Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Effects of Tin on Enzyme Activity in Holothuria grisea (Echinodermata: Holothuroidea)


This study evaluated the effect of tin exposure on enzyme activity in the sea cucumber (Holothuria grisea Selenka, 1867). After exposure to 0 (control), 0.04, 0.08, or 0.12 mg L−1 tin, we tested the activities of total cholinesterase in longitudinal muscles, acid phosphatase in gonads and the respiratory tree, as well as alkaline phosphatase in the intestines during a 96-h bioassay. Regression analyses showed that all enzyme activities declined with increasing tin concentrations, except for acid phosphatase in the respiratory tree, which were similarly, inhibited at all tin concentrations. These results indicate that H. grisea is a potential bioindicator for seascape habitat monitoring programs, as its biochemical markers show sensitivity to trace elements that can indicate a rise in pollution levels.

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

Fig. 1


  1. Alves C, Arruti R (2009) Hiperfosfatasemia transitória benigna da infância. Acta Orto Bras. doi:10.1590/S1413-78522009000100011

  2. Atli G, Canli M (2007) Enzymatic responses to metal exposures in a freshwater fish Oreochromis niloticus. Comp Biochem Physiol C Toxicol Pharmacol 145:282–287

  3. Barrett AJ (1972) Lysosomal enzymes. In: Dingle JT (ed) Lysosomes: a laboratory handbook. North-Holland, Amsterdam, pp 46–135

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

  5. Benali I, Boutiba Z, Merabet A, Chévre N (2015) Integrated use of biomarkers and condition indices in mussels (Mytilus galloprovincialis) for monitoring pollution and development of biomarker index to assess the potential toxic of coastal sites. Mar Pollut Bull 95:385–394

  6. Bocquené G, Galgani F, Truquet P (1990) Characterization and assay conditions for use of ACHe activity from several marine species in pollution monitoring. Mar Environ Res 30:75–89

  7. Bonacci S, Corsi I, Focardi S (2009) Cholinesterases in the Antarctic scallop Adamussium colbecki: characterization and sensitivity to pollutants. Ecotoxicol Environ Saf 72:1481–1488

  8. Cajaraville MP, Bebianno MJ, Blasco J, Porte C, Sarasquete C, Viarengo A (2000) The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Sci Total Environ 247:295–311

  9. Chan KM, Cheung SG, Cai Z, Qiu J (2008) Sensitivity of different biological responses to accumulation and depuration of butylins in the neogastropod Thais clavigera: implications for biomonitoring. Ecotoxicology 17:860–868

  10. Chandran R, Sivakumar AA, Mohandass S, Aruchami M (2005) Effect of cadmium and zinc on antioxidant enzyme activity in the gastropod, Achatina fulica. Comp Biochem Physiol C Toxicol Pharmacol 140:422–426

  11. CONAMA (2005) Conselho Nacional do Meio Ambiente, Resolução N° 357, de 17 de março de 2015, Brazil

  12. Filgueiras CAI (2002) Tin chemistry in the 18th century, or how an inquiry became a research project. Quím nova 25:1211–1219

  13. Gill TS, Tewari H, Pande J (1990) Use of the fish enzyme system in monitoring water quality: effects of mercury on tissue enzymes. Comp Biochem Physiol C Toxicol Pharmacol 97:287–292

  14. Guardiola FA, Dioguardi M, Parisi MG, Trapani MR, Meseguer J, Cuesta A, Cammarata M, Esteban MA (2015) Evaluation of waterborne exposure to heavy metals in innate immune defences present on skin mucus of gilthead seabream (Sparus aurata). Fish Shellfish Immunol 45:112–123

  15. Guilhermino L, Lopes MC, Carvalho AP, Soares AM (1996) Inhibition of acetylcholinesterase activity as effect criterion in acute tests with juvenile Daphnia magna. Chemosphere 32:727–738

  16. Jamet D, Aleya L, Devaux J (1995) Diel changes in the alkaline phosphatase activity of bacteria and phytoplankton in the hypereutrophic Villerest reservoir (Roanne, France). Hydrobiologia 300:49–56

  17. Jing G, Li Y, Xie L, Zhang R (2006) Metal accumulation and enzyme activities in gills and digestive gland of pearl oyster (Pinctada fucata) exposed to copper. Comp Biochem Physiol C Toxicol Pharmacol 144:184–190

  18. Kristoff G, Guerrero NV, de D’Angelo AM, Cochón AC (2006) Inhibition of cholinesterase activity by azinphos-methyl in two freshwater invertebrates: Biomphalaria glabrata and Lumbriculus variegatus. Toxicology 222:185–194

  19. Lowry OH, Rosembrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

  20. Mazorra MT, Rubio JA, Blasco J (2002) Acid and alkaline phosphatase activities in the clam Scrobicularia plana: kinetic characteristics and effects of heavy metals. Comp Biochem Physiol B Biochem Mol Biol 131:241–249

  21. Milatovic D, Dettbarn WD (1996) Modification of acetylcholinesterase during adaptation to chronic, subacute paraoxon application in rat. Toxicol Appl Pharmacol 136:20–28

  22. Nagaraja TN, Desiraju T (1994) Effects on operant learning and brain acetylcholine esterase activity in rats following chronic inorganic arsenic intake. Hum Exp Toxicol 13:353–356

  23. Napierska D, Barsiene J, Mulkiewicz E, Podolska M, Rybakovas A (2009) Biomarker responses in flounder Platichthys flesus from the Polish coastal area of the Baltic Sea and applications in biomonitoring. Ecotoxicology 18:846–859

  24. Oliva M, Perales JA, Gravato C, Guilhermino L, Galindo-Riaño MD (2012) Biomarkers responses in muscle of Senegal sole (Solea senegalensis) from a heavy metals and PAHs polluted estuary. Mar Pollut Bull 64:2097–2108

  25. Payne JF, Mathieu A, Melvin W, Fancey LL (1996) Acetylcholinesterase, an old bio-marker with a new future? Field trials in association with two urban rivers and a paper mill in Newfoundland. Mar Pollut Bull 32:225–231

  26. Pereira ER, Cogo AJD, Cruz ZMA (2014). Biomarcadores enzimáticos em Holothuria grisea (Selenka, 1867) expostas ao chumbo, cádmio e cobre. Nat On 12:1–9

  27. Pretto A, Loro VL, Morsch VM, Moraes BS, Menezes C, Clasen B, Hoehne L, Dressler V (2010) Acetylcholinesterase activity, lipid peroxidation, and bioaccumulation in silver catfish (Rhamdia quelen) exposed to cadmium. Arch Environ Contam Toxicol 58:1008–1014

  28. Quintaneiro C, Monteiro M, Pastorinho R, Soares AM, Nogueira AJ, Morgado F, Guilhermino L (2006) Environmental pollution and natural populations: a biomarkers case study from the Iberian Atlantic coast. Mar Pollut Bull 52:1406–1413

  29. Rabitto IS, Costa JRA, de Assis HCS, Pelletier EE, Akaishi FM, Anjos A, Randi MA, Ribeiro CAO (2005) Effects of dietary Pb (II) and tributyltin on neotropical fish, Hoplias malabaricus: histopathological and biochemical findings. Ecotoxicol Environ Saf 60:147–156

  30. Rajalakshmi S, Mohandas A (2005) Copper-induced changes in tissue enzyme activity in a freshwater mussel. Ecotoxicol Environ Saf 62:140–143

  31. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

  32. Regoli F, Nigro M, Orlando E (1998) Lysosomal and antioxidant responses to metals in the Antartic scallop Adamussium colbecki. Aquat Toxicol 40:375–392

  33. Reichardt W, Overbeck J, Steubing L (1967) Free dissolved enzymes in lake waters. Nature 216:1345–1347

  34. Richetti SK, Rosemberg DB, Ventura-Lima J, Monserrat JM, Bogo MR, Bonan CD (2011) Acetylcholinesterase activity and antioxidant capacity of zebrafish brain is altered by heavy metal exposure. Neurotoxicology 32:116–122

  35. Rodrigues SR, Caldeira C, Castro BB, Gonçalves F, Nunes B, Antunes SC (2011) Cholinesterase (ChE) inhibition in pumpkinseed (Lepomis gibbosus) as environmental biomarker: ChE characterization and potential neurotoxic effects of xenobiotics. Pestic Biochem Physiol 99:181–188

  36. Romani R, Antognelli C, Baldracchini F, De Santis A, Isani G, Giovannini E, Rosi G (2003) Increased acetylcholinesterase activities in specimens of Sparus auratus exposed to sublethal copper concentrations. Chem Biol Interact 145:321–329

  37. Sant’Anna BS, dos Santos DM, Sandron DC, de Souza SC, de Marchi MRR, Zara FJ, Turra A (2012) Hermit crabs as bioindicators of recent tributyltin (TBT) contamination. Ecol Indic 14:184–188

  38. Szabó A, Nemcsók J, Asztalos B, Rakonczay Z, Kása P, Hieu LH (1992) The effect of pesticides on carp (Cyprinus carpio L). Acetylcholinesterase and its biochemical characterization. Ecotoxicol Environ Saf 23:39–45

  39. Warnau M, Dutrieux S, Ledente G, Baena ALMR, Dúbois P (2006) Heavy metals in the sea cucumber Holothuria tubulosa (Echinodermata) from the Mediterraneam Posidonia oceanica ecosystem: body compartment, seasonal, geographical and bathymetric variations. Environ Bioind 1:268–285

  40. Woo S, Yum S, Park HS, Lee TK, Ryu JC (2009) Effects of heavy metals on antioxidants and stress-responsive gene expression in Javanese medaka (Oryzias javanicus). Comp Biochem Physiol C Toxicol Pharmacol 149:289–299

Download references


We thank FAPES (Fundação de Amparo à Pesquisa e Inovação do Espírito Santo) for its financial support. Capes (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) also provided a fellowship at UVV in the Programa de Graduação em Ecologia de Ecossistema. UVV and LabPeixe also provided logistical support, for which we are grateful.

Author information

Correspondence to Zilma Maria Almeida Cruz.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pereira, T.M., Mattar, L.P., Pereira, E.R. et al. Effects of Tin on Enzyme Activity in Holothuria grisea (Echinodermata: Holothuroidea). Bull Environ Contam Toxicol 98, 607–611 (2017).

Download citation


  • Marine pollution
  • Echinoderm
  • Biomarkers
  • Bioindicators
  • Enzyme activity