific, theIndian Ocean and the Red Sea. Australian Institute of Marine Science, 264pp.

Fabricius, K.E., De’ath, G., 2001. Biodiversity on the Great Barrier Reef: Large-scalePatterns and Turbidity-Related Local Loss of Soft Coral Taxa. OceanographicProcesses of Coral Reefs: Physical and Biological Links in the Great Barrier Reef.CRC Press, London, pp. 127–144.

Fabricius, K.E., Klumpp, D.W., 1995. Widespread mixotrophy in reef-inhabiting softcorals: the influence of depth, and colony expansion and contraction onphotosynthesis. Mar. Ecol. Prog. Ser. 125, 195–204.

Fabricius, K.E., McCorry, D., 2006. Changes in octocoral communities and benthiccover along a water quality gradient in the reefs of Hong Kong. Mar. Pollut. Bull.52, 22–33.

Fabricius, K., De’ath, G., McCook, L., et al., 2005. Changes in algal, coral and fishassemblages along water quality gradients on the inshore Great Barrier Reef.Mar. Pollut. Bull. 51, 384–398.

Feary, D.A., 2007. The influence of resource specialization on coral reef fishesresilience to coral disturbance. Mar. Biol. 153, 153–161.

Feary, D.A., Almany, G.R., Jones, G.P., McCormick, M.I., 2007. Coral degradation andthe structure of tropical reef fish communities. Mar. Ecol. Prog. Ser. 333, 243–248.

Feary, D.A., Burt, J.A., Cavalcante, G.H., Bauman, A.G., 2012. Extreme physical factorsand the structure of Gulf fish and reef communities. In: Riegl, B., Purkis, S. (Eds.),Coral Reefs of the Gulf. Springer, pp. 163–170.

Feely, R.A., Sabine, C.L., Lee, K., et al., 2004. Impact of anthropogenic CO2 on theCaCO3 system in the oceans. Science 305, 362–366.

Feely, R.A., Doney, S.C., Cooley, S.R., 2009. Ocean acidification: present conditionsand future changes in a high-CO2 world. Oceanography 22, 36–47.

Ferrari, M.C.O., McCormick, M.I., Munday, P.L., et al., 2011. Putting prey andpredator into the CO2 equation – qualitative and quantitative effects of oceanacidification on predator–prey interactions. Ecol. Lett. 14, 1143–1148.

Foster, N.L., Box, S.J., Mumby, P.J., 2008. Competitive effects of macroalgae on thefecundity of the reef-building coral Montastraea annularis. Mar. Ecol. Prog. Ser.367, 143–152.

Fox, H.E., Mous, P., Pet, J., Muljadi, A., Caldwell, R.L., 2005. Experimental assessmentof coral reef rehabilitation following blast fishing. Conserv. Biol. 19, 98–107.

Gabay, Y., Benayahu, Y., Fine, M., 2012. Does elevated pCO2 affect reef octocorals?Ecol. Evol. 3, 465–473.

Gardner, T.A., Cote, I.M., Gill, J.A., et al., 2003. Long-term region-wide declines inCaribbean corals. Science 301, 958–960.

Gardner, T.A., Cote, I., Gill, J.A., et al., 2005. Hurricanes and Caribbean coral reefs:impacts, recovery patterns, and role in long-term decline. Ecology 86, 174–184.

Garpe, K.C., Yahya, S.A.S., Lindahl, U., Ohman, M.C., 2006. Long-term effects of the1998 coral bleaching event on reef fish assemblages. Mar. Ecol. Prog. Ser. 315,237–247.

Garrett, P., Ducklow, H., 1975. Coral diseases in Bermuda. Nature 253, 349–350.


































http://dx.doi.org/10.1371/journal.pone.0000711




http://dx.doi.org/10.1371/journal.pbio.0050124





































































































































Gates, R.D., Edmunds, P.J., 1999. The physiological mechanisms of acclimatization intropical reef corals. Am. Zool. 39, 30–43.

Gil-Agudelo, D.L., Smith, G.W., Garzón-Ferreira, J., et al., 2004. Dark spots diseaseand yellow band disease, two poorly known coral diseases with high incidencein Caribbean reefs. In: Rosenberg, E., Loya, Y. (Eds.), Coral Health and Disease.Springer, Berlin, pp. 337–350.

Gilmour, J., 1999. Experimental investigation into the effects of suspended sedimenton fertilisation, larval survival and settlement in a scleractinian coral. Mar. Biol.135, 451–462.

Glynn, P.W., 1996. Coral reef bleaching: facts, hypotheses and implications. Glob.Change Biol. 2, 495–509.

Graham, N.A.J., Wilson, S.K., Jennings, S., et al., 2006. Dynamic fragility of oceaniccoral reef ecosystems. Proc. Natl. Acad. Sci. U.S.A. 103, 8425–8429.

Graham, N.A.J., McClanahan, T.R., MacNeil, M.A., et al., 2008. Climate warming,marine protected areas and the ocean-scale integrity of coral reef ecosystems.PLoS ONE 3, e3039. http://dx.doi.org/10.1371/journal.pone.0003039.

Graham, N.A.J., Wilson, S.K., Pratchett, M.S., et al., 2009. Coral mortality versusstructural collapse as drivers of corallivorous butterflyfish decline. Biodivers.Conserv. 18, 3325–3336.

Graham, N.A.J., Nash, K.L., Kool, J.T., 2011. Coral reef recovery dynamics in achanging world. Coral Reefs 30, 283–294.

Green, E.P., Bruckner, A.W., 2000. The significance of coral disease epizootiology forcoral reef conservation. Biol. Conserv. 96, 347–361.

Guinotte, J.M., Fabry, V.J., 2008. Ocean acidification and its potential effects onmarine ecosystems. Ann. N. Y. Acad. Sci. 1134, 320–342.

Guzman, H.M., Robertson, D.R., 1989. Population and feeding responses of thecorallivorous pufferfish Arothron meleagris to coral mortality in the EasternPacific. Mar. Ecol. Prog. Ser. 55, 121–131.

Halford, A., Cheal, A.J., Ryan, C.D., Willims, D.M., 2004. Resilience to large-scaledisturbance in coral and fish assemblages on the Great Barrier Reef. Ecology 85,1892–1905.

Hansen, J., Sato, M., Ruedy, R., et al., 2007. Dangerous human-made interferencewith climate: a GIS model study. Atmos. Chem. Phys. 7, 2312.

Hansen, J., Sato, M., Kharecha, P., et al., 2008. Target atmospheric CO2: where shouldhumanity aim? Open Atmos. Sci. J. 2, 217–231.

Harvell, C.D., Kim, K., Burkholder, J.M., et al., 1999. Emerging marine diseases-climate links and anthropogenic factors. Science 285, 1505–1510.

Harvell, C.D., Mitchell, C.E., Ward, J.R., et al., 2002. Climate warming and disease riskfor terrestrial and marine biota. Science 296, 2158–2162.

Harvell, D., Aronson, R., Baron, N., et al., 2004. The rising tide of ocean diseases:unsolved problems and research priorities. Front. Ecol. Environ. 2, 375–382.

Harvell, D., Jordán-Dahlgren, E., Merkel, S., et al., 2007. Coral disease, environmentaldrivers, and the balance between coral and microbial associates. Oceanography20, 172–195.

Haslun, J.A., Strychar, K.B., Buck, G., Sammarco, P.W., 2011. Coral bleachingsusceptibility is decreased following short-term (1–3 year) prior temperatureexposure and evolutionary history. Journal of Marine Biology. http://dx.doi.org/10.1155/2011/406812 (Article ID 406812).

Hendriks, I.E., Duarte, C.M., Alvarez, M., 2010. Vulnerability of marine biodiversityto ocean acidification: a meta-analysis. Estuar. Coast. Shelf Sci. 86, 157–164.

Henry, L.A., Hart, M., 2005. Regeneration from injury and resource allocation insponges and corals: a review. Int. Rev. Hydrobiol. 90, 125–158.

Herfort, L., Thake, B., Taubner, I., 2008. Bicarbonate stimuation of cacification andphotosynthesis in two hermatypic corals. J. Phycol. 44, 91–98.

Hixon, M.A., 2011. 60 Years of coral reef fish ecology: past, present, future. Bull. Mar.Sci. 87, 727–765.

Hoegh-Guldberg, O., 1999. Climate change, coral bleaching and the future of theworld’s coral reefs. Mar. Freshw. Res. 50, 839–866.

Hoegh-Guldberg, O., Jones, R.J., Ward, S., Loh, W.K., 2002. Is coral bleaching reallyadaptive? Nature 415, 601–602.

Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., et al., 2007. Coral reefs under rapidclimate change and ocean acidification. Science 318, 1737–1742.

Hofmann, G.E., Barry, J.P., Edmunds, P.J., et al., 2010. The effect of ocean acidificationon calcifying organisms in marine ecosystems: an organism-to-ecosystemperspective. Annu. Rev. Ecol. Evol. Syst. 41, 127–147.

Holcomb, M., McCorkle, D.C., Cohen, A.L., 2010. Long-term effects of nutrient andCO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander,1786). J. Exp. Mar. Biol. Ecol. 386, 27–33.

Hughes, T.P., 1994. Catastrophes, phase shifts, and large-scale degradation of aCaribbean coral reef. Science 265, 1547–1551.

Hughes, T.P., Baird, A.H., Bellwood, D.R., et al., 2003. Climate change, humanimpacts, and the resilience of coral reefs. Science 301, 929–933.

Hughes, T.P., Rodrigues, M.J., Bellwood, D.R., et al., 2007. Phase shift, herbivory, andthe resilience of coral reefs to climate change. Curr. Biol. 17, 1–6.

Hughes, T.P., Baird, A.H., Dinsdale, E.A., et al., 2012. Assembly rules of reef corals areflexible along a steep climatic gradient. Curr. Biol. 22, 736–741.

IPCC, 2007. Impacts, Adaptation and Vulnerability, Cambridge Univ. Press, NewYork, 978pp.

Jackson, J.B.C., Kirby, M.X., Berger, W.H., et al., 2001. Historical overfishing and therecent collapse of coastal ecosystems. Science 293, 629–637.

Jokiel, P.L., Rodgers, K.S., Kuffner, I.B., et al., 2008. Ocean acidification and calcifyingreef organisms: a mesocosm investigation. Coral Reefs 27, 473–483.

Jones, G.P., Syms, C., 1998. Disturbance, habitat structure and the ecology of fisheson coral reefs. Aust. J. Ecol. 23, 287–297.


Jones, G.P., McCormick, M.I., Srinivasan, M., Eagle, J.V., 2004. Coral decline threatensfish biodiversity in marine reserves. Proc. Natl. Acad. Sci., U.S.A. 101, 8251–8258.

Jury, C.P., Whitehead, R.F., Szmant, A.M., 2010. Effects of variations in carbonatechemistry on the calcification rates of Madracis auretenra (=Madracis mirabilissensu Wells, 1973): bicarbonate concentrations best predict calcification rates.Glob. Change Biol. 16, 1632–1644.

Kleypas, J.A., Feely, R.A., Fabry, V.J., et al., 2006. Impacts of Ocean Acidification onCoral Reefs and Other Marine Calcifiers: A Guide for Future Research, Report of aWorkshopheld 18–20 April 2005, St. Petersburg, FL, Sponsored by NSF, NOAA,and the U.S. Geological Survey, 88pp.

Knowlton, N., Jackson, J.B.C., 2008. Shifting baselines, local impacts, and globalchange on coral reefs. PLoS Biol. 6, e54. http://dx.doi.org/10.1371/journal.pbio.0060054.

Koop, K., Booth, D., Broadbent, A.D., et al., 2001. ENCORE: the effect of nutrientenrichment on coral reefs. Synthesis of results and conclusions. Mar. Pollut.Bull. 42, 91–120.

Kroeker, K.J., Kordas, R.L., Crim, R.N., Singh, G.G., 2010. Meta-analysis revealsnegative yet variable effects of ocean acidification on marine organisms. Ecol.Lett. 13, 1419–1434.

Kuntz, N.M., Kline, D.I., Sandin, S.A., Rohwer, F., 2005. Pathologies and mortalityrates caused by organic carbon and nutrient stressors in three Caribbean coralspecies. Mar. Ecol. Prog. Ser. 294, 173–180.

Kuta, K., Richardson, L., 2002. Ecological aspects of black band disease of corals:relationships between disease incidence and environmental factors. Coral Reefs21, 393–398.

Lafferty, K.D., Holt, R.D., 2003. How should environmental stress affect thepopulation dynamics of disease? Ecol. Lett. 6, 654–664.

Langdon, C., Atkinson, M.J., 2005. Effect of elevated pCO2 on photosynthesis andcalcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J. Geophys. Res. 110, C09S07. http://dx.doi.org/10.1029/2004JC002576.

Lapointe, B.E., Barile, P.J., Yentsch, C.S., et al., 2004. The relative importance ofnutrient enrichment and herbivory on macroalgal communities near Norman’sPond Cay, Exumas Cays, Bahamas: a ‘‘natural’’ enrichment experiment. J. Exp.Mar. Biol. Ecol. 298, 275–301.

Lasker, H.R., 2003. Zooxanthella densities within a Caribbean octocoral duringbleaching and non-bleaching years. Coral Reefs 22, 23–26.

Lasker, H.R., Coffroth, M.A., 1999. Responses of clonal reef taxa to environmentalchange. Am. Zool. 39, 92–103.

Leon, L.M., Warnken, J., 2008. Copper and sewage inputs from recreational vessels atpopular anchor sites in a semi-enclosed Bay (Qld, Australia): estimates ofpotential annual loads. Mar. Pollut. Bull. 57, 838–845.

Lirman, D., Fong, P., 2007. Is proximity to land-based sources of coral stressors anappropriate measure of risk to coral reefs? An example from the Florida ReefTract. Mar. Pollut. Bull. 54, 779–791.

Logan, C.A., Donner, S.D., Eakin, C., Dunne, J.P., 2010. Modeling the effects of climatechange and acidification on global coral reefs. In: American Geophysical Union,Fall Meeting 2010, Abstract #OS13A-1217.

Loya, Y., Sakai, K., Yamazato, K., et al., 2001. Coral bleaching: the winners and thelosers. Ecol. Lett. 4, 122–131.

Maina, J., Venus, V., McClanahan, T.R., Ateweberhan, M., 2008. Modellingsusceptibility of coral reefs to environmental stress using remote sensing dataand GIS models. Ecol. Model. 212, 180–199.

Marshall, P.A., Baird, A.H., 2000. Bleaching of corals on the Great Barrier Reef:differential susceptibilities among taxa. Coral Reefs 19, 155–163.

Marshall, A.T., Clode, P., 2004. Calcification rate and the effect of temperature in azooxanthellate and an azooxanthellate scleractinian reef coral. Coral Reefs 23,218–224.

Marubini, F., Davies, P.S., 1996. Nitrate increases zooxanthellae population densityand reduces skeletogenesis in corals. Mar. Biol. 127, 319–328.

Maynard, J.A., Anthony, K.R.N., Marshall, P.A., Masiri, I., 2008. Major bleachingevents can lead to increased thermal tolerance in corals. Mar. Biol. 155, 173–182.

McClanahan, T.R., 2000. Recovery of the coral reef keystone predator, Balistapusundulatus, in East African marine parks. Biol. Conserv. 94, 191–198.

McClanahan, T.R., Muthiga, N.A., Mangi, S., 2001. Coral and algal changes after the1998 coral bleaching: interaction with reef management and herbivores onKenyan reefs. Coral Reefs 19, 380–391.

McClanahan, T.R., Maina, J., Pet-Soede, L., 2002a. Effects of the 1998 coral mortalityevent on Kenyan coral reefs and fisheries. Ambio 31, 543–550.

McClanahan, T., Polunin, N., Done, T., 2002b. Ecological states and the resilience ofcoral reefs. Conserv. Ecol. 6, 18(1–27). <http://www.ecologyandsociety.org/vol6/iss2/art18/print.pdf>.

McClanahan, T.R., Ateweberhan, M., Muhando, C., et al., 2007a. Effects of climateand seawater temperature variation on coral bleaching and mortality. Ecol.Monogr. 77, 503–525.

McClanahan, T.R., Ateweberhan, M., Sebastián, C.R., et al., 2007b. Predictability ofcoral bleaching from synoptic satellite and in situ temperature observations.Coral Reefs 26, 695–701.

McClanahan, T.R., Ateweberhan, M., Graham, N.A.J., et al., 2007c. Western IndianOcean coral communities, bleaching responses, and susceptibility to extinction.Mar. Ecol. Prog. Ser. 337, 1–13.

McClanahan, T.R., Donner, S.D., Maynard, J.A., et al., 2012. Prioritizing key resilienceindicators to support coral reef management in a changing climate. PLoS ONE 7,e42884. http://dx.doi.org/10.1371/journal.pone.0042884.














































http://dx.doi.org/10.1155/2011/406812

http://dx.doi.org/10.1155/2011/406812




























































http://dx.doi.org/10.1029/2004JC002576

http://dx.doi.org/10.1029/2004JC002576





































http://www.ecologyandsociety.org/vol6/iss2/art18/print.pdf

http://www.ecologyandsociety.org/vol6/iss2/art18/print.pdf













McCormick, M.I., Hoey, A.S., 2004. Larval growth history determines juvenilegrowth and survival in a tropical marine fish. Oikos 106, 225–242.

McManus, J.W., Polsenberg, J.F., 2004. Coral-algal phase shifts on coral reefs:ecological and environmental aspects. Prog. Oceanogr. 60, 263–279.

McManus, J.W., Reyes, J.R.B., Nañola, J.C.L., 1997. Effects of some destructive fishingmethods on coral cover and potential rates of recovery. Environ. Manage. 21,69–78.

Meehl, G.A., Stocker, T.F., Collins, W.D., et al., 2007. Chapter 10 supplementarymaterials: global climate projections. In: Solomon, S., Qin, D., Manning, M., et al.(Eds.), Climate Change 2007: The Physical Science Basis. Contribution ofWorking Group I to the Fourth Assessment Report of the IntergovernmentalPanel on Climate Change. Cambridge University Press, Cambridge, UnitedKingdom and New York, NY, USA, pp. SM10.1–SM10.8.

Meesters, E.H., Pauchli, W., Bak, R.P.M., 1997. Predicting regeneration of physicaldamage on a reef-building coral by regeneration capacity and lesion shape. Mar.Ecol. Prog. Ser. 146, 91–99.

Meinshausen, M., Meinshausen, N., Hare, W., et al., 2009. Greenhouse-gas emissiontargets for limiting global warming to 2 C. Nature 458, 1158–1162.

Melzner, F., Gutowska, M.A., Langenbuch, M., et al., 2009. Physiological basis forhigh CO2 tolerance in marine ectothermic animals: pre-adaptation throughlifestyle and ontogeny? Biogeosciences 6, 2313–2331.

Middlebrrok, R., Hoegh-Guldberg, O., Leggat, W., 2008. The effect of thermal historyon the susceptibility of reef-building corals to thermal stress. J. Exp. Biol. 211,1050–1056.

Michalek-Wagner, K., Willis, B.L., 2001. Impacts of bleaching on the soft coralLobophytum compactum. I. Fecundity, fertilization and offspring viability. CoralReefs 19, 231–239.

Miller, J., Muller, E., Rogers, C., et al., 2009. Coral disease following massivebleaching in 2005 causes 60% decline in coral cover on reefs in the US VirginIslands. Coral Reefs 28, 925–937.

Mullen, K.M., Peters, E.C., Harvell, C.D., 2004. Coral resistance to disease. In:Rosenberg, E. (Ed.), Coral Health and Disease. Springer-Verlag, Berlin, pp. 376–399.

Mumby, P.J., 1999. Bleaching and hurricane disturbances to populations of coralrecruits in Belize. Mar. Ecol. Prog. Ser. 190, 27–35.

Mumby, P.J., 2006. The impact of exploiting grazers (Scaridae) on the dynamics ofCaribbean coral reefs. Ecol. Appl. 16, 747–769.

Mumby, P.J., Steneck, R.S., 2008. Coral reef management and conservation in light ofrapidly evolving ecological paradigms. Trends Ecol. Evol. 23, 555–563.

Mumby, P.J., Edwards, A.J., Arias-González, J.E., et al., 2004. Mangroves enhance thebiomass of coral reef fish communities in the Caribbean. Nature 427, 533–536.

Mumby, P.J., Dahlgren, C.P., Harborne, A.R., et al., 2006. Fishing, trophic cascades,and the process of grazing on coral reefs. Science 311, 98–101.

Munday, P.L., Jones, G.P., Caley, M.J., 1997. Habitat specialisation and thedistribution and abundance of coral-dwelling gobies. Mar. Ecol. Prog. Ser. 152,227–239.

Munday, P.L., Jones, G.P., Pratchett, M.S., Williams, A.J., 2008. Climate change andthe future for coral reef fishes. Fish Fish. 9, 261–285.

Munday, P.L., Crawley, N.E., Nilsson, G.E., 2009a. Interacting effects of elevatedtemperature and ocean acidification on the aerobic performance of coral reeffishes. Mar. Ecol. Prog. Ser. 388, 235–242.

Munday, P.L., Donelson, J.M., Dixson, D.L., Endo, G.G.K., 2009b. Effects of oceanacidification on the early life history of a tropical marine fish. Proc. Roy. Soc. B:Biol. Sci. 276, 3275–3283.

Munday, P.L., Dixson, D.L., McCormick, M.I., et al., 2010. Replenishment of fishpopulations is threatened by ocean acidification. Proc. Natl. Acad. Sci. U.S.A. 107,12930–12934.

Munday, P.L., Gagliano, M., Donelson, J.M., et al., 2011. Ocean acidification does notaffect the early life history development of a tropical marine fish. Mar. Ecol.Prog. Ser. 423, 211–221.

Munday, P.L., McCormick, M.I., Nilsson, G.E., 2012. Impact of global warming andrising CO2 levels on coral reef fishes: what hope for the future? J. Exp. Biol. 215,3865–3873.

Mydlarz, L.D., Couch, C.S., Weil, E., et al., 2009. Immune defenses of healthy,bleached and diseased Montastraea faveolata during a natural bleaching event.Diseases Aquat. Organ. 87, 67–78.

Nakamura, M., Ohki, S., Suzuki, A., Sakai, K., 2011. Coral larvae under oceanacidification: survival, metabolism, and metamorphosis. PLoS ONE 6, e14521.http://dx.doi.org/10.1371/journal.pone.0014521.

Nilsson, G.E., Crawley, N., Lunde, I., Munday, P.L., 2008. Elevated temperaturereduces the respiratory scope of coral reef fishes. Glob. Change Biol. 15, 1405–1412.

Nilsson, G.E., Dixson, D.L., Domenici, P., et al., 2012. Near-future carbon dioxidelevels alter fish behaviour by interfering with neurotransmitter function. Nat.Clim. Change 2, 201–204.

Nordemar, I., Nystrom, M., Dizon, R., 2003. Effects of elevated seawater temperatureand nitrate enrichment on the branching coral Porites cylindrica in the absenceof particulate food. Mar. Biol. 142, 669–677.

Norström, A.V., Nyström, M., Lokrantz, J., Folke, C., 2009. Alternative states on coralreefs: beyond coral-macroalgal phase shifts. Mar. Ecol. Prog. Ser. 376, 295–306.

Nugues, M.M., Roberts, C.M., 2003a. Coral mortality and interaction with algae inrelation to sedimentation. Coral Reefs 22, 507–516.

Nugues, M.M., Roberts, C.M., 2003b. Partial mortality in massive reef corals as anindicator of sediment stress on coral reefs. Mar. Pollut. Bull. 46, 314–323.

Nugues, M.M., Smith, G.W., Hooidonk, R.J., et al., 2004. Algal contact as a trigger forcoral disease. Ecol. Lett. 7, 919–923.


Nyström, M., 2006. Redundancy and response diversity of functional Groups:implications for the resilience of coral reefs. Ambio 35, 30–35.

Nyström, M., Graham, N.A.J., Lokrantz, J., Norström, A.V., 2008. Capturing thecornerstones of coral reef resilience: linking theory to practice. Coral Reefs 27,795–809.

Obura, D.O., 2001. Can differential bleaching and mortality among coral speciesoffer useful indicators for assessment and management of reefs under stress?Bull. Mar. Sci. 69, 421–442.

Obura, D.O., 2005. Resilience and climate change: lessons from coral reefs andbleaching in Western Indian Ocean. Estuar. Coast. Shelf Sci. 63, 353–372.

Oren, U., Benayahu, Y., Lubinevsky, H., Loya, Y., 2001. Colony integration duringregeneration in the stony coral Favia favus. Ecology 82, 802–813.

Orr, J., Fabry, V.J., Olivier, A., et al., 2005. Anthropogenic ocean acidification over thetwenty-first century and its impact on calcifying organisms. Nature 437, 681–686.

Page, C., Willis, B., 2006. Distribution, host range and large-scale spatial variabilityin black band disease prevalence on the Great Barrier Reef, Australia. DiseasesAquat. Organ. 69, 41–51.

Pandolfi, J.M., Jackson, J.B.C., 2006. Ecological persistence interrupted in Caribbeancoral reefs. Ecol. Lett. 9, 818–826.

Pandolfi, J.M., Jackson, J.B.C., Baron, N., et al., 2005. Are U.S. coral reefs on theslippery slope to slime? Science 307, 1725–1726.

Patterson, K.L., Porter, J.W., Ritchie, K.B., et al., 2002. The etiology of white pox, alethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc. Natl. Acad.Sci., U.S.A. 99, 8725–8730.

Perry, C.T., Hepburn, L.J., 2008. Syn-depositional alteration of coral reef frameworkthrough bioerosion, encrustation and cementation: taphonomic signatures ofreef accretion and reef depositional events. Earth Sci. Rev. 86, 106–144.

Pörtner, H.O., 2008. Ecosystem effects of ocean acidification in times of oceanwarming: a physiologist’s view. Mar. Ecol. Prog. Ser. 373, 203–217.

Pörtner, H.O., Knust, R., 2007. Climate change affects marine fishes through oxygenlimitation of thermal tolerance. Science 315, 95–97.

Pratchett, M.S., Wilson, S.K., Baird, A.H., 2006. Declines in the abundance ofChaetodon butterflyfishes following extensive coral depletion. J. Fish Biol. 69, 1–12.

Pratchett, M.S., Munday, P.L., Wilson, S.K., et al., 2008. Effects of climate-inducedcoral bleaching on coral-reef fishes-ecological and economic consequences.Annu. Rev. Oceanogr. Mar. Biol. 46, 251–296.

Purkis, S.J., Riegl, B., 2005. Spatial and temporal dynamics of Arabian Gulf coralassemblages quantified from remote-sensing and in situ monitoring data. Mar.Ecol. Prog. Ser. 287, 99–113.

Rasher, D.B., Hay, M.E., 2010. Chemically rich seaweeds poison corals when notcontrolled by herbivores. Proc. Natl. Acad. Sci., U.S.A. 107, 9683–9688.

Rasher, D.B., Stout, E.P., Engel, S., et al., 2011. Macroalgal terpenes function asallelopathic agents against reef corals. Proc. Natl. Acad. Sci. 108, 17726–17731.

Rau, G.H., McLeod, E.L., Hoegh-Guldberg, O., 2012. The need for new oceanconservation strategies in a high carbon-dioxide world. Nat. Clim. Change.http://dx.doi.org/10.1038/NCLIMATE1555.

Rayner, N.A., Parker, D.E., Horon, E.B., et al., 2003. Global analyses of sea surfacetemperature, sea ice, and night marine air temperature since the latenineteenth century. J. Geophys. Res. 108, D14, 4407. http://dx.doi.org/10.1029/2002JD002670.

Reid, P.C., Beaugrand, G., 2012. Global synchrony of an accelerating rise in seasurface temperature. J. Mar. Biol. Assoc. U.K.. http://dx.doi.org/10.1017/S0025315412000549.

Renegar, D.A., Riegl, B.M., 2005. Effect of nutrient enrichment and elevated CO2

partial pressure on growth rate of Atlantic scleractinian coral Acroporacervicornis. Mar. Ecol. Prog. Ser. 293, 69–76.

Riegl, B.M., Purkis, S., 2012. Coral reefs of the Gulf: adaptation to climatic extremesin the world’s hottest sea. In: Riegl, B., Purkis, S. (Eds.), Coral Reefs of the Gulf.Springer, pp. 1–4.

Rinkevich, B., 1996. Do reproduction and regeneration in damaged corals competefor energy allocation? Mar. Ecol. Prog. Ser. 143, 297–302.

Rodrigues, L.J., Grottoli, A.G., 2006. Calcification rate and the stable carbon, oxygen,and nitrogen isotopes in the skeleton, host tissue, and zooxanthellae ofbleached and recovering Hawaiian corals. Geochim. Cosmochim. Acta 70,2781–2789.

Rodriguez-Román, A., Hernández-Pech, X., Thomé, P.E., et al., 2006. Photosynthesisand light utilization in the Caribbean coral Montastraea faveolata recoveringfrom a bleaching event. Limnol. Oceanogr. 51, 2702–2710.

Rogelj, J., Nabel, J., Chen, C., et al., 2010. Copenhagen Accord pledges are paltry.Nature 464, 1126–1128.

Rogers, C.S., 1983. Sub-lethal and lethal effects of sediments applied to commonCaribbean reef corals in the field. Mar. Pollut. Bull. 14, 378–382.

Rogers, C.S., 1990. Responses of coral reefs and reef organisms to sedimentation.Mar. Ecol. Prog. Ser. 62, 185–202.

Rogers, K.S., Cox, E.F., 2003. The effects of trampling on Hawaiian corals along agradient of human use. Biol. Conserv. 112, 383–389.

Rosenberg, E., Ben-Haim, Y., 2002. Microbial diseases of corals and global warming.Environ. Microbiol. 4, 318–326.

Sammarco, P.W., 1996. Comments on coral reef regeneration, bioerosion,biogeography, and chemical ecology: future directions. J. Exp. Mar. Biol. Ecol.200, 135–168.

Schleyer, M.H., Benayahu, Y., 2010. Pre-and post-1998 ENSO records of shallow-water octocorals (Alcyonacea) in the Chagos Archipelago. Mar. Pollut. Bull. 60,2197–2200.





































































































































http://dx.doi.org/10.1038/NCLIMATE1555

http://dx.doi.org/10.1029/2002JD002670

http://dx.doi.org/10.1029/2002JD002670

http://dx.doi.org/10.1017/S0025315412000549

http://dx.doi.org/10.1017/S0025315412000549


































Schleyer, M.H., Cellieris, L., 2003. Coral dominance at the reef-sediment interface inmarginal coral communities at Sodwana Bay, South Africa. Mar. Freshw. Res. 54,967–972.

Schleyer, M.H., Celliers, L., 2003. Coral dominance at the reef-sediment interface inmarginal coral communities at Sodwana Bay, South Africa. Mar. Freshw. Res. 54,967–972.

Schleyer, M.H., Kruger, A., Celliers, L., 2008. Long-term community changes on ahigh-latitude coral reef in the Greater St Lucia Wetland Park, South Africa. Mar.Pollut. Bull. 56, 493–502.

Schulunacher, H., 1997. Soft corals as reef builders. In: Proceedings of the 8thInternational Coral Reef Symposium, vol. 1, pp. 499–502.

Schutte, V., Selig, E.R., Bruno, J.F., 2010. Regional spatio-temporal trends inCaribbean coral reef benthic communities. Mar. Ecol. Prog. Ser. 402, 115–122.

Sheppard, C.R.C., 2003. Predicted recurrences of mass coral mortality in the IndianOcean. Nature 425, 294–297.

Sheppard, C.R.C., 2006. Longer term impacts of climate change. In: Cote, I., Reynolds,J. (Eds.), Coral Reef Conservation. Cambridge University Press, Cambridge, pp.264–290.

Sheppard, C.R.C., Loughland, R., 2002. Coral mortality and recovery in response toincreasing temperature in the southern Arabian Gulf. Aquat. Ecosyst. HealthManage. 5, 395–402.

Sheppard, C.R.C., Rioja-Nieto, R., 2005. Sea surface temperature 1871–2099 in 38cells in the Caribbean region. Mar. Environ. Res. 60, 389–396.

Sheppard, C.R.C., Matheson, K., Bythell, J.C., et al., 1995. Habitat mapping in theCaribbean for management and conservation: use and assessment of aerialphotography. Aquat. Conserv.: Mar. Freshw. Ecosyst. 5, 277–298.

Sheppard, C.R.C., Dixon, D.J., Gourlay, M., et al., 2005. Coral mortality increases waveenergy reaching shores protected by reef flats: examples from the Seychelles.Estuar. Coast. Shelf Sci. 64, 223–234.

Sheppard, C.R.C., Harris, A., Sheppard, A.L.S., 2008. Archipelago-wide coral recoverypatterns since 1998 in the Chagos Archipelago, central Indian Ocean. Mar. Ecol.Prog. Ser. 362, 109–117.

Sheppard, C., Al-Husiani, M., Al-Jamali, F., et al., 2010. The Gulf: a young sea indecline. Mar. Pollut. Bull. 60, 13–38.

Sheppard, C.R.C., Ateweberhan, M., Bowen, B.W., et al., 2012. Reefs and islands ofthe Chagos Archipelago, Indian Ocean: why it is the world’s largest no-takemarine protected area. Aquat. Conserv.: Mar. Freshw. Ecosyst. 22, 232–261.

Sheppard, C.R.C., et al., 2013. Coral reefs of the Chagos Archipelago, Indian Ocean.In: Sheppard, C.R.C. (Ed.), Coral Reefs of the UK Overseas Territories. Springer,241–252.

Silverman, J., Lazar, B., Cao, L., et al., 2009. Coral reefs may start dissolving whenatmospheric CO2 doubles. Geophys. Res. Lett. 36, L05606. http://dx.doi.org/10.1029/2008GL036282.

Smith, J.E., Shaw, M., Edwards, R.A., et al., 2006. Indirect effects of algae on coral:algae-mediated, microbe-induced coral mortality. Ecol. Lett. 9, 835–845.

Smith, J.E., Hunter, C.L., Smith, C.M., 2009. The effects of top–down versus bottom–up control on benthic coral reef community structure. Oecologia 163, 497–507.

Sokolow, S., 2009. Effects of a changing climate on the dynamics of coral infectiousdisease: a review of the evidence. Diseases Aquat. Organ. 87, 5–18.

Sutherland, K.P., Porter, J.W., Torres, C., 2004. Disease and immunity in Caribbeanand Indo-Pacific zooxanthellate corals. Mar. Ecol. Prog. Ser. 266, 273–302.

Suwa, R., Nakamura, M., Morita, M., et al., 2010. Effects of acidified seawater onearly life stages of scleractinian corals (Genus Acropora). Fish. Sci. 76, 93–99.

Syms, C., Jones, G.P., 2000. Disturbance, habitat structure, and the dynamics of acoral-reef fish community. Ecology 81, 2714–2729.

Szmant, A.M., 2002. Nutrient enrichment on coral reefs: is it a major cause of coralreef decline? Estuar. Coasts 25, 743–766.

Tanner, J.E., 1995. Competition between scleractinian corals and macroalgae: anexperimental investigation of coral growth, survival and reproduction. J. Exp.Mar. Biol. Ecol. 190, 151–168.

Thompson, A.A., Dolman, A.M., 2010. Coral bleaching: one disturbance too many fornear-shore reefs of the Great Barrier Reef. Coral Reefs 29, 637–648.

Trenberth, K.E., Jones, P.D., Ambenje, P., et al., 2007. Chapter 3 observations: surfaceand atmospheric climate change. In: Solomon, S., Qin, D., Manning, M., et al.(Eds.), Climate Change 2007: The Physical Science Basis. Contribution ofWorking Group I to the Fourth Assessment Report of the IntergovernmentalPanel on Climate Change. Cambridge University Press, Cambridge, UnitedKingdom and New York, NY, USA, pp. 236–336.

Tribollet, A., Decherf, G., Hutchings, P., Peyrot-Clausade, M., 2002. Large-scalespatial variability in bioerosion of experimental coral substrates on the GreatBarrier Reef (Australia): importance of microborers. Coral Reefs 21, 424–432.


Tripati, A., Allmon, W.D., Sampson, D.E., 2009. Possible evidence for a large decreasein seawater strontium/calcium ratios and strontium concentrations during theCenozoic. Earth Planet. Sci. Lett. 282, 122–130.

van Hooidonk, R., Maynard, J.A., Planes, S., 2013. Temporary refugia for coral reefs ina warming world. Nat. Clim. Change. http://dx.doi.org/10.1038/NCLIMATE1829.

Veron, J.E.N., Hoegh-Guldberg, O., Lenton, T.M., et al., 2009. The coral reef crisis: thecritical importance of <350 ppm CO2. Mar. Pollut. Bull. 58, 1428–1436.

Voss, J.D., Richardson, L.L., 2006. Nutrient enrichment enhances black band diseaseprogression in corals. Coral Reefs 25, 569–576.

Ward, S., 1995. The effect of damage on the growth, reproduction and storage oflipids in the scleractinian coral Pocillopora damicornis (Linnaeus). J. Exp. Mar.Biol. Ecol. 187, 193–206.

Ward, J.R., Kim, K., Harvell, C.D., 2007. Temperature affects coral disease resistanceand pathogen growth. Mar. Ecol. Prog. Ser. 329, 115–121.

Weis, V.M., 2010. The susceptibility and resilience of corals to thermal stress:adaptation, acclimatization or both. Mol. Ecol. 19, 1515–1517.

Wicks, L.C., Sampayo, E., Gardner, J.P.A., Davy, S.K., 2010. Local endemicity and highdiversity characterise high-latitude coral-Symbiodinium partnerships. CoralReefs 29, 989–1003.

Wiedenmann, J., D’Angelo, C., Smith, E.G., et al., 2012. Nutrient enrichment canincrease the susceptibility of reef corals to bleaching. Nat. Clim. Change 3, 160–164.

Wild, C., Hoegh-Guldberg, O., Naumann, M.S., et al., 2011. Climate change impedesscleractinian corals as primary reef ecosystem engineers. Mar. Freshw. Res. 62,205–215.

Wilkinson, C., Linden, O., Cesar, H., et al., 1999. Ecological and socioeconomicimpacts of 1998 coral mortality in the Indian Ocean: an ENSO impact and awarning of future change? Ambio 28, 188–196.

Williams, D.M., 1986. Temporal variation in the structure of reef slope fishcommunities (central Great Barrier Reef): short-term effects of Acanthasterplanci infestation. Mar. Ecol. Prog. Ser. 28, 157–164.

Williams, G.J., Aeby, G.S., Cowie, R.O.M., Davy, S.K., 2010. Predictive modelling ofcoral disease distribution within a reef system. PLoS ONE 5, e9264. http://dx.doi.org/10.1371/journal.pone.0009264.

Wilson, S.K., Graham, N.A.J., Pratchett, M.S., et al., 2006. Multiple disturbances andthe global degradation of coral reefs: are reef fishes at risk or resilient? Glob.Change Biol. 12, 2220–2234.

Wilson, S.K., Burgess, S.C., Cheal, A.J., et al., 2008a. Habitat utilization by coral reeffish: implications for specialists vs. generalists in a changing environment. J.Anim. Ecol. 77, 220–228.

Wilson, S.K., Dolman, A.M., Cheal, A.J., et al., 2009. Maintenance of fish diversity ondisturbed coral reefs. Coral Reefs 28, 3–14.

Wilson, S.K., Depczynski, M., Fisher, R., et al., 2010. Habitat associations of juvenilefish at Ningaloo Reef, Western Australia: the importance of coral and algae. PLoSONE 5, e15185. http://dx.doi.org/10.1371/journal.pone.0015185.

Wilson, S.K., Graham, N.A.J., Fisher, R., et al., 2012. Effect of macroalgal expansionand marine protected areas on coral recovery following a climatic disturbance.Conserv. Biol. 26, 995–1004.

Winkler, R., Antonius, A., Renegar, D.A., 2004. The skeleton eroding band disease oncoral reefs of Aqaba, Red Sea. Mar. Ecol. 25, 129–144.

Wolanski, E., Richmond, R.H., McCook, L., 2004. A model of the effects of land-based,human activities on the health of coral reefs in the Great Barrier Reef and inFouha Bay, Guam, Micronesia. J. Mar. Syst. 46, 133–144.

Wooldridge, S.A., 2009. Water quality and coral bleaching thresholds: formalisingthe linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar. Pollut.Bull. 58, 745–751.

Wooldridge, S.A., Done, T.J., 2009. Improved water quality can ameliorate effects ofclimate change on corals. Ecol. Appl. 19, 1492–1499.

Yee, S.H., Santavy, D.L., Barron, M.G., 2011. Assessing the effects of disease andbleaching on Florida Keys corals by fitting population models to data. Ecol.Model. 222, 1323–1332.

Zakai, D., Chadwick-Furman, N.E., 2002. Impacts of intensive recreational diving onreef corals at Eilat, northern Red Sea. Biol. Conserv. 105, 179–187.

Zimmerman, R.C., 2008. Seagrass response to Ocean Acidification: From IndividualLeaves to Populations. American Geophysical Union, 2000 Florida Ave., N. W.Washington, DC 20009, USA.

Zvuloni, A., Artzy-Randrup, Y., Stone, L., et al., 2009. Spatio-temporal transmissionpatterns of black-band disease in a coral community. PLoS ONE 4, e4993. http://dx.doi.org/10.1371/journal.pone.0004993.





































http://dx.doi.org/10.1029/2008GL036282

http://dx.doi.org/10.1029/2008GL036282
































http://dx.doi.org/10.1038/NCLIMATE1829




























































Climate change impacts on coral reefs: Synergies with local effects, possibilities for acclimation,...

Documents

Transcript of Climate change impacts on coral reefs: Synergies with local effects, possibilities for acclimation,...