Global Warming on Coral

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Effects of Climate Change/Global Warming on Coral Reefs: Adaptation/Exaptation in Corals, Evolution in Zooxanthellae, and Biogeographic Shifts Paul W. Sammarco a; Kevin B. Strychar b a Louisiana Universities Marine Consortium (LUMCON), Chauvin, La, USA b Department of Life Sciences Texas A&M University, Corpus Christi, Texas, USA Online Publication Date: 01 January 2009

To cite this Article Sammarco, Paul W. and Strychar, Kevin B.(2009)'Effects of Climate Change/Global Warming on Coral Reefs:

Adaptation/Exaptation in Corals, Evolution in Zooxanthellae, and Biogeographic Shifts',Environmental Bioindicators,4:1,9 — 45 To link to this Article: DOI: 10.1080/15555270902905377 URL: http://dx.doi.org/10.1080/15555270902905377

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Environmental Bioindicators, 4:9–45, 2009 Copyright © Taylor & Francis Group, LLC ISSN: 1555-5275 print/ 1555-5267 online DOI: 10.1080/15555270902905377

Effects of Climate Change/Global Warming on Coral Reefs: Adaptation/Exaptation in Corals, Evolution in Zooxanthellae, and Biogeographic Shifts

1555-5267 1555-5275 UEBI Environmental Bioindicators, Bioindicators Vol. 4, No. 1, April 2009: pp. 1–81

Effects of Climate Sammarco and Strychar Change on Coral Reefs

PAUL W. SAMMARCO1 AND KEVIN B. STRYCHAR2 1

Louisiana Universities Marine Consortium (LUMCON), Chauvin, La Department of Life Sciences Texas A&M University, Corpus Christi, Texas

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Increased sea-surface temperatures (SSTs) associated with climate change/global warming have caused bleaching in scleractinian corals (the loss of obligate symbiotic zooxanthellae) on a global basis, resulting in mass mortality of corals and decimation of reefs. This symbiotic relationship makes these corals an excellent bioindicator of climate change. It has been hypothesized that bleaching is a mechanism by which corals can adapt to changing environmental conditions via the “shuffling” of symbiont clades and acquisition of better-adapted symbionts. Experimental research has confirmed that zooxanthellae are sensitive to increases in seawater temperatures, exhibiting apoptosis (a form of programmed cell death) at temperatures of ³30oC while in situ. The coral hosts, however, tolerate experimental temperatures up to 34oC, not showing signs of apoptosis and necrosis until 36oC. Thus, zooxanthellae currently appear to be poorly adapted to temperature increases, while the corals are resistant to higher temperatures, indicating that they are either already adapted or exapted (previously termed preadapted) to such. Coral hosts are experiencing no mortality from increased temperatures but a great deal of mortality from the death of their zooxanthellar symbionts. Symbiodinium sp. has a short generation time of one to several days, vs. that of its host coral—one to several years, affording the symbionts a distinct advantage for adaptation. Mutation rates are low in micro-organisms and higher in larger organisms. Smaller organisms have a disproportionately higher mutation rate than larger organisms, however, when compared on a per-generation basis. Thus, zooxanthellae are positioned better to adapt more rapidly than their coral hosts. Zooxanthellae have numerous clades, some of which are suspected to be better-adapted to higher seawater temperatures than others. The discovery of new Symbiodinium clades may be due to our ability to detect them via better technology or due to mutation, adaptation, and directional selection. Changes in the frequency of occurrence of different clades betteradapted to higher temperatures may be due to the emergence of newly mutated strains (i.e., sub-clades or sub-types) or re-distribution of existing clades. Predictions for the future of coral reefs include the following: a) Some tropical corals may be lost to local or global extinction, based on species-specific susceptibility to temperature increases; b) it is unlikely that other symbionts such as cyanobacteria will be able to replace Symbiodinium in the host-symbiont relationship; c) the tropics and sub-tropics will expand poleward and the other climatic zones will shift poleward, at the expense of the polar and sub-polar zones; d) a new “hyper-tropical zone” may appear near the equator, within which corals may be less species diverse, ill represented, or absent; and e) the depth distribution of corals may be extended, but probably only nominally so. Address correspondence to Paul W. Sammarco, Louisiana Universities Marine Consortium, 8124 Hw. 56, Chauvin, LA 70344. E-mail: [email protected]

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Introduction Over the last 160,000 years, the temperature of the Earth’s atmosphere has varied substantially— by as much as 15oC (Moberg and others 2005; Miller and others 2005; Huber and others 2006). The industrial revolution has caused an increase in the concentration of greenhouse gases. For example, CO2 concentrations have increased from 280 ppm to 384 ppm; N2O, from 270 ppb to 314 ppb; CH4, from 700 ppb to 1,745 ppb; and SO2, 50 to 200 mg per ton of ice (Keeling and others 1996; Linacre and Geerts 2002; IPCC 2007). These increases in greenhouse gases have also caused changes in both sea surface temperatures (SST) (Cane and others 1997) and global weather and climate patterns. SSTs have increased globally, from the tropics to the poles (Huybers and Curry 2006; Fig. 1), and this, in conjunction with atmospheric temperature changes, have altered major patterns in weather and climate (Mann and others 1998; Jordan 2006), including monsoonal rains (Anderson and others 2002), El Niño (Corrège and others 2000; IPCC 2001; Donner and others 2005; EEA 2008), desertification (Trumper and others 2008), and precipitation patterns (Ledley and others 1999; IPCC 2007), and sea level (see Goreau and Hayes, 2007 for review). For example, there has been a steady and substantial increase in the frequency of severe floods from 1950 to 2000 in North America, Europe, Asia, Africa, and Oceania (CIG 2004; Dale 2005; US Climate Change Science Program 2008). In the last 140 yrs, SSTs have increased by an average of 1oC. This seemingly minor increase in temperature, when integrated over the entire surface of the world’s oceans, represents a substantial amount of energy. An analysis of seawater temperature in the Pacific Ocean between the 1960s and 1985–94 has revealed that significant warming has occurred in the 10oN and 24oN latitude regions, yielding a net heat gain for the Pacific of 1.79 × 108 J m−2 (Wong and others, 2001). For reference, a joule represents the approximate amount of energy required to lift an apple from the floor to a table (Heckert, 2008). An electric power plant rated as 500 megawatts (MW) has a power output of 500 million joules or 5 × 108 joules of energy production each second. Since the 1950s, it is estimated that the world’s oceans have absorbed an extra 15 × 1022 J (J.A. Church, 2007, pers. comm.). Church has reported that even if atmospheric warming ceased completely in 2007, because of the amount of heat stored by the ocean at that time and the time lag associated with the onset of their cooling, SSTs would not begin to decrease until the year 2075. The consequences of that include the loss of polar ice through melting and rupturing in the arctic regions, which are experiencing the highest rates of temperature increase in the world (Vincent and others 2001; van der Veen 2001). For example, in the Arctic, the Ward Hunt Ice Shelf – previously the largest piece of ice known to exist in the world, dated to be approximately 3,000 yrs old - began to fracture in 2000 and is continuing to do so (Mueller and others 2003; Sturm and others 2003; NRDC 2007; Science Daily 2008). El Niño events have increased not only in frequency but also in intensity (Trenberth and Hurrell 1994; Tompkins 2002; Emanuel and others, unpublished manuscript). These events have been accompanied by the emergence of “hot spots” in the tropical and subtropical oceans with respect to SSTs (Goreau and Hayes, 1994, 2005; Morgan and others, 2006; see Fig 2). That is, localized SSTs have been rising well above average and have been sustained for days to weeks (Smithers and others 2003; Goreau and others, 2005; Sammarco and others 2005; NECIA 2006), stressing marine communities (Bandura and Vucson 2006; Harley and others 2006), including planktonic (Harvell and others 1999; Hare and others 2007; Richardson, 2008; Sommer and Langfellner, 2008, pelagic (Verity and others 2002; Richardson and Schoeman 2004; Roessig and others 2004; Beaugrand

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Figure 1. A) Patterns of increases in both sea surface and land surface temperatures (SST and LST, respectively) since 1880. Temperatures have been increasing globally and steadily since that time. The increase is particularly noticeable since the 1930s and becomes pronounced beginning in the 1980s. (National Climatic Data Center 2009). B) Average seawater temperatures in the upper 300 m of the water column. Temperature has increased dramatically from 1979 to 2009. (Map courtesy of Yan Xue, NOAA Climate Prediction Center, 2009).

and others, 2008;), and benthic communities (Hiscock and others 2004; Aronson and others 2007; Hoegh-Guldberg 2007; Reid, 2008). Scleractinian corals are excellent bioindicators of environmental stress, and particularly of above-average SSTs (Obura, 1999, 2001; Kramer, 2003; Gledhill and others, 2006; Shinn, 2008; Strychar and Sammarco, 2009). In fact, corals have been compared to canaries which were used as a bioindicator of the presence of dangerous levels of methane and carbon monoxide in coal mines, and have been referred to as the “canaries” of the marine environment (Pockley, 2001; Fenner 2004; Stone 2007). They are the key component of coral reefs and are primary contributors of calcium carbonate to them. Optimal growth of coral reefs occurs between 26–28oC, but they are known to exist between temperature ranges of 18oC to 36oC (NOAA 2009a; Fig. 2).

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Figure 2. A) Satellite imagery has revealed the emergence of “hot spots” in tropical and sub-tropical oceans (NOAA 2009b, http://www.osdpd.noaa.gov/PSB/EPS/SST/climo&hot.html). Such data are used to predict bleaching events. B) Localized sea surface temperatures sustained for days to weeks, are termed “degree-heating weeks” and can be used to help characterize coral bleaching events and predict the potential duration of such episodes (NOAA 2009c, http://www.osdpd.noaa.gov/PSB/ EPS/SST/dhw_retro.html).

An increase in SST above the range of thermal tolerance in corals can result in their bleaching. Bleaching is the process by which corals that possess symbiotic dinoflagellates, commonly called zooxanthellae (Symbiodinium sp.), lose them in response to a variety of environmental stresses, particularly elevated seawater temperature (see Mayor, 1917, 1918; Yonge and Nicholls, 1931 for earliest accounts, and McClanahan and others 2007; Baird and others 2009 as examples of later accounts; see http://divedeep.sakura.ne.jp/cb/ min.htm for photographic time-series of a bleaching episode, M. Tanaka). Zooxanthellae are responsible for facilitating coral growth and development by providing the host with nutrients and oxygen (Szmant-Froelich and Pilson 2004; Stanley 2006). Once these symbionts are lost, the corals may die within a certain period of time unless vertical transmission (the transfer of zooxanthellae from parent to its young through its larvae; Kinzie and others, 2001; Toller and others 2001a,b) or horizontal transmission (colonization of the coral tissue by new zooxanthellae in the water column) occurs (Jones and Yellowlees 1997). Between 1876 and 1979, only three bleaching events were recorded (Mayor 1917, 1918; Yonge and Nicholls 1931); between 1980 and 1993, there were ∼60 reported (Glynn 1983; Williams and Bunkley-Williams 1990; Sullivan 2003). Since 1980, there has been a dramatic increase in the frequency and duration of bleaching events on a global scale, with six major world-wide bleaching events devastating coral reefs. These have been associated with

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El Niño events occurring in 1979–80, 1982–83, 1987–1988, 1994–1995, 1998–1999, and 2002 (Huppert and Stone 1998; Hoegh-Guldberg 1999; Hoegh-Guldberg and others 2005; see Glynn 1983, 1984 for early detailed accounts). In 1998, 48% of western Indian Ocean reefs and 16% of all reef areas globally exhibited extensive bleaching (Butler 2005). In 2002, extensive bleaching occurred on 60–95% of the world’s barrier reefs, causing the loss of 50–90% of the coral there (UNESCO World Heritage Committee Climate Change Working Group 2006; UNEP 2008). On the Great Barrier Reef, Australia, 50–60 % of the reefs bleached, affecting ∼75,000–210,000 km2 (Corder 2006; Australian Government 2008). Between 1984 and 1991, live coral cover decreased by as much as 49.3% at certain sites in the Florida Keys (Porter and Meier 1992). These events, in combination with an increase in the incidence of coral disease (Harvell and others, 1999, 2002; Lafferty and others, 2004; Weil and others, 2002, 2006), have resulted in a major decrease in live coral cover world-wide. There are many factors causing the demise of coral reefs worldwide, and other factors have been identified as potential influencing factors for the future (e.g., ocean acidification; Kleypas and others, 1999; see Baker and others, 2008; McClanahan and others, 2008 for discussion). Here, we will only discuss the effects of increasing seawater temperatures in relation to coral bleaching.

Corals are Adapted/Exapted to Global Warming; Zooxanthellae are not There is no doubt that corals are highly sensitive to seawater temperature, particularly temperatures well above average. One must remember, however, that a coral is actually comprised of two organisms from two different kingdoms—the coral itself, a coelenterate, and its symbiotic zooxanthellae—microscopic dinoflagellates that live within the coral tissue. The question may be posed—are the corals temperature-sensitive and dying from the temperature stress, or is it the zooxanthellae, or is it both organisms? The Adaptive Bleaching Hypothesis, as proposed by Buddemeier and Fautin (1993; Kinzie and others, 2001; Fautin and Buddemeier, 2004), states that when corals are exposed to temperature stress, they release a proportion of their symbiotic associates and at a later time, re-associate with some combination of zooxanthellae that are better adapted to conditions of increased seawater temperature. This results in a coral which as a whole is better adapted to these environmental conditions. This hypothesis is well-founded in evolutionary theory and proposes a viable mechanism by which symbiotic corals may be able to adapt to rapidly changing environmental conditions, particularly increases in seawater temperature. Experimental evidence exists to support this hypothesis (Kinzie and others, 2001; Baker and others, 2004; Ulstrup and others, 2006; Muller-Parker and others, 2007). By contrast, it has also been proposed that most symbiotic scleractinian corals and octocorals are not capable of exchanging their endosymbiotic clades and that such adaptation is only possible in a small subset of species (Goulet 2006). In either case, natural selection on the zooxanthellae will be key to the survival of any corals in the future, whether this pertains to all currently existing species or a small subset. The mechanism by which this adaptation takes place is now better understood, for it is now known that the levels of mortality in symbiotic zooxanthellae are much higher than previously suspected. We have found that, of the symbiont cells released by the host, only ∼10% are viable for re-association with the host (Strychar and others, 2004a,b). Further, we found that the zooxanthellae exposed to high seawater temperatures exhibit high levels of apoptosis and necrosis while in situ – i.e., while they are still within the host, prior to their separation from it (Strychar and Sammarco, 2009; Fig 3). This indicates that most of the zooxanthellae have already entered a process of cell death before they are released

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Figure 3. Transmission electron micrographs showing symbiont (Symbiodinium spp.) cells in-situ. A) Cell shown under control seawater temperature conditions of 28°C. Cell appears normal. Scale bar = 1 μm. B) Cells shown under temperature conditions of 32°C, exhibiting symptoms of apoptosis. C) Cells under experimental temperatures of 32oC exhibiting necrosis. Scale bars in B&C = 500 μm. Symbols: ab = apoptotic body, chr = chromosome, cl = chloroplast, cw = cell wall, gx = glyoxysome, m = mitochondria, n = nucleus, py = pyrenoid, sg = starch grain.

from the host. In that case, after the bleaching process has occurred, a large proportion of temperature-sensitive zooxanthellae will have died and been removed from the population. This would leave a small proportion of better-adapted zooxanthellae behind. It is this small proportion of surviving symbionts that is responsible for adaptation of the zooxanthellae in this system. The high mortality levels observed in this population is an indicator of their high degree of heat sensitivity. Variation in the response to heat stress—primarily mortality, even if it has occurred in only a small proportion of the zooxanthellar population—is the key to survival in the corals and this group to higher heat tolerances in this changing environment. It is not the proportion of the population that survives which will permit adaptation, but the mere fact that survival has occurred, and that the capacity for survival is genetically based and heritable (Futuyma, 1998). Thus, the better-adapted genes responsible for that heat-tolerant character will be passed on to future generations (Fabricius and others, 2004; Ulstrup and others, 2006). It has been demonstrated that coral hosts will play little to no role in the adaptation to rising seawater temperature (Strychar and Sammarco, 2009). This is because they simply are not sensitive to it. They are already adapted or exapted to this environmental perturbation. Exaptation is defined as a character that has evolved for another function, or no function at all, but which has been co-opted for a new use (Gould and Vrba, 1982, cf Futuyma, 1998; McLennan 2008; also see Brown and Howard 1985; Fang and others 1997; Salm and Coles 2001; Strychar and Sammarco, 2009). Exaptation was previously referred to as “pre-adaptation”, and has been described by Mettler and Gregg (1969) as follows: “. . . populations can . . . maintain genetic variance and can generate many genotypes with varying degrees of adaptedness. Those forms produced each generation on the non-adapted end of the scale are weeded out by selection, but they are continuously produced and are considered to be ‘stores on hand’ which would become the progenitors of future generations in the event of a changed environment. They are ‘preadapted’ genotypes ready for new situations which might be met by the population . . . However, the group becomes extinct when no genotypes exist which are preadapted for a novel set of conditions under which the population is shifted.” The term “preadaptation” is no longer used in the field of evolution to denote this phenomenon because of its implications for “intentional plan” or “Creationism” (http:// en.wikipedia.org/wiki/Preadaptation, 2009; http://www.zainar.com/incip.html, 2009).

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We have found that cells within the coral host show few or no signs of apoptosis or necrosis in their cells when exposed to experimental temperatures up to 34oC (Strychar and Sammarco, 2009; Figs. 4 & 5), unlike their endosymbionts. This indicates that the coral hosts themselves have not been responding negatively to SST increases that have occurred as a result of climate change in recent years in the world’s tropical oceans. This suggests that the zooxanthellae are doing the lion’s share of adaptation to temperature. The symbionts are the bioindicators of temperature stress—organisms sensitive to the temperature perturbation. The coral animals are not themselves the indicators, although the sensitivity may be manifested through them. These observations were made on the order of hours, but the differences in temperature tolerance were so striking that it was clear which of the two symbionts was more sensitive. Experiments examining responses over longer periods of time might reveal some host sensitivity to moderate increases in temperature (TJ Goreau, pers. comm.).

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Generation Time vs. Mutation Rate in Host vs. Symbiont: A Key to Adaptation in Corals One of the factors that will permit the rapid adaptation of the coral symbiotic system to the detrimental effects of global climate change or any other environmental perturbation involving the zooxanthellae is their rapid rate of reproduction. It is a well-established fact that, on the average, larger species have longer generation times and lower rates of reproduction than smaller species (Bonner, 1965; McNaughton and Wolf, 1979; Fig. 6). The maximum life-span of a coral can be on the order of hundreds and possibly thousands of years (Isdale, 1983; Boto and Isdale, 1985; Lough and Barnes, 1997), although, more commonly, a coral lives for on the order of decades (e.g., Hughes and Jackson, 1985; Darke and Barnes, 1993; Hall and Hughes, 1996; Chadwick-Furman and others, 2000; Guzner and others, 2007). By comparison, however, the life-span of a zooxanthella is two to five days (Deane and others 1979). Thus, the zooxanthellae and their coral hosts exhibit very

Figure 4. Transmission electron micrographs showing cells of host coral (Acropora hyacinthus) and symbiont (Symbiodinium spp.) in-situ. A) Both host and symbiont cells shown under control seawater temperature conditions of 28°C. Note normal appearance. Scale bar = 5 μm. B) Both host and symbiont cells shown under conditions of 34°C. Symbiont cells exhibiting symptoms of apoptosis and necrosis. Host cells remain normal in appearance. Scale bar = 10 μm. sym = Symbiodinium spp. (Reprinted from Journal of Experimental Marine Biology and Ecology, Vol. 369 (1), K. B. Strychar and P. W. Sammarco, “Exaption in corals to high Seawater temperatures: Low concentrations of apoptotic and necrotic cells in host coral tissue under bleacing conditions”, pp. 31–42, 2009, with permission from Elsevier. http://www.sciencedirect.com/science/journal/00220981).

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Figure 5. Effect of seawater temperature on the percentage of viable host coral Acropora hyacinthus cells and endosymbiont Symbiodinium cells - in-situ, collected over a12 h period. Data shown here relate to corals exposed to 28°C (control; top panel) and 34°C (bottom panel). Open circle (❍) or square (ⵧ) = viable cells. Solid circle (䊉) or square (䊏) = apoptotic cells. Changes in coral host cells denoted via dashed lines (…..); changes in symbiont cells by dot-dash lines (_ . _ . _ .). Data presented as mean from nine separate experiments with 95% confidence intervals. Some confidence limits are too small to be seen. Each point represents the percentage (%) of different cell types analyzed via transmission electron microscopy (TEM). Time intervals correspond to peak periods where corals bleached at elevated temperatures. A. hyacinthus tissues were sampled and prepared for TEM analysis at these times. One hundred zooxanthellar cells were randomly examined per experimental temperature per time interval. (Data derived from Strychar and Sammarco 2009).

different life-history traits, such as those characteristic of r- vs. K-selected species, respectively (MacArthur and Wilson, 1967; Pianka, 1970). The coral host can reproduce sexually and asexually. Free-living dinoflagellates can also reproduce both sexually and asexually (Seo and Fritz 2001; Glimn-Lacy and Kaufman 2006). Symbiotic Symbiodinium, however,

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are only known to reproduce asexually in situ (Schoenberg and Trench, 1980 a,b,c; Brown and Zamani 1992; Titlyanov and others, 1997; Santos and Coffroth 2003; Stat and others 2006; Porto and others 2008), although some evidence also exists for in situ sexual reproduction (Baillie and others, 1998, 2000). With respect to generation time, zooxanthellae can reproduce at a rate on the order of hours or days (Titlyanov and others, 1997; Wilkerson and others 1983, 1988; Deane and others 1979; Obura 2008; Fig. 6). The frequency of reproduction in corals, however, is on the order of months to years (Harrison and others, 1984; Babcock and others, 1986; Levitan and others, 2004; Sammarco and others, 2007, 2008). For example, several coral species do not reach first age of reproduction until 1–3 yrs old (Sakai, 1998; Kai and Sakai, 2008); this is also partially dependent upon colony size (Hall and Hughes, 1996; Fig. 7). Some brooders, such as Porites astreoides, will reproduce continually over a period of ∼10 days per month for up to 6 months per year (McGuire, 1998). Even these seemingly high rates of reproduction in corals cannot compare to the rapid rates characteristic of Symbiodinium spp. which occur in populations of millions of individuals within a single coral colony.

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Mutation is a primary factor driving adaptation through natural selection, and these highly disparate reproductive rates create contrasting frameworks for mutation rates in these two symbiotic organisms. Mutation rate may be generally defined as the average frequency of occurrence of heritable changes in a species that occur in the nucleotide sequence of DNA, involving substitutions, insertions, or deletions of one or more nucleotides (from Futuyma, 1998; Farabee, 2000). As we discussed above, the coral host appears to be adapted or exapted to seawater temperatures well above those being experienced today. Thus, adaptation to increasing seawater temperatures must default to the zooxanthellae in this symbiotic relationship. The temperature itself is a “non-issue” for the corals, except for their dependence upon an organism which is highly sensitive to temperature. One means by which adaptation to temperature changes can occur is if a zooxanthella experiences a mutation which increases its temperature tolerance. Such mutations are expected to be rare and arise randomly through time; however, considering the population size of zooxanthellae on a given reef (tens to hundreds of billions of cells) and their short generation time, it is certainly possible that such a beneficial mutation could occur. For example, virus-like particles and bacteria are known to have short generation times and high reproductive rates. Virus-like particles have generation times ranging from 1–5 h (Hewson and Fuhrman 2003) to 1–4 days (Fischer and others 2003; Glud and Middelboe 2004). Bacteria divide one to two times per day (Loewe and others 2003; also see Todar 2008). Bacterial mutation rates are known to be approximately one mutation every 1,200 replications (or 1 mutation every 4 months; Tago and others 2005; Moran 2007). The question arises—do faster reproducing organisms, such as zooxanthellae, have higher mutation rates than those that reproduce more slowly? Dobzhansky (1970) and others (see Strickberger, 1968; Drake, 1974; Futuyma, 1998) have shown that they do not; in fact, it is exactly the opposite. Whether measured as mutations per 100,000 cells/gametes or per genome per generation, mutation rates are orders of magnitude higher in more highly evolved organisms than micro-organisms, and there is a highly significant, positive correlation between these two variables (Fig. 7). A generally effective way to compensate for differences in generation time would be through adjusting mutation rate, which are magnitudes lower in micro-organisms. If mutation rates of different species increase at the same rate as generation time, then these species could be expected to adapt to their environment equally well. This assumes that mutations are, on the average, equally deleterious, adaptive, or neutral between species, and that generation time does not greatly exceed the time-scale of the environmental perturbation. This relationship is depicted in a hypothetical expected 1:1 relationship between mutation rate and generation time, shown as a dashed line in Fig. 8. That line has been forced through the mean mutation rate for Escheria coli. The regression line produced by the empirical data shown in Fig. 7, however, has a distinctively lower slope. The predicted mutation rates for Symbiodinium as a function of generation time are shown for both a) the hypothetical relationship between mutation rate and generation time under the 1:1 relationship, and b) that predicted for this species from empirical data. Both points fall within the 95% confidence limits derived from empirical data. The predicted, hypothetical mutation rate for the coral host, however, similarly calculated and based on a 1:1 increase in mutation rate with generation time, falls well above the regression line produced by the empirical data, and outside its 95% confidence limits. Thus, the mutation rate for corals appears to be lower than that for its zooxanthellae when considered on a per generation basis. Based on these concepts, we predict that the coral hosts have a lower capacity for rapid adaptation to their environment than their symbiotic zooxanthellae. Once again, in

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1 1 1 10 day mo yr yrs Generation Time (mins) (Log10)

100 yrs

Figure 7. The relationship between generation time and genetic mutation rate in 8 taxonomic groups, ranging from bacteria to humans. Data transformed by log10. Highly significant correlation between these two variables (r = 0.776, Pearson’s Product-Moment Correlation, p < 0.001). Model II regression plotted with 95% confidence limits to demonstrate derived empirical relationship between these variables, also highly significant (Y = −3.340 + 0.585 X, Least Squares Linear Regression, p < 0.001). Mutation rates derived from Strickberger (1968; c.f. Dobzhansky, 1970; Futuyma, 1998).

the case of seawater temperatures, the coral hosts are already exapted to higher seawater temperatures, and the zooxanthellae must, based on comparative mutation rate, generation time, and sensitivity to temperature, do the “lion’s share” of adaptation. In a bleaching event, those zooxanthellae ill-adapted to tolerate temperature increases will be selected out of the population (Colley and Trench 1983; Sachs and Wilcox 2006), leaving those adapted to the higher temperatures to survive (Baker 2001; Obura 2008), creating a betteradapted zooxanthellar population (Weir, 1990; Slatkin and others, 1955; Thorpe and Smartt, 1995). The respective responses of corals and their symbionts to environmental perturbations other than seawater temperature are not yet known, but it is likely that adaptation or exaptation in one group or the other will play an important role in defining the rate and success of adaptation.

Zooxanthellar Clades – A Potential Bioindicator of Climate Change The critical role of Symbiodinium microadriaticum (previously Gymnodinium microadriaticum) in coral physiology has been known since the middle of the 20th Century. In recent decades, however, it has been determined that there is more than one species of Symbiodinium, and that these species are comprised of a number of clades and sub-clades (Tables 1 and 2; LaJeunesse and Trench, 2000; LaJeunesse, 2001, 2002, 2004; LaJeunesse and others,

20

Sammarco and Strychar Generation Time vs. Mutation Rate

Mutation Rate (no. / 100,000 cells or gametes) (Log10)

104 Symbiodinium

Coral

102

Predicted for Equitability in Mutation Rate Empirical

100

10–2

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10–4

1 min

1 hr

1 1 1 day mo yr Generation Time (mins) (Log10)

10 yrs

100 yrs

Figure 8. The relationship between generation time and mutation rate in organisms ranging from bacteria to humans. The solid regression line is that calculated from empirical data (see Fig. 7), shown with 95% confidence limits. The dashed line indicates a hypothetical relationship where mutation rate increases in direct proportion to generation rate on a 1:1 basis. This line indicates mutation rate equivalence between species when considered on a per-generation basis. This line has been forced through the mean mutation rate for Escheria coli (see Fig. 7). Note that the empirically derived line has a lower slope than the hypothetical one, indicating that on a per generation basis, organisms with a higher generation rate, although possessing a higher mutation rate than organisms with a lower generation time in absolute terms, actually have a lower relative mutation rate. Also, note that estimates of mutation rates for Symbiodinium sp. derived from both empirical or a hypothetical situation (see Figs 6 & 7) fall within the 95% confidence limits of the empirical line. The hypothetical mutation rate for coral, however, projected from organism size (see Fig. 6), occurs above the confidence limits for the empirical line, indicating that the relative mutation rate of coral is predicted to be lower than that of its endosymbiotic zooxanthellae.

2003, 2004; Pochon and others 2004; van Oppen and others 2005; Visram and Douglas 2006; Mostafavi and others 2007; Venn and others 2008; Stat and others 2008). In fact, the number of descriptions of these species has been increasing since the 1970s (Trench 2000; Trench and Blank 1987; McNally and others 1994; Littman and others 2008), based upon differential behavior, morphology, biochemistry, physiological adaptation (Kinsey, 1974; Leutenegger, 1977; Schoenberg and Trench, 1980a,b,c; Blank and Trench 1985a,b; Blank and Trench 1986; Trench and Blank 1987; Blank and others 1988; Blank and Huss 1989; Yacobovitch and others 2004; Pasternak and others 2006), and molecular genetics (Rowan and Powers 1992; Baker 2003). Several questions arise in association with the discovery of new clades. Are we discovering new clades of zooxanthellae because of our increased ability to detect them (e.g., Rowan and Powers, 1991a,b; Baker, 2003)? Or, rather, are we witnessing the advent of new, rapidly evolving clades that are responding to climate change/global warming (Baker and others 1997, 2004; Baker 2001; Toller and others 2001a,b; Berkelmans and

21

A

Symbiodinium clades

S. meandrinae

S. (= Gymnodinium) linucheae

A2 A3

A4

A7, A9 A11 A13, A14

S. microadriaticum

S. pilosum

Symbiodinium species designation

A1

Symbiodinium sub-clades

LaJeunesse and others (2003) Barneah and others (2007) LaJeunesse (2005)

Rowan and Powers (1991b) Baker and others (1997), Baker (2001), Loh and others (2001), Pochon and others (2001), van Oppen and others (2001), Riddle (2006) Rodriguez-Lanetty and others (2002) Baker (2001) Riddle (2006) Pochon and others (2001) Baker (2001), Pochon and others (2001), Riddle (2006) Baker (2001), Riddle (2006) LaJeunesse (2001), Visram and Douglas (2006) LaJeunesse (2001) Warner and others (2006), Riddle (2006), Riddle (2007) LaJeunesse (2002), Warner and others (2006)

Clade reference

Acropora, Millepora Turbinaria Madracis, Porites (Continued)

Meandrina Montastrea, Siderastrea, Acropora, Stephanocoenia Porites, Millepora

Stephanocoenia Stylophora, Acropora

Dendrophyllia Diploria Meandrina, Montastrea Millepora Porites

Acropora

Scleractinian genera

Table 1 Symbiodinium clades and subclades associated with scleractinian corals. Symbiodinium species designation shown along with genus of coral associate. Missing clade or sub-clade designations (e.g., “E”, “A5”) indicates scleractinian-host association is unknown

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22

C

B

Symbiodinium clades

B6, B7, B9, B13, B17, B22 B10

B2 B5

B1 B1

Symbiodinium sub-clades

S. goreaui

S. muscatinei

Symbiodinium species designation

Rowan and Powers (1991b) Baker (2001), Loh and others (2001), van Oppen and others (2001), Pochon and others (2001), LaJeunesse and others (2003), Rodriguez-Lanetty and others (2002), Goulet and Coffroth (2004), Strychar and others (2005), Riddle (2006)

Thornhill and others (2005)

Rowan and Powers (1991b) LaJeunesse (2002), Banaszak and others (2006), Riddle (2006) LaJeunesse (2001), LaJeunesse (2004) LaJeunesse (2004), Thornhill and others (2006) LaJeunesse (2004)

Baker (2001), Pochon and others (2001), van Oppen and others (2001), Chen and others (2005), Strychar and others (2005), Riddle (2006)

Clade reference

Table 1 (Continued)

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Acropora, Agaricia, Alveopora, Diploria, Erythropodia, Eusmilia, Favia, Heliopora, Isophyllastrea, Isophyllia, Leptoseris, Lobophyllia, Manicina, Montastrea, Oulophyllia, Pachyseris, Pavona, Pocillopora, Porites, Scolymia, Seriatopora, Siderastrea, Stephanocoenia

Colpophyllia, Madracis, Montastraea

Oculina, Diploria, Favia, Manicina, Montastrea, Pocillopora Montastrea,Oculina Siderastraea

Acropora, Calpophyllia, Dendrogyra, Dichocoenia, Diploria, Eusmilia, Favia, Isophyllastrea, Madracis, Manicina, Meandrina, Montastrea, Plesiastrea, Porites

Scleractinian genera

23 van Oppen and others (2001), Chen and others (2005) van Oppen and others (2001), Chen and others (2003, 2005), LaJeunesse and others (2003), LaJeunesse (2004)

C3

Chen and others (2005), van Oppen and others (2001), LaJeunesse and others (2003, 2004), LaJeunesse (2004), Riddle (2006)

C2

C1

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(Continued)

Acropora, Montastrea, Mycedium, Oulophyllia, Oxypora, Pachyseris, Palythoa, Pavona, Pectinia, Platygyra, Podobacia, Polyphyllia, Protopalythoa, Seriatopora, Siderastrea, Stephanocoenia, Symphyllia,Turbinaria

Acropora, Astreopora, Coscinaraea, Cyphastrea, Discosoma, Echinophyllia, Echinopora, Euphyllia, Favia, Favites, Fungia, Galaxea, Goniastrea, Goniopora, Herpolitha, Hydnophora, Leptastrea, Leptoria, Lithophyllia, Lobophyllia, Merulina, Millepora, Montastrea, Montipora, Mycedium, Mycetophyllia, Pachyseris, Palauastrea, Palythoa, Pavona, Plerogyra, Plesiastrea, Pocillopora, Polyphyllia, Porites, Protopalythoa, Psammocora, Pseudosiderastrea, Rhodactis, Scolymia, Siderastrea, Stylocoeniella, Stylophora, Stylophora, Tubipora, Turbinaria, Turbinaria Acropora, Pocillopora

24

Symbiodinium clades

Riddle (2006)

C9, C44, C47

Porites Agaricia, Barabattoia, Caulastrea, Cyphastrea, Diploastrea, Diploria, Discosoma, Echinopora, Erythropodia, Favia,

Lobophyllia, Pocillopora, Stylophora, Turbinaria

LaJeunesse and others (2003, 2004)

Scleractinian genera Acropora, Agaricia, Coeloseris, Cyphastrea, Discosoma, Diploastrea, Diploria, Echinopora, Favia, Favites, Fungia, Galaxea, Goniastrea, Hydnophora, Isophyllastrea, Lobophyllia, Manicina, Merulina, Montipora, Montastrea, Mycetophyllia, Palythoa, Pectinia, Platygyra, Plesiastrea, Pocillopora, Porites, Scolymia, Seriatopora, Siderastrea, Stephanocoenia, Stylophora, Symphyllia, Turbinaria,

Clade reference LaJeunesse and others (2003)

Symbiodinium species designation

C4, C6, C7, C10–C14, C16–C18, C21, C24, C28, C30, C32, C33, C35–C43, C46, C48–C53, C56, C58, C59, C61, C65, C66, C72, C75, C77–C79 C8, C22, C34

Symbiodinium sub-clades

Table 1 (Continued)

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25

C57

C45, C54 C55, C60

C31

LaJeunesse and others (2003), LaJeunesse (2004) LaJeunesse and others (2003), Riddle (2006) LaJeunesse and others (2003), Pochon and others (2004) Pochon and others (2001), LaJeunesse and others (2003)

Pochon and others (2004) LaJeunesse and others (2003), Chen and others (2005) Pochon and others (2001), LaJeunesse and others (2003, 2004), LaJeunesse (2004)

C19 C26

C27

LaJeunesse and others (2003), Pochon and others (2004), Chen and others (2005)

C15

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Millepora

Favia, Isophyllia, Porites Platygyra, Porites

(Continued)

Alveopora, Fungia, Hydnophora, Millepora, Pachyseris, Pavona, Pavona Alveopora, Montipora

Favites, Fungia, Galaxea, Gardineroseris, Goniastrea, Heliofungia, Hydnophora, Isophyllastrea, Leptoria, Leptoseris, Lithophyllia, Lobophyllia, Merulina, Millepora, Montipora, Porites Acropora Montipora

26

F

D

Symbiodinium clades

F5

F1, F2

D2

D1

Symbiodinium sub-clades

S. kawagutii

Symbiodinium species designation

Pochon and others (2001), LaJeunesse and others (2003), LaJeunesse (2004), Chen and others (2005) Carlos and others (1999), Pochon and others (2001), Iglesias-Prieto and others (2004), Chen and others (2005) LaJeunesse (2001) Rodriguez-Lanetty and others (2002, 2005) LaJeunesse and others (2003) Santos and others (2002a), LaJeunesse and others (2003)

Baker (2001), Loh and others (2001), van Oppen and others (2001), Riddle (2006)

Clade reference

Table 1 (Continued)

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Montipora Alveopora Meandrina, Montipora Montipora

Agaricia, Acropora, Diploria, Montastrea, Pocillopora, Seriatopora, Siderastrea, Stephanocoenia Acropora, Echinopora, Euphyllia, Goniastrea, Hydnophora, Montipora, Oulastrea, Turbinaria Acropora, Goniopora, Pavona, Pocillopora

Scleractinian genera

27

B

A

Symbiodinium clades

S. bermudense S. pulchorum

S. corculorum S. meandrinae S. microadriaticum Gymnodinium linucheae S. cariborum

Symbiodinium species designation

(Continued)

Actiniaria Zoanthidea, Alcyonacea, Rhizostomea, Hydroida, Gorgonacea, Veneroida

Alcyonacea, Gorgonacea Actiniaria,

Hydroida, Gorgonacea, Veneroida, Foramniferida

Stat and others (2006) Goulet and Coffroth (2004) LaJeunesse and others (2003), LaJeunesse (2004), Riddle (2006) Rowan and Powers (1991b) Rowan and Powers (1991b)

Rhizostomea Actiniaria Zoanthidea Alcyonacea Rhizostomea

Veneroida Siphonophorae Gorgonacea, Veneroida Actiniaria

Order

Baillie and others (2000) Riddle (2006) Banaszak and others (2000) LaJeunesse and others (2003), Rodriguez-Lanetty and others (2002), Santos (2002a) LaJeunesse (2004) Rowan and Powers (1991b) Stat and others (2006) Stat and others (2006) Stat and others (2006)

Reference

Table 2 Symbiodinium clades associated with taxa other than scleractinian corals. Symbiodinium species designation shown along with the associated taxonomic group and the reference(s) for that association.

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28 LaJeunesse (2001) Pawlowski and others (2001), LaJeunesse in Pochon and others (2005) Pochon and others (2004)

F

G

H

LaJeunesse and Trench (2000) Stat and others (2006)

E

Foramnifera

Actiniaria, Alcyonacea, Foramniferida

Actiniaria, Foramnifera,

Actiniaria Veneroida

Actiniaria, Zoanthidea, Alcyonacea, Veneroida, Haplosclerida, Foramniferida, Oligotrichida,

Actiniaria, Alcyonacea, Gorgonacea, Leptothecatae, Siphonophorae, Triclada, Veneroida Actiniaria, Zoanthidea, Corallimorpharia, Alcyonacea, Rhizostomea, Hydroida, Gorgonacea, Veneroida, Nudibranchia, Foramniferida, Oligotrichida,

LaJeunesse and others (2003)

Rowan and Powers (1991b)

Siphonophorae, Alcyonacea

Order

Banaszak and others (2000) Goulet and Coffroth (2004)

Reference

Carlos and others (1999)

Gymnodinium varians S. californium

Symbiodinium species designation

D

C

Symbiodinium clades

Table 2 (Continued)

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Effects of Climate Change on Coral Reefs

29

van Oppen 2006)? The latter would be a result of natural selection, in which case betteradapted clades, previously rare in the population, become dominant (Buddemeier and Fautin, 1993; Baker 2001, 2003; Fabricius and others 2004; Sotka and Thacker 2004). Alternatively, their predominance may have been a result of an adaptive mutation. Whether or not these clades are indeed arising from selection, or mutation plus directional selection, they would still represent an excellent environmental bioindicator of climate change/global warming. One way to confirm this would be to first describe the DNA sequence of each previously existing clade along with that for each newly discovered one. One could then determine the temperature tolerances of each clade. After that, one could determine any changes which have occurred in frequency of occurrence of each clade through time (Baker and Romanski, 2007; Mieog and others, 2007).

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Predictions for the Future Some investigators claim that climate change is occurring too rapidly to allow adaptation in corals, and that they will not be able to keep pace with increasing SSTs and other environmental perturbations, such as ocean acidification (Munday 2004; Hoegh-Guldberg and others 2007; Fabricius 2008). The issue of zooxanthellar adaptation to temperature change has been investigated and reviewed extensively, and the reader is referred to that literature for further discussion. Here we discuss several other issues. It is known that susceptibility to increased seawater temperatures varies inter-specifically. This refers to both the onset of bleaching and resultant mortality. For example, Acropora spp. in the Indo-Pacific are known to be among the first scleractinians to bleach and the first group to experience mortality, if the bleaching is protracted (Strychar and others 2004a,c; Anthony and others 2007). More specifically, the zooxanthellae of A. hyacinthus are more sensitive to high temperatures than those in Porites solida and Favites complanata (Strychar and others 2004a). Some coral species also exhibit intra-specific variability in susceptibility to bleaching; i.e., some will bleach at different times and may also die at different times under the same environmental conditions. This variation (existing clades and sub-clades) is genetically based, which, of course, is necessary for natural selection to work and adaptation to occur. Interestingly, the host corals of the three species mentioned above do not exhibit heat sensitivity until the extreme temperatures of 34oC or higher (Strychar and Sammarco, 2009; see above and Fig. 5). If the corals could survive bleaching without their symbionts, they would clearly survive because of their exaptation to high seawater temperatures. Thus, we would predict that these species could potentially become less dependent on their symbionts, reverting to mutualism, commensalism, or, indeed, the absence of Symbiodinium altogether. It is known that certain soft corals, such as the octocoral Leptogorgia virgulata, which exhibits an extremely broad depth range, possesses zooxanthellae in shallow water yet is azooxanthellate in deeper water (S. France, pers. comm. to PWS). In this species, the symbiotic relationship is clearly facultative, as may be the case with other octocorals, particularly in the western Indo-Pacific (van Oppen and others, 2001, 2005). It is generally accepted that bleached corals tend to survive only about 6–8 weeks once they have lost their symbionts. In that case, it is possible that the cause of the coral’s death is starvation due to loss of carbohydrates produced by the zooxanthellae. In order to survive these conditions, they would have to increase their feeding rate to meet their energy requirements, as has been documented in Montipora capitata and Porites compressa under bleaching conditions (Grottoli and others 2006). In fact, in the 1950s, Goreau and Goreau (1960) were able to keep some species of corals alive for years in the dark

30

Sammarco and Strychar

while bleached by feeding them Artemia nauplii (also see Goreau and Goreau, 1959; Goreau and others, 1971; Pecheux, 1997). They believed that mortality was due to the cumulative effects of thermal stress and starvation. Leder and others (1991) were also able to keep bleached corals alive in a laboratory setting for 10–12 mos. In addition to requiring additional food, the coral host would have to be adapted or exapted to tolerate lower O2 levels, higher CO2 levels, or both—or to accommodate by decreasing its respiratory rate (Coles and Jokiel 1977; Rodrigues and Grottoli 2007).

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Acquistion of Replacement Symbiotic Species It is possible but unlikely that a coral that is bleached and has lost all of its zooxanthellae could acquire a new, more temperature-tolerant symbiont unrelated to Symbiodinium. An example might be the cyanobacterium Prochloron, thus far only reported to occur in sponges and didemnid ascidians (Larkum, 1999). In order to accept such a new symbiont, the coral would require a mutation (or set of mutations) permitting a new symbiont to be recognized as “self” to permit colonization of the host tissue. It would also be necessary for that new symbiont to be adapted to reproduce, sexually, asexually, or both, within the coral’s tissue in order to expand its population. The probability of all these characters aligning—in both the host and symbiont—would appear to be negligible (Belda-Baillie and others 2002). Nonetheless, in terms of evolutionary time, this scenario is possible. There are instances where a symbiotic partner has been successfully replaced with another phylogenetically distant partner (Douglas 2003). For example, arbuscular mycorrhizal fungi associated with the roots of trees have been replaced with ectomycorrhizal fungi (Brundrett 2002). Buchnera bacteria have been replaced by yeasts in aphids (Fukatsu and Ishikawa 1996). Plastids that contain peridinin have been replaced by endosymbiotic algae in some dinoflagellates (Saldarriaga and others 2001). The capability of corals to accept other symbionts is not known and has not yet been investigated. Latitudinal Expansion of Corals The oceans may be viewed as a large, deep basin of water heated from above by the sun. The tropical and subtropical seas may be viewed as a thin layer of warm water on top of this basin full of colder water. The width of the sub-tropical bands extend beyond the Tropics of Cancer and Capricorn, and the limits of the warm-water layer shift back and forth, north and south, with the change of the seasons. Increasing the heat of the earth’s atmosphere and thus of the surface of the ocean may be expected to expand the width of these sub-tropical limits by an amount on the order of hundreds of kms, and move the other climatic zones poleward with time (Kleypas and others, 1999). Increasing seawater temperatures cannot, at present, be tolerated by the symbionts of the scleractinian corals within the tropics and sub-tropics. The warming, however, is not restricted to these regions. Global warming is exactly that—increased SSTs throughout the world and its oceans, including the polar regions. Changes in cover of sea ice, glaciers, and snow which constitute the polar ice caps are good physical indicators of global warming. Symbiotic corals, and particularly their zooxanthellae, however, are probably the most sensitive of environmental bioindicators. Examples of other highly sensitive marine bioindicators would include bacteria (Merkley and others 2004), coastal invertebrates (Lawrence and Soame 2004), the early blooming of Arctic plants (Parmesan 2006; Jovan 2008), mis-timed reproduction in birds (e.g., Parus major; Visser and others 2004; Gaston

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Effects of Climate Change on Coral Reefs

31

and others 2005; Kudo and others 2008), changes in migration patterns and/or the timing of migrations (UNEP 2005), etc. Because of these temperature changes, each climatic zone is rising in average temperature (IPCC 2002; Science Daily 2007). This is documented to be ∼1oC since the late 19th Century (Le Treut 2007). The tropical zone may be expected to expand beyond 21oN and S latitude, while the sub-tropics will most likely retain the same latitudinal width but be moved towards the poles, encroaching on the sub-temperate zone (IPCC 2002). Likewise, the sub-temperate zones will also move poleward, encroaching on the temperate zones. The polar and sub-polar zones may, of course, be expected to shrink; this has been documented via satellite imagery (IPCC 2002), submarine reconnaissance (Science Daily 1998; NRC 2002), and oceanographic field observations (Kim 2007; IPCC 2007). This shrinking of the polar zone includes a shorter winter and extensive thinning of polar ice (Smetacek and Nicol 2005; WMO 2007; IPCC 2002, 2008). It is the encroachment of the sub-tropics into the sub-temperate zone that will permit coral reefs to develop in areas where they could not only a few decades ago (Precht and Aronson, 2004). Under these circumstances, we predict the following: 1) Corals will be able to colonize warmer marginal habitats. Hermatypic scleractinian corals known to thrive at the current latitudinal limits of their distribution will be the first colonizers of these new habitats. This has already been documented for Acropora palmata on the Flower Garden Banks, northern Gulf of Mexico (Zimmer and others, 2006). In addition to this, large thickets of A. cervicornis have been found in waters offshore from Broward County, Florida—well north of the previously known northernmost reefs on the eastern Florida coast—Key Biscayne (Vargas and others, 2003). Coral larvae are apparently already being dispersed to these regions, and changing climatic conditions are permitting them to survive there. 2) It is possible that a region closest to the equator could warm to the point where they become unable to support coral reefs, particularly if the zooxanthellae are not able to adapt their new environment. It is therefore possible that a new climatic zone could emerge in the vicinity of the equator, possibly to be labeled “The Hyper-Tropical Zone”, and might be characterized by tropical reefs with communities depauperate in hermatypic corals and other zooxanthellate organisms, if not devoid of them. 3) Because of the potential loss of hermatypic corals in the tropics, near the equator, the poleward movement of sub-tropical zones does not necessarily imply that coral reefs will increase in number or cover with time under global warming conditions. Although the distribution of coral reefs may be expected to expand poleward, the density of live reefs may also be expected to decrease in the tropics due to high levels of mass coral mortality there derived from temperature stress. 4) It is possible that, under conditions of excessively high SSTs and resultant geographical changes discussed above, overall species diversity of hermatypic scleractinian corals may well decline with time. This would occur if the dispersal capabilities of the corals cannot keep pace with changes in the geographic limits of climatic zones suitable to their survival. The decline will be characterized by extinction of those species most sensitive to high-temperature stress, e.g. most acroporids and pocilloporids (Marshall and Baird 2000), such as Acropora hyacinthus (Strychar and others 2004b). This also applies to some alcyonacean soft corals, e.g. Xenia sp (Goreau and others 2001; Strychar and others, 2005;), Lobophytum sp. (Paulay and Benayahu 1999; Michalek-Wagner and Willis 2001), and Sarcophyton sp. (Floros and others 2004, Strychar and others 2005). Those species that are less effective at dispersal may also experience a

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32

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decline. On the whole, the less effective dispersers are broadcasters (see Sammarco and others, 2004, 2007, 2008; Brazeau and others, 2005; Atchison and others, 2008). It has been demonstrated that brooding corals are much more successful at colonizing new habitats which have a patchy distribution at the meso-scale than broadcasting corals. This is due to the successful utilization of an island-hopping strategy of colonization, enhanced by frequent release of larvae with short planktonic periods over long periods of time throughout the year. On the other hand, broadcasters that reproduce only once per year and have longer obligate planktonic periods are less effective at dispersal and successful settlement. For these reasons, examples of likely candidates for local extinction might include, in the Indo-Pacific, Acropora hyacinthus and Favites complanata (Strychar and others 2004a) and, in the Caribbean, Montastraea annularis and Colpophyllia natans – all of which are broadcasters (see Bassim and others, 2002; Bassim and Sammarco, 2003; Sammarco and others, 2004; Atchison and others, 2008). Examples of species that would most likely successfully keep pace with changes in climatic zones would be Pocillopora damicornis and Stylophyra pistillata in the Indo-Pacific and Madracis decactis, Porites astreoides, and Montastraea cavernosa in the Caribbean. All of these species have broad geographic representation in their provinces (Veron, 2008) and recruit commonly in their habitats. This concept also applies to some alcyonacean soft corals in the Indo-Pacific. With respect to high temperature sensitivity, species such as Xenia sp., Sinularia sp., (Strychar and others 2005), Heteroxenia sp., Cespitularia sp., Efflatounaria sp., and Anthelia sp. might also be expected to exhibit local extinction (Goulet and others 2008). At higher latitudes, coral species diversity may be expected to increase as SSTs increase. 5) With climatic change, tropical and sub-tropical corals may also be expected to increase their depth distribution upon warming of the seas, but only by a small amount. As considering the analogy described above, the heating of the oceans’ surface from above by the sun is not efficient with respect to allowing that heat to be transmitted vertically, due to the relationship between heat and water density properties (see Garrison, 1999 for overview). We hypothesize that temperature regimes capable of supporting coral growth and survival may expand depth-wise by on the order of meters to 10 m. We would expect expansion of depth distributions to be much smaller and more subtle than latitudinal expansion.

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