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Research Article
Breaking free from thermodynamic constraints: thermal acclimation and metabolic compensation in a freshwater zooplankton species
B. L. Coggins, C. E. Anderson, R. Hasan, A. C. Pearson, M. N. Ekwudo, J. R. Bidwell, L. Y. Yampolsky
Journal of Experimental Biology 2021 224: jeb237727 doi: 10.1242/jeb.237727 Published 19 February 2021
B. L. Coggins
1Department of Biological Sciences, East Tennessee State University, Johnson City, TN 37691, USA
2Department of Biological Sciences, University of Notre Dame, Galvin Life Science Center, Notre Dame, IN 46556, USA
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C. E. Anderson
1Department of Biological Sciences, East Tennessee State University, Johnson City, TN 37691, USA
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R. Hasan
1Department of Biological Sciences, East Tennessee State University, Johnson City, TN 37691, USA
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A. C. Pearson
1Department of Biological Sciences, East Tennessee State University, Johnson City, TN 37691, USA
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M. N. Ekwudo
1Department of Biological Sciences, East Tennessee State University, Johnson City, TN 37691, USA
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J. R. Bidwell
1Department of Biological Sciences, East Tennessee State University, Johnson City, TN 37691, USA
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L. Y. Yampolsky
1Department of Biological Sciences, East Tennessee State University, Johnson City, TN 37691, USA
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  • ORCID record for L. Y. Yampolsky
  • For correspondence: yampolsk@etsu.edu
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ABSTRACT

Respiration rates of ectothermic organisms are affected by environmental temperatures, and sustainable metabolism at high temperatures sometimes limits heat tolerance. Organisms are hypothesized to exhibit acclimatory metabolic compensation effects, decelerating their metabolic processes below Arrhenius expectations based on temperature alone. We tested the hypothesis that either heritable or plastic heat tolerance differences can be explained by metabolic compensation in the eurythermal freshwater zooplankton crustacean Daphnia magna. We measured respiration rates in a ramp-up experiment over a range of assay temperatures (5–37°C) in eight genotypes of D. magna representing a range of previously reported acute heat tolerances and, at a narrower range of temperatures (10–35°C), in D. magna with different acclimation history (either 10 or 25°C). We discovered no difference in temperature-specific respiration rates between heat-tolerant and heat-sensitive genotypes. In contrast, we observed acclimation-specific compensatory differences in respiration rates at both extremes of the temperature range studied. Notably, there was a deceleration of oxygen consumption at higher temperature in 25°C-acclimated D. magna relative to their 10°C-acclimated counterparts, observed in active animals, a pattern corroborated by similar changes in filtering rate and, partly, by changes in mitochondrial membrane potential. A recovery experiment indicated that the reduction of respiration was not caused by irreversible damage during exposure to a sublethal temperature. Response time necessary to acquire the respiratory adjustment to high temperature was lower than for low temperature, indicating that metabolic compensation at lower temperatures requires slower, possibly structural changes.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: B.L.C., J.R.B., L.Y.Y.; Methodology: J.R.B., L.Y.Y.; Validation: R.H., L.Y.Y.; Formal analysis: B.L.C., L.Y.Y.; Investigation: B.L.C., C.E.A., A.C.P., R.H., M.N.E., L.Y.Y.; Resources: J.R.B.; Data curation: B.L.C., C.E.A., L.Y.Y.; Writing - original draft: L.Y.Y.; Writing - review & editing: B.L.C., C.E.A., A.C.P., L.Y.Y.; Visualization: C.E.A., L.Y.Y.; Supervision: J.R.B., L.Y.Y.; Project administration: J.R.B., L.Y.Y.

  • Funding

    This research has been funded by East Tennessee State University Small RDC and Student-Faculty Collaborative grants to L.Y.Y.

  • Data availability

    Measurements of respiration rates and mitochondrial potential are available from the Dryad Digital Repository (Yampolsky et al., 2020): https://doi.org/10.5061/dryad.c2fqz616k

  • Supplementary information

    Supplementary information available online at https://jeb.biologists.org/lookup/doi/10.1242/jeb.237727.supplemental

  • Received September 14, 2020.
  • Accepted December 9, 2020.
  • © 2021. Published by The Company of Biologists Ltd
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Keywords

  • Acclimation
  • Daphnia
  • Plasticity
  • Respiration
  • Temperature

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Research Article
Breaking free from thermodynamic constraints: thermal acclimation and metabolic compensation in a freshwater zooplankton species
B. L. Coggins, C. E. Anderson, R. Hasan, A. C. Pearson, M. N. Ekwudo, J. R. Bidwell, L. Y. Yampolsky
Journal of Experimental Biology 2021 224: jeb237727 doi: 10.1242/jeb.237727 Published 19 February 2021
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Research Article
Breaking free from thermodynamic constraints: thermal acclimation and metabolic compensation in a freshwater zooplankton species
B. L. Coggins, C. E. Anderson, R. Hasan, A. C. Pearson, M. N. Ekwudo, J. R. Bidwell, L. Y. Yampolsky
Journal of Experimental Biology 2021 224: jeb237727 doi: 10.1242/jeb.237727 Published 19 February 2021

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