Skip to main content
SpringerLink
Log in

Is current information on organochlorine exposure sufficient to conserve birds in India?

  • Review
  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Organochlorine compounds (OCs) pose a serious threat towards the wildlife due to their well-known adverse effects. India is the second largest producer of pesticides in Asia, with DDT production still ongoing, and is ranked amongst the leading countries of pesticide consumption. However, a significant data gap in avian biomonitoring studies has been identified in Asia. The objective of this review is to compile and discuss the available literature on concentrations of organochlorine pesticides and PCBs in Indian birds. The review of 18 articles showed that DDTs were the OCs most frequently analysed, followed by HCHs and PCBs (highest hepatic mean values: 11.6, 1.8 and 1.03 µg/g ww, respectively). The most frequently analysed matrix was whole body homogenates, followed by internal tissues. Plasma, eggs, feathers and guano were poorly sampled. The range of sampling years was 1980–2007. In general, hepatic OC concentrations were below the level known to cause adverse effects, although p,p’-DDE in eggs was found in concentrations associated with eggshell thinning. Most of the studies were carried out in Southern India (Tamil Nadu). Out of 106 species studied, house crow (Corvus splendens) was the most frequently monitored. However, the number of individuals sampled per species is generally low and different sample types are used, thus, huge limitations to compare OC exposure exist. This review shows that there is a clear deficit of data on OC concentrations and sublethal effects that needs to be addressed to understand the status of OC exposure, spatio-temporal trends and potential impacts in Indian avifauna.

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

  • Abbasi NA, Eulaers I, Jaspers VLB, (2016a) Use of feathers to assess polychlorinated biphenyl and organochlorine pesticide exposure in top predatory bird species of Pakistan Sci Total Environ 569:1408–1417

    Article  CAS  Google Scholar 

  • Abbasi NA, Malik RN, Frantz A, Jaspers VL, (2016b) A review on current knowledge and future prospects of organohalogen contaminants (OHCs) in Asian birds Sci Total Environ 542:411–26

    Article  CAS  Google Scholar 

  • Blus LJ (1996) DDT, DDD and DDE in Birds. In: Beyer WN, Meador JP Ed. Environmental contaminants in biota: interpreting tissue concentrations. CRC Press, Taylor & Francis, Boca Raton, p 49–72

    Google Scholar 

  • Burger J, Gochfeld M (2004) Marine birds as sentinels of environmental pollution. EcoHealth 1:263–274

    Article  Google Scholar 

  • Bustnes JO, Kristiansen KO, Helberg M (2007) Immune status, carotenoid coloration, and wing feather growth in relation to organochlorine pollutants in great black-backed gulls. Arch Environ Contam 53:96–102

    Article  CAS  Google Scholar 

  • Cortinovis S, Galassi S, Melone G, Saino N, Porte C, Bettinetti R (2008) Organochlorine contamination in the Great Crested Grebe (Podiceps cristatus): effects on eggshell thickness and egg steroid levels. Chemosphere 73:320–325

    Article  CAS  Google Scholar 

  • Dhananjayan V (2012) Organochlorine pesticides and polychlorinated biphenyls in various tissues of waterbirds in Nalabana bird sanctuary, Chilika Lake, Orissa. Bull Environ Contam Toxicol 89:197–201

    Article  CAS  Google Scholar 

  • Dhananjayan V (2013) Accumulation pattern of persistent organochlorine pesticides in liver tissues of various species of birds from India. Environ Sci Pollut Res 20:3149–3156

    Article  CAS  Google Scholar 

  • Dhananjayan V, Muralidharan S (2010) Levels of organochlorine pesticide residues in blood plasma of various species of birds from India. Bull Environ Contam Toxicol 85:129–136

    Article  CAS  Google Scholar 

  • Dhananjayan V, Muralidharan S (2013) Levels of polycyclic aromatic hydrocarbons, polychlorinated biphenyls and organochlorine pesticides in various tissues of white backed vulture in India. BioMed Res Int 2013:190353. https://doi.org/10.1155/2013/190353

    Article  CAS  Google Scholar 

  • Dhananjayan V, Muralidharan S, Ranapratap S (2011a) Organochlorine pesticide residue in eggs and tissues of House sparrow Passer domesticus, from Tamil Nadu, India. Bull Environ Contam Toxicol 87:684–688

    Article  CAS  Google Scholar 

  • Dhananjayan V, Muralidharan S, Jayanthi P (2011b) Distribution of persistent organochlorine chemical residues in blood plasma of three species of vultures from India. Environ Monit Assess 173:803–811

    Article  CAS  Google Scholar 

  • Eens M, Jaspers VLB, Van den Steen E, Bateson M, Carere C, Clergeau P, Costantini D, Dolenec Z, Elliot JE, Flux J, Gwinner H, Halbrook RS, Heeb P, Mazagajski TD, Maksnes A, Polo V, Soler JJ, Sinclair R, Veiga JP, Williams TD, Covaci A, Pinxten R (2013) Can starling eggs be useful as a biomonitoring tool to study organohalogenated contaminants on a worldwide scale? Environ Int 51:141–149

    Article  CAS  Google Scholar 

  • Elliot KH, Cesh LH, Dooley JA, Letcher RJ, Elliot JE (2009) PCBs and DDE, but not PBDEs, increase with trophic level and marine input in nestling bald eagles. Sci Total Environ 407:3867–3875

    Article  CAS  Google Scholar 

  • Espín S, García-Fernández AJ, Herzke D, Shore RF, van Hattum B, Martínez-López E, Coeurdassier M, Eulaers I, Fritsch C, Gómez-Ramírez P, Jaspers VLB, Krone O, Duke G, Helander B, Mateo R, Movalli P, Sonne C, van den Brink NW (2016) Tracking pan-continental trends in environmental contamination using sentinel raptors-what types of samples should we use? Ecotoxicology 25(4):777–801

    Article  CAS  Google Scholar 

  • Espín S, García-Fernández AJ, Herzke D, Shore RF, van Hattum, B, Martínez-López E, Coeurdassier M, Eulaers I, Fritsch C, Gómez-Ramírez P, Jaspers VLB, Krone O, Duke G, Helander B, Mateo, R, Movalli P, Sonne C & van den Brink NW (2014) Sampling and contaminant monitoring protocol for raptors. Research Networking Programme-EURAPMON, Research and monitoring for and with raptors in Europe. www.eurapmon.net. Accessed 8 feb 2018

  • Espín S, Martínez-López E, María-Mojica P, García-Fernández AJ (2012) Razorbill (Alca torda) feathers as an alternative tool for evaluating exposure to organochlorine pesticides. Ecotoxicology 21(1):183–90

    Article  CAS  Google Scholar 

  • Espín S, Terraube J, Arroyo B, Camarero PR, Mateo R, Limiñana R, Vázquez-Pumariño X, Pinilla A, García JT, Mougeot F (2018) Blood concentrations of p,p’-DDE and PCBs in harriers breeding in Spain and Kazakhstan. Sci Total Environ 624:1287–1297

    Article  CAS  Google Scholar 

  • Eulaers I, Covaci A, Hofman J, Nygard T, Halley DJ, Pinxten R, Eens M, Jaspers VLB (2011) A comparison of non-destructive sampling strategies to assess the exposure of white tailed eagle nestlings (Haliaeetus albicilla) to persistent organic pollutants. Sci Total Environ 410-411:258–265

    Article  CAS  Google Scholar 

  • Furness RW (1993) Birds as monitors of pollutants. Birds as monitors of environmental change. Chapman and Hall, London, UK, p 86–143

    Google Scholar 

  • García-Fernández AJ, Espín S, Martínez-López E (2013) Feathers as a biomonitoring tool of polyhalogenated compounds: a review. Environ Sci Technol 47(7):3028–3043

    Article  CAS  Google Scholar 

  • Gómez-Ramírez P, Shore RF, van den Brink NW, van Hattum B, Bustnes JO, Duke G, Fritsch C, García-Fernández AJ, Helander BO, Jaspers V, Krone O, Martínez-López E, Mateo R, Movalli P, Sonne C (2014) An overview of existing raptor contaminant monitoring activities in Europe. Environ Int 67:12–21

    Article  CAS  Google Scholar 

  • Gómez-Ramírez P, Martínez-López E, García-Fernández AJ, Zweers AJ, van den Brink NW (2012) Organohalogen exposure in a Eurasian Eagle owl (Bubo bubo) population from Southeastern Spain: temporal-spatial trends and risk assessment. Chemosphere 88(8):903–11

    Article  CAS  Google Scholar 

  • Goutner V, Frigis K, Konstantinou IK, Sakellarides TM, Albanis TA (2012) Organochlorine pesticide residue concentration and accumulation patterns in waterbirds and in their prey at Lake Kerkini, a Ramsar wetland, Greece. J Biol Res 17:154–168

    CAS  Google Scholar 

  • Hickey JJ (1969) Peregrine falcon populations: their biology and decline. University of Wisconsin Press, pp 446. Madison, Wisconsin, United States

  • Hoffman DJ, Clifford PR, Kubiak TJ (1996) PCBs and dioxins in birds. In: Beyer WN, Meador JP Ed. Environmental contaminants in biota: interpreting tissue concentrations. CRC Press, Taylor & Francis, Boca Raton, p 165–208

    Google Scholar 

  • Hong SH, Shim WJ, Han GM, Ha SY, Jang M, Rani M, Hong S, Yeo GY (2014) Levels and profiles of persistent organic pollutants in resident and migratory birds from an urbanized coastal region of South Korea. Sci Total Environ 470:1463–1470

    Article  CAS  Google Scholar 

  • Hu Y, Qi S, Yuan L, Liu H, Xing X (2016) Assessment of organochlorine pesticide contamination in waterbirds from an agricultural region, Central China. Environ Geochem Health 40:175–187

    Article  CAS  Google Scholar 

  • Huang K, Lin K, Guo J, Zhou X, Wang J, Zhao J, Zhou P, Xu F, Liu L, Zhang W (2013) Polybrominated diphenyl ethers in birds from Chongming Island, Yangtze estuary, China: insight into migratory behaviour. Chemosphere 91:1416–1425

    Article  CAS  Google Scholar 

  • IUCN Red list of threatened species (2016) https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22727487A86579835.en & https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22690066A86070297.en

  • Jaspers VLB, Covaci A, Deleu P, Neels H, Eens M (2008) Preen oil as the main source of external contamination with organic pollutants onto feathers of the common magpie (Pica pica). Environ Int 34:741–748

    Article  CAS  Google Scholar 

  • Joshi M, Bakre PP, Bhatnagar P (2013) Avian guano: a non-destructive biomonitoring tool for organic pollutants in environment. Ecol Indic 24:284–286

    Article  CAS  Google Scholar 

  • Kaphalia BS, Hussain MM, Seth TD, Kumar A, Krishnamurti CR (1981) Organochlorine pesticide residues in some Indian wild birds. Pestic Monit J 15:9–13

    CAS  Google Scholar 

  • Kumar KS, Kannan K, Paramasivan ON, Sundaram VP, Nakanishi J, Masunga S (2001) Polychlorinated dibenzo-p-dioxins, dibenzofurans and polychlorinated biphenyls in human tissues, meat, fish and wildlife samples from India. Environ Sci Technol 35:3448–3455

    Article  CAS  Google Scholar 

  • Kumari B, Kumar R, Kathpal TS (2001) An improved multi-residue procedure for determination of 30 pesticides in vegetables. Pestic Res J 13(1):32–35

    Google Scholar 

  • Kunisue T, Watanbe M, Subramanian A, Sethuraman A, Titenko AM, Qui V, Prudente M, Tanabe S (2003a) Accumulation features of persistent organochlorines in resident and migratory birds from Asia. Environ Pollut 125:157–172

    Article  CAS  Google Scholar 

  • Kunisue T, Watanbe M, Subramanian A, Titenko AM, Tanabe S (2003b) Congener specific patterns and toxic assessment of polychlorinated biphenyls in resident and migratory birds from Southern India and Lake Baikal in Russia. Arch Environ Contam Toxicol 45:547–561

    Article  CAS  Google Scholar 

  • Mañosa S, Mateo R, Freixa C, Guitart R (2003) Persistent organochlorine contaminants in eggs of northern goshawk and Eurasian buzzard from northeastern Spain: Temporal trends related to changes in the diet. Environ Pollut 122(3):351–359

    Article  Google Scholar 

  • Mitra A, Chatterjee C, Mandal FB (2011) Synthetic chemical pesticides and their effects on birds. Res J Environ Toxicol 5(2):81–96

    Article  CAS  Google Scholar 

  • Muralidharan S (1993) Aldrin poisoning of Sarus cranes (Grus antigone) and a few granivorous birds in Keoladeo National Park, Bharatpur, India. Ecotoxicology 2:196–202

    Article  CAS  Google Scholar 

  • Muralidharan S, Dhananjayan V, Risebrough R, Prakash V, Jayakumar R, Bloom PH (2008) Persistent organochlorine pesticide residues in tissues and eggs of white backed vulure, Gyps bengalensis from different locations in India. Bull Environ Contam Toxicol 81:561–565

    Article  CAS  Google Scholar 

  • Newton I, Wyllie I (1992) Recovery of a sparrowhawk population in relation to declining pesticide contamination. J Appl Ecol 29:476–484

    Article  CAS  Google Scholar 

  • Nisbet ICT (1989) Organochlorines, reproductive impairment and declines in Bald eagle (Hailaeetus leucocephalus) populations: mechanisms and dose response relationships. In: Meyburg B-U, Chancellor RD (eds) Raptors in the modern world. WWGBP, Berlin, London, Paris, p 483–490

    Google Scholar 

  • Peakall (1996) Dieldrin and other cyclodiene pesticides in wildlife. In: Beyer WN, Meador JP Ed. Environmental contaminants in biota: interpreting tissue concentrations. CRC Press, Taylor & Francis, Boca Raton, p 73–98

    Google Scholar 

  • Ramesh A, Tanabe S, Kannan K, Subramanian AN, Kumaran PL, Tatsukawa R (1992) Characteristic trend of persistent organochlorine contamination in wildlife from a tropical agricultural watershed, South India. Arch Environ Contam Toxicol 23:26–36

    Article  CAS  Google Scholar 

  • Ratcliffe DA (1970) Changes attributable to pesticides in egg breakage frequency and eggshell thickness in some British birds. J Appl Ecol 7:67–115

    Article  Google Scholar 

  • Senthilkumar K, Kannan K, Subramanian A, Tanabe S (2001) Accumulation of organochlorine pesticides and polychlorinated biphenyls in sediments, aquatic organisms, birds, bird’s eggs, and Bat collected from South India. Environ Sci Pollut Res 8(1):35–47

    Article  CAS  Google Scholar 

  • Senthilkumar K, Watanabe M, Kannan K, Subramanian A, Tanabe S (1999) Isomer specific patterns and toxic assessment of polychlorinated biphenyls in resident, wintering migrant birds and bat collected from South India. Toxicol Environ Chem 71:221–239

    Article  CAS  Google Scholar 

  • Sethuraman A, Subramanian AN (2003) Organochlorine residues in the avifauna of Tamil Nadu (South East coast of India). Chem Ecol 19(4):247–261

    Article  CAS  Google Scholar 

  • Tanabe S, Senthilkumar 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

    Article  CAS  Google Scholar 

  • Van den Berg HVD, Manuweera G, Konradsen F (2017) Global trends in the production and use of DDT for control of malaria and other vector borne diseases. Malar J 16:401

    Article  Google Scholar 

  • Van den Steen E, Pinxten R, Jaspers VLB, Covaci A, Barba E, Covere C, Cichon M, Dubiec A, Eeva T, Heeb P, Kempenaera B, Lifjeld JT, Lubjuhn T, Mand R, Massa B, Nilsson J, Norte AC, Orell M, Podzemny P, Sanz JJ, Senar JC, Soler JJ, Sorace A, Torok J, Visser ME, Winkel W, Eens M (2009) Brominated flame retardants and organochlorines in the European environment using great tit eggs as a biomonitoring tool. Environ Int 35:310–317

    Article  CAS  Google Scholar 

  • Watanabe MX, Iwata H, Watanabe M, Tanabe S, Subramanian A, Yoneda K, Hashimoto T (2005) Bioaccumulation of organochlorines in crows from an Indian open waste dumping site: Evidence for direct transfer of dioxin like congeners from the contaminated soil. Environ Sci Technol 39:4421–4430

    Article  CAS  Google Scholar 

  • WHO (2011) The use of DDT in malaria vector control - WHO position statement. World Health Organization. Madison, Wisconsin, United States

  • Wiemeyer SN (1996) Other organochlorine pesticides in birds. In: Beyer WN, Meador JP Ed. Environmental contaminants in biota: interpreting tissue concentrations. CRC Press, Taylor & Francis, Boca Raton, p 99–116

    Google Scholar 

  • Yadav IC, Devi NL, Syed JH, Cheng Z, Li J, Zhang G, Jones KC (2015) Current status of persistent organic pesticides residues in air, water, and soil and their possible effect on neighbouring countries: a comprehensive review of India. Sci Total Environ 511:123–137

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Rufford Foundation (Rufford Small Grants for Nature Conservation to Arzoo Malik, 20828-1). Silvia Espín was financially supported by Fundación Séneca-Agencia de Ciencia y Tecnología de la Región de Murcia (20031/SF/16 to Dr Silvia Espín) and Academy of Finland (project 265859 to Dr Tapio Eeva). We thank the Wildlife and Conservation Biology Lab (Hemchandrachrya North Gujarat University) where the current work has been carried out.

Author information

Authors and Affiliations

  1. Wildlife and Conservation Biology Lab, Hemchandracharya North Gujarat University, Patan, Gujarat, 384265, India

    Arzoo Malik & Nishith Dharaiya

  2. Department of Health Sciences, Faculty of Veterinary, Area of Toxicology, University of Murcia, Campus de Espinardo, Murcia, 30100, Spain

    Silvia Espín

  3. Toxicology and Risk Assessment Group, Biomedical Research Institute of Murcia (IMIB-Arrixaca), University of Murcia, Campus de Espinardo, Murcia, 30100, Spain

    Silvia Espín

  4. Department of Biology, Section of Ecology, University of Turku, Turku, 20014, Finland

    Silvia Espín

Authors
  1. Arzoo Malik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nishith Dharaiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Silvia Espín
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arzoo Malik.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Malik, A., Dharaiya, N. & Espín, S. Is current information on organochlorine exposure sufficient to conserve birds in India?. Ecotoxicology 27, 1137–1149 (2018). https://doi.org/10.1007/s10646-018-1969-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-018-1969-6

Keywords

Search

Navigation