The predictability of fluctuating environments shapes the thermal tolerance of marine ectotherms and compensates narrow safety margins.
Biogeography
Circadian cycle
Climate sensitivity
Macro-physiology
Phenotypic plasticity
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
30 10 2024
30 10 2024
Historique:
received:
25
04
2024
accepted:
23
10
2024
medline:
31
10
2024
pubmed:
31
10
2024
entrez:
31
10
2024
Statut:
epublish
Résumé
Aquatic species living in productive coastal habitats with abundant primary producers have evolved in highly dynamic diel and seasonally fluctuating environments in terms of, for example, water temperature and dissolved oxygen. However, how environmental fluctuations shape the thermal tolerance of marine species is still poorly understood. Here we hypothesize that the degree of predictability of the diel environmental fluctuations in the coastal area can explain the thermal response of marine species. To test this hypothesis, we measured the thermal tolerance of 17 species of marine ectotherm from tropical, warm temperate and cold temperate latitudes under two levels of oxygen (around saturation and at supersaturation), and relate the results to their site-specific temperature and oxygen fluctuation and their environmental predictability. We demonstrate that oxygen and temperature fluctuations at tropical latitudes have a higher predictability than those at warm and cold temperate latitudes. Further, we show that marine species that are adapted to high predictability have the potential to tune their thermal performance when exposed to oxygen supersaturation, despite being constrained within a narrow safety margin. We advocate that the predictability of the environmental fluctuation needs to be considered when measuring and forecasting the response of marine animals to global warming.
Identifiants
pubmed: 39478107
doi: 10.1038/s41598-024-77621-1
pii: 10.1038/s41598-024-77621-1
doi:
Substances chimiques
Oxygen
S88TT14065
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
26174Informations de copyright
© 2024. The Author(s).
Références
Bernhardt, J. R., O’Connor, M. I., Sunday, J. M. & Gonzalez, A. Life in fluctuating environments. Philos. Trans. R. Soc. Lond. B Biol. Sci. 375, 20190454 (2020).
pubmed: 33131443
pmcid: 7662201
doi: 10.1098/rstb.2019.0454
Kroeker, K. J. et al. Ecological change in dynamic environments: Accounting for temporal environmental variability in studies of ocean change biology. Glob. Change Biol. 26, 54–67 (2020).
doi: 10.1111/gcb.14868
Helmuth, B. et al. Mosaic patterns of thermal stress in the rocky intertidal zone: Implications for climate change. Ecol. Monogr. 76, 461–479 (2006).
doi: 10.1890/0012-9615(2006)076[0461:MPOTSI]2.0.CO;2
Giomi, F. et al. Oxygen dynamics in marine productive ecosystems at ecologically relevant scales. Nat. Geosci. 16, 560–566 (2023).
doi: 10.1038/s41561-023-01217-z
Lima, F. P. & Wethey, D. S. Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nat. Commun. 3 (2012).
Giomi, F. et al. Oxygen supersaturation protects coastal marine fauna from ocean warming. Sci. Adv. 5, 1–8 (2019).
doi: 10.1126/sciadv.aax1814
Fusi, M., Daffonchio, D., Booth, J. & Giomi, F. Dissolved oxygen in heterogeneous environments dictates the metabolic rate and thermal sensitivity of a tropical aquatic crab. Front. Mar. Sci. 8, 1–9 (2021).
doi: 10.3389/fmars.2021.767471
Booth, J. et al. Diel oxygen fluctuation drives the thermal response and metabolic performance of coastal marine ectotherms. Proc. R. Soc. B Biol. Sci. 288, 20211141 (2021).
doi: 10.1098/rspb.2021.1141
Bitter, M. C. et al. Fluctuating selection and global change: A synthesis and review on disentangling the roles of climate amplitude, predictability and novelty. Proc. R. Soc. B Biol. Sci. 288 (2021).
Bitter, M. C. et al. The importance of incorporating natural thermal variation when evaluating physiological performance in wild species. J. Exp. Biol. 221 (2018).
Cabrerizo, M. J. & Marañón, E. Net effect of environmental fluctuations in multiple global-change drivers across the tree of life. Proc. Natl. Acad. Sci. USA 119, 1–8 (2022).
doi: 10.1073/pnas.2205495119
McArley, T. J., Morgenroth, D., Zena, L. A., Ekström, A. T. & Sandblom, E. Prevalence and mechanisms of environmental hyperoxia-induced thermal tolerance in fishes. Proc. R. Soc. B Biol. Sci. 289 (2022).
Harada, A. E. & Burton, R. S. Ecologically relevant temperature ramping rates enhance the protective heat shock response in an intertidal ectotherm. Physiol. Biochem. Zool. 92, 152–162 (2019).
pubmed: 30694107
doi: 10.1086/702339
Cleves, P. A. et al. Reduced thermal tolerance in a coral carrying CRISPR-induced mutations in the gene for a heat-shock transcription factor. Proc. Natl. Acad. Sci. USA 117, 28899–28905 (2020).
pubmed: 33168726
pmcid: 7682433
doi: 10.1073/pnas.1920779117
Vannini, M., Lori, E., Coffa, C. & Fratini, S. Cerithidea decollata: a snail that can foresee the future?. Anim. Behav. 76, 983–992 (2008).
doi: 10.1016/j.anbehav.2008.05.016
Bennett, J. M. et al. GlobTherm, a global database on thermal tolerances for aquatic and terrestrial organisms. Sci. Data 5, 1–7 (2018).
pubmed: 30482902
pmcid: 6300048
doi: 10.1038/sdata.2018.22
Pinsky, M. L., Eikeset, A. M., McCauley, D. J., Payne, J. L. & Sunday, J. M. Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature 569, 108–111 (2019).
pubmed: 31019302
doi: 10.1038/s41586-019-1132-4
Sunday, J. M. et al. Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc. Natl. Acad. Sci. USA 111, 5610–5615 (2014).
pubmed: 24616528
pmcid: 3992687
doi: 10.1073/pnas.1316145111
Blauw, A. N., Benincà, E., Laane, R. W. P. M., Greenwood, N. & Huisman, J. Predictability and environmental drivers of chlorophyll fluctuations vary across different time scales and regions of the North Sea. Prog. Oceanogr. 161, 1–18 (2018).
doi: 10.1016/j.pocean.2018.01.005
Guadayol, Ò., Silbiger, N. J., Donahue, M. J. & Thomas, F. I. M. Patterns in temporal variability of temperature, oxygen and pH along an environmental gradient in a coral reef. PLoS One 9 (2014).
Serrão, João Neiva, E. A. et al. Seaweed Phylogeography: Adaptation and Evolution of Seaweeds under Environmental Change. Seaweed Phylogeography. https://doi.org/10.1007/978-94-017-7534-2 (2016).
Jørgensen, S. & Bendoricchio, G. Fundamentals of Ecological Modelling (Elsevier, 2021).
Yamori, W., Noguchi, K., Hikosaka, K. & Terashima, I. Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant Physiol. 152, 388–399 (2010).
pubmed: 19880611
pmcid: 2799372
doi: 10.1104/pp.109.145862
Iñiguez, C., Galmés, J. & Gordillo, F. J. L. Rubisco carboxylation kinetics and inorganic carbon utilization in polar versus cold-temperate seaweeds. J. Exp. Bot. 70, 1283–1297 (2019).
pubmed: 30576461
doi: 10.1093/jxb/ery443
Davey, M. C. The effects of freezing and desiccation on photosynthesis and survival of terrestrial Antarctic algae and cyanobacteria. Polar Biol. 10, 29–36 (1989).
doi: 10.1007/BF00238287
Smith, C. M. & Berry, J. A. Oecologia to osmotic and temperature stresses: comparative studies of species with differing distributional limits. Response 6–12 (1986).
Vargas, C. A. et al. Upper environmental pCO2 drives sensitivity to ocean acidification in marine invertebrates. Nat. Clim. Change 12, 200–207 (2022).
doi: 10.1038/s41558-021-01269-2
Jiang, M., Felzer, B. S., Nielsen, U. N. & Medlyn, B. E. Biome-specific climatic space defined by temperature and precipitation predictability. Glob. Ecol. Biogeogr. 26, 1270–1282 (2017).
doi: 10.1111/geb.12635
Straus, D. M. & Paolino, D. Intermediate time error growth and predictability: Tropics versus mid-latitudes. Tellus Ser. A Dyn. Meteorol. Oceanogr. 61, 579–586 (2009).
doi: 10.1111/j.1600-0870.2009.00411.x
Judt, F. Atmospheric predictability of the tropics, middle latitudes, and polar regions explored through global storm-resolving simulations. J. Atmos. Sci. 77, 257–276 (2020).
doi: 10.1175/JAS-D-19-0116.1
McArley, T. J., Hickey, A. J. R. & Herbert, N. A. Hyperoxia increases maximum oxygen consumption and aerobic scope of intertidal fish facing acutely high temperatures. J. Exp. Biol. 221 (2018).
Krause-Jensen, D. et al. Long photoperiods sustain high pH in Arctic kelp forests. Sci. Adv. 2, e1501938 (2016).
pubmed: 27990490
pmcid: 5156516
doi: 10.1126/sciadv.1501938
Andersen, M. R., Kragh, T. & Sand-Jensen, K. Extreme diel dissolved oxygen and carbon cycles in shallow vegetated lakes. Proc. Biol. Sci. 284, 20171427 (2017).
pubmed: 28904141
pmcid: 5597838
Booth, J. M., Giomi, F., Daffonchio, D., Mcquaid, C. D. & Fusi, M. Disturbance of primary producer communities disrupts the thermal limits of the associated aquatic fauna. Sci. Total Environ. 872, 162135 (2023).
pubmed: 36775146
doi: 10.1016/j.scitotenv.2023.162135
Bitter, M. C., Kapsenberg, L., Silliman, K., Gattuso, J. P. & Pfister, C. A. Magnitude and predictability of pH fluctuations shape plastic responses to ocean acidification. Am. Nat. 197, 486–501 (2021).
pubmed: 33755541
doi: 10.1086/712930
Botero, C. A., Weissing, F. J., Wright, J. & Rubenstein, D. R. Evolutionary tipping points in the capacity to adapt to environmental change. Proc. Natl. Acad. Sci. USA 112, 184–189 (2015).
pubmed: 25422451
doi: 10.1073/pnas.1408589111
Bonamour, S., Chevin, L. M., Charmantier, A. & Teplitsky, C. Phenotypic plasticity in response to climate change: The importance of cue variation. Philos. Trans. R. Soc. B Biol. Sci. 374 (2019).
McArley, T. J., Morgenroth, D., Zena, L. A., Ekström, A. T. & Sandblom, E. Experimental hyperoxia (O2 supersaturation) reveals a gill diffusion limitation of maximum aerobic performance in fish. Biol. Lett. 18, 20220401 (2022).
pubmed: 36321431
pmcid: 9627442
doi: 10.1098/rsbl.2022.0401
Verberk, W. C. E. P. et al. Can respiratory physiology predict thermal niches? Ann. N. Y. Acad. Sci. 1–16. https://doi.org/10.1111/nyas.12876 (2015).
Fusi, M. et al. Thermal specialization across large geographical scales predicts the resilience of mangrove crab populations to global warming. Oikos 124, 784–795 (2015).
doi: 10.1111/oik.01757
Huey, R. B. & Kingsolver, J. G. Climate warming, resource availability, and the metabolic meltdown of ectotherms. Am. Nat. 194, E140–E150 (2019).
pubmed: 31738103
doi: 10.1086/705679
Reusch, T. B. H. Climate change in the oceans: Evolutionary versus phenotypically plastic responses of marine animals and plants. Evol. Appl. 7, 104–122 (2014).
pubmed: 24454551
doi: 10.1111/eva.12109
Broitman, B. R., Aguilera, M. A., Lagos, N. A. & Lardies, M. A. Phenotypic plasticity at the edge: Contrasting population-level responses at the overlap of the leading and rear edges of the geographical distribution of two Scurria limpets. J. Biogeogr. 45, 2314–2325 (2018).
doi: 10.1111/jbi.13406
Bujan, J., Roeder, K. A., Yanoviak, S. P. & Kaspari, M. Seasonal plasticity of thermal tolerance in ants. Ecology 101, 1–6 (2020).
doi: 10.1002/ecy.3051
Sokolova, I. M., Frederich, M., Bagwe, R., Lannig, G. & Sukhotin, A. A. Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar. Environ. Res. 79, 1–15 (2012).
pubmed: 22622075
doi: 10.1016/j.marenvres.2012.04.003
Angilletta, M. J. Jr. & Angilletta, M. J. Thermal Adaptation: A Theoretical and Empirical Synthesis (Oxford University Press, 2009).
doi: 10.1093/acprof:oso/9780198570875.001.1
Angilletta, M. J., Cooper, B. S., Schuler, M. S. & Boyles, J. G. The evolution of thermal physiology in endotherms. J. Therm. Biol. 2, 249–268 (2002).
doi: 10.1016/S0306-4565(01)00094-8
Angilletta, M. J., Niewiarowski, P. H. & Navas, C. A. The evolution of thermal physiology in ectotherms. J. Therm. Biol. 27, 249–268 (2002).
doi: 10.1016/S0306-4565(01)00094-8
Morawska, L. P., Hernandez-Valdes, J. A. & Kuipers, O. P. Diversity of bet-hedging strategies in microbial communities—Recent cases and insights. WIREs Mech. Dis. 14, 1–15 (2022).
Shumway, R. H. & Stoffer, D. S. Time Series: A Data Analysis Approach Using R. (Chapman and Hall/CRC, 2019). https://doi.org/10.1201/9780429273285
Giomi, F. et al. The importance of thermal history: Costs and benefits of heat exposure in a tropical, rocky shore oyster. J. Exp. Biol. 219, 686–694 (2016).
pubmed: 26747904
Grinsted, A., Moore, J. C. & Jevrejeva, S. Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Process Geophys. 11, 515–533 (2004).
doi: 10.5194/npg-11-561-2004
Moore, D. F. Applied Survival Analysis Using R (Springer International Publishing, Cham, 2016). https://doi.org/10.1007/978-3-319-31245-3
Knezevic, S. Z., Streibig, J. C. & Ritz, C. Utilizing R software package for dose-response studies: the concept and data analysis. Weed Technol. 21, 840–848 (2007).
doi: 10.1614/WT-06-161.1
Rosseel, Y. lavaan: An R package for structural equation modeling. J. Stat. Softw. 48 (2012).