Environmental Science and Pollution Research

, Volume 26, Issue 6, pp 5577–5587 | Cite as

Ecotoxicological effects of trace element contamination in talitrid amphipod Orchestia montagui Audouin, 1826

  • Raja JelassiEmail author
  • Hajer Khemaissia
  • Chedliya Ghemari
  • Maryline Raimond
  • Catherine Souty-Grosset
  • Karima Nasri-Ammar
Research Article


This study deals with the evaluation of trace element bioaccumulation and histological alterations in the hepatopancreas of the supralittoral amphipod Orchestia montagui Audouin, 1826 due to the exposure to cadmium, copper, and zinc. Orchestia montagui individuals were maintained during 14 days in soils contaminated with different trace elements namely cadmium, copper, and zinc; a control was also prepared. Our results show that the mortality and the body mass vary according to the metal and the nominal concentration used. In general, the mortality increases from the seventh day. However, the body mass shows a decrease with cadmium exposure and an increase with copper and zinc exposures. Furthermore, the concentration factor highlights that this species is considered a macroconcentrator for copper and zinc. The hepatopancreas of unexposed and exposed animals were compared to detect histological changes. Our results show significant alterations in the hepatopancreas of the exposed animals after the experiment. The degree of these alterations was found to be dose-dependent. Among the histological changes in the hepatopancreas in O. montagui, a loss of cell structure was noted, especially cell remoteness and border lyses, the reduction of nuclear volume, an increase in the cytoplasm density with the presence of trace element deposits in both the nucleus and vacuoles, a disorganization and destruction of microvilli, and a condensation of the majority of cell organelles and mitochondria swelling. Through this study, we have confirmed that O. montagui can be a relevant model to assess trace metal element pollution in Tunisian coastal lagoons with the aim of using it in future biomonitoring programs.


Wetlands Crustaceans Microcosms Storage organ Cellular alterations 



The study was supported by the Erasmus Mundus Al Idrisi II Programme of the European Union for a stay at the University of Poitiers and the Research Unit of Bio-ecology and Evolutionary Systematics (UR11ES11), Faculty of Science of Tunis, University of Tunis El Manar. TEM observations were made in “Image UP” service at the University of Poitiers.

We wish to thank Mrs. Najwa Abdelkefi MSci. Astrophysics Translator/Interpreter for his constructive remarks and for revising the English of the manuscript.


  1. Ahsanullah M, Williams AR (1991) Sublethal effects and bioaccumulation of cadmium, chromium, copper and zinc in the marine amphipod Allorchestes compressa. Mar Biol 108:59–65CrossRefGoogle Scholar
  2. Ayari A, Raimond M, Souty-Grosset C, Nasri-Ammar K (2016) Hierarchical organization of the cuticle of the subsocial desert isopod, Hemilepistus reaumurii. J Struct Biol 193:115–123Google Scholar
  3. Bach L, Ferguson L, Feltelius V, Sondergaard J (2014) Orchomenella pinguis (amphipoda)—a possible species for heavy metal biomonitoring of marine sediments. J Coast Life Med 2:116–123Google Scholar
  4. Beyer WN, Pattee OH, Sileo L, Hoffman DJ, Mulhern BM (1985) Metal contamination in wildlife living near two zinc smelters. Environ Poll 38:63–86CrossRefGoogle Scholar
  5. Bessa F, Scapini F, Cabrini TMB, Cardoso RS (2017) Behavioural responses of talitrid amphipods to recreational pressures on oceanic tropical beaches with contrasting extension. J Exp Mar Biol Ecol 486:170–177CrossRefGoogle Scholar
  6. Cardoso RS, Barboza CAM, Skinner VB, Cabrini TMB (2016) Crustaceans as ecological indicators of sandy beaches health. Ecol Indic 62:154–162CrossRefGoogle Scholar
  7. Clifford B, Witkus ER (1971) The fine structure of the hepatopancreas of the woodlouse, Oniscus asellus. J Morphol 135:335–350CrossRefGoogle Scholar
  8. Collins P (2010) Environmental stress upon hepatopancreatic cells of freshwater prawns (Decapoda: Caridea) from the floodplain of Paraná River. Nat Sci 2(7):748–759Google Scholar
  9. Dallinger R (1993) Strategies of metal detoxification in terrestrial invertebrate. In: Dallinger RAR, Rainbow PS (eds) Ecotoxicology of metals in invertebrates. Lewis, Boca Raton, pp 245–290Google Scholar
  10. Drobne D, Hopkin SP (1995) The toxicity of zinc to terrestrial isopods in a “standard” laboratory test. Ecotoxicol Environ Saf 31:1–6CrossRefGoogle Scholar
  11. Donker MH (1992) Energy reserves and distribution of metals in populations of the isopod Porcellio scaber from metal-contaminated sites. Funct Ecol 6:445–454CrossRefGoogle Scholar
  12. Donker MH, Zonneveld C, Van Straalen N (1993) Early reproduction and increased reproductive allocation in metal-adapted populations of the terrestrial isopod Porcellio scaber. Oecologia 96:316–323CrossRefGoogle Scholar
  13. Enserink EL, Maas-Diepeveen JL, Van Leeuwen CJ (1991) Combined effects of metals; an ecotoxicological evaluation. Wat Res 25:679–687CrossRefGoogle Scholar
  14. Al-Fartusie FS, Mohssan SN (2017) Essential trace elements and their vital roles in human body. Indian J Adv Chem Sci 5(3):127–136Google Scholar
  15. Fialkowskia W, Rainbow PS, Smith BD, Zmudzinski L (2003) Seasonal variation in trace metal concentrations in three talitrid amphipods from the Gulf of Gdansk, Poland. J Exp Mar Biol Ecol 288:81–93CrossRefGoogle Scholar
  16. Fialkowski W, Calosi P, Dahlke S, Dietrich A, Moore PG, Olenin S, Persson LE, Smith BD, Špegys M, Rainbow PS (2009) The sandhopper Talitrus saltator (Crustacea: Amphipoda) as a biomonitor of trace metal bioavailabilities in European coastal waters. Mar Poll Bull 58:39–44Google Scholar
  17. Gál J, Markiewicz Patkowska J, Hursthouse A, Tatner P (2008) Metal uptake by woodlice in urban soils. Ecotoxicol Environ Saf 69:139–149CrossRefGoogle Scholar
  18. García-Hernández J, Hurtado LA, Leyva-García G, Güido-Moreno A, Aguilera-Márquez D, Mazzei V, Ferrante M (2015) Isopods of the genus Ligia as potential biomonitors of trace metals from the Gulf of California and pacific coast of the Baja California peninsula. Ecotoxicol Environ Saf 112:177–185CrossRefGoogle Scholar
  19. Ghadially FN (1988a) Ultrastructural pathology of the cell and matrix. Butterworths, LondonGoogle Scholar
  20. Ghadially FN (1988b) Ultrastructural pathology of the cell and matrix. Butterworths, LondonGoogle Scholar
  21. Ghemari C (2017) Ecophysiologie de la reproduction et écotoxicologie chez l'espèce Porcellio laevis (Crustacé, Isopode). Thèse de Doctorat, Université Tunis El Manar, 286 pp.Google Scholar
  22. Ghemari C, Waterlot C, Ayari A, Leclerq J, Douay F, Nasri-Ammar K (2017) Assessment of heavy metals in soil and terrestrial isopod Porcellio laevis in Tunisian industrialized areas. Environ Earth Sci 76(223).
  23. Godet JP, Demuynck S, Waterlot C, Lemière S, Souty-Grosset C, Scheifler R, Douay F, Leprêtre A, Pruvot C (2011) Growth and metal accumulation in Porcellio scaber exposed to poplar litter from Cd, Pb and Zn contaminated sites. Ecotoxicol Environ Saf 74:451–458CrossRefGoogle Scholar
  24. Gopinath R, Paul Raj R (2009) Histological alterations in the hepatopancreas of Penaeus monodon Fabricius (1798) given aflatoxin B1-incorporated diets. Aquac Res 40:1235–1242CrossRefGoogle Scholar
  25. Gräff S, Berkus M, Alberti G, Köhler HR (1997) Metal accumulation strategies in saprophagous and phytophagous soil invertebrates: a quantitative comparison. BioMetals 10:45–53CrossRefGoogle Scholar
  26. Hagner-Holler S, Schoen A, Erker W, Marden JH, Rupprecht R, Decker H, Burmester T (2004) A respiratory hemocyanin from an insect. Proc Natl Acad Sci U S A 101(3):871–874CrossRefGoogle Scholar
  27. Heikens A, Peijnenburg W, Hendriks AJ (2001) Bioaccumulation of heavy metals in terrestrial invertebrates. Environ Poll 113:385–393CrossRefGoogle Scholar
  28. Hopkin SP, Martin MH (1982) The distribution of zinc, cadmium, lead and copper within the woodlouse Oniscus asellus (Crustacea, Isopoda). Oecologia 54:227–232CrossRefGoogle Scholar
  29. Hopkin SP (1993) In situ biological monitoring of pollution in terrestrial and aquatic ecosystems. In: Calow P (ed) Handbook of ecotoxicology. Blackwell, Oxford, pp 397–427Google Scholar
  30. Hopkin SP, Martin MH (1985) Assimilation of zinc, cadmium, lead, copper, and iron by the spider Dysdera crocata, a predator of woodlice. Bull Environ Cont Toxicol 34:183–187CrossRefGoogle Scholar
  31. Hopkin SP, Hardisty GN, Martin MH (1986) The woodlouse Porcellio scaber as a biological indicator of zinc, cadmium, lead and copper pollution. Environ Poll 11(4):271–290CrossRefGoogle Scholar
  32. Icely JD, Nott JA (1980) Accumulation of copper within the “hepatopancreatic” caeca of Corophium volutator (Crustacea: Amphipoda). Mar Biol 57:193–1990CrossRefGoogle Scholar
  33. Jelassi R, Nasri-Ammar K (2013) Seasonal variation of locomotor activity rhythm of Orchestia montagui in the supralittoral zone of Bizerte lagoon (North of Tunisia). Biol Rhythm Res. 44:718–729Google Scholar
  34. Jelassi R, Khemaissia H, Nasri-Ammar K (2012) Intra-annual variation of the spatiotemporal distribution and abundance of Talitridae and Oniscidea (Crustacea, Peracarida) at Bizerte Lagoon (northern Tunisia). Afr J Ecol 50:381–392CrossRefGoogle Scholar
  35. Jelassi R, Khemaissia H, Zimmer M, Garbe-Schönberg D, Nasri-Ammar K (2015) Biodiversity of Talitridae family (Crustacea, Amphipoda) in some Tunisian coastal lagoons. Zool Stud 54(17).
  36. Jelassi R, Khemaissia H, Zimmer M, Garbe-Schönberg D, Nasri-Ammar K (2017a) Influence of environmental conditions on the distribution of Amphipoda, Talitridae, in the lagoon complex of Ghar El Melh (north-east of Tunisia). Afr J Ecol 55(4):451–464CrossRefGoogle Scholar
  37. Jelassi R, Bouslama MF, Khemaissia H, Nasri-Ammar K (2017b) Biology and population dynamics of three sympatric talitrid species (Crustacea: Amphipoda) from the supralittoral zone of Bizerte Lagoon, Northern Tunisia. Acta Zool Bulg 69(1):71–88Google Scholar
  38. Khemaissia H, Jelassi R, Souty-Grosset C, Nasri-Ammar K (2017) Terrestrial isopod diversity along three transects at the lagoon complex of Ichkeul (Tunisia) in relation to environmental conditions. Vie & Milieu 67(1):33–42Google Scholar
  39. Köhler HR, Hüttenrauch K, Berkus M, Gräff S, Alberti G (1996) Cellular hepatopancreatic reactions in Porcellio scaber (Isopoda) as biomarkers for the evaluation of heavy metal toxicity in soils. App Soil Ecol:1–15Google Scholar
  40. Legras S, Mouneyrac C, Amiard JC, Amiard-Triquet C, Rainbow PS (2000) Changes in metallothionein concentrations in response to variation in natural factors (salinity, sex, weight) and metal contamination in crabs from a metal-rich estuary. J Exp Mar Biol Ecol 246:259–279CrossRefGoogle Scholar
  41. Loizzi RF (1971) Interpretation of cray fish hepatopancreatic function based on fine structural analysis of epithelial cell liver and muscle network. Z Zellforsch mikrosk Anat 113:420–440CrossRefGoogle Scholar
  42. Longo G, Trovato M, Mazzei V, Ferrante M, Oliveri Conti G (2013) Ligia italica (Isopoda, Oniscidea) as bioindicator of mercury pollution of marine rocky coasts. PLoS One 8(3):e58548.
  43. Manisseri MK, Menon NR (1996) Copper induced damage to the hepatopancreas of the penaeid shrimp Metapenaeus dobson—an ultrastructural study. Dis Aquat Org 22:51–57CrossRefGoogle Scholar
  44. Marsden ID, Rainbow PS (2004) Does the accumulation of trace metals in crustaceans affect their ecology—the amphipod example? J Exp Mar Biol Ecol 300:373–408CrossRefGoogle Scholar
  45. Mazzei V, Longo G, Brundo MV, Copat C, Oliveri Conti G, Ferrante M (2013) Effects of heavy metal accumulation on some reproductive characters in Armadillidium granulatum Brandt (Crustacea, Isopoda, Oniscidea). Ecotoxicol Environ Saf 98:66–73CrossRefGoogle Scholar
  46. Mazzei V, Longo G, Brundo MV, Sinatra F, Copat C, Oliveri Conti G, Ferrante M (2014) Bioaccumulation of cadmium and lead and its effects on hepatopancreas morphology in three terrestrial isopod crustacean species. Ecotoxicol Environ Saf 110:269–279CrossRefGoogle Scholar
  47. Moore PG, Rainbow PS, Haynes E (1991) The beach-hopper Orchestia gammarellus (Crustacea: Amphipoda) as a biomonitor for copper and zinc: North Sea trials. Sci Total Environ 106:221–238CrossRefGoogle Scholar
  48. Mouneyrac C, Amiard JC, Amiard-Triquet C, Cottier A, Rainbow PS, Smith BD (2002) Partitioning of accumulated trace metals in the talitrid amphipod crustacean Orchestia gammarellus: a cautionary tale on the use of metallothionein-like proteins as biomarkers. Aquat Toxicol 57:225–242CrossRefGoogle Scholar
  49. Nassiri Y, Rainbow PS, Amiard-Triquet C, Rainglet F, Smith BD (2000) Trace metal detoxification in the ventral caeca of Orchestia gammarellus (Crustacea: Amphipoda). Mar Biol 136:477–484CrossRefGoogle Scholar
  50. Odendaal JP, Reinecke AJ (1999) The sublethal effects and accumulation of cadmium in the terrestrial isopod Porcellio laevis Latr. (Crustacea, Isopoda). Arch Environ Contam Toxicol 36:64–69CrossRefGoogle Scholar
  51. Phillips DJH, Rainbow PS (1994) Biomonitoring of trace aquatic contaminants. Chapman and Hall, LondonGoogle Scholar
  52. Rainbow PS (1985) Accumulation of Zn, Cu and Cd by crabs and barnacles. Estuar Coast Shelf Sci 21:669–686CrossRefGoogle Scholar
  53. Rainbow PS (1999) Bioaccumulation of trace metals: biological significance. Océanis 24:547–561Google Scholar
  54. Rainbow PS (2002) Trace metal concentrations in aquatic invertebrates: why and so what? Environ Pollut 120:497–507CrossRefGoogle Scholar
  55. Rainbow PS (2007) Trace metal bioaccumulation: model, metabolic availability and toxicity. Environ Int 33:576–582CrossRefGoogle Scholar
  56. Rainbow PS, Moore PG (1986) Comparative metal analyses in amphipod crustaceans. Hydrobiologia 141:273–289CrossRefGoogle Scholar
  57. Rainbow PS, Luoma SN (2011) Trace metal in aquatic invertebrates. In: Beyer, WN, Meador, JP (Eds.). Environment contaminants in biota. Interpreting tissue concentrations. Taylor and Francis books, Boca Raton, FL, USA, pp 231–252Google Scholar
  58. Rainbow PS, Moore PG, Watson D (1989) Talitrid amphipods as biomonitors for copper and zinc. Estuar Coast Shelf Sci 28:567–582CrossRefGoogle Scholar
  59. Rainbow PS, Amiard-Triquet C, Amiard JC, Smith BD, Best SL, Nassiri Y, Langston WJ (1999) Trace metal uptake rates in crustaceans (amphipods and crabs) from coastal sites in NW Europe differentially enriched with trace metals. Mar Ecol Prog Ser 183:189–203CrossRefGoogle Scholar
  60. Ramadevi KRLS, Shyamasundari K, Hanumantha Rao K (1990) Observation on the hepatopancreas of Ocypoda platytarsis (Milne-Edwards) (Crustacea, Brachyura). Ital J Zool 57:261–265Google Scholar
  61. Ray S, McLeese DW (1987) Biological cycling of cadmium in the marine environment. In: Nriagu JO, Sprague JB (eds) Cadmium in the aquatic environment. John Wiley & Sons, New York, pp 199–229Google Scholar
  62. Scapini F (2014) Behaviour of mobile macrofauna is a key factor in beach ecology as response to rapid environmental changes. Estuar Coast Shelf Sci 150:36–44CrossRefGoogle Scholar
  63. Schill RO, Köhler HR (2004) Energy reserve and metal-storage granules in the hepatopancreas of Oniscus asellus and Porcellio scaber (Isopoda) from a metal gradient at Avonmouth, UK. Ecotoxicology 13:787–796CrossRefGoogle Scholar
  64. Ugolini A, Borghini F, Calosi P, Bazzicalupo M, Chelazzi G, Focardi S (2004) Mediterranean Talitrus saltator (Crustacea, Amphipoda) as a biomonitor of heavy metals contamination. Mar Poll Bull 48:526–532CrossRefGoogle Scholar
  65. Ugolini A, Borghini F, Focardi S, Chelazzi G (2005) Heavy metals accumulation in two syntopic sandhopper species: Talitrus saltator (Montagu) and Talorchestia ugolinii Bellan Santini and Ruffo. Mar Poll Bull 50:1328–1334CrossRefGoogle Scholar
  66. Van Cappelleveen HE (1985) The ecotoxicity of zinc and cadmium for terrestrial isopods. In: Consultants, C., (Ed.), Heavy metals in the environment, Edinburgh, pp 245–247Google Scholar
  67. Warburg MR (1993) Evolutionary biology of land isopods. Springer-Verlag, Berlin Heidelberg, 159 pp. doi:
  68. Ward DJ, Simpson SL, Jolley DF (2013) Avoidance of contaminated sediments by an amphipod (Melita plumulosa), a harpacticoid copepod (Nitocra spinipes), and a snail (Phallomedusa solida). Environ Toxicol Chem 32(3):644–652Google Scholar
  69. Waterlot C, Bidar G, Peldrêne A, Roussel H, Fourrier H, Douay F (2013) Contamination, fractionation and availability of metals in urban soils in the vicinity of former lead and zinc smelters, France. Pedosphere 23:143–159Google Scholar
  70. Weeks JM (1992) Copper-rich granules in the ventral caeca of talitrid amphipods (Crustacea: Amphipoda: Talitridae). Ophelia 36:119–133CrossRefGoogle Scholar
  71. Weeks JM, Rainbow PS (1991) The uptake and accumulation of zinc and copper from solution by two species of talitrid amphipods (Crustacea). J Mar Biol Assoc UK 71:811–826CrossRefGoogle Scholar
  72. Weeks JM, Rainbow PS (1993) The relative importance of food and seawater as sources of copper and zinc to talitrid amphipods (Crustacea; Amphipoda; Talitridae). J Appl Ecol 30:722–735CrossRefGoogle Scholar
  73. White SL, Rainbow PS (1982) Regulation and accumulation of copper, zinc and cadmium by the shrimp Palaemon elegans. Mar Ecol Prog Ser 8:95–101CrossRefGoogle Scholar
  74. Witzel B (2000) The influence of zinc on the uptake and loss of cadmium and lead in the woodlouse, Porcellio scaber (Isopoda, Oniscidea). Ecotoxicol Environ Saf 47(1):43–53Google Scholar
  75. Zidar P, Drobne D, Štrus J, Blejec A (2003) Intake and assimilation of zinc, copper, and cadmium in the terrestrial isopod Porcellio scaber Latr. (Crustacea, Isopoda). Bull Environ Contam Toxicol 70:1028–1035CrossRefGoogle Scholar
  76. Zidar P, Drobne D, Štrus J, Van Gestel CAM, Donker M (2004) Food selection as a mean of Cu intake reduction in the terrestrial isopod Porcellio scaber (Crustacea, Isopoda). App Soil Ecol 25:257–265CrossRefGoogle Scholar
  77. Zilli L, Schiavone R, Scordella G, Zonno V, Verri T, Storelli C, Vilella S (2003) Changes in cell type composition and enzymatic activities in the hepatopancreas of Marsupenaeus japonicas during the moulting cycle. J Comp Physiol B 173:355–363CrossRefGoogle Scholar
  78. Znidarsic N, Strus J, Drobne D (2003) Ultrastructural alterations of the hepatopancreas in Porcellio scaber under stress. Environ Toxicol Pharmacol 13:161–174CrossRefGoogle Scholar
  79. Zödl B, Wittmann KJ (2003) Effects of sampling, preparation and defection on metal concentrations in selected invertebrates at urban sites. Chemosphere 52:1095–1103CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.National Institute of Marine Sciences and Technologies (INSTM)TunisTunisia
  2. 2.University of Tunis El Manar, Faculty of Sciences of Tunis, Laboratory of Diversity, Management and Conservation of Biological Systems (LR18ES06)TunisTunisia
  3. 3.Laboratory Ecology and Biology of Interactions (UMR CNRS 7267 EBI), Team Ecology Evolution Symbiosis, University of PoitiersPoitiers Cedex 9France

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