Skip to main content
Log in

Energy dispersive X-Ray microanalysis in conjunction with scanning electron micrography to establish nematodes as bioindicators in marine fish environment

  • Original Article
  • Published:
Journal of Parasitic Diseases Aims and scope Submit manuscript

Abstract

Energy Dispersive X-Ray Microanalysis has been used as the non-invasive technique on Indian helminthes to explore the role of nematode parasites as bioindicators in the marine ecosystem of Central West coast of India for the first time. The accumulation of sulphur and iron were analysed from a raphidascaridoid roundworm, Rostellascaris spinicaudatum (Malhotra and Anas) parasitizing marine catfish, Arius maculatus from the Central West coast of India at Goa. Quantitatively, the cuticle on oral armature comprised as much as ten times more sulphur than iron content in the roundworm under study. However, only carbon and oxygen were detected over caudal papillae, where no metals or other elements were recorded. The utility of a raphidascaridoid nematode to act as a bioindicator, that had the potential of a bioaccumulator effector, is highlighted.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akinsanya B, Kuton MP (2016a) Bioaccumulation of heavy metals and parasitic fauna in Synodontis clarias (Linnaeus, 1758) and Chrysichthys nigrodigitatus (Lacepede, 1803) from Lekki Lagoon, Lagos, Nigeria. Asian Pac J Trop Dis 6:615–621. https://doi.org/10.1016/S2222-1808(16)61096-4

    Article  Google Scholar 

  • Akinsanya B, Kuton MP (2016b) Parasitic diseases and heavy metal analysis in Parachanna obscura (Gunther 1861) and Clarias gariepinus (Burchell 1901) from Epe Lagoon, Lagos, Nigeria. Asian Pac J Trop Dis 6:685–690. https://doi.org/10.1016/S2222-1808(16)61110-6

    Article  Google Scholar 

  • Antoniou M, Tselentis Y (1993) Studies on Echinococcus granulossus using the scanning electron microscope II. The Hooks. Parasitol Res 79:543–546

    Article  CAS  Google Scholar 

  • Azmat R, Fayyaz S, Kazi N, Mahmood SJ, Uddin F (2008) Natural bioremediation of heavy metal through nematode parasite of fish. Biotechnology 7(1):139–143

    Article  CAS  Google Scholar 

  • Baby J, Raj JS, Biby ET, Shankarganesh P, Jeevitha M.V, Ajisha, S.U., Rajan SS (2010) Toxic effect of heavy metals on aquatic environment. Intern. J Biol Chem Sci 4(4): 939–952. ISSN 1991–8631.

  • Bird AF, Bird J (1991) The Structure of Nematodes. New York: Academic 2.

  • Colovic MB, Vasic VM, Djuric DM, Krstic DZ (2018) Sulphur-containing amino acids: Protective role against free radicals and heavy metals. Curr Med Chem 25(3):324–335. https://doi.org/10.2174/0929867324666170609075434

    Article  CAS  PubMed  Google Scholar 

  • Dural M, Genc E, Sangun MK, Güner Ö (2011) 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 174(1–4):147–155. https://doi.org/10.1007/s10661-010-1445-0

    Article  CAS  PubMed  Google Scholar 

  • Fairweather- Tait SJ, Fox TE, Wharf SG, Ghani NA (1992) A preliminary study of the bioavailability of iron- and zinc- glycine chelates. Food Add Contam 9:97–101

    Article  CAS  Google Scholar 

  • Foden CS, Islam S, Fernandez-Garcia C, Maugeri LM, Sheppard TD, Powner MW (2020) Probiotic synthesis of cysteine peptides that catalyze peptide ligation in neutral water. PLoS ONE 370(6518):865–869. https://doi.org/10.1126/science.abd5680

    Article  CAS  Google Scholar 

  • Galli P, Crosa G, Occhipinti-Ambrogi A (1998) Heavy metals concentrations in acanthocephalan parasites compared to their fish host. Chemosphere 37:2983–2988

    Article  CAS  Google Scholar 

  • Geetanjali M, Sandeep K, Malhotra A, Ansari Z, Chatterjee A (2002) The role of nematodes as bioindicators in marine and freshwater habitats. Current Sci 82:505–507

    Google Scholar 

  • Gunkel G (1994) Bioindikation in aquatischen Ökosystemen. Fischer Verlag, Jena

    Google Scholar 

  • Heckmann RA (1996) Energy dispersive x-ray microanalysis in conjunction with electron optics, a tool for analyzing aquatic animal diseases and deaths. Micro Anal 17:27–29

    Google Scholar 

  • Heckmann RA, Amin OM, Standing MD (2007) Chemical analysis of metals in Acanthocephalans using Energy Dispersive X-Ray Analysis (EDXA) in conjunction with a scanning electron microscope (SEM). Comp Parasitol 74(2):388–391

    Article  Google Scholar 

  • Hofer R, Lackner R (1995) Fischtoxikologie - Theorie und Praxis. Fischer Verlag, Jena

    Google Scholar 

  • Khalaj V, Eslami H, Azizi M, Nuria R-G, Bromley M (2007) Efficient Downregulation of alb1 Gene 284 using an AMA1-Based Episomal Expression of RNAi Construct in Aspergillus fumigates. Microbiol Let 285(2):250–254

    Article  Google Scholar 

  • Köck G (1996) Die toxische Wirkung von Schwermetallen auf Fische. In: Steinberg C, Bernhardt H and Klapper H (eds) Handb Angew Limnol pp 1–167. Ecomed Verlagsgesellschaft, Landsberg am Lech.

  • Le ITY, Zimmermann S, Sures B (2016) How does the metallothionein in induction in bivalves meet the criteria for biomarkers of metal exposure. Environ Pollut 212:257–268

    Article  CAS  Google Scholar 

  • Leite LA, Pedro NH, de Azevedo RK, Kinoshita A, Gennari RF, Watanabe S, Abdallah VD (2017) Contracaecum sp. parasitizing Acestrorhynchus lacustris as a bioindicator for metal pollution in the Batalha River, southeast Brazil. Sci Total Environ 575:836–840. https://doi.org/10.1016/j.scitotenv.2016.09.132

    Article  CAS  PubMed  Google Scholar 

  • Malhotra Sandeep K, Anas M (2001) A unique piscine ascaridid Rostellascaris spinicaudatum gen et sp n with key to genera of subfamily Ascaridinae. In: Professor V.N. Capoor Commem Vol, GBP Univ Agric Technol, Pantnagar 20–25, 1–3

  • Morsy K, Bashtar A-R, Abdel-Ghaffar F, Mehlhorn H, Al Quraishy S, El-Mahdi M, Al-Ghamdi A, Mostafa N (2012) First record of anisakid juveniles (Nematoda) in the European seabass Dicentrarchus labrax (family: Moronidae), and their role as bio-indicators of heavy metal pollution. Parasitol Res 110:1131–1138. https://doi.org/10.1007/s00436-011-2600-4

    Article  PubMed  Google Scholar 

  • Nachev M, Schertzinger G, Sures B (2013) Comparison of the metal accumulation capacity between the acanthocephalan Pomphorhynchus laevis and larval nematodes of the genus Eustrongylides sp. infecting barbel (Barbus barbus). Parasit Vect 6:21. https://doi.org/10.1186/1756-3305-6-21

    Article  CAS  Google Scholar 

  • Nies DH (1999) Microbial heavy metal resistance. Appl Microbiol Biotechnol 51:730–750

    Article  CAS  Google Scholar 

  • Nozaki T, Asai T, Kobayashi S, Ikegami F, Noji M, Saito K, Takeuchi T (1998) Molecular cloning and characterization of the genes encoding two isoforms of cysteine synthase in the enteric protozoan parasite Entamoeba histolytica. Mol Biochem Parasitol 97(1–2):33–44

    Article  CAS  Google Scholar 

  • Oscar R, Roberto C, Maria BG, Marta D, Paolo L (2003) Trace element concentrations in freshwater mussels and macrophytes as related to those in their environment. J Limnol 62(1):61–67. https://doi.org/10.4081/jlimnol.2003.61

    Article  Google Scholar 

  • Pineda D, Ashamead H DeWa (2001) The absorption and metabolism 01 iron amino acid chelate. Archivos Latinoamericanos de Nutricion ver. Imp. ISSN0004–0622. ALANv.51.1supl.1 Caracasmar.:19pp.

  • Radwan NA, Abou Shafeey HE, Khalil AI (2012) Chemical characterization of tegumental spines of four digenean species using energy dispersive X-ray microanalysis (EDXA). Internat Jour Parasitol Res ISSN: 3250975–3702 & E-ISSN: 0975- 9182, 4(2), 100–105.

  • Stedman JK (2001) Stedmans medical dictionary for the health professions, 4th edn. Lippincott, Williams and Wilkins, Philadelphia, p 1597

    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. Parasitol 126(Suppl.):S53–S60

    Article  CAS  Google Scholar 

  • Sures B (2004) Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Tr Parasitol 20:170–177

    Article  CAS  Google Scholar 

  • Sures B, Siddall R (1999) Pomphorhynchus laevis: the intestinal acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus). Exp Parasitol 93:66–72

    Article  CAS  Google Scholar 

  • Sures B, Siddall R, Taraschewski H (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitol Today 15:16–21

    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 Vect 10:57

    Article  Google Scholar 

  • Szefer P, Rokicki J, Frelek K, Skora K, Malinga M (1998) Bioaccumulation of selected trace elements in lung nematodes, Pseudalius inflexus, of harbor porpoise (Phocoena phocoena) in a Polish zone of Baltic Sea. Sci Tot Environ 220:19–24. https://doi.org/10.1016/S0048-9697(98)00221-6

    Article  CAS  Google Scholar 

  • Tellez M, Merchant M (2015) Biomonitoring heavy metal pollution using an aquatic apex predator, the American alligator, and its parasites. PLoS ONE 10:e0142522. https://doi.org/10.1371/journal.pone.0142522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thielen F, Zimmermann S, Baska F, Taraschewski H, Sures B (2004) The intestinal parasite, Budapest, Hungary. Environ Poll 129:421–429

    Article  CAS  Google Scholar 

  • Turcˇekova´ L, Hanzelova´ V, Sˇpakulova´ M (2002) Concentration of heavy metals in perch and its endoparasites in the polluted water reservoir in Eastern Slovakia. Helminthologia 39(1):23–28

  • Wang X, Zhang L, Zhang L, Wang W, Wei S, Wang J, Che H, Zhang Y (2020) Effects of excess sugars and lipids on the growth and development of Caenorhabditis elegans. Gene Nutr 15:1. https://doi.org/10.1186/s12263-020-0659-1

    Article  CAS  Google Scholar 

Download references

Acknowledgements

AY and NK are thankful to the Head, Department of Zoology, CMP P.G. College, (A ConstituentCollege of the University of Allahabad), and AA is grateful to Aligarh Muslim University for facilities.The assistance from Mr. Abul Maz Sr. Tech. Asstt., USIF, Aligarh is thankfully acknowledged.

Funding

No funding is provided for the preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sandeep K. Malhotra.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical approval

No approval by an ethical committee was required to achieve the goals of the present study.

Additional information

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

Yadav, A., Kapoor, N., Arif, A. et al. Energy dispersive X-Ray microanalysis in conjunction with scanning electron micrography to establish nematodes as bioindicators in marine fish environment. J Parasit Dis 46, 664–671 (2022). https://doi.org/10.1007/s12639-022-01480-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12639-022-01480-8

Keywords

Navigation