Inter- and intra- specific variation in bleaching susceptibility among scleractinian corals

Bradbury, Dominique (2013) Inter- and intra- specific variation in bleaching susceptibility among scleractinian corals. PhD thesis, James Cook University.

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Abstract

Coral bleaching is the disassociation (either expulsion or degradation) of zooxanthellae and the coral host, and it is a general stress response of corals. Anomalous sea surface temperatures have caused widespread incidence of bleaching referred to as mass bleaching; however, chronic, longer-term stress from global climate change is also potentially increasing coral vulnerability to subsequent stress. Sustained and ongoing increases in sea surface temperatures are expected to result in greater incidence of mass bleaching of scleractinian corals, assuming that corals are incapable of acclimating or adapting at required rates. Acclimation is a short-term relief from stress, such as producing heat shock proteins; whereas, adaptation works on populations, hence would use natural selection to produce corals that are more tolerant to stress. A significant limitation in assessing the fate of corals subject to changing environmental conditions is a precise quantitative metric for measuring incidence and severity of coral bleaching. In the field, bleaching is often reported based on the conspicuous "paling" of individual coral colonies, species, or assemblages, but there is not currently a clear and unambiguous definition that can be used to say exactly when individual corals (or populations) are bleached. The purpose of this thesis was to compare among alternative methods used to quantify the incidence and severity of coral bleaching, both at the level of individual colonies and local populations or species, to establish a rigorous quantitative definition for coral bleaching. Bleaching, therefore, can be defined as a loss of greater than half of the zooxanthellae population density, concurrent with rapid changes in physiological quenching efforts, and often displayed as a colour change of 2-3 shades. This metric was then used to explore taxonomic, spatial (geographical), and temporal variation in bleaching susceptibility among scleractinian corals.

Chapter 2 of the thesis focused on measures of zooxanthellae density, specifically testing for intraspecific variation in zooxanthellae densities of the common reef coral, Acropora millepora, in the Palm Islands, inshore Great Barrier Reef. Various methods are available to quantify zooxanthellae densities; however, a direct comparison of these techniques has yet to be done. Here, we compare destimates of zooxanthellae densities obtained using conventional airbrushing coupled with post-tissue-blasting surface area determination, versus a technique whereby zooxanthellae densities are quantified from a known area (0.25 cm²) of tissue after corals have been fixed and decalcified. Estimates of zooxanthellae densities obtained using the two different methods were significantly correlated (R=0.40, n=81, p<0.01), such that both techniques revealed similar patterns of variation among locations. The main benefit of the decalcification technique was reduced handling time, because the technique eliminates the time-consuming process of tissue blasting and retrospective estimates of surface area. We estimate that decalcification halves the handling time per sample, and produces a more accurate estimate of zooxanthellae density.

Chapter 3 analysed published estimates of zooxanthellae densities for a wide range of different corals and locations, testing whether there are consistent thresholds that distinguish bleached versus unbleached corals. Moreover, zooxanthellae densities are naturally regulated (e.g. due to season, light availability), so an important point to this chapter was to determine if bleaching could be distinguished from these natural variations in zooxanthellae densities. Normal zooxanthellae densities ranged from 0.1x10⁶ cells/cm² up to 18.0 x 10⁶ cells/cm²; whereas, zooxanthellae densities reported for bleached corals were between 0.001 and 6.5 x10⁶ cells/cm². Marked variation in published estimates of zooxanthellae densities was largely attributable to differences in the methods among studies (e.g. size of tissue sample, method of tissue removal and surface area determination), though there were significant and consistent differences among coral species, with growth form and with depth. It is not possible therefore, to establish a single threshold density of zooxanthellae that distinguished bleached and unbleached corals. However, after accounting for taxa (genera) it does appear that relative changes in zooxanthellae densities are a good indication of the fate of individual corals. In the absence of distinct bleaching events, natural variation in zooxanthellae densities (e.g., among seasons) was typically <50% of the mean. During bleaching events however, zooxanthellae loss within individual corals often ranged from 55-100%. Moreover, corals that experienced >78% zooxanthellae loss almost invariably died, whereas those corals that lost 55-77% of zooxanthellae were bleached, but generally recovered. Sub-lethal bleaching caused by pollutants did not adhere to the bleaching definition, as conspicuous loss of zooxanthellae density was often observed at levels of what is considered “natural variation”. For other stresses however, (and particularly, thermal stress) it may be possible to define when corals have bleached, and predict their fate based on proportional declines in zooxanthellae densities.

To specifically test for inter- and intra-specific variation in bleaching susceptibility, Chapter 4 exposed twenty whole colonies of Acropora nasuta and Pocillopora damicornis to controlled warming in experimental facilities (with carefully controlled light and temperature environments) at Orpheus Island. Corals, after acclimated to laboratory conditions, were subjected to a simulated warm water anomaly, with a slow rate of increase of 0.5°C every third day until they reached 31.6°C, which is equivalent to the 1998 temperature anomaly that lead to extensive mass bleaching of scleractinian corals in the central Great Barrier Reef, Australia. Daily observations of coral health were made with coral colour charts and Pulse- Amplitude Modulated Fluorometry measurements; corals were considered to have bleached when marked changes in the quenching analyses occurred simultaneously with a change in 2- 3 shades of colour. Post hoc measurements of zooxanthellae densities were used to confirm when bleaching occurred. There was marked variation in the time to bleaching both within and among coral species. For A. nasuta, the mean time to bleach was 8 days, but ranged 12 days, while, for P. damicornis, mean time to bleach was 12 days and ranged 15 days. Moreover, both corals showed phenotypic variation in the timing of bleaching responses, therefore there may be underlying genetic variation upon which the corals could adapt.

Chapter 5 explored temporal changes in bleaching susceptibility among key genera of reef-building corals in Moorea, French Polynesia, comparing bleaching incidence of four genera (Acropora, Montipora, Pocillopora and Porites) during mass-bleaching events in 1991, 1994, 2002 and 2007. Acropora and Montipora consistently bleached in far greater proportions (up to 98%) than Pocillopora and Porites. However, there was an apparent and sustained decline in the proportion of colonies that bleached during successive bleaching events, especially for Acropora and Montipora. Coral genera that are highly susceptible to coral bleaching, and especially Acropora and Montipora, exhibited temporal declines in their susceptibility to thermal anomalies at Moorea, French Polynesia. One possible explanation for these findings is that gradual removal of highly susceptible genotypes (through selective mortality of individuals, populations, and/ or species) is producing a coral assemblage that is more resistant to sustained and ongoing ocean warming.

Chapter 6 tests whether taxonomic variation in bleaching susceptibility and mortality is spatially consistent among geographic regions, comparing extensive data sets from the Indian, Pacific and Atlantic oceans. Data was compiled from 105 distinct studies, spanning the Pacific, Indian and Atlantic Oceans, and from 1982 to 2013. Differences in bleaching susceptibility and mortality were apparent among different coral genera, but the hierarchy of bleaching susceptibility differed on geographic scales, among ocean basins. These large-scale differences may be attributable to inherent differences in biology (e.g., geographic variation in associations between corals and their symbionts), but may also reflect taxonomic differences in the capacity of corals to acclimate or adapt when facing extreme environmental changes. Among decades, it is apparent that bleaching susceptibility and mortality have generally declined over time, possibly reflecting increased bleaching resistance at the level of populations or communities due to selective removal of highly susceptible phenotypes.

This thesis shows that there is phenotypic variation at many scales within and among corals. For instance, phenotypic variation was found in mean zooxanthellae densities, both within and among species. Then, phenotypic variation was observed as marked variation in the timing of the bleaching response within and between two commonly susceptible coral species. Next, phenotypic variation was observed for a bleaching event, where the proportion of susceptible corals decreased over the course of time. Most notably, however, there is marked variation in bleaching susceptibility among different coral taxa, which is likely to lead to directional shifts in the structure of coral assemblages with increasing incidence of mass-bleaching. Establishing exactly how these assemblages will change is, however, critically dependent on understanding species-specific susceptibility to bleaching and recovery capacity of these corals in the aftermath of periodic bleaching events. Future research needs to focus much more on the longer-term fate of coral colonies, populations and species subject to ongoing bleaching.

Item ID: 33425
Item Type: Thesis (PhD)
Keywords: Acropora millepora; bleaching susceptibility; climate change; coral bleaching; coral loss; coral reefs; coral stress response; global warming; mass bleaching; scleractinia; scleractinian corals; zooxanthellae densities
Additional Information:

Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Mccowan, Dominique. M. , Pratchett, Morgan, Paley, Allison, Seeley, Michelle, and Baird, Andrew (2011) A comparison of two methods of obtaining densities of zooxanthellae in Acropora millepora. Galaxea, Journal of Coral Reef Studies, 13. pp. 29-34.

Chapter 5: Pratchett, Morgan S., McCowan, Dominique, Maynard, Jeffrey A., and Heron, Scott (2013) Changes in bleaching susceptibility among corals subject to ocean warming and recurrent bleaching in Moorea, French Polynesia. PLoS ONE, 8 (7). pp. 1-10.

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Date Deposited: 25 Jun 2014 05:35
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 100%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 50%
96 ENVIRONMENT > 9603 Climate and Climate Change > 960307 Effects of Climate Change and Variability on Australia (excl. Social Impacts) @ 50%
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