Skip to main content

Advertisement

Log in

Investigations of temperature and pH variations on metal trophic transfer in turbot (Scophthalmus maximus)

  • Aquatic organisms and biological responses to assess water contamination and ecotoxicity
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Studying dietary metal transfer kinetics is essential to gain a better understanding in global metal accumulation rates and its impacts in marine fish. While there exists a solid understanding on the influence of various biotic factors on this transfer, metal assimilation in fish might be also affected by abiotic factors, as has been observed in marine invertebrates. The present study therefore aims to understand the potential effects of two climate-related master variables, temperature and pH, on the assimilation efficiency (AE) of essential (Co and Zn) and non-essential (Ag) metals in the turbot Scophthalmus maximus using radiotracer tools. Juvenile turbots were acclimated for 8 weeks at two temperatures (17 and 20 °C) and pH (7.5 and 8.0) regimes, under controlled laboratory conditions, and then fed with radiolabelled shrimp (57Co, 65Zn and 110mAg). Assimilation efficiencies of Co and Ag in juvenile turbot, determined after a 21-day depuration period, were not affected by pre-exposition to the different environmental conditions. In contrast, temperature did significantly influence Zn AE (p < 0.05), while pH variations did not affect the assimilation of any of the metals studied. In fact, temperature is known to affect gut physiology, specifically the membrane properties of anterior intestine cells where Zn is adsorbed and assimilated from the ingested food. These results are relevant to accurately assess the influence of abiotic factors in AEs of metals in fish as they are highly element-dependent and also modulated by metabolic processes.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Beitinger TL, Fitzpatrick LC (1979) Physiological and ecological correlates of preferred temperature in fish. Am Zool 19:319–329

    Article  Google Scholar 

  • Belivermiş M, Warnau M, Metian M, et al (2015) Limited effects of increased CO2 and temperature on metal and radionuclide bioaccumulation in a sessile invertebrate, the oyster Crassostrea gigas. ICES J Mar Sci J Cons fsv236

  • Boyd PW, Hutchins DA (2012) Introduction: understanding the responses of ocean biota to a complex matrix of cumulative anthropogenic change. Mar Ecol Prog Ser 470:125–135

    Article  Google Scholar 

  • Brett JR, Higgs DA (1970) Effect of temperature on the rate of gastric digestion in finger ling sockeye salmon, Oncorhynchus nerka. J Fish Res Board Can 27:1767–1779

    Article  Google Scholar 

  • Bury NR, Walker PA, Glover CN (2003) Nutritive metal uptake in teleost fish. J Exp Biol 206:11–23

    Article  CAS  Google Scholar 

  • Dickson AG (2016) Information on batches of CO2 in seawater reference material. http://cdiac.ornl.gov/oceans/Dickson_CRM/batches.html. Accessed 17 October 2016

  • Dickson AG, Sabine CL, Christian JR (eds) (2007) Guide to best practices for ocean CO2 measurements. PICES special publication 3. North Pacific marine science organization Sidney, British Columbia

  • Edwards DJ (1971) Effect of temperature on rate of passage of food through the alimentary canal of the plaice Pleuronectes platessa L. J Fish Biol 3:433–439

    Article  Google Scholar 

  • Florin A-B, Lavados G (2010) Feeding habits of juvenile flatfish in relation to habitat characteristics in the Baltic Sea. Estuar Coast Shelf Sci 86:607–612

    Article  Google Scholar 

  • Flynn EE, Bjelde BE, Miller NA, Todgham AE (2015) Ocean acidification exerts negative effects during warming conditions in a developing Antarctic fish. Conserv Physiol 3:cov033

    Article  Google Scholar 

  • Frommel AY, Maneja R, Lowe D, Pascoe CK, Geffen AJ, Folkvord A, Piatkowski U, Clemmesen C (2014) Organ damage in Atlantic herring larvae as a result of ocean acidification. Ecol Appl 24:1131–1143

    Article  Google Scholar 

  • Götze S, Matoo OB, Beniash E, Saborowski R, Sokolova IM (2014) Interactive effects of CO2 and trace metals on the proteasome activity and cellular stress response of marine bivalves Crassostrea virginica and Mercenaria mercenaria. Aquat Toxicol Amst Neth 149:65–82

    Article  Google Scholar 

  • Gunderson AR, Armstrong EJ, Stillman JH (2016) Multiple stressors in a changing world: the need for an improved perspective on physiological responses to the dynamic marine environment. Annu Rev Mar Sci 8:357–378

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Imsland AK, Foss A, Gunnarsson S et al (2001) The interaction of temperature and salinity on growth and food conversion in juvenile turbot (Scophthalmus maximus). Aquaculture 198:353–367

    Article  Google Scholar 

  • IPCC (2013) Climate Change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change, Cambridge University Press. Intergovernmental Panel on Climate Change (IPCC), Cambridge, United Kingdom and New York, NY, USA

  • Ivanina AV, Hawkins C, Beniash E, Sokolova IM (2015) Effects of environmental hypercapnia and metal (Cd and Cu) exposure on acid-base and metal homeostasis of marine bivalves. Comp Biochem Physiol Toxicol Pharmacol CBP 174-175:1–12

    Article  CAS  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434

    Article  Google Scholar 

  • Lacoue-Labarthe T, Martin S, Oberhänsli F, Teyssié J-L, Markich S, Jeffree R, Bustamante P (2009) Effects of increased pCO2 and temperature on trace element (Ag, Cd and Zn) bioaccumulation in the eggs of the common cuttlefish, Sepia officinalis. Biogeosciences 6:2561–2573

    Article  CAS  Google Scholar 

  • Lacoue-Labarthe T, Réveillac E, Oberhänsli F, Teyssié J-L Jeffree R, Gattuso J-P (2011) Effects of ocean acidification on trace element accumulation in the early-life stages of squid Loligo vulgaris. Aquat Toxicol 105:166–176

    Article  CAS  Google Scholar 

  • Lacoue-Labarthe T, Martin S, Oberhänsli F, Teyssié J-L, Jeffree R, Gattuso J-P, Bustamante P (2012) Temperature and pCO2 effect on the bioaccumulation of radionuclides and trace elements in the eggs of the common cuttlefish, Sepia officinalis. J Exp Mar Biol Ecol 413:45–49

    Article  CAS  Google Scholar 

  • Lanceleur L, Schäfer J, Chiffoleau J-F et al (2011) Long-term records of cadmium and silver contamination in sediments and oysters from the Gironde fluvial–estuarine continuum: evidence of changing silver sources. Chemosphere 85:1299–1305

    Article  CAS  Google Scholar 

  • Lavigne H, Epitalon J-M, Gattuso J-P (2011) Seacarb: seawater carbonate chemistry with R. R package version 3.0

  • Lee J-S, Lee B-G (2005) Effects of salinity, temperature and food type on the uptake and elimination rates of cd, Cr, and Zn in the asiatic clam Corbicula fluminea. Ocean Sci J 40:79–89

    Article  CAS  Google Scholar 

  • Mathews T, Fisher NS (2009) Dominance of dietary intake of metals in marine elasmobranch and teleost fish. Sci Total Environ 407:5156–5161

    Article  CAS  Google Scholar 

  • Mathews T, Fisher NS, Jeffree RA, Teyssié J-L (2008) Assimilation and retention of metals in teleost and elasmobranch fishes following dietary exposure. Mar Ecol Prog Ser 360:1–12

    Article  CAS  Google Scholar 

  • Miegel RP, Pain SJ, van Wettere WHEJ, Howarth GS, Stone DAJ (2010) Effect of water temperature on gut transit time, digestive enzyme activity and nutrient digestibility in yellowtail kingfish (Seriola lalandi). Aquaculture 308:145–151

    Article  CAS  Google Scholar 

  • Orr JC, Fabry VJ, Aumont O et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686

    Article  CAS  Google Scholar 

  • Parker LM, Ross PM, O’Connor WA (2011) Populations of the Sydney rock oyster, Saccostrea glomerata, vary in response to ocean acidification. Mar Biol 158:689–697

    Article  Google Scholar 

  • Pentreath RJ (1976) Some further studies on the accumulation and retention of 65Zn and 54Mn by the plaice, Pleuronectes platessa L. J Exp Mar Biol Ecol 21:179–189

    Article  CAS  Google Scholar 

  • Pimentel MS, Faleiro F, Diniz M, Machado J, Pousão-Ferreira P, Peck MA, Pörtner HO, Rosa R (2015) Oxidative stress and digestive enzyme activity of flatfish larvae in a changing ocean. PLoS One 10:e0134082

    Article  Google Scholar 

  • Pouil S, Warnau M, Oberhänsli F, Teyssié J-L, Metian M (2015) Trophic transfer of 110mAg in the turbot Scophthalmus maximus through natural prey and compounded feed. J Environ Radioact 150:189–194

    Article  CAS  Google Scholar 

  • Pouil S, Warnau M, Oberhänsli F, Teyssié J-L, Bustamante P, Metian M (2016) Influence of food on the assimilation of essential elements (Co, Mn, and Zn) by turbot Scophthalmus maximus. Mar Ecol Prog Ser 550:207–218

    Article  CAS  Google Scholar 

  • Pouil S, Teyssié J-L, Rouleau C, Fowler SW, Metian M, Bustamante P, Warnau M (2017) Comparative study of trophic transfer of the essential metals Co and Zn in two tropical fish: a radiotracer approach. J Exp Mar Biol Ecol 486:42–51

    Article  CAS  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (2010) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourg

    Google Scholar 

  • Rodriguez y Baena AM, Miquel JC, Masqué P, Povinec PP, La Rosa J (2006) A single vs. double spike approach to improve the accuracy of 234Th measurements in small-volume seawater samples. Mar Chem 100:269–281

    Article  CAS  Google Scholar 

  • Rosa R, Pimentel M, Galan JG, Baptista M, Lopes VM, Couto A, Guerreiro M, Sampaio E, Castro J, Santos C, Calado R, Repolho T (2016) Deficit in digestive capabilities of bamboo shark early stages under climate change. Mar Biol 163:60

    Article  Google Scholar 

  • Rouleau C, Gobeil C, Tjälve H (2000) Accumulation of silver from the diet in two marine benthic predators: the snow crab (Chionoecetes opilio) and American plaice (Hippoglossoides platessoides). Environ Toxicol Chem 19:631–637

    Article  CAS  Google Scholar 

  • Shears MA, Fletcher GL (1983) Regulation of Zn2+ uptake from the gastrointestinal tract of a marine teleost, the winter flounder (Pseudopleuronectes americanus). Can J Fish Aquat Sci 40:s197–s205

    Article  Google Scholar 

  • Smit H (1967) Influence of temperature on the rate of gastric juice sectretion in the brown bullhead, Ictalurus nebolosus. Comp Biochem Physiol 21:125–132

    Article  Google Scholar 

  • Sparrevohn CR, Støttrup J (2008) Diet, abundance and distribution as indices of turbot (Psetta maxima L.) release habitat suitability. Rev Fish Sci 16:338–347

    Article  Google Scholar 

  • Van Campenhout K, Bervoets L, Blust R (2007) Assimilation efficiencies of Cd and Zn in the common carp (Cyprinus carpio): effects of metal concentration, temperature and prey type. Environ Pollut 145:905–914

    Article  CAS  Google Scholar 

  • Wang W-X, Fisher NS (1999) Assimilation efficiencies of chemical contaminants in aquatic invertebrates: a synthesis. Environ Toxicol Chem 18:2034–2045

    Article  CAS  Google Scholar 

  • Wang W-X, Wong RS (2003) Bioaccumulation kinetics and exposure pathways of inorganic mercury and methylmercury in a marine fish, the sweetlips Plectorhinchus gibbosus. Mar Ecol Prog Ser 261:257–268

    Article  CAS  Google Scholar 

  • Wang W-X, Onsanit S, Dang F (2012) Dietary bioavailability of cadmium, inorganic mercury, and zinc to a marine fish: effects of food composition and type. Aquaculture 356–357:98–104

    Article  Google Scholar 

  • Warnau M, Bustamante P (2007) Radiotracer techniques: a unique tool in marine ecotoxicological studies. Environ Bioindic 2:217–218

    Article  Google Scholar 

  • Warnau M, Teyssié J-L, Fowler SW (1996) Biokinetics of selected heavy metals and radionuclides in the common Mediterranean echinoid Paracentrotus lividus: sea water and food exposures. Mar Ecol Prog Ser 141:83–94

    Article  CAS  Google Scholar 

  • Wernberg T, Smale D, Thomsen M (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob Change Biol 18:1491–1498

    Article  Google Scholar 

  • Xu Y, Wang W-X (2002) Exposure and potential food chain transfer factor of Cd, Se and Zn in marine fish Lutjanus argentimaculatus. Mar Ecol Prog Ser 238:173–186

    Article  CAS  Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice-Hall, Upper Saddle River

    Google Scholar 

  • Zehmer JK, Hazel JR (2005) Thermally induced changes in lipid composition of raft and non-raft regions of hepatocyte plasma membranes of rainbow trout. J Exp Biol 208:4283–4290

    Article  Google Scholar 

  • Zhang L, Wang W-X (2005) Effects of Zn pre-exposure on Cd and Zn bioaccumulation and metallothionein levels in two species of marine fish. Aquat Toxicol 73:353–369

    Article  CAS  Google Scholar 

  • Zhang L, Wang W-X (2007) Size-dependence of the potential for metal biomagnification in early life stages of marine fish. Environ Toxicol Chem 26:787–794

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to P. Swarzenski for his constructive comments on this work and H. Jacob for his help with alkalinity measurements. The IAEA is grateful for the support provided to its Environment Laboratories by the Government of the Principality of Monaco.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paco Bustamante.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pouil, S., Oberhänsli, F., Bustamante, P. et al. Investigations of temperature and pH variations on metal trophic transfer in turbot (Scophthalmus maximus). Environ Sci Pollut Res 25, 11219–11225 (2018). https://doi.org/10.1007/s11356-017-8691-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-8691-4

Keywords

Navigation