Skip to main content

Advertisement

Log in

Heavy metal concentrations in Caspian pond turtle (Mauremys caspica) in Zarivar International Wetland, Kurdistan Province of Iran

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

In the present study, the cadmium, lead, and zinc levels in the blood and shell of Caspian pond turtles (Mauremys caspica) were investigated at five stations in Zarivar International Wetland in Kurdistan Province. All specimens were released at their capture locations within 2 h of capture. Water samples were collected at each station. Heavy metal concentrations were determined using an atomic absorption spectrometer. The mean cadmium, lead, and zinc concentrations were 0.04, 32.10, and 11.45 mg/l in blood samples; 1.82, 16.91, and 89.22 mg/l in shell samples; 0.005, 1.30, and 0.07 mg/l in water samples, respectively. In this study, the highest metal adsorption was zinc and was observed in shell. According to the results of this study, the shell of the Caspian Pond Turtle can be used to estimate the concentration of heavy metals. Our results suggest that Caspian pond turtle can be used as a biological indicator to estimate heavy metals.

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

Similar content being viewed by others

References

  • Adel M, Cortés-Gómez AA, Dadar M, Riyahi H, Girondot M (2017) A comparative study of inorganic elements in the blood of male and female Caspian pond turtles (Mauremys caspica) from the southern basin of the Caspian Sea. Environ Sci Pollut Res 24(32):24965–24979. https://doi.org/10.1007/s11356-017-0067-2

    Article  CAS  Google Scholar 

  • Adel MH, Saravi N, Dadar M, Niyazi L, Ley-Quinonez CP (2015) Mercury, lead, and cadmium in tissues of the Caspian Pond Turtle (Mauremys caspica) from the southern basin of Caspian Sea. Environ Sci Pollut Res 24(4):3244–3250. https://doi.org/10.1007/s11356-015-5905-5

    Article  CAS  Google Scholar 

  • Ali H, Khan E, Ilahi I (2019) Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem 2019, Article ID 6730305. https://doi.org/10.1155/2019/6730305

  • Allender MC, Dreslik MJ, Patel B, Luber EL, Byrd J, Phillips CA, Scott JW (2015) Select metal and metalloid surveillance of freeranging Eastern box turtles from Illinois and Tennessee (Terrapene carolina carolina). Ecotoxicology 24:1269–1278. https://doi.org/10.1007/s10646-015-1498-5

    Article  CAS  Google Scholar 

  • Barbieri E (2010) Acute toxicity of ammonia in white shrimp (Litopenaeus- schmitti) (Burkenroad, 1936, Crustacea) at different salinity levels. Aquaculture 306(1–4):329–333

    Article  CAS  Google Scholar 

  • Bishop BE, Savitzky BA, Abdel-Fattah T (2010) Lead bioaccumulation in emydid turtles of an urban lake and its relationship to shell disease. Ecotoxicol Environ Safe 73(4):565–571. https://doi.org/10.1016/j.ecoenv.2009.12.027

    Article  CAS  Google Scholar 

  • Cohn B, Wallace B, Grouios C, Dickson B, Scherer R, Kissel A, Gray ME, Jackson TG (2021) Heavy metal concentrations in mojave desert tortoises (Gopherus agassizii) related to a mitigation translocation project, Ivanpah Valley, California, USA. Herpetol Conserv Biol 16(1):128–141

    Google Scholar 

  • Dos Santos RL, De Sousa Correia JM, Dos Santos EM (2021) Freshwater aquatic reptiles (Testudines and Crocodylia) as biomonitor models in assessing environmental contamination by inorganic elements and the main analytical techniques used: a review. Environ Monit Assess 193:498. https://doi.org/10.1007/s10661-021-09212-w

    Article  Google Scholar 

  • García-Fernández AJ, Sánchez-García JA, Jiménez-Montalbán P, Luna A (1995) Lead and cadmium in wild birds in southeastern Spain. Environ Toxicol Chem 14(12):2049–2058

    Article  Google Scholar 

  • Griboff J, Horacek M, Wunderlin DA, Monferran MV (2018) Bioaccumulation and trophic transfer of metals, As and Se through a freshwater food web affected by antrophic pollution in Córdoba, Argentina. Ecotoxicol Environ Safe 148:275–284. https://doi.org/10.1016/j.ecoenv.2017.10.028

    Article  CAS  Google Scholar 

  • Guillot H, Bonnet X, Bustamante P, Churlaud C, Trotignon J, Brischoux F (2018) Trace element concentrations in european pond turtles (Emys orbicularis) from Brenne Natural Park. France Bull Environ Contam Toxicol 101(3):300–304. https://doi.org/10.1007/s00128-018-2376-7

    Article  CAS  Google Scholar 

  • Hillenbrand M (2020) Trace element accumulation and distribution in two turtle species, malaclemys terrapin and chelydra serpentine in New Jersey, USA. Dissertation, Montclair State University

  • Juncos R, Arcagni M, Squadrone S, Rizzo A, Arribére M, Barriga JP, Battini MA, Campbell LM, Brizio P, Abete MC, Ribeiro Guevara S (2019) Interspecific differences in the bioaccumulation of arsenic of three Patagonian top predator fish: organ distribution and arsenic speciation. Ecotoxicol Environ Safe 168:431–442. https://doi.org/10.1016/j.ecoenv.2018.10.077

    Article  CAS  Google Scholar 

  • Kami HG, Hojati V, Rad SP, Sheidaee M (2006) A biological study of the European Pond Turtle, Emys orbicularis persica, and the Caspian Pond Turtle, (Mauremys caspica caspica), in the Golestan and Mazandaran provinces of Iran. Zool Middle East 37(1):21–28. https://doi.org/10.1080/09397140.2006.10638145

    Article  Google Scholar 

  • Khan FU, Rahman AU, Jan A, Riaz M (2004) Toxic and trace metals (Pb, Cd, Zn, Cu, Mn, Ni, Co and Cr) in dust, dustfall/soil. J Chem Soc Pak 26(4):453–456

    CAS  Google Scholar 

  • Ley-Quiñónez C, Zavala-Norzagaray AA, Espinosa-Carreon TL, Peckham H, Marquez-Herrera C, Campos-Villegas L, Aguirre AA (2011) Baseline heavy metals and metalloid values in blood of loggerhead turtles (Caretta caretta) from Baja California Sur. Mexico Mar Pollut Bull 62(9):1979–1983. https://doi.org/10.1016/j.marpolbul.2011.06.022

    Article  CAS  Google Scholar 

  • Majnoonian H (2020) National Parks and protected areas, selection of scientific and technical guidelines. Department of Environment, College of Environment, Tehran (in Persian)

  • Mashroofeh A, Bakhtiari AR, Pourkazemi M, Rasouli S (2013) Bioaccumulation of Cd, Pb and Zn in the edible and inedible tissues of three sturgeon species in the Iranian coastline of the Caspian Sea. Chemosphere 90(2):573–580. https://doi.org/10.1016/j.chemosphere.2012.08.034

    Article  CAS  Google Scholar 

  • Martinez-Lopez E, Gómez-Ramírez P, Espín S, Aldeguer MP, García-Fernández AJ (2017) Influence of a former mining area in the heavy metals concentrations in blood of free-living Mediterranean pond turtles (Mauremys leprosa). Bull Environ Contam Toxicol 99(2):167–172. https://doi.org/10.1007/s00128-017-2122-6

    Article  CAS  Google Scholar 

  • Namroodi S, Zaccaroni A, Rezaei H, Hosseini SM (2018) Evaluating heavy metal contamination effects on the Caspian pond turtle health (Mauremys caspica caspica) through analyzing oxidative stress factors. Int J Epidemiol 5(4): 145–150. https://doi.org/10.15171/IJER.2018.30

  • Olaifa FE, Olaifa AK, Adelaja AA, Owolabi AG (2004) Heavy metal contamination of Clarias garpinus from a lake and Fish farm in Ibadan, Nigeria. Afric J of Biomed Res 7:145–148. https://doi.org/10.4314/ajbr.v7i3.54185

    Article  Google Scholar 

  • Paez-Osuna F, Calderón-Campuzano MF, Soto-Jiménez MF, Ruelas-Inzunza JR (2010) Trace metals (Cd, Cu, Ni, and Zn) in blood and eggs of the sea turtle lepidochelys olivacea from a nesting colony of oaxaca, mexico. Arch Environ Contam Toxicol 59:632–641. https://doi.org/10.1007/s00244-010-9516-3

    Article  CAS  Google Scholar 

  • Papathanassiou E (1983) Effects of cadmium and mercury ions and respiration and survival of the common prawn Palaemon serratus (Pennant). Rev Int Oceanogr Med 72:21–35

    CAS  Google Scholar 

  • Qayyum MA, Shah MH (2017) Study of trace metal imbalances in the blood, scalp hair and nails of oral cancer patients from Pakistan. Sci Total Environ 593:191–201. https://doi.org/10.1016/j.scitotenv.2017.03.169

    Article  CAS  Google Scholar 

  • Quiñónez CP, Zavala-Norzagaray AA, Réndon-Maldonado JG, Espinosa-Carreon TL, Canizales-Román A, Escobedo-Urías DC, Aguirre AA (2013) Selected heavy metals and selenium in the blood of Black Sea turtle (Chelonia mydas agasiizzi) from Sonora. Mexico Bull Environ Contam Toxicol 91(6):645–651. https://doi.org/10.1007/s00128-013-1114-4

    Article  CAS  Google Scholar 

  • Ramsar Information Sheet for site no. 2369 (2019), Zarivar, Iran. https://rsis.ramsar.org. Accessed 26 February 2022

  • Safaei-Mahroo B, Ghaffari H, Fahimi H, Bromand S, Yazdanian M, Najafi Majid E, Yousefkhani M, Rezazadeh E, Hosseinzadeh M, Nasrabadi R, Rajabzadeh M, Mashaykhi M, Moteshari A, Naderi A, Kazemi M (2015) The Herpetofauna of Iran: checklist of Taxonomy, distribution and conservation status. Asian Herpetol Res 6(4):257–290. https://doi.org/10.16373/j.cnki.ahr.140062

  • Schifer TDS, Junior SB, Montano MAE (2005) Aspectos Toxicológicos Do Chumbo Infarma 17(5–6):67–71

    Google Scholar 

  • Sheklabadi M, Mahmoudzadeh H, Mahboubi AA, Gharabaghi B, Ahrens B (2014) Long-term land-use change effects on phosphorus fractionation in Zrêbar Lake margin soils. Archives of Agronomy and Soil Science 61(6):737–749. https://doi.org/10.1080/03650340.2014.954106

    Article  CAS  Google Scholar 

  • Slimani T, El-Hassani MS, El-Mouden EH, Bonnet M, Bustamante P, Brischoux F, Brault-Favrou M, Bonnet X (2018) Large-scale geographic patterns of mercury contamination in Morocco revealed by freshwater turtles. Environ Sci Pollut Res 25:2350–2360. https://doi.org/10.1007/s11356-017-0643-5

    Article  CAS  Google Scholar 

  • Smith DL, Cooper MJ, Kosiara JM, Lamberti GA (2016) Body burdens of heavy metals in Lake Michigan wetland turtles. Environ Monit Assess 188(2):128. https://doi.org/10.1007/s10661-016-5118-5

    Article  CAS  Google Scholar 

  • Torabi Kachoosangi F, Karbassi A, Sarang A, Noori R (2020) Sedimentation rate determination and heavy metal pollution assessment in Zariwar Lake. Iran SN Appl Sci 2:1483. https://doi.org/10.1007/s42452-020-03279-9

    Article  CAS  Google Scholar 

  • Vieira LM, Nunes VDS, Amaral MDA, Oliveira AC, Hauser-Davis RA, Campos RC (2011) Mercury and methyl mercury ratios in caimans (Caiman crocodilus yacare) from the Pantanal area Brazil. J Environ Manage 13(2):280–287

    CAS  Google Scholar 

  • Yadollahvand R, Kami HG, Mashroofeh A, Bakhtiari AR (2014) Assessment trace elements concentrations in tissues in Caspian pond turtle (Mauremys caspica) from Golestan province. Iran Ecotoxicol Environ Saf 101:191–195. https://doi.org/10.1016/j.ecoenv.2013.12.028

    Article  CAS  Google Scholar 

  • Yipel M, Tekeli İO, İşler CT, Altuğ ME (2017) Heavy metal distribution in blood, liver and kidneys of Loggerhead (Caretta caretta) and Green (Chelonia mydas) sea turtles from the Northeast Mediterranean Sea. Mar Pollut Bull 25(1–2):487–491. https://doi.org/10.1016/j.marpolbul.2017.08.011

    Article  CAS  Google Scholar 

  • Yu SY, Halbrook RS, Sparling DW, Colombo R (2011) Metal accumulation and evaluation of effects in a freshwater turtle. Ecotoxicology 20(8):1801–1812. https://doi.org/10.1007/s10646-011-0716-z

    Article  CAS  Google Scholar 

  • Zarei F, Hosseini SN, Amini SS, Pezeshk J, Maleki L, Rajabi-Mahan H (2017) Proposing Zarivar Wildlife Refuge (Western Iran) as a Ramsar site based on avian diversity and conservation criteria. Podoces 12(2):27–42

    Google Scholar 

  • Zavala-Norzagaray AA, Ley-Quiñónez CP, Espinosa-Carreón TL, Canizalez-Román A, Hart CE, Aguirre AA (2014) Trace elements in blood of sea turtles Lepidochelys olivacea in the Gulf of California, Mexico. Bull Environ Contam Toxicol 93:536–541

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Amir Rostami and Masood Mostafa Soltani for their assistance with the blood sampling and Ataolah Tarank, Madeh Hoseini, Salah Dehghani, Fatah Boutimar, Abed Daneshvar, Kamal Rastkhaneh for their assistance with the field surveys. We are grateful to Houshyar Gavilian for his help with conducting the trace elements analysis. We would like to express our gratitude to Semko Azimi, Seyvan Amini, Sharif Bajour, and his wife for their assistance during the fieldwork.

Funding

This work was financially supported by University of Kurdistan.

Author information

Authors and Affiliations

Authors

Contributions

All the authors carried out the study conception, design, and material preparation. Elham Moradi collected the data. Elham Moradi and Hanyeh Ghaffari wrote the first draft of the manuscript, and all the authors provided comments on previous versions. All the authors read and approved the final manuscript.

Corresponding author

Correspondence to Hanyeh Ghafari.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Philippe Garrigues

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 18 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moradi, E., Ghafari, H. & Ghorbani, F. Heavy metal concentrations in Caspian pond turtle (Mauremys caspica) in Zarivar International Wetland, Kurdistan Province of Iran. Environ Sci Pollut Res 29, 89691–89697 (2022). https://doi.org/10.1007/s11356-022-22056-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-22056-2

Keywords

Navigation