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Influence of Cadmium Exposure on Growth and Fecundity of Freshwater Mosquitofish Gambusia affinis: In Situ and In Vivo Studies

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Abstract

This study aims to investigate the effect of cadmium (Cd) exposure on growth and fecundity of mosquitofish Gambusia affinis. For this purpose, two natural populations of pregnant females of G. affinis captured from two sites were differently contaminated with Cd (S1 present Cd levels 5-fold higher than S2) and a sublethal exposure to 0.4 mg CdCl2/L (10% of LC50) during 56 days was conducted in vivo. The length–weight regression revealed a significant difference in the growth between these two populations. A significant difference in fecundity was also noted between the two populations. Indeed, the embryo numbers in pregnant females captured from S1 are significantly higher than those noted in pregnant females from S2 (21.17 ± 5 and 7.97 ± 2.12, respectively; p < 0.05). Following Cd exposure, we noted a growth perturbation resulting in lower values of both indices BWG and SGR following 7 and 21 days (−5.21 and −1.18 for BWG, and −2.09 and −0.46 for SGR, respectively) and a recuperation of growing weight at 42 and 56 days (1.32 and 1.71 for BWG, and 0.45 and 0.54 for SGR, respectively). For CF index, we observed a significant difference (p < 0.05) between control and Cd groups at 7 and 21 days of exposure, and at 21 and 56 days respectively for HSI and GSI indices. Furthermore, Cd contents in both tissues (liver and yolk sac) and fractions (cytosolic and membrane) are significantly different between groups during experimentation. In addition, the Cd contents noticed in the liver membrane fraction are significantly higher than those noted in the yolk sac tissue. The MTs levels revealed a significant difference between the control and Cd groups. In liver tissue, a significant difference was noted, in MTs levels, during the Cd exposure (7, 21, 42, and 56 days) while in the yolk sac tissue the difference was noted at 42 days of exposure. Taken together, these results imply the potential negative effect of Cd on physiological status of G. affinis as evidenced by decreasing growth and fecundity rate.

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References

  1. Gill T, Tewari H, Pande J (1991) In vivo and in vitro effects of cadmium on selected enzymes in different organs of the fish Barbus conchonius Ham. (rosy barb). Comp Biochem Physiol 100C:501–505

    CAS  Google Scholar 

  2. Sadiq M (1992) Toxic metal chemistry in marine environments. Marcel Dekker, New York, p 390

    Google Scholar 

  3. Friberg I, Piscator M, Nordberg GF, Kjellstrom T (1973) Cadmium in the environment. Second report for the Swedish Environment Protection Agency. Karolinska Institutet, Stockholm

    Google Scholar 

  4. Sunderman FW Jr, Plowman MC, Hopfer SM (1991) Embryotoxicity and teratogenicity of cadmium chloride in Xenopus laevis, assayed by the FETAX procedure. Ann Clin Lab Sci 21:381–391

    PubMed  CAS  Google Scholar 

  5. Chen B, Hales BF (1994) Cadmium-induced rat embryotoxicity in vitro is associated with increased abundance of E-cadherin protein in the yolk sac. Toxicol Appl Pharmacol 128:293–231

    Article  PubMed  CAS  Google Scholar 

  6. Larsson A, Johans Sons Jobeck ML, Fange R (1976) Comparative study of some haematological and biochemical blood parameters in fishes from the Skagerrak. J Fish Biol 9:425–444

    Article  CAS  Google Scholar 

  7. Thomas P (1990) Teleost model for studying the effects of chemicals on female reproductive endocrine function. J Exp Zool 4:126–128

    Article  CAS  Google Scholar 

  8. Hontela A, Daniel C, Ricard AC (1996) Effects of acute and subacute exposures to cadmium on the interrenal and thyroid function in rainbow trout, Oncorhynchus mykiss. Aquat Toxicol 35:171–182

    Article  CAS  Google Scholar 

  9. Zhang W, Pang F, Huang Y, Yan P, Lin W (2008) Cadmium exerts toxic effects on ovarian steroid hormone release in rats. Toxicol Lett 182:18–23

    Article  PubMed  CAS  Google Scholar 

  10. Luckenbach T, Kilian M, Triebskorn R, Oberemm A (2001) Fish early life stage tests as a tool to assess embryotoxic potentials in small streams. J Aquat Ecosyst Stress Recov 8:355–370

    Article  CAS  Google Scholar 

  11. Ke C, Wang WX (2001) Bioaccumulation of metals (Cd, Se, and Zn) in an estuarine oyster and a coastal oyster. Aquat Toxicol 56:33–51

    Article  PubMed  CAS  Google Scholar 

  12. Sassi A, Annabi A, Kessabi K, Kerkeni A, Said K, Messaoudi I (2010) Influence of high temperature on cadmium-induced skeletal deformities in juvenile mosquitofish (Gambusia affinis). Fish Physiol Biochem 36:403–409

    Article  PubMed  CAS  Google Scholar 

  13. Espina S, Salibian A, Diaz F (2000) Influence of cadmium on the respiratory function of the grass carp Ctenopharyngodon idella. Water Air Soil Poll 119:1–10

    Article  CAS  Google Scholar 

  14. Berntssen MH, Lundebye AK (2001) Energetics in Atlantic salmon (Salmo salar L.) parr fed elevated dietary cadmium. Comp Biochem Physiol 128:311–323

    CAS  Google Scholar 

  15. Marr JCA, Lipton J, Cacela D, Hansen JA, Bergman HL, Meyer JS, Hogstrand C (1996) Relationship between copper exposure duration, tissue copper concentration and rainbow trout growth. Aquat Toxicol 36:17–30

    Article  CAS  Google Scholar 

  16. Kazlauskienė N, Stasiūnaitė P (1999) The lethal and sublethal effect of heavy metal mixture on rainbow trout (Oncorhynchus mykiss) in its early stages of development. Acta Zool Lithuanica Hydrobiol 1:47–54

    Google Scholar 

  17. Hamza-Chaffai A, Amiard-Triquet C, Abed AH (1997) Metallothionein-like protein: is it an efficient biomarker of metal contamination? A case study based on fish from the Tunisian coast. Arch Environ Contam Toxicol 33:53–62

    Article  PubMed  CAS  Google Scholar 

  18. Annabi A, Messaoudi I, Kerkeni A, Said K (2009) Comparative study of the sensitivity to cadmium of two populations of Gambusia affinis from two different sites. Environ Monit Assess 155:459–465

    Article  PubMed  CAS  Google Scholar 

  19. Messaoudi I, Deli T, Kessabi K, Barhoumi S, Kerkeni A, Saïd K (2009) Association of spinal deformities with heavy metal bioaccumulation in natural populations of grass goby, Zosterisessor ophiocephalus Pallas, 1811 from the Gulf of Gabès (Tunisia). Environ Monit Assess 156:551–560

    Article  PubMed  CAS  Google Scholar 

  20. Peden AE (1973) Variation in anal spot expression of Gambusia females and its effect on male courtship. Copeia 2:250–263

    Article  Google Scholar 

  21. Mayrat A (1959) Nouvelle méthode pour l’étude comparée d’une croissance relative dans deux echantillons. Application à la carapace de Penaeus kerathurus (Forskal). Bull Inst Franç Afr Noire A 21:21–59

    Google Scholar 

  22. Edwards TM, Miller HD, Guillette LJ (2006) Water quality influences reproduction in female mosquitofish (Gambusia holbrooki). Eight Florida Springs 114:69–75

    Google Scholar 

  23. Azaza MS, Dhraief MN, Kraiem MM (2008) Effects of water temperature on growth and sex ratio of juvenile Nile tilapia Oreochromis niloticus (Linnaeus) reared in geothermal waters in southern Tunisia. J Therm Biol 33:98–105

    Article  Google Scholar 

  24. Viarengo A, Ponzano E, Dondero F, Fabbri R (1997) A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic molluscs. Mar Environ Res 44:69–84

    Article  CAS  Google Scholar 

  25. Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  26. Bervoets L, Blust R (2003) Metal concentrations in water, sediment and gudgeon (Gobio gobio) from a pollution gradient: relationship with fish condition factor. Environ Pollut 126:9–19

    Article  PubMed  CAS  Google Scholar 

  27. Morato TP, Afonso P, Lourinho P, Barreiros JP, Santos RS, Nash RDM (2001) Length–weight relationships for 21 coastal fish species of the Azores, north-eastern Atlantic. Fish Res 50:297–302

    Article  Google Scholar 

  28. Annabi A, Messaoudi I, Kerkeni A, Said K (2011) Cadmium accumulation and histological lesion in mosquitofish (Gambusia affinis) tissues following acute and chronic exposure. Inter J Env Res 5:745–756

    CAS  Google Scholar 

  29. Gulati RD, Bodar CWM, Schuurmans ALG, Faber JAJ, Zandee DI (1988) Effect of cadmium exposure on feeding of freshwater planktonic crustaceans. Comp Biochem Physiol C 90:335–340

    Article  PubMed  CAS  Google Scholar 

  30. Szczerbik P, Mikołajczyk T, Sokołowska-Mikołajczyk M, Socha M, Chyb J, Epler P (2006) Influence of long-term exposure to dietary cadmium on growth, maturation and reproduction of goldfish (subspecies: Prussian carp Carassius auratus gibelio B.). Aqua Toxicol 77:126–135

    Article  CAS  Google Scholar 

  31. Miliou H, Zaboukas N, Moraitou-Apostolopoulou M (1998) Biochemical composition, growth, and survival of the guppy, Poecilia reticulata, during chronic sublethal exposure to cadmium. Arch Environ Contam Toxicol 35:58–63

    Article  PubMed  CAS  Google Scholar 

  32. Eaton JG, McKim JM, Holcombe GW (1978) Metal toxicity to embryos and larvae of seven fresh water fish species—I. Cadmium. Bull Environ Contam Toxicol 19:95–113

    Article  PubMed  CAS  Google Scholar 

  33. Spehar RL (1976) Cadmium and zinc toxicity to flagfish, Jordanella floridae. J Fish Res Bd Canada 33:1939–1945

    Article  CAS  Google Scholar 

  34. Scherer E, McNicol RE, Evans RE (1997) Impairment of lake trout foraging by chronic exposure to cadmium: a black-box experiment. Aquat Toxicol 37:1–7

    Article  CAS  Google Scholar 

  35. Hansen JA, Welsh PG, Lipton J, Suedkamp M (2002) The effects of long-term cadmium exposure on the growth and survival of juvenile bulltrout (Salvelinus cofluentus). Aquat Toxicol 58:165–174

    Article  PubMed  CAS  Google Scholar 

  36. Tyler CR, Sumpter JP (1996) Oocyte growth and development in teleosts. Rev Fish Biol Fish 6:287–318

    Article  Google Scholar 

  37. Thomas P (1993) Effect of cadmium on gonadotropin secretion from Atlantic croaker pituitaries incubated in vitro. Mar Environ Res 35:141–145

    CAS  Google Scholar 

  38. Pundir R, Saxena AB (1992) Chronic toxic exposure of cadmium on the pituitary gland of fish Puntius ticto and pattern of recoupment. J Environ Biol 13:69–74

    CAS  Google Scholar 

  39. Al-Yousuf MH, El-Shahawi MS, Al-Ghais SM (2000) Trace metals in the liver, skin and muscle of Lethrinus lentjan fish species in relation to body length and sex. Sci Total Environ 256:87–94

    Article  PubMed  CAS  Google Scholar 

  40. Bouaziz A, Semroud R, Djabali F, Maurin C (1998) Reproduction du merlu Merluccius merluccius (Linnaeus, 1758) dans la région de Bou-Ismail. Cah Opt Méditer 35:109–117

    Google Scholar 

  41. Brown V, Shurben D, Miller W, Crane M (1994) Cadmium toxicity to rainbow trout Oncorhynchus mykiss Walbaum and brown trout Salmo trutta L. over extended exposure periods. Ecotox Env Saf 29:38–46

    Article  CAS  Google Scholar 

  42. Jezierska B, Witeska M (2001) Metal toxicity to fish. Monographs No. 42, Wydawnictwo Akademii Podlaskiej, Siedlce, Poland

  43. Roch M, McCarter JA, Matheson AT, Clark MJR, Olafson RW (1982) Hepatic metallothionein in rainbow trout (Salmo gaidnen) as indicator of metal pollution in the Campbell River system. Can J Fish Aquat Sci 39:1596–1601

    Article  CAS  Google Scholar 

  44. Chan KM, Davidson WS, Hew CL, Fletcher GL (1989) Molecular cloning of metallothionein cDNA and analysis of metallothionein gene expression in winter flounder tissues. Can J Zool 67:2520–2527

    Article  CAS  Google Scholar 

  45. Povlsen AF, Korsgaard B, Bjerregaard P (1990) The effect of cadmium on vitellogenin metabolism in estradiol-induced flounder (Platichthys flesus (L.)) males and females. Aquat Tox 17:253–262

    Article  CAS  Google Scholar 

  46. Pereirra JJ, Ziskowski J, Mercaldo-Allen R, Luedke D, Gould E (1992) Vitellogenin studies in winter flounder (Pleuronectes americanus) from long Island Sound and Boston Harbor. Estuaries 15:289–297

    Article  Google Scholar 

  47. Olsson PE, Kling P, Petterson C, Silversand C (1995) Interaction of cadmium and oestradiol-17 beta on metallothionein and vitellogenin synthesis in rainbow trout (Oncorhynchus mykiss). Biochem J 307:197–203

    PubMed  CAS  Google Scholar 

  48. Michibata H, Nojima Y, Kojma MK (1987) Stage sensitivity of eggs of the teleost Oryzias latipes to cadmium exposure. Environ Res 42:321–327

    Article  PubMed  CAS  Google Scholar 

  49. Victor B, Mahalingam S, Sarojini R (1986) Toxicity of mercury and cadmium on oocyte differentiation and vitellogenesis of the teleost, Lepidocephalichthys thermalis (Bleeker). J Environ Biol 7:209–214

    CAS  Google Scholar 

  50. Kime DE (1984) The effect of cadmium on steroidogenesis by testes of the rainbow trout, Salmo gairdneri. Toxicol Lett 22:83–88

    Article  PubMed  CAS  Google Scholar 

  51. Kagi JHR, Schaffer A (1988) Biochemistry of metallothionein. J Biochem 27:8509–8515

    Article  CAS  Google Scholar 

  52. Ochi T, Takahashi K, Ohsawa M (1997) Indirect evidence for the induction of a pro-oxidant state by cadmium chloride in cultured mammalian cells and a possible mechanism for the induction. Mut Res 180:257–266

    Google Scholar 

  53. Casilino E, Calzaretti G, Sbalno C, Landriscina C (2000) Cadmium-dependent enzyme activity alteration is not imputable to lipid peroxidation. Arch Biochem Biophys 383:288–295

    Article  Google Scholar 

  54. Dondero F, Piacentini L, Banni M, Rebelo M, Burlando B, Viarengo A (2005) Quantitative PCR analysis of two molluscan metallothionein genes unveils differential expression and regulation. Gene 345:259–270

    Article  PubMed  CAS  Google Scholar 

  55. Allen P (1995) Chronic accumulation of cadmium in the edible tissues of Oreochromis aureus (Steindachner): modification by mercury and lead. Arch Environ Contam Toxicol 29:8–14

    Article  PubMed  CAS  Google Scholar 

  56. Shackley SE, King PE, Gordon SM (1981) Vitellogenesis and trace metals in a marine teleost. J Fish Biol 18:349–352

    Article  CAS  Google Scholar 

  57. Lin H, Hsu S, Hwang P (2000) Maternal transfer of cadmium tolerance in larval Oreochromis mossambicus. J Fish Biol 57:239–249

    Article  CAS  Google Scholar 

  58. Bernado J (1996) Maternal effects in animal ecology. Amer Zool 36:83–105

    Google Scholar 

  59. Flint PL (2003) Incubation behavior of greater scaup on the Yukon–Kuskokwim Delta, Alaska. Wildfowl 54:97–105

    Google Scholar 

  60. Scheuhammer AM (1996) Influence of reduced dietary calcium on the accumulation and effects of lead, cadmium and aluminum in birds. Environ Pollut 94:337–343

    Article  PubMed  CAS  Google Scholar 

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Annabi, A., Kessabi, K., Kerkeni, A. et al. Influence of Cadmium Exposure on Growth and Fecundity of Freshwater Mosquitofish Gambusia affinis: In Situ and In Vivo Studies. Biol Trace Elem Res 148, 345–355 (2012). https://doi.org/10.1007/s12011-012-9372-2

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