Skip to main content

Advertisement

SpringerLink
Log in

Habitat selection disruption and lateralization impairment of cryptic flatfish in a warm, acid, and contaminated ocean

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

An Erratum to this article was published on 16 November 2016

Abstract

Anthropogenic release of greenhouse gases is leading to significant changes in ocean physicochemical properties. Although marine organisms will have to deal with combined effects of ocean warming and acidification, little is known about the impact of interactions between these climate change variables and contaminants. Nowadays, mercury emissions are mostly of anthropogenic origin, and part of these emissions is deposited in the ocean sediment. Within this context, our goal was to determine the acclimation potential of a benthic flatfish, Solea senegalensis, to future climate change scenarios and methylmercury (MeHg) neurotoxicity. After 28 days of exposure under three-factor crossed treatments of MeHg contamination (non-contaminated and contaminated feed, 0.08 ± 0.02 and 8.51 ± 0.15 mg kg−1 dry weight, respectively), high CO2 (ΔCO2 ≈ 500 ppm), and temperature (ΔT = 4 °C), we investigated brain mercury accumulation, habitat preference, and relative/absolute lateralization, as well as acetylcholinesterase (AChE) activity in five brain regions. Our results indicate a differential effect of hypercapnia (decrease) on brain mercury accumulation. MeHg-contaminated flatfish displayed decreased AChE activity, impaired lateralization, and bottom choosing judgment. Contaminated fish spent significantly higher amounts of time in the complex habitat, where they could neither bury nor match the background. While warming led to higher enzymatic activity, acidification decreased Hg accumulation, but also affected AChE activity and disrupted habitat selection. Present-day MeHg environmental concentrations may lead to severe disruption of behavioral and neurological functions, which, combined with ocean warming and acidification, might further jeopardize the ecological fitness of flatfish.

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

Access this article

Log in via an institution

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

  • Andén NE, Dahlström A, Fuxe K et al (1966) Ascending monoamine neurons to the telencephalon and diencephalon. Acta Physiol Scand 67:313–326

    Article  Google Scholar 

  • Baatrup E (1991) Structural and functional effects of heavy metals on the nervous system, including sense organs, of fish. Comp Biochem Physiol C Comp Pharmacol 100:253–257

    Article  CAS  Google Scholar 

  • Basbaum AI, Fields HL (1984) Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7:309–338

    Article  CAS  Google Scholar 

  • Beauvais SL, Jones SB, Parris JT et al (2001) Cholinergic and behavioral neurotoxicity of carbaryl and cadmium to larval rainbow trout (Oncorhynchus mykiss). Ecotoxicol Environ Saf 49:84–90

    Article  CAS  Google Scholar 

  • Beliles RP, Yule CL (1968) The effects of exposure to mercury vapos on behavior of rats. Toxicol Appl Pharmacol 12:15–21

    Article  CAS  Google Scholar 

  • Bisazza A, Rogers LJ, Vallortigara G (1998) The origins of cerebral asymmetry: a review of evidence of behavioural and brain lateralization in fishes, reptiles and amphibians. Neurosci Biobehav Rev 22:411–426

    Article  CAS  Google Scholar 

  • Bisazza A, Facchin L, Vallortigara G (2000) Heritability of lateralization in fish: concordance of right-left asymmetry between parents and offspring. Neuropsychologia 38:907–912

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3

    Article  CAS  Google Scholar 

  • Castoldi AF, Coccini T, Ceccatelli S, Manzo L (2001) Neurotoxicity and molecular effects of methylmercury. Brain Res Bull 55:197–203

    Article  CAS  Google Scholar 

  • Caston J, Chianale C, Delhaye-Bouchaud N, Mariani J (1998) Role of the cerebellum in exploration behavior. Brain Res 808:232–237

    Article  CAS  Google Scholar 

  • Chang LW (1977) Neurotoxic effects of mercury—a review. Environ Res 14:329–373

    Article  CAS  Google Scholar 

  • Coccini T, Randine G, Candura SM et al (2000) Low-level exposure to methylmercury modifies muscarinic cholinergic receptor binding characteristics in rat brain and lymphocytes: physiologic implications and new opportunities in biologic monitoring. Environ Health Perspect 108:29–33

    Article  CAS  Google Scholar 

  • Cornwall CE, Hurd CL (2015) Experimental design in ocean acidification research: problems and solutions. ICES J Mar Sci 73:572–581

    Article  Google Scholar 

  • Decker MW, McGaugh JL (1991) The role of interactions between the cholinergic system and other neuromodulatory systems in learning and memory. Synapse 7:151–168

    Article  CAS  Google Scholar 

  • Dickson A, Millero F (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res 34:1733–1743

    Article  CAS  Google Scholar 

  • Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication 3

  • Dijkstra JA, Buckman KL, Ward D et al (2013) Experimental and natural warming elevates mercury concentrations in estuarine fish. PLoS ONE 8:1–9

    Google Scholar 

  • Dizer H, de Assis H, Hansen P (2001) Cholinesterase activity as bioindicator for monitoring marine pollution in the Baltic Sea and the Mediterranean Sea. In: Garrigues P, Barth H, Walker C, Narbone JF (eds) Biomarker in marine organisms: a practical approach. Elsevier Science, Amsterdam, pp 331–342

    Chapter  Google Scholar 

  • Domenici P, Allan B, McCormick MI, Munday PL (2012) Elevated carbon dioxide affects behavioural lateralization in a coral reef fish. Biol Lett 8:78–81

    Article  CAS  Google Scholar 

  • Domenici P, Allan BJM, Watson S-A et al (2014) Shifting from right to left: the combined effect of elevated CO2 and temperature on behavioural lateralization in a coral reef fish. PLoS ONE 9:e87969

    Article  Google Scholar 

  • Donald DA (1998) Autonomic nervous system. In: Evans DH (ed) The physiology of fishes, 2nd edn. CRC Press, Boca Raton, pp 407–439

    Google Scholar 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  Google Scholar 

  • EPA (2007) Mercury in solids and solutions by thermal decomposition, amalgamation, and atomic absorption spectrophotometry. Method 7473:1–17

    Google Scholar 

  • Fonseca VF, França S, Serafim A et al (2011) Multi-biomarker responses to estuarine habitat contamination in three fish species: Dicentrarchus labrax, Solea senegalensis and Pomatoschistus microps. Aquat Toxicol 102:216–227. doi:10.1016/j.aquatox.2011.01.018

    Article  CAS  Google Scholar 

  • Friberg L, Mottet NK (1989) Accumulation of methylmercury and inorganic mercury in the brain. Biol Trace Elem Res 21:201–206. doi:10.1007/BF02917253

    Article  CAS  Google Scholar 

  • Frisch C, Dere E, Silva MA et al (2000) Superior water maze performance and increase in fear-related behavior in the endothelial nitric oxide synthase-deficient mouse together with monoamine changes in cerebellum and ventral striatum. J Neurosci 20:6694–6700

    CAS  Google Scholar 

  • Gibson RN, Nash RDM, Geffen AJ, van der Veer HW (2014) Flatfishes: biology and exploitation. Wiley, New York

    Book  Google Scholar 

  • Giorgetti M, Bacciottini L, Giovannini MG et al (2000) Local GABAergic modulation of acetylcholine release from the cortex of freely moving rats. Eur J Neurosci 12:1941–1948

    Article  CAS  Google Scholar 

  • Hamilton TJ, Holcombe A, Tresguerres M (2014) CO2-induced ocean acidification increases anxiety in Rockfish via alteration of GABA A receptor functioning. Proc R Soc B 281:20132509

    Article  Google Scholar 

  • Hara TJ, Law YMC, Macdonald S (1976) Effects of mercury and copper on the olfactory response in rainbow trout, Salmo gairdneri. J Fish Res Board Can 33:1568–1573

    Article  CAS  Google Scholar 

  • Healey EG (1999) The skin pattern of young plaice and its rapid modification in response to graded changes in background tint and pattern. J Fish Biol 55:937–971

    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, Cambridge

  • Jozet-Alves C, Viblanc VA, Romagny S et al (2012) Visual lateralization is task and age dependent in cuttlefish, Sepia officinalis. Anim Behav 83:1313–1318

    Article  Google Scholar 

  • Kelman EJ, Tiptus P, Osorio D (2006) Juvenile plaice (Pleuronectes platessa) produce camouflage by flexibly combining two separate patterns. J Exp Biol 209:3288–3292

    Article  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 

  • Langenbuch M, Pörtner HO (2004) High sensitivity to chronically elevated CO2 levels in a eurybathic marine sipunculid. Aquat Toxicol 70:55–61

    Article  CAS  Google Scholar 

  • Leakey CDB, Attrill MJ, Fitzsimons MF (2009) Multi-element otolith chemistry of juvenile sole (Solea solea), whiting (Merlangius merlangus) and European seabass (Dicentrarchus labrax) in the Thames Estuary and adjacent coastal regions. J Sea Res 61:268–274

    Article  CAS  Google Scholar 

  • Leclercq E, Taylor JF, Migaud H (2010) Morphological skin colour changes in teleosts. Fish Fish 11:159–193

    Article  Google Scholar 

  • Lee RF, Windom H, Summers JK (1998) Distribution of total mercury and methyl mercury in water, sediment, and fish from south Florida estuaries. Arch Environ Contam Toxicol 34:109–118

    Article  Google Scholar 

  • Levene H (1960) Robust tests for equality of variances. In: Olkin I, Hotelling H (eds) Contributions to probability and statistics: essays in honor of Harold Hotelling. Stanford University Press, Stanford, pp 278–292

    Google Scholar 

  • Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, TN

  • Marques A, Nunes ML, Moore SK, Strom MS (2010) Climate change and seafood safety: human health implications. Food Res Int 43:1766–1779

    Article  Google Scholar 

  • Mason RP (2001) The bioaccumulation of mercury, methylmercury and other toxic elements into pelagic and benthic organisms. In: Newman N, Roberts M Jr, Hale R (eds) Coastal and estuarine risk assessment. Lewis Publishers, Boca Raton, pp 127–149

    Google Scholar 

  • McClellan AD (1984) Descending control and sensory gating of “fictive” swimming and turning responses elicited in an in vitro preparation of the lamprey brainstem/spinal cord. Brain Res 302:151–162

    Article  CAS  Google Scholar 

  • Mehrbach C, Culberson CH, Hawley JE, Pytkowicx RM (1973) Measurement of the apparent dissociation constantes of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    Article  CAS  Google Scholar 

  • Michaelidis B, Spring A, Pörtner HO (2007) Effects of long-term acclimation to environmental hypercapnia on extracellular acid-base status and metabolic capacity in Mediterranean fish Sparus aurata. Mar Biol 150:1417–1429

    Article  Google Scholar 

  • Munday PL, Cheal AJ, Dixson DL et al (2014) Behavioural impairment in reef fishes caused by ocean acidification at CO2 seeps. Nat Clim Change 4:487–492. doi:10.1038/nclimate2195

    Article  CAS  Google Scholar 

  • Nilsson GE, Dixson DL, Domenici P et al (2012) Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat Clim Change 2:201–204

    Article  CAS  Google Scholar 

  • Nunes M, Coelho JP, Cardoso PG et al (2008) The macrobenthic community along a mercury contamination in a temperate estuarine system (Ria de Aveiro, Portugal). Sci Total Environ 405:186–194

    Article  CAS  Google Scholar 

  • Perry SF, Walsh PJ, Mommsen TP, Moon TW (1988) Metabolic consequences of hypercapnia in the rainbow trout Salmo airdneri: β-adrenergic effects. Gen Comp Endocrinol 69:439–447

    Article  CAS  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Rapoport M, van Reekum R, Mayberg H (2000) The role of the cerebellum in cognition and behavior: a selective review. J Neuropsychiatry Clin Neurosci 12:193–198

    Article  CAS  Google Scholar 

  • R Development Core Team (2014) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. Available at http://www.R-project.org

  • Roeser T, Baier H (2003) Visuomotor behaviors in larval zebrafish after GFP-guided laser ablation of the optic tectum. J Neurosci 23:3726–3734

    CAS  Google Scholar 

  • Rouleau C, Borg-Neczak K, Gottofrey J, Tjälve H (1999) Accumulation of waterborne mercury(II) in specific areas of fish brain. Environ Sci Technol 33:3384–3389

    Article  CAS  Google Scholar 

  • Ryer CH, Lemke JL, Boersma K, Levas S (2008) Adaptive coloration, behavior and predation vulnerability in three juvenile north Pacific flatfishes. J Exp Mar Bio Ecol 359:62–66

    Article  Google Scholar 

  • Saidel WM (1988) How to be unseen: An essay in obscurity. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer New York, New York, NY, pp 487–513

    Chapter  Google Scholar 

  • Sakamoto M, Kakita A, Wakabayashi K et al (2002) Evaluation of changes in methylmercury accumulation in the developing rat brain and its effects: a study with consecutive and moderate dose exposure throughout gestation and lactation periods. Brain Res 949:51–59

    Article  CAS  Google Scholar 

  • Sarazin G, Michard G, Prevot F (1999) A rapid and accurate spectroscopic method for alkalinity measurements in sea water samples. Water Res 33:290–294

    Article  CAS  Google Scholar 

  • Scerbo R, Barghigiani C (1998) organic mercury determination in fish samples using an automatic mercury analyser. Environ Technol 19:339–342

    Article  CAS  Google Scholar 

  • Schiedek D, Sundelin B, Readman JW, Macdonald RW (2007) Interactions between climate change and contaminants. Mar Pollut Bull 54:1845–1856

    Article  CAS  Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611

    Article  Google Scholar 

  • Springer AD, Easter SS, Agranoff BW (1977) The role of the optic tectum in various visually mediated behaviors of goldfish. Brain Res 128:393–404

    Article  CAS  Google Scholar 

  • Stevens RJ (1973) A cholinergic inhibitory system in the frog optic tectum: its role in visual electrical responses and feeding behavior. Brain Res 49:309–321

    Article  CAS  Google Scholar 

  • Stoner AW, Titgen RH (2003) Biological structures and bottom type influence habitat choices made by Alaska flatfishes. J Exp Mar Biol Ecol 292:43–59

    Article  Google Scholar 

  • Summers CH, Winberg S (2006) Interactions between the neural regulation of stress and aggression. J Exp Biol 209:4581–4589

    Article  CAS  Google Scholar 

  • Sumner FB (1911) The adjustment of flatfishes to various backgrounds. J Exp Zool 10:409–506

    Article  Google Scholar 

  • Toscano-Márquez B, Dunn RJ, Krahe R (2013) Distribution of muscarinic acetylcholine receptor mRNA in the brain of the weakly electric fish Apteronotus leptorhynchus. J Comp Neurol 521:1054–1072

    Article  Google Scholar 

  • Vieira LR, Gravato C, Soares A et al (2009) Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behaviour. Chemosphere 76:1416–1427

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The research leading to these results (as well as ES, VB, and RA) was funded from the European Union Seventh Framework Programme (FP7/2007-2013) under the ECsafeSEAFOOD project (Grant Agreement No. 311820). Sparos Lda, team for preparing the contaminated and non-contaminated feed. IPMA DivAV team from Olhão (aquaculture facilities) for providing juvenile sole specimens for the trials. The Portuguese Foundation for Science and Technology (FCT) supported the contract of RR and AM in the framework of the IF 2013 and IF2014 programs. FCT also funded PhD scholarships (ALM, SFRH/BD/103569/2014; VML, SFRH/BD/97633/2013; JRP, SFRH/BD/111153/2015), and by a FCT Postdoctoral scholarship (TR, SFRH/BPD/98590/2013).

Author information

Authors and Affiliations

  1. Divisão de Aquacultura e Valorização (DivAV), Instituto Português do Mar e da Atmosfera (IPMA, I.P.), Av. Brasília, 1449-006, Lisbon, Portugal

    Eduardo Sampaio, Ana Luísa Maulvault, Vera Barbosa, Ricardo Alves, Pedro Pousão-Ferreira & António Marques

  2. Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Rua das Bragas, 289, 4050-123, Porto, Portugal

    Ana Luísa Maulvault & António Marques

  3. MARE - Marine Environmental Science Centre, Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa, Av. Nossa Senhora do Cabo 939, 2750-374, Cascais, Portugal

    Eduardo Sampaio, Ana Luísa Maulvault, Vanessa M. Lopes, José R. Paula, Tiago Repolho & Rui Rosa

Authors
  1. Eduardo Sampaio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana Luísa Maulvault
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vanessa M. Lopes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José R. Paula
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vera Barbosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ricardo Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pedro Pousão-Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tiago Repolho
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. António Marques
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Rui Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eduardo Sampaio.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

All procedures followed ARRIVE guidelines, overseen by the Portuguese National Competent Authority (Direção-Geral de Alimentação e Veterinária, DGAV). Moreover, personnel involved in this experiment had professional certification in handling and humane killing of laboratory animals by the Federation of European Laboratory Animal Science Associations (FELASA).

Additional information

Responsible Editor: A. E. Todgham.

Reviewed by S. S. Killen and undisclosed experts.

An erratum to this article is available at http://dx.doi.org/10.1007/s00227-016-3019-3.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 420 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sampaio, E., Maulvault, A.L., Lopes, V.M. et al. Habitat selection disruption and lateralization impairment of cryptic flatfish in a warm, acid, and contaminated ocean. Mar Biol 163, 217 (2016). https://doi.org/10.1007/s00227-016-2994-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-2994-8

Keywords

Search

Navigation