Skip to main content
Log in

Impact of Waterborne Copper on the Structure of Gills and Hepatopancreas and Its Impact on the Content of Metallothionein in Juvenile Giant Freshwater Prawn Macrobrachium rosenbergii (Crustacea: Decapoda)

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

An Erratum to this article was published on 17 March 2009

Abstract

This study aims to elucidate both the impact of copper on the structure of the gills and hepatopancreas and the induction of metallothionein (MT) during waterborne copper exposure in juvenile Macrobrachium rosenbergii. Structural observations were performed with light microscopy, and the MT titrations were performed with the cadmium saturation assay. The structural changes that occurred in the gills and hepatopancreas appeared to result from copper accumulation, and the degree of damage observed in both tissues was relevant to the elevated waterborne copper concentration. Exposure to copper concentrations ranging from 0.01 mg/L to 0.4 mg/L for 7 days resulted in profound structural changes including the accumulation of hemocytes in the hemocoelic space; swelling and fusion of the lamellae; abnormal gill tips; and hyperplastic, necrotic, and clavate–globate lamellae in the gills. Similarly, hemocytic infiltration in the interstitial sinuses, an increased number of hemocytes, thickening and ruptures of the basal laminae, and necrosis of the tubules were observed in the hepatopancreas. The MT measurements showed no significant differences in MT contents between the control group and the group treated with 0.01 mg/L waterborne copper. The maximum MT content was observed at the level of 0.4 mg/L waterborne copper.

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.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

References

  • Ahsanullah M, Ying W (1995) Toxic effect of dissolved copper on Penaeus merguiensis and Penaeus monodon. Bull Environ Contam Toxicol 55:81–88

    Article  CAS  Google Scholar 

  • Bambang Y, Thuet P, Daures CM, Trilles JP (1995) Effect of copper on survival and osmoregulation of various developmental stages of the shrimp Penaeus japonicus Bate (Crustacea, Decapoda). Aquat Toxicol 33:125–139

    Article  CAS  Google Scholar 

  • Baticados MCL, Coloso RM, Duremdez RC (1987) Histopathology of the chronic soft shell syndrome in tiger prawn, Penaeus monodon. Aquat Org 3:13–28

    Google Scholar 

  • Baticados MCL, Tendencia EA (1991) Effect of gusathion A on the survival and shell quality of juvenile Penaeus monodon. Aquaculture 93:9–19

    Article  CAS  Google Scholar 

  • Battistella S, Bonivento P, Amirante GA (1996) Hemocytes and immunological reactions in crustaceans. Ital J Zool 63:337–343

    Google Scholar 

  • Bautista MN, Lavilla-Pitogo CR, Subosa PF (1994) Aflatoxin B1 contamination of shrimp feeds and its effect on growth and hepatopancreas of pre-adult Penaeus monodon. J Sci Food Agric 65:5–11

    Article  CAS  Google Scholar 

  • Bjerregaard P (1990) Influence of physiological condition on cadmium transport from haemolymph to hepatopancreas in Carcinus maenas. Mar Biol 106:199–209

    Article  CAS  Google Scholar 

  • Bjerregaard P, Vislie T (1985) Effects of cadmium on hemolymph composition in the shore crab Carcinus maenas (L.). Mar Ecol Prog Ser 27:135–142

    CAS  Google Scholar 

  • Boitel F, Truchot JP (1989) Effects of sublethal and lethal copper levels on hemolymph acid–base balance and ion concentrations in the shore crab Carcinus maenas kept in undiluted sea water. Mar Biol 103:495–501

    Article  CAS  Google Scholar 

  • Boyd CE (1990) Water quality in ponds for aquaculture. Birmington Publishing, Birmington, Alabama, pp 112–125

    Google Scholar 

  • Brouwer M, Whaling P, Engel DW (1986) Copper-metallothionein in the American lobster Homarus americanus: potential role as Cu (І) donors to apohemocyanin. Environ Health Perspectives 65:93–100

    CAS  Google Scholar 

  • Brouwer M, Winge DR, Gray WR (1989) Structural and functional diversity of copper-metallothioneins from the American lobster Homarus americanus. J Inorgan Biochem 35:289–303

    Article  CAS  Google Scholar 

  • Brouwer M, Schlenk D, Ringwood AH, Brouwer-Hoexum TM (1992) Metal-specific induction of metallothionein isoforms in the blue crab, Callinectes sapidus, in response to single and mixed-metal exposure. Arch Biochem Biophys 294:461–468

    Article  CAS  Google Scholar 

  • Brouwer M, Enghild J, Hoexum-Brouwer TM, Thogersen I, Truncali A (1995) Primary structure and tissue-specific expression of blue crab (Callinectes sapidus) metallothionein isoforms. J Biochem 311:617–622

    CAS  Google Scholar 

  • Brouwer M, Syring R, Brouwer TH (2002) Role of a copper-specific metallothionein of the blue crab, Callinectes sapidus, in copper metabolism associated with degradation and synthesis of hemocyanin. J Inorgan Biochem 88:228–239

    Article  CAS  Google Scholar 

  • Bubel A (1976) Histological and electron microscopical observations on the effects of different salinities and heavy metal ions on the gills of Jeara nordmanni (Rathke) (Crustacea, Isopoda). Cell Tissue Res 167:65–95

    Article  CAS  Google Scholar 

  • Buikema AL, Niedertehner PR, Cairns J (1982) Biological monitoring: part IV toxicity testing. Water Res 16: 239–262

    Article  CAS  Google Scholar 

  • Chen CY, Gregory AW, Bowser PR (2004) Comparative blood chemistry and histopathology of tilapia infected with Vibrio vulnificus or Streptococcus iniae or exposed to carbon tetrachloride, gentamicin, or copper sulfate. Aquaculture 239:421–443

    Article  CAS  Google Scholar 

  • Chen JC, Lin CH (2001) Toxicity of copper sulfate for survival, growth, molting and feeding of juveniles of the tiger shrimp, Penaeus monodon. Aquaculture 192:55–65

    Article  CAS  Google Scholar 

  • Couillard Y, Campbell PGC, Tessier A, Pellerinmassicotte J, Auclair A (1995) Field transplantation of a fresh-water bivalve Pyganodon grandis, across a metal contamination gradient. Temporal changes in metallothionein and metal (Cd, Cu and Zn) concentrations in soft tissues. Can J Fish Aquat Sci 52:690–702

    Article  CAS  Google Scholar 

  • Daly HR, Campbell IC, Hart BT (1990) Copper toxicity to Paratya australiensis I. Influence of nitriloacetic acid and glycine. Environ Toxicol Chem 9:997–1006

    CAS  Google Scholar 

  • Del Ramo J, Martinez M, Pastor A, Torreblanca A, Diaz-Mayans J (1993) Effect of cadmium pre-exposure in cadmium accumulation by brine shrimp Artemia. Involvement of low-molecular-weight cadmium-binding ligands. Mar Environ Res 35:29–33

    Article  Google Scholar 

  • Drach P, Tchernigovtzeff C (1967) Sur la méthode de détermination des stades d’intermue et son application général aux crustacés. Vie Milieu 18A:595–610

    Google Scholar 

  • Engel DW, Brouwer M (1986) Cadmium and copper metallothioneins in the American lobster, Homarus amiricanus. Environ Health Perspective 65:87–92

    CAS  Google Scholar 

  • Engel DW, Brouwer M (1987) Metal regulation and moulting in the blue crab, Callinectes sapidus; Metallothoinein function in metal metabolism. Biol Bull 173:239–251

    Google Scholar 

  • Ghate HV, Mulherkar L (1979) Histological changes in the gills of two freshwater prawn species exposed to copper sulphate. Indian J Exp Biol 17:838–840

    CAS  Google Scholar 

  • Guo JJ, Liao IC (1992) Toxicity of copper sulfate to juvenile grass prawn, Penaeus monodon. COA Fish Ser 33:1–7

    Google Scholar 

  • Gurr E (1962) Staining animal tissues, practical and theoretical. Leonard Hill, London, pp 45–52

    Google Scholar 

  • Hinton DE, Kemdall MW, Silver BB (1973) Biological methods for the assessment of water quality. ASTM STP 528, USA, 194 pp

  • Hogstrand C, Haux C (1990) Metallothionein as an indicator of heavy–metal exposure in two subtropical fish species. J Exp Mar Biol Ecol 138:69–84

    Article  CAS  Google Scholar 

  • Jiravanichpaisal P, Miyazaki T (1994) Histopathology, biochemistry and pathogenicity of Vibrio harveyi infecting black tiger prawn Penaeus monodon. J Aquat Anim Health 6:27–35

    Article  Google Scholar 

  • Kagi JHR, Kojima Y (1987) Chemistry and biochemistry of metallothionein. In: Kagi JHR, Kojima Y (eds) Metallothionein II. Birkhauser, Boston, pp 25–61

    Google Scholar 

  • Kaliamurthy J, Bhavan PS, Geraldine P (1994) Alterations in the protein profile and microstructure of gills and hepatopancreas in the prawn, Macrobrachium lamarrei following exposure to hospital wastes. Proceedings of the International Conference on Agrotechnology in the Commonwealth Focus for the 21st Century, Singapore National University, Singapore, pp 121–124

  • Karin M (1985) Metallothioneins: proteins in search of function. Cell 41:9–10

    Article  CAS  Google Scholar 

  • Li N, Zhao YL, Yang J (2005) Accumulation, distribution, and toxicology of copper sulfate in juvenile giant freshwater prawns, Macrobrachium rosenbergii. Bull Environ Contam Toxicol 75:497–504

    Article  CAS  Google Scholar 

  • Lightner DV, Redman RM, Price RL, Wiseman MO (1982) Histopathology of aflatoxicosis in the marine shrimp Penaeus stylirostris and Penaeus vannamei. J Invert Pathol 40:279–291

    Article  CAS  Google Scholar 

  • Lightner DV, Hasson KW, White BL, Redman RM (1996) Chronic toxicity and histopathological studies with Benlate, a commercial grade of benomyl in Penaeus vannamei (Crustacea: Decapoda). Aquat Toxicol 34:105–118

    Article  CAS  Google Scholar 

  • Lin F, Ren HW, Ru BG (2001) Studies of relationship between metallothionein and aquatic environment in fishes. J Beijing University (Natural Sciences) 37:779–784

    CAS  Google Scholar 

  • Liu FY, Liang DH, Sun F, Li HF, Lan X (1990) Effects of dietary copper on the prawn Penaeus orientalis. Oceanol Limnol Sin 21:404–410

    Google Scholar 

  • Liu FY, Wu YL, Zhao HR, Hou LY, Sun F (1988) Accumulation and toxicity of copper in prawn Penaeus orientalis. Oceanol Limnol Sin 19:133–138

    CAS  Google Scholar 

  • Liu XM, Sun ZW, Shi L, Qiu BY, Li CY, Wang ZW (2000) Study on hepatic metallothionein of mice injected with zinc. Chinese Commonality Sanitation 16:315–316

    CAS  Google Scholar 

  • Lundebye AK, Depledge MH (1998) Molecular and physiological responses in shore crabs Carcinus maenas following exposure to copper. Mar Environ Res 46:567–572

    Article  CAS  Google Scholar 

  • Mallatt J (1985) Fish gill structural changes induced by toxicants and their irritants: a statistical review. Can J Fish Aquat Sci 42:630–648

    Article  CAS  Google Scholar 

  • Martınez M, Del Ramo J, Torreblanca A, Pastor A, Dıaz-Mayans J (1996) Cadmium toxicity, accumulation and metallothionein induction in Echinogammarus echinosetosus. J Environ Sci Health 317:1605–1617

    Google Scholar 

  • Mazon AF, Nolan DT, Lock RAC, Fernandes MN, Wendelaar Bonga SE (2004) A short-term in vitro gill culture system to study the effects of toxic (copper) and non-toxic (cortisol) stressors on the rainbow trout, Oncorhynchus mykiss (Walbaum). Toxicol In Vitro 18:691–701

    Article  CAS  Google Scholar 

  • Méndez L, Racotta IS, Acosta B, Rodríguez-Jaramillo C (2001) Mineral concentrations in tissue during ovarian development of white shrimp Penaeus vannamei (Decapoda: Penaeidae). Mar Biol 138:687–692

    Article  Google Scholar 

  • Moksnes PO, Lindahl U, Haux C (1995) Metallothionein as a biodicator of heavy metal exposure in the tropical shrimp Penaeus vannamei: a study of dose-dependent indication. Mar Environ 39:143–146

    Article  CAS  Google Scholar 

  • Olafson RW, Kearns A, Sim RG (1979) Heavy metal induction of metallothionein synthesis in the hepatopancreas of the crab Scylla Serrata. Comp Biochem Physiol 62B:417–424

    CAS  Google Scholar 

  • Overnell J, McIntosh R, Fletcher TC (1987) The levels of liver metallothionein and zinc in plaice, Pleuronectes platessa L., during breeding season, and effects of oestradiol injection. J Fish Biol 30:539–546

    Article  CAS  Google Scholar 

  • Rabin H (1970) Hemocytes, hemolymph, and defense-reactions in crustaceans. J Reticuloendothel Soc 7:195–207

    CAS  Google Scholar 

  • Roesijadi G (1992) Metallothioneins in metal regulation and toxicity in aquatic animals. Aquat Toxicol 22:81–114

    Article  CAS  Google Scholar 

  • Saravana Bhavan P, Geraldine P (2000) Histopathology of the hepatopancreas and gills of the prawn Macrobrachium malcolmsonii exposed to endosulfan. Aquat Toxicol 50:331–339

    Article  CAS  Google Scholar 

  • Sung H, Kao W, Su Y (2003) Effects and toxicity of phthalate esters to hemocytes of giant freshwater prawn, Macrobrachium rosenbergii. Aquat Toxicol 64:25–37

    Article  CAS  Google Scholar 

  • Tamse CT, Gacutan RG, Tamse AF (1995) Changes induced in the gills of Milkfish (Chanos chanos Forsskal) fingerlings after acute exposure to Nifurprinol (Furanace; P-7138). Bull Environ Contam Toxicol 54:591–596

    Article  CAS  Google Scholar 

  • Tsing A, Arcier JM, Brehelin M (1989) Hemocytes of penaeid and palaemonid shrimps: morphology, cytochemistry, and hemograms. J Invertebr Pathol 53:64–77

    Article  Google Scholar 

  • Van Heerder D, Andr V, Mikko N (2004) Effects of short-term copper exposure on gill structure, metallothionein and hypoxia-inducible factor-1 small alpha, Greek (HIF-1 small alpha, Greek) levels in rainbow trout (Oncorhynchus mykiss) Aquat Toxicol 69:271–280

    Article  CAS  Google Scholar 

  • Victor B, Narayanan M, Nelson DJ (1990) Gills pathology and hemocyte response in mercury exposed Macrobrachium idae (Heller). J Environ Biol 11:61–65

    CAS  Google Scholar 

  • Vijayaraman K (1993) Physiological responses on the freshwater prawn, Macrobrachium malcolmsonii (Milne Edwards) to the heavy metals, cadmium, copper, chromium and Zinc. Ph.D. thesis. Bharathidasan University, Tiruchirappalli, India

  • Vogt G (1987) Monitoring of environmental pollutants such as pesticides in prawn aquaculture by histopathological diagnosis. Aquaculture 67:157–164

    Article  Google Scholar 

  • Vogt G (1990) Pathology of midgut gland-cells of Penaeus monodon post-larvae after Leucaena leucocephala feeding. Aquat Org 9:45–61

    Google Scholar 

  • Vosloo A, van Aardt WJ, Mienie LJ (2002) Sublethal effects of copper on the freshwater crab Potamonautes warreni. Comp Biochem Physiol 133A:695–702

    CAS  Google Scholar 

  • White SL, Rainbow PS (1986) Regulation and accumulation of cadmium by Palaemon elegants (Crustacea: Decapoda). Comp Biochem Physiol 83C:111–116

    CAS  Google Scholar 

  • Yamuna A, Kabila V, Geraldine P (1996) Biochemical and histological alterations in the prawn Macrobrachium lamarrei following exposure to automobile discharge. Geo J 40:233–237

    Google Scholar 

Download references

Acknowledgments

This work was supported by the Ministry of Personnel (Scientific Research Foundation of for Returned Overseas Chinese Scholars, 2004, Project No. 2-105053), and the Chinese Academy of Fishery Sciences for Chief Scientists (Project No. 1-105011).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jian Yang.

Additional information

An erratum to this article is available at http://dx.doi.org/10.1007/s00244-009-9306-y.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, N., Zhao, Y. & Yang, J. Impact of Waterborne Copper on the Structure of Gills and Hepatopancreas and Its Impact on the Content of Metallothionein in Juvenile Giant Freshwater Prawn Macrobrachium rosenbergii (Crustacea: Decapoda). Arch Environ Contam Toxicol 52, 73–79 (2007). https://doi.org/10.1007/s00244-005-0214-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-005-0214-5

Keywords

Navigation