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.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
Metals are typically found in the marine environment at low concentrations. Some metals are metabolically required at the correct amount for organisms, such as Co and Zn (i.e. essential metals), and others can be toxic even at very low concentrations, such as Ag (i.e. non-essential metals). Anthropogenic activities tend to increase metal concentrations in coastal environments, which can cause detrimental effects to the organisms living in these areas. This is particularly problematic due to the emergence of new emission sources, especially for Ag, including cloud seeding nanoparticles or electronic component manufacturing (Lanceleur et al. 2011). Fish are exposed to these metals from both the dissolved and the particulate phases (Warnau and Bustamante 2007). Since food has been recognized as a pathway of major importance for metal intake in fish (Xu and Wang 2002; Mathews and Fisher 2009), investigating the factors influencing the trophic transfer of metals in fish is of paramount importance.
A key parameter for understanding metal trophic transfer in fish is the assimilation efficiency (AE; Wang and Fisher 1999). Numerous studies have focused on the determination of factors that influence metal AE in several aquatic species, including fish (e.g. Xu and Wang 2002; Zhang and Wang 2005; Pouil et al. 2016). For example, the importance of the composition and nature of the food source, both qualitatively and quantitatively, on metal AE has been determined in different species of marine fish (e.g. Wang and Wong 2003; Wang et al. 2012; Pouil et al. 2016). Similarly, the influence of the physiological state and life stage of the organism on metal AE has also been studied in several fish species (e.g. Zhang and Wang 2005; Zhang and Wang 2007; Pouil et al. 2017). These different studies have shown that biological, physiological and ecological factors can importantly influence AE of trace metals. Nevertheless, the trophic transfer of metals can also be impacted by environmental variables (abiotic factors) as it has been shown in marine invertebrates (Lee and Lee 2005) or in freshwater fish (Van Campenhout et al. 2007). Surprisingly, such an influence is poorly documented in the literature on marine fish.
Temperature and pH are two key environmental variables influencing marine fish physiology. For example, temperature, one of the main abiotic drivers of fish physiology (Beitinger and Fitzpatrick 1979), was shown to affect gut transit time or the activity of the enzymes involved in the digestion process when fish are chronically exposed to temperatures away from their thermic preferences (Edwards 1971; Miegel et al. 2010). Effects of environmental pH on fish physiology seem to be, on the other hand, more limited (Kroeker et al. 2010). However, few studies indicated that pH can alter the structure and functioning of the digestive tract (e.g. Frommel et al. 2014) and even the digestive enzyme activities (Pimentel et al. 2015; Rosa et al. 2016) of early stages of marine fish. The variation of temperature and pH may occur simultaneously, and organisms can be affected differently by them. Indeed, interactions of temperature with pH could theoretically generate a simple sum of the effect of each individual factor (additive effect) or more complex situations (antagonistic or synergistic effects) as explained by Flynn et al. (2015). In their natural environment, marine fish are most probably facing these possible complex interactions.
In this context, the present study aims to assess the possible effects of two environmental variables (temperature and pH) on the assimilation of two essential (Co and Zn) and one non-essential (Ag) metals in the juvenile turbot Scophthalmus maximus. Radiotracer techniques were used to determine depuration parameters in controlled conditions of juvenile turbot previously acclimated at two temperatures (17 and 20 °C) and pH (7.5 and 8.0) after a single feeding with radiolabelled shrimp.
Materials and methods
Origin and acclimation of fish
Juvenile turbot S. maximus were purchased from a fish farm (France Turbot, www.france-turbot.com) and shipped to the International Atomic Energy Agency premises in the Principality of Monaco. Fish were randomly placed in four 20-L aquaria (n = 8) and acclimated for minimum of 1 month to laboratory conditions (open circuit, water renewal 60 L h−1; 0.45 μm filtered seawater; salinity 38; light/dark 12/12 h; temperature 17 °C; pH 8.00). During this period, the fish were fed one time per day (as described by Pouil et al. 2015 and Pouil et al. 2016) with a ration of 1.5% of their biomass with 1.1-mm pellets (proteins 55% and lipids 12%; Le Gouessant, www.legouessant.com). After this period, fish were acclimated to the target temperature and pH values (see Table 1) for 8 weeks prior to a unique radiotracer exposure (i.e. one single feeding using radiolallebed shrimp following by 21 days of depuration as described in the “Exposure of turbot via radiolabelled shrimp” section).
Juveniles were exposed under controlled temperature and pH conditions in a crossed experimental design (two temperatures × two pH levels). The two temperatures were 17 and 20 °C, and the two pH values were 8.00 (pCO2 of approx. 450 μatm) and 7.50 (pCO2 of approx. 1800 μatm). These values were chosen based on the optimal food conversion efficiency (FCE) ratio of juvenile turbot at 17.4 ± 0.5 °C at normal pH (Imsland et al. 2001) and the current projections provided by the literature for the next two centuries (ΔT°C +3 °C and ΔpH −0.5; Orr et al. 2005; IPCC 2013).
Concerning the method used to regulate the seawater pH, we followed the recommendations of the Guide to best Practices for Ocean Acidification Research and Data Reporting (Riebesell et al. 2010). The pHNBS was monitored every 15 min in each aquarium to within ±0.05 pHNBS units using a pH probe connected to a multi-probe aquaristic computer (IKS ComputerSysteme, www.iks-aqua.com) that bubbled pure CO2 into the aquaria. Temperature in each aquarium was also monitored, using a dedicated probe connected to the same computer. The pH probes were calibrated weekly using Tris-HCl and NBS buffer solutions (Dickson et al. 2007). Total alkalinity was measured by titration using Metrohm 809 Titrando calibrated with NBS buffers, Tris-HCl (Batch 150, Dickson 2016) and reference materials (Batch 137, Dickson 2016). pCO2 was determined from pH, temperature and total alkalinity measurements using the R package seacarb (Lavigne et al. 2011).
Experimental procedures
Shrimp radiolabelling
Since crustaceans dominated the natural diet of turbot (Sparrevohn and Støttrup 2008; Florin and Lavados 2010), we used shrimp as radiolabelled prey. Preparation of the 80 radiolabelled shrimp Palaemon sp. (approx. 1 to 2 cm in total length) was carried out by exposing them for 7 days to dissolved radiotracers in an aerated 20-L aquarium (closed circuit; shrimp density 4 shrimps L−1, 0.45 μm filtered seawater; salinity 38; light/dark 12/12 h; temperature 17 °C; pH 8.00). Radiotracers of high specific activity were purchased from Polatom, Poland (57Co as CoCl2 in 0.1 M HCl, t 1/2 = 272 days; 65Zn as ZnCl2 in 0.1 M HCl, t 1/2 = 244 days and 110mAg as AgNO3 in 0.1 M HNO3, t 1/2 = 252 days). Seawater was spiked with small volumes (>0.2 mL) of radiotracers (nominal activity of 2 kBq L−1 for 57Co and 8 kBq L−1 for 65Zn and 110mAg). No change in pH was detectable in the aquarium (close circuit) after the tracer additions. During the 7-day exposure, seawater was renewed and spiked four times to eliminate ammonia generated by shrimp excretion and keep the radiotracer activity constant. The activity of the radiolabelled metal tracers in seawater was checked before and after each seawater renewal, to determine time-integrated activities (Warnau et al. 1996; Rodriguez y Baena et al. 2006). Each organism was kept isolated during the duration of the experiment in a buoyant cylindrical polystyrene container (drilled to allow for free water circulation) in order to avoid cannibalism. The shrimps were fed with non-contaminated minced mussels one time between each water renewal.
Exposure of turbot via radiolabelled shrimp
A total of eight acclimatized turbot were randomly selected for each experimental treatment (viz. 4 × 20-L tanks with each time eight organisms; wet weights were 22.4 ± 3.4, 22.1 ± 3.8, 22.3 ± 5.4 and 23.7 ± 4.2 g respectively for the turbot exposed to pH 8.0 at 17 °C, pH 8.0 at 20 °C, pH 7.5 at 17 °C and pH 7.5 at 20 °C). Slits cut into the fins were performed on anaesthetised fish to facilitate individual recognition, ensuring at the same time the welfare of the fish (see e.g. Pouil et al. 2016). For the last three feedings before the exposure to radiolabelled shrimp, fish, previously fed with pellets, were fed with non-labelled shrimp. The experiment consisted of a single feeding of fish in the different experimental conditions with radiolabelled shrimp. To facilitate ingestion, radiolabelled shrimp were cut into pieces (Pouil et al. 2016). During and after the 5-min radiolabelled feeding, an additional turbot was placed in each aquarium to assess any possible radiotracer recycling from seawater due to leaching from the radiolabelled food or, later on, from fish depuration. Two hours after the radiolabelling feeding, all the fish (including control individual of each condition) were whole-body γ-counted alive (Pouil et al. 2016). They were then replaced in the same open-circuit aquarium and were regularly radioanalysed to follow the radiotracer depuration kinetics over 21 days. During the first week of depuration, turbot were fed using non-labelled shrimp and then fed daily with non-labelled pellets (1.5% of their biomass) to cover their nutritional needs.
Radioanalysis
The radioactivity of the tracers was measured using a high-resolution γ-spectrometer system composed of four germanium —N or P type— detectors (EGNC 33-195-R, Canberra® and Eurysis®) connected to a multi-channel analyser and a computer equipped with a spectra analysis software (Interwinner 6, Intertechnique®). The radioactivity in living organisms and samples was determined by comparison with standards of known activity and of appropriate geometry (calibration and counting). Measurements were corrected for background and physical radioactive decay. Living organisms were placed in counting tubes (diameter 160 mm, height 80 mm) filled with clean seawater (at the appropriated conditions of pH and temperature) during the counting period. The counting period was adjusted to obtain a propagated counting error less than 5% (e.g. Rodriguez y Baena et al. 2006) and varied between 15 and 60 min in order to maintain fish health and ensure normal behaviour. Variations of temperature and pH during the counting have not exceeded +2 °C and −0.2 respectively. These recorded values were the extreme variation measured at the end of long counting times which occurred at the last days of depuration; at the beginning, average increase temperature and decrease of pH were negligible.
Data treatment and statistical analysis
Depuration of radiotracers was expressed as the percentage of remaining radioactivity [(radioactivity at time t divided by the initial radioactivity measured in the organism at the beginning of the depuration period, following methods developed in Warnau et al. (1996)]. The depuration kinetics of of the three studied elements were best fitted using a two-component exponential model:
where A t and A 0 are the remaining activities (%) at time t (days) and 0 respectively; k e is the depuration rate constant (day−1). “s” and “l” subscripts are related to the short-lived and long-lived components respectively. The s component represents the depuration of the radiotracer fraction that is weakly associated with the organisms and rapidly eliminated (i.e. proportion associated with the faeces). The l component describes the depuration of the radiotracer fraction that is actually absorbed by the organism and eliminated slowly. The long-lived component allows estimating the assimilation efficiency (AE) of the radiotracer ingested with food (AE = A 0l ). Because depuration of the assimilated fraction of the three studied elements was extremely slow, the long-term depuration rate constant (k el ) might not be significantly different from 0, then T b1/2l tends towards +∞ and thus the l component of the model could therefore be simplified and replaced by a constant (as shown by Pouil et al. 2016). The equation becomes
For the short-lived component, a biological half-life can be calculated (T b1/2) from the corresponding depuration rate constant according to the relation T b1/2s = ln2/k es . Model constants and their statistics were estimated by iterative adjustment of the model and Hessian matrix computation respectively using the non-linear curve-fitting routines in the Statistica® software 7.0.
Comparison of assimilation of metals among the different experimental conditions was performed using two-way ANOVA on k es and AE calculated for each individual turbot (the best fitting model obtained for the entire set of turbots was applied to individuals; Zar 1996). For Co, two individuals per condition with an insufficient initial activity (i.e. activity measured 2 h after the radiolabelled feeding) have been excluded from statistical analysis. The level of significance for statistical analyses was always set at α = 0.05. All the statistical analyses were performed using R software 3.0.1 (R Core Team 2014).
Results
In order to evaluate whether different abiotic factors (i.e. temperature and pH) affect metal assimilation in the juvenile turbot S. maximus, depuration kinetics of two essential (Co and Zn) and one non-essential metals (Ag) were followed after a pulse-chase feeding, using radiolabelled shrimp. During the whole experimental period (i.e. 8 weeks of acclimation to the targeted temperature and pH values and 3 weeks of depuration) where the fish were exposed to four different conditions (combinations of two temperatures and two pH; see the “Materials and methods” section), only a limited growth of the individuals was measured and no mortality was recorded. Before the pulse-chase feeding of the fish, the activity level of each metal in the shrimps was measured: The average activities (Bq g-1 wwt) were 20 ± 5 Bq 57Co g−1, 213 ± 65 Bq 65Zn g−1 and 134 ± 62 Bq 110mAg g−1. During the entire experiment, no activity was measured in the control turbot.
Whole-body depuration kinetics of 57Co, 65Zn and 110mAg in turbot were best fitted by a two-phase model (simple exponential model and a constant; Fig. 1; R 2 0.89–0.99). A large proportion (71–96%) of the ingested radiotracers was associated with the short-term component for all the studied elements. This component was characterized by a very rapid loss (T b1/2s ranged from 0.3 to 0.7 days). Comparison of k es determined for each individual turbot indicated that, for all the elements (Co, Zn and Ag), there is no significant difference (p ANOVA >0.05, Fig. 2) independently of the pH and temperature conditions.
Estimated AEs in turbot ranged from 19 to 29% for Zn whereas Co and Ag were very poorly assimilated by turbot (AE <9% for Co and AE <5% for Ag; Fig. 2). Statistical analyses carried out on individual estimated AEs revealed that neither temperature nor pH significantly affected the trophic transfer of Ag and Co in turbots (p > 0.05; Fig. 2). In contrast, a significant effect of the temperature was observed between the two treatments at pH 8.0 for Zn (p ANOVA = 0.03; Fig. 2) but not at the lower pH.
Discussion
Scientists increasingly realize that single-stressor experiments may not be appropriate to assess the realistic effects of environmental variables in marine habitats (Wernberg et al. 2012). In this context, the present study analysed the combined effects of two abiotic factors on the assimilation efficiency of three metals in a coastal marine fish, turbot. Temperature and pH are important drivers of fish physiology and are subject to important fluctuations at various temporal scales, especially in coastal environments; therefore, it is important to better understand the influence of such environmental factors on the assimilation of metals in marine fish.
The main result of this study is that temperature and pH together have limited influence on the AE of Ag and Co, while the Zn AE appears to be only influenced by temperature. At optimal pH for the turbot (pH = 8.0), increasing the seawater temperature resulted in a significantly increase of Zn AE, which could be due to either from the following: (1) the gut passage of Zn reduced at lower temperature, and/or (2) less Zn was strongly retained by the body at lower temperature. In some flatfish species (i.e. the winter flounder Pseudopleuronectes americanus and the European plaice Pleuronectes platessa), anterior intestine is the most important body compartment involved in Zn assimilation (Pentreath 1976; Shears and Fletcher 1983). For this element, although the mechanisms of transfer from the gut lumen to the intern compartment (adsorption) are not completely elucidated yet, it seems dominated by active processes involving specific transporters (Bury et al. 2003). Temperature variations have been shown to provoke changes in the structure and the protein status of the gut cell membranes (Hazel 1995; Zehmer and Hazel 2005) or in digestive enzyme kinetics (Smit 1967; Brett and Higgs 1970) which can, in turn, possibly influence the active transport mechanisms of Zn and lead to the increase of Zn AE observed in this study at the highest temperature.
In the current experimental setup, AE of Zn was much higher (AE >19%) compared to the AEs for Ag and Co, both being poorly assimilated by the turbot (AE <9%). These results are in accordance with the literature (Zn AE 17–32%, Ag AE 0.3–3%, Co AE 5–43%; see Mathews et al. 2008; Pouil et al. 2015; Pouil et al. 2016) and could explain why temperature only influenced Zn AE. Indeed, for these other metals (Co and Ag), a poor assimilation makes difficult to highlight any significant effect. A temperature-dependent effect on Zn assimilation has been already shown in freshwater fish: the common carp Cyprinus carpio (fed with Zn-contaminated prey; Van Campenhout et al. 2007). However, in marine fish, although a temperature-dependent effect on metal assimilation was not identified yet, Pouil et al. (2017) have also shown, using the concentration index defined by Rouleau et al. (2000), that the intestine is involved in the absorption process of Zn in the silver moony Monodactylus argenteus. As discussed by Van Campenhout et al. (2007), one of the possible explanations for the observed differences might be possibly explained by the higher concentration of Zn transporters in the intestine of fish exposed to higher temperatures.
In contrast to temperature, fewer studies investigated the influence of pH on the assimilation of metals by marine biota (Lacoue-Labarthe et al. 2011; Götze et al. 2014; Ivanina et al. 2015), and to the best of our knowledge, even none has investigated the influence of pH on metal trophic transfer in fish. However, in the context of the current ocean acidification, some authors have recently highlighted the effects of the partial pressure of CO2 (pCO2) on the digestion of fish (Pimentel et al. 2015; Rosa et al. 2016). Indeed, these authors have shown that the activity of the digestive enzymes in marine fish is dependent of pCO2. Usually, pH values were converted in pCO2 from seawater carbonate chemistry. In the present study, in addition to the constant monitoring of pH, the total alkalinity has also been regularly monitored (see the “Materials and methods” section). Thus, pH values were converted in pCO2. In the present paper, we have used an integrated approach for assessing the effect of pH on fish physiology using assimilation efficiency as an end-point, but no effect of pH was found on the trophic transfer of the three studied metals in turbot.
Temperature and pH can interact in different ways on the physiology of marine organisms (Boyd and Hutchins 2012; Gunderson et al. 2016). In the present study, we did not find any combined effect of temperature and pH on metal assimilation. Contrasting responses regarding the bioaccumulation of metal in marine organisms have been reported in the scientific literature. Temperature can affect the bioconcentration of essential (Co, Mn, Se and Zn) and non-essential (Cd and Ag) metals with similar patterns at different pH (7.60, 7.85 and 8.10) as already demonstrated in cuttlefish eggs (Lacoue-Labarthe et al. 2009; Lacoue-Labarthe et al. 2012). However, Belivermiş et al. (2015) have shown, in Pacific oyster Crassostrea gigas, that the effects of temperature on the bioaccumulation of Cd, Co and Mn were dependent of the pH conditions (7.5, 7.8 and 8.1). Even if the relations between temperature and pH effects can be complex to interpret, the absence of effect of the temperature at the lower pH (i.e. 7.5) observed in our study could be related to antagonistic effects of these abiotic factors. Thus, further studies investigating a wider range of exposure of temperature and pH and based on a mechanistic approach will be needed to support this assumption.
Conclusions
This study provides new information on the assimilation efficiency of two essential (Co and Zn) and one non-essential (Ag) metals in marine fish (turbot). Our results suggest that two abiotic factors (temperature and pH) do not have a significant role in the assimilation efficiency of Co and Ag; however, temperature has a slight effect on Zn assimilation in the juvenile turbot S. maximus. Based on these results, further studies should be carried out in order to cover a wider range of exposure of temperature and pH to assess precisely its effect on Zn assimilation in fish, taking into account the high variability of the responses between marine organism (Parker et al. 2011) and the adaptive capacities of organisms, especially in the context of global change where organisms are facing long-term modifications of the environmental conditions.
References
Beitinger TL, Fitzpatrick LC (1979) Physiological and ecological correlates of preferred temperature in fish. Am Zool 19:319–329
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
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
Bury NR, Walker PA, Glover CN (2003) Nutritive metal uptake in teleost fish. J Exp Biol 206:11–23
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
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
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
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
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
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
Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42
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
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
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
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
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
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
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
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
Mathews T, Fisher NS (2009) Dominance of dietary intake of metals in marine elasmobranch and teleost fish. Sci Total Environ 407:5156–5161
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
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
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
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
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
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
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
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
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
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
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
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
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
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
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
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
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
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
Wang W-X, Fisher NS (1999) Assimilation efficiencies of chemical contaminants in aquatic invertebrates: a synthesis. Environ Toxicol Chem 18:2034–2045
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
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
Warnau M, Bustamante P (2007) Radiotracer techniques: a unique tool in marine ecotoxicological studies. Environ Bioindic 2:217–218
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
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
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
Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice-Hall, Upper Saddle River
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
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
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
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
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-8691-4