Perspectives on Massive Coral Growth Rates in a Changing Ocean

2 downloads 3028 Views 2MB Size Report
environmental control on both coral reef distribution (Kley- pas et al., 1999a) and ..... lipid content, tissue layer, tissue biomass before and after stress (Carilli et al. ..... Global Coral Reef Monitoring Network, Australian Institute of Marine. Science ...
Reference: Biol. Bull. 226: 187–202. (June 2014) © 2014 Marine Biological Laboratory

Perspectives on Massive Coral Growth Rates in a Changing Ocean JANICE M. LOUGH* AND NEAL E. CANTIN Australian Institute of Marine Science, PMB 3, Townsville M.C., Queensland 4810, Australia

Introduction

Abstract. The tropical ocean environment is changing at an unprecedented rate, with warming and severe tropical cyclones creating obvious impacts to coral reefs within the last few decades and projections of acidification raising concerns for the future of these iconic and economically important ecosystems. Documenting variability and detecting change in global and regional climate relies upon highquality observational records of climate variables supplemented, prior to the mid-19th century, with reconstructions from various sources of proxy climate information. Here we review how annual density banding patterns that are recorded in the skeletons of massive reef-building corals have been used to document environmental change and impacts within coral reefs. Massive corals provide a historical perspective of continuous calcification processes that pre-date most ecological observations of coral reefs. High-density stress bands, abrupt declines in annual linear extension, and evidence of partial mortality within the skeletal growth record reveal signatures of catastrophic stress events that have recently been attributed to mass bleaching events caused by unprecedented thermal stress. Comparison of recent trends in annual calcification with century-scale baseline calcification rates reveals that the frequency of growth anomalies has increased since the late 1990s throughout most of the world’s coral reef ecosystems. Continuous coral growth histories provide valuable retrospective information on the coral response to environmental change and the consequences of anthropogenic climate change. Co-ordinated efforts to synthesize and combine global calcification histories will greatly enhance our understanding of current calcification responses to a changing ocean.

Tropical coral reef ecosystems exist in the warmest parts of the oceans and have already demonstrated their sensitivity to observed warming through more frequent reports of mass coral bleaching due to thermal stress events. At the heart of these dynamic and complex ecosystems is the process of calcification. Sustained calcification, significantly enhanced by the coral-algal symbiosis, has to occur fast enough to withstand the natural forces of physical (e.g., waves, tropical cyclones) and biological erosion. This allows formation of the complex hard coral structures, cemented by crustose coralline algae, that provide habitat and food for many thousands of reef-associated organisms and, hence, the highly diverse tropical coral reef ecosystems. Coral reefs occur within relatively narrow limits of their physical environment in terms of temperature, salinity, light, nutrients, and bathymetry (Kleypas et al., 1999a; Done, 2011). The surface oceans and therefore the physical environments where coral reefs reside are, however, changing. The tropical oceans are warming (Fig. 1; Lough, 2012) and becoming more acidic (Doney et al., 2009). These changes are highly likely to continue and intensify with continued global warming due to increasing atmospheric greenhouse gas emissions from human activities (IPCC, 2013). In addition, nearshore coral reefs are likely to experience more extreme rainfall and river flood events, resulting in more frequent episodes of low salinity and high sediment, which can also be a source of stress (Kerswell and Jones, 2003; Fabricius, 2005; Berkelmans et al., 2012). Outside of the equatorial region (where tropical cyclones do not form; Emanuel, 2003), coral reefs are also likely to experience more intense tropical cyclones that can be a significant source of physical destruction and resulting loss of hard coral cover (Fabricius et al., 2008; De’ath et al., 2012). Reef-building corals are, therefore, entering a new era in their long history that is taking them outside their

Received 6 November 2013; accepted 29 January 2014. * To whom correspondence should be addressed. E-mail: j.lough@ aims.gov.au Abbreviations: CT, computerized tomography; GBR, Great Barrier Reef; SST, sea surface termperature. 187

188

J. M. LOUGH AND N. E. CANTIN

0.6

0.4

Overal warming (1983-2012) - (1871-1900) = +0.43oC Trend 1901-2012 = 0.05oC/decade Trend 1951-2012 = 0.08oC/decade Trend 1971-2012 = 0.10oC/decade

oC

0.2

0.0

-0.2

-0.4

-0.6 1870

1890

1910

1930

1950 Year

1970

1990

2010

Figure 1. Annual average tropical (30°N–30°S) sea surface temperature anomalies (from 1961 to 1990 average), 1871–2012. Thick line is 10-year Gaussian filter illustrating decadal variability. Dashed line is linear trend (R2 ⫽ 0.56). Also shown is overall warming between first and last 30 years of record and decadal rates of warming from 1901, 1951, and 1971 through 2012. Data from HadISST1 (Rayner et al., 2003).

environmental comfort zone (Hughes et al., 2003; HoeghGuldberg et al., 2007) and reducing the time for recovery between stress events such as bleaching, tropical cyclones, and freshwater floods (Pandolfi et al., 2011). Global-scale changes to the world’s oceans due to increasing greenhouse gases (Sen Gupta and McNeil, 2012; Mora et al., 2013) are already producing an imprint on a range of marine biota (Poloczanska et al., 2013) and are superimposed on local and regional-scale stressors to coral reefs arising from overfishing, changing land-use, and polluted river runoff (Hoegh-Guldberg et al., 2007). Warming and acidification of the oceans, along with other global and regional environmental changes, can affect many aspects of the functioning of tropical coral reef ecosystems and their associated organisms (e.g., Lough, 2008a). Here we focus on the fundamental reef process of calcification. What do we expect will happen to coral calcification rates as the oceans warm and acidify? Our understanding of the carbonate chemistry of the oceans clearly indicates that because the oceans absorb nearly a third of the extra atmospheric CO2, the pH drops, as does the concentration of carbonate ions that are required for calcification processes (Kleypas et al., 1999b; Doney et al., 2009). As a consequence, and supported by many experimental studies, the rate of coral calcification is expected to decline (e.g., Iguchi et al., 2012). It should be noted, however, that our understanding of the biological and environmental controls on rates of calcification in corals is still rudimentary (Tam-

butte et al., 2011), as is our understanding of how calcification in corals is likely to respond to progressive ocean acidification (Venn et al., 2013). There are two possible consequences as temperatures rise. First, mass coral bleaching due to thermal stress events can, if the coral does not die, result in setbacks to coral growth rates and even cessation of growth (e.g., Carilli et al., 2009). Second, coral growth will decline as a result of water temperatures exceeding the coral’s thermal optimum, which is suggested to be about 26 –27 °C (Jokiel and Coles, 1978; Cooper et al., 2008). If, therefore, coral calcification is responding simply and directly to these increasing environmental stressors, we might expect calcification rates to show a general decline possibly interspersed with marked drops in growth associated with thermal stress events. Documenting variability and detecting change in global and regional climate relies upon high-quality observational records of climate variables. Prior to the mid-19th century, these records are supplemented by reconstructions obtained from various sources of proxy climate information (Jones et al., 2009). Similarly, to document and detect changes in coral reef calcification, we need dateable and measurable records of calcification rates. The discovery of annual density bands in massive coral skeletons (Knutson et al., 1972) opened the door for retrospectively monitoring coral growth rates as well as a wealth of proxy environmental information incorporated into the coral skeleton (e.g., Lough, 2010).

PERSPECTIVES ON CORAL GROWTH

189

Figure 2. (a) X-ray positive print of top 50-cm section of Porites coral core slice from Tantabiddi Reef, Western Australia (AIMS ID ⫽ TNT03BS2), collected in October 2008, showing unusual density band in 1998; (b) X-ray positive print of 65-cm section of Porites coral core slice from Thevenard Island, Western Australia (AIMS ID ⫽ THV01BS3), collected in October 2008, showing growth disruption in 1958; and (c) digitally enhanced photograph of top 46-cm section of Porites coral core slice from Pandora Reef, GBR (AIMS ID ⫽ PAN37AS2) collected in August 2012. Image illustrates annual luminescent lines of varying intensity.

Here, we focus on measurements of calcification rates obtained from annually banded massive coral skeletons. We present an updated perspective (see earlier reviews of Lough, 2008b; Lough and Cooper, 2011) on what long-term measures of coral growth, obtained from annually banded massive coral skeletons, are telling us about life in a changing ocean. We first describe the types of growth records that can be obtained from massive corals and how they are measured; we then review recent studies documenting temporal variations in coral calcification rates. We conclude with some recommendations on maximizing the usefulness of these natural coral reef growth archives for understanding coral reefs in a changing ocean. Measuring Growth Records in Massive Coral Skeletons The use of coral skeletal characteristics for environmental hindcasting and ecological analysis is a challenging field with substantial promise but elusive answers, many of which may have to wait for an improved understanding of calcification mechanisms and their external control. Buddemeier and Kinzie (1976).

The discovery of seasonal variations in skeletal density in certain massive coral species, as revealed by X-radiography (Knutson et al., 1972), provides an annual chronology that can be used to retrospectively measure coral growth rates, often over several centuries. These annually and sub-annually resolved variations in skeletal architecture also provide

the basis for extracting a wealth of proxy environmental information for the tropical oceans from various geochemical tracers whose incorporation into the skeleton is mediated by ambient seawater characteristics (Lough, 2010). These, in turn, contribute to the global jig-saw puzzle of past climate variability and change (e.g., from tree rings, ice cores, documentary records) that predates instrumental climate records (Jones et al., 2009). Coral growth records are also part of a suite of aquatic biochronologies (i.e., generated from hard parts of fish, molluscs, and corals) that can provide long-term ecological insights into the impacts of environmental changes in marine and freshwater environments (Morrongiello et al., 2012). The basic tool for examining coral growth rates is an X-ray of a slice (typically 5–7-mm thick) taken along a major growth axis from a coral core or colony. Positive prints of X-rays reveal the annual pattern consisting of alternating high- and low-density bands. Knowing the date of collection of the sample, each year can be dated backward through time. Visual assessment of such images can also reveal dateable “events” recorded during skeletal growth (“stress bands”; Hudson et al., 1976). A coral from Tantabiddi Reef, Western Australia, for example, shows extremely regular increments of growth within the annual density banding pattern (Fig. 2a) dating back to 1832. The single hiatus in this coral’s growth occurred in 1998 and is linked to the major thermal stress event that affected many of the world’s coral reefs, leading to mass coral bleaching

190

J. M. LOUGH AND N. E. CANTIN

and mortality (Wilkinson, 1998). That the 1998 thermal anomaly is the only event that appeared to disrupt growth in this coral during 177 years of continuous growth tells us something about the benign nature of this coral’s environment during most of its life and underlines the unprecedented nature of the 1998 event. Not all corals, however, show such regular annual density banding. A coral from Thevenard Island (Fig. 2b) shows highly contorted annual density bands (which make annual measurements difficult to obtain accurately) that are typical of corals growing in turbid waters and a major growth disruption that significantly altered the major growth axis of the colony. This event is most likely a result of the close passage of an unnamed Category 4 tropical cyclone in March 1958 (Australian Bureau of Meteorology, http://www.bom.gov.au/ cyclone/history/). X-rays such as these reveal the annual density bands averaged through the thickness of the coral slice and thus help guide measurements of coral growth parameters as well as optimum sampling tracks for geochemical analyses (Lough, 2010). Another way that coral growth can be visualized is when slices from inshore corals in certain locations—for example, Great Barrier Reef (GBR), Australia (Lough et al., 2002); East Africa (Fleitmann et al., 2007); Madagascar (Grove et al., 2010)—are viewed under ultra-violet light. Such images (Fig. 2c) reveal annual luminescent lines of varying intensity that are directly related to the occurrence and intensity of freshwater flood events affecting nearshore coral reefs. The summer wet season of 1991 in northeast Queensland, for example, experienced exceptionally high rainfall: the adjacent Burdekin River achieved an annual flow of 40.3 km3, which was recorded in the coral as a very intense luminescent line. This contrasts with the faint luminescent line of 1996 when Burdekin River flow totaled only 2.3 km3, compared to its long-term median flow of 6.0 km3. Luminescent lines are considered to result from incorporation of humic acids from adjacent catchment soils into the coral skeleton (Boto and Isdale, 1985; Llewellyn et al., 2012) and appear to be most useful on reefs adjacent to land areas with highly seasonal rainfall regimes (Scoffin et al., 1989). As well as being used in their own right—for example, to reconstruct rainfall and river flow (Grove et al., 2010; Lough, 2011)—luminescent lines can also help with dating the annual density bands on inshore reefs and those from occasional large flood events that reach mid-shelf reefs (1 in every 3–5 years on the GBR; Hendy et al., 2003). Obtaining annual measures of coral calcification rates from massive coral skeletons involves (1) dating of the annual growth increments, (2) measuring annual linear extension rates (i.e., how much the coral is extending outward each year), and (3) measuring annual skeletal density. Annual coral calcification is then calculated as the product of linear extension and skeletal density. Ideally, all three growth variables should be obtained to identify growth

characteristics of different massive species in different locations because skeletal density and calcification rates are directly related to the extension rate of the individual colony (Dodge and Brass, 1984; Lough and Barnes, 2000). Linear extension is the most common, and sometimes the only, measurement of coral growth undertaken because it can be measured directly from X-radiographic images. The bandwidth is defined as the linear distance between equivalent points on adjacent density bands; for example, the top or start of a high-density band (Aller and Dodge, 1974; Carricart-Ganivet et al., 2000). Linear extension has also been measured directly from images of luminescent lines (D’Olivo et al., 2013; Tanzil et al., 2013) and from highresolution geochemical sampling of the coral skeleton (e.g., ␦18O; Stortz and Gischler, 2011), though these approaches are rare. More commonly, linear extension is now obtained from continuous measures of skeletal density along a core slice. Such measures can be obtained from X-ray densitometry whereby the X-ray image is scanned, along with appropriate CaCO3 standards and corrections for the “heel effect” (Chalker et al., 1985), to derive absolute skeletal density (Helmle and Dodge, 2011). Skeletal density can also be measured continuously along a coral slice by gamma densitometry (Chalker and Barnes, 1990; Draschba et al., 2000) and by computerized tomography (CT) scanning of either a coral slice or a completely intact core (Logan and Anderson, 1991; Bosscher, 1993; Bessat and Buigues, 2001). Comparable skeletal density measurements have been reported from gamma and X-ray densitometry of the same coral slices (e.g., Carricart-Ganivet and Barnes, 2007; Tanzil et al., 2013). CT scanning has a distinct advantage over 2-dimensional gamma or X-ray densitometry in that it can be undertaken on the whole coral core, and optimum growth axes for density measurements can be freely chosen and manipulated from the digital images throughout the length of the coral core (Fig. 3; Saenger et al., 2009; Cantin et al., 2010; Carilli et al., 2012). Although some flexibility in track selection is possible with X-ray densitometry (Helmle et al., 2002), this is not possible with gamma densitometry: obtaining continuous skeletal density measures along a maximum growth axis is rarely achieved due to the often convoluted architecture of coral colonies (e.g., Lough and Barnes, 1992). Annual linear extension rates can then be extracted from continuous measurements of density versus distance (obtained by X-ray, gamma or CT densitometry) as the linear distance between equivalent points of the annual bands (e.g., annual density minima or maxima; see fig. 3 in Lough and Cooper, 2011). Skeletal density has also been measured by the water displacement technique (e.g., Brown et al., 1990; Carricart-Ganivet et al., 2000; D’Olivo et al., 2013). This typically involves excision of 1–5 years of coral growth and depends upon precise identification of the annual growth bands. Given the more widely available techniques for continuously measuring

PERSPECTIVES ON CORAL GROWTH

191

Figure 3. Example analysis of annual coral growth from 3D computed-tomography (CT) scanning. (a) 3D volume reconstruction of an intact Diploastrea heliopora core; (b) virtual slice of the D. heliopora core (2.5-mm thickness) that follows the absolute maximum growth axis along the entire length of the core; (c) 3D volume reconstruction of an intact Porites spp. core; and (d) virtual slice of the Porites spp. core (5-mm thickness) that follows the absolute maximum growth axis along the entire length of the core.

skeletal density along long coral cores, this approach is not often used. Finally, once measures of linear extension and skeletal density have been obtained, the annual calcification rate (mass of CaCO3 skeleton deposited per year, g䡠cm⫺2䡠y⫺1) can be calculated. It should be noted that the three growth variables (linear extension, density, and calcification) are inter-related but that this relationship varies with species. For the commonly used Indo-Pacific massive coral, Porites, there is a significant inverse relationship (r2 ⫽ 0.57) between skeletal density and extension, with faster extension rates associated with less dense skeleton. Skeletal density is significantly, but weakly, inversely related to calcification (r2 ⫽ 0.35), with linear extension rates being the primary driver of variations in calcification rates in Porites (r2 ⫽ 0.94) (Lough, 2008b). In contrast, for the commonly used Atlantic massive species, Montastrea, although linear extension is also inversely related to skeletal density (r2 ⫽ ⬃0.74), extension and calcification are inversely related (r2 ⫽ ⬃0.38), and it is skeletal density that is the primary driver of variations in calcification rate (r2 ⫽ ⬃0.86) (Carricart-Ganivet, 2004). There has, to date, been little exploration of the relationships between these three growth variables in other massive coral species with annual density bands, for example, Siderastrea and Diploastrea. One of the problems when Buddemeier and Kinzie (1976) reviewed the then-current understanding of coral growth rates was the wide range of techniques used to determine coral growth. At least for annually banded mas-

sive corals, we are now in a better position to undertake comparisons of comparable measures of growth rates across different species, reef environments, and time. We review these sources of variability in massive coral growth rates in the following sections, focusing on studies that have derived measures from annual density bands. Variations in Coral Growth Rates with Species and Record Lengths Coral growth rates, as revealed by density banding, vary with species (Weber et al., 1975). Linear extension rates of the most commonly measured Indo-Pacific massive coral, Porites spp., are typically about 10 –15 mm䡠y⫺1 (Lough et al., 1999) but with values ranging from about 4 mm䡠y⫺1 in the marginal reef environment of Hong Kong (Goodkin et al., 2011) to about 25–30 mm䡠y⫺1 at Lihir Island in the Western Pacific Warm Pool (Lough, 2008b). The Atlantic/ Caribbean massive coral, Porites astreoides, tends to grow more slowly at about 3–5 mm䡠y⫺1 (Elizalde-Rendon et al., 2010). Linear extension rates for the most commonly measured Caribbean/Atlantic massive coral, Montastrea spp., are typically about 8 –10 mm䡠y⫺1 (Carricart-Ganivet, 2004). Massive Diploastrea heliopora, which occurs throughout the Indo-Pacific, has relatively slow growth rates with linear extension rates of about 2– 6 mm䡠y⫺1 (Bagnato et al., 2004; Damassa et al., 2006; Cantin et al., 2010). Another slowgrowing Atlantic/Caribbean massive coral species is Siderastrea with linear extension rates of about 2– 8 mm䡠y⫺1

192

J. M. LOUGH AND N. E. CANTIN

(Gischler and Oschmann, 2005; Castillo et al., 2011; Vasquez-Bedoya et al., 2012). The Indo-Pacific massive coral, Platygyra spp., has been less commonly used in growth band studies but has reported linear extension rates between 5 and 17 mm䡠y⫺1 (Weber and White, 1974; Quinn et al., 1993; Shimamura et al., 2008). To assess how coral growth rates may be responding to a changing ocean environment requires long-term records that, ideally, predate human interference on coral reefs. The longest reported continuous growth records include annual linear extension for a Sidereastrea siderea coral core from the Bahamas, which starts in 1552 (Saenger et al., 2009), and annual linear extension for a Pavona coral core from the Galapagos, which starts in 1587 (Dunbar et al., 1994). A “window” of stable oxygen isotope and skeletal density records, 1350 –1630, was obtained from a Diploria spp. coral core from Bermuda by Draschba et al. (2000). These authors also refer to an 800-year record of linear extension rate obtained from a Montastrea cavernosa coral core, also from Bermuda (Pa¨tzold et al., 1999). Such long records tend, however, to be rare and, although valuable, almost exclusively come from a single coral colony. Although large and old corals do occur with records dating back to the 16th century (e.g., Fig. 4a for the GBR), the earliest the majority of growth records tend to start is the mid-late 19th century (e.g., Fig. 4b for Western Australian coral reefs). There are, however, a number of long geochemical records obtained from massive corals for which growth and calcification rates are rarely reported (Fig. 4c). Given evidence that coral growth rates and skeletal characteristics can modulate the environmental signal in geochemical tracers, such as Sr/Ca ratios as a proxy for sea surface temperature (SST) (Delong et al., 2012; Grove et al., 2013) and ␦18O as a proxy for SST and salinity (Felis et al., 2003; Maier et al., 2004), it is worth considering that coral growth rates should be routinely measured when undertaking all such analyses. This would substantially increase the availability of measured long-term growth rates from massive corals. The variability in coral growth rates among corals, even from the same reef (e.g., Lough et al., 1999), means that the most reliable growth histories for assessing coral responses to environmental gradients and through time must be based on multiple coral samples. This is true for all sources of proxy climate/environmental information (Jones et al., 2009), not just corals (Lough, 2004). Coral Growth Rates Across Environmental Gradients Fundamental to coral growth history analysis (sclerochronology) is the premise that coral growth rates are influenced by changes in the environment. Growth rate increases to an optimum level when conditions are most favorable and conversely declines when conditions are poor. Hudson et al. (1982).

Figure 4. Percentage of coral records starting within each 50-year period for (a) 55 Great Barrier Reef coral growth records (Dea’th et al., 2009); (b) 52 Western Australian coral reefs coral growth records (AIMS Coral Core Archive); and (c) 53 global geochemical coral records (NOAA Paleoclimatology Data Base; http://www.ncdc.noaa.gov/data-access/paleo climatology-data/datasets/coral-sclerosponge.

In measuring, comparing, and interpreting coral growth rates, it is important to recognize that average growth characteristics vary across environmental gradients. Water depth, for example, clearly mediates the amount of light available to corals, and the published literature (see Lough and Cooper, 2011) indicates that linear extension and calcification rates tend to decrease with increasing water depth, whereas skeletal density increases. Optimal coral growth rates in massive coral species occurs at a water depth of about 10 m.

PERSPECTIVES ON CORAL GROWTH

193

Figure 5. Annual average Porites calcification rate vs. annual average sea surface temperature for 49 Indo-Pacific sites (gray diamonds; Lough, 2008b). Dashed line is linear regression for these 49 sites. Data also shown for Hong Kong (green triangle; Goodkin et al., 2011; calcification rate estimated from strong linear relationship between Porites linear extension and calcification rate (see Lough, 2008b)), 6 reef sites in the Thai-Malay peninsula (blue triangles; Tanzil et al., 2013), 4 sites in Indonesia (dark green triangles; Edinger et al., 2000), 1 reef site in the South China Sea (purple triangle; Shi et al., 2011), Milne Bay, Papua New Guinea (orange triangles; Fabricius et al., 2011), and for 7 reef sites in Western Australia (red triangles; Cooper et al., 2012).

Another important environmental gradient reflected in coral growth characteristics relates to proximity to terrestrial versus open-ocean influences. In their review, Lough and Cooper (2011) reported variable responses to inshoreoffshore gradients, with some corals growing faster in inshore waters while others grew faster in offshore locations. They suggested that these different responses might reflect additional environmental controls that are not well constrained, such as wave action, light, nutrient upwelling, and sediments. The commonly used Indo-Pacific massive coral, Porites, is also notable for its ability to grow in a wide range of reef environments. The marginal and apparently inhospitable environment for coral growth in Hong Kong waters, for example, supports colonies that have grown over at least 200 years, albeit with very low growth rates (Goodkin et al., 2011). Progressive acidification of the oceans and reef waters is expected to increasingly compromise calcification and thus reef growth over time. There are a few “natural laboratories” where coral reefs grow in proximity to low pH waters and where the spatial gradient in ocean acidification can be compared with in situ massive coral growth rates. At Milne Bay, Papua New Guinea, where CO2 seeps from the sea floor, Fabricius et al. (2011) found no significant differences in massive Porites calcification rates between sites at normal aragonite saturation states and those where aragonite saturation is comparable to that expected by the end of this

century if the current levels of anthropogenic CO2 emissions are maintained. Although hard coral cover showed little change, species diversity declined dramatically between control and low pH sites, with loss of the structurally complex, fast-growing corals and the simpler, slower-growing massive Porites being virtually the only hard coral species occurring at the low pH sites. This suggests that calcification rates in massive Porites may be relatively insensitive to ocean acidification; a finding supported by some experimental studies (e.g., Edmunds et al., 2012). In contrast, however, Crook et al. (2013) reported a significant decrease in skeletal extension, density, and calcification of Porites astreoides along a natural gradient in pH and aragonite saturation on the Caribbean coast of the Yutacan Peninsula. There is abundant evidence that average SST is a major environmental control on both coral reef distribution (Kleypas et al., 1999a) and coral growth rates, as measured in annually banded massive corals. Massive Porites calcification rates tend to increase by about 0.3 g䡠cm⫺2䡠y⫺1 for each 1 °C increase in SST, based on multiple shallow-water coral samples from 49 Indo-Pacific reefs (r2 ⫽ 0.85) growing across a temperature range from about 23–30 °C (grey diamonds in Fig. 5; Lough and Barnes, 2000; Lough, 2008b). As calcification rates in Porites are primarily driven by linear extension rates, there is a similar strong and significant relationship between average linear extension

194

J. M. LOUGH AND N. E. CANTIN

and average SST (r2 ⫽ 0.84), with extension increasing by about 3 mm䡠y⫺1 for each 1 °C increase in SST. Linear extension rates of Platygyra corals are also significantly related to average SST (r2 ⫽ 0.79) across a temperature range of about 24 –29 °C, based on samples from 21 shallow-water Indo-Pacific sites. Linear extension in Platygyra increases by about 1 mm䡠y⫺1 for each 1 °C increase in SST (Weber and White, 1974; reanalysed by Lough and Cooper, 2011). For Montastrea annularis in the western Atlantic, Carricart-Ganivet (2004) found that average calcification rates increased by about 0.6 g䡠cm⫺2䡠y⫺1 for each 1 °C increase in SST. As calcification in Montastrea is primarily driven by changes in skeletal density, this increase in calcification rate with SST was also associated with a significant increase in skeletal density, while linear extension tended to decrease in warmer waters. It would be useful to examine these relationships between average coral growth rates and SST for other commonly used massive coral species such as Sidereastrea siderea, whose growth rates appear to vary inversely with SST, at least over time (e.g., Saenger et al., 2009; Vasquez-Bedoya et al., 2012). The strong linear relationship between average Porites calcification rates and average SST can also be used to assess whether corals are performing as expected in different reef environments in order to identify locations where SST is the dominant driver of calcification. This is illustrated for several recent studies by the colored triangles in Figure 5. Average calcification rates at eight reef sites off Western Australia between 17° and 28°S (red triangles; Cooper et al., 2012) generally conform with the expected relationship except for the two most southerly sites (Coral Bay and the Houtman Abrolhos), where calcification rates are significantly higher than expected based on average SST. This “over-achievement” suggests that other factors, including efficient light utilization and water clarity, are providing sufficient energy from photosynthesis to support above-average carbonate production at these, the most southerly reefs in the Indian Ocean (Smith, 1981). In contrast, Porites calcification rate (estimated from reported linear extensions rates) in the marginal reef environment of Hong Kong are very close to that expected for this thermal environment (green triangle; Goodkin et al., 2011). Similarly, average calcification rates at four reef locations on the Thai-Malay Peninsula are calcifying at expected rates (light blue triangles), but two (dark blue triangles) are not (Tanzil et al., 2013). These are reefs near Port Dickson and Singapore, on the south/southwest coast of the Thai-Malay Peninsula, where local influences may be lowering average calcification rates. Average calcification rates are also substantially below expected rates at the isolated Meiji Reef in the South China Sea (purple triangle; Shi et al., 2011). Average calcification rates are below expected at four reef sites in Indonesia where Porites growth rates were considered to be insensitive to sources of pollution (green trian-

gles; Edinger et al., 2000). Although Fabricius et al. (2011) found no effect of lowered pH on massive Porites calcification rates at a natural CO2 seep site in the warm waters off Papua New Guinea (PNG), average calcification rates at both control and impacted sites were about 30% lower than expected (orange triangles). They suggest that these low average calcification rates may be similar to recently reported declines in coral calcification (see next section) as, over the recent 12-year period common to the cores they examined, 9 years had summer maximum SSTs greater than the long-term average: that is, temperature stress, the thermal optimum, or both may already have been exceeded at this location.

Evidence for Recent Changes in Coral Calcification Rates? Given the strong dependence of average calcification rates on average SST, is it likely that calcification may, at least initially, increase as the oceans warm, as suggested by Lough and Barnes (2000)? Or are we seeing evidence that corals may have exceeded their thermal optimum or are experiencing setbacks in growth as a result of mass coral bleaching events? Current linear projections of ocean acidification are based on data collected from open-ocean environments (Doney et al., 2009; Zeebe, 2012). Seasonal and diurnal variation in pCO2 is relatively small in open-ocean environments (⬃40 –50 ␮atm; Bates et al., 1996; Doney et al., 2009), which makes long-term trends in ocean pCO2 obvious (increasing from 280 to 390 ppm from 1960 to 2010; Doney et al., 2009). Conversely, coral reefs exhibit much larger fluctuations in carbonate chemistry on diurnal and seasonal timescales (⬃250 –300; Bates et al., 2010; Shamberger et al., 2011; Albright et al., 2013) with extreme fluctuations of up to 900 ␮atm (Shaw et al., 2012), which makes understanding the susceptibility of coral reef ecosystems to ocean acidification projections more complex due to this large background variability. Here we review recent studies that have examined temporal variations in coral growth rates obtained from annually banded massive corals. We focus on studies that examine continuous time series of annual growth. This excludes a few discontinuous studies in which coral growth rates have been “re-sampled” in recent years and compared to earlier published growth rates (e.g., Bak et al., 2009; Tanzil et al., 2009; Manzello, 2010), though these studies all found evidence for lower growth rates for some species and some locations when measurements made in the 2000s were compared with those in the 1970s and 1980s. We also focus on studies that have calculated growth rates across multiple coral samples rather than a single coral (e.g., Bessat and Buigues, 2001; Saenger et al., 2009; Stortz and Gischler, 2011).

PERSPECTIVES ON CORAL GROWTH

Coral Growth Responses to Mass Coral Bleaching Events During the 1997–1998 El Nin˜o event, the tropical oceans were the warmest in the observational record period (Fig. 1), resulting in major thermal stress anomalies (Eakin et al., 2009) and mass coral bleaching throughout most of the world’s coral reefs (Wilkinson, 1998). For at least one coral in the eastern Indian Ocean, this was the only event that disturbed its regular pattern of annual density banding in 177 years of continuous growth (Fig. 2a). Are major bleaching events recorded in coral growth records from other coral reefs? The majority (95%) of 92 Montastrea faveolata core slices from four Mesoamerican Reef sites showed visual evidence on X-rays of a high-density stress band associated with the 1998 bleaching event (Carilli et al., 2009). Only three stress bands were evident in individual coral cores prior to 1998 in records back to the 1950s, and none of these were coincident among different samples. The majority of the coral cores also showed a marked decrease in linear extension rates and an increase in skeletal density after the 1998 thermal stress event. Recovery of pre-1998 linear extension rates occurred after 2 years at two sites not subject to chronic local stress, whereas recovery had not occurred after 8 years (when the cores were collected) at two sites subject to high chronic local stress (as measured by sediments, nutrients, population size, and fishing pressure). Longer term perspectives on these findings, based on growth records 75–150-years-long (Carilli et al., 2010), show that the 1998 event was unprecedented in at least the past century. They also confirmed that the magnitude of the impact of the 1998 event on coral growth was mediated by chronic local stressors lowering the thermal tolerance levels (see Wooldridge, 2009, for the GBR). The 1998 thermal stress event also had a major impact on growth of apparently healthy Diploastrea heliopora colonies in the Red Sea. Cantin et al. (2010) found a 30% decrease in a replicated record of linear extension from 1998 to 2008 compared with 1925 to 1997 averages. Although an earlier thermal stress event (1941– 42) was recorded in the corals, normal growth rates recovered within 3 years. These corals are now growing in a substantially warmer environment than previously, and the authors suggest that their sustained lower growth rates since 1998 likely reflect that they have now exceeded their optimum SST for growth of less than 30.5 °C. The 1998 thermal stress event also left its signature in massive Porites colonies of the GBR, Australia. D’Olivo et al. (2013) found a reduction in linear extension rates of about 40% for Porites from three nearshore reefs in the central GBR. Reduced growth was followed by recovery to pre-1998 rates within 2–3 years. They did not find a decline in growth at one offshore and two mid-shelf reef sites.

195

Cantin and Lough (2014) examined the evidence for growth hiatuses and growth changes in multiple coral cores from inshore, midshelf, and offshore reef sites of the central GBR over the common period, 1980 –2003. This period encompassed 1998 and 2002 when the GBR experienced mass coral bleaching with 42% and 54% of reefs, respectively, affected to some extent (Berkelmans et al., 2004). Cantin and Lough (2014) found that the corals showed various growth signatures associated with coral bleaching, including high-density stress bands, partial mortality, and an abrupt decrease in linear extension and calcification rates. The occurrence and magnitude of these growth responses varied between reef sites (e.g., visual hiatuses were most evident in inshore corals in 1998 and in midshelf corals in 2002) and between the two thermal stress events (e.g., the inshore corals showed markedly fewer growth anomalies in 2002 compared to 1998). They also found reduced calcification rates of about 13%–18% on two inshore reefs due to the 1998 bleaching event; these recovered to pre-1998 rates within 4 years. A major thermal stress event affected the Gilbert Islands (Kiribati) in the central equatorial Pacific in 2004. Examination of annual growth in multiple Porites cores from three reef locations showed that the site with the lowest background SST variability experienced the greatest impact on growth, with about 30% of sampled corals showing partial mortality and a marked decline (⬃45%) in linear extension and calcification rates (Carilli et al., 2012). Two sites, which experience greater inter-annual SST variability, showed no partial mortality in 2004 and only about 20% reduction in linear extension and calcification. The authors suggest, from this analysis of growth records in massive corals, that higher background thermal variability confers greater resistance to thermal stress events. Exceeding Their Thermal Optimum—Is Coral Growth Slowing? The levels of background SST and environmental variability have also been reported to affect the magnitude of coral growth responses for Siderastrea siderea corals from the Mesoamerican Barrier Reef System (Belize). By analyzing linear extension rates in multiple samples across an inshore-to-offshore gradient, Castillo et al. (2011, 2012) found a significant decline between 1920 to 1934 and 1995 to 2008 only at the exposed forereef site; over the same time period, the backreef and nearshore sites had relatively constant extension rates. The authors suggest that these differences in growth rates through time are a result of the forereef corals living in a cooler and more thermally stable environment compared to the backreef and nearshore sites. Over the recent period,1982 to 2008, extension in the forereef corals significantly declined as summer SST and degree heating months increased; this was not found for the inshore

196

J. M. LOUGH AND N. E. CANTIN

and backreef corals. The authors conclude that corals from the more variable environments of the inshore and backreef are more thermally tolerant than those of the forereef, with the latter now showing a decline in growth rates associated with SST warming and likely to be more sensitive to future global warming. That some sort of tipping point for massive coral calcification has been reached, in which coral calcification decreases rather than increases with ongoing ocean warming, is also supported by the study of Carricart-Ganivet et al. (2012). They report significant inverse relationships between recent calcification rates and SST for Porites spp. (from one location in the central GBR) and P. astreoides, M. Faveolata, and M. franski (from two locations in the Mesoamerican Barrier Reef System). They conclude, on the basis of relatively short records (⬃8 –27 years), that Porites spp. are more sensitive to further SST warming than Montastrea spp., with declines in calcification per 1 °C increase of 0.40 g䡠cm⫺2䡠y⫺1 and 0.12 g䡠cm⫺2䡠y⫺1, respectively. There have been several studies of temporal variations in Porites growth rates on the GBR, Australia. A 10-coral average calcification series, 1746 –1982, was interpreted as a proxy for SST and showed substantial variability on decadal time scales (Lough and Barnes, 1997). The authors suggested that “interpretation of a recent decline in growth along the Great Barrier Reef should take into account similar declines and recoveries over the past several hundred years.” The authors also emphasized potential problems in accurately measuring annual growth variables in Porites due to skeletal architecture and favored examining data at 5–10-year timescales. Subsequently, Lough and Barnes (2000) demonstrated that the temporal relationship between SST and Porites calcification was evident spatially and extended across the wider Indo-Pacific (i.e., average conditions, see Fig. 5). They also suggested that, at least initially, calcification rates may increase as the oceans warm. In support of this prediction, they showed that long-term calcification rates (based on 10-coral average series) were stable over the 50-year periods 1780 –1829, 1830 –1879, and 1880 –1929, but that there was a significant (4%) increase from 1880 –1929 to 1930 –1979 that matched the observed warming of about 0.25 °C of GBR SST between the same two time periods. That recent Porites growth rates on the GBR might be declining was first reported by Cooper et al. (2008) on the basis of 10 colonies from two nearshore locations in the northern GBR. Over the 16-year period 1988 –2003, they found a decrease in calcification rates of about 20% associated with a decline in linear extension of about 16% and a decline of only 6% in skeletal density. They also demonstrated the nonlinear effect of annual SST on calcification, with maximum calcification occurring at about 26.7 °C—very close to the optimum value determined experimentally by Jokiel and Coles (1978) and Marshall and Clode (2004). Cooper et al. (2008) suggested their findings

were consistent with the expected combined effects of warming and acidification on coral growth, but they did not directly attribute either of these factors to the observed decline. A significant linear decrease in calcification rates between 1961–1965 and 2001–2005 was reported for Porites from an inshore and offshore reef (⬃15% and 10%, respectively) of the central GBR and no significant change in a midshelf reef (Lough, 2008b); however, there was a decline in the two most recent 5-year periods that would match that reported by Carricart-Ganivet et al. (2012) for the same reef. The observed declines in calcification did not match the estimated increase of about 12%–13% expected on the basis of calcification responding positively to observed SST rise. In a statistically robust analyis (allowing for the imbalanced spatial and temporal coverage) of up to 328 Porites growth records from 69 reefs throughout the GBR, De’ath et al. (2009) found that although calcification initially increased over the 20th century (see Lough and Barnes, 2000), there had been a significant decline from 1990 to 2005. This decline was primarily driven by changes in linear extension and appeared to be unprecedented in at least the past 400 years. The magnitude of the decline (14%) has recently been updated (to allow for identified errors in some final year band widths) to 11%, but it is still statistically significant (De’ath et al., 2013). Again, the authors could not specifically attribute the cause of the decline to ocean warming, acidification, or both, but they did rule out a variety of local factors such as coastal water quality. Although apparently criticizing the findings of De’ath et al. (2009), D’Olivo et al. (2013), examining growth rates in inshore-to-offshore reefs of the central GBR, concluded that inshore growth rates have significantly declined (which they attribute to declining water quality) and that midshelf and offshore growth rates “appear to be undergoing a transition from increasing to decreasing rates of calcification, possibly reflecting the effects of CO2-driven climate change.” Turning to the scattered coral reefs off the Western Australian coastline, Cooper et al. (2012) presented calcification rates, for the common period 1900 –2010, for 27 Porites cores from six reef sites between 17° and 28°S. Averaged across all sites, although SST had significantly warmed, there was no significant change in calcification rates. Rates of SST warming varied, however, between sites, being only about 0.02 °C/decade in the most northerly reef sites (Rowley Shoals) and up to 0.10 °C/decade at the most southerly (Houtman Abrolhos) reef. When examined by location, the rate of change in calcification appeared to match the rate of SST warming, with only small changes in calcification rates in areas of small change in SST and larger increases in calcification rates at the two most southerly reefs where warming has been greatest. These two sites (highlighted in Fig. 5) have unusually high average calcification rates for their relatively cool water location. That Porites calcification has increased here suggests that temperature has been

PERSPECTIVES ON CORAL GROWTH

the limiting factor in coral calcification. This study further supports the notion that coral calcification rates are currently responding to rates of change in tropical SST and that marginal reefs in the southeast Indian Ocean have been able to take advantage of the warming observed to date. As the authors note, whether such increases in calcification are sustainable is debatable, especially given the observed thermal stress event that impacted Western Australia coral reef ecosystems and resulted in significant coral bleaching in 2011 (Wernberg et al., 2012; Feng et al., 2013). Declines in massive Porites growth rates have also recently been reported for very warm-water (⬎28.5 °C) reefs surrounding the Thai-Malay peninsula (Tanzil et al., 2013). On the basis of analyses of 70 colonies from six locations, a region-wide decline of about 19% in calcification, 15% in linear extension, and about 4% in skeletal density occurred between 1980 and 2010. The authors also note variability in growth responses, with one site not showing a decrease. They also find at these warm water sites that the thermal threshold, beyond which calcification rates have declined, is about 29.4 °C. At Meiji Reef in the South China Sea, combined Porites growth records from 14 colonies, although showing variability between samples, suggest that calcification initially increased in the 20th century but has declined in recent decades (Shi et al., 2011). Porites calcification rates have also been reported to have decreased in the Arabian Gulf between 1987–1990 and 1999 –2002 (Poulsen et al., 2006) and at Misima Island, PNG, between 1984 –1988 and 1989 – 1993 (Barnes and Lough, 1999). Rates of decline in observed massive coral calcification rates appear to be linked to rates of SST warming, with evidence that the thermal optimum for sustained calcification has been exceeded in some locations. Clearly the time period studied and whether SST has warmed need to be taken into consideration. Helmle et al. (2011), for example, examined Montastrea annularis growth rates in the Florida Keys. Over their study period, 1937–1996, there was no long-term increase in SST at this site, and they found a significant decrease in density, a significant increase in extension rate, but no significant change in calcification rate. Noting the high variability of coral growth parameters, they also considered decadal changes. They found no significant difference in extension and calcification between the first and last decades of their study period, that is, 1937–1946 and 1987–1996. They also modeled the change in aragonite saturation state over their study period; it showed a decline of about 15% and is significantly correlated with the decline in skeletal density. The authors are, however, cautious in linking this change in skeletal density to ocean chemistry. One explanation for the outcomes of this study is that the environmental changes at the study site over the study period have not yet reached the critical thresholds necessary to affect coral calcification rates.

197

Growth declines due to local environmental changes Hudson et al. (1994) noted the “waxing and waning coral growth” over the period 1860 –1986 in M. annularis colonies from the Biscayne National Park, Florida. They found consistently lower growth rates after 1950 and suggested these may be related to local anthropogenic factors, especially nutrients affecting the reefs from sewage outfalls. Working with M. annularis from Barbados along a gradient of eutrophication, Tomascik (1990) showed a general pattern of decreasing linear extension in the 30 years up to 1983 (when the corals were collected) that was suggested to be linked to a gradual deterioration in water quality. Guzman et al. (2008), examining linear extension rates in 77 Siderastrea siderea cores, linked observed declines in coral growth up to 1990 (when an oil spill killed most large colonies) to activities associated with the construction of the Panama Canal and changes in adjacent land use. Using two published coral growth records from the western Caribbean, 1880 –2000, Kwiatkowski et al. (2013) highlight decadal variability, which they link to SST and solar radiation. The authors suggest that these variables, and hence coral growth variations, are responding to regional climatic drivers (e.g., volcanic and anthropogenic aerosols) rather than global-scale changes in greenhouse gases. Substantial decadal variability is also evident in linear extension rates obtained from three Siderastrea siderea coral cores from the Yucatan Peninsula, Mexico (Vasquez-Bedoya et al., 2012). Linear extension in this species is inversely correlated with SST (see also Saenger et al. 2009), and so a recent apparent decline in extension of these corals is linked to warming water temperatures. The presence of decadal climate variability can, however, disguise or hamper interpretation of recent trends in coral growth rates if the primary drivers of coral growth are being similarly modulated. Discussion and Recommendations For coral growth banding to be useful for environmental reconstruction, it is necessary to have a firm knowledge of the physiological processes of recent corals, how these processes are affected by environmental factors, and how, in turn, the environmental changes are recorded, if at all, in the coral skeleton. Dodge and Vaisnys (1979).

We know that the tropical ocean environment for coral reefs is already changing and becoming warmer and more acidic. These changes are highly likely to intensify over the coming century unless we move away from the high-emissions scenario we are currently tracking (Peters et al., 2013). Rapid calcification that withstands the natural forces of biological and physical erosion is fundamental to the maintenance of tropical coral reef ecosystems but will be increasingly compromised by warmer and more acidic waters. These global-scale stressors are superimposed, in many coral reef areas, by local sources of anthropogenic stress.

198

J. M. LOUGH AND N. E. CANTIN

Dateable, continuous, growth records, obtained from measurements of annually banded massive coral skeletons, are our only means for assessing past responses of calcification to environmental gradients and changes. Because most of the current ocean warming has occurred since about 1950 (Fig. 1), we can use baseline calcification rates from coral calcification histories prior to anthropogenic climate change as our target for a healthy coral reef ecosystem. Such understanding, in turn, contributes to determining possible futures for coral reef ecosystems in a changing ocean. Coral growth rates are, however, highly variable between corals, between species, within reefs, and over wider spatial scales. Some of this variability can be linked to environmental gradients, such as average water temperature and terrestrial versus oceanic influences. There is still an overarching question as to how calcification rates, measurable in certain massive coral species, relate to calcification rates of other coral species on reefs. An additional question is to what extent other measures of reef “health” (e.g., biodiversity, hard coral cover) are reflected in massive coral growth rates. Do in situ measurements of calcification and their spatial variations (e.g., Kuffner et al., 2013) reflect what would be measured in massive corals from the same sites? We still have only limited understanding of the process of calcification, how it is modulated under different environmental conditions, and how this is recorded in the subset of massive species on coral reefs that contain annual density bands. Despite these limitations, we have come a long way, since the annual nature of density bands was first identified (Knutson et al., 1972), in applying coral growth records to current issues for tropical coral reefs in a changing ocean. We have developed routine techniques for measuring linear extension, skeletal density, and calcification rates. We have learned not to rely on a single coral record and that multiple samples are necessary to characterize growth and its variability in a particular environment. We have identified temperature as a major environmental control on average coral calcification rates. We have also identified, though less clearly, other important environmental factors that modulate average rates of coral growth, such as light/depth and relative proximity to terrestrial versus oceanic influences. We have found that recent mass coral bleaching events do leave their signature in massive coral growth records and that the recent occurrence of these events appears unprecedented in the historical context provided by long-lived corals. These records also provide insights into the time it takes for corals to recover to their pre-stress growth rates and that this recovery period can be modulated by the influence of local environmental stressors. The severity of impact of recent thermal stress events on coral growth rates also appears to depend on the natural environmental variability of the reef, with corals from locations with lower historical thermal variability suffering more than those used to more variable

thermal environments. We also have evidence from several reef locations for a recent slowing of massive coral growth rates. The occurrence and rate of slowing appears, up to now, to be largely driven by the local rate of SST warming and is not, as yet, attributable to ocean acidification compromising the calcification process. Observed declines in coral growth likely reflect two types of responses to warmer ocean temperatures: setbacks in growth due to distinct thermal stress events, with recovery to pre-stress growth rates observed in some instances; and a general decline in growth as a result of the temperatures now persistently exceeding optimum values for growth. It is unclear, as yet, whether changes in ocean carbonate chemistry have contributed to observed temporal changes in growth rates within coral reefs. Baseline data about coral growth characteristics and their changes with environment and environmental variation is necessary to fully develop their application to retrospective monitoring of coral reef environments; comparisons are also needed between measures of coral performance obtained from skeletal growth histories and other measures of reef health. (Lough and Barnes, 1997).

We still have much to learn in our application of massive coral growth histories to understanding coral reefs in a changing ocean. So, finally we present some recommendations for enhancing this contribution: ●







The most consistent annual measurements (along major growth axes) of skeletal growth parameters are obtained with CT scanning with its inherent flexibility in choice of sampling tracks and capability of maintaining maximum vertical growth axes throughout the entire length of the intact volume of core. Cost-effective access to these relatively specialist facilities would greatly enhance the consistency, accuracy, and comparability of coral growth measurements. Temporal variations in coral growth parameters should be examined at sites that have historical and ongoing measurements of ocean chemistry such as HOT (Hawaii Ocean Time-Series, 2014); BATS (Bermuda Atlantic Time-Series Study, 2014); and now Heron Island (NOAA PMEL Carbon Program) on the GBR since 2010 http://www.pmel.noaa.gov/co2/story/Heron⫹ Island). There is much scope for linking observed growth hiatuses/partial mortality and annual growth rates with other measures of coral performance, for example, lipid content, tissue layer, tissue biomass before and after stress (Carilli et al., 2012; Thornhill et al., 2011), and reef health (e.g., hard coral cover, biodiversity). Improved understanding of massive coral growth responses to temperature and acidification can inform future models of the impacts of changes in these variables on coral growth and overall reef health (e.g.,

199

PERSPECTIVES ON CORAL GROWTH













Hoeke et al., 2011). Novel experimental comparisons of historical calcification records with calcification responses to future temperature and acidification conditions will greatly improve our understanding of the variability that has been observed in the calcification response to acidification. The value of high-resolution spatial SST data sets, compared to large-scale compilations, should be recognized as more accurately reflecting thermal environments experienced by corals (e.g., Castillo et al., 2012; Tanzil et al., 2013). Different measurement techniques (X-ray, gamma, and CT densitometry) should be compared (calibrated) on the same suite of corals. The advantage of using robust/tough massive species (e.g., Siderastrea, Porites, Montastrea) is that they are likely to continue growing through stressful conditions and hence leave a record compared to less robust species (Castillo et al., 2012). It is still essential, however, that we establish the relationship between growth in these massive species and other major frameworkbuilding coral species. We strongly encourage researchers who undertake geochemical analyses of coral records for climate/environmental reconstructions to also measure and report coral growth variables (at least linear extension rates), as this would greatly increase the spatial and temporal coverage of coral growth histories, at least back to the mid-19th century (Fig. 4). Coral calcification histories provide annual estimates of individual colony carbonate production. Our ability to predict the response of coral reef communities to future acidified ocean conditions depends upon a solid understanding of the rates of individual coral calcification that are required to develop and maintain coral reefs. Continued research efforts should seek to establish the link between individual calcification rates and net ecosystem calcification. Such an understanding will identify the attributes of a reef community that are required to resist the rates of dissolution and bioerosion that are predicted by the end of the 21st century. Creation of a global repository for all dated coral growth measurements, once published and of whatever length, would allow more robust determinations of environmental controls on coral growth rates and their responses as the environment changes. The Australian Institute of Marine Science, for example, currently lodges its published growth data in the AIMS data centre, which could be expanded to a global database. Alternatively, the paleoclimatology site at the NOAA National Climate Data Center (www.ncdc.noaa.gov/ data-access/paleoclimatology-data/datasets) or ReefBase (Global Information System for Coral Reefs)

(www.reefbase.org/main.aspx) might consider hosting such a database. Literature Cited Albright, R., C. Langdon, and K. R. N. Anthony. 2013. Dynamics of seawater carbonate chemistry, production, and calcification of a coral reef flat, central Great Barrier Reef. Biogeosciences 10: 6747– 6758. Aller, R. C., and R. E. Dodge. 1974. Animal-sediment relations in a tropical lagoon, Discovery Bay, Jamaica. J. Mar. Res. 32: 209 –232. Bagnato, S., B. K. Linsley, S. S. Howe, G. M. Wellington, and J. Salinger. 2004. Evaluating the use of the massive coral Diploastrea heliopora for paleoclimate reconstruction. Paleoceanography 19: doi: 10.1029/2003PA000935. Bak, R. P. M., G. Nieuwland, and E. H. Meesters. 2009. Coral growth rates revisited after 31 years: what is causing lower extension rates in Acropora palmata? Bull. Mar. Sci. 84: 287–294. Barnes, D. J., and J. M. Lough. 1999. Porites growth in a changed environment: Misima Island, Papua New Guinea. Coral Reefs 18: 213–218. Bates, N. R., A. F. Michaels, and A. H. Knap. 1996. Seasonal and interannual variability of the oceanic carbon dioxide system at the US JGOFS Bermuda Atlantic Time-series site. Deep-Sea Res. II 43: 347– 383. Bates, N. R., A. Amat, and A. J. Andersson. 2010. Feedbacks and responses of coral calcification on the Bermuda reef system to seasonal changes in biological processes and ocean acidification. Biogeosciences 7: 2509 –2530. BATS (Bermuda Atlantic Time-Series Study). 2014. Bermuda Institute of Ocean Sciences study. [Online]. Available: http://bats.bios.edu/ [2014, June 23] Berkelmans, R., G. De’ath, S. Kininmonth, and W. Skirving. 2004. A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns and predictions. Coral Reefs 23: 74 – 83. Berkelmans, R., A. M. Jones, and B. Shaffelke. 2012. Salinity thresholds of Acropora spp. on the Great Barrier Reef. Coral Reefs 31: 1103–1110. Bessat, F., and D. Buigues. 2001. Two centuries of variation in coral growth in a massive Porites colony from Moorea (French Polynesia): a response of ocean-atmosphere variability from south central Pacific. Palaeogeogr. Palaeoclimatol. Palaeoecol. 175: 381–392. Bosscher, H. 1993. Computerized tomography and skeletal density of coral skeletons. Coral Reefs 12: 97–103. Boto, K., and P. Isdale. 1985. Fluorescent bands in massive corals result from terrestrial fulvic acid inputs to nearshore zone. Nature 315: 396 –397. Brown, B. E., M. D. A. Le Tissier, T. P. Scoffin, and A. W. Tudhope. 1990. Evaluation of the environmental impact of dredging on intertidal coral reefs at Ko Phuket, Thailand, using ecological and physiological parameters. Mar. Ecol. Prog. Ser. 65: 273–281. Buddemeier, R. W., and R. A. Kinzie. 1976. Coral growth. Oceanogr. Mar. Biol. Annu. Rev. 14: 183–225. Cantin, N. E., and J. M. Lough. 2014. Surviving coral bleaching events: Porites growth anomalies on the Great Barrier Reef. PLoS ONE doi:10.1371/journal.pone.0088720. Cantin, N. E., A. L. Cohen, K. B. Karnauskas, A. M. Tarrant, and D. C. McCorkle. 2010. Ocean warming slows coral growth in the central Red Sea. Science 329: 322–325. Carilli, J. E., R. D. Norris, B. A. Black, S. M. Walsh, and M. McField. 2009. Local stressors reduce coral resilience to bleaching. PLoS ONE doi:10.1371/journal.poe.0006324. Carilli, J. E., R. D. Norris, B. Black, S. M. Walsh, and M. McField. 2010. Century-scale records of coral growth rates indicate that local

200

J. M. LOUGH AND N. E. CANTIN

stressors reduce thermal tolerance threshold. Glob. Change Biol. 16: 1247–1257. Carilli, J., S. D. Donner, and A. C. Hartmann. 2012. Historical temperature variability affects coral response to heat stress. PLoS ONE doi:10.1371/journal.pone.0034418. Carricart-Ganivet, J. P. 2004. Sea surface temperature and the growth of the West Atlantic reef-building coral Montastrea annularis. J. Exp. Mar. Biol. Ecol. 302: 249 –260. Carricart-Ganivet, J. P., and D. J. Barnes. 2007. Densitometry from digitized images of X-radiographs: methodology for measurement of coral skeletal density. J. Exp. Mar. Biol. Ecol. 344: 67–72. Carricart-Ganivet, J. P., A. U. Beltran-Torres, M. Merino, and M. A. Ruiz-Zarate. 2000. Skeletal extension, density and calcification rate of the reef building coral Montastraea annularis (Ellis and Solander) in the Mexican Caribbean. Bull. Mar. Sci. 66: 215–224. Carricart-Ganivet, J. P., N. Cabanillas-Teran, I. Cruz-Ortega, and P. Blanchon. 2012. Sensitivity of calcification to thermal stress varies among genera of massive reef-building corals. PLoS ONE doi:10.1371/ journal.pone.0032859. Castillo, K. D., J. B. Ries, and J. M. Weiss. 2011. Declining coral skeletal extension for forereef colonies of Siderastrea sidereal on the Mesoamercian Barrier Reef system, southern Belize. PLoS ONE doi: 10.1371/journal.pone.0014615. Castillo, K. D., J. B. Ries, J. M. Weiss, and F. P. Lima. 2012. Decline of forereef corals in response to recent warming linked to history of thermal exposure. Nat. Clim. Chang. 2: doi:10.1038/NCLIMATE1577. Chalker, B. E., and D. J. Barnes. 1990. Gamma densitometry for the measurement of skeletal density. Coral Reefs 9: 11–23. Chalker, B. E., D. J. Barnes, and P. J. Isdale. 1985. Calibration of x-ray densitometry for the measurement of coral skeletal density. Coral Reefs 4: 95–100. Cooper, T. F., G. De’ath, K. E. Fabricius, and J. M. Lough. 2008. Declining coral calcification in massive Porites in two nearshore regions of the northern Great Barrier Reef. Glob. Change Biol. 14: 529 –538. Cooper, T. F., R. A. O’Leary, and J. M. Lough. 2012. Growth of Western Australian corals in the Anthropocene. Science 335: 593–596. Crook, E. D., A. L. Cohen, M. Rebolledo-Vieyra, L. Hernandez, and A. Paytan. 2013. Reduced calcification and lack of acclimatization by coral colonies growing in areas of persistent natural acidification. Proc. Natl. Acad. Sci. 110: doi:10.1073/pnas.1301589110. Damassa, T. D., J. E. Cole, H. R. Barnett, T. R. Ault, and T. R. McClanahan. 2006. Enhanced multidecadal climate variability in the seventeenth century from coral isotope records in the western Indian Ocean. Paleoceanography 21: doi:10.1029/2005PA001217. De’ath, G., J. M. Lough, and K. E. Fabricius. 2009. Declining coral calcification on the Great Barrier Reef. Science 323: 116 –119. De’ath, G., K. E. Fabricius, H. Sweatman, and M. Puotinen. 2012. The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc. Natl. Acad. Sci. 109: 17995–17999. De’ath, G., K. Fabricius, and J. Lough. 2013. Yes— coral calcification rates have decreased in the last twenty-five years. Mar. Geol. 346: doi: 10.1016/j.margeo.2013.09.008. Delong, K. L., T. M. Quinn, F. Taylor, C.-C. Shen, and K. Lin. 2012. Improving coral-base paleoclimate reconstructions by replicating 350 years of coral Sr/Ca variations. Palaeogeogr. Palaeoclimatol. Palaeoecol. 373: 6 –24. Dodge, R. E., and G. W. Brass. 1984. Skeletal extension, density and calcification of the reef coral, Montastrea annularis: St. Croix, U.S. Virgin Islands. Bull. Mar. Sci. 34: 288 –307. Dodge, R. E., and J. R. Vasinys. 1979. Skeletal growth chronologies of recent and fossil corals. Pp. 493–517 in Skeletal Growth of Aquatic Organisms, D. C. Rhoads and A. Lutz, eds. Plenum Press, New York. D’Olivo, J. P., M. T. McCulloch, and K. Judd. 2013. Long-term

records of coral calcification across the central Great Barrier Reef: assessing the impacts of river runoff and climate change. Coral Reefs 32: doi:10.1007/s00338-013-1071-8. Done, T. J. 2011. Corals: environmental controls on growth. Pp. 281– 293 in Encyclopedia of Modern Coral Reefs, D. Hopley, ed. Springer, Dordrecht. Doney, S. C., V. J. Fabry, R. A. Feely, and J. A. Kleypas. 2009. Ocean acidification: the other CO2 problem. Annu. Rev. Mar. Sci. 1: 169 –192. Draschba, S., J. Patzold, and G. Wefer. 2000. North Atlantic climate variability since AD 1350 recorded in ␦18O and skeletal density of Bermuda corals. Int. J. Earth Sci. 88: 733–741. Dunbar, R. B., G. M. Wellington, M. W. Colgan, and P. W. Glynn. 1994. Eastern Pacific sea surface temperature since 1600 A.D.: the ␦18O record of climate variability in Galapagos corals. Paleoceanography 9: 291–315. Eakin, C. M., J. M. Lough, and S. F. Heron. 2009. Climate variability and change: monitoring data and evidence for increased coral bleaching stress. Pp. 41– 67 in Coral Bleaching. Patterns, Processes, Causes and Consequences, M. J. H. van Oppen and J. M. Lough, eds. SpringerVerlag, Berlin. Edinger, E. N., G. V. Limmon, J. Jompa, W. Widjatmoko, J. M. Heikoop, and M. J. Risk. 2000. Normal coral growth rates on dying reefs: are coral growth rates good indicators of reef health? Mar. Pollut. Bull. 40: 404 – 425. Edmunds, P. J., D. Brown, and V. Moriarty. 2012. Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea, French Polynesia. Glob. Change Biol. 18: doi:10.1111/j.13652486.2012.02695.x. Elizalde-Rendon, E. M., G. Horta-Puga, P. Gonzalez-Diaz, and J. P. Carricart-Ganivet. 2010. Growth characteristics of the reef-building coral Porites astreoidies under different environmental conditions in the western Atlantic. Coral Reefs 29: 607– 614. Emanuel, K. 2003. Tropical cyclones. Annu. Rev. Earth Planet. Sci. 31: 75–104. Fabricius, K. E. 2005. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar. Pollut. Bull. 50: 125–146. Fabricius, K. E., G. De’ath, M. L. Puotinen, T. Done, T. F. Cooper, and S. C. Burgess. 2008. Disturbance gradients on inshore and offshore coral reefs caused by a severe tropical cyclone. Limnol. Oceanogr. 53: 690 –704. Fabricius, K., C. Langdon, S. Uthicke, C. Humphrey, S. Noonan, G. De’ath, R. Okazaki, N. Muehllehner, M. Glas, and J. M. Lough. 2011. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat. Clim. Chang. 1: doi:10.1038/ nclimate1122. Felis, T., J. Patzold, and Y. Loya. 2003. Mean oxygen-isotope signatures in Porites spp. corals: inter-colony variability and correction for extension-rate effects. Coral Reefs 22: 328 –336. Feng, M., M. McPhaden, S. P. Xie, and J. Hafner. 2013. La Nin˜a forces unprecedented Leeuwin Current warming in 2011. Sci. Rep. 3: 1277. Fleitmann, D., R. B. Dunbar, M. McCulloch, M. Mudelsee, M. Vuille, T. R. McClanahan, J. E. Cole, and S. Eggins. 2007. East African soil erosion recorded in a 300 year old coral colony from Kenya. Geophys. Res. Lett. 34: doi:10.1029/2006GL028525. Gischler, E., and W. Oschmann. 2005. Historical climate variation in Belize (Central America) as recorded in scleractinian coral skeletons. Palaios 20: 159 –174. Goodkin, N. F., A. D. Switzer, D. McCorry, L. DeVantier, J. D. True, K. A. Hughen, N. Angeline, and T. T. Yang. 2011. Coral communities of Hong Kong: long-lived corals in a marginal reef environment. Mar. Ecol. Prog. Ser. 426: 185–196. Grove, C. A., R. Nagtegaal, J. Zinke, T. Scheufen, B. Koster, S.

PERSPECTIVES ON CORAL GROWTH Kasper, M. T. McCulloch, G. van den Bergh, and G.-J. A. Brummer. 2010. River runoff reconstruction from novel spectral luminescence scanning of massive coral skeletons. Coral Reefs 29: doi: 10.1007/s00338-010-0629-y. Grove, C. A., S. Kasper, J. Zinke, M. Pfeiffer, D. Garbe-Schonberg, and G.-J. A. Brummer. 2013. Confounding effects of coral growth and high SST variability on skeletal Sr/Ca: implications for coral paleothermometry. Geochem. Geophys. Geosyst. 14: 1277–1293. Guzman, H. M., R. Cipriani, and J. B. C. Jackson. 2008. Historical decline of coral reef growth after the Panama Canal. Ambio 37: 342–346. Helmle, K. P., and R. E. Dodge. 2011. Sclerochronology. Pp. 958 –966 in Encyclopedia of Modern Coral Reefs: Structure, Form and Process, D. Hopley, ed. Springer, Dordrecht. Helmle, K. P., R. E. Dodge, and R. A. Ketcham. 2002. Skeletal architecture and density banding in Diploria strigosa by x-ray computed tomography. Pp. 365–371 in Proceedings of the Ninth International Coral Reef Symposium, Vol. 1, M. K. Moosa, S. Soemodihardjo, A. Soegiarto, K. Romimohtarta, A. Nontji, Soekarno and Suharsono, eds. 23–27 October 2000, Bali, Indonesia. Helmle, K. P., R. E. Dodge, P. K. Swart, D. K. Gledhill, and C. M. Eakin. 2011. Growth rates of Florida corals from 1937 to 1996 and their response to climate change. Nat. Commun. 2: doi:10.1038/ ncomms1222. Hendy, E. J., M. K. Gagan, and J. M. Lough. 2003. Chronological control of coral records using luminescent lines and evidence for non-stationary ENSO teleconnections in northeast Australia. The Holocene 13: 187–199. Hoegh-Guldberg, O., P. J. Mumby, A. J. Hooten, R. S. Steneck, P. Greenfield, E. Gomez, C. D. Harvell, P. F. Sale, A. J. Edwards, K. Caldeira, M. Knowlton, C. M. Eakin et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318: 1737–1742. Hoeke, R. K., P. L. Jokiel, R. W. Buddemeier, and R. E. Brainard. 2011. Projected changes to growth and mortality of Hawaiian corals over the next 100 years. PloS ONE. doi:101371/journal.pone.0018038. HOT (Hawaii Ocean Time-Series). 2014. Research project of the Laboratory for Microbial Oceanography, University of Hawaii at Manoa. [Online]. Available: http://hahana.soest.hawaii.edu/hot/ [2014, June 23]. Hudson, J. H., E. A. Shinn, R. B. Halley, and B. Lidz. 1976. Sclerochronology: a tool for interpreting past environments. Geology 4: 361–364. Hudson, J. H., E. A. Shinn, and D. M. Robbin. 1982. Effects of offshore oil drilling on Philippine reef corals. Bull. Mar. Sci. 32: 890 –908. Hudson, J. H., K. J. Hanson, R. B. Halley, and J. L. Kindinger. 1994. Environmental implications of growth rate changes in Montastrea annularis: Biscayne National Park, Florida. Bull. Mar. Sci. 54: 647– 669. Hughes, T. P., A. H. Baird, D. R. Bellwood, M. Card, S. R. Connolly, C. Folke, R. Grosberg, O. Hoegh-Guldberg, J. B. C. Jackson, J. Kleypas et al. 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301: 929 –933. Iguchi, A., S. Ozaki, T. Nakamura, M. Inoue, Y. Tanaka, A. Suzuki, H. Kowahata, and K. Sakai. 2012. Effects of acidified seawater on coral calcification and symbiotic algae on the massive coral Porites australiensis. Mar. Environ. Res. 73: 32–36. IPCC (Intergovernmental Panel on Climate Change). 2013. Summary for Policymakers. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Stocker, T. F., D. Qin, G.-K. Plattner, M. Tigno, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P. M. Midgely, eds. Cambridge University Press, Cambridge, UK.

201

Jokiel, P. L., and S. L. Coles. 1978. Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar. Biol. 43: 201–208. Jones, P. D., K. R. Briffa, T. J. Osborn, J. M. Lough, T. D. van Ommen, B. M. Vinther, J. Luterbacher, E. R. Wahl, F. W. Zwiers, M. E. Mann et al. 2009. High-resolution paleoclimatology of the last millennium: a review of current status and future prospects. The Holocene 19: 3– 49. Kerswell, A. P., and R. J. Jones. 2003. Effects of hypo-osmosis on the coral Stylophora pistillata: nature and cause of ‘low-salinity bleaching.’ Mar. Ecol. Prog. Ser. 253: 145–154. Kleypas, J. A., J. W. McManus, and L. A. B. Men˜ez. 1999a. Environmental limits to coral reef development: where do we draw the line? Am. Zool. 39: 146 –159. Kleypas, J. A., R. W. Buddemeier, D. Archer, J.-P. Gattuso, C. Langdon, and B. N. Opdyke. 1999b. Geochemical consequences of increased atmospheric CO2 on coral reefs. Science 284: 118 –120. Knutson, D. W., R. W. Buddemeier, and S. V. Smith. 1972. Coral chronometers: seasonal growth bands in reef corals. Science 177: 270 –272. Kuffner, I. B., T. D. Hickey, and J. M. Morrison. 2013. Calcification rates of the massive coral Sidereastrea siderea and crustose coralline algae along the Florida Keys (USA) outer-reef tract. Coral Reefs 32: doi:10.1007/s00338-013-1047-8. Kwiatkowski, L., P. M. Cox, T. Economou, P. R. Halloran, P. J. Memb, B. B. B. Booth, J. Carilli, and H. M. Guzman. 2013. Caribbean coral growth influenced by anthropogenic aerosol emissions. Nat. Geosci. 6: doi: 10.1038/NGEO1780. Llewellyn, L. E., Y. L. Everingham, and J. M. Lough. 2012. Pharmokinetic modelling of multi-decadal luminescence time series in coral skeletons. Geochim. Cosmochim. Acta 83: 263–271. Logan, A., and I. H. Anderson. 1991. Skeletal extension growth rate assessment in corals, using CT scan imagery. Bull. Mar. Sci. 49: 847– 850. Lough, J. M. 2004. A strategy to improve the contribution of coral data to high-resolution paleoclimatology. Palaeogeogr. Palaeoclimatol. Palaeoecol. 204: 115–143. Lough, J. M. 2008a. A changing climate for coral reefs. J. Environ. Monit. 10: 21–29. Lough, J. M. 2008b. Coral calcification from skeletal records revisited. Mar. Ecol. Prog. Ser. 373: 257–264. Lough, J. M. 2010. Climate records from corals. Wiley Interdiscip. Rev. Clim. Change 1: doi: 10.1002/wcc.39. Lough, J. M. 2011. Great Barrier Reef coral luminescence reveals rainfall variability over northeastern Australia since the 17th century. Paleoceanography 26: doi:10.1029/2010PA002050. Lough, J. M. 2012. Small change, big difference: sea surface temperature distributions for tropical coral reef ecosystems, 1950 –2011. J. Geophys. Res. 117: C09018 doi: 10.1029/2012JC008199. Lough, J. M., and D. J. Barnes. 1992. Comparisons of skeletal density variations in Porites from the central Great Barrier Reef. J. Exp. Mar. Biol. Ecol. 155: 1–25. Lough, J. M., and D. J. Barnes. 1997. Several centuries of variation in skeletal extension, density, and calcification in massive Porites colonies from the Great Barrier Reef: a proxy for seawater temperature and a background of variability against which to identify unnatural change. J. Exp. Mar. Biol. Ecol. 211: 29 – 67. Lough, J. M., and D. J. Barnes. 2000. Environmental controls on growth of the massive coral Porites. J. Exp. Mar. Biol. Ecol. 245: 225–243. Lough, J. M., and T. F. Cooper. 2011. New insights from coral growth band studies in an era of rapid environmental change. Earth-Sci. Rev. 108: 170 –184. Lough, J. M., D. J. Barnes, M. J. Devereux, B. J. Tobin, and S. Tobin. 1999. Variability in Growth Characteristics of Massive Porites on

202

J. M. LOUGH AND N. E. CANTIN

the Great Barrier Reef. CRC Reef Research Centre Technical Report No. 28, CRC Reef Research Centre, Townsville, Australia. 95 pp. Lough, J. M., D. J. Barnes, and F. A. McAllister. 2002. Luminescent lines in corals from the Great Barrier Reef provide spatial and temporal records of reefs affected by land runoff. Coral Reefs 21: 333–343. Maier, C., T. Felis, J. Patzold, and R. P. M. Bak. 2004. Effect of skeletal growth and lack of species effects in the skeletal oxygen isotope climate signal within the coral genus Porites. Mar. Geol. 207: 193–208. Manzello, D. P. 2010. Coral growth with thermal stress and ocean acidification: lessons from the eastern tropical Pacific. Coral Reefs 29: 749 –758. Marshall, A. T., and P. Clode. 2004. Calcification rate and the effect of temperature in a zooxanthellate and an azooxanthellate scleractinian reef coral. Coral Reefs 23: 218 –224. Mora, C., C.-L. Wei, A. Rollo, T. Amaro, A. R. Baco, D. Billett, L. Bopp, Q. Chen, M. Collier, R. Donovaro et al. 2013. Biotic and human vulnerability to projected changes in ocean biogeochemistry over the 21st century. PloS Biol 11: doi:10.10371/journal.pbio. 1001682. Morrongiello, J. R., R. E. Thresher, and D. C. Smith. 2012. Aquatic biochronologies and climate change. Nat. Clim. Change 2: doi: 10.1038/NCLIMATE1616. Pandolfi, J. M., S. R. Connolly, D. J. Marshall, and A. L. Cohen. 2011. Projecting coral reef futures under global warming and ocean acidification. Science 333: 418 – 422. Pa¨tzold, J., T. Bickert, B. Flemming, H. Grobe, and G. Wefer. 1999. Holoza¨nes Klima des Nordatlantiks rekonstruiert aus massiven Korallen von Bermuda. Nat. Mus. 129: 165–177. Peters G. P., R. M. Andrew, T. Boden, J. G. Canadell, P. Ciais, C. Le Quere, G. Marland, M. R. Raupach, and C. Wilson. 2013. The challenge to keep global warming below 2 °C. Nat. Clim. Change 3: 4 – 6. Poloczanska, E. S., C. J. Brown, W. J. Sydeman, W. Kiessling, D. S. Schoeman, P. J. Moore, K. Brander, J. F. Bruno, L. B. Buckely, M. T. Burrows et al. 2013. Global imprint of climate change on marine life. Nat. Clim. Change 3: 919 –925. Poulsen, A., K. Burns, J. Lough, D. Brinkman, and S. Delean. 2006. Trace analysis of hydrocarbons in coral cores from Saudi Arabia. Org. Geochem. 37: 1913–1930. Quinn, T. M., F. W. Taylor, and T. J. Crowley. 1993. A 173 year stable isotope record from a tropical South Pacific coral. Quat. Sci. Rev. 12: 407– 418. Rayner, N. A., D. E. Parker, E. B. Horton, C. K. Folland, L. V. Alexander, D. P. Rowell, E. C. Kent, and A. Kaplan. 2003. Global analyses of sea surface temperature, sea ice, and night marine air temperature since the late nineteenth century. J. Geophys. Res. 108: doi:10.1029/2002JD002670. Saenger, C., A. L. Cohen, D. W. Oppo, R. B. Halley, and J. E. Carilli. 2009. Surface-temperature trends and variability in the low-latitude North Atlantic since 1552. Nat. Geosci. 2: doi:10.1038/NGEO552. Scoffin, T. P., A. W. Tudhope, and B. E. Brown. 1989. Fluorescent and skeletal density banding in Porites lutea from Papua New Guinea and Indonesia. Coral Reefs 7: 169 –178. Sen Gupta, A., and B. McNeil. 2012. Variability and change in the ocean. Pp. 141–165 in The Future of the World’s Climate, A. Henderson-Sellers and K. McGuffie, eds. Elsevier, Amsterdam. Shamberger, K. E. F., R. A. Feely, C. L. Sabine, M. J. Atkinson, E. H. DeCarlo, and F. T. Mackenzie. 2011. Calcification and organic production on a Hawaiian coral reef. Mar. Chem. 127: 64 –75. Shaw, E. C., B. I. McNeil, and B. Tilbrook. 2012. Impacts of ocean

acidification on naturally variable coral reef flat ecosystems. J. Geophys. Res. Oceans 117: doi:10.1029/2011JC007655. Shi, Q., K.-F. Yu, T.-R. Chen, H.-L. Zhang. M.-X. Zhao, and H.-Q. Yan. 2011. Two centuries-long records of skeletal calcification in massive Porites colonies from Meiji Reef in the southern South China Sea and its responses to atmospheric CO2 and seawater temperature. Sci. China Ser. D Earth Sci. 55: doi: 10.1007/s11430-011-4320-0. Shimamura, M., K. Hyeong, C. M. Yoo, T. Watanabe, T. Irino, and H.-S. Jung. 2008. High resolution stable isotope records of scleractinian corals near Ishigaki Island: their implications as a potential paleoclimatic recorder in middle latitude regions. Geosci. J. 12: 25–31. Smith, S. V. 1981. The Houtman Abrolhos Islands: carbon metabolism of coral reefs at high latitude. Limnol. Oceanogr. 26: 612– 621. Storz, D., and E. Gischler. 2011. Coral extension rates in the NW Indian Ocean I: reconstruction of 20th century SST variability and monsoon current strength. Geo-Mar. Lett. 31: 141–154. Tambutte, S., M. Holcomb, C. Ferrier-Pages, S. Reynaud, E. Tambutte, D. Zoccola, and D. Allemand. 2011. Coral biomineralization: from the gene to the environment. J. Exp. Mar. Biol. Ecol. 408: 58 –78. Tanzil, J. T. I., B. E. Brown, A. W. Tudhope, and R. P. Dunne. 2009. Decline in skeletal growth of the coral Porites lutea from the Andaman Sea, South Thailand between 1984 and 2005. Coral Reefs 28: 519 –528. Tanzil, J. T. I., B. E. Brown, R. P. Dunne, J. N. Lee, J. A. Kaandorp, and P. A. Todd. 2013. Regional decline in growth rates of massive Porites corals in southeast Asia. Glob. Change Biol. 19: 3011–3023. Thornhill, D. J., R. D. Totjan, B. D. Todd, G. C. Chilcoat, R. IglesiasPrieto, D. W. Kemp, T. C. LaJeunesse, J. McCabe Reynolds, G. W. Schmidt, T. Shannon, M. E. Warner, and W. K. Fitt. 2011. A connection between colony biomass and death in Caribbean reefbuilding corals. PLoS ONE 6: doi:10.1371.journal.pone.0029535. Tomascik, T. 1990. Growth rates of two morphotypes of Montastrea annularis along a eutrophication gradient, Barbados, W. I. Mar. Pollut. Bull. 21: 376 –381. Vasquez-Bedoya, L. F., A. L. Cohen, D. W. Oppo, and P. Blanchon. 2012. Corals record persistent multidecadal SST variability in the Atlantic warm pool since 1775 AD. Paleoceanography 27: doi: 10.1029/2012PA002313. Venn, A. A., E. Tambutte, M. Holcomb, J. Laurent, D. Allemand, and S. Tambutte. 2013. Impact of seawater acidification on pH at the tissue-skeleton interface and calcification in reef corals. Proc. Nat. Acad. Sci. 110: doi:10.1073/pnas.1216153110. Weber, J. N., and E. W. White. 1974. Activation energy for skeletal aragonite deposited by the hermatypic coral Platygyra spp. Mar. Biol. 26: 353–359. Weber, J. N., E. W. White, and P. H. Weber. 1975. Correlation of density banding in reef coral skeletons with environmental parameters: the basis for interpretation of chronological records preserved in the coralla of corals. Paleobiology 1: 137–149. Wernberg, T., D. A. Smale, F. Tuya, M. S. Thomsen, T. J. Langlois, T. de Bettignies, S. Bennett, and C. S. Rousseaux. 2012. An extreme climate event alters marine ecosystem structure in a global biodiversity hotspot. Nat. Clim. Change 3: 78 – 82. Wilkinson, C., ed. 1998. Status of Coral Reefs of the World: 1998. Global Coral Reef Monitoring Network, Australian Institute of Marine Science, Townsville, Australia, 184 pp. Wooldridge, S. 2009. Water quality and coral bleaching thresholds: formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar. Pollut. Bull. 58: 745–751. Zeebe, R. E. 2012. History of seawater carbonate chemistry, atmospheric CO2 and ocean acidification. Annu. Rev. Earth Planet. Sci. 40: 141–165.