Skip to main content

Advertisement

SpringerLink
Log in

Absence of cellular damage in tropical newly hatched sharks (Chiloscyllium plagiosum) under ocean acidification conditions

  • Original Paper
  • Published:
Cell Stress and Chaperones Aims and scope

Abstract

Sharks have maintained a key role in marine food webs for 400 million years and across varying physicochemical contexts, suggesting plasticity to environmental change. In this study, we investigated the biochemical effects of ocean acidification (OA) levels predicted for 2100 (pCO2 ~ 900 μatm) on newly hatched tropical whitespotted bamboo sharks (Chiloscyllium plagiosum). Specifically, we measured lipid, protein, and DNA damage levels, as well as changes in the activity of antioxidant enzymes and non-enzymatic ROS scavengers in juvenile sharks exposed to elevated CO2 for 50 days following hatching. Moreover, we also assessed the secondary oxidative stress response, i.e., heat shock response and ubiquitin levels. Newly hatched sharks appear to cope with OA-related stress through a range of tissue-specific biochemical strategies, specifically through the action of antioxidant enzymatic compounds. Our findings suggest that ROS-scavenging molecules, rather than complex enzymatic proteins, provide an effective defense mechanism in dealing with OA-elicited ROS formation. We argue that sharks’ ancient antioxidant system, strongly based on non-enzymatic antioxidants (e.g., urea), may provide them with resilience towards OA, potentially beyond the tolerance of more recently evolved species, i.e., teleosts. Nevertheless, previous research has provided evidence of detrimental effects of OA (interacting with other climate-related stressors) on some aspects of shark biology. Moreover, given that long-term acclimation and adaptive potential to rapid environmental changes are yet experimentally unaccounted for, future research is warranted to accurately predict shark physiological performance under future ocean conditions.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alamdari DH, Kostidou E, Paletas K, Sarigianni M, Konstas AG, Karapiperidou A, Koliakos G (2005) High sensitivity enzyme-linked immunosorbent assay (ELISA) method for measuring protein carbonyl in samples with low amounts of protein. Free Radic Biol Med 39:1362–1367

    Article  PubMed  CAS  Google Scholar 

  • Bartosz G (2003) Total antioxidant capacity. In: Spiegel HE, Nowacki G, Hsiao K-J (eds) Advances in clinical chemistry, vol 37. Academic press, California, pp 220–272

    Google Scholar 

  • Baum JK, Myers RA, Kehler DG, Worm B, Harley SJ, Doherty PA (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299:389–392

    Article  PubMed  CAS  Google Scholar 

  • Baumann H, Talmage SC, Gobler CJ (2012) Reduced early life growth and survival in a fish in direct response to increased carbon dioxide. Nat Clim Chang 2:38–41

    Article  CAS  Google Scholar 

  • Bond U, Agell N, Haas AL, Redman K, Schlesinger MJ (1988) Ubiquitin in stressed chicken embryo fibroblast. J Biol Chem 263:2384–2388

    PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Burnett LE (1997) The challenges of living in hypoxic and hypercapnic aquatic environments. Integr Comp Biol 37:633–640

    Google Scholar 

  • Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:C09S04

    Article  CAS  Google Scholar 

  • Clements JC, Hunt HL (2014) Influence of sediment acidification and water flow on sediment acceptance and dispersal of juvenile soft-shell clams (Mya arenaria L.) J Exp Mar Biol Ecol 453:62–69

    Article  CAS  Google Scholar 

  • Dean JB (2010) Hypercapnia causes cellular oxidation and nitrosation in addition to acidosis: implications for CO2 chemoreceptor function and dysfunction. J Appl Physiol 108:1786–1795

    Article  PubMed  PubMed Central  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 

  • Dixson DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol Lett 13:68–75

    Article  PubMed  Google Scholar 

  • Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Polovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4:11–37

    Article  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  PubMed  CAS  Google Scholar 

  • Filho DW, Boveris A (1993) Antioxidant defences in marine fish—II. Elasmobranchs. Comp Biochem Physiol C 106:415–418

    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  PubMed  Google Scholar 

  • Gattuso J-P, Hansson L (2011) Ocean acidification: background and history. In: Gattuso J-P, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, pp 1–17

    Google Scholar 

  • Hanna J, Meides A, Zhang DP, Finley D (2007) A ubiquitin stress response induces altered proteasome composition. Cell 129:747–759

    Article  PubMed  CAS  Google Scholar 

  • Heinrich DDU, Rummer JL, Morash AJ, Watson S-A, Simpfendorfer CA, Heupel MR, Munday PL (2014) A product of its environment: the epaulette shark (Hemiscyllium ocellatum) exhibits physiological tolerance to elevated environmental CO2. Conservation Physiology 2(1):cou047–cou047

  • Heinrich DDU, Watson S-A, Rummer JL, Brandl SJ, Simpfendorfer CA, Heupel MR, Munday PL (2016) Foraging behaviour of the epaulette shark Hemiscyllium ocellatum is not affected by elevated CO2. ICES J Mar Sci: J Conseil 73(3):633–640

  • Heuer RM, Grosell M (2014) Physiological impacts of elevated carbon dioxide and ocean acidification on fish. Am J Physiol—Regul Integr Comp Physiol 307:R1061–R1084

    Article  PubMed  CAS  Google Scholar 

  • Hoeijmakers JHJ (2009) DNA damage, aging and cancer. N Engl J Med 361(15):1475–1485

    Article  PubMed  CAS  Google Scholar 

  • Hofmann GE, Barry JP, Edmunds PJ, Gates RD, Hutchins DA, Klinger T, Sewell MA (2010) The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism-to-ecosystem perspective. Annu Rev Ecol Evol Syst 41:127–147

    Article  Google Scholar 

  • Hu M, Li L, Sui Y, Li J, Wang Y, Lu W, Dupont S (2015) Effect of pH and temperature on antioxidant responses of the thick shell mussel Mytilus coruscus. Fish Shellfish Immunol 46:573–583

    Article  PubMed  CAS  Google Scholar 

  • Johansson LH, Borg LA (1988) A spectrophotometric method for determination of catalase activity in small tissue samples. Anal Biochem 174(1):331–336

    Article  PubMed  CAS  Google Scholar 

  • Kambayashi Y, Binh NT, Asakura HW, Hibino Y, Hitomi Y, Nakamura H, Ogino K (2009) Efficient assay for total antioxidant capacity in human plasma using a 96-well microplate. J Clin Biochem Nutr 44:46–51

    Article  PubMed  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  PubMed  Google Scholar 

  • Kumar R (2009) Role of naturally occurring osmolytes in protein folding and stability. Arch Biochem Biophys 49:1–6. https://doi.org/10.1016/j.abb.2009.09.007

    Article  CAS  Google Scholar 

  • Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71:952–958

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lewis E, Wallace DWR (1998) CO2SYS-Program developed for the CO2 system calculations. Report ORNL/CDIAC-105

  • López-Cruz RI, Dafre AL, Filho DW (2012) Oxidative stress in sharks and rays. In: D Abele Vázquez-Medina JP, Zenteno-Savín T (eds) Oxidative stress in aquatic ecosystems. Wiley-Blackwell, Oxford, pp 157–163

    Google Scholar 

  • Lund R, Grogan ED (2004) The origin and relationships of early Chondrichthyes. In: Musick JA, Carrier JC, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press Inc, Boca Raton, pp 3–31

    Chapter  Google Scholar 

  • Lüthi D, Le Floch M, Bereiter B, Blunier T, Barnola J-M (2008) High-resolution carbon dioxide concentration record 650,000-800,000 years before present. Nature 453:379–382

    Article  PubMed  CAS  Google Scholar 

  • MacLellan RJ, Tunnah L, Barnett D, Wright PA, MacCormack T, Currie S (2015) Chaperone roles for TMAO and HSP70 during hyposmotic stress in the spiny dogfish shark (Squalus acanthias). J Comp Physiol B 185:729–740

    Article  PubMed  CAS  Google Scholar 

  • Maclouf J, Grassi J, Pradelles P (1987) Development of enzyme-immunoassay techniques for measurement of eicosanoids. In: Walden TL, Hughes HN (eds) Prostaglandin and lipid metabolism in radiation injury. Springer, New York, pp 355–364

    Chapter  Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055

    PubMed  CAS  Google Scholar 

  • Mehrbach C, Culberson C, Hawley J, Pytkowicz R (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    Article  CAS  Google Scholar 

  • Morrison J (1954) The activation of aconitase by ferrous ions and reducing agents. Biochem J 58:685–692

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nagelkerken I, Munday PL (2015) Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community-level responses. Glob Chang Biol 22:974–989

    Article  PubMed  Google Scholar 

  • Njemini R, Lambert M, Demanet C, Mets T (2005) Heat shock protein 32 in human peripheral blood mononuclear cells: effect of aging and inflammation. J Clin Immunol 25:405–417

    Article  PubMed  CAS  Google Scholar 

  • NOAA (2017) Trends in atmospheric carbon dioxide. Global Greenhouse Gas Reference Network

  • Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G-K, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M-F, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686

    Article  PubMed  CAS  Google Scholar 

  • Pamplona R, Constantini D (2011) Molecular and structural antioxidant defenses against oxidative stress in animals. Am J Physiol Regul Integr Comp Physiol 301:R843–R863

    Article  PubMed  CAS  Google Scholar 

  • Pimentel M, Pegado MR, Repolho T, Rosa R (2014) Impact of ocean acidification in the metabolism and swimming behavior of the dolphinfish (Coryphaena hippurus) early larvae. Mar Biol 161:725–729

    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  PubMed  PubMed Central  CAS  Google Scholar 

  • Pistevos JC, Nagelkerken I, Rossi T, Olmos M, Connell SD (2015) Ocean acidification and global warming impair shark hunting behaviour and growth. Sci Rep 5:16293

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pörtner H-O, Karl DM, Cheung WWL, Lluch-Cota SE, Nojiri Y, Schmidt DN, Zavialov PO (2014) Ocean systems. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD (eds) Climate change 2014: impacts, adaptation and vulnerabilities. part A: global and sectorial aspects contribution of working group II to the fifth assessement report of the intergovernmental panel on climate change. Cambridge, United Kingdom and New York, USA, pp 411–484

    Google Scholar 

  • Ridgwell A, Zeebe RE (2005) The role of the global carbonate cycle in the regulation and evolution of the earth system. Earth Planet Sci Lett 234:299–315

    Article  CAS  Google Scholar 

  • Rosa R, Baptista M, Lopes VM, Pegado MR, Paula JR, Trübenbach K, Leal MC, Calado R, Repolho T (2014) Early-life exposure to climate change impairs tropical shark survival. Proc R Soc Lond B Biol Sci 281:20141738

    Article  Google Scholar 

  • Rosa R, Paula JR, Sampaio E, Pimentel M, Lopes AR, Baptista M, Guerreiro M, Santos C, Campos D, Almeida-Val VMF, Calado C, Diniz M, Repolho T (2016a) Neuro-oxidative damage and aerobic potential loss of sharks under elevated CO2. Mar Biol 163:119

    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 C, Repolho T (2016b) Deficit in digestive capabilities of bamboo shark early stages under climate change. Mar Biol 163:1–5

    Article  CAS  Google Scholar 

  • Rosa R, Rummer JL, Munday PL (2017) Biological responses of sharks to ocean acidification. Biol Lett 13:20160796

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rudneva II (1997) Blood antioxidant system of black sea elasmobranch and teleosts. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 118:255–260

    Article  Google Scholar 

  • Rudneva II (1999) Antioxidant system of Black Sea animals in early development. Comp Biochem Physiol C Toxicol Pharmacol 122:265–271

    CAS  Google Scholar 

  • Rudneva II, Dorokhova II, Skuratovskaya EN, Kuz'minova NS (2014) Comparative studies of hepatic and blood biomarkers in three species of black sea elasmobranchs. Int J Mar Sci 4:1–14

    Google Scholar 

  • Rummer JL, Munday PL (2016) Climate change and the evolution of reef fishes: past and future. Fish Fish 18:22–39

    Article  Google Scholar 

  • Sampaio E, Lopes AR, Francisco S, Paula JR, Pimentel M, Maulvault AL, Repolho T, Grilo TF, Pousão-Ferreira P, Marques A, Rosa R (2018) Ocean acidification dampens physiological stress response to warming and contamination in a commercially-important fish (Argyrosomus regius). Sci Total Environ 618:388–398

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sejersted Y, Aasland AL, Bjørås M, Eide L, Saugstad OD (2009) Accumulation of 8-oxoguanine in liver DNA during hyperoxic resuscitation of newborn mice. Pediatr Res 66(5):533–538

    Article  PubMed  CAS  Google Scholar 

  • Shen J, Deininger P, Hunt JD, Zhao H (2007) 8-hydroxy-2′-deoxyguanosine (8-OH-dG) as a potential survival biomarker in patients with nonsmall-cell lung cancer. Cancer 109:574–580

    Article  PubMed  CAS  Google Scholar 

  • Silva CSE, Novais SC, Lemos MFL, Mendes S, Oliveira AP, Gonçalves EJ, Faria AM (2016) Effects of ocean acidification on the swimming ability, development and biochemical responses of sand smelt larvae. Sci Total Environ 563-564:89–98

    Article  PubMed  CAS  Google Scholar 

  • Solé M, Rodríguez S, Papiol V, Maynou F, Cartes JE (2009) Xenobiotic metabolism markers in marine fish with different trophic strategies and their relationship to ecological variables. Comparative Biochemistry and Physiology, Part C 149:83–89

    Google Scholar 

  • Sswat M, Stiasny MH, Jutfelt F, Riebesell U, Clemmesen C (2018) Growth performance and survival of larval Atlantic herring, under the combined effects of elevated temperatures and CO2. PLoS One 13(1):e0191947

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stiasny MH, Mittermayer FH, Sswat M, Voss R, Jutfelt F, Chierici M, Puvanendran V, Mortensen A, Reusch TBH, Clemmesen C (2016) Ocean acidification effects on Atlantic cod larval survival and recruitment to the fished population. PLoS One 11:e0155448

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stohs S, Bagchi D (1995) Mechanisms in the toxicity of metal ions. Free Radic Biol Med 18(2):321–336

    Article  PubMed  CAS  Google Scholar 

  • Sunday JM, Calosi P, Dupont S, Munday PL, Stillman JH, Reusch TBH (2014) Evolution in an acidifying ocean. Trends Ecol Evol 29:117–125

    Article  PubMed  Google Scholar 

  • Tomanek L (2010) Variation in the heat shock response and its implication for predicting the effect of global climate change on species’ biogeographical distribution ranges and metabolic costs. J Exp Biol 213:971–979

    Article  PubMed  CAS  Google Scholar 

  • Tomanek L, Zuzow MJ, Ivanina AV, Beniash E, Sokolova IM (2011) Proteomic response to elevated P CO2 level in eastern oysters, Crassostrea virginica: evidence for oxidative stress. J Exp Biol 214:1836–1844

    Article  PubMed  CAS  Google Scholar 

  • Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271–278

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Wu L, Aouffen M, Mateescu M-A, Nadeau R, Wang R (1999) Novel cardiac protective effects of urea: from shark to rat. Br J Pharmacol 128:1477–1484

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wittmann AC, Pörtner H-O (2013) Sensitivities of extant animal taxa to ocean acidification. Nat Clim Chang 3:995–1001

    Article  CAS  Google Scholar 

  • Wood CM, Liew HJ, Boeck GD, Walsh PJ (2013) A perfusion study of the handling of urea analogues by the gills of the dogfish shark (Squalus acanthias). PeerJ 1:e33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zeebe RE, Ridgwell A (2011) Past changes in ocean carbonate chemistry. In: Gattuso J-P, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, New York, pp 21–37

    Google Scholar 

Download references

Acknowledgments

We would like to thank Eduarda Pinto for the fundamental technical support during the preparation of the experimental setup and shark acclimation.

Funding

The Portuguese Foundation for Science and Technology (FCT) supported this work through the project grant PTDC/AAG-GLO/1926/2014 and Programa Investigador FCT 2013 to R.R. FCT also supported this work through (i) the strategic project UID/MAR/04292/2013 granted to MARE and (ii) PhD grants to ARL (SFRH/BD/97070/2013), ES (SFRH/BD/131771/2017), CS (SFRH/BD/117890/2016), and MRP (SFRH/BD/111691/2015). Both PLM and JLR are supported by funding from the Australian Research Council (ARC) Centre of Excellence for Coral Reef Studies.

Author information

Authors and Affiliations

  1. MARE - Marine and Environmental Sciences Centre, Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa, Avenida Nossa Senhora do Cabo 939, 2750-374, Cascais, Portugal

    Ana Rita Lopes, Eduardo Sampaio, Catarina Santos, Ana Couto, Maria Rita Pegado & Rui Rosa

  2. UCIBIO, REQUIMTE, Departamento de Química, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Quinta da Torre, 2829-516, Caparica, Portugal

    Ana Rita Lopes & Mário Diniz

  3. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, 4811, Australia

    Philip L. Munday & Jodie L. Rummer

Authors
  1. Ana Rita Lopes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eduardo Sampaio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catarina Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ana Couto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Rita Pegado
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mário Diniz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Philip L. Munday
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jodie L. Rummer
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rui Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ana Rita Lopes.

Ethics declarations

Competing of interests

The authors declare that they have no conflicts of interest.

Electronic supplementary material

ESM 1

(DOCX 13.6 kb)

ESM 2

(DOCX 14.2 kb)

ESM 3

(DOCX 15.1 kb)

ESM 4

(DOCX 13.7 kb)

ESM 5

(DOCX 14.1 kb)

ESM 6

(DOCX 15.3 kb)

ESM 7

(DOCX 13.8 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lopes, A.R., Sampaio, E., Santos, C. et al. Absence of cellular damage in tropical newly hatched sharks (Chiloscyllium plagiosum) under ocean acidification conditions. Cell Stress and Chaperones 23, 837–846 (2018). https://doi.org/10.1007/s12192-018-0892-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12192-018-0892-3

Keywords

Search

Navigation