Effects of enhanced climate change and sea level rise on shallow-water reef corals: an experimantal analysis of coral demographic and photophysiological responses to depth changes

As a result of predicted global climate changes, over the next century eustatic sea level is expected to rise around 5 cm / decade and sea-surface temperatures are expected to increase by 2°C, concurrent with greater seasonal and inter-annual climatic variability. This study assesses the potential consequences of depth changes on three species of common shallow-water reef corals, Goniastrea retiformis Lamarck, Acropora aspera Dana and Acropora millepora Ehrenberg. Field transplant experiments conducted from 1992 to 1994 were used to simulate sea level rises and to determine the effects of depth increases of 25 cm, 50 cm and 1 m on the size-specific demographic and photophysiological responses of the corals. The feasibility of using transplant experiments to simulate predicted sea level rise was assessed, and the long-term effects of depth changes on the demography of the corals was quantified using size-structured population projection models.\ud \ud The three species responded differently to depth changes because of differences in their morphology and life history traits (G. retiformis > A. aspera > A. millepora). Massive colonies of G. retiformis, which had high rates of survival (ca. 84% / year) and slow rates of linear growth (ca. 6 mm / year), exhibited no change in rates of survival in response to a 1 m depth change after 12 months, relative to controls. Of the three species, branching colonies of A. aspera which also had high rates of survival (ca. 83% / year) but fast rates of linear growth (ca. 46 mm / year), exhibited a 19%, 40% and 100% decrease in annual rates of survival in response to depth changes of 25 cm, 50 cm and 1 m respectively, relative to controls. Corymbose colonies of A. millepora which had low rates of survival (ca. 56% / year) and moderate rates of linear growth (ca. 22 mm / year), exhibited major reductions in annual rates of survival of 34%, 85% and 100% in response to depth changes of 25 cm, 50 cm and 1 m respectively, relative to controls. Rates of linear growth and colony fecundity decreased with increasing depth in all species, but this trend was particularly marked in A. millepora, even in response to a depth change of 25 cm. Therefore, rises in sea level of 25 cm, 50 cm or 1 m may significantly affect rates of coral survival, growth and fecundity, particularly for short-lived colonies of A. millepora, which are the most vulnerable to changes in environmental conditions. Because rises in sea level may affect species differently, they have the potential to alter the relative abundance and diversity of species in extant assemblages of shallow-water reef corals.\ud \ud Colonies of A. millepora were more capable of photoadaptation in response to depth-related alterations in light after 10 months, compared to those of A. aspera. Photoadaptation by A. millepora in response to depth increases of 25 cm and 50 cm was manifested by marked increases in photopigment content per zooxanthellate cell (ca. 65% & 142%, respectively, c.f. the controls). These changes occurred with concurrent reductions in zooxanthellae densities and tissue mass index (estimates of tissue volume). In contrast, the more perforate A. aspera (with 24% more endodermal and gastrodermal tissue than A. millepora), maintained zooxanthellae densities in response to depth changes of 25 cm and 50 cm, and showed little ability to increase photopigment contents per zooxanthellate cell. Despite the ability of A. millepora to photoadapt to depth-related changes in visible light, its survival was significantly lower than A. aspera, which showed little ability to photoadapt.\ud \ud The acclimatization ability of A. aspera and A. millepora in response to sequential increases in depth was determined, and used to assess the feasibility of using transplant experiments to simulate more gradual rates of sea level rise. Rates of colony survivorship in response to stepwise changes in depth did not differ from those exhibited in response to direct depth changes in either of the two species. This indicates that direct transplantation of these species provides an adequate proxy to determine how corals respond to more gradual changes in sea level.\ud \ud For the purposes of demographic analyses, the corals on experimental racks at depths of 25 cm, 50 cm and 1 m were considered as separate populations. Their projected demographic fate over 50 years at these depths was assessed. Projection models show that the length of time the populations will persist at different depths is limited, particularly at deeper sites, and depends on their resilience in response to environmental conditions and the proficiency of their reproductive strategies. Without sexual recruitment, populations of A. millepora would be the first to disappear from deeper sites as sea level rises 25 cm or 50 cm, within an estimated 6 and 2 years, respectively, from their initial depth change. In contrast, populations of A. aspera could potentially persist indefinitely in response to a 25 cm sea level rise without recruitment, because of their propensity for asexual propagation. However, the difference in environmental conditions between a 25 cm and 50 cm sea level rise would exceed the resilience threshold for populations of A. aspera. Without sexual recruitment, they would only persist for 6 years in response to a 50 cm rise in sea level, because gains through asexual propagation would be exceeded by losses through higher rates of mortality. Populations of G. retiformis would be the last to disappear from deeper sites as sea level rises, because they could persist for an estimated 22 years without recruitment, even in response to a 1 m rise in sea level. The recruitment rates required for populations to persist indefinitely at deeper sites, were estimated through matrix model simulations. Based on these estimates and previous accounts of net rates of recruitment observed in field populations for these species, it is unlikely that sufficient recruitment would occur at deeper sites, and as a consequence extant populations of these corals would not persist significantly longer than predicted above.\ud \ud Extant colonies of the three species located in very shallow reef sites may survive a rise in sea level, but survival could depend on colony size. Photophysiological studies show that large colonies of A. millepora could photoadapt and increase photopigment contents per unit tissue volume more effectively than smaller ones. Therefore, if small colonies of A. millepora cannot rapidly attain a size at which they may photoadapt more effectively, they may not persist even at this depth. Demographic studies also show that mortality patterns in all three species were inversely related to colony size. Therefore, if small colonies cannot rapidly attain a size refuge from mortality, they may not persist despite remaining within the depth confines of the species, particularly those of G. retiformis which have slow rates of areal and linear growth. These results indicate that while extant colonies may disappear from deeper sites in response to a sea level rise, they may also disappear from sites where old and new distributions overlap.\ud \ud The persistence of the three species in response to sea level rise will depend on their ability to colonize presently unsuitable shallow reef sites. Acropora millepora and G. retiformis are more reliant on sexual reproduction than A. aspera, which may persist through asexual propagation. Based on previous limited accounts of recruitment rates observed in field populations, it is likely that A. millepora will colonize new sites at the greatest rate, and G. retiformis the lowest. Acropora aspera, which showed much lower rates of sexual recruitment than the other species, may colonize new sites through clonal propagation. Alterations in sea state or increases in the frequency and intensity of tropical storms are likely to enhance the dispersal of dislodged branch fragments of A. aspera and increase the chances of their establishment in new sites.\ud \ud The persistence of the species following sea level rise will also depend on the ability of recruits to endure exposure to any physical stresses associated with enhanced climate change. Following a partial bleaching event, coincident with extreme summer temperatures ranging from 18.5 to 33.6°C, all species readily recovered irrespective of their morphology. This indicates thata gradual rise in sea-surface temperatures of 2°C over the next century, which could resultin partial bleaching, may have little affect on these shallow reef coral species. A more rapid increase in sea-surface temperatures or greater extremes, may significantly affect recruits, particularly those of A. millepora, which are likely to be the most vulnerable to seasonal mortality.\ud \ud This study indicates that corals will respond differently to rises in sea level and enhanced climate change, because of differences in their morphology, life history traits and reproductive strategies. Short-lived genets, like A. millepora, with the least resilience to changes in environmental conditions may be the most useful bioindicators of early responses of coral reef ecosystems to environmental change. Long-lived clones, like A. aspera, with much lower rates of sexual recruitment and therefore little ability for genotypic adaptation, may be the most vulnerable to the long-term effects of enhanced climate change and sea level rise