Skip to main content
Log in

The reef building coral Stylophora pistillata uses stored carbohydrates to maintain ATP levels under thermal stress

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Coral reefs are on the brink of collapse from global warming and associated coral bleaching. Coral bleaching is the loss of algal symbionts from the coral tissue. The reduction in photosynthates produced by the symbionts makes the survival of the coral dependent on heterotrophy and stored resources, which are catabolized into available energy, i.e., Adenosine Triphosphate (ATP). The present study examined how an increase in water temperature affects energetic reserves and available ATP in the Red Sea coral Stylophora pistillata. Following a 9-d hold at 1, 3, 5 °C above ambient summer temperature (~ 26 °C), ATP levels in the coral tissue remained constant. Similarly, no significant differences in the stored energy (proteins, carbohydrates, and lipids) of the holobiont were measured. However, half of the coral nubbins in the + 7 °C treatment experienced tissue dissociation, while the remaining nubbins bleached with a 34% decline in stored energy and a decline in respiration and photosynthesis rates by 69 and 72%, respectively. The + 7 °C treated coral nubbins had 75% lower carbohydrates compared to nubbins at ambient conditions and the lowest carbohydrates to lipid and protein ratio. This study demonstrates that exceeding the high bleaching threshold of S. pistillata in the Gulf of Aqaba is associated with a catabolic response to maintain ATP levels and highlights the energetic cost of thermal stress. Understanding anabolic and catabolic processes in corals under environmental stress is key to understanding their capacity to survive future thermal stress scenarios.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Al-Horani FA, Al-Moghrabi SM, De Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426

    Article  CAS  Google Scholar 

  • Am S, Gassman NJ (1990) The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217–224

    Article  Google Scholar 

  • Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Bio Ecol 252:221–253

    Article  CAS  Google Scholar 

  • Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23:539–550

    Article  Google Scholar 

  • Baumann J, Grottoli AG, Hughes AD, Matsui Y (2014) Photoautotrophic and heterotrophic carbon in bleached and non-bleached coral lipid acquisition and storage. J Exp Mar Bio Ecol 461:469–478

    Article  CAS  Google Scholar 

  • Bellworthy J, Fine M (2017) Beyond peak summer temperatures, branching corals in the Gulf of Aqaba are resilient to thermal stress but sensitive to high light. Coral Reefs 36:1071–1082

    Article  Google Scholar 

  • Bellworthy J, Spangenberg JE, Fine M (2019) Feeding increases the number of offspring but decreases parental investment of Red Sea coral Stylophora pistillata. Ecol Evol 9:12245–12258

  • Bellworthy J, Fine M (2018) The Red Sea Simulator: A high-precision climate change mesocosm with automated monitoring for the long-term study of coral reef organisms. Limnol Oceanogr Methods 16:367–375

  • Berg JM, Tymoczko JL, Stryer L (2002) The regulation of cellular respiration is governed primarily by the need for ATP. Biochem 5th edn; WH Freedman, New York, NY, USA

  • Cheng YS, Zheng Y, VanderGheynst JS (2011) Rapid quantitative analysis of lipids using a colorimetric method in a microplate format. Lipids 46:95–103

    Article  CAS  PubMed  Google Scholar 

  • Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol 43:209–216

    Article  CAS  Google Scholar 

  • Crossland CJ (1987) In situ release of mucus and DOC-lipid from the corals Acropora variabilis and Stylophora pistillata in different light regimes. Coral Reefs 6:35–42

    Article  CAS  Google Scholar 

  • Davies PS (1991) Effect of daylight variations on the energy budgets of shallow-water corals. Mar Biol 108:137–144

    Article  Google Scholar 

  • Dunn SR, Pernice M, Green K, Hoegh-Guldberg O, Dove SG (2012) Thermal stress promotes host mitochondrial degradation in symbiotic cnidarians: Are the batteries of the reef going to run out? PLoS One 7:e39024

  • Edmunds PJ, Davies PS (1986) An energy budget for Porites porites (Scleractinia). Mar Biol Int J Life Ocean Coast Waters 92:339–347

    Google Scholar 

  • Edmunds PJ, Davies PS (1989) An energy budget for Porites porites (Scleractinia), growing in a stressed environment. Coral Reefs 8:37–43

    Article  Google Scholar 

  • Evensen NR, Fine M, Perna G, Voolstra CR, Barshis DJ (2021) Remarkably high and consistent tolerance of a Red Sea coral to acute and chronic thermal stress exposures. Limnol Oceanogr,66:1718–1729

  • Fang L-S, Chen Y-WJ, Soong K-Y (1987) Methodology and measurement of ATP in coral. Bull Mar Sci 41:605–610

    Google Scholar 

  • Fang L-S, Chen Y-WJ, Chen C-S (1989) Why does the white tip of stony coral grow so fast without zooxanthellae? Mar Biol 103:359–363

    Article  Google Scholar 

  • Fang L-S, Chen Y-W, Chen C-S (1991) Feasibility of using ATP as an index for environmental stress on hermatypic coral. Mar Ecol Prog Ser 70:257–262

    Article  CAS  Google Scholar 

  • Ferrier-Pagès C, Gattuso JP, Cauwet G, Jaubert J, Allemand D (1998) Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis. Mar Ecol Prog Ser 172:265–274

    Article  Google Scholar 

  • Ferrier-Pagès C, Rottier C, Beraud E, Levy O (2010) Experimental assessment of the feeding effort of three scleractinian coral species during a thermal stress: Effect on the rates of photosynthesis. J Exp Mar Bio Ecol 390:118–124

    Article  Google Scholar 

  • Fine M, Oren U, Loya Y (2002) Bleaching effect on regeneration and resource translocation in the coral Oculina. Mar Ecol-Prog Ser 234:119–125

    Article  Google Scholar 

  • Fine M, Gildor H, Genin A (2013) A coral reef refuge in the Red Sea. Glob Chang Biol 19:3640–3647

    Article  PubMed  Google Scholar 

  • Fitt WK, Spero HJ, Halas J, White MW, Porter JW (1993) Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean “bleaching event.” Coral Reefs 12:57–64

    Article  Google Scholar 

  • Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685

    Article  CAS  Google Scholar 

  • Frederich M, O’Rourke MR, Furey NB, Jost JA (2009) AMP-activated protein kinase (AMPK) in the rock crab, Cancer irroratus: An early indicator of temperature stress. J Exp Biol 212:722–730

    Article  CAS  PubMed  Google Scholar 

  • Freeman BA, Crapo JD (1982) Biology of disease: free radicals and tissue injury. Lab Invest 47:412

    CAS  PubMed  Google Scholar 

  • Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17

    Article  Google Scholar 

  • Gnaiger E, Bitterlich G (1984) Proximate biochemical composition and caloric content calculated from elemental CHN analysis: a stoichiometric concept. Oecologia 62:289–298

    Article  CAS  PubMed  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol 145:621–631

    Article  CAS  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189

    Article  CAS  PubMed  Google Scholar 

  • Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, Mcginley M, Baumann J, Matsui Y (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Chang Biol 20:3823–3833

    Article  PubMed  Google Scholar 

  • Grottoli AG, Tchernov D, Winters G (2017) Physiological and biogeochemical responses of super-corals to thermal stress from the northern gulf of Aqaba, Red Sea. Front Mar Sci 4:1–12

    Article  Google Scholar 

  • Hardie DG, Scott JW, Pan DA, Hudson ER (2003) Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett 546:113–120

    Article  CAS  PubMed  Google Scholar 

  • Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42

    Article  CAS  PubMed  Google Scholar 

  • Hinkle PC, Kumar MA, Resetar A, Harris DL (1991) Mechanistic stoichiometry of mitochondrial oxidative phosphorylation. Biochemistry 30:3576–3582

    Article  CAS  PubMed  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Holcomb M, Tambutté E, Allemand D, Tambutté S (2014) Light enhanced calcification in Stylophora pistillata: Effects of glucose, glycerol and oxygen. PeerJ 2014:1–18

    Google Scholar 

  • Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17

    Article  PubMed  Google Scholar 

  • Hughes AD, Grottoli AG (2013) Heterotrophic compensation: a possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress? PLoS ONE 8:1–10

    Article  Google Scholar 

  • Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377

    Article  CAS  PubMed  Google Scholar 

  • Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83

  • Imbs AB, Yakovleva IM (2012) Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress: an experimental approach. Coral Reefs 31:41–53

    Article  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Und Physiol Der Pflanz 167:191–194

    Article  CAS  Google Scholar 

  • Jitrapakdee S, Wallace JC (1999) Structure, function and regulation of pyruvate carboxylase. Biochem J 340:1–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155–162

    Article  Google Scholar 

  • Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230

    Article  CAS  Google Scholar 

  • Kenkel CD, Meyer E, Matz MV (2013) Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments. Mol Ecol 22:4322–4334

    Article  CAS  PubMed  Google Scholar 

  • Krueger T, Horwitz N, Bodin J, Giovani ME, Escrig S, Meibom A, Fine M (2017) Common reef-building coral in the northern red sea resistant to elevated temperature and acidification. R Soc Open Sci 4 (5):170038

  • LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580

    Article  CAS  PubMed  Google Scholar 

  • Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41:271–283

    Article  CAS  Google Scholar 

  • Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192

    Article  Google Scholar 

  • Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Bio Ecol 300:217–252

    Article  Google Scholar 

  • Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278

    Article  CAS  PubMed  Google Scholar 

  • Lesser MP (2013) Using energetic budgets to assess the effects of environmental stress on corals: Are we measuring the right things? Coral Reefs 32:25–33

    Article  Google Scholar 

  • Leuzinger S, Anthony KRN, Willis BL (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136:524–531

    Article  PubMed  Google Scholar 

  • Levas S, Grottoli AG, Warner ME, Cai WJ, Bauer J, Schoepf V, Baumann JH, Matsui Y, Gearing C, Melman TF, Hoadley KD, Pettay DT, Hu X, Li Q, Xu H, Wang Y (2015) Organic carbon fluxes mediated by corals at elevated pCO2 and temperature. Mar Ecol Prog Ser 519:153–164

    Article  CAS  Google Scholar 

  • Levas S, Grottoli AG, Schoepf V, Aschaffenburg M, Baumann J, Bauer JE, Warner ME (2016) Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals? Coral Reefs 35:495–506

    Article  Google Scholar 

  • Liu G, Strong AE, Skirving W, Arzayus LF (2006) Overview of NOAA coral reef watch Program’s near-real time satellite global Coral Bleaching Monitoring Activities. Proceedings of 10th International Coral Reef Symposium, Okinawa, Japan. 1793:1783–1793

  • Maor-Landaw K, Karako-Lampert S, Ben-Asher HW, Goffredo S, Falini G, Dubinsky Z, Levy O (2014) Gene expression profiles during short-term heat stress in the red sea coral Stylophora pistillata. Glob Chang Biol 20:3026–3035

    Article  PubMed  Google Scholar 

  • Masuko T, Minami A, Iwasaki N, Majima T, Nishimura SI, Lee YC (2005) Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Anal Biochem 339:69–72

    Article  CAS  PubMed  Google Scholar 

  • Nii CM, Muscatine L (1997) Oxidative stress in the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943): contribution of the animal to superoxide ion production at elevated temperature. Biol Bull 192:444–456

    Article  CAS  PubMed  Google Scholar 

  • NOAA (2020) NOAA coral reef watch homepage and near-real-time products portal. https://coralreefwatch.noaa.gov/satellite/index.php

  • Oakley CA, Davy SK (2018) Cell biology of coral bleaching. Coral bleaching 189–211

  • Ohad I (1994) Light-induced degradation of the photosystem II reaction centre D1 protein in vivo: an integrative approach. Photoinhibition Photosynth from Mol Mech to Field 161–178

  • Omori M, Fukami H, Kobinata H, Hatta M (2001) Significant drop of fertilization of Acropora corals in 1999: An after-effect of heavy coral bleaching? Limnol Oceanogr 46:704–706

    Article  Google Scholar 

  • Osman EO, Smith DJ, Ziegler M, Kürten B, Conrad C, El-Haddad KM, Voolstra CR, Suggett DJ (2018) Thermal refugia against coral bleaching throughout the northern Red Sea. Glob Chang Biol 24:e474–e484

    Article  PubMed  Google Scholar 

  • Patton JS, Burris JE (1983) Lipid synthesis and extrusion by freshly isolated zooxanthellae (symbiotic algae). Mar Biol 75:131–136

    Article  CAS  Google Scholar 

  • Porter JW, Fitt WK, Spero HJ, Rogers CS, White MW (1989) Bleaching in reef corals: physiological and stable isotopic responses. Proc Natl Acad Sci U S A 86:9342–9346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pörtner H-O (2010) Oxygen-and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213:881–893

    Article  PubMed  Google Scholar 

  • Pörtner HO (2012) Integrating climate-related stressor effects on marine organisms: Unifying principles linking molecule to ecosystem-level changes. Mar Ecol Prog Ser 470:273–290

    Article  CAS  Google Scholar 

  • Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882

    Article  Google Scholar 

  • Savary R, Barshis DJ, Voolstra CR, Cárdenas A, Evensen NR, Banc-Prandi G, Fine M, Meibom A (2021) Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea. Proc Natl Acad Sci U S A 118:19

  • Sokolova IM (2013) Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr Comp Biol 53:597–608

    Article  PubMed  Google Scholar 

  • Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15

    Article  CAS  PubMed  Google Scholar 

  • Somero GN (2012) The physiology of global change: Linking patterns to mechanisms. Ann Rev Mar Sci 4:39–61

    Article  PubMed  Google Scholar 

  • Stambler N, Dubinsky Z (2004) Stress effects on metabolism and photosynthesis of hermatypic corals. Coral Health and disease 195–215

  • Tagliafico A, Rudd D, Rangel MS, Kelaher BP, Christidis L, Cowden K, Scheffers SR, Benkendorff K (2017) Lipid-enriched diets reduce the impacts of thermal stress in corals. Mar Ecol Prog Ser 573:129–141

    Article  CAS  Google Scholar 

  • Tchernov D, Gorbunov MY, De Vargas C, Yadav SN, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci 101:13531–13535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tilghman SM, Hanson RW, Reshef L, Hopgood MF, Ballard FJ (1974) Rapid loss of translatable messenger RNA of phosphoenolpyruvate carboxykinase during glucose repression in liver. Proc Natl Acad Sci 71:1304–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiwari BS, Belenghi B, Levine A (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol 128:1271–1281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tremblay P, Naumann MS, Sikorski S, Grover R, Ferrier-Pagès C (2012) Experimental assessment of organic carbon fluxes in the scleractinian coral Stylophora pistillata during a thermal and photo stress event. Mar Ecol Prog Ser 453:63–77

    Article  CAS  Google Scholar 

  • Tremblay P, Gori A, Maguer JF, Hoogenboom M, Ferrier-Pagès C (2016) Heterotrophy promotes the re-establishment of photosynthate translocation in a symbiotic coral after heat stress. Sci Rep 6:1–14

    Article  CAS  Google Scholar 

  • Veal CJ, Carmi M, Fine M, Hoegh-Guldberg O (2010) Increasing the accuracy of surface area estimation using single wax dipping of coral fragments. Coral Reefs 29:893–897

    Article  Google Scholar 

  • Voolstra CR, Buitrago-López C, Perna G, Cárdenas A, Hume BCC, Rädecker N, Barshis DJ (2020) Standardized short-term acute heat stress assays resolve historical differences in coral thermotolerance across microhabitat reef sites. Glob Chang Biol 26:4328–4343

    Article  PubMed  Google Scholar 

  • Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: Stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066

    Article  CAS  PubMed  Google Scholar 

  • Wild C, Niggl W, Naumann MS, Haas AF (2010) Organic matter release by Red Sea coral reef organisms-Potential effects on microbial activity and in situ O2 availability. Mar Ecol Prog Ser 411:61–71

    Article  CAS  Google Scholar 

  • Yahel R, Yahel G, Genin A (2005) Near- bottom depletion of zooplankton over coral reefs: I: Diurnal dynamics and size distribution. Coral Reefs 24:75–85

    Article  Google Scholar 

  • Zamaraeva MV, Sabirov RZ, Maeno E, Ando-Akatsuka Y, Bessonova SV, Okada Y (2005) Cells die with increased cytosolic ATP during apoptosis: A bioluminescence study with intracellular luciferase. Cell Death Differ 12:1390–1397

    Article  CAS  PubMed  Google Scholar 

  • Zor T, Selinger Z (1996) Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. Anal Biochem 236:302–308

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported in part by an Israel Science Foundation (ISF) grant (1794/16 and 1746/11) to MF. The authors thank Dror Komet for his valuable technical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Na’ama-Rose Kochman.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Simon Davy

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 575 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kochman, NR., Grover, R., Rottier, C. et al. The reef building coral Stylophora pistillata uses stored carbohydrates to maintain ATP levels under thermal stress. Coral Reefs 40, 1473–1485 (2021). https://doi.org/10.1007/s00338-021-02174-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-021-02174-y

Keywords

Navigation