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F I S H and F I S H E R I E S , 2008, 9, 261–285

Climate change and the future for reef fishes

Philip L Munday1,2, Geoffrey P Jones1,2, Morgan S Pratchett1 & Ashley J Williams3

1ARC Centre of Excellence for Studies, James Cook University, Townsville, Qld 4811, Australia; 2School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia; 3Fishing and Research Centre, School of and Environmental Sciences, James Cook University, Townsville, Qld 4811, Australia

Abstract Correspondence: Climate change will impact coral-reef fishes through effects on individual perfor- Philip L Munday, ARC CentreofExcellencefor mance, trophic linkages, recruitment dynamics, population connectivity and other Coral Reef Studies, and processes. The most immediate impacts will be a loss of diversity and School of Marine and changes to fish community composition as a result of . Coral- Tropical Biology, dependent fishes suffer the most rapid population declines as coral is lost; however, JamesCookUniversity, many other will exhibit long-term declines due to loss of settlement Townsville, Qld 4811, Australia and erosion of habitat structural complexity. Increased temperature will affect Tel/Fax: +61 7 the physiological performance and behaviour of coral reef fishes, especially during 47815341 their early history. Small temperature increases might favour larval development, E-mail: philip. but this could be counteracted by negative effects on adult reproduction. Already [email protected] variable recruitment will become even more unpredictable. This will make optimal Received 27 Nov 2007 harvest strategies for coral reef fisheries more difficult to determine and populations Accepted 28 Feb 2008 more susceptible to overfishing. A substantial number of species could exhibit range shifts, with implications for risk of small-range species near the margins of reef development. There are critical gaps in our knowledge of how climate change will affect tropical marine fishes. Predictions are often based on temperate examples, which may be inappropriate for tropical species. Improved projections of how ocean currents and primary will change are needed to better predict how reef fish population dynamics and connectivity patterns will change. Finally, the potential for to climate change needs more attention. Many coral reef fishes have geographical ranges spanning a wide temperature gradient and some have short generation times. These characteristics are conducive to acclimation or local adaptation to climate change and provide hope that the more resilient species will persist if immediate action is taken to stabilize Earth’s climate.

Keywords Climate change adaptation, community structure, global warming, habitat loss, population dynamics, range shifts

Introduction 262 Sensitivity of reef fishes to predicted climate changes 263 surface temperature 264 Ocean acidification 267 Ocean circulation 268 Cyclones and extreme weather 268 Sea level rise 269

Ó 2008 The Authors Journal compilation Ó 2008 Blackwell Publishing Ltd 261 Climate change and coral reef fishes P L Munday et al.

Impact of climate change on populations and communities 269 Life-history traits 269 Recruitment and population dynamics 269 Population connectivity 270 Habitat loss and community structure 271 Geographic ranges 273 Interactions with other stessors 274 Adaptation to climate change 275 Coral reef fisheries 275 The future 276 Future ecology 277 Future 277 Future management 278 Future science 278 Acknowledgements 279 References 279

compromise the reef-building capacity of and Introduction could see some reefs enter a state of net erosion by the Climate change is expected to have serious conse- end of this century (Guinotte et al. 2003). Coral reefs quences for Earth’s ecological systems, resulting in an are among the most diverse on Earth and overall loss of diversity, disruptions to ecosystem continued loss of coral cover and the erosion of the processes and a reduction in the ecological goods and complex habitat structure associated with healthy services provided to societies (Thomas et al. coral reefs is expected to have significant conse- 2004; Lovejoy and Hannah 2005). Shifts in quences for a vast number of reef-associated species, and distributions, changes to population although these consequences are only just beginning abundances, adjustments to the timing of seasonal to be understood (Munday and Holbrook 2006; activities, increased prevalence of disease and the Hoegh-Guldberg et al. 2007; Munday et al. 2007; spread of have already been linked to Pratchett et al. 2008, in press). Changes to ocean climate change (Harvell et al. 2002; Walther et al. temperature, pH, ocean currents and extreme weath- 2002; Parmesan and Yohe 2003; Root et al. 2003; er events that will accompany climate change will Parmesan 2006). Impacts such as these are expected have additional impacts on reef-associated species to become more pervasive as the climate changes through effects on individual performance, trophic rapidly over the next 50–100 (Intergovern- linkages, recruitment dynamics, connectivity mental Panel on Climate Change (IPCC) 2007a). between populations and other key ecosystem pro- Coral reefs are particularly susceptible to rapid cesses. climate change because exposure to maximum ocean Over 4000 species of fishes are associated temperatures just a few degrees above the long-term with coral reefs (Lieske and Myers 1994; Allen 2007), average at any location can cause corals to become yet how they will be affected by climate change has stressed, bleach and die (Hoegh-Guldberg 1999). received remarkably little attention (Roessig et al. Repeated episodes of mass coral bleaching since 1970 2004; Harley et al. 2006). The impacts of climate have already caused a decline in coral cover at a change will vary among life stages, with the larval global scale (Wilkinson 2002; Gardner et al. 2003; and reproductive stage expected to be most vulner- Hughes et al. 2003) and this trend is expected to able. Most coral reef fishes have a life cycle that continue as ocean temperatures increase further over includes a pelagic larval stage lasting for a few weeks the coming decades (Hoegh-Guldberg 1999; Donner to months (Leis 1991). When they are sufficiently et al. 2005). Coral reefs are also threatened by ocean well developed, the larvae settle to the reef and acidification, which reduces the ability of scleractin- become part of the reef-based population. Patterns of ian corals to form carbonate (Feely et al. larval survival and dispersal play a key role in the 2004; Kleypas et al. 2006). Ocean acidification will dynamics of reef fish populations (Doherty 1991;

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Caley et al. 1996) and the ecological and genetic climate change on populations and communities of connectivity between populations (Sale 1991; Cowen coral reef fishes could have far-reaching ramifica- 2002). Larval reef fishes are highly sensitive to tion for coral reef ecosystems and for the human environmental conditions (Leis and McCormick societies that depend on them. 2002) and any effects of climate change on the In this review, we assess and predict the likely number of larvae produced, or their growth, survival impacts of climate change on populations and com- and dispersal patterns, could have significant munities of coral fishes. We first examine the sensi- consequences for adult populations. tivity of marine fishes to changes in the physical Changes to the composition and structure of coral environment and consider how predicted changes in reef are expected to have further significant the ocean climate will affect the growth, survival, consequences for fish populations and communities behaviour and reproductive success of individuals. (Pratchett et al. 2008). The loss of coral from We then consider how these effects could influence bleaching has already caused significant declines in life histories, population dynamics, community struc- the diversity and abundances of reef fishes in some ture and the geographical distributions of coral reef places (Jones et al. 2004; Wilson et al. 2006) and this fishes. We also explore the potential for adaptation of effect will be magnified if the structural complexity of coral reef fishes to rapid climate change. Finally, we reefs declines following bleaching events (Graham examine the potential consequences for coral reef et al. 2006). The effects of coral bleaching and ocean fisheries and consider how climate change might acidification are additional to existing disturbances interact with other anthropogenic stresses to affect that kill live coral, such as outbreaks of crown of reef fish populations. thorns starfish or pollution from terrestrial run-off. There are critical gaps in our understanding of We expect that the on-going degradation of coral reef how the tropical ocean will change over the coming habitat as a result of climate change will result in century, especially at regional and local scales. impoverished reef fish communities. There are even larger gaps in our understanding of Changes to fish populations and communities how rapid changes in the ocean climate will affect could have important feedbacks to other parts of the reef fishes at the individual, population and com- reef ecosystem and to human societies. have munity levels. These knowledge gaps introduce a a significant presence in all major feeding groups high level of uncertainty to many of our assess- and are important for energy transfer throughout ments. Nevertheless, our synthesis identifies areas of the reef system (Depczynski et al. 2007). They are major concern regarding the possible effects of the dominant large predators on reefs and their climate change on coral reef fishes and highlights presence influences the community structure and critical issues for future research. of smaller species (Hixon 1991; Jones 1991; Almany and Webster 2004). Some reef Sensitivity of reef fishes to predicted fishes, such as grazing herbivorous fishes have key climate changes functional roles, preventing the growth of macroal- gae that might otherwise smother corals (Steneck The ocean and the act as a linked 1988; McCook et al. 2001; Bellwood et al. 2004; system, with changes in one part of the system Hughes et al. 2007). Other species facilitate the having feedback to the other. Both the atmosphere settlement of corals by removing sediment and fine and the are getting warmer due to the from the substratum (Steneck 1997). Reef enhanced greenhouse effect caused by the accumu- fishes also have high social and economic value. lation of dioxide and other greenhouse gases They are the basis for subsistence and artisanal in the atmosphere (IPCC 2007b). The ocean is an lifestyles of coastal communities in many tropical enormous reservoir of heat, with the top few metres countries and they also support significant com- storing a similar amount of heat as the entire mercial fisheries (Russ 1991; Polunin and Roberts atmosphere (Houghton 2004). Additional heat 1996; McClanahan et al. 2005; Sadovy 2005). contained within the oceans is redistributed around Coral reefs also generate significant tourism revenue the globe via major circulation patterns. Changes in for some countries (Cesar et al. 2003). For example, ocean temperature in turn influence wind stress, Australia’s is responsible for over which is a major driver of ocean circulation. Ocean $5 billion per annum in tourism revenue (Access temperature also influences the evaporation of Economics 2007). Clearly, significant impacts of vapour into the atmosphere, with consequences

Ó 2008 The Authors Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 261–285 263 Climate change and coral reef fishes P L Munday et al.

for rainfall patterns (Houghton 2004). The oceans global average surface temperature is projected to absorb from the atmosphere and increase 1.1–6.4 °C by 2100, with best estimates nearly half the additional carbon dioxide produced placing the range between 1.8 and 4.0 °C (IPCC by human societies over the past 250 years is 2007b). Average tropical sea surface temperature estimated to have been taken up by the ocean (SST) is expected to increase by 50–80% of the (Royal Society 2005). This additional dissolved average atmospheric change over the same period carbon dioxide changes the chemistry of the oceans (Lough 2007). Therefore, average sea temperatures and decreases their pH (Caldiera and Wickett in the vicinity of coral reefs will probably increase 2003). by several degrees Celsius over the course of this The atmosphere and the ocean will continue to century (Guinotte et al. 2003), although there will warm over the next 50–100 years, sea level will rise be considerable regional and local variations. For due to thermal expansion of water and melting of example, it appears that the equatorial western , ocean pH will decline as more carbon Pacific, which is already one of the warmest parts of dioxide is absorbed, and circulation patterns could the Indo-Pacific, may warm more slowly than other change at local, regional and global scales (Bindoff tropical (Kleypas et al. 2008). There is no et al. 2007). In addition, cyclones are expected to consensus on how El Nin˜o Southern Oscillation will become stronger and extreme flood and drought change, but these events will continue to be a events more frequent (IPCC 2007b). All of these significant source of periodic variability in sea changes will have consequences for fishes living on surface temperature in the Pacific region (Lough coral reefs (Fig. 1), although some impacts will be 2007). more pronounced and have greater certainty than Unlike corals, most reef fishes are probably not others (Table 1). living very close to their lethal thermal limits (Mora and Ospı´na 2001). Nevertheless, increased sea temperatures could have significant effects on indi- Sea surface temperature vidual performance. Fishes are ectotherms and Water has a higher heat capacity than air, which temperature changes of a few degrees Celsius can means that ocean temperature increases more influence their physiological condition, developmen- slowly than the atmosphere for the same heat tal rate, growth rate, swimming ability, reproduc- input. Depending on future emission scenarios, tive performance and behaviour (Wood and

Figure 1 The influence of climate change on fish populations and communities through interactions between the physical environment, metabolic and behavioural responses of larvae and adults, energy transfer between trophic levels, and the effect of habitat structure on ecological interactions. Adapted from Munday et al. (2007).

Ó 2008 The Authors 264 Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 261–285 ora compilation Journal Ó Table 1 Predicted impacts of climate change on populations and communities of coral reef fishes and the level of certainty associated with these predictions. 08TeAuthors The 2008

Impact Drivers Details Certainty

Reduction in local diversity and Loss of coral cover and erosion of reef Loss of coral-dependent species and declines in abundance of species that prefer to settle High Ó

08BakelPbihn t,FISHadFISHERIES, S E I R E H S I F and H S I F Ltd, Publishing Blackwell 2008 changes to community composition structural complexity near live coral. Further declines in abundances of a broad suite of species as habitat structure erodes. Generalist planktivores, small and rubble dwellers will tend to be favoured. Geographic range shifts Increased ocean temperature Species distributions will shift to match the position of preferred temperature gradients. High Some low-latitude species will expand ranges towards higher latitudes. Some high- latitude species will contract ranges towards margins of reef development. Increased extinction risk of small range, coral-dependent species near margins of reef development. Reduced pelagic duration Increased ocean temperature Small increases in water temperature will tend to accelerate larval development and High competency to settle. Larger increases in temperature may be detrimental. Life-history modification Increased ocean temperature On average, populations will have individuals that tend to be shorter lived, reach shorter Moderate–high maximum sizes and mature earlier. Shift of breeding season Increased ocean temperature Breeding will commence earlier. Populations may breed longer at higher latitudes. Moderate Bimodal breeding seasons could develop at low latitudes. Reproductive decline Increased ocean temperature Low-latitude species and species that do not shift the timing of breeding will experience Moderate reduced reproductive performance. A mismatch between timing of reproduction and

optimum conditions for larvae could develop. fishes reef coral and change Climate More extremes in recruitment Increased ocean temperature and/or Shorter pelagic durations and faster larval growth will tend to increase survival during the Moderate 9

6–8 265 261–285 , changes in ocean circulation and productivity larval stage. However, higher metabolic rates will increase the risk of starvation where food supply is patchy or unpredictable. Highly variable and unpredictable – some locations may tend to have better recruitment and others poorer recruitment. Reduced productivity Increased ocean temperature and/or Less enrichment due to increased stratification of surface in combination Low changes in ocean circulation with higher metabolic demands of consumers could reduce productivity at higher trophic levels. Planktonic food chains will be less productive at higher temperatures. Highly variable and unpredictable - productivity may increase at some locations. Reduced connectivity Habitat loss and increased Increased habitat fragmentation and smaller population sizes will reduce population Low ocean temperature connectivity. Reduced pelagic larval durations and earlier reef-seeking behaviour might tend to reduce the average scale of larval dispersal. Reduced population Increased ocean Strong selection favouring temperature-tolerant genotypes and reduced populations sizes Low temperature and habitat loss from habitat degradation will reduce local genetic diversity. al. et Munday L P

Reduced performance Ocean acidification More dissolved CO2 and lower pH could increase metabolic demands, especially of larval Low fishes. Potential problems for development.

High-certainty predictions are well supported by empirical observations and experimentation. Moderate-certainty predictions have some empirical or experimental support, but are not conclusive. Low-certainty predictions are speculative and lack good supportive evidence. Climate change and coral reef fishes P L Munday et al.

McDonald 1997). Fishes are particularly sensitive to not populations are currently close to their thermal temperature during their early life history. Across a optimum for reproduction. Ruttenberg et al. (2005) wide range of fish species, found that mass-specific production of white- rate increases nearly threefold for every 10 °C tailed damselfish (Stegastes beebei, Pomacentridae) in increase in temperature (Rombough 1997), the Gala´pagos Islands declined rapidly from a peak although it is not known if this rate holds for near 25 °C to very low rates at 20 and 27 °C. This tropical reef fishes. After hatching, increased tem- indicates that a temperature increase of just a few perature tends to increase larval growth rate, degrees Celsius could significantly depress reproduc- decrease the age at and increase tive success in fish populations that are near their swimming ability (McCormick and Molony 1995; thermal optimum, unless they shift the timing of Benoıˆt et al. 2000; Hunt von herbing 2002; Meekan reproduction. et al. 2003). In a recent experimental analysis, Fishes on equatorial coral reefs often breed Green and Fisher (2004) showed that larval dura- throughout much of the (Srinivasan and Jones tion of the red-and-black anemonefish (Amphiprion 2006) and reproductive success in these popula- melanopus, Pomacentridae) was 25% shorter, tions could be seriously compromised if higher growth rate was higher and swimming ability temperatures in future mean that the thermal enhanced at 28 °C compared with that at 25 °C. optimum for reproduction is exceeded for large Similarly, Sponaugle et al. (2007) found a strong parts of the year. Breeding tends to be more seasonal correlation between water temperature, growth at higher latitudes (Robertson 1991; Srinivasan and rates and larval duration of the bluehead Jones 2006) and is often associated with increasing (Thalassoma bifasciatum, Labridae). Cohorts recruit- water temperature in spring (Colin 1992; ing during periods of warmer water exhibited faster Danilowicz 1995; Sadovy 1996; Samoilys 1997; growth and shorter larval durations. Consequently, Hilder and Pankhurst 2003). The upward trend in it appears that small increases in water temperature water temperature may be sufficient to trigger will generally hasten the developmental rate of breeding in many species, but others may require larval reef fishes and decrease their larval duration, a threshold temperature to be reached before they provided that ambient temperatures do not exceed breed. For example, coral trout at several locations optimum levels for growth and development, and on the Great Barrier Reef appear to commence the larvae can consume sufficient additional food to spawning when the sea temperature reaches support the increased energetic demand of develop- approximately 26 °C (Samoilys 1997; Frisch et al. ing at a higher temperature. 2007; D. Williamson, personal communication). Although increased temperature may accelerate Increased ocean temperatures could cause an earlier growth and development, it may also increase start to the breeding season for species with temper- mortality rates. Pre-hatching mortality of Ambon ature thresholds for reproduction, and possibly a damselfish (Pomacentrus amboinensis, Pomacentri- longer breeding season if thermal limits for reproduc- dae) embryos was higher at 31 °C compared with tion are not exceeded. Alternatively, a split breeding that at 29 °C and larvae survived for a shorter season might develop, with reproduction occurring period of time on their endogenous yolk-sac either side of the summer maximum (Fig. 2). resources at the higher temperature (Gagliano et al. Although some species probably use temperature 2007). This indicates that even relatively small to cue breeding, other species may use photoperiod increase in temperature could have a negative effect or a combination of photoperiod and temperature to on the total number of larvae reaching settlement. start the breeding season (Pankhurst and Porter Very little is know about the effects of abnormally 2003). These species would suffer the greatest high temperatures on the interactions between impacts of increased temperature on reproduction growth, development and survival of early life- because they are less likely to adjust the timing of history stages of reef fishes and this is a serious gap reproduction to suit the thermal environment. in our knowledge. Reproductive success could be seriously compro- Reproduction of tropical reef fishes appears to be mised if higher water temperatures: (i) cause egg highly sensitive to temperature fluctuations production to be impaired (Van Der Kraak and (Pankhurst and Porter 2003). Increased tempera- Pankhurst 1997); (ii) increase embryonic mortality ture could have either a positive or negative effect (Gagliano et al. 2007); or (iii) lead to a mismatch on reproductive output, depending on whether or between the timing of breeding (set by photoperiod)

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Figure 2 Possible alternate breeding scenarios at higher sea temperatures: (a) conceptual current-day breeding season, (b) longer breeding season with lower effort, similar to that currently seen in lower latitude pop- ulations (c) earlier start to breeding season, (d) bimodal breeding season.

and the optimal conditions in the for that caused by acid pollution in freshwater lakes, survival and dispersal of larvae (set by temperature) the impact of reducing pH through elevated CO2 (Edwards and Richardson 2004). levels appear to be more dramatic than an equiv- alent reduction in pH by the direct addition of acids (Ishimatsu et al. 2004). Furthermore, coral reef Ocean acidification fishes have evolved in a relatively stable pH envi-

The amount of carbon dioxide (CO2) dissolved in the ronment, and therefore, may tend to be more ocean increases as atmospheric partial pressure of sensitive to pH changes than freshwater fishes.

CO2 increases. Additional CO2 reacts with water to Consequently, there is at least room for concern that form carbonic acid, which through a series of reduced pH could have negative effects on coral reef reactions leads to a decline in pH and a shift in the fishes. embryos and young larvae are more carbonate–bicarbonate balance (Feely et al. sensitive to pH changes than are juveniles and

2004). Atmospheric CO2 concentrations have adults (Brown and Sadler 1989), therefore, effects of increased from an estimated 280 p.p.m. in pre- acidification are most likely to be detected at these industrial times to approximately 380 p.p.m. today early life stages. of pelagic spawning fishes (IPCC 2007b). Depending on emission scenarios, might be more susceptible to pH changes than those

CO2 concentrations are predicted to reach 540– of demersal spawners because they are released 979 p.p.m. by the end of the century (IPCC 2007b) directly into ocean waters where pH remains and this will cause the average ocean pH to drop relatively stable over the nocturnal–diurnal cycles. 0.4–0.5 points compared with pre-industrial levels By contrast, pH fluctuations can occur close to the

(Royal Society 2005). This would make the ocean reef substratum due to daytime consumption of CO2 more acidic than at any time in the past by algae and night-time release of CO2 by all reef 400 000 years (Feely et al. 2004). The effects that . For this reason, eggs of benthic increased levels of dissolved CO2 and reduced pH spawners may have a greater tolerance to pH will have on reef fishes remain highly speculative fluctuations. because very little research has been conducted on Increased levels of dissolved CO2 not only acidify this issue. the ocean, but they also act to decrease the pH of The acidification of lakes by atmospheric pollu- animal (Po¨rtner et al. 2004). In fishes, the tants has caused significant reductions in the internal pH level is controlled by the exchange of growth rate, reproductive success and survival of , mostly across the , and small changes in some freshwater fishes (Jackson and Harvey 1995). internal or external pH can be readily compensated Although the decrease in ocean pH as a result of (Claiborne et al. 2002). Although this compensa- climate change is not expected to be as severe as tory mechanism is not detrimental in the short

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term, ultimately it might have some physiological in strength due to the increased thermal stability of costs, especially for species or life stages with high the shallow surface zone (Steinberg 2007), metabolic demands (Po¨rtner et al. 2004) and when although this effect could be counteracted by compounded by higher metabolic demands at ele- changes in the strength or direction of surface vated temperatures (Po¨rtner and Langenbuch winds at some locations. 2005). Larval reef fishes have exceptionally high Changes to current patterns could impact fishes demands (Nilsson et al. 2007) and are more in several ways. First, local and meso-scale currents likely to be challenged by changes in pH than are often play an important role in the dispersal post-settlement fish. patterns of larval fishes (James et al. 2002; Suthers Ocean acidification is expected to have serious et al. 2004; Sponaugle et al. 2005; Cowen et al. consequences for calcifying organisms, such as 2006). Any changes in the strength or direction of corals, because it reduces the availability of carbon- these currents could influence larval transport ate ions (Feely et al. 2004; Kleypas et al. 2006). among reefs. Second, nutrient supply influences Skeletal growth in and adult fishes is the production and distribution of plankton (Hays unlikely to be impacted because these life stages et al. 2005; McKinnon et al. 2007), which is food have precise control over their internal ionic envi- for larval fishes and planktivorous adults. Changes ronment. However, changes in the carbonate ion to primary and secondary productivity brought balance might be sufficient to retard skeletal or about by change to oceanographic circulation could otolith (ear ) development during embryonic or influence the growth and survival of larval fishes larval stages. Experiments have shown that skeletal (Searcy and Sponaugle 2000; Sponaugle and calcification of some larvae is reduced Pinkard 2004; Meekan et al. 2006) and the growth at CO2 concentrations within those predicted to and reproductive success of planktivorous adults, exist by 2100 (Shirayama and Thornton 2005). such as caesionids and many pomacentrids, and Whether these levels will affect the skeletal or acanthurids. otolith development of larval fish is currently unknown, but should be a priority area for research Cyclones and extreme weather because disruption to the development of these structures could have significant effects on the The frequency of intense cyclones is predicted to swimming and feeding efficiency of larvae or their increase as a result of climate change (Webster et al. ability to orient towards the sound of reefs or other 2005; IPCC 2007b). Whether the total number or relevant signals. locations of tropical cyclones will change is uncer- tain. More extreme droughts and floods are pre- dicted in a warmer world, and consequently, the Ocean circulation extremes of rainfall and river flow are expected to Climate change will almost certainly influence become more common over the next 100 years ocean circulation and ; however, the (Lough 2007). More extreme rainfall patterns will changes are expected to differ greatly among lead to greater variability in patterns of nutrient regions and locations, and the magnitude of change enrichment to coastal waters, with possible conse- at any location is difficult to predict (Bindoff et al. quences for the quality and quantity of planktonic 2007; Steinberg 2007). Nevertheless, some broad food available to larval and adult coral reef fishes in trends have been suggested. Increased thermal nearshore waters (Hays et al. 2005; McKinnon et al. stratification of the ocean surface layer is expected, 2007). reducing the input of from cooler waters Tropical cyclones often cause a temporary decline below the thermocline (Bindoff et al. 2007; in the abundance of some fishes on impacted reefs Poloczanska et al. 2007). Increased heat content (Halford et al. 2004) due to the loss of critical of the ocean and changes to wind fields may tend to habitat or food for certain species (Wilson et al. increase the strength of some ocean currents. For 2006). Recovery of the fish populations occurs as example, the South Equatorial Current, which is a the benthic habitat recovers over a period of years to major oceanographic driver on the Great Barrier decades (Halford et al. 2004). Stronger cyclones will Reef, is expected to increase in strength over the increase the disturbance regime experienced by reef next 50 years (Cai et al. 2005; Poloczanska et al. communities, with increased impacts on fish com- 2007). Surface currents might also tend to increase munities at local scales. A more troubling conse-

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quence of increased cyclone intensity is the inter- there are exceptions to this pattern (Williams et al. action with other disturbances, such as coral 2003). Therefore, we might expect life histories bleaching, that also decrease coral cover and within local populations to shift towards smaller degrade habitat structure. The cumulative effect of maximum size and reduced maximum longevity as an increasing number of disturbances on the temperature increases. Average age or size at physical structure of reefs has the potential to maturation of fishes is often correlated with max- systematically degrade reef fish communities. imum age or size (Beverton 1992); so, we also expect that size or age at maturation will tend to decrease if life histories shift towards smaller max- Sea level rise imum size and younger average age at higher Sea level is rising due to thermal expansion of the temperatures. These shifts would be observed as oceans and additional contributions of water from long-term trends in mean values for particular melting glaciers and continental sheets. Average populations. sea level has risen nearly 20 cm since 1870 and is Increased temperature might be expected to predicted to rise at least another 30–40 cm by 2100 increase growth rate within populations, but will (Church and White 2006; IPCC 2007b). Sea level only do so if individuals can consume more food at rise will be far greater if melting of ice sheets and higher temperatures to compensate for increased glaciers accelerates dramatically, as has been sug- metabolic rate (Jobling 1997). Some reef fishes gested by some recent studies (Velicogna and Wahr exhibit an inverse relationship between growth rate 2006). It is unlikely that coral reef fishes will be and temperature across their geographic ranges seriously affected by a vertical sea level rise of <1 m. (Choat and Robertson 2002; Robertson et al. 2005), Many species can be found across a range of depths, which contrasts with the evidence for increased either within or among reefs, and most experience growth rate at higher temperatures for larval fishes daily tidal fluctuations in depths greater than that (Wilson and Meekan 2002; Meekan et al. 2003; predicted to occur from sea level rise. Even for those Sponaugle et al. 2007), and suggests that adult species with narrow depth distributions, reef struc- growth is often food limited. The effect of increased ture and profile are probably more important than sea temperatures on the growth of reef-based sea level height in setting their depth distributions. individuals is difficult to predict and will depend Inundation of coastal environments might have on interactions between temperature, metabolic consequences for the small number of coral reef rate, food availability and nutritional quality and species that inhabit , and sea- population density. grass beds as juveniles and migrate to reefs later in Reef fishes exhibit considerable variation in life- life (Sheaves 1995). history traits among habitats. On the Great Barrier Reef, for example, parrotfishes on the outer reef grow slower, have higher mortality rates, reach Impact of climate change on populations smaller maximum sizes and change sex earlier than and communities individuals of the same species living just 10–20 km away on the midshelf (Gust et al. 2002; Gust 2004). Life-history traits Consequently, expected changes to life-history traits Life-history traits of reef fishes can differ markedly are not expected to be large compared to natural between populations and much of this variability variation that already exists among populations appears to be influenced by complex interactions occupying different habitats. between temperature, density, food availability and mortality rates (Gust et al. 2001; Meekan et al. Recruitment and population dynamics 2001; Choat and Robertson 2002; Robertson et al. 2005; Ruttenberg et al. 2005). Within-species vari- Recruitment to reef fish populations is often highly ations in maximum size and age have been corre- variable and many populations exhibit significant lated with temperature at geographical (Choat and variation in their age structure that can be linked to Robertson 2002; Robertson et al. 2005) and local variation in the magnitude of recruitment pulses scales (Ruttenberg et al. 2005). In general, individ- (Doherty 1991). Warmer conditions (within the uals tend to reach smaller maximum sizes and have range currently experienced by reef fishes) generally shorter in warmer environments, although appear to enhance recruitment. For example, good

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recruitment to bicolour damselfish (Stegastes ation in larval supply to reefs, and thus cause partitus, Pomacentridae) populations in San Blas greater variability in recruitment to reef-based has been correlated with higher water temperatures populations – there will be more good recruitment and favourable winds (Wilson and Meekan 2002). events and more recruitment failures. Strong year classes of several damselfishes in the Recruitment at higher temperatures will tend to Gala´pagos Islands were correlated with warm be enhanced at times or locations where larvae El Nin˜o events (Meekan et al. 2001) and synchro- have reliable food supplies, but will be negatively nized increases in the population size of damselfish affected at times or locations where food is less species on the Great Barrier Reef often follow warm abundant or difficult to locate. Upwelling and El Nin˜o conditions (Cheal et al. 2007). There is convergence zones generate abundant food increasing evidence that the survival of larval coral resources for larval fishes (Suthers et al. 2004; reef fishes is linked to growth rate, with individuals Meekan et al. 2006). Larval survival and recruit- from strong recruitment pulses often exhibiting ment may generally be improved at these locations, higher growth rates during the larval period than provided climate change does not affect patterns of those from weak recruitment pulses (Searcy and primary and secondary productivity. At other loca- Sponaugle 2000; Bergenius et al. 2002; Wilson and tions, the condition of larvae at settlement appears Meekan 2002; Meekan et al. 2003). Furthermore, to be dependent on less predictable encounters with numerous studies have found a positive correlation oceanographic features (Sponaugle and Pinkard between larval growth rate and ocean temperature 2004). Recruitment will probably become more (McCormick and Molony 1995; Wilson and Meekan variable at these locations. Larger increases in water 2002; Meekan et al. 2003; Sponaugle et al. 2007). temperature could lead to widespread recruitment All these observations suggests that small increases failure due to reproductive failure of adults. in temperature might tend to have a favourable influence on recruitment, although these benefits Population connectivity could be counteracted by reduced egg production and increased egg mortality at higher temperatures, Currents and tides potentially play an important thereby reducing the number of larvae entering the role in the retention and dispersal of larval fishes pelagic phase in the first place. (Cowen 2002; James et al. 2002; Burgess et al. Warmer conditions tend to increase the develop- 2007). Any changes to circulation patterns as a mental rates of larval fishes and reduce the time to result of climate change could have fundamental metamorphosis (McCormick and Molony 1995; effects on the spatial and temporal patterns of larval Benoıˆt et al. 2000; Green and Fisher 2004). Larval supply to individual reefs and the degree of connec- mortality rates are typically very high; so, even a tivity among reefs. Additionally, increased sea small reduction in larval duration might have a temperatures could modify connectivity between positive influence on the magnitude of recruitment reefs through effects on larval development and (O’Connor et al. 2007). However, additional energy behaviour. Larval swimming ability develops must be consumed by larval fishes to maintain through ontogeny (Fisher et al. 2000) and late- higher metabolic rates at higher temperatures and stage larvae of many reef fish species are capable of to sustain increased growth. Although there is little swimming long distances (Stobutski and Bellwood evidence that larval fishes are food limited (Leis 1997). They can also orient to reefs using a range 1991), and other food resources favoured of sensory mechanisms (Kingsford et al. 2002; by larval fishes are not uniformly distributed Montgomery et al. 2006). Theoretical models pre- (Suthers et al. 2004; Meekan et al. 2006) and dict that the spatial scale of larval dispersal is highly higher energetic demands at higher temperatures sensitive to the ontogenetic timing of reef-seeking mean that larvae have a greater chance of starving behaviour and active swimming ability (Armsworth before encountering favourable patches of food. 2000; Cowen et al. 2006). Increased temperature Furthermore, climate change will probably cause tends to accelerate larval development and enhance greater fluctuations in the quality and quantity of swimming ability (Benoıˆt et al. 2000; Hunt von planktonic food resources for larval fish (Edwards herbing 2002; Green and Fisher 2004). Therefore, and Richardson 2004; McKinnon et al. 2007). the average scale of dispersal between reefs might Consequently, we expect that warmer sea temper- be reduced due to earlier reef-seeking ability and atures will increase the spatial and temporal vari- improved swimming ability in warmer condi-

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tions, although this remains highly speculative, and Munday 2004; Bellwood et al. 2006; Pratchett et al. would be difficult to detect because of the interact- 2006). Coral-dependent species include obligate ing effects of currents on dispersal patterns and the coral dwellers (Munday et al. 1997; Gardiner and prospect of more variable larval survival and Jones 2005), (Pratchett 2005) and recruitment at higher temperatures. species that always settle into live coral (Booth and Wellington 1998; O¨ hman et al. 1998; Holbrook et al. 2000). Some reef fish families are more reliant Habitat loss and community structure on corals than others, with a higher proportion of The frequency of coral bleaching is predicted to species in diverse reef fish families such as butterf- increase as sea temperatures rise (Hoegh-Guldberg lyfish (Chaetodontidae), cardinalfish () 1999; Hughes et al. 2003). Repeated bleaching will and gobies () directly at risk from loss of change the composition of benthic reef communities corals (Pratchett et al. 2008). Many of these fish– and lead to fundamental shifts in the composition of coral relationships are species specific and so the the associated fish communities. Declines in live magnitude of the threat depends on the susceptibil- coral cover, changes in the species composition of ity of particular coral species to bleaching, combined those corals remaining and a loss of habitat with the degree of coral specialization of the fish complexity will all combine to decrease the diversity species (Munday 2004; Feary et al. 2007a). and abundance of reef fish assemblages and alter Declines in coral cover nearly always cause their species composition (Pratchett et al. 2008) corresponding declines in the abundances of coral- (Fig. 3). dependent species (Wilson et al. 2006), but special- Approximately 10% of coral reef fishes can be ist species that inhabit or consume just one or a few classified as coral dependent (Pratchett et al. 2008) coral species often suffer the greatest declines and these species are the ones most immediately because they are unable to use alternative coral affected by coral loss (Kokita and Nakazono 2000; resources as their preferred corals decline in abun- Spalding and Jarvis 2002; Halford et al. 2004; dance (Munday 2004; Pratchett et al. 2008). Community responses to loss of coral cover can extend to a greater range of coral reef fishes than the 10% of species that are directly coral dependent. Seventy-five per cent of fish species declined in abundance, with 50% of species declining by more than 50%, following a severe loss of live coral on coastal reefs in Papua New Guinea, and only a relatively small number of species increased in abundance (Jones et al. 2004). This response to a severe loss of coral cover does not appear to be particularly unusual. In a recent meta-analysis of studies that monitored fish assemblages following disturbances to coral communities, Wilson et al. (2006) found that an average of 62% of the fish species investigated declined in abundance follow- Figure 3 Conceptual diagram of changes in key attributes ing a loss of at least 10% coral cover. Declines in of coral reef habitats (solid lines) and fish communities abundance were the greatest among coral dwellers (dashed line) following severe coral bleaching. Initially, and coral feeders; however, some invertebrate species richness of local coral reef fish assemblages declines feeders and planktivores also declined in due to the loss of species that are strongly dependent on abundance. live coral. In habitats where coral contribute most of the Many reef fishes prefer to settle near live coral topographic complexity, the collapse of dead coral skele- even if adults are not coral dependent (Jones et al. tons over a period of several years will greatly reduce habitat complexity, causing a further decline in species 2004; Feary et al. 2007b). This may explain why a richness. If coral communities do not recover (as illus- broader range of species exhibit a response to large- trated) over 50% of species may ultimately be lost due to scale coral loss than would be predicted based on the combination of declines in habitat complexity and adult habitat associations alone (Booth and Beretta delayed effects of coral loss. 2002). Jones et al. (2004) estimated that 65% of fish

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species on the reefs they studied preferentially settle dramatic effects on the growth and longevity of in or near live coral. Moreover, the proportional coral-dwelling fishes (Munday 2001), with poten- decline in abundance of each species was correlated tially serious implications for reproductive success with their proportional use of live coral at settle- (Fig. 4). Therefore, the negative effects of habitat ment. This suggests that loss of suitable habitat for loss on the survival of adults and the availability of new settlers, and a suppression of cues that substratum for the settlement of new recruits are encourage settlement, are likely to be responsible likely to be reinforced by a decline in adult repro- for declines in abundance of a variety of species ductive performance. following significant coral loss. Reef fish communities have considerable resil- The structural complexity of the reef usually ience to disturbance and can recover from cyclones declines after coral bleaching due to erosion of the and bleaching events over years to decades, pro- dead coral skeletons, and because many of the vided that benthic habitat recovers (Halford et al. corals most susceptible to coral bleaching are also 2004). However, even where coral cover has the ones with the highest structural complexity returned, recovery of the fish communities may be (Marshall and Baird 2000). Reefs with high struc- incomplete if a different suite of coral species tural complexity support more individuals and more dominate the new assemblage (Berumen and species of fishes than reefs with low structural Pratchett 2006). The consequences of habitat loss complexity (Jones 1991; Syms and Jones 2000; on reef fish communities will depend on the Garpe et al. 2006; Graham et al. 2006). Therefore, frequency and intensity of bleaching events, com- we expect to observe a decline in the diversity and abundance of the associated fish communities as the increased frequency of coral bleaching causes an overall decline in the structural complexity of coral reefs. Herbivores often increase in abundance following a loss of coral cover (Wilson et al. 2006), presumably because more area becomes available for algal growth. However, even these species ultimately decline when habitat structure is lost (Sano et al. 1987; Garpe et al. 2006). The only species likely to benefit from coral loss and reef degradation are small generalist species and herbi- vores that live in areas of low relief and rubble, such as various gobies, blennies, and some damself- ishes (Syms and Jones 2000; Bellwood et al. 2006; Glynn 2006, Feary et al. 2007a). The full impacts of coral loss on adult populations may take years to eventuate, even for coral-depen- dent species. Adults are often able to persist for a considerable time following a loss of preferred coral Figure 4 Estimated cumulative reproductive success for resources (Pratchett et al. 2006) and recruitment two species of coral-dwelling gobies (Gobiodon histrio and failures may take some time to affect adult popula- Gobiodon brochus, Gobiidae) inhabiting two different coral tion sizes, especially in long-lived species (Graham habitats ( nasuta and Acropora loripes, Acropori- et al. 2007). Rather than immediate responses to dae). Differential loss of A. nasuta colonies from coral coral loss, populations of many reef fishes will bleaching would have a negative effect on the reproductive exhibit a slow and insidious decline due to increased success of both goby species because estimated reproduc- tive success over an average goby’s lifetime is lower when attrition of adults and reduced replenishment by inhabiting A. loripes compared with A. nasuta for both goby recruits over many years. Loss of coral can have species. Calculations were based on age-based growth rates serious effects on the growth (Kokita and Nakazono of gobies in each species of coral from Munday (2001), a 2000) and body condition (Pratchett et al. 2004) of maximum body size of 49mm for G. brochus and 62 mm corallivorous species, which will probably flow on to for G. histrio (P.L. Munday, unpublished data) and using the reproductive success of the population. Simi- the size-fecundity relationships for coral-dwelling gobies larly, use of alternative coral hosts can have reported by Kuwamura et al. (1993).

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bined with the impacts of other disturbances, mid-latitude ranges (Table 2) that might tend to relative to the potential for the reefs and their contract towards higher latitudes (Fig. 5c). Finally, associated fish communities to rebound. nearly one-quarter of species have small ranges near the high-latitude margins of reef development (Table 2). Many of these small-range species could Geographic ranges experience dangerous range contractions as sea Range shifts correlated with higher than average temperatures increase (Fig. 5d). Of course, whether oceanic temperatures have been observed in tem- a species shifts its range, or not, as temperature perate marine fishes (Holbrook et al. 1997; Parker increases will depend on its thermal tolerance in and Dixon 1998; Perry et al. 2005). Similar relation to the current-day range (Po¨rtner and responses should be expected for coral reef fishes Knust 2007), the potential for acclimation and local as average sea surface temperatures increase. How adaptation, interactions with other species at the geographic ranges will change and the conse- range boundary, dispersal capacity and the avail- quences this will have on species persistence ability of suitable habitat outside the existing range. depends to a large degree on existing latitudinal The latitudinal range of coral reefs is not expected distributions and temperature tolerances. Some to expand significantly in response to increasing sea coral reef fishes currently have ranges that span temperatures (Hoegh-Guldberg 2005) and although the latitudinal extent of coral reefs, others have some fishes found on coral reefs also occur on rocky ranges centred near the , and others only reefs at higher latitudes, the majority of coral reef occur near the high-latitude edges of coral reef species are unlikely to persist in non-reef areas, even development (Jones et al. 2002; Allen 2007). Range if temperatures become more favourable at higher shift scenarios differ for these different geographic latitudes. Consequently, species that already have distributions. small ranges near the limits of coral reef growth will Geographic ranges are well known for species experience further range contractions that would from the families Chaetodontidae and Pomacanthi- ultimately increase their risk of extinction from dae and these species serve to illustrate a range of other impacts. Areas of high endemism associated possible outcomes. A large proportion of species in with isolated island groups, such as the Hawaiian both families have ranges that span the latitudinal Islands (Allen 2007), are likely to experience extent of coral reefs (Table 2) and these species have multiple as isolation restricts the poten- limited potential for range shifts (Fig. 5a) although tial for range shifts. populations may decline in low latitute waters if The ability of tropical species to establish perma- thermal tolerances are exceeded. Less than one- nent populations at higher latitudes will depend on quarter of the species have ranges centred near the their degree of dependence on coral reefs for food, equator, but do not reach higher latitudes (Table 2). shelter and reproduction, their tolerance to lower Many of these species might expand their ranges minimum temperatures in winter, and competition into higher latitudes as sea temperatures increase from established sub-tropical and temperate water (Fig. 5b). A slightly smaller number of species have species. Some species of fishes common on coral

Table 2 Current-day latitudinal dis- tributions and potential range shifts due to increased sea surface temper- ature for species of Chaetodontidae Existing distribution Possible range shift Chaetodontidae Total and Pomacanthidae.

Pan-latitudinal Limited range change 45 28 73 Equatorial Range expansion 23 18 41 Mid-latitude Range contraction 20 14 34 Small range at Range contraction 33 23 56 margin of reef and/or population decline development

Possible range shifts are based on the geographical ranges described in Allen et al. (1998) and assume that the preferred thermal environment is found near the middle of the current-day range.

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(a) (b)

(c) (d)

Figure 5 Examples of potential range shifts that could occur among species of butterflyfishes (Chaetodon, Chaetodintidae) as sea temperatures increase. Orange shading represents existing range, purple represents possible range expansion and faded orange represents possible range contraction. (a) Existing geographical range spanning the latitudinal extent of coral reef development – range shift unlikely to occur. (b) Existing geographical range centred near the equator and not extending to the latitudinal extent of coral reef development – range expansion possible. (c) Existing geographical range centred near mid-latitudes, often reaching the latitudinal extent of coral reef development – range contraction likely. (d) Existing small range near the latitudinal extent of coral reef development – range contraction leading to serious reduction in area is possible. Species selected for illustrative purposes only.

reefs already have populations beyond the latitudi- Overfishing is a serious problem on coral reefs in nal extent of coral reefs (Randall et al. 1997) and many parts of the world (Sadovy 2005; Berkes et al. these species will probably expand their southern 2006; Newton et al. 2007) and some reef fish range limits as sea temperatures increase. However, populations are already greatly depleted, even the appearance of entire communities of coral reef before they face the challenges of climate change. fishes at higher latitudes than current distributions Overfishing of herbivorous fishes is particularly is highly unlikely. problematic because it can potentially lead to the proliferation of algae and a regime shift to an alternative stable state were corals are less domi- Interactions with other stressors nant (Hughes et al. 2003; Bellwood et al. 2004; Climate change will interact with other anthro- Mumby et al. 2006a; Hoegh-Guldberg et al. 2007). pogenic stressors to compound the problem of reef A regime shift on coral reefs would almost certainly degradation. Destructive fishing practices and cause a loss of fish diversity, especially among coral- terrestrial pollution (especially elevated sedimenta- dependent species, and a shift towards communities tion) have degraded coral reefs in many parts of containing fewer specialist and more generalist the world (Birkeland 1997; Burke et al. 2002; species (Munday 2004; Bellwood et al. 2006; Wilkinson 2002) and will continue to be chronic Wilson et al. 2006). Unfortunately, the combined stresses for reefs near large human populations. effects of overfishing and climate change impacts on Elevated sedimentation, in particular, can increase herbivorous fishes may make undesirable phase coral mortality from bleaching and reduce the shifts more likely. Although some herbivorous fishes capacity of reefs to recover after mass bleaching tend to increase in abundance immediately after a (Fabricius 2005; Hoegh-Guldberg et al. 2007). The coral bleaching event, they usually decline below combined effect on reef fishes would be an their original numbers once habitat structure acceleration of the changes to community struc- is eroded (Sano et al. 1987; Garpe et al. 2006). ture and abundance described above due to A decline in numbers would increase the habitat degradation. probability of regime shifts to algal-dominated reefs,

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and could reduce the potential for recovery because Bellwood 2005; Hernaman and Munday 2005), even healthy herbivore populations do not always which means there is the opportunity for selection control a rapid proliferation of macroalgae (Ledlie to occur over 50–100 generations before the end et al. 2007). of the century. Other coral reef fishes are long lived, but still tend to mature within a few years, e.g. 2–4 years in some acanthurids that can live Adaptation to climate change 30–40 years (Choat and Robertson 2002). The Heritable changes in life-history characteristics that relatively short generation times of these species are consistent with climate change predictions have should provide some potential for local adaptation been detected in a number of terrestrial to climate change. Yet other species are both long (Bradshaw and Holzapfel 2006; Skelly et al. 2007). lived and late maturing, e.g. 9–10 years in some In each case, the phenotypic change corresponds to serranids and lutjanids (Pears et al. 2006; Marriott an increase in fitness under the new climate regime, et al. 2007). There is little potential for local indicating that genetic adaptation to climate change adaptation of these species, unless there is consid- is already underway in some animal populations. erable genetic input from populations already Some acclimation and adaptation to climate change adapted to warmer waters. will almost certainly occur in reef fish populations; Although some acclimation or adaptation to however, the extent will vary greatly among increased temperature seems possible, especially species, depending on their current ranges, temper- for species with short generation times, there is ature tolerances, genetic connectivity with other little prospect of adaptation to habitat degradation. populations and generation times. As discussed above, some reef fishes depend on Species with geographic ranges already spanning live coral at one or more critical life stages and large temperature gradients have the greatest many more require complex habitat structure to potential for acclimation and adaptation because escape predators (Beukers and Jones 1997; Syms they must either have considerable plasticity in and Jones 2000; Almany 2004). Significant thermal tolerance, or be locally adapted to the declines in fish diversity following large-scale loss temperature gradient. This means there should be of live coral (Wilson et al. 2006) and further some potential to accommodate increases in sea declines following loss of habitat structure temperatures by individual acclimation or flow (Graham et al. 2006) indicate that many species are from low-latitude populations. There is evidence for unable to persist once their habitat has seriously strong genetic connectivity among populations of degraded. There is little prospect of genetic adaptation coral reef fishes in some regions, such as the Great under these circumstances. Habitat degradation will Barrier Reef in Australia (Doherty et al. 1995; also retard adaptation to other climate change Messmer et al. 2005; Bay et al. 2006). Conse- impacts (e.g. increased temperature) by reducing quently, high-latitude populations in these locations genetic variability within populations (decreased might already contain some tolerance to higher population size) and by reducing genetic connectivity temperatures due to regular genetic input from between populations (smaller and more patchily lower latitude populations. Furthermore, as sea distributed populations). temperatures increase, gene flow from low-latitude populations might assist high-latitude populations Coral reef fisheries in adapting to the new conditions. More isolated populations, such as those inhabiting island groups Total global fisheries yield from coral reefs is in the central Pacific or Indian Oceans, have lower estimated to be worth at least US$5 billion annually levels of genetic connectivity to other populations and many millions of people in tropical countries (Planes 2002), which greatly reduces the potential are directly dependent on food harvested from local for local adaptation to increasing ocean temperature reefs (Cesar et al. 2003, Sadovy 2005). Most coral by transfer of favourable genotypes. reef fisheries exploit multiple species (Polunin and To a large degree, the potential for genetic Roberts 1996), and although diverse multi-species adaptation will depend on generation time. Some fisheries are likely to be more resilient to environ- coral reef fishes have very short generation times mental change than highly specialized fisheries that should favour rapid local adaptation. For exam- ( et al. 2006), this depends on specific vul- ple, many goby species are annuals (Depczynski and nerabilities of target species and assuming there are

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not other major impacts that influence overall structure and might be affected on coral diversity and productivity. A serious concern is that reefs are difficult, because the net impact of climate many of the fisheries that provide food and live- change on tropical marine productivity is uncertain lihoods for millions are already over-exploited and is likely to vary greatly from place to place – (Newton et al. 2007; Hoegh-Guldberg et al. 2007) there might be positive effects on biomass in some and, therefore, have little resilience to additional locations and negative effects in others (Gregg et al. impacts from climate change. 2003; Steinberg 2007). However, more generally, Numerous studies have demonstrated a strong we expect an overall decline in biomass at higher link between climatic fluctuations, such as El Nin˜o trophic levels as a result of a general decline in and La Nin˜a events, and the distribution or primary productivity caused by increased thermal productivity of exploited fish populations (Lehodey stratification of the and reduced et al. 1997; O’Brien et al. 2000; Worm et al. 2005; nutrient input from cooler, deeper waters, combined Ottersen et al. 2006). However, these impacts tend with increased metabolic rates of most organisms at to be species specific (Lehodey et al. 2003), making higher ocean temperatures (Bopp et al. 2001, 2005; it difficult to predict the magnitude and direction of Loukos et al. 2003; Hobday et al. 2006). Reduced changes in fisheries productivity arising from envi- productivity would add further pressure to coral reef ronmental change. The consensus is that while fisheries that are already over-exploited (Newton some fisheries target species will be negatively et al. 2007). impacted by climate change, others may benefit Most coral reef species of commercial importance (McLean et al. 2001). Importantly, the coral reef are broadly distributed and their geographical fish species that are most vulnerable to environ- distributions might not be significantly affected by mental change (e.g. small bodied, restricted range climate change in the short-to-medium term, but and highly specialized coral-dependent species) are there are clear exceptions. The sweetlip emperor not generally targeted by coral reef fisheries (Lethrinus miniatus, Lethrinidae), an important com- (Pratchett et al. 2008). Perhaps this is why there mercial and recreational fisheries species, has a is currently little evidence for changes in the size, restricted anti-equatorial distribution with an composition or total value of landings from reef- apparent upper thermal limit of about 28°C (Wil- based fisheries following severe episodes of climate- liams et al. 2003). On the Great Barrier Reef, induced coral bleaching (McClanahan et al. 2002; sweetlip emperor are restricted to south of 18ºS Grandcourt and Cesar 2003). However, it is also where the impact of climate change on water possible that effects of environmental change and temperature is predicted to be the greatest (Lough coral bleaching on fisheries target species are 2007). The distribution of this species will probably delayed due to lag effects from recruitment failure, shift south as water temperature increases, poten- and not yet apparent (Graham et al. 2007). Lag tially causing a shift in fishing effort and reducing effects will make climate change impacts difficult to fisheries productivity. detect, and difficult to separate from the effects of fishing, but nonetheless important in the long term. The future Changes to primary productivity brought about by climate change could affect biomass at all trophic Climate change will undoubtedly be the major levels. For example, slower growth appears to have factor determining the future of most coral reef occurred in benthic populations of three species of fishes, impacting on them through all life stages herbivorous damselfishes during warm El Nin˜o and through a variety of mechanisms. Recent conditions in the Gala´pagos Islands (Meekan et al. ecological advances provide some capacity for 1999). The green and preferred by these predicting the future, but great uncertainty damselfishes was largely replaced by of remains (Table 1). Some of the impacts of climate lower nutritional value during the warm period, change on coral reef fish are predictable and are probably causing a food shortage that curtailed in fact already in progress (e.g. effects of habitat growth rates. Similarly, climate-induced changes to degradation). Other impacts are much less certain plankton communities could affect the growth and for a variety of reasons, including uncertainty in abundance of planktivorous fishes, with flow-on climate change projections, poor understanding of effects to larger predatory species that are favoured the responses likely to accompany changes to by fishers (Fig. 1). Predictions about how trophic environmental factors at individual, population

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and community levels, and the complexity of will probably experience range contractions. Of interactions that can occur between different greatest concern are small-range species currently physical and biological factors that will be affected living near the margins of coral reef distributions, by climate change. However, what is certain is which will face an increased risk of extinction as that without immediate action to limit further their ranges contract. global warming, the future is bleak for many reef- Increased temperature will probably cause a shift associated species. in life-history traits of local populations, although these changes will be relatively small compared with the natural variation already exhibited by Future ecology many species across their geographic ranges. The The most immediate and identifiable impacts of most likely response to rising temperatures will be a climate change on coral reef fishes will be changes shift in life-history traits in high-latitude popula- in community composition and loss of tions to more closely match those currently seen in as a result of coral bleaching. There is now sufficient low-latitude populations. evidence to indicate that large-scale declines in coral Recruitment may tend to be enhanced by small cover will have serious consequences for the diver- increases in temperatures, but will become more sity and abundance of reef fish assemblages. Coral- variable where food supply for larvae is spatially or dependent fishes suffer the most rapid declines in temporally unpredictable. Temperature changes at abundance as coral cover is lost. Many other species the upper range of climate change predictions are will exhibit longer term declines in abundance, due likely to have serious consequences for the repro- to loss of settlement habitat and the erosion of reef ductive performance of adults, potentially leading to architecture and structural complexity that are complete reproductive failure and subsequent pop- essential for recruitment and survival. Some species, ulation collapse. such as territorial herbivores and invertebrate Major ecological processes, such as , feeders, may initially increase in abundance as competition and herbivory will be affected by shifts coral cover declines, but even these species will in the relative abundances of species in local decrease in abundance if habitat structure erodes. assemblages. The strength of predator–prey and Declines in species richness and abundance will be competitive interactions could also be altered by the highly patchy, and interspersed with cycles of reduction in habitat structure (Beukers and Jones recovery, but the overall trend will be negative if 1997; Holbrook and Schmitt 2002; Almany 2004) climate change continues to cause severe and and greater variability in the number of individuals repeated impacts on the composition and physical recruiting to local populations (Caley et al. 1996). structure of the reef . The only species likely How changes in the relative strength of predation to benefit are some generalist planktivores, small and competition will affect fish communities, and herbivores and rubble dwellers. the function of coral reef ecosystems as a whole, The different impacts of climate will interact with remains largely unknown. Alteration of benthic each other and with other threats and stresses to habitat structure could favour some herbivorous coral reefs, potentially leading to synergistic or fishes over others. Whether the species favoured are cumulative effects that compound the problem. For the ones that consume macroalgae will have example, increased bleaching and ocean acidificat- important consequences for the ability of reefs to ion will have cumulative effects on the degradation resist phase shifts (Hughes et al. 2007; Ledlie et al. of coral reef habitat. These impacts could interact 2007). However, even if key herbivores remain, with overfishing and compound the effects of coral reefs are not guaranteed to return to a coral terrestrial pollution to further degrade benthic dominated state after a disturbance if other stresses communities, or even cause a regime shift from limit coral recruitment and recovery (McClanahan coral- to algal-dominated reefs. Dramatic phase 2008). shifts in the benthic habitat would, in turn, further affect the composition of reef fish communities. Future evolution Range expansions and contractions will occur as ocean temperature increases. Some coral reef fish Some fish species may acclimatize to increased sea species will extend their distribution limits as temperatures as a result of existing phenotypic temperature increases. A similar number of species plasticity in their populations. Connectivity between

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populations should also promote some genetic Climate change is likely to increase the risk of adaptation to increased temperature by gene flow fisheries collapses. The predicted increase in recruit- from extant populations residing in warmer loca- ment variability will make optimal harvest strate- tions. Local adaptation to climate change will be gies more difficult to determine and fisheries may most evident in small, short-lived species, where become more susceptible to overfishing during selection can operate over a large number of episodes of low recruitment. Incorporating larger generations. Larger species, with long generation ‘safety margins’ into harvest levels could provide times, have little potential for local genetic adapta- some insurance from greater variability in popula- tion to rapid climate change. A serious concern for tion fluctuations and uncertainty about other all reef fishes is that habitat loss could have a climate change impacts. In some cases, lower negative effect on the potential for adaptation to harvest rates will need to be considered because of environmental change, because smaller and more the possibility that reduced planktonic productivity fragmented populations will have less genetic var- and loss of benthic shelter will lead to a reduction in iability for selection to act upon and will be less food supply for larger predatory species that are effective in spreading favourable genotypes. Small- favoured by most commercial fisheries. More gen- range species near the latitudinal margins of reef erally, incorporating climate change scenarios and development and species living on isolated island the range of potential effects on fish populations into groups are mostly at risk because they cannot move stock assessments and management strategy eval- to more favourable locations as environmental uations is essential for sustainable management of conditions change and because their isolation will coral reef fisheries in future. restrict the exchange of from other popula- tions that might otherwise help them adapt to Future science climate change. Much more research is required before we can predict the full ramifications of climate change on Future management coral reef fishes and develop more and better First and foremost, there is a critical need to control strategies for minimizing the loss of biodiversity. and reduce greenhouse gas emissions to give at least More information is required on the effects that the more resilient component of the coral reef fish changes in the physical environment will have on fauna a long-term future. Management strategies the function and behaviour of reef fishes, because that target other human impacts, such as over- much of the available data on how fishes respond exploitation and poor water quality, may help to to changes in temperature comes from temperate minimize the shorter term impacts by increasing the species and these results might not be directly resilience of reef ecosystems (Hughes et al. 2003). applicable to tropical marine fishes. Improved Given the evidence for the top-down control of coral projections of how ocean currents and primary reefs, maintaining healthy predator and herbivore productivity will change at regional and local fish populations may provide a certain amount of scales are sorely needed, as these projections are resilience to climatically induced changes. Marine critical for predicting how individual performance, protected areas, while not a ‘cure-all’ solution to the population dynamics and connectivity pattern will problems faced by coral reefs, may contribute to reef change over the coming century. More informa- resilience by protecting exploited, ecologically tion is needed on the habitat requirements of reef important species (Mumby et al. 2006a,b). How- fishes, especially around the time of settlement. ever, as the majority of small reef fish species are not Many reef fishes are closely associated with live exploited, protected areas offer reef fish biodiversity coral habitat at the time of settlement, even if limited protection from extrinsic disturbances such adults are not. Understanding the habitat require- as climate change (Boersma and Parrish 1999; ments of fishes throughout their life will enable Jones et al. 2004, 2007; Aronson and Precht more precise predictions to be made about the 2006). A rapid reduction in greenhouse gas emis- long-term consequences of declining coral cover sions, leading to a stabilization of global tempera- for reef fish assemblages. tures and ocean pH, is the only viable, long-term Finally, more attention needs to be given to the solution to the climate change crisis facing coral potential for acclimation and adaptation of reef reefs. fishes to a changing climate. Ultimately, it is the

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potential for species to adapt that will determine Bellwood, D.R., Hoey, A.S., Ackerman, J.L. and Depczyin- whether tolerance limits can keep pace with the ski, M. (2006) Coral bleaching, reef fish community changing environment. If global action can reduce phase shifts and the resilience of coral reefs. Global the rate of climate change to bring it in line with the Change Biology 12, 1587–1594. potential rate of adaptation of many species, and at Benoıˆt, H.P., Pepin, P. and Brown, J.A. (2000) Patterns of metamorphic age and length in marine fishes, from the same time prevent irreversible damage to the individuals to taxa. Canadian Journal of Fisheries and coral reef habitat, there is at least a glimmer of hope Aquatic Sciences 57, 856–869. on an otherwise bleak horizon. Bergenius, M.A.J., Meekan, M.G., Robertson, D.R. and McCormick, M.I. (2002) Larval growth predicts the recruitment success of a coral reef fish. Oecologia 131, Acknowledgements 152–525. We thank Gerald Allen for data and maps of the Berkes, F., Hughes, T.P., Steneck, R.S. et al. (2006) geographical distribution of butterflyfishes, Marian Globalization, roving bandits, and marine resources. Wong for assisting with the figures and Gerald Allen, Science 311, 1557–1558. Howard Choat, Ove Hoegh-Guldberg, Terry Hughes, Berumen, M.L. and Pratchett, M.S. (2006) Recovery Johanna Johnson, Jeff Leis, Janice Lough, Laurence without resilience: persistent disturbance and long- term shifts in the structure of fish and coral com- McCook, David McKinnon, Mike Kingsford, Paul munities at Tiahura Reef, Moorea. Coral Reefs 25, Marshall, Serge Planes, Peter Sale, Marcus Sheaves, 647–653. Maya Srinivasan and David Williamson for discus- Beukers, J.S. and Jones, G.P. (1997) Habitat complexity sions, comments and support that have helped in the modifies the impact of piscivores on a coral reef fish development of this manuscript. population. Oecologia 114, 50–59. Beverton, R.J.H. (1992) Patterns of reproductive strategy parameters in some marine teleost fishes. Journal of Fish References Biology 41, 137–160. Access Economics (2007) Measuring the economic and Bindoff, N.L., Willebrand, J., Artale, V. et al. (2007) financial value of the Great Barrier Reef Marine Park Observation, oceanic climate change and sea level. In: 2005/6. Report by Access Economics Pty Limited for the Climate Change 2007: The Physical ScienceBasis. Contri- Great Barrier Reef Marine Park Authority. Great Barrier bution of Working Group I to the Fourth Assessment Report Reef Marine Park Authority, Townsville, Qld. 84 pp. of the Intergovernmental Panel on Climate Change (eds S. Allen, G.R. (2007) Conservation hotspots of biodiversity Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. and endemism for Indo-Pacific coral reef fishes. Aquatic Averyt, M. Tignor and H.L. Miller). Cambridge Conservation: Marine and Freshwater Ecosystems. DOI: University Press, Cambridge, UK, pp. 385–432. 10.1002/aqc.880. Birkeland, C. (1997) Life and Death of Coral Reefs. Chapman Allen, G.R., Steene, R. and Allen, M. (1998) Angelfishes and & Hall, New York. Butterflyfishes. Odyssey, Perth. Boersma, P.D. and Parrish, J.K. (1999) Limiting abuse: Almany, G.R. (2004) Does increased habitat complexity marine protected areas, a limited solution. Ecological reduce predation and competition in coral reef fish Economics 31, 287–304. assemblages? Oikos 106, 275–284. Booth, D.J. and Beretta, G.A. (2002) Changes in a fish Almany, G.R. and Webster, M.S. (2004) Odd species out as assemblage after a coral bleaching event. Marine Ecology predators reduce diversity of coral-reef fishes. Ecology Progress Series 245, 205–212. 85, 2933–2937. Booth, D.J. and Wellington, G. (1998) Settlement prefer- Armsworth, P.R. (2000) Modeling the swimming response ences in coral reef fishes: effects on patterns of adult and of late stage larval reef fish to different stimuli. Marine juvenile distributions, individual fitness and population Ecology Progress Series 195, 231–247. structure. Australian Journal of Ecology 23, 274–279. Aronson, R.B. and Precht, W.F. (2006) Conservation, Bopp, L., Monfray, P., Aumont, O. et al. (2001) Potential precaution, and Caribbean reefs. Coral Reefs 25, 441–450. impacts of climate change on marine export production. Bay, L.K., Crozier, R.H. and Caley, M.J. (2006) The Global Biogeochemical Cycles 15, 81–99. relationship between population and genetic struc- Bopp, L., Aumont, O., Cadule, P., Alvain, S. and Gehlen, M. ture and pelagic larval duration in coral reef fishes on (2005) Response of distribution to global the Great Barrier Reef. 149, 1247– warming and potential implications: a global model 1256. study. Geophysical Research Letters 32, L19606. Bellwood, D.R., Hughes, T.P., Folke, C. and Nystrom, C. Bradshaw, W.E. and Holzapfel, C.M. (2006) Evolutionary (2004) Confronting the coral reef crisis. 429, response to rapid climate change. Science 312, 1477– 827–833. 1478.

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