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Pre-exposure to a variable temperature treatment improves the response of Acropora cervicornis to acute thermal stress

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Abstract

Given that global warming is the greatest threat to coral reefs, coral restoration projects have expanded worldwide with the goal of replenishing habitats whose reef-building corals succumbed to various stressors. In many cases, however, these efforts will be futile if outplanted corals are unable to withstand warmer oceans and an increased frequency of extreme temperature events. Stress-hardening is one approach proposed to increase the thermal tolerance of coral genotypes currently grown for restoration. Previous studies have shown that corals from environments with natural temperature variability experience less bleaching when exposed to thermal stress, though it remains unclear if this localized acclimatization or adaptation to variable temperatures can be operationalized for enhancing restoration efforts. To evaluate this approach, fragments from six source colonies of nursery-raised Caribbean staghorn coral (Acropora cervicornis) were treated with a variable temperature regime (oscillating twice per day from 28 to 31 °C) or static temperatures (28 °C) in the laboratory for 89 d. Following this, fragments were subjected to a heat-stress assay (32 °C) for 2 weeks. Corals treated with variable temperatures manifested signs of severe thermal stress later than static temperature laboratory controls as well as untreated field controls collected from the nursery. Furthermore, there was a stark contrast in the physiological response to heat stress, whereby the laboratory and field control groups had a significantly higher incidence of rapid tissue sloughing and necrosis, while the variable temperature-treated corals succumbed to bleaching more gradually. Overall, our data show that pre-acclimation to a variable temperature regime improves acroporid thermotolerance. As corals continue to be outplanted back onto Florida’s changing reef scape, understanding the molecular mechanisms underlying this enhanced thermal tolerance and its endurance in situ will be critical for future research and restoration applications.

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Acknowledgements

We would like to thank L. Chomiak, L. Shea, L. Dutra, C. Aguilar, J. Morris, J. Unsworth, N. Soderberg, R. van Hooidonk, B. Young, M. D’Alessandro, C. Dennison, and A. Palacio for their contributions to this project and manuscript. This project was funded by NOAA’s Coral Reef Conservation Program. Corals were collected under Florida’s Fish and Wildlife Commission Permit SAL-19-1794-SCRP issued to Diego Lirman. We would like to thank the reviewers and the editor of Coral Reefs for their constructive feedback.

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Authors and Affiliations

  1. Atlantic Oceanographic and Meteorological Laboratory, Ocean Chemistry and Ecosystems Division, U.S. National Oceanic and Atmospheric Administration, 4301 Rickenbacker Cswy, Miami, FL, 33149, USA

    Allyson DeMerlis, Anderson B. Mayfield, Nathan Formel, Graham Kolodziej & Ian C. Enochs

  2. Rosenstiel School for Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Cswy, Miami, FL, 33149, USA

    Allyson DeMerlis, Madeline L. Kaufman, Diego Lirman & Nikki Traylor-Knowles

  3. Department of Biological Sciences, The University of New Orleans, 2000 Lakeshore Dr, New Orleans, LA, 70148, USA

    Amanda Kirkland

  4. Cooperative Institute for Marine and Atmospheric Studies, University of Miami, 4600 Rickenbacker Cswy, Miami, FL, 33149, USA

    Anderson B. Mayfield, Nathan Formel & Graham Kolodziej

  5. Coral Reef Watch, Center for Satellite Applications and Research, Satellite Oceanography and Climatology Division, U.S. National Oceanic and Atmospheric Administration, 5830 University Research Ct, College Park, MD, 20740, USA

    Derek P. Manzello

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  1. Allyson DeMerlis
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338_2022_2232_MOESM1_ESM.eps

(a) Image of setup with Coral Color Reference Card (Siebeck et al. 2006) and Kodak Gray Scale bar used for initial color score categorization (D1–D6) and white balance standardization in ImageJ, respectively. This image was taken prior to the start of the 8 d temperature increase to 32 ºC for the heat-stress assay. (b) Observed signs of paling (first and third fragments) and rapid tissue loss (the central fragment) during the heat-stress assay. (EPS 88084 kb)

338_2022_2232_MOESM2_ESM.eps

Mean number of days until coral fragments demonstrated tissue sloughing (dark shading) or bleached to a color score of D1 (light shading) for each genotype during the heat-stress assay after being subjected to one of two treatments (laboratory control or variable) or directly after removal from the field (field control). Error bars are standard deviation. (EPS 1102 kb)

338_2022_2232_MOESM3_ESM.xlsx

Supplementary file3: Supplemental Table 1: Recorded temperatures during both the temperature treatment and heat-stress assays, as well as their respective calculated means and standard deviations. (XLSX 4574 kb)

338_2022_2232_MOESM4_ESM.xlsx

Supplementary file4: Supplemental Table 2: Metadata for each individual coral fragment during both the temperature treatment and heat-stress assays. Color scores (D1-D6), R-intensities, maximum dark-adapted yield of photosystem II (Fv/Fm), and number of days in heat-stress assay before either reaching a color score of D1 (fully bleached) or exhibiting signs of rapid tissue loss. (XLSX 208 kb)

338_2022_2232_MOESM5_ESM.xlsx

Supplementary file5: Supplemental Table 3: Results of post hoc Tukey's HSD test of multiple comparison of means for 2 analyses of variances: 1) the effect of genotype and treatment on the number of days corals persisted in the heat-stress assay, and 2) the effect of original reef site and treatment on the number of days corals persisted in the heat-stress assay, both with a 95% family-wise confidence interval. (XLSX 23 kb)

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DeMerlis, A., Kirkland, A., Kaufman, M.L. et al. Pre-exposure to a variable temperature treatment improves the response of Acropora cervicornis to acute thermal stress. Coral Reefs 41, 435–445 (2022). https://doi.org/10.1007/s00338-022-02232-z

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