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Oxythermal window drastically constraints the survival and development of European sturgeon early life phases

  • Multi-Stressors in Freshwater and Transitional Environments: from Legacy Pollutants to Emerging Ones
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Abstract

European sturgeon Acipenser sturio is an anadromous fish species being classified “critically endangered” with only one remaining population in the Gironde-Garonne-Dordogne basin (France). In the global warming context, this paper aims to determine the sensitivity of A. sturio early life phases to temperature and oxygen saturation. Embryos were experimentally exposed to a combination of temperature (12 to 30 °C) and oxygen (30 to 90% O2 saturation) conditions. Lethal and sublethal effects were evaluated using embryonic mortality, hatching success, malformation rate, yolk sac resorption, tissue development and swimming speed. Embryonic survival peaked at 20 °C and no survival was recorded at 30 °C regardless of the associated oxygen saturation. No hatching occurred at 50% O2 sat or below regardless of temperature. Malformation frequency appeared to be minimum at 20 °C and 90% O2 sat. Swimming speed peaked at 16 °C. The temperature optimum of early life phases of A. sturio was determined to be close to 20 °C. Its upper tolerance limit is between 26 and 30 °C and its lower tolerance limit is below 12 °C. Oxygen depletion induces sublethal effects at 70% O2 sat and lethal effects at 50% O2 sat. Within the spawning period in the Gironde-Garonne-Dordogne basin, we identified yearly favourable oxythermal windows. Consequences of climate change would depend of the phenological adaptation of the species for its spawning period.

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Notes

  1. R Development Core Team (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL: http://www.R-project.org.

References

  • Abe T, Sakamoto T (2011) Embryonic development and larval behavior of the kissing loach (Parabotia curta): adaptations to an ephemeral, hypoxic environment. Ichthyol Res 58:238–244

    Article  Google Scholar 

  • Acolas ML, Castelnaud G, Lepage M, Rochard E (2011) Chapter 10 biological cycle and migrations. In: Williot P, Rochard E, Desse-Berset N, Kirschbaum F, Gessner J (eds) Biology and conservation of the Atlantic European sturgeon Acipenser sturio L., 1758. Springer, Berlin Heidelberg, pp 147-152

  • Burggren WW, Pinder AW (1991) Ontogeny of cardiovascular and respiratory physiology in lower vertebrates. Annu Rev Physiol 53:107–135

    Article  CAS  Google Scholar 

  • Caballero Y, Voirin-Morel S, Habets F, Noilhan J, LeMoigne P, Lehenaff A, Boone A (2007) Hydrological sensitivity of the Adour-Garonne river basin to climate change. Water Resour Res 43:19

    Google Scholar 

  • Claireaux G, Lefrançois C (2007) Linking environmental variability and fish performance: integration through the concept of scope for activity. Philos Trans R Soc Lond B Biol Sci 362:2031–2041

    Article  Google Scholar 

  • Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exp Biol 216:2771–2782

    Article  Google Scholar 

  • Dalla Via J, Van Den Thillart G, Cattani O, Cortesi P (1998) Behavioural responses and biochemical correlates in Solea solea to gradual hypoxic exposure. Can J Zool 76:2108–2113

    Article  Google Scholar 

  • Darias MJ, Lan Chow Wing O, Cahu C, Zambonino-Infante JL, Mazurais D (2010) Double staining protocol for developing European sea bass (Dicentrarchus labrax) larvae. J Appl Ichthyol 26:280–285

    Article  Google Scholar 

  • Delage N, Cachot J, Fraty R, Jatteau P (2014) Hypoxia tolerance of European sturgeon (Acipenser sturio L., 1758) young stages at two temperatures. J Appl Ichthyol 30:1195–1202

    Article  CAS  Google Scholar 

  • Detlaf TA, Ginzburg TA, Shmal’gauzen OI (1981) Development of sturgeon: egg maturation, fertilization, embryonic and prelarval development. Nauka Publishers, Moscow

    Google Scholar 

  • Detlaf TA, Ginzburg AS, Shmal'gauzen OI (1993) Sturgeon fishes: developmental biology and aquaculture. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Domenici P, Lefrançois C, Shingles A (2007) Hypoxia and the antipredator behaviours of fishes. Philos Trans R Soc Lond B Biol Sci 362:2105–2121

    Article  CAS  Google Scholar 

  • Elliott JM, Elliott JA (2010) Temperature requirements of Atlantic salmon Salmo salar, brown trout Salmo trutta and Arctic charr Salvelinus alpinus: predicting the effects of climate change. J Fish Biol 77:1793–1817

    Article  CAS  Google Scholar 

  • Elshout PMF, Dionisio Pires LM, Leuven RSEW, Wendelaar Bonga SE, Hendricks AJ (2013) Low oxygen tolerance of different life stages of temperate freshwater fish species. J Fish Biol 83:190–206

    Article  CAS  Google Scholar 

  • Fry FEJ (1971) Fish physiology. Academic press, New York

    Google Scholar 

  • Gisbert E, Cech JJ Jr, Doroshov SI (2002) Routine metabolism of larval green sturgeon (Acipenser medirostris Ayres). Fish Physiol Biochem 25:195–200

    Article  Google Scholar 

  • Hassell KL, Coutin PC, Nugegoda D (2008a) Hypoxia impairs embryo development and survival in black bream (Acanthopagrus butcheri). Mar Pollut Bull 57:302–306

    Article  CAS  Google Scholar 

  • Hassell KL, Coutin PC, Nugegoda D (2008b) Hypoxia, low salinity and lowered temperature reduce embryo survival and hatch rates in black bream Acanthopagrus butcheri (Munro, 1949). J Fish Biol 72:1623–1636

    Article  Google Scholar 

  • IPCC (2013) Summary for policymakers. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Doschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds). Cambridge University Press, pp. 3–29. https://doi.org/10.1017/CBO9781107415324.004

  • Jego S, Gazeau C, Jatteau P, Elie P, Rochard E (2002) Les frayères potentielles de l'esturgeon européen Acipenser sturio L. 1758 dans le bassin Garonne-Dordogne. Méthodes d'investigation, état actuel et perspectives. Bull Fr Peche Piscic 365-366:487–505

    Article  Google Scholar 

  • Johnston IA, Lee HT, Macqueen DJ, Paranthaman K, Kawashima C, Anwar A, Kinghorn JR, Dalmay T (2009) Embryonic temperature affects muscle fibre recruitment in adult zebrafish: genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes. J Exp Biol 212:1781–1793

    Article  CAS  Google Scholar 

  • Kappenman KM, Webb MAH, Greenwood M (2013) The effect of temperature on embryo survival and development in pallid sturgeon Scaphirhynchus albus (Forbes & Richardson 1905) and shovelnose sturgeon S. platorynchus (Rafinesque, 1820). J Appl Ichthyol 29:1193–1203

    Article  Google Scholar 

  • Kieffer JD, Baker DW, Wood AM, Papadopoulos CN (2011) The effects of temperature on the physiological response to low oxygen in Atlantic sturgeon. Fish Physiol Biochem 37:809–819

    Article  CAS  Google Scholar 

  • Killen SS, Marras S, Metcalfe NB, McKenzie DJ, Domenici P (2013) Environmental stressors alter relationships between physiology and behaviour. Trends Ecol Evol 28:651–658

    Article  Google Scholar 

  • Killen SS, Reid D, Marras S, Domenici P (2015) The interplay between aerobic metabolism and antipredator performance: vigilance is related to recovery rate after exercise. Front Physiol 6:111

    Article  Google Scholar 

  • Kovacs TG, Martel PH, Voss RH (2002) Assessing the biological status of fish in a river receiving pulp and paper mill effluents. Environ Pollut 118:123–140

    Article  CAS  Google Scholar 

  • Lanoux A, Etcheber H, Schmidt S, Sottolichio A, Chabaud G, Richard M, Abril G (2013) Factors contributing to hypoxia in a highly turbid, macrotidal estuary (the Gironde, France). Environ Sci Processes Impacts 15:585–595

    Article  CAS  Google Scholar 

  • Larnier K, Roux H, Dartus D, Croze O (2010) Water temperature modeling in the Garonne River (France). Knowl Manag Aquat Ecosyst 398:20

    Google Scholar 

  • Lassalle G, Crouzet P, Gessner J, Rochard E (2010) Global warming impacts and conservation responses for the critically endangered European Atlantic sturgeon. Biol Conserv 143:2441–2452

    Article  Google Scholar 

  • Lefrançois C, Domenici P (2006) Locomotor kinematics and behaviour in the escape response of European sea bass, Dicentrarchus labrax L., exposed to hypoxia. Mar Biol 149:969–977

    Article  Google Scholar 

  • Lepage, M. & Rochard, E. (2011). Chapter 22 fishery by-catch of European sturgeon in the Bay of Biscay. In: Williot P, Rochard E, Desse-Berset N, Kirschbaum F, Gessner J (eds) Biology and conservation of the Atlantic European sturgeon Acipenser sturio L., 1758. Springer, Berlin Heidelberg, pp 335-342

  • Lo KH, Hui MNY, Yu RMK, Wu RSS, Cheng SH (2011) Hypoxia impairs primordial germ cell migration in zebrafish (Danio rerio) embryos. PLoS One 6:e24540

    Article  CAS  Google Scholar 

  • MAGEST (2011) http://www.magest.u-bordeaux1.fr

  • Magnin E (1962) Recherches sur la systématique et la biologie des Acipenséridés. Annales de la Station Centrale d'Hydrobiologie Appliquée 9:7–242

    Google Scholar 

  • Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-KÜBler K, Bissolli P, BraslavskÁ OG, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl Å, Defila C, Donnelly A, Filella Y, Jatczak K, Måge F, Mestre A, Nordli Ø, Peñuelas J, Pirinen P, RemiŠOvÁ V, Scheifinger H, Striz M, Susnik A, Van Vliet AJH, Wielgolaski F-E, Zach S, Zust ANA (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–1976

    Article  Google Scholar 

  • Mueller CA, Joss JMP, Seymour RS (2011) The energy cost of embryonic development in fishes and amphibians, with emphasis on new data from the Australian lungfish, Neoceratodus forsteri. J Comp Physiol B 181:43–52

    Article  Google Scholar 

  • Mustafa SA, Al-Subiai SN, Davies SJ, Jha AN (2011) Hypoxia-induced oxidative DNA damage links with higher level biological effects including specific growth rate in common carp, Cyprinus carpio L. Ecotoxicology 20:1455–1466

    Article  CAS  Google Scholar 

  • Nicholson G, Jenkins GP, Sherwood J, Longmore A (2008) Physical environmental conditions, spawning and early-life stages of an estuarine fish: climate change implications for recruitment in intermittently open estuaries. Mar Freshw Res 59:735–749

    Article  CAS  Google Scholar 

  • Pörtner H (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146

    Article  Google Scholar 

  • Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692

    Article  Google Scholar 

  • Rabalais NN, Díaz RJ, Levin LA, Turner RE, Gilbert D, Zhang J (2010) Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences 7:585–619

    Article  CAS  Google Scholar 

  • Rochard E (2011) Chapter 18 present legal status of the European sturgeon Acipenser sturio. In: Williot P, Rochard E, Desse-Berset N, Kirschbaum F, Gessner J (eds) Biology and conservation of the Atlantic European sturgeon Acipenser sturio L., 1758. Springer, Berlin Heidelberg, pp 251-256

  • Rochard E, Castelnaud G, Lepage M (1990) Sturgeons (Pisces: Acipenseridae); threats and prospects. J Fish Biol 37:123–132

    Article  Google Scholar 

  • Rochard E, Lepage M, Meauze L (1997) Identification et caractérisation de l'aire de répartition marine de l’esturgeon européen Acipenser sturio à partir de déclarations de captures. Aquat Living Resour 10:101–109

    Article  Google Scholar 

  • Rochard E, Lepage M, Dumont P, Tremblay S, Gazeau C (2001) Downstream migration of juvenile European sturgeon Acipenser sturio L. in the Gironde estuary. Estuaries 24:108–115

    Article  Google Scholar 

  • Rombough PJ (1988) 2 Respiratory gas exchange, aerobic metabolism, and effects of hypoxia during early life. Fish Physiol 11:59–161

    Article  Google Scholar 

  • Rosenthal H, Bronzi P, Gessner J, Moreau D, Rochard E, Lasen C (2007) Draft action plan for the conservation and restoration of the European sturgeon (Acipenser sturio). Council of Europe, Convention on the conservation of European wildlife and natural habitats, Strasbourg, p 47

    Google Scholar 

  • Shang EHH, Wu RSS (2004) Aquatic hypoxia is a teratogen and affects fish embryonic development. Environ Sci Technol 38:4763–4767

    Article  CAS  Google Scholar 

  • Shields RJ, Brown NP, Bromage NR (1997) Blastomere morphology as a predictive measure of fish egg viability. Aquaculture 155:1–12

    Article  Google Scholar 

  • Spitsbergen JM, Tsai HW, Reddy A, Miller T, Arbogast D, Hendricks JD, Bailey GS (2000) Neoplasia in zebrafish (Danio rerio) treated with 7,12-dimethylbenz[a]anthracene by two exposure routes at different developmental stages. Toxicol Pathol 28:705–715

    Article  CAS  Google Scholar 

  • Wang YL, Binkowski FP, Doroshov SI (1985) Effect of temperature on early development of white and lake sturgeon, Acipenser transmontanus and A. fulvescens. Environmental Biology of Fishes 14:43–50

    Article  Google Scholar 

  • Williot P, Castelnaud G (2011) Chapter 20 historic overview of the European sturgeon Acipenser sturio in France: surveys, regulations, reasons for the decline, conservation, and analysis. In: Williot P, Rochard E, Desse-Berset N, Kirschbaum F, Gessner J (eds) Biology and conservation of the Atlantic European sturgeon Acipenser sturio L., 1758. Springer, Berlin Heidelberg, pp. 285-308

  • Williot P, Rochard E, Desse-Berset N, Gessner J, Kirschbaum F (2011) Chapter 1 brief introduction to sturgeon with a special focus on the European sturgeon, Acipenser sturio L. 1758. In: Williot P, Rochard E, Desse-Berset N, Kirschbaum F, Gessner J (eds) Biology and conservation of the Atlantic European sturgeon Acipenser sturio L., 1758. Springer, Berlin Heidelberg, pp 3-12

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Acknowledgements

This study was carried out as part of the Cluster of Excellence COTE. Temperature and Oxygen data from the field were provided by the NGO Migrateurs Garonne Dordogne (MIGADO) (http://www.migado.fr/) and the consortium MAGEST. The English has been revised by James Emery. Thanks to David Mc Kenzie and Patrick Kestemont for reviewing a previous version of this text in the PhD manuscript of Nicolas Delage and two anonymous reviewers.

Funding

This study was funded by the Région Aquitaine, IRSTEA and the French National Research Agency (SturTOP research project No. ANR-13-CESA-0018-01).

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Correspondence to Eric Rochard.

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Delage, N., Couturier, B., Jatteau, P. et al. Oxythermal window drastically constraints the survival and development of European sturgeon early life phases. Environ Sci Pollut Res 27, 3651–3660 (2020). https://doi.org/10.1007/s11356-018-4021-8

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