Skip to main content
SpringerLink
Log in

Contamination of habu (Protobothrops flavoviridis) in Okinawa, Japan by persistent organochlorine chemicals

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

Abstract

Persistent organochlorine chemicals (OCs), including chlordane compounds (CHLs), DDTs, PCBs, and chlorinated dioxins and related compounds (DRCs), were examined in the adipose tissue and liver from 33 specimens of habu (Protobothrops flavoviridis), a species of venomous pit viper endemic to the Japanese Southwest Islands. The median concentrations of CHLs, DDTs, and PCBs in adipose tissue of 22 habus collected from an urban area were 4400 ng g−1 lipid weight (lw), 610 ng g−1 lw, and 1600 ng g−1 lw, respectively. Their DDT and PCB concentrations were higher in comparison with the specimens from a rural area. Liver of 10 specimens from the urban area were subjected to DRCs analysis, and PCDDs, PCDFs, and DL-PCBs were detected with median values of 1300, 350, and 150,000 pg g−1 lw, respectively. Among PCDD/F congeners, octa-CDD was detected at the highest concentrations in seven liver samples, but considerable concentrations of penta- and hexa-CDD/Fs were found in two samples. Relatively higher concentrations of PCB, DDTs, and PCDD/Fs were found in habus collected within 1 km of the boundary of military facilities, suggesting that OCs from some unknown sources of these OCs inside and/or around some of the facilities accumulated in habus.

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
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aksoy A, Das YK, Yavuz O, Guvenc D, Atmaca E, Agaoglu S (2011) Organochlorine pesticide and polychlorinated biphenyls levels in fish and mussel in Van region, Turkey. Bull Environ Contam Toxicol 87:65–69. https://doi.org/10.1007/s00128-011-0286-z

    Article  CAS  Google Scholar 

  • Campbell KR, Campbell TS (2001) The accumulation and effects of environmental contaminants on snakes: a review. Environ Monit Assess 70:253–301. https://doi.org/10.1023/a:1010731409732

    Article  CAS  Google Scholar 

  • Ciliberti A, Berny P, Delignette-Muller ML, de Buffrénil V (2011) The Nile monitor (Varanus niloticus; Squamata: Varanidae) as a sentinel species for lead and cadmium contamination in sub-Saharan wetlands. Sci Total Environ 409:4735–4745. https://doi.org/10.1016/j.scitotenv.2011.07.028

    Article  CAS  Google Scholar 

  • Colombo A, Bettinetti R, Strona G, Cambria F, Fanelli R, Zubair Z, Galli P (2014) Maldives: an archipelago that burns. A first survey of PCDD/Fs and DL-PCBs from human activities. Sci Total Environ 497–498:499–507. https://doi.org/10.1016/j.scitotenv.2014.08.013

    Article  CAS  Google Scholar 

  • Erickson MD, Kaley RG II (2011) Applications of polychlorinated biphenyls. Environ Sci Pollut Res 18:135–151. https://doi.org/10.1007/s11356-010-0392-1

    Article  CAS  Google Scholar 

  • Fiedler H (1996) Sources of PCDD/PCDF and impact on the environment. Chemosphere 32:55–64. https://doi.org/10.1016/0045-6535(95)00228-6

    Article  CAS  Google Scholar 

  • Fleet RR, Plapp FW Jr (1978) DDT residues in snakes decline since DDT ban. Bull Environ Contam Toxicol 19:383–388. https://doi.org/10.1007/BF01685814

    Article  CAS  Google Scholar 

  • Goto A, Tue NM, Someya M, Isobe T, Takahashi S, Takahashi S, Tanabe S, Kunisue T (2017) Occurrence of natural mixed halogenated dibenzo-p-dioxins: specific distribution and profiles in mussels from Seto Inland Sea, Japan. Environ Sci Technol 51:11771–11779. https://doi.org/10.1021/acs.est.7b03738

    Article  CAS  Google Scholar 

  • Hayashi Y, Tanaka H (1981) Age determination in the venomous snake, habu, Trimeresurus flavoviridis. Jpn J Exp Med 51:209–213 (in Japanese)

    Google Scholar 

  • Heinz GH, Haseltine SD, Hall RJ, Krynitsky AJ (1980) Organochlorine and mercury residues in snakes from Pilot and Spider Islands, Lake Michigan—1978. Bull Environ Contam Toxicol 25:738–743. https://doi.org/10.1007/BF01985601

    Article  CAS  Google Scholar 

  • Heydari Sereshk Z, Riyahi Bakhtiari A (2014) Distribution patterns of PAHs in different tissues of annulated sea snake (Hydrophis cyanocinctus) and short sea snake (Lapemis curtus) from the Hara Protected Area on the North Coast of the Persian Gulf, Iran. Ecotox Environ Safe 109:116–123. https://doi.org/10.1016/j.ecoenv.2014.06.004

    Article  CAS  Google Scholar 

  • Iatrou EI, Tsygankov V, Seryodkin I, Tzatzarakis MN, Vakonaki E, Barbounis E, Zakharenko AM, Chaika VV, Sergievich AA, Tsatsakis AM, Golokhvast K (2019) Monitoring of environmental persistent organic pollutants in hair samples collected from wild terrestrial mammals of Primorsky Krai, Russia. Environ Sci Pollut Res 26:7640–7650. https://doi.org/10.1007/s11356-019-04171-9

    Article  CAS  Google Scholar 

  • Japan Environment Agency (1998) Endocrine disrupting chemicals interim investigation manual (water, sediment, and aquatic organisms). Water Quality Management Division, Water Quality Conservation Bureau, Japan Environment Agency, Tokyo (in Japanese)

  • Jones DE, Magnin-Bissel G, Holladay SD (2009) Detection of polycyclic aromatic hydrocarbons in the shed skins of corn snakes (Elaphe guttata). Ecotox Environ Safe 72:2033–2035. https://doi.org/10.1016/j.ecoenv.2008.11.001

    Article  CAS  Google Scholar 

  • Kinjo K, Yamashiro Y, Uehara T (1977) Monitoring of PCBs and heavy metals in fish (3). Report of Okinawa Prefectural Institute of Health and Environment 11:74–75 (in Japanese)

    Google Scholar 

  • Kuehl DW, Butterworth BC, De Vita VM, Suer CP (1987) Environmental contamination by polychlorinated dibenzo-p dioxins and dibenzofurans associated with pulp and paper mill discharge. Biomed Environ Mass Spectrom 14:443–447. https://doi.org/10.1002/bms.1200140811

    Article  CAS  Google Scholar 

  • Kunisue T, Watanabe MX, Iwata H, Tsubota T, Yamada F, Yasuda M, Tanabe S (2006) PCDDs, PCDFs, and coplanar PCBs in wild terrestrial mammals from Japan: congener specific accumulation and hepatic sequestration. Environ Pollut 140:525–535. https://doi.org/10.1016/j.envpol.2005.07.020

    Article  CAS  Google Scholar 

  • Kunisue T, Takayanagi N, Tsubota T, Tanabe S (2007) Persistent organochlorines in raccoon dogs (Nyctereutes procyonoides) from Japan: hepatic sequestration of oxychlordane. Chemosphere 66:203–211. https://doi.org/10.1016/j.chemosphere.2006.06.001

    Article  CAS  Google Scholar 

  • Kunisue T, Takayanagi N, Isobe T, Takahashi S, Nakatsu S, Tsubota T, Okumoto K, Bushisue S, Shindo K, Tanabe S (2008) Regional trend and tissue distribution of brominated flame retardants and persistent organochlorines in raccoon dogs (Nyctereutes procyonoides) from Japan. Environ Sci Technol 42:685–691. https://doi.org/10.1021/es071565z

    Article  CAS  Google Scholar 

  • Lemaire J, Bustamante P, Olivier A, Lourdais O, Michaud B, Boissinot A, Galán P, Brischoux F (2018) Determinants of mercury contamination in viperine snakes, Natrix maura, in Western Europe. Sci Total Environ 635:20–25. https://doi.org/10.1016/j.scitotenv.2018.04.029

    Article  CAS  Google Scholar 

  • Masunaga S, Takasuga T, Nakanishi J (2001) Dioxin and dioxin-like PCB impurities in some Japanese agrochemical formulations. Chemosphere 44:873–885. https://doi.org/10.1016/S0045-6535(00)00310-6

    Article  CAS  Google Scholar 

  • Minakami K (1977) Age determination of the yellow-green pit viper, habu by the vertebral centrum. Zool Mag 86:82–86 (in Japanese)

    Google Scholar 

  • Niethammer KR, White DH, Baskett TS, Sayre MW (1984) Presence and biomagnification of organochlorine chemical residues in oxbow lakes of Northeastern Louisiana. Arch Environ Contam Toxicol 13:63–74. https://doi.org/10.1007/BF01055647

    Article  CAS  Google Scholar 

  • Nishimura M (1993) Estimation of age and growth of habu, Trimeresurus flavoviridis (serpents: Viperidae), in the Okinawa Islands. Jpn J Ecol 43:83–90 (in Japanese)

    Google Scholar 

  • Nishimura M, Araki Y, Ueda H, Kawashima Y (1991) Frequencies of prey items of habu, Trimeresurus flavoviridis (viperidae), in the Okinawa Islands 1. Snake 23:81–83

    Google Scholar 

  • Okinawa City Hall (2013) Investigation report on the soil pollution at a football field in Okinawa City. Okinawa City Hall, Okinawa (in Japanese)

    Google Scholar 

  • Okinawa Prefectural Government (2018) Annual Report on the Environment in Okinawa 2018. Okinawa Prefectural Government, Okinawa (in Japanese)

    Google Scholar 

  • Oshiro Z (1981) Chlordane and environmental pollution (1)—analytical method and contamination status. Report of Okinawa Prefectural Institute of Health and Environment 14:1–16 (in Japanese)

    Google Scholar 

  • Oshiro Z, Yamashiro O, Shiroma H, IKema J, Oyama M, Kinjo K (1986) Contamination of chlordanes in man resided in Okinawa. Report of Okinawa Prefectural Institute of Health and Environment 20:77–86 (in Japanese)

    CAS  Google Scholar 

  • Oshiro Y, Uechi S, Asato N, Kinjo K, Yoshida N, Toguchi A, Tamaki F, Futenma T, Miyagi T, Uehara T (2006) Environmental survey and monitoring of chemicals in Okinawa (1995–2004). Report of Okinawa Prefectural Institute of Health and Environment 40:179–186 (in Japanese)

    Google Scholar 

  • Oyama C, Moriyama C, Ikema S, Chibana Y, Oshiro S, Kinjo Y, Tagashira M, Oyama M, Kinjo K, Yamashiro Y, Oshiro N (1972) PCP contamination of water supply in southern part of Okinawa Island. Report of Okinawa Prefectural Institute of Health and Environment 6:78–88 (in Japanese)

    Google Scholar 

  • Roberts CM, McClean CJ, Veron JEN, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne FC, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284. https://doi.org/10.1126/science.1067728

    Article  CAS  Google Scholar 

  • Santos X, Pastor D, Llorente GA, Albaigrs J (1999) Organochlorine levels in viperine snake Natrix maura carcasses from the Ebro Delta (NE Spain): sexual and size-related differences. Chemosphere 39:2641–2650. https://doi.org/10.1016/S0045-6535(99)00199-X

    Article  CAS  Google Scholar 

  • Seston RM, Fredricks TB, Tazelaar DL, Coefield SJ, Bradley PW, Roark SA, Newsted JL, Kay DP, Zwiernik MJ, Giesy JP (2011) Dietary exposure of great blue heron (Ardea herodias) to PCDD/DFs in the Tittabawassee River flood plain, MI. Ecotox Environ Safe 74:494–503. https://doi.org/10.1016/j.ecoenv.2010.10.024

    Article  CAS  Google Scholar 

  • Someya M, Kunisue T, Tashiro Y, Asakawa M, Iwata H, Tanabe S (2007) Contamination status and accumulation features of dioxins and related compounds in terrestrial mammals from Japan. Organohalogen Compounds 69:1721–1724

  • Tanabe S, Minh TB (2010) Dioxins and organohalogen contaminants in the Asia-Pacific region. Ecotoxicology 19:463–478. https://doi.org/10.1007/s10646-009-0445-8

    Article  CAS  Google Scholar 

  • Tanabe S, Senthilkumar K, Kannan K, Subramanian AN (1998) Accumulation features of polychlorinated biphenyls and organochlorine pesticides in resident and migratory birds from South India. Arch Environ Contam Toxicol 34:387–397. https://doi.org/10.1007/s002449900335

    Article  CAS  Google Scholar 

  • Tanabe S, Takahashi S, Malarvannan G, Ikemoto T, Anan Y, Kunisue T, Isobe T, Agusa T (2008) Survey on hazardous chemicals in aquatic organisms inhabiting Nansei Shoto Islands: report on the contamination status of fish and shellfish. In: Japan WWF (ed) Wildlife contamination assessment of Nansei Shoto Islands (2005–2007). WWFJ, Tokyo, pp 25–46

    Google Scholar 

  • Tashiro Y, Goto A, Kunisue T, Kurahashi T, Tanabe S (2016) Contamination status of PCBs and organochlorine pesticides in the Okinawa Island, Japan: utilization of small Indian mongoose (Herpestes auropunctatus) as a bioindicator. J Environ Chem 26:115–122. https://doi.org/10.5985/jec.26.115

    Article  CAS  Google Scholar 

  • Van den Berg M, Birnbaum L, Denison M, De Vito M, Farland W, Feeley M, Fiedler H, Hakansson H, Hanberg A, Haws L, Rose M, Safe S, Schrenk D, Tohyama C, Tritscher A, Tuomisto J, Tysklind M, Walker N, Peterson RE (2006) The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci 93:223–241. https://doi.org/10.1093/toxsci/kfl055

    Article  CAS  Google Scholar 

  • Yoshinaga A, Oyama M, Oshiro Z, Ikema S, Chibana Y, Sakugawa H, Shimoji K, Miyagi K, Takeuchi T, Takara T (1978) Survey results of drainages from U.S. military bases in 1977. Report of Okinawa Prefectural Institute of Health and Environment 12:44–51 (in Japanese)

    CAS  Google Scholar 

  • Zhou Y, Asplund L, Yin G, Athanassiadis I, Wideqvist U, Bignert A, Qiu Y, Zhu Z, Zhao J, Bergman Å (2016) Extensive organohalogen contamination in wildlife from a site in the Yangtze River Delta. Sci Total Environ 554–555:320–328. https://doi.org/10.1016/j.scitotenv.2016.02.176

    Article  CAS  Google Scholar 

Download references

Acknowledgment

Part of this research was carried out by the Grant-in-Aid for Scientific Research (C) Project No. 25340062 and the Ministry of Education, Culture, Sports, Science and Technology , Japan (MEXT) to a project on Joint Usage/Research Center—Leading Academia in Marine and Environment Pollution Research (LaMer). Authors are grateful to Mr. Yoshiyasu Iha and Dr. Gloria Esther Luyo Acero de Tashiro for valuable comments on the research design and manuscript. We also received the cooperation of the Okinawa Prefectural Institute for Hygiene and Environment and local residents in collecting samples for the present study.

Author information

Authors and Affiliations

  1. School of International Studies, Meio University, 1220-1 Biimata, Nago, Okinawa, 905-8585, Japan

    Yutaka Tashiro

  2. Center for Marine Environmental Studies (CMES), Ehime University, 2-5 Bunkyo, Matsuyama, Ehime, 790-8577, Japan

    Akitoshi Goto, Tatsuya Kunisue & Shinsuke Tanabe

Authors
  1. Yutaka Tashiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akitoshi Goto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatsuya Kunisue
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shinsuke Tanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yutaka Tashiro.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Philippe Garrigues

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

Tashiro, Y., Goto, A., Kunisue, T. et al. Contamination of habu (Protobothrops flavoviridis) in Okinawa, Japan by persistent organochlorine chemicals. Environ Sci Pollut Res 28, 1018–1028 (2021). https://doi.org/10.1007/s11356-020-10510-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-10510-y

Keywords

Search

Navigation