Limits...
The roles and interactions of symbiont, host and environment in defining coral fitness.

Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJ - PLoS ONE (2009)

Bottom Line: Our results showed that: (1) Symbiodinium type was the most important predictor of holobiont fitness, as measured by growth, survival, and thermo-tolerance; (2) growth and survival, but not heat-tolerance, were also affected by local environmental conditions; and (3) host population had little to no effect on holobiont fitness.Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora.An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.

View Article: PubMed Central - PubMed

Affiliation: Australian Institute of Marine Science, Townsville, Queensland, Australia. josmieog@gmail.com

ABSTRACT

Background: Reef-building corals live in symbiosis with a diverse range of dinoflagellate algae (genus Symbiodinium) that differentially influence the fitness of the coral holobiont. The comparative role of symbiont type in holobiont fitness in relation to host genotype or the environment, however, is largely unknown. We addressed this knowledge gap by manipulating host-symbiont combinations and comparing growth, survival and thermal tolerance among the resultant holobionts in different environments.

Methodology/principal findings: Offspring of the coral, Acropora millepora, from two thermally contrasting locations, were experimentally infected with one of six Symbiodinium types, which spanned three phylogenetic clades (A, C and D), and then outplanted to the two parental field locations (central and southern inshore Great Barrier Reef, Australia). Growth and survival of juvenile corals were monitored for 31-35 weeks, after which their thermo-tolerance was experimentally assessed. Our results showed that: (1) Symbiodinium type was the most important predictor of holobiont fitness, as measured by growth, survival, and thermo-tolerance; (2) growth and survival, but not heat-tolerance, were also affected by local environmental conditions; and (3) host population had little to no effect on holobiont fitness. Furthermore, coral-algal associations were established with symbiont types belonging to clades A, C and D, but three out of four symbiont types belonging to clade C failed to establish a symbiosis. Associations with clade A had the lowest fitness and were unstable in the field. Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora.

Conclusions/significance: These results highlight the complex interactions that occur between the coral host, the algal symbiont, and the environment to shape the fitness of the coral holobiont. An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.

Show MeSH

Related in: MedlinePlus

Heat-stress experiment 1: PAM-fluorometry.Effect of four different temperature regimes on the excitation pressure over photosystem II of four groups of juvenile coral outplanted to Magnetic Island. See materials and methods for nomenclature. L:D = light-dark regime, $ = target temperature is reached, # = significant difference between C1 corals and D corals. C1 corals responded stronger to the highest temperature treatment than D corals, as indicated by a stronger increase in Q for C1 corals towards the end of the experiment.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2710517&req=5

pone-0006364-g002: Heat-stress experiment 1: PAM-fluorometry.Effect of four different temperature regimes on the excitation pressure over photosystem II of four groups of juvenile coral outplanted to Magnetic Island. See materials and methods for nomenclature. L:D = light-dark regime, $ = target temperature is reached, # = significant difference between C1 corals and D corals. C1 corals responded stronger to the highest temperature treatment than D corals, as indicated by a stronger increase in Q for C1 corals towards the end of the experiment.

Mentions: This experiment compared the thermal tolerances of four coral groups outplanted to Magnetic Island (MMC1, MMD, MKC1, MKD corals). There was a significant difference in photosynthetic performance, measured as the excitation pressure on PSII (Q), between C1 corals (MMC1 and MKC1 corals) and D corals (MMD and MKD corals, Fig. 2 and Table 1c). In contrast, no significant effect of host population origin (i.e., host genetic background) over time was found (Table 1c). At the intermediate temperatures (30.5 and 31.5°C, Fig. 2b, c), the Q of C1 corals decreased at the beginning of the experiment, whereas the Q of D corals remained mostly level, resulting in a significantly lower Q for C1 corals (p<0.05) for most of the experiment. Exposure to 32.5°C (Fig. 2d) initially resulted in a similar reduction of Q in C1 corals (not seen in the D corals), but after ∼11 days of exposure, Q increased in the C1 corals to exceed the Q of D corals by the end of the experiment (p<0.05). The Q of the D corals showed a smaller increase at the end of the experiment. These results were interpreted to indicate a lower thermo-tolerance of C1 corals compared to D corals. This difference in thermo-tolerance was further supported by an earlier and stronger reduction in Fv/Fm for C1 corals than for D corals at 32.5°C (supporting information, Fig. S3).


The roles and interactions of symbiont, host and environment in defining coral fitness.

Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJ - PLoS ONE (2009)

Heat-stress experiment 1: PAM-fluorometry.Effect of four different temperature regimes on the excitation pressure over photosystem II of four groups of juvenile coral outplanted to Magnetic Island. See materials and methods for nomenclature. L:D = light-dark regime, $ = target temperature is reached, # = significant difference between C1 corals and D corals. C1 corals responded stronger to the highest temperature treatment than D corals, as indicated by a stronger increase in Q for C1 corals towards the end of the experiment.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2710517&req=5

pone-0006364-g002: Heat-stress experiment 1: PAM-fluorometry.Effect of four different temperature regimes on the excitation pressure over photosystem II of four groups of juvenile coral outplanted to Magnetic Island. See materials and methods for nomenclature. L:D = light-dark regime, $ = target temperature is reached, # = significant difference between C1 corals and D corals. C1 corals responded stronger to the highest temperature treatment than D corals, as indicated by a stronger increase in Q for C1 corals towards the end of the experiment.
Mentions: This experiment compared the thermal tolerances of four coral groups outplanted to Magnetic Island (MMC1, MMD, MKC1, MKD corals). There was a significant difference in photosynthetic performance, measured as the excitation pressure on PSII (Q), between C1 corals (MMC1 and MKC1 corals) and D corals (MMD and MKD corals, Fig. 2 and Table 1c). In contrast, no significant effect of host population origin (i.e., host genetic background) over time was found (Table 1c). At the intermediate temperatures (30.5 and 31.5°C, Fig. 2b, c), the Q of C1 corals decreased at the beginning of the experiment, whereas the Q of D corals remained mostly level, resulting in a significantly lower Q for C1 corals (p<0.05) for most of the experiment. Exposure to 32.5°C (Fig. 2d) initially resulted in a similar reduction of Q in C1 corals (not seen in the D corals), but after ∼11 days of exposure, Q increased in the C1 corals to exceed the Q of D corals by the end of the experiment (p<0.05). The Q of the D corals showed a smaller increase at the end of the experiment. These results were interpreted to indicate a lower thermo-tolerance of C1 corals compared to D corals. This difference in thermo-tolerance was further supported by an earlier and stronger reduction in Fv/Fm for C1 corals than for D corals at 32.5°C (supporting information, Fig. S3).

Bottom Line: Our results showed that: (1) Symbiodinium type was the most important predictor of holobiont fitness, as measured by growth, survival, and thermo-tolerance; (2) growth and survival, but not heat-tolerance, were also affected by local environmental conditions; and (3) host population had little to no effect on holobiont fitness.Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora.An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.

View Article: PubMed Central - PubMed

Affiliation: Australian Institute of Marine Science, Townsville, Queensland, Australia. josmieog@gmail.com

ABSTRACT

Background: Reef-building corals live in symbiosis with a diverse range of dinoflagellate algae (genus Symbiodinium) that differentially influence the fitness of the coral holobiont. The comparative role of symbiont type in holobiont fitness in relation to host genotype or the environment, however, is largely unknown. We addressed this knowledge gap by manipulating host-symbiont combinations and comparing growth, survival and thermal tolerance among the resultant holobionts in different environments.

Methodology/principal findings: Offspring of the coral, Acropora millepora, from two thermally contrasting locations, were experimentally infected with one of six Symbiodinium types, which spanned three phylogenetic clades (A, C and D), and then outplanted to the two parental field locations (central and southern inshore Great Barrier Reef, Australia). Growth and survival of juvenile corals were monitored for 31-35 weeks, after which their thermo-tolerance was experimentally assessed. Our results showed that: (1) Symbiodinium type was the most important predictor of holobiont fitness, as measured by growth, survival, and thermo-tolerance; (2) growth and survival, but not heat-tolerance, were also affected by local environmental conditions; and (3) host population had little to no effect on holobiont fitness. Furthermore, coral-algal associations were established with symbiont types belonging to clades A, C and D, but three out of four symbiont types belonging to clade C failed to establish a symbiosis. Associations with clade A had the lowest fitness and were unstable in the field. Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora.

Conclusions/significance: These results highlight the complex interactions that occur between the coral host, the algal symbiont, and the environment to shape the fitness of the coral holobiont. An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.

Show MeSH
Related in: MedlinePlus