Trophic strategy and bleaching resistance in reef-building corals

Abstract

Ocean warming increases the incidence of coral bleaching, which reduces or eliminates the nutrition corals receive from their algal symbionts, often resulting in widespread mortality. In contrast to extensive knowledge on the thermal tolerance of coral-associated symbionts, the role of the coral host in bleaching patterns across species is poorly understood. Here, we applied a Bayesian analysis of carbon and nitrogen stable isotope data to determine the trophic niche overlap between corals and their symbionts and propose benchmark values that define autotrophy, heterotrophy, and mixotrophy. The amount of overlap between coral and symbiont niche was negatively correlated with polyp size and bleaching resistance. Our results indicated that as oceans warm, autotrophic corals lose their competitive advantage and thus are the first to disappear from coral reefs.

Fig. 1. SIBER analysis of paired coral host and algal symbiont stable isotope data.

Across species, there is variation in the overlap of the isotopic niches of the coral (purple) and algal (green) partners indicating trophic strategies that fall on a continuum ranging from autotrophic [(A) Acropora and (B) Goniopora] to mixotrophic [(C) Porites and (D) Pavona] to heterotrophic [(E) Turbinaria, (F) Favites, and (G) Platygyra). See bottom right for a key to (A) to (G). Dotted lines represent convex hulls, solid lines represent Standard Ellipse Areas corrected for sample size (SEA_c). Significant P values generated from a Residual Permutation Procedure and Hotelling’s T² test indicate genera where coral and symbiont niches occupy distinct isotopic spaces. The corallite area of each species is displayed relative to the largest corallite area included in this study (F. abdita; 49.9 mm²). Photo credit: Philip D. Thompson, The University of Hong Kong.

Fig. 2. Correlation between corallite area and trophic strategy.

Corallite area, a proxy for polyp area, was significantly correlated with two estimates of trophic strategy: (A) the distance between the centroid (mean) of host and symbiont SEA_c ellipses generated with SIBER analysis and (B) the difference of host and symbiont δ¹⁵N. SEA_cs were fitted to δ¹⁵N and δ¹³C values measured in Acropora, Favites, Goniopora, Pavona, Porites, Platygyra, and Turbinaria collected in the field, while δ¹⁵N_Host − δ¹⁵N_Symbiont values were calculated from δ¹⁵N values of eight species grown in a common garden: A. samoensis, A. pruinosa, F. abdita, G. lobata, P. decussata, P. lobata, P. carnosus, and T. peltata. The colors and shapes of the points indicate trophic strategy, as determined from the isotopic niche separation of hosts and symbionts in field samples (i.e., distance between host and symbiont ellipse centroids).

Fig. 3. Mean daily water temperature and number of DHW (degree heating weeks) from days 45 to 70 of the warming experiment.

Mean daily water temperature (orange line; error bars represent SD) and number of DHW [goldenrod line; a measurement of accumulated thermal stress that incorporates both magnitude and duration; see (44)] from days 45 to 70 of the warming experiment. The gray dashed line indicates the maximum monthly mean [the temperature above which corals experience thermal stress (44)] water temperature of a Hong Kong coral community over the past 10 years. The vertical lines indicate the day when >50% of the individuals within a species bleached as determined with color cards (41). The vertical line color indicates the trophic strategy of each species, as determined from the isotopic niche separation of hosts and symbionts in field samples (i.e., amount of overlap between host and symbiont isotopic niches). Photo credit: Nara L. Oliveira, Universidade Estadual de Santa Cruz.

Fig. 4. Correlation between bleaching resistance and trophic strategy.

Bleaching resistance of seven coral species was significantly correlated with three different estimates of trophic strategy (A) the distance between the centroid (mean) of host and symbiont standard ellipse areas corrected for sample size (SEA_c) generated by SIBER analysis, (B) the proportion of host SEA_c overlapping the symbiont SEA_c, and (C) the difference of host and symbiont δ¹⁵N. SEA_cs were fitted to δ¹⁵N and δ¹³C values measured in Acropora, Favites, Goniopora, Porites, Platygyra, and Turbinaria collected in the field while δ¹⁵N_Host − δ¹⁵N_Symbiont values were calculated from δ¹⁵N values of seven species grown in a common garden: A. samoensis, A. pruinosa, F. abdita, G. lobata, P. lobata, P. carnosus, and T. peltata. The colors and shapes of the points indicate the trophic strategy as determined from isotopic niche separation of hosts and symbionts in field samples.

Fig. 5. Correlation between bleaching resistance and corallite area under field conditions.

Despite uncontrolled field conditions, corallite area (a proxy for trophic strategy) explains 43% of the variation in bleaching susceptibility among corals off the east coast of Africa during the 1997 bleaching event (28). Black line represents a power function fit to the data using a square root transformation of corallite area. A power function was chosen in consideration of the upper and lower bound constraints on percentage of minimum and maximum corallite diameters used in the calculation of corallite area. Corallite diameter values were extracted from the Coral Trait Database (–54).