At the time of transplanting, all colonies from the Keppels contained type C2 (sensu van Oppen et al. 2001
) zooxanthellae with ca
80% of A. millepora
colonies dominant in this type (). The remaining colonies were dominated by type D zooxanthellae, but also contained type C2 in lower abundance. Of the 22 Keppels colonies transplanted to Magnetic Island in July 2002, all bleached pale to white and seven colonies containing type C zooxanthellae died during the 2003 Austral summer (). By April 2003, all surviving colonies had regained their coloration and contained only type D zooxanthellae, including those that were originally dominated by C2. Of the 22 Davies Reef colonies transplanted to Magnetic Island in late February 2002, 13 survived the 2002 and 2003 summers, most bleaching pale to white at this time. All of these colonies contained only type C2 zooxanthellae at the time of transplantation and, in contrast to the Keppels colonies, recovered with the same strain (). Thus, of the transplanted corals, only the Keppel corals changed zooxanthella type, most likely as a direct result of the temperature-induced bleaching they underwent during the warm 2003 summer at Magnetic Island.
Figure 3 Condition and genotype of zooxanthellae in colonies of Acropora millepora (n=22) from Magnetic Island and those transplanted from Davies Reef and North Keppel Island at various time points leading up to the thermal stress experiment. Four Keppels colonies (more ...)
The C2 zooxanthellae harboured by A. millepora
colonies at Davies Reef differed in ribosomal DNA ITS1 sequence from the C2 zooxanthellae of their conspecifics from the Keppels (). Hence, these zooxanthellae represent a distinct strain and we refer to them as type C2*
. All 22 native Magnetic Island colonies transplanted onto racks at the same location in late February 2002 survived the 2002 and 2003 summers without bleaching and consistently harboured only type D zooxanthellae through time. The native Keppels population collected at the time of the temperature experiments were all dominant in type C2 zooxanthellae, indicating a slight change in the relative proportion of C- and D-zooxanthella types naturally over the 9 month transplantation period. This may reflect a natural population drift toward type C zooxanthellae as it recovered from the 2002 bleaching event (Berkelmans et al. 2004
; Elvidge et al. 2004
; van Oppen et al. 2005
). A similar drift back to pre-bleaching zooxanthella types was noted in three Montastraea
species in the Florida Keys following a bleaching event in 1998 (Thornhill et al. 2005
). The native Davies Reef population harboured only type C2*
zooxanthellae, unchanged over time (). The natural occurrence of particular zooxanthella strains in some areas and not others, and the apparent stability of coral–algal associations in some areas and not others, are important issues in understanding climate change effects on reefs. The association of corals and their symbionts is complex and considerable work is required to determine how these associations are shaped by biological and/or environmental factors.
Figure 4 (a) Single stranded conformation polymorphism (SSCP) profile of zooxanthellae from the five A. millepora populations (Davies native, Keppel Islands native, Magnetic Island native and the Davies and Keppel populations transplanted to Magnetic Island) after (more ...)
We tested the thermal tolerance limits of the transplanted (Keppels, Davies Reef) and native colonies (Magnetic Island, Keppels and Davies) under controlled experimental conditions and found that thermal tolerance among native populations was strongly linked with location. Corals from the Keppels population bleached at lower temperatures and more quickly than those from Davies. The photosynthetic yield of the C2 Keppels population diverged and was significantly different from the D and C2*
populations (Magnetic Island, Keppel transplants and Davies native and transplants) after 11 days at 30
°C and after 7 days at 31
°C (, ). Similarly, the C2*
Davies Reef corals were more sensitive than the D-dominant Magnetic Island and Keppel transplant corals, with photosynthetic yield significantly different after 7 days at 31
°C and after 3 days at 32
°C. The relative thermal sensitivity among these populations was also demonstrated by contrasting and significantly different patterns in zooxanthella density and the visual condition of corals after temperature treatment (unbleached, bleached, dead; , ). Having changed zooxanthella type from C to D, the thermal tolerance of the transplanted Keppels corals was indistinguishable from that of Magnetic Island D-dominated corals, the most thermally tolerant population. Photosynthetic yields of the Keppel transplants were not significantly different to those of the native Magnetic Island population at any of the treatment temperatures and at any time point during the experiment. Zooxanthella densities were significantly lower in the Keppels transplants compared with the Magnetic Island corals in all except the 32
°C post-experiment treatment, possibly indicating some variation in physiological response between these populations (a
). However, the reduced algal density in the Keppels transplants did not affect their ultimate thermal resistance, since their mortality was lower than the Magnetic Island corals at 32
°C (). Transplanted Davies Reef corals, having failed to alter zooxanthella type even after 14 months at Magnetic Island, performed as if they had never been transplanted. Photosynthetic yield and zooxanthella densities of transplanted and native Davies populations were not significantly different from each other at any of the treatment temperatures or time points during the experiment. Mortality was also comparable among these populations.
Figure 5 Pulsed amplitude modulation (PAM) fluorescence yield of dark-adapted Acropora millepora colonies from five populations over the time course of the experiment in each temperature treatment. Values are means of 18 nubbins±s.e. Magnetic Island: red, (more ...)
Repeated measures ANOVA results of arcsin-transformed PAM fluorescence yield over eight time points with time as the within-subjects factor.
Figure 6 Zooxanthella density±s.e. (bars) and coral condition (pies) of coral nubbins (n=18 per temperature treatment) before and after 15d of heat stress at control (27.5), 30, 31 and 32°C in each of five experimental populations: (more ...)
Mixed model ANOVA results of square root-transformed zooxanthellae densities.
These results indicate a causal link between zooxanthella type and thermal tolerance. Moreover, our data indicate that zooxanthella type is probably entirely responsible for levels of thermal tolerance in these A. millepora
populations, since the Davies transplanted population that retained its original zooxanthella type responded to thermal stress the same as its native counterparts, even after 14 months of transplantation. While coral host biochemistry (e.g. heat shock proteins and antioxidants) may play a role in regulating the biochemical processes of coral within tolerable limits (i.e. capacity acclimation), these processes appear to play little, if any, role in determining the final thermal tolerance of this species (i.e. resistance acclimation). Phenotypic plasticity or intraspecific genetic differences (we did not test for this here) may exist between the coral host populations, but the evidence suggests that these either have little measurable effect on temperature thresholds in A. millepora
, or only have an appreciable effect in the presence of type D zooxanthellae. Thus, the thermal tolerance of host–algal symbiosis appears to be dependent on the physiological characteristics of the zooxanthellae under temperature (and light) stress, with the zooxanthellae being the weakest link in the symbiotic partnership. Thermal tolerance among different zooxanthella types is in large part due to the thermal stability of the thylakoid lipid membranes of the chloroplasts, with sensitive types having lower concentrations of saturated polyunsaturated fatty acids and greater susceptibility to attack by reactive oxygen molecules which ultimately damages host cells (Tchernov et al. 2004
). The lack of acclimatization response in transplanted Davies Reef corals after 14 months in a warmer region compared to their native counterparts, without changing zooxanthella type, supports the conclusion of Tchernov et al. (2004)
that the zooxanthellae themselves have limited capacity to acclimatize. Their conclusion is based on the limited ability of zooxanthellae to modify their thylakoid membrane lipid composition, a trait held by eukaryotic algae capable of physiological acclimation.
These results indicate that autonomous thermal acclimatization/adaptation, mediated by zooxanthella change, is a real and naturally operating process in reef corals. As such, this study supports the adaptive bleaching hypothesis as originally proposed (Buddemeier & Fautin 1993
) and later refined (Buddemeier et al. 2004
), although not all populations appear to have the ability to change symbiont type. Whether the process of symbiont change in our Keppels population was brought about simply by a shuffling of the zooxanthella types already contained in the coral tissues, or was the result of taking up new types (‘switching’) from the environment is uncertain (Hoegh-Guldberg et al. 2002
). Zooxanthella switching has been observed experimentally in adult octocorals (Lewis & Coffroth 2004
), but so far not in adult stony corals. Since, type D zooxanthellae did exist in some of the Keppel corals and was not evident in the Davies population, even after a long period of transplantation and despite bleaching, the change is likely to have been a shuffling of existing zooxanthella types. Low background levels of zooxanthella type D (as low as ca
0.001%) have been detected using quantitative PCR methods in C-dominated Acropora valida
corals on the GBR (Ulstrup & van Oppen 2003
), suggesting that this strategy is potentially available to other coral populations and species. However, the fact that Davies transplants did not change symbiont type suggests that symbiont switching may only take place under certain conditions. We postulate that one of those conditions may be that a minimum background density of type D zooxanthellae is required in order for them to out-compete potentially faster reproducing type C zooxanthellae in the recovering host coral. Further research is required to substantiate this hypothesis.
The range of increased tolerance attained by A. millepora
from the Keppels with type D zooxanthellae was only marginally more than with the original C2 type. Nearly all native Keppels colonies were white after 15 days at 31
°C, whereas the transplants with D-type symbionts were all healthy at this temperature, but at 32
°C, more than 40% were white or dead. Since the photosynthetic fitness of the type D transplants was deteriorating rapidly at 32
°C, it is unlikely that they would survive 33
°C under these experimental conditions. Thus, the increased tolerance of Keppel corals with type D zooxanthellae is only about 1–1.5
°C. While this is likely to be of huge ecological benefit, it may not be enough to help these populations cope with the predicted increases in average tropical
sea temperatures over the next 100 years (1–3
°C, multi-model ensemble; IPCC 2001
). It may, however, be enough to ‘buy time’ while measures are put in place to reduce greenhouse gas emissions. Thus, while our results suggest that considerable capacity may exist for rapid acclimatization of corals and thus are a nugget of hope for coral reefs in an era of climate change, it is unclear how many coral species, and populations within species, are likely to benefit from this acclimatization mechanism and hence what the overall implications are for coral reefs. What it does highlight, however, is that corals harbouring mixed symbiont populations are likely to have a distinct ecological advantage over those that do not, in terms of their ability to cope and respond rapidly to thermal stress events. Understanding the response of reefs to climate change, and any management actions in ameliorating additional threats, is likely to benefit greatly from an improved understanding of the conditions under which corals can change symbiont type, the biogeography of zooxanthellae and the factors shaping the interaction of zooxanthellae with their coral hosts.