The aim of this study was (i) to compare levels of accumulated heavy metals in the fox intestines with and without parasites. Moreover, our research also dealt with (ii) examination of the relationship between heavy metal content in fox intestines and between the presence of fox intestinal parasites. The intestines of 34 hunter-killed foxes were dissected to detect the occurrence of parasites. In 15 intestinal samples, parasitic intestinal helminths were found. Heavy metal content in small intestine tissue and in parasites was determined using atomic absorption spectrometry (AAS). The prevalence of parasites was significantly dependent on Cd content in the host's small intestine (p < 0.01). To conclude, the authors suggest that parasites are sensitive to Cd levels; their prevalence in the intestines of the fox host decreases to zero with increasing Cd content.

Department of Food Analysis and Chemistry Tomas Bata University in Zlin 760 01 Zlin Czech Republic

Department of Microelectronics Brno University of Technology 616 00 Brno Czech Republic

Department of Morphology Physiology and Animal Genetics Mendel University in Brno 61300 Brno Czech Republic

Infrastructure Department Mendel University in Brno 61300 Brno Czech Republic

Institute for Teacher Training Constantine the Philosopher University in Nitra 949 74 Nitra Slovakia

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Sures B. Environmental parasitology: Relevancy of parasites in monitoring environmental pollution. Trends Parasitol. 2004;20:170–177. doi: 10.1016/j.pt.2004.01.014. PubMed DOI

Poulin R. The functional importance of parasites in animal communities: Many roles at many levels? Int. J. Parasitol. 1999;29:903–914. doi: 10.1016/S0020-7519(99)00045-4. PubMed DOI

Marcogliese D.J. Food webs and the transmission of parasites to marine fish. Parasitology. 2002;124:83–99. doi: 10.1017/S003118200200149X. PubMed DOI

Khaleghzadeh-Ahangar H., Malek M., McKenzie K. The parasitic nematodes Hysterothylacium sp. type MB larvae as bioindicators of lead and cadmium: A comparative study of parasite and host tissues. Parasitology. 2011;138:1400–1405. doi: 10.1017/S0031182011000977. PubMed DOI

Yen Nhi T.T., Mohd Shazili N.A., Shaharom-Harrison F. Use of cestodes as indicator of heavy-metal pollution. Exp. Parasitol. 2013;133:75–79. doi: 10.1016/j.exppara.2012.10.014. PubMed DOI

Dural M., Genc E., Sangun M.K., Güner Ö. Accumulation of some heavy metals in Hysterothylacium aduncum (Nematoda) and its host sea bream, Sparus aurata (Sparidae) from North-Eastern Mediterranean Sea (Iskenderun Bay) Environ. Monit. Assess. 2011;174:147–155. doi: 10.1007/s10661-010-1445-0. PubMed DOI

Sures B., Grube K., Taraschewski H. Experimental studies on the lead accumulation in the cestode Hymenolepis diminuta and its final host, Rattus norvegicus. Ecotoxicology. 2002;11:365–368. doi: 10.1023/A:1020561406624. PubMed DOI

Sures B. Fish macroparasites as indicators of heavy metal pollution in river sites in Austria. Parasitology. 2003;126:61–69. PubMed

Tenora F., Barus V., Kracmar S., Dvoracek J. Concentrations of some heavy metals in Ligula intestinalis plerocercoids (Cestoda) and Philometraovata (Nematoda) compared to some their hosts (Osteichthyes) Helminthologia. 2000;37:15–22.

Sures B. Accumulation of heavy metals by intestinal helminths in fish: An overview and perspective. Parasitology. 2003;126:S53–S60. doi: 10.1017/S003118200300372X. PubMed DOI

Lafferty K.D. Environmental parasitology: What can parasites tell us about human impacts on the environment? Parasitol. Today. 1997;13:251–255. doi: 10.1016/S0169-4758(97)01072-7. PubMed DOI

Barus V., Tenora V., Sumbera R. Relative concentrations of four heavy metals in the parasites Protospirura muricola (Nematoda) and Inermicapsifer arvicanthidis (Cestoda) in their definitive host silvery mole-rat (Heliophobius argenteocinereus: Rodentia) Helminthologia. 2003;40:227–232.

Azmat R., Fayyaz S., Kazi N., Mahmood S., Uddin F. Natural bioremediation of heavy metals through Nematode parasite of fish. Biotechnology. 2008;7:139–143. doi: 10.3923/biotech.2008.139.143. DOI

Höss S., Schlottmann K., Traunspurger W. Toxicity of ingested cadmium to the nematode Caenorhabditis elegans. Environ. Sci. Technol. 2011;45:10219–10225. doi: 10.1021/es2027136. PubMed DOI

Meloun M., Hill M., Militký J., Kupka K. Analysis of large and small samples of biochemical and clinical data. Clin. Chem. Lab. Med. 2001;39:53–61. doi: 10.1515/CCLM.2001.013. PubMed DOI

Sures B. Competition for minerals between Acanthocephalus lucii and its definitive host perch (Perca fluviatilis) Int. J. Parasitol. 2002;32:1117–1122. doi: 10.1016/S0020-7519(02)00083-8. PubMed DOI

Torres J., Eira C., Miquel J., Foronda P., Feliu C. Cadmium and lead concentrations in Moniliformis moniliformis (Acanthocephala) and Rodentolepis microstoma (Cestoda), and in their definitive hosts, Rattus rattus and Mus domesticus in El Hierro (Canary Archipelago, Spain) Acta Parasitol. 2011;56:320–324. doi: 10.2478/s11686-011-0064-4. DOI

Scheef G., Sures B., Taraschewski H. Cadmium accumulation in Moniliformis moniliformis (Acanthocephala) from experimentally infected rats. Parasitol. Res. 2000;86:688–691. doi: 10.1007/PL00008553. PubMed DOI

Sures B., Franken M., Taraschewski H. Element concentrations in the archiacanthocephalan Macracanthorhynchus hirudinaceus compared with those in the porcine definitive host from a slaughterhouse in La Paz, Bolivia. Int. J. Parasitol. 2000;30:1071–1076. doi: 10.1016/S0020-7519(00)00094-1. PubMed DOI

Jankovská I., Lukešová D., Száková J., Langrová I., Vadlejcj J., Čadková Z., Válek P., Petrtýl M., Kudrnáčová M. Competition for minerals (Zn, Mn, Fe, Cu) and Cd between sheep tapeworm (Moniezia expansa) and its definitive host sheep (Ovis aries) Helminthologia. 2011;48:237–243. doi: 10.2478/s11687-011-0033-3. DOI

Jankovská I., Miholová D., Petrtýl M., Romočuský Š., Kalous L., Vadlejcj J., Čadková Z., Langrová I. Intestinal parasite Acanthocephalus lucii (Acanthocephala) from European perch (Perca fluviatilis) as a bioindicator for lead pollution in the stream “Jevanský potok” near Prague, Czech Republic. Bull. Environ. Contam. Toxicol. 2011;86:342–346. doi: 10.1007/s00128-011-0210-6. PubMed DOI

Jankovská I., Miholová D., Bejček V., Vadlejch J., Šulc M., Száková J., Langrová I. Influence of parasitism on trace element contents in tissues of Red Fox (Vulpes vulpes) and its parasites Mesocestoides spp. (Cestoda) and Toxascaris leonina (Nematoda) Arch. Environ. Contam. Toxicol. 2010;58:469–477. doi: 10.1007/s00244-009-9355-2. PubMed DOI

European Commission Commission Regulation (EU) No 488/2014 of 12 May 2014 amending Regulation (EC) No 1881/2006 as regards maximum levels of cadmium in foodstuffs Text with EEA relevance. OJEU. 2014;L138:75–79.

Tsukada H. A division between foraging range and territory related to food distribution in the red fox. J. Ethol. 1997;15:27–37. doi: 10.1007/BF02767323. DOI

Sures B., Reimann N. Analysis of trace metals in the Antarctic host-parasite system Notothenia coriiceps and Aspersentis megarhynchus (Acanthocephala) caught at King George Island, South Shetland Islands. Polar Biol. 2003;26:680–686. doi: 10.1007/s00300-003-0538-4. DOI

Retief N.R., Avenant-Oldewage A., du Preez H.H. The use of cestode parasites from the largemouth yellowfish, Labeobarbus kimberleyensis (Gilchrist and Thompson, 1913) in the Vaal Dam, South Africa as indicators of heavy metal bioaccumulation. Phys. Chem. Earth. 2006;31:840–847. doi: 10.1016/j.pce.2006.08.004. DOI

Oyoo-Okoth E., Wim A., Osano O., Kraak M.H., Ngure V., Makwali J., Orina P.S. Use of the fish endoparasite Ligula intestinalis (L., 1758) in an intermediate cyprinid host (Rastreneobola argentea) for biomonitoring heavy metal contamination in Lake Victoria, Kenya. Lakes Reserv. Res. Manag. 2010;15:63–73. doi: 10.1111/j.1440-1770.2010.00423.x. DOI

Filistowicz A., Dobrzaňski Z., Przysiecki P., Nowicki S., Filistowicz A. Concentration of heavy metals in hair and skin of silver and red foxes (Vulpes vulpes) Environ. Monit. Assess. 2011;182:477–484. doi: 10.1007/s10661-011-1891-3. PubMed DOI

Dobrzaňski Z., Filistowicz A., Przysiecki P., Filistowicz A., Nowicki S., Walkowiak K., Czyz K. Mercury bioaccumulation in hair and skin of arctic foxes (Vulpes lagopus) and silver foxes (Vulpes vulpes) in rural and urbanised region. Czech. J. Anim. Sci. 2014;59:480–487. doi: 10.17221/7711-CJAS. DOI

Chand N., Tyagi S., Prasad R., Sirohi A.S., Srivastava N., Kumar S., Yadav B.P.S. Heavy metal and trace mineral in blood and hair of cattle reared around industrial effluent contaminated area. J. Anim. Res. 2017;7:685–689. doi: 10.5958/2277-940X.2017.00105.X. DOI

Popham J.D., Webster J.M. Cadmium toxicity in the free-living nematode, Caenorhabditis elegans. Environ. Res. 1979;20:183–191. doi: 10.1016/0013-9351(79)90096-3. PubMed DOI

Phillips C.J.C., Chiy P.C., Zachou E. Effects of cadmium in herbage on the apparent absorption of elements by sheep in comparison with inorganic cadmium added to their diet. Environ. Res. 2005;99:224–234. doi: 10.1016/j.envres.2004.12.013. PubMed DOI

Rahimzadeh M.R., Rahimzadeh M.R., Kazemi S., Moghadamnia A. Cadmium toxicity and treatment: An update. Caspian J. Intern. Med. 2017;8:135–145. PubMed PMC

Vig K., Megharaj M., Sethunathan N., Naidu R. Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: A review. Adv. Environ. Res. 2003;8:121–135. doi: 10.1016/S1093-0191(02)00135-1. DOI

Loppi S., Frati L., Paoli L., Bigagli V., Rossetti C., Bruscoli C., Corsini A. Biodiversity of epiphytic lichens and heavy metal contents of Flavoparmelia caperata thalli as indicators of temporal variations of air pollution in the town of Montecatini Terme (central Italy) Sci. Total Environ. 2004;326:113–122. doi: 10.1016/j.scitotenv.2003.12.003. PubMed DOI

Li J.-T., Duan H.-N., Li S.-P., Kuang J.-L., Zeng Y., Shu W.-S. Cadmium pollution triggers a positive biodiversity–productivity relationship: Evidence from a laboratory microcosm 4experiment. Sci. Total Environ. 2010;47:890–898. doi: 10.1111/j.1365-2664.2010.01818.x. DOI

Hursky O., Pietrock M. Chemical contaminants and parasites: Assessment of human health risks associated with consumption of whitefish (Coregonus clupeaformis) from two boreal lakes in northern Saskatchewan, Canada. Sci. Total Environ. 2012;424:97–103. doi: 10.1016/j.scitotenv.2012.02.071. PubMed DOI

Zmudzki S., Laskowski R. Biodiversity and structure of spider communities along a metal pollution gradient. Ecotoxicology. 2012;21:1523–1532. doi: 10.1007/s10646-012-0906-3. PubMed DOI PMC

Kirin D., Boyanov B., Ilieva N. Biodiversity and heavy metal pollutions in freshwater ecosystems in border areas from Tunja river. Zaštita Mater. 2013;54:153–160.

Chunhabundit R. Cadmium exposure and potential health risk from foods in contaminated area, Thailand. Toxicol. Res. 2016;32:65–72. doi: 10.5487/TR.2016.32.1.065. PubMed DOI PMC

Godt J., Scheidig F., Grosse-Siestrup C., Esche V., Brandenburg P., Groneberg D.A. The toxicity of cadmium and resulting hazards for human health. J. Occup. Med. Toxicol. 2006;1:22. doi: 10.1186/1745-6673-1-22. PubMed DOI PMC

Metcheva R., Yurukova L., Bezrukov V., Beltcheva M., Yankov Y., Dimitrov K. Trace and toxic elements accumulation in food chain representatives at Livingston Island (Antarctica) Int. J. Biol. 2010;2:155–161. doi: 10.5539/ijb.v2n1p155. DOI

Ruprich J., Drápal J., Řehůřková I., Šťastný K., Kalivodová M. Cattle tissues as a source of cadmium for consumers. Acta Vet. Brno. 2015;84:289–295. doi: 10.2754/avb201584030289. DOI

Sriprachote A., Kanyawongha P., Pantuwan G., Ochiai K., Matoh T. Evaluation of Thai rice cultivars with low-grain cadmium. Soil Sci. Plant Nutr. 2012;58:568–572. doi: 10.1080/00380768.2012.715070. DOI