Does Trophic Status Enhance or Reduce the Thermal Tolerance of Scleractinian Corals? A Review, Experiment and Conceptual Framework

Global warming, and nutrient and sediment runoff from coastal development, both exert increasing pressures on coastal coral reefs. The objective of this study was to resolve the question of whether coastal eutrophication may protect corals from thermal stress by improving their nutritional status, or rather diminish their thermal tolerance through the synergy of dual stressors. A review of previous studies on the topic of combined trophic status and heat exposure on the thermal tolerance of corals reveals a broad range of outcomes, including synergistic, additive and antagonistic effects. We conducted a 90-day long experiment exposing corals to realistic levels of elevated nutrients and sediments, and heat stress. Colonies of two common scleractinian corals (Acropora millepora and Montipora tuberculosa) were kept in coastal seawater, or coastal seawater that was further organically and nutrient enriched (OE), and/or enriched with nitrate. Batches of OE were created daily, facilitating nutrient uptake, plankton succession and organic enrichment as observed in coastal waters. After 10 days of acclimation, 67% of the colonies had their temperature gradually increased from 27° to 31.2°C. After 3–7 weeks of heat stress, colonies of both species had significantly greater reductions in fluorescence yields and lower survival in OE than without addition of OE. Furthermore, photophysiological recovery was incomplete 31–38 days after ending the heat stress only in the OE treatments. Nitrate alone had no measurable effect on survival, bleaching and recovery in either species. Skeletal growth rates were reduced by 45% in heat-stressed A. millepora and by 24% in OE-exposed M. tuberculosa. We propose a conceptual trophic framework that resolves some of the apparently contradictory outcomes revealed by the review. Our study shows that management actions to reduce coastal eutrophication can improve the resistance and resilience of vulnerable coastal coral reefs to warming temperatures

Effects of organic enrichment and nitrate on the survival of heat-stressed and control corals.

<p>Survival of <i>Acropora millepora</i> (a, b) and <i>Montipora tuberculosa</i> (c, d) at the end of the recovery period for the treatments of temperature (25°C (a, c) vs. 31°C (b, d), organic enrichment (+OE), and/or nitrate addition (+NO3; +OE +NO3). The horizontal bars indicate mean percent survival for each treatment; circles mark the percent of surviving colonies for each tank (four colonies per species and tank, four tanks per treatment; points are jittered for clarity).</p

Effects of organic enrichment and nitrate on the fluorescent yields of heat-stressed and control <i>M. tuberculosa</i>.

<p>Time series of the fluorescence yields in <i>Montipora tuberculosa.</i> For details see the legend for <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0054399#pone-0054399-g002" target="_blank">Fig. 2</a>. In this species, heat stress (31.2°C) was applied between Days 10 and 59.</p

Effects of organic enrichment and nitrate on the fluorescent yields of heat-stressed and control <i>A. millepora</i>.

<p>Time series of the fluorescence yields in <i>Acropora millepora.</i> Two treatments (Controls and +OE +NO3) remained at ambient temperature (mean: 25°C) throughout the experimental period (a, b). Tanks in the other treatments were exposed to heat stress (31.2°C) between Days 10 and 33, followed by a recovery period at ambient temperature (c-f). The nutrient treatments applied to these tanks were (c) Controls, (d) +NO3, (e) +OE and (f) +OE +NO3. Points represent means across colonies for each tank; solid lines are estimated temporal trends and dashed lines are 95% confidence intervals.</p

Mean fluorescence yields in <i>Montipora tuberculosa</i> at the beginning of the experiment (Day 3), at the end of the heat stress (Day 59), and after recovery (Day 90<i>;</i>Fig. 3).

<p>Values are mean yields and SE across four tanks (four colonies per tank) for each of the four heat stressed treatments (31°C). The last three rows show the differences in mean fluorescence yields between days, with significant differences (>2 SE) marked in bold.</p

Relationship between nutrient availability and thermal tolerance in corals.

<p>The conceptual diagram illustrates the commonly non-linear and divergent relationships between thermal tolerance of heat-stressed coral species and the trophic status of their environment and/or food provision in experiments. See text for definitions and explanations.</p

Effects of temperature and organic enrichment on skeletal growth in <i>A. millepora</i> and <i>M. tuberculosa</i>.

<p>Change in weight (g) of surviving colonies over 67 days for (a) <i>Acropora millepora</i> and (b) <i>Montipora tuberculosa</i>. Fitted grey lines show the relationship between initial weight and weight gain. In <i>A. millepora,</i> weight gains were 45% reduced in colonies exposed to 31.2°C (crosses) than those exposed to 25°C (circles), and not related to initial weight. In <i>M. tuberculosa,</i> weight gains were 24% reduced in colonies exposed to +OE (crosses) than those not exposed to OE (circles), and declined with initial size for small colony fragments. The other factors under consideration did not significantly affect weight gains in the two species.</p