Abstract
Concentrations of essential metals (Cu, Co, Cr, Fe, Ni, Mn, and Zn) and non-essential and toxic metals (Ag, Cd, Hg, and Pb) were quantified in hepatopancreas and abdominal muscle for 73 specimens (37 males and 36 females) of Procambarus clarkii from Lake Trasimeno (Italy) in a year’s campaign (July 2018 to June 2019). Elemental concentrations determined in crayfish differed in tissues, seasons, and gender. Both sexes showed lower concentrations in abdominal muscle than in hepatopancreas. Essential metals accumulated in higher concentrations in both tissues than non-essential elements, while associations between essential metals were stronger, especially for females; however, a strong correlation was also observed between Cu and Ag in both sexes. No significant differences in concentrations were recorded between sexes for all seasons; contrarily, significant differences among the total seasonal concentrations (males plus females) were observed only for essential metals and for Ag. Seasonal Toxic Contamination Index (TCI) for Cr, Ni, Cu, Zn, Cd, Pb, and Hg were calculated to assess the toxicity level of metals in the sediments. TCI higher than 1 was detected for Ni only in summer, confirming the close connection between the fluctuating hydrological levels of the shallow Lake Trasimeno, strongly dependent on precipitation, and the metal contamination levels of sediments.
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References
Ackefors H (1999) The positive effects of established crayfish introductions in Europe. In: Gherardi e Holdich D.M., (Eds). Crayfish in Europe as alien species (How to make the best of a bad situation?). Crustacean issues, 11, A.A. Balkema, Rotterdam, Netherlands, pp 49-62
Alcorlo P, Otero M, Crehuet M, Baltanás A, Montes C (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. Total Environ. 366:380–390
Alikhan MA, Zia S (1989) Nickel uptake and regulation in a copper-tolerant decapod, Cambarus bartoni (Fabricius) (Decapoda, Crustacea). Bulletin of Environmental Contamination and Toxicology 42:94–102
Allen HE, Fu G, Deng B (1993) Analysis of acid-volatile sulfide (AVS) and simultaneously extracted metals (SEM) for the estimation of potential toxicity in aquatic sediments. Environ. Toxicol. Chem. 12(8):1441–1453
Analytical Methods Committee (1994) Is my calibration linear? Analyst 119:2363
Anandkumar A, Li J, Prabakaran K, Xi JZ, Leng ZI, Nagarajan R, Du D (2020) Accumulation of toxic elements in an invasive crayfish species (Procambarus clarkii) and its health risk assessment to humans. J. Food Compos. Anal. 88:103449
Anderson M, Preslan J, Jolibois L, Bollinger J, George W (1997) Bioaccumulation of lead nitrate in red swamp crayfish (Procambarus clarkii). J Hazard Mater 54:15–29
Ayodeji OJ, Ikem A, Wetzel J, Awoyemi OM, Garth J (2021) Sex-specific and inter-species differences in the accumulation and distribution profile of metal(loid)s in crayfish specimens. Toxicol. Environ. Health Sci. 13:143–152
Bellante A, Maccarone V, Buscaino G, Buffa G, Filiciotto F, Traina A, Del Core M, Mazzola S, Sprovieri (2015) M. Trace element concentrations in red swamp crayfish (Procambarus clarkii) and surface sediments in Lake Preola and Gorghi Tondi natural reserve, SW Sicily. Environ. Monit. Assess. 187:1–18
Bianchi N, Fortino S, Leonzio C, Ancora S (2011) Ecotoxicological study on lead shot from hunting in the Padule di Fucecchio marsh (Tuscany, Italy). Chem. Ecol. 27:153–166
Bollinger JE, Bundy K, Anderson MB, Millet L, Preslan JE, Lolibois L, Chen H-L, Kamath B, George WJ (1997) Bioaccumulation of chromium in red swamp crayfish (Procambarus clarkii). J. Hazard. Mater. 54:1–13
Cisar P, Saberioon M, Kozák P, Pautsina A (2018) Fully contactless system for crayfish heartbeat monitoring: undisturbed crayfish as bio-indicator. Sens Actuators B Chem 255(P1):29–34
Davies-Colley RJ, Nelson PO, Williamson KJ (1985) Sulfide control of cadmium and copper concentrations in anaerobic estuarine sediments. Mar. Chem. 16:173–186
De Bartolomeo A, Poletti L, Sanchini G, Sebastiani B, Morozzi G (2004) Relationship among parameters of lake polluted sediments evaluated by multivariate statistical analysis. Chemosphere 55:1323–1329
Devesa V, Súñer MA, Lai VWM, Granchinho SCR, Martínez JM, Vélez D, Cullen WR, Montoro R (2002) Determination of arsenic species in a freshwater crustacean Procambarus clarkii. Appl. Organomet. Chem. 16:123–132
Devi M, Thomas DA, Barber JT, Fingerman M (1996) Accumulation and physiological and biochemical effects of cadmium in a simple aquatic food chain. Ecotoxicol. Environ. Saf. 33:38–43
Di Toro DM, Mahony JD, Hansen DJ, Scott KJ, Carlsori AR, Ankley GT (1992) Acid volatile sulfide predicts the acute toxicity of cadmium and nickel in sediments. Environ. Sci. Technol. 26:96–101
Di Veroli , Selvaggi R, Goretti E (2012) Chironomid mouthpart deformities as indicator of environmental quality: a case study in Lake Trasimeno (Italy). J Environ Monitoring 14(5) 1473. https://doi.org/10.1039/c2em10882h
Dörr A.J.M., La Porta G., Pedicillo G., Lorenzoni M. (2006). Biology of Procambarus clarkii (Girard, 1852) in Lake Trasimeno. Knowl Manag Aquat Ecosyst (Bull. Fr. Pêche. Piscic.) 380-381:1155-1168
Dörr AJM, Pedicillo G, Lorenzoni M (2001) Prima segnalazione in Umbria di Procambarus clarkii (Girard, 1852), Orconectes limosus (Rafinesque) e Astacus leptodactylus Eschscholtz (Crustacea Decapoda). Rivista di Idrobiologia 40:2–3
Dörr AJM, Elia AC, Rodolfi M, Garzoli L, Picco AM, D’amen M, Scalici M (2012) A model of co-occurrence: segregation and aggregation patterns in the mycoflora of the crayfish Procambarus clarkii in Lake Trasimeno (central Italy). Journal of Limnology 71(1)
Dörr AJM, Scalici M, Caldaroni B, Magara G, Scoparo M, Goretti E, Elia AC (2020) Salinity tolerance of the invasive red swamp crayfish Procambarus clarkii (Girard, 1852). Hydrobiologia 847:2065–2081
Dörr AJM, Scalici M (2013) Revisiting reproduction and population structure and dynamics of Procambarus clarkii eight years after its introduction into Lake Trasimeno (Central Italy). Knowl. Manag. Aquat. Ecosyst. 408:10
Dörr AJM, Scoparo M, Cardinali I, La Porta G, Caldaroni B, Magara G, Pallottini M, Selvaggi R, Cenci-Goga B, Goretti E, Cappelletti D, Lancioni H, Elia AC (2021) Population ecology and genetic diversity of the invasive alien species Procambarus clarkii in Lake Trasimeno (Italy). Biology 10:1059
Dragoni W (1989) Idrogeologia del Lago Trasimeno: sintesi, problemi, aggiornamenti. CNR 49:191–206
Eisler, R. (1998). Nickel hazards to fish, wildlife, and invertebrates: a synoptic review. U. S. Geological Survey. Biological Science Report USGS/BRD/BSR- 1998-0001
Eisler R (1986) Chromium hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish and Wildlife Service Biological Report 85 (1.6)
Elia AC, Dörr AJM, Mastrangelo C, Prearo M, Abete MC (2006) Glutathione and antioxidant enzymes in the hepatopancreas of crayfish Procambarus clarkii (Girard, 1852) of Lake Trasimeno (Italy). Bull Fr Pêche Piscic 1351-1361
Eurachem (1998) The fitness for purpose of analytical methods. A laboratory guide to method validation and related topics. 1st Internet version. Athens: EURACHEM
Frondini F, Dragoni W, Morgantini N, Donnini M, Cardellini C, Caliro S, Melillo M, Chiodini G (2019) An Endorheic Lake in a Changing Climate: Geochemical Investigations at Lake Trasimeno (Italy). Water 11:1319
Gherardi F (2006) Crayfish invading Europe: the case study of Procambarus clarkii. Mar Fresh Behav Physiol 39(3):175–191
Gherardi, F., Baldaccini, G.N., Ercolini, P., Barbaresi, S., De Luise, G., Mazzoni, D., Mori, M. (1999) The situation in Italy. Crustac. 11: 107–128
Goretti E, Pallottini M, Ricciarini MI, Selvaggi R, Cappelletti D (2016) Heavy metals bioaccumulation in selected tissues of red swamp crayfish: an easy tool for monitoring environmental contamination levels. Sci Total Environ. 559:339–346
Goretti E, Pallottini M, Pagliarini S, Catasti M, La Porta G, Selvaggi R, Gaino E, Di Giulio AM, Ali A (2020) Use of larval morphological deformities in Chironomus plumosus (Chironomidae: Diptera) as an indicator of freshwater environmental contamination (Lake Trasimeno, Italy). Water 12:1
Guner U (2010) Cadmium bioaccumulation and depuration by freshwater crayfish. Astacus leptodactylus. Ecology 19(77):23–28
Gutiérrez-Yurrita P, Montes C (1999) Bioenergetics and phenology of reproduction of the introduced red swamp crayfish, Procambarus clarkii, in Doñana National Park, Spain, and implications for species management. Freshw. Biol. 42:561–574
Hammer Ø, Harper DAT, Ryan PD (2001) Past: paleontological statistics software package for education and data analysis. 4, pp 1–9
Hasburgo-Lorena AS (1986) The status of the Procambarus clarkii population in Spain. Freshwat. Crayfish 6:131–136
Hobbs HH, Jess JP, Huner JV (1989) A review of global crayfish introductions with particular emphasis on two north American species (Decapoda, Cambaridae). Crustaceana 56:299–316
Hothem RL, Bergen DR, Bauer ML, Crayon JJ, Meckstroth AM (2007) Mercury and trace elements in crayfish from Northern California. Bulletin of Environmental Contamination and Toxicology 79:628–632
Huner JV (1994) Ecological observations of red swamp crayfish, Procambarus clarkii (Girard, 1852), and white river crayfish, Procambarus zonangulus (Hobbs and Hobbs 1990), as regards their cultivation in earthen ponds. Freshwat. Crayfish 10:456–468
Khan S, Nugegoda D (2003) Australian Freshwater Crayfish Cherax destructor accumulates and depurates nickel. Bull. Environ. Contam. Toxicol. 70:0308–0314
Kouba A, Buric M, Kozak P (2010) Bioaccumulation and effects of heavy metals in crayfish: a review. Water Air Soil Pollut 211(1–4):5–16
Loukola-Ruskeeniemi K, Kantola M, Halonen T, Seppänen K, Henttonen P, Kallio E et al (2003) Mercury bearing black shales and human Hg intake in eastern Finland: impact and mechanisms. Environmental Geology 43:283–297
Lindvquist OV, Huner JV (1999) Life history characteristics of crayfish: what makes some of them good colonizers? Crustac. 11:23–30
MacDonald DD, Ingersoll CG, Berger TA (2000) Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Arch. Environ. Contam. Toxicol. 39:20–31
Madigosky SR, Álvarez-Hernández X, Glass J (1991) Lead, cadmium and aluminium accumulation in the red swamp crayfish Procambarus clarkii G. collected from roadside drainage ditches in Louisiana. Arch. Environ. Contam. Toxicol. 20:253–258
Mann RM, Grosell M, Bianchini A, Wood CM (2004) Biologically incorporated dietary silver has no ionoregulatory effects in American red crayfish (Procambarus clarkii). Environ Toxicol Chem. 23(2):388–395
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. Freshwater Crayfish 10:282–286
Marchegiano M, Francke A, Gliozzi E, Wagner B, Arizteguia D (2018) High-resolution palaeohydrological reconstruction of central Italy during the Holocene. Holocene 29:481–492
Muyssen BTA, Brix KV, DeForest DK, Janssen CR (2004) Nickel essentiality and homeostasis in aquatic organisms. Environmental Reviews 12:113–131
Naqvi SM, Howell RD (1993) Cadmium and lead uptake by red swamp crayfish (Procambarus clarkii) of Louisiana. Bull. Environ. Contam. Toxicol. 51:296–302
Naqvi SM, Devalraju I, Naqvi NH (1998) Copper Bioaccumulation and Depuration by Red Swamp Crayfish, Procambarus clarkia. Bull. Environ. Contam. Toxicol. 61:65–71
Nagpal NK (2004) Water quality guidelines for cobalt. Ministry of Water, Land and Air Protection, Water Protection Section, Water, Air and Climate Change Branch, Victoria
Norwood WP, Borgmann U, Dixon DG (2007) Interactive effects of metals in mixtures on bioaccumulation in the amphipod Hyalella azteca. Aquat Toxicol 84(2):255–267
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. Crustac. Biol. 24:140–148
Pastor A, Medina J, Del Ramo J, Torreblanca A, Díaz-Mayans J, Fernández F (1998) Determination of lead in treated crayfish Procambarus clarkii: accumulation in different tissues. Bull. Environ. Contam. Tox. 41:412–418
Pennuto CM, Lane OP, Evers DC, Taylor RJ, Loukmas J (2005) Mercury in the northern crayfish, Orconectes virilis (Hagen), in New England, USA. Ecotoxicology 14(2005):149–162
Piersanti S, Pallottini M, Salerno G, Goretti E, Elia AC, Dörr AJM, Rebora M (2018) Resistance to dehydration and positive hygrotaxis in the invasive red swamp crayfish Procambarus clarkii. Knowl Manag Aquat Ecosyst 419:36
Rigler FH, Downing JA (1984) The calculation of secondary production. In: J.A., Downing, F.H., Rigler (Eds.), A manual on methods for the assessment of secondary productivity in fresh waters, second ed. 17. IBP Handbook, Blackwell, Oxford pp19–58
Rincón-León 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. Contam. Toxicol. 17:251–256
Roldan BM, Shivers RR (1987) The uptake and storage of iron and lead in cells of the crayfish (Orconectes propinquus) hepatopancreas and antennal gland. Comp. Biochem. Physiol. 86C:201–214
Rubio R, Tineo J, Torreblanca A, Del Ramo J, Díaz-Myans J (1991) Histological and electron microscopical observations on the effects of lead on gills and midgut gland of Procambarus clarkii. Toxicol. Environ. Chem. 31-32:347–352
Simon O, Boudou A (2001) Simultaneous experimental study of direct and direct plus trophic contamination of the crayfish Astacus astacus by inorganic mercury and methylmercury. Environmental Toxicology and Chemistry 20:1206–1215
Simon O, Ribeyre F, Boudou A (2000) Comparative experimental study of cadmium and methylmercury trophic transfers between the asiatic clam Corbicula fluminea and the crayfish Astacus astacus. Archives of Environmental Contamination and Toxicology 38:317–326
Sánchez-López FJ, Gil Garcia MD, Sánchez Morito NP, Martínez Vidal JL (2003) Determination of heavy metals in crayfish by ICP-MS with a microwave-assisted digestion treatment. Ecotoxicol. Environ. Saf. 54:223–228
Scalici M, Chiesa S, Scuderi S, Celauro D, Gibertini G (2010) Population structure and dynamics of Procambarus clarkii (Girard, 1852) in a Mediterranean brackish wetland (Central Italy). Biol Inv 12:1415–1425
Stinson MD, Eaton DL (1983) Concentrations of lead, cadmium, mercury, and copper in the crayfish (Pacifasticus leniusculus) obtained from a lake receiving urban runoff. Archives of Environmental Contamination and Toxicology 12:693–700
Suárez-Serrano A, Alcaraz C, Ibáñez C, Trobajo R, Barata C (2010) Procambarus clarkii as a bioindicators of heavy metal pollution sources in the lower Ebro River and Delta. Ecotoxicol. Environ. Saf. 73:280–286
Tunca E, Üçüncü E, Kurtuluş B, Özkan AD, Atasagun S (2013) Accumulation trends of metals and a metalloid in the freshwater crayfish Astacus leptodactylus from Lake Yeniçağa (Turkey). Chem Ecol 29(8):754–769
UNICHIM Chemistry laboratory guides to method validation (2001) N. 179/1. Milan, UNICHIM
Varol M, Sünbül M (2018) Biomonitoring of trace metals in the Keban Dam Reservoir (Turkey) using mussels (Unio elongatulus eucirrus) and crayfish (Astacus leptodactylus). Biol Trace Elem Res 185(1):216–224
Vogt G (2002) Functional anatomy. In: Holdich DM (ed) Biology of Freshwater Crayfish Blackwell Science Ltd. United Kingdom, Oxford, pp 53–151
Wright DA, Welbourn PM, Martin AVM (1991) Inorganic and organic mercury uptake and loss by the crayfish Orconectes propinquus. Water, Air, and Soil Pollution 56:697–707
Acknowledgements
This work was supported by the Fondazione Cassa Risparmio Perugia, project code 82832.018.0425, Ricerca Scientifica e Tecnologica. We also thank MIUR (Ministero dell’Istruzione, dell’Università e della Ricerca) and the Università degli Studi di Perugia for financial support to the project AMIS, through the program “Dipartimenti di Eccellenza 2018-2022”.
Funding
This work was supported by the Fondazione Cassa Risparmio Perugia, project code 82832.018.0425, Ricerca Scientifica e Tecnologica. We also thank MIUR (Ministero dell’Istruzione, dell’Università e della Ricerca) and the Università degli Studi di Perugia for financial support to the project AMIS, through the program “Dipartimenti di Eccellenza 2018-2022”.
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The authors whose names appear on the submission made substantial contributions to the conception or design of the work, or the acquisition, analysis, or interpretation of data:
R. Selvaggi: Conceptualization, methodology, investigation, validation, data curation, writing—original draft preparation;
D. Cappelletti: Conceptualization, methodology, investigation, validation, data curation;
M. Pallottini, B. Caldaroni, A.J.M. Dörr, G. Magara, P. Gravina, L. Grispoldi, B. Cenci Goga, E. Goretti, G. La Porta, and A. C. Elia: Methodology, investigation;
D. Cappelletti and A. C. Elia: Supervision, Funding acquisition;
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Selvaggi, R., Pallottini, M., Caldaroni, B. et al. Sex and seasonal differences in metal accumulation of selected tissues in red swamp crayfish from Lake Trasimeno (Umbria, Italy). Environ Sci Pollut Res 30, 6234–6244 (2023). https://doi.org/10.1007/s11356-022-22582-z
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DOI: https://doi.org/10.1007/s11356-022-22582-z