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Heavy metals effects on life traits of juveniles of Procambarus clarkii

1 Department of Ecology, Faculty of Sciences, Universidad Autónoma de Madrid, C/Darwin nº2, 28049 Madrid, Spain
2 Golder Associates Global Ibérica S.L.U. Paseo de la Castellana, 140-3º Izda. Edificio Lima, 28046, Madrid, Spain

Topical Section: Ecotoxicology

An incubation experiment of juvenile crayfish (Procambarus clarkii) following a three- level treatment design approach was performed to assess the effect of different heavy metal concentrations on their life history traits (lifespan, growth, moult and feeding activity). The aims were to: (1) address the response of the life traits; (2) check for the correlation between heavy metal concentrations in crayfish whole bodies with the ones of the experimental solutions; (3) analyse the variation of crayfish carbon and nitrogen stable isotopes signatures grown under these treatments. Treatments were: control or absence of pollutants (C); low level contamination (L) similar to those found in the water of the Guadiamar River (SW, Spain) one year after the Aznalcóllar mine accident, and high level contamination (H) maximum concentrations of metals measured in the water of the river after the spill. The study concludes that the H treatment produced lethal effects on juveniles of crayfish, whereas those undergoing the L treatment showed less marked effects. Crayfish’s juveniles grown in L treatment seemed able to regulate and manage this range of pollution while maintaining their biological traits. Juvenile’s capacity to bioaccumulate toxic substances also changes with the nature of the particular metals. The reduction in lifespan was mainly influenced by Cu, Zn and As. 13 C of C and juveniles from L treatment had similar values but different from those individuals of H treatment, reflecting the isotopic signature of the food source used (liver), and were also influenced by the concentration of Cu and As.
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Keywords crayfish; feeding activity; Guadiamar River; metal accumulation; moulting; stable isotope analysis

Citation: Paloma Alcorlo, Irene Lozano, Angel Baltanás. Heavy metals effects on life traits of juveniles of Procambarus clarkii. AIMS Environmental Science, 2019, 6(3): 147-166. doi: 10.3934/environsci.2019.3.147


  • 1. Sabater S (2008) Alterations of the global water cycle and their effects on river structure, function and services. Freshw Rev 1: 75–88.    
  • 2. Prat N, Toja J, Solá C, et al. (1999) Effect of dumping and cleaning activities on the aquatic ecosystems of the Guadiamar River following a toxic flood. Sci Tot Environ 242: 231–248.    
  • 3. Grimalt JO, Ferrern M, Macpherson E (1999) The mine tailing accident in Aznalcóllar. Sci Tot Environ 242: 3–11.    
  • 4. Arenas JM, Carrascal JF (2004) Situación medioambiental del Corredor Verde del Guadiamar 6 años después del vertido de Aznalcóllar. Ecosystemas 13: 69–78.
  • 5. Habsburgo-Lorena AS (1979) Preset situation of exotics species of crayfish introduced into Spanish continental waters. Freshw Crayfish 4: 175–84.
  • 6. Gutiérrez-Yurrita PJ (1997). El papel ecológico del cangrejo rojo (Procambarus clarkii) en los ecosistemas acuáticos del Parque Nacional de Doñana. Una perspectiva ecofisiológica y bioenergética. PhThesis. Dept. de Ecología. Universidad Autónoma de Madrid.
  • 7. Gherardi F (2006) Crayfish Invading Europe, the Case Study of Procambarus clarkii. Mar Freshw Behav Phy 39: 175–191.    
  • 8. Maranhão P, Marques JC, Madeira V (1995) Copper concentrations in soft tissues of the red swamp crayfish Procambarus clarkii (Girard, 1852), after exposure to a range of dissolved copper concentrations. Freshw Crayfish 10: 282–286.
  • 9. Naqvi SM, Flagge CT (1990). Chronic effects of arsenic on American red crayfish, Procambarus clarkii, exposed to Monosodium Methanearsonate (MSMA) Herbicide. B Environ Contam Tox 45: 101–106.    
  • 10. Antón A, Serrano T, Angulo E, et al. (2000) The use of two species of crayfish as environmental quality sentinels: the relationship between heavy metal content, cell and tissue biomarkers and physico-chemical characteristics of the environment. Sci Tot Environ 247: 239–251.    
  • 11. Alcorlo P, Otero M, Crehuet M et al. (2006) The use of the red swamp crayfish (Procambarus clarkii, Girard) as indicator of the bioavailability of heavy metals in environmental monitoring in the River Guadiamar (SW, Spain). Sci Tot Environ 366: 380–390.    
  • 12. Martín-Díaz ML, Tuberty SR, McKenney C, et al. (2006) The use of bioaccumulation, biomarkers and histopathology diseases in Procambarus clarkii to establish bioavailability of Cd and Zn after a mining spill. Environ Monit Assess 116: 169–184.    
  • 13. Vioque-Fernández A, Alves de Almeida E, Ballesteros J, et al. (2007). Doñana National Park survey using crayfish (Procambarus clarkii) as bioindicator: esterase inhibition and pollutant levels. Toxicol Lett 168: 260–268.    
  • 14. Vioque-Fernández A, Alves de Almeida, E, López-Barea J (2009) Assessment of Doñana National Park contamination in Procambarus clarkii: Integration of conventional biomarkers and proteomic approaches. Sci Tot Environ 407: 1784–1797.    
  • 15. Faria M, Huertas D, Soto DX, et al. (2010) Contaminant accumulation and multi-biomarker responses in field collected zebra mussels (Dreissena polymorpha) and crayfish (Procambarus clarkii), to evaluate toxicological effects of industrial hazardous dumps in the Ebro river (NE Spain). Chemosphere 78: 232–240.    
  • 16. Suárez-Serrano A, Alcaraz C, Ibáńez C, et al. (2010) Procambarus clarkii as a bioindicator of heavy metal pollution sources in the lower Ebro River and Delta. Ecotox Environ Saf 73: 280–286.    
  • 17. Geiger G, Alcorlo P, Baltanás A, et al. (2005) Impact of an introduced Crustacean on the trophic webs of Mediterranean wetlands. Biol Invasions 7: 49–73.    
  • 18. Tablado Z, Tella JL, Sánchez-Zapata JA, et al. (2010) The paradox of the long-term positive effects of a North American crayfish on a European Community of predators. Conserv Biol 24: 1230–1238.    
  • 19. Rodríguez EM, Medesani DA, Fingerman M (2007) Endocrine disruption in crustaceans due to pollutants: a review. Comp Biochem Phys A 146: 661–671.    
  • 20. Kouba A, Buric M, Kozák P (2010) Bioaccumulation and effects of heavy metals in crayfish: a review. Wat Air Soil Pollut 211: 5–16.    
  • 21. Peterson BJ, Howarth RW, Garritt RH (1985) Multiple stable isotopes used to trace the flow of organic matter in estuarine food webs. Science 227: 1361–1363.    
  • 22. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol and Syst 18: 293–320.    
  • 23. Lajtha K, Michener RH (1994) Introduction, In: Lajtha K, Michener RH, Stable isotopes in ecology and environmental science, Eds., London, UK: Blackwell Scientific Publication.
  • 24. Hershey AE, Peterson BJ (1996) Stream food webs. In: Hauer FR, Lamberti GA, Methods in stream ecology, Eds., San Diego, California: Academic Press, 511–529.
  • 25. Gannes LZ, Río CM, Koch P (1998) Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comp Biochem Phys C 119: 725–737.    
  • 26. Inger R, Bearhop S (2008) Applications of stable isotope analysis to avian ecology. Ibis 150: 447–461.    
  • 27. Martínez del Rio C, Wolf N, Carleton SA, et al. (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev Camb Philos 84: 91–111.    
  • 28. Deniro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Ac 42: 495–506.    
  • 29. Deniro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Ac 45: 341–351.    
  • 30. Reynolds JD (2002) Growth and Reproduction, In: D.M. Holdich Biology of Freshwater Crayfish Blackw, Eds, UK: Blackwell Science, 152–191.
  • 31. Nyström P (2002) Ecology, In: Holdich DM. Biology of Freshwater Crayfish. Ed., UK: Blackwell Science, 192–224.
  • 32. Martín G, Alcalá E, Burgos MD, et al. (2004) Efecto de la contaminación minera sobre el perifiton del río Guadiamar. Limnetica 23: 315–330.
  • 33. Toja J (2008) Efecto del accidente minero en el perifiton del río Guadiamar. Las algas bentónicas como indicadoras de la calidad del agua. In: Redondo I, Montes C., Carrascal F, La restauración ecológica del río Guadiamar y el proyecto del Corredor Verde. La historia de un paisaje emergente, Eds, Consejería de Medio Ambiente. Junta de Andalucía: 205–220.
  • 34. Chen WJ, Wu J, Malone RF (1995) Effects of temperature on mean molt interval, molting and mortality of Red Swamp Crawfish. Aquaculture 131: 205–217.    
  • 35. Paglianti A, Gherardi F (2004) Combined effects of temperature and diet on growth and survival of young-of-year crayfish: a comparison between indigenous and invasive species. J Crus Biol 24: 140–148.    
  • 36. Del Ramo J, Díaz-Mayans J, Torreblanca A, et al. (1987) Effects of temperature on the acute toxicity of heavy metals (Cr, Cd and Hg) to the freshwater crayfish Procambarus clarkii (Girard). B Environ Contam Tox 38: 736–741.    
  • 37. Zar JH (1999) Biostatistical Analysis, 4th Ed, New Jersey, USA.
  • 38. Anderson MB, Reddy P, Preslan JE, et al. (1997a) Metal accumulation in crayfish, exposed to a petroleum-contaminated Bayou in Louisiana. Ecotox Environ Safe 37: 267–272.
  • 39. Anderson MB, Preslan JE, Jolibois L, et al. (1997b) Bioaccumulation of lead nitrate in Red Swamp Crayfish (Procambarus clarkii). J Hazard Mater 54: 15–29.
  • 40. Mirenda RJ (1986) Toxicity and accumulation of cadmium in the crayfish, Orconectes virilis(Hagen). Arch Environ Con Tox 15: 401–407.    
  • 41. Naqvi SM, Howell RD (1993) Toxicity of cadmium and lead to juvenile red swamp crayfish, Procambarus clarkii, and effects on fecundity of adults. B Environ Contam Tox 51: 303–308.
  • 42. Martínez M, Torreblanca A, Del Ramo J, et al. (1994) Effects of sublethal exposure to lead on levels of energetic compounds in Procambarus clarkii (Girard, 1852). B Environ Contam Tox 52: 729–733.    
  • 43. Taylor RM, Watson GD, Alikhan MA (1995) Comparative sub-lethal and letal acute toxicity of copper to the freshwater crayfish, Cambarus robutus (Cambaridae, Decapoda, Crustacea) from an acidic metal-contaminated lake and a circumneutral uncontaminated stream. Water Resour 29: 401–408.
  • 44. Rainbow PS, Amiard-Triquet C, Amiard JC, et al. (2000) Observations on the interaction of zinc and cadmium uptake rates in crustaceans (amphipods and crabs) from coastal sites in UK and France differentially enriched with trace metals. Aquat Toxicol 50: 189–204.    
  • 45. Bardeggia M, Alikhan MA (1991) The relationship between copper and nickel levels in the diet, and their uptake and accumulation by Cambarus bartoni (Fabricius) (Decapoda, Crustacea). Water Resour 25(10): 1187–1192
  • 46. Kim SD (2003) The removal by crab shell of mixed heavy metal ions in aqueous solution. Bioresource Technol 87: 355–357.    
  • 47. Torreblanca A, Díaz-Mayans J, Del Ramo J (1987) Oxygen uptake and gill morphological alterations in Procambarus clarkii (Girard) after sublethal exposure to lead. Comp Biochem Phys C 86: 219–224.    
  • 48. Vosloo A, Van Aardt WJ, Mienie LJ (2002) Sublethal effects of copper on the freshwater crab Potamonautes warreni. Comp Biochem Phys C 133: 695–702.    
  • 49. Rowe CL, Hopkins WA, Zehnder C, et al. (2000) Metabolic costs incurred by crayfish (Procambarus acutus) in a trace element-polluted habitat: further evidence of similar responses among diverse taxonomic groups. Comp Biochem Phys C, 129: 275–283.
  • 50. López-López S, Nolasco H, Vega-Villasante F (2003) Characterization of digestive gland esterase-lipase activity of juvenile redclaw crayfish Cherax quadricarinatus. Comp Biochem Phys C 135: 337–347.
  • 51. Sherba M, Dunham DW, Harvey HH (2000) Sublethal copper toxicity and food response in the freshwter crayfish Cambarus bartonii (Cambridae, Decapoda, Crustacea). Ecotox Environ Saf 46: 329–333.    
  • 52. Weis JS, Cristini A, Rao KK (1992) Effects of pollutants on molting and regeneration in Crustacea. Amer Zool 32: 495–500.    
  • 53. 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.    
  • 54. Carmona-Osalde C, Rodríguez-Serna M, Olvera-Novoa MA et al (2004) Gonadal development, spawning, growth and survival of the crayfish Procambarus llamasi at three different water temperatures. Aquaculture 232: 305–316.    
  • 55. Zanotto FP, Wheatly MG (2003) Calcium balance in crustaceans: nutritional aspects of physiological regulation. Comp Biochem Phys A 133: 645–660.
  • 56. Stinson MD, Eaton DL (1983) Concentrations of Lead, Cadmium, Mercury, and Koper in the Crayfish (Pacifastacus leniusculus) Obtained from a Lake Receiving Urban Runoff. Arch Environ Con Tox 12: 693–700.    
  • 57. Depledge MH, Forbes TL, Forbes VE (1993) Evaluation of cadmium, copper, zinc and iron concentrations and tissue distributions in the benthic crab, Dorippe granulata (De Haan, 1841) from Tolo Harbour, Hong Kong. Environ Pollut 81: 15–19.    
  • 58. Rainbow PS (1995). Physiology, Physicochemistry and metal uptake: a crustacean perspective. Marine Pollut Bull 31: 55–59.    
  • 59. Zia S, Alikhan MA (1989) Copper uptake and regulation in a copper-tolerant decapod Cambarus bartoni (Fabricius) (Decapoda, Crustacea). B Environ Contam Tox 42: 103–110.
  • 60. Rainbow PS (1997). Ecophysiology of trace metal uptake in Crustaceans. Estuar Coast Shelf S 44: 169–175.    
  • 61. Alcorlo P, Geiger W, Otero, M (2008) Reproductive biology and life cycle of the invasive crayfish Procambarus clarkii (Crustacea: Decapoda) in diverse aquatic habitats of South-Western Spain: Implications for population control. Fund Appl Limnol 173(3): 197–212.
  • 62. Allison G, Laurenson LJB, Pistone G, et al. (2000) Effects of dietary copper on the Australian Freshwater Crayfish Cherax destructor. Ecotox Environ Safe 46: 117–123.    
  • 63. Pastor A, Medina J, Del Ramo J, et al. (1988) Determination of lead in treated crayfish Procambarus clarkii: Accumulation in different tissues. B Environ Contam Tox 41: 412–418.    
  • 64. Rincón-Leon F, Zurera-Cosano G, Pozo-Lora R (1988) Lead and cadmium concentrations in Red Crayfish (Procambarus clarkii, G.) in the Guadalquivir River Marshes (Spain). Arch Environ Con Tox 17: 251–256.
  • 65. Del Ramo J, Pastor A, Torreblanca A, et al. (1989) Cadmium-Blinding proteins in midgut gland of freshwater crayfish Procambarus clarkii. B Environ Contam Tox 42: 241–246.    
  • 66. Naqvi SM, Glagge CT, Hawkins RL (1990) Arsenic uptake and depuration by red crayfish, Procambarus clarkii, exposed to various concentrations of Monosodium Methanearsonate (MSMA) Herbicide. B Environ Contam Tox 45: 94–100.    
  • 67. Junger M, Planas D (1994) Quantitative use of stable carbon isotope analysis to determine the trophic base of invertebrate communities in a boreal forest lotic system. Can J Fish Aquat Sci 51: 52–61.    
  • 68. Quinn MR, Feng X, Folt CL, et al. (2003) Analyzing trophic transfer of metals in stream food webs using nitrogen isotopes. Sci Tot Environ, 17: 73–89.
  • 69. Larsson P, Holmqvist N, Stenroth P, et al. (2007) Heavy Metals and Stable Isotopes in a Benthic Omnivore in a Trophic Gradient of Lakes. Environ Sci Technol 41(17): 5973–5979.
  • 70. Alcorlo P, Baltanás A (2013) The trophic ecology of the red swamp crayfish (Procambarus clarkii) in Mediterranean aquatic ecosystems: a stable isotope study. Limnetica 32(1): 121–138.
  • 71. Power M, Klein G., Guiguer KRRA, et al. (2002) Mercury accumulation in the fish community of a sub-arctic lake in relation to trophic position and carbon sources. J Appl Ecol 39: 819–830.    
  • 72. Watanabe K, Monaghan MT, Takemon Y, et al. (2008) Biodilution of heavy metals in a stream macroinvertebrate food web: Evidence from stable isotope analysis. Sci Tot Environ 394: 57–67.    


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