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Positive interactions between corals and damselfish increase coral resistance to temperature stress

Citation

Shantz, Andrew et al. (2022), Positive interactions between corals and damselfish increase coral resistance to temperature stress, Dryad, Dataset, https://doi.org/10.5061/dryad.zpc866t9t

Abstract

By the century’s end, many tropical seas will reach temperatures exceeding most coral species’ thermal tolerance on an annual basis. The persistence of corals in these regions will therefore depend on their abilities to tolerate recurrent thermal stress. Although ecologists have long recognized that positive interspecific interactions can ameliorate environmental stress to expand the realized niche of plants and animals, coral bleaching studies have largely overlooked how interactions with community members outside of the coral holobiont shape the bleaching response. Here, we subjected a common coral, Pocillopora grandis, to 10 days of thermal stress in aquaria with- and without the damselfish Dascyllus flavicaudus (yellowtail dascyllus), which commonly shelter within these corals, to examine how interactions with damselfish impacted coral thermal tolerance. Corals often benefit from nutrients excreted by animals they interact with and prior to thermal stress, corals grown with damselfish showed improved photophysiology (Fv/Fm) and developed larger endosymbiont populations. When exposed to thermal stress, corals with fish performed as well as corals maintained at ambient temperatures without fish. In contrast, corals exposed to thermal stress without fish experienced photophysiological impairment, a more than 50% decline in endosymbiont density, and a 36% decrease in tissue protein content. By the end of the experiment, thermal stress caused average calcification rates to decrease by over 80% when damselfish were absent but increase nearly 25% when damselfish were present. Our study indicates that damselfish-derived nutrients can increase coral thermal tolerance and are consistent with the Stress Gradient Hypothesis, which predicts that positive interactions become increasingly important for structuring communities as environmental stress increases. Because warming of just a few degrees can exceed corals’ temperature tolerance to trigger bleaching and mortality, positive interactions could play a critical role maintaining some coral species in warming regions until climate change is aggressively addressed.

Methods

To assess how fishes influenced coral physiology and thermal tolerance, we measured the dark-adapted quantum yield, symbiont density, and tissue protein content of coral fragments throughout a thermal stress experiment. Measurements were taken on Day 1 when the corals were brought to shore, prior to acclimation with damselfish, and on Day 14 after two weeks of acclimation with or without damselfish present. Temperatures were then increased in half of the tanks over 24 hours to 30.5°C, and subsequent measurements made on Days 17, 20, and 24, corresponding to 3, 6, and 10 days of temperature stress, respectively. After completing our measurements on Day 24, we lowered the temperatures in the heated aquaria back to 27.5°C over 24 hours and collected final measurements on Day 34, after 10 days of recovery.

At each sampling time point we haphazardly selected one fragment from each tank for sampling. We used PAM fluorometry to measure the maximum dark-adapted quantum yield of PSII (FV/FM) after 30 minutes of dark acclimation. After taking fluorescence measurements, we removed the tissue from each fragment with a waterpik and centrifuged the resulting tissue slurry at 5,000xG for 5 minutes to separate the coral tissue and Symbiodineaceae. Symbiont pellets were resuspended in 1 ml filtered seawater while the coral tissue was rapidly frozen by submersing the sample tubes in -80°C acetone for 5 minutes, followed by storage at -80°C for protein analysis. Symbiont density of each fragment was calculated from eight replicate counts on a Neubauer hemocytometer and normalized to the fragments skeletal surface area, as determined by wax dipping (Stimson and Kinzie, 1991). To determine protein content of coral tissue, we lyophilized the frozen coral tissue at -80°C to a constant weight. Next, the freeze-dried tissue was homogenized and diluted in 0.5 ml of PBS buffer, vortexed for 20 min, and immersed in a sonicating water bath for an additional 20 min. The solution was then filtered through a 0.2 μm filter and the resulting supernatant analyzed on a Millipore Direct Detect infrared spectrometer against a bovine serum albumin standard (EMD Millipore, Billerica MA, USA). Finally, we measured differences in coral calcification rates, as determined by changes in buoyant weight (Davies 1989), for the fragments collected on the final day of thermal stress and after the 10 day recovery period.

To determine how the yellowtail dascyllus impacted nutrient levels we measured ammonium (NH4+), nitrate (NO3-), and soluble reactive phosphorus (SRP) in every aquarium approximately weekly throughout the experiment.

Funding

National Science Foundation, Award: OCE-1547952

National Science Foundation, Award: OCE-1637396