What's the cost of high heat tolerance in corals?

Here, we report substantial variability of heat tolerance in a single coral population, despite colonies hosting the same microalgal symbionts. We find no trade-off between heat tolerance and either colony growth or fecundity. Against expectations, heat tolerance was positively correlated to growth.
Published in Ecology & Evolution
What's the cost of high heat tolerance in corals?

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The future of coral reef ecosystems is a growing concern in the face of climate change. Coral bleaching events have led to mass coral mortality because of marine heatwaves, which are projected to become more intense and more frequent in the future. The capacity for corals to adapt will in part determine whether coral populations persist or are lost. Therefore, natural selection for high coral heat tolerance will continue to play an important role for coral populations.

But does heat tolerance come at a cost to corals?

Following a recent paper in Communications Biology, here are some of my informal musings on this topic. But first, I have to say a huge thanks to the co-authors of this study from across the globe for sharing their knowledge, resources, and enthusiasm.

Corals have a symbiotic relationship with microalgae which are located within the coral host cells. These algae provide the coral with food and energy through photosynthesis, allowing individual corals to grow and build up new skeleton, while the coral provides the algae a safe environment in which to live. However, the Achilles' heel of this relationship is that it can become compromised under temperature stress. When the symbiosis breaks down the algae is expelled from the coral and the white skeleton underneath the coral tissue becomes clearly visible, a process known as coral bleaching.

We know that some groups of symbiotic microalgae help corals cope with hot temperatures better than others, thus making the coral more heat tolerant (e.g., Durusdinium spp. rather than Cladocopium spp.). Yet, this can come at a cost to calcification, with more heat tolerant colonies being slower to build new skeleton. However, in some populations almost all coral colonies host the same type of symbiotic microalgae (e.g., all have Cladocopium spp.) yet still show remarkable variation in heat tolerance. Do we still see trade-offs with heat tolerance in these populations?

Our study explores this idea for an Indo-Pacific coral population (Fig. 1), whose colonies ubiquitously host Cladocopium spp. symbionts. Spoiler alert – we didn’t find any evidence for trade-offs when considering growth and reproduction traits. If anything, we find some signs of co-benefits among these different traits. Here is a quick run-down of what we measured.

Figure 1. Study species and population. The shallow-water reef-building coral Acropora digitifera is common on the outer reefs of Palau, Micronesia.

Heat tolerance. Marine heatwaves that cause mass coral bleaching and mortality events are usually linked with high temperatures that last for several weeks or even months. Ultimately, after a mass bleaching event, the most important thing is ‘who survived and who didn’t’. To determine individual coral heat tolerance, we tagged over 70 colonies in a single population and reef. We then sampled six fragments from each colony and exposed them to a simulated marine heatwave in aquaria at the Palau International Coral Reef Center. In the absence of heat stress, we wanted our corals to be happy in the aquaria tanks, and to achieve this we took our do-it-yourself skills to the next level: building tanks; setting up lights; labelling each fragment with a unique ID. We then exposed the fragments to a long 5-week heat stress which caused a range of bleaching and mortality responses. Based on the health status decline of replicate fragments we were able to determine the individual heat tolerance of each coral colony (Fig. 2).

Figure 2. Coral heat tolerance was highly variable within a single population. Here we show the progression of bleaching responses of four coral fragments during a long-term 5-week marine heatwave experiment. The lower fragments bleached earlier than the upper fragments. This exposure also led to mortality for many coral fragments (not shown).

Reproduction. For organisms across the tree of life, having kids is a high energy pursuit. For some mammals it is well known that when life is tough (e.g., during drought years), mothers will put less investment into their offspring. Perhaps they have a smaller litter, or smaller babies at birth. For corals, eggs are rich in fats and require energy investment to be produced. Perhaps reproductive investment could be a potential trade-off with coral heat tolerance. We measured fecundity-related traits for each colony by decalcifying and dissecting colony fragments sampled prior to spawning (when corals release their eggs into the water column in a synchronous event, Fig. 3). Fecundity variables included the number of eggs per polyp and per colony, egg size, and total egg volume per colony. However, we found no relationship between these traits and heat tolerance.

Figure 3. Coral reproduction. As a proxy of reproductive effort, we estimated a variety of fecundity-related traits. See the mollusc and crab feasting frenzy at the beginning of this video!

Growth. In order to measure coral colony growth on the reef, we teamed up with underwater 3D photogrammetry specialists from the Australian Institute of Marine Science and the University of Sydney. Following the same tagged coral colonies over a period of three years, we determined a variety of growth metrics including surface area growth and volumetric growth. However, again we detected no trade-offs between heat tolerance and any of these growth metrics across the population.

Figure 4. Coral colony growth. Colonies were tagged on the reef and monitored over the course of three years. See more interannual tansitions in this video, and explore a 3D model on sketchfab.

High performance across the board. In contrast to our expectations of a trade-off, we found evidence for the opposite – positive correlations between heat tolerance and colony growth. In short, the coral colonies growing fastest on the reef were the ones whose fragments performed best in our aquarium experiment, withstanding slightly higher levels of heat stress before the onset of bleaching and mortality. Various biological mechanisms could explain this unexpected finding, but here is one of the possibilities.

Intuitively, we expect to find trade-offs between energy intensive traits, like growth, stress tolerance, or reproduction. However, when looking at whole populations, it can be common to find positive associations where we expect negative ones. This can be explained by different total energy budgets among individuals. On a single reef, we could assume all coral colonies have the same amount of energy available to them. However, perhaps some individuals are more efficient at acquiring this energy from the environment (e.g., through photosynthesis or particulate feeding). Such individuals will end up with large overall energy budgets as a result, which can lead to high performance across multiple different traits. In comparison, the colonies with very low total energy budgets would likely perform poorly across the board. Thus, across the whole population we would see positive trait correlations. Energy allocation trade-offs between resource intensive traits must still be happening. However, the trade-off could be occurring at a finer scale, for instance, within individuals or at cellular levels. As such, the subtle energy allocation trade-off is masked at the scale of the whole population.

So what? The paradigm for corals is that heat tolerance must come at a cost to some other traits. This can have considerable implications for the broader ecosystem, as has been shown for the growth cost associated to certain more heat tolerant symbiont taxa. However, for a population that hosts the same symbiont taxa, our study found no apparent trade-offs between coral heat tolerance and either growth or fecundity. Ultimately, our work suggests that natural selection for coral host heat tolerance under climate change may not necessarily have negative implications for the persistence of coral populations (based on colony growth and fecundity). To secure a future for coral reefs, the major remaining challenge is reduction of carbon emissions to limit ocean warming and ecological impacts.

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