Skip to main content

Advertisement

SpringerLink
Log in

Morphological abnormalities in fish parasites: a potential tool for biomonitoring natural contaminants?

  • Fish Parasitology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

A comparative study on the strobilar morphology of the tapeworm Proteocephalus percae (Müller, 1780) (Cestoda), a parasite of the perch Perca fluviatilis (L.), showed a high percentage of abnormally developed parasite individuals. The evaluation of biological samples showed seven types of morphological abnormalities, mostly related to reproductive organs of the model tapeworm species. The most commonly identified deformity was an incomplete segmentation of the strobila. A malformed ovary, which is a structural anomaly linked with proglottization and maturation of the strobila, was also shown to be rather frequent. Offish hosts (P. percae) were collected from two localities with different levels of heavy metal pollution, the highly contaminated water reservoir Ružín and a control locality, the water reservoir Palcmanská Maša, which belongs to the European network of protected areas in Slovakia. Tapeworm abnormalities occurred more frequently in individuals from the contaminated environment (29.9%) compared with individuals from the control site (4.9%). The concentrations of heavy metals found in the parasites and their fish hosts from the heavily polluted reservoir support our assumption that the occurrence of abnormalities could be linked with the destructive effect of toxic substances. The present study also demonstrates that the enumeration of body deformities exceeding the common level of phenotypic variability of particular parasitic species could potentially be used as an indicator of environmental problems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Al Quraishy S, Abdel-Gaber R, Alajmi R, Dkhil MA, Al Jawher M, Morsy K (2019) Morphological and molecular appraisal of cyclophyllidean cestoda parasite Raillietina saudiae sp. nov. infecting the domestic pigeon Columba livia domestica and its role as a bio-indicator for environmental quality. Parasitol Int 71:59–72

    Article  PubMed  Google Scholar 

  • Amin OM (1989) Abnormalities in some helminth-parasites of fish. Trans Am Microsc Soc 108:27–39

    Article  Google Scholar 

  • Amoatey P, Baawain MS (2019) Effects of pollution on freshwater aquatic organisms. Water Environ Res 91:1272–1287

    Article  CAS  PubMed  Google Scholar 

  • Anikieva LV (1992) Morphological variability of the population of Proteocephalus percae (Cestoda: Proteocephalidea) from lake Rindozero. Parazitologiya 26:389–395 (In Russian)

    CAS  Google Scholar 

  • Bigazzi M, Selvi F (2003) Chromosome variation in Anatolian species of Nonea Medik. (Boraginaceae), with special reference to endemics and N-persica. Caryologia 56:509–5019

    Article  Google Scholar 

  • Brázová T, Torres J, Eira C, Hanzelová V, Miklisová D, Šalamún P (2012) Perch and its parasites as heavy metal biomonitors in a freshwater environment: the case study of the Ružín water reservoir, Slovakia. Sensors 12:3068–3081

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brázová T, Hanzelová V, Miklisová D, Šalamún P, Vidal-Martínez VM (2015) Host-parasite relationships as determinants of heavy metal concentrations in perch (Perca fluviatilis) and its intestinal parasite. Ecotoxicol Environ Saf 122:551–556

    Article  PubMed  CAS  Google Scholar 

  • Chapman JM, Marcogliese DJ, Suski CD, Cooke SJ (2015) Variation in parasite communities and health indices of juvenile Lepomis gibbosus across a gradient of watershed land-use and habitat. Ecol Indic 57:564–572

    Article  Google Scholar 

  • Diamare V (1893) Il genere Dipylidium Lt. Atti Accad Sci Neapoli II 167:1–31

    Google Scholar 

  • Dražil T, Šefferová-Stanová V (2008) Conservation of habitat diversity in Slovenský raj National Park. [online]. https://ec.europa.eu/environment/life/project/Projects/index.cfm

  • Dušek L, Gelnar M, Šebelová Š (1998) Biodiversity of parasites in a freshwater environment with respect to pollution: metazoan parasites of chub (Leuciscus cephalus L.) as a model for statistical evaluation. J Parasitol 28:1555–1571

    Google Scholar 

  • Falasco E, Bona F, Badino G, Hoffmann L, Ector L (2009) Diatom teratological forms and environmental alterations: a review. Hydrobiologia 623:1–35

    Article  CAS  Google Scholar 

  • Falis M, Krupicer I, Legáth J, Pitoňák V (2013) The effects of heavy metals and pesticides on survival of miracidia stage of Fasciola hepatica. Helminthologia 50:287–290

    Article  CAS  Google Scholar 

  • Findoráková L, Šestinová O, Danková Z, Findorák R, Hančuľák J (2015) Thermal and spectral characterization of bottom sediment from the water reservoir Ružín no.1 in eastern Slovakia. J Soils Sediments 15:1781–1788

    Article  CAS  Google Scholar 

  • Freeman RS (1960) Another hymenolepid with great morphological variation, Hymenolepis bennetti n. sp. (Cestoda) from Napaeozalpus insignis algonquinensis Price. Can J Zool 38:737–743

    Article  Google Scholar 

  • Gelnar M, Šebelová Š, Dušek L, Koubková B, Jurajda P, Zahrádková S (1997) Biodiversity of parasites in freshwater environment in relation to pollution. Parasitologia 39:189–199

    CAS  Google Scholar 

  • Giagia E, Soldatović Savić I, Zimonjić D (1985) Karyotype study of the genus Apodemus (Kaup, 1829) populations from the Balkan peninsula. Acta Vet (Beograd) 35:289–298

    Google Scholar 

  • Hanzelová V, Šnábel V, Kráľová I, Scholz T, D’Amelio S (1999) Genetic and morphological variability in cestodes of the genus Proteocephalus: geographic variation in Proteocephalus percae populations. Can J Zool 77:1450–1458

  • Honigberg B (1944) A morphological abnormality in the cestode Dipylidium caninum. Trans Am Microsc Soc 63:342–344

    Article  Google Scholar 

  • Hucko P, Roško V, Babej L, Lenártová D (2017) Proceedings from VIII. Conference with international participation. Sediments of water flows and dams. Occurrence of trace elements in sediments of water reservoirs of Slovakia – the results of monitoring from 2016. Bratislava, 17. – 18. May 2017, pp 207–21 (In Slovak)

  • Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182

    Article  PubMed  Google Scholar 

  • Jezierska B, Lugowska K, Witeska M (2009) The effects of heavy metals on embryonic development of fish (a review). Fish Physiol Biochem 35:625–640

    Article  CAS  PubMed  Google Scholar 

  • Kertész V, Fáncsi T (2003) Adverse effects of (surface water pollutants) Cd, Cr and Pb on the embryogenesis of the mallard. Aquat Toxicol 65:425–433

    Article  PubMed  CAS  Google Scholar 

  • Khalil LF, Jones A, Bray RA (1994) Keys to the cestode parasites of vertebrates. CABI publishing, Wallingford, United Kingdom, pp 1–768

    Google Scholar 

  • Koga G, Iwata S (1976) On the abnormal proglottids of broad tapeworm Diphyllobothrium latum (L. 1758) with a single or double set of reproductive organs. J Kurume Med Assoc 39:475–505 (In Japanese)

    Google Scholar 

  • Leskovjanská A, Viceníková A, Dražil T (2006) The habitats of EU importance in the Slovenský Raj National Park. State Nature Conservancy of the Slovak Republic – Administration of the Slovenský Raj National Park, DAPHNE – Institute of Applied Ecology, pp. 1–37

  • Leuckart CGFR (1886) Die menschlichen Parasiten und die von ihnen herrührenden Krankheiten. University of Oxford, Winter, Bodleian Libraries, pp 1–766

    Google Scholar 

  • Linzey DW, Burroughs J, Hudson L, Marini M, Robertson J, Nagarcatti M, Bacon JP, Nagarcatti PS (2003) Role of environmental pollutants on immune functions, parasitic infections and limb malformations in marine toads and whistling frogs from Bermuda. Int J Environ Health Res 13:125–148

    Article  CAS  PubMed  Google Scholar 

  • Mackiewicz JS (1978) Duplication of reproductive systems in monozoic cestodes (Caryophyllidea). In proceedings of the helminthological Society of Washington. ISSN: 0018-01301978, 45:28–33

  • Macko JK (1968) About some morphological peculiarities and abnormalities in the species of the genus Diorchis Clerc, 1903 (Cestoda) from Fulica atra. Biologia 23:148–153

    CAS  PubMed  Google Scholar 

  • Martinez EA, Moore BC, Schaumloffel J, Dasgupta N (2002) The potential association between mental deformities and trace elements in Chironomidae (diptera) taken from a heavy metal contaminated river. Arch Environ Contam Toxicol 42:286–291

    Article  CAS  PubMed  Google Scholar 

  • Miller JR, Lechler PJ, Hudson-Edwards KA, Macklin MG (2002) Lead isotopic fingerprinting of heavy metal contamination, Rio Pilcomayo, Bolivia. In: Allan R, Horowitz AJ, and Miller JR (eds) Metal mining in the environment. Special Issue. Geochem Explor, Environ Anal 2:225–233

    Article  Google Scholar 

  • Monroy-Vilchis O, Lizzouli Parra-Lopez L, Beltran-Leon T, Lugo JA, Balderas A, Zarco-Gonzalez MM (2015) Morphological abnormalities in anurans from central Mexico: a case study. Herpetozoa 27:115–121

    Google Scholar 

  • Nachev M, Sures B (2015) Environmental parasitology: parasites as accumulation bioindicators in the marine environment. J Sea Res 113:45–50

    Article  Google Scholar 

  • Nhi TTY, Mohd Shazili NA, Shaharom-Harrison F (2013) Use of cestodes as indicator of heavy-metal pollution. Exp Parasitol 133:75–79

    Article  CAS  Google Scholar 

  • Olson PD, Littlewood DTJ, Bray RA, Mariaux J (2001) Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Mol Phylogenet Evol 18:443–467

    Article  CAS  Google Scholar 

  • Oros M, Scholz T, Hanzelová V, Mackiewicz JS (2010) Scolex morphology of monozoic cestodes (Caryophyllidea) from the Palearctic region: an useful tool for species identification. Folia Parasitol 57:37–46

    Article  Google Scholar 

  • Oros M, Brabec J, Kuchta R, Choudhury A, Scholz T (2016) A synoptic review of the Promonobothrium Mackiewicz, 1968 (Cestoda: Caryophyllidea), parasites of suckers (Catostomidae) in North America, with description of two new species. Folia Parasitol 63:1–14

    Article  CAS  Google Scholar 

  • Oyoo-Okoth E, Admiraal W, Osano O, Hoitinga L, Kraak MH (2010) Metal specific partitioning in a parasite-host assemblage of the cestode ligula intestinalis and the cyprinid fish Rastrineobola argentea. Sci Total Environ 408:1557–1562

    Article  CAS  PubMed  Google Scholar 

  • Pandey LK, Kumar D, Yadav A, Rai J, Gaur JP (2014) Morphological abnormalities in periphytic diatoms as a tool for biomonitoring of heavy metal pollution in a river. Ecol Indic 36:272–279

    Article  CAS  Google Scholar 

  • Patrick I, Tualla B, Bitacura J (2016) Effects of cadmium and zinc on the gamete viability, fertilization, and embryonic development of Tripneustes gratilla (Linnaeus). Scientifica, Article ID 8175213:1–10. https://doi.org/10.1155/2016/8175213

    Article  CAS  Google Scholar 

  • Pečínková M, Matějusová I, Koubková B, Gelnar M (2005) Classification and occurrence of abnormally developed Paradiplozoon homoion (Monogenea, Diplozoinae) parasitizing gudgeon Gobio gobio. Dis Aquat Org 64:63–68

    Article  Google Scholar 

  • Pečínková M, Vøllestad LA, Koubková B, Huml J, Jurajda P, Gelnar M (2007) The relationship between developmental instability of gudgeon Gobio gobio and abundance or morphology of its ectoparasite Paradiplozoon homoion (Monogenea). J Fish Biol 71:1358–1370

    Article  Google Scholar 

  • Pedlar RM, Ptashynski MD, Evans R, Klaverkamp JF (2002) Toxicological effects of dietary arsenic exposure in lake whitefish (Coregonus clupeaformis). Aquat Toxicol 57:167–189

    Article  CAS  PubMed  Google Scholar 

  • Pourang N (1995) Heavy-metal bioaccumulation in different tissues of 2 fish species with regards to their feeding-habits and trophic levels. Environ Monit Assess 35:207–219

    Article  CAS  PubMed  Google Scholar 

  • Retief N-R, Avenant-Oldewage A, Du Preez H (2006) 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 31:840–847

    Article  Google Scholar 

  • Rice KM, Walker EM, Wu M, Gillette C, Blough ER (2014) Environmental mercury and its toxic effects. J Prev Med Public Health 47:74–83

    Article  PubMed  PubMed Central  Google Scholar 

  • Sagerup K, Savinov V, Savinov T, Kuklin V, Muir D, Gabrielsen G (2009) Persistent organic pollutants, heavy metals and parasites in glaucous gull (Larus hyperboreus) on Spitsbergen. Environ Pollut 157:2282–2290

    Article  CAS  PubMed  Google Scholar 

  • Scholz T, Hanzelová V (1998) Tapeworms of the genus Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae), parasites of fishes in Europe. Studie AV ČR, No. 2/98, Academia, Praha, 119 pp.

  • Šebelová Š, Kuperman B, Gelnar M (2002) Abnormalities of the attachment clamps of representatives of the family Diplozoidae. J Helminthol 76:249–259

    Article  PubMed  Google Scholar 

  • Singh J, Kalamdhad AS (2011) Effects of heavy metals on soil, Plants, Human Health and Aquatic Life. Int J Res Chem Environ 1:15–21

    Google Scholar 

  • Špakulová M, Cassanova JC (2004) Current knowledge on B chromosomes in natural populations of helminth parasites: a review. Cytogenet Genome Res 106:222–229

    Article  PubMed  Google Scholar 

  • Špakulová M, Kráľová-Hromadová I, Dudiňák V, Reddy PV (2002) Karyotype of Acanthocephalus lucii: the first record of supernumerary chromosomes in thorny-headed worms. Parasitol Res 88:778–780

    Article  PubMed  Google Scholar 

  • Sun PL, Hawkins WE, Overstreet RM, Brown-Peterson NJ (2009) Morphological deformities as biomarkers in fish from contaminated rivers in Taiwan. Int J Environ Res Public Health 6:2307–2331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sures B (2001) The use of fish parasites as bioindicators of heavy metals in aquatic ecosystems: a review. Aquat Ecol 35:245–255

    Article  CAS  Google Scholar 

  • Sures B (2003) Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126:53–60

    Article  CAS  Google Scholar 

  • Sures B (2004) Environmental Parasitology: relevancy of parasites in monitoring environmental pollution. Environ Toxicol Chem 20:170–177

    CAS  Google Scholar 

  • Sures B, Steiner W, Rydlo M, Taraschewski H (1999) Concentrations of 17 elements in the Zebra mussel (Dreissena polymorpha), in different tissues of perch (Perca fluviatilis), and in perch intestinal parasites (Acanthocephalus lucii) from the subalpine lake Mondsee, Austria. Environ Toxicol Chem 18:2574–2579

    Article  CAS  Google Scholar 

  • Sures B, Nachev M, Selbach C, Marcogliese DJ (2017) Parasite responses to pollution: what we know and where we go in ‘Environmental Parasitology’. Parasit Vectors 10:65

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Taraschewski H (2000) Host-parasite interactions in Acanthocephala – a morphological approach. Adv Parasitol 46:1–179

    Article  CAS  PubMed  Google Scholar 

  • Tenora F, Baruš V, Kráčmar S, Dvořáček J (2000) Concentrations of some heavy metals in Ligula intestinalis plerocercoids (Cestoda) and Philometra ovata (Nematoda) compared to some of their hosts (Osteichthyes). Helminthologia 37:15–18

    CAS  Google Scholar 

  • Tenora F, Koubková B, Feliu C (2002) Redescription of Andrya cuniculi (Blanchard, 1891) (Cestoda: Anoplocephalidae), a parasite of Oryctolagus cuniculus (Lagomorpha) in Spain. Folia Parasitol 49:50–54

    Article  Google Scholar 

  • Turčeková Ľ, Hanzelová V, Špakulová M (2002) Concentrations of heavy metals in perch and its endoparasites in the polluted water reservoir in eastern Slovakia. Helminthologia 39:23–28

    Google Scholar 

  • Vidal-Martínez VM, Pech D, Sures B, Purucker ST, Poulin R (2010) Can parasites really reveal environmental impact? Trends Parasitol 26:44–50

    Article  PubMed  Google Scholar 

  • Yanagida T, Matsuoka H, Kanai T, Nakao T, Ito A (2010) Anomalous segmentation of Diphyllobothrium nihonkaiense. Parasitol Int 59:268–270

    Article  CAS  PubMed  Google Scholar 

  • Zima J, Ieradi LA, Allegra F, Sartoretti A, Wlosoková E, Cristaldi M (1999) Frequencies of B chromosomes in Apodemus flavicolis are not directly related to mutagenic environmental effects. Folia Zool 48:115–119

    Google Scholar 

Download references

Acknowledgements

Thanks are due to Ing. Stanislav Géci for assisting with the fish collection.

Funding

This work was supported by research grants of the Slovak Research and Development Agency, project no. APVV-18-0467 and Grant Agency of the Ministry of Education of the Slovak Republic and Slovak Academy of Sciences (VEGA), project no. 2/0126/20.

Author information

Authors and Affiliations

  1. Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 04001, Košice, Slovakia

    Tímea Brázová, Martina Orosová, Peter Šalamún & Vladimíra Hanzelová

Authors
  1. Tímea Brázová
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martina Orosová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter Šalamún
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vladimíra Hanzelová
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martina Orosová.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Section Editor: Stephen A. Bullard

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brázová, T., Orosová, M., Šalamún, P. et al. Morphological abnormalities in fish parasites: a potential tool for biomonitoring natural contaminants?. Parasitol Res 119, 3297–3304 (2020). https://doi.org/10.1007/s00436-020-06860-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-06860-8

Keywords

Search

Navigation