Skip to main content

Advertisement

Log in

Odonata larvae as a bioindicator of metal contamination in aquatic environments: application to ecologically important wetlands in Iran

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

The objectives of this study were twofold: (i) assess the bioaccumulation characteristics of a suite of metals associated with several different species of Odonata and (ii) examine Odonata species richness as a reflection of ecosystem health in two ecologically important wetlands of southwestern Iran, the Shadegan and Hawr Al Azim wetlands. Levels of arsenic (As), cadmium (Cd), cobalt (Co), chromium (Cr), copper (Cu), iron (Fe), mercury (Hg), manganese (Mn), lead (Pb), and zinc (Zn) were determined using inductively coupled plasma optical emission spectrometry (ICP-OES) in nine different Odonata larva species. Based on these data, biota-sediment accumulation factors (BSAFs) were calculated and generally, it was found that Cr, Cu, Mn, and Zn were being taken up by the Odonata (BSAFs >1). Because of its prevalence in the wetland and its observed ability to take up metals, it is suggested that Ischnura ramburii is an appropriate indicator of ecosystem health for these wetlands with respect to metal contamination. Odonata species richness across all sites was 49, while for the individual sites, the greatest species richness was 26 and the lowest species richness was 13. The species richness value across all sites is quite healthy, given the arid climate of the region.

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

  • Alhashemi, A. H., Sekhavatjou, M. S., Kiabi, B. H., & Karbassi, A. R. (2012). Bioaccumulation of trace elements in water, sediment, and six fish species from a freshwater wetland, Iran. Microchemical Journal, 104, 1–6.

    Article  Google Scholar 

  • Al-Hilli, M. R. A., Warner, B. G., Asada, T., & Douabul, A. (2009). An assessment of vegetation and environmental controls in the 1970s of the Mesopotamian wetlands of sourthern Iraq. Wetlands Ecology and Management, 17, 207–223.

    Article  Google Scholar 

  • Berger, B., & Dallinger, R. (1993). Terrestrial snails as quantitative indicators of environmental metal pollution. Environmental Toxicology. Assessment, 25, 65–84.

    CAS  Google Scholar 

  • Brix, K. V., DeForest, D. K., & Adams, W. J. (2011). The sensitivity of aquatic insects to divalent metals: A comparative analysis of laboratory and field data. Science of the Total Environment, 409, 4187–4197.

    Article  CAS  Google Scholar 

  • Buchwalter, D. B., Cain, D. J., Clements, W. H., & Luoma, S. N. (2007). Using biodynamic models to reconcile differences between laboratory toxicity tests and field biomonitoring with aquatic insects. Environmental Science & Technology, 41, 4821–4828.

    Article  CAS  Google Scholar 

  • Burton Jr., G. A. (2002). Sediment quality criteria in use around the world. Limnology, 3, 65–75.

    Article  CAS  Google Scholar 

  • Catling, P. M. (2005). A potential for the use of dragonfly (Odonata) diversity as a bioindicator of the efficiency of sewage lagoons. Canadian Field-Naturalist, 119(2), 233–236.

    Article  Google Scholar 

  • Chapman, P. M. (2011). Indices: attractive delusions. Integrated Environmental Assessment and Management, 7(3), 313–313.

    Article  Google Scholar 

  • Chevre, N., Loepfe, C., Singer, H., Stamm, C., Fenner, K., & Escher, B. I. (2006). Including mixtures in the determination of water quality criteria for herbicides in surface water. Environmental Science & Technology, 40(2), 426–435.

    Article  CAS  Google Scholar 

  • Chu, K. W., & Chow, K. L. (2002). Synergistic toxicity of multiple heavy metals is revealed by a biological assay using a nematode and its transgenic derivative. Aquatic Toxicology, 61, 53–64.

    Article  Google Scholar 

  • Corbi, J. J., Trivinho-Strixino, S., & Dos Santos, A. (2008). Environmental evaluation of metals in sediments and dragonflies due to sugar cane cultivation in Neotropical streams. Water, Air, and Soil Pollution, 195(1–4), 325–333.

    Article  CAS  Google Scholar 

  • Costanza, R. R., d’Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., O’Neill, R. V., Paruelo, J., Raskin, G., Sutton, P., & van der Belt, M. (1997). The value of the world’s ecosystem services and natural capital. Nature, 387, 253–260.

    Article  CAS  Google Scholar 

  • Crane, M. (2003). Proposed development of sediment quality guidelines under the European Water Framework Directive: a critique. Toxicology Letters, 142, 195–206.

    Article  CAS  Google Scholar 

  • Dallinger, R., Berger, B., & Birkel, S. (1992). Terrestrial isopods: useful biological indicators of urban pollution. Oecologia, 89, 32–41.

    Article  Google Scholar 

  • Davodi, M., Esmalli, A., & Bahramifarr, N. (2011). Concentration of polychlorinated biphenyls and organochlorine pesticides in some edible fish species from the Shadegan Marshes (Iran). Ecotoxicology and Environmental Safety, 74(3), 294–300.

    Article  CAS  Google Scholar 

  • Diagomanolin, V., Farhang, M., Ghazi-Khansari, M., & Jafarzadeh, N. (2004). Heavy metals (Ni, Cr, Cu) in the Karoon waterway river, Iran. Toxicology Letters, 151, 63–68.

    Article  CAS  Google Scholar 

  • Dijkstra, K. D. B., & Lempert, J. (2003). Odonate asseblages of running waters in the Upper Guinean forest. Archiv für Hydrobiologie, 157(3), 397–412.

    Article  Google Scholar 

  • Dolny, A., Harabis, F., Barta, D., Lhota, S., & Drozd, P. (2012). Aquatic insects indicate terrestrial habitat degradation: changes in taxonomical structure and functional diversity of dragonflies in tropical rainforest of East Kalimantan. Tropical. Zoology, 25(3), 141–157.

    Article  Google Scholar 

  • Eimanifar, A., & Mohebbi, F. (2007). Urmia Lake (Northwest Iran): a brief review. Saline Systems, 3(5), 1–8.

    Google Scholar 

  • Erwin, K. L. (2009). Wetlands and global climate change: the role of wetland restoration in a changing world. Wetlands Ecology and Management, 17, 71–84.

    Article  Google Scholar 

  • Fan, W., Xu, Z., & Wang, W.-X. (2014). Metal pollution in a contaminated bay: relationship between metal geochemical fractionation in sediments and accumulation on a polycheate. Environmental Pollution, 191, 50–57.

    Article  CAS  Google Scholar 

  • Foote, A. L., & Rice Hornung, C. L. (2005). Odonates as biological indicators of grazing effects on Canadian prairie wetlands. Ecological Entomology, 30, 273–283.

    Article  Google Scholar 

  • Ghosh, D. (2016). Revisiting East Kolkata Wetlands: globality of the locals. Journal of Geography, Environment and Earth Science International, 5(3), 1–14.

    Article  Google Scholar 

  • Goodyear, K. L., & McNeill, S. (1999). Bioaccumulation of heavy metals by aquatic macro-invertebrates of different feeding guilds: a review. The Science of the Total Environment, 229, 1–19.

    Article  CAS  Google Scholar 

  • Green, R., & Chapman, P. M. (2011). The problem with indices. Marine Pollution Bulletin, 62, 1377–1380.

    Article  CAS  Google Scholar 

  • Hao, O. J. (1996). Bioindicators for water quality evaluation—a review. Journal of the Chinese Institute of Environmental Engineering, 6(1), 1–19.

    CAS  Google Scholar 

  • Hardersen, S. (2000). The role of behavioural ecology of damselflies in the use of fluctuating asymmetry as a bioindicator of water pollution. Ecological Entomology, 25, 45–53.

    Article  Google Scholar 

  • Hare, L. (1992). Aquatic insects and trace metals: bioavailability, bioaccumulation, and toxicity. Critical Reviews in Toxicology, 22(5–6), 327–369.

    Article  CAS  Google Scholar 

  • Hart, L. A., Bowker, M. B., Tarboton, W., & Downs, C. T. (2014). Species composition, distribution and habitat types of Odonata in the iSimangaliso Wetland Park, Kwa Zulu-Natal, South Africa and the associated conservation implications. PloS One, 9(3), 1–11.

    Article  Google Scholar 

  • Hartig, J. H. (2010). Burning rivers, revival of four urban-industrial rivers that caught fire. Ecovision world monograph series. Burlington: Aquatic Ecosystem Health & Management Society.

    Google Scholar 

  • Hashemi, S. A. R., & Ansary, H. (2012). Biomass and production of fish species in the Shadegan Wetland, Iran. Global Veterinaria, 9(2), 123–128.

    Google Scholar 

  • Herman, M. R., & Nejadhashemi, A. P. (2015). A review of macroinvertebrate- and fish-based stream health indices. Ecohydrology & Hydrobiology, 15(2), 53–67.

    Article  Google Scholar 

  • Hopkin, S. P. (1989). Ecophysiology of metals in terrestrial invertebrates. London: Elsevier Applied Science.

    Google Scholar 

  • Iliopoulou-Georgudaki, J., Kantzaris, V., Katharios, P., Kaspiris, P., Georgiadis, T., & Montesantou, B. (2003). An application of different bioindicators for assessing water quality: a case study in the rivers Alfeios and Pineios (Peloponnisos, Greece). Ecological Indicators, 2, 345–360.

    Article  CAS  Google Scholar 

  • Irvine, K. N., & Murphy, T. P. (2009). Assessment of eutrophication and phytoplankton community impairment in the Buffalo River Area of Concern. Journal of Great Lakes Research, 35, 83–93.

    Article  CAS  Google Scholar 

  • Irvine, K. N., Frothingham, K. M., Rossi, M. C., Pickard, S., Atkinson, J., & Bajak, T. (2003). Contaminated sediment in the Buffalo River Area of Concern—historical trends and current conditions. in: Munawar, M. (Ed.), Sediment quality assessment and management: insight and progress., Ecovision World Monograph Series, Aquatic Ecosystem Health and Management Society, pp. 81–112.

  • Irvine, K., Sampson, M., Visoth, T., Yim, M., Veasna, K., Koottatep, T., & Rupp, J. (2008). Spatial patterns of E. coli and detergents in the Boeng Cheung Ek treatment wetland, Phnom Penh, Cambodia. The 6th International Symposium on Southeast Asian Water Environment. SEAWE, Bandung, pp. 78–81.

  • Javedankherad, I., Esmaili-Sair, A., & Bahramifar, N. (2013). Levels and distribution of organochlorine pesticides and polychlorinated biphenyls in water and sediment from the international Anzali Wetland, North of Iran. Bulletin of Environmental Contamination and Toxicology, 90, 285–290.

    Article  CAS  Google Scholar 

  • Junior, C. S. M., Juen, L., & Hamada, N. (2015). Analysis of urban impacts on aquatic habitats in the central Amazon basin: Adult odonates as bioindicators of environmental quality. Ecological Indicators, 48, 303–311.

    Article  Google Scholar 

  • Kaffashi, S., Shamsudin, M. N., Radam, A., Rahim, K. A., Yacob, M. R., Muda, A., & Yazid, M. (2011). Economic valuation of Shadegan International Wetland, Iran: notes for conservation. Regional Environmental Change, 11(4), 925–934.

    Article  Google Scholar 

  • Kaffashi, S., Shamsudin, M. N., Radam, A., Yacob, M. R., Rahim, K. A., & Yazid, M. (2012). Economic valuation and conservation: do people vote for better preservation of Shadegan International Wetland? Biological Conservation, 150, 150–158.

    Article  Google Scholar 

  • Kane, D. D., Gordon, S. I., Munawar, M., Charlton, M. N., & Culver, D. A. (2009). The Planktonic Index of Biotic Integrity (P-IBI): an approach for assessing lake ecosystem health. Ecological Indicators, 9, 1234–1247.

    Article  CAS  Google Scholar 

  • Karr, J. R. (1981). Assessment of biotic integrity using fish communities. Fisheries, 6(6), 21–27.

    Article  Google Scholar 

  • Luo, W., Lu, Y., Wang, T., Kong, P., Jiao, W., Hu, W., Jia, J., Naile, J. E., Khim, J. S., & Giesy, J. P. (2013). Environmental concentrations and bioaccumulations of cadmium and zinc in coastal watersheds along the Chinese Northern Bohai and Yellow Seas. Environmental Toxicology and Chemistry, 32(4), 831–840.

    Article  CAS  Google Scholar 

  • Luoma, S. N., & Rainbow, P. S. (2005). Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Environmental Science & Technology, 39(7), 1921–1931.

    Article  CAS  Google Scholar 

  • Lydy, M. J., Crawford, C. G., & Frey, J. W. (2000). A comparison of selected diversity, similarity, and biotic indices for detecting changes in benthic-invertebrate community structure and stream quality. Archives of Environmental Contamination and Toxicology, 39, 469–479.

    Article  CAS  Google Scholar 

  • Lynch, T. R., Popp, C. J., & Jacobi, G. Z. (1988). Aquatic insects as environmental monitors of trace metal contamination: Red River, New Mexico. Water Air & Soil Pollution, 42(1–2), 19–31.

    CAS  Google Scholar 

  • Mac Donald, D. D., Ingersoll, C. G., & Berger, T. A. (2000). Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Archives of Environmental Contamination and Toxicology, 39, 20–31.

    Article  CAS  Google Scholar 

  • Mahan, C. G., Young, J. A., Miller, B. J., & Saunders, M. C. (2015). Using ecological indicators and a decision support system for integrated ecological assessment at two national park units in the mid-Atlantic region, USA. Environmental Management, 55, 508–522.

    Article  Google Scholar 

  • Mansoori, J. (2009). The avian community of five Iranian wetlands, Miankaleh, Fereidoon-Kenar, Bujagh, Anzali and Lavandevil, in the South Caspian Lowlands. Podoces, 4(1), 44–59.

    Google Scholar 

  • McGeer, J. C., Brix, K. V., Skeaff, J. M., DeForest, D. K., Brigham, S. I., Adams, W. J., & Green, A. (2003). Inverse relationship between bioconcentration factor and exposure concentration for metals: implications for hazard assessment of metals in the aquatic environment. Environmental Toxicology and Chemistry, 22(5), 1017–1037.

    Article  CAS  Google Scholar 

  • Meijerink, A. M. J., Gieske, A. S. M., & Vekerdy, Z. (2005). Surface energy balance using satellite data for the water balance of a traditional irrigation-wetland system in SW Iran. Irrigation and Drainage Systems, 19, 89–105.

    Article  Google Scholar 

  • Ministry of Environment and Energy (MOEE). (1993). Guidelines for the protection and management of aquatic sediment quality in Ontario. Toronto: Queen’s Printer for Ontario ISBN 0-7729-9248-7.

    Google Scholar 

  • Mireji, P. O., Keating, J., Hassanali, A., Mbogo, C. M., Nyambaka, H., Kahindi, S., & Beier, J. C. (2008). Heavy metals in mosquito larval habitats in urban Kisumu and Malindi Kenya and their impact. Ecotoxicology and Environmental Safety, 70, 147–153.

    Article  CAS  Google Scholar 

  • Mitchell, M. K., & Stapp, W. B. (1995). Field manual for water quality monitoring: an environmental education program for schools (9th ed.). Ann Arbor: Green Project.

    Google Scholar 

  • Najafi, A., & Vatanfada, J. (2011). Environmental challenges in trans-boudary waters, case study: Hamoon Hirmand Wetland (Iran and Afghanistan). International Journal of Water Resources and Arid Environments, 1(1), 16–24.

    Google Scholar 

  • Nasirian, H. (2013). Using insects for heavy metal contamination survey in Shadegan Wetland. Thesis for fulfillment of the PhD Degree in Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences.

  • Nasirian, H. (2014). Evaluation of water quality and organic pollution of Shadegan and Hawr Al Azim wetlands by biological indices using insects. Journal of Entomology and Zoology Studies, 2(5), 193–200.

    Google Scholar 

  • Nasirian, H., Mahvi, A. H., Hosseini, M., Vazirianzadeh, B., Sadeghi, S. M., & Nazmara, S. (2013). Study on the heavy metal bioconcentrations of the Shadegan international wetland mosquitofish, Gambusia affinis, by inductively coupled plasma technique. Journal of Environmental Health Science & Engineering, 11, 22.

  • Nasirian, H., Vazirianzadeh, B., Sadeghi, S. M. T., & Nazmara, S. (2014a). Culiseta subochrea as a bioindicator of metal contamination in Shadegan international wetland, Iran (Diptera: Culicidae). Journal of Insect Science, 14(258), 1–5.

  • Nasirian, H., Sadeghi, S. M. T., Vazirianzadeh, B., & Moosa-Kazemi, S. H. (2014b). New record of Aedes vittatus and Culiseta subochrea (Diptera: Culicidae) and their distribution from Shadegan Wetland, South Western Iran. Journal of Entomology and Zoology Studies, 2, 271–275.

  • Nasirian, H., Nasirian, Z., & Sadeghi, S. M. T. (2014c). Use of inductively coupled plasma-mass spectrometry, ICP-MS, in entomology. International Journal of Entomological Research, 2(2), 47–57.

  • Nasirian, H., Nazmara, S., Mahvi, A. H., Hosseini, M., Shiri, L., & Vazirianzadeh, B. (2015). Assessment of some heavy metals in the Shadegan and Hawr Al Hawizea wetland waters from Iran. Indian Journal of Science and Technology, 8(33), 1–9.

    Article  CAS  Google Scholar 

  • Nasirian, H., Irvine, K. N., Sadeghi, S. M. T., Mahvi, A. H., & Nazmara, S. (2016). Assessment of bed sediment metal contamination in the Shadegan and Hawr Al Azim wetlands, Iran. Environmental Monitoring and Assessment, 188(2), 1–15.

    Article  CAS  Google Scholar 

  • Partow, H. (2001). The Mesopotamian Marshlands: demise of an ecosystem. Nairobi: UNEP Report.

    Google Scholar 

  • Pazira, E. & Homaee, M. (2010). Salt leaching efficiency of subsurface drainage systems at presence of diffusing saline water table boundary: a case study in Khuzestan Plains, Iran. In. XVIIth World Congress of the International Commission of Agriculture and Biosystems Engineering (CIGR), Quebec, Canada.

  • Pizl, V., & Josens, G. (1995). Earthworm communities along a gradient of urbanization. Environmental Pollution, 90, 7–14.

    Article  CAS  Google Scholar 

  • Rabitsch, W. B. (1995a). Metal accumulation in arthropods near a lead/zinc smelter in Arnoldstein, Austria. II. Formicidae. Environmental Pollution, 90, 239–247.

    Article  CAS  Google Scholar 

  • Rabitsch, W. B. (1995b). Metal accumulation in arthropods near a lead/zinc smelter in Arnoldstein, Austria. III. Arachnida Environmental Pollution, 90, 249–257.

    Article  CAS  Google Scholar 

  • Raburu, P. O., Masese, F. O., & Mulanda, C. A. (2009). Macroinvertebrate Index of Biotic Integrity (M-IBI) for monitoring rivers in the upper catchment of Lake Victoria Basin, Kenya. Aquatic Ecosystem Health & Management, 12(2), 197–205.

    Article  CAS  Google Scholar 

  • Reece, B. A., & McIntyre, N. E. (2009). Community assemblage patterns of odonates inhabiting a wetland complex influenced by anthropogenic disturbance. Insect Conservation and Diversity, 2(2), 73–80.

    Article  Google Scholar 

  • Remsburg, A. J., & Turner, M. G. (2009). Aquatic and terrestrial drivers of dragonfly (Odonata) assemblages within and among north-temperate lakes. Journal of the North American Benthological Society, 28(1), 44–56.

    Article  Google Scholar 

  • Richardson, C. J. (2010). The status of Mesopotamian Marsh restoration in Iraq: a case study of transboundary water issues and internal water allocation problems. In K. Korhonen-Kurki & M. Fox (Eds.), Towards new solutions in managing environmental crisis (pp. 59–72). Helsinki: Helsinki University Printing House.

    Google Scholar 

  • Ross, P. E., Burton, G. A., Crecelius, E. A., Filkins, J. C., Giesy, J. P., Ingersoll, C. G., Landrum, P. F., Mac, M. J., Murphy, T. J., Rathbun, J. E., Smith, V. E., Tatem, H. E., & Taylor, R. W. (1992). Assessment of sediment contamination at Great Lakes Areas of Concern: the ARCS Program Toxicity-Chemistry Work Group strategy. Journal of Aquatic Ecosystem Health, 1, 193–200.

    Article  Google Scholar 

  • Sadeghi, S., & Mohammadalizedeh, J. (2009). Additions to the Odonata fauna of Iran. Iranian Journal of Sciences & Technology, Transactions A, 33(A4), 355–359.

    Google Scholar 

  • Sato, M., & Riddiford, N. (2008). A preliminary study of the Odonata of S’Albufera Natural Park, Mallorca: status, conservation priorities and bio-indicator potential. Journal of Insect Conservation, 12, 539–548.

    Article  Google Scholar 

  • Scott, D. A. (2007). A review of the status of breeding waterbirds in Iran in the 1970s. Podoces, 2(1), 1–21.

    Google Scholar 

  • Silva, D., De Marco, P., & Resende, D. C. (2010). Adult odonate abundance and community assemblage measures as indicators of stream ecological integrity: A case study. Ecological Indicators, 10, 744–752.

    Article  CAS  Google Scholar 

  • Silveira, M. P., Baptista, D. F., Buss, D. F., Nessimian, J. L., & Egler, M. (2005). Application of biological measures for stream integrity assessment in South-East Brazil. Environmental Monitoring and Assessment, 101, 117–128.

    CAS  Google Scholar 

  • Simon, E., Kis, O., Jakab, T., Kolozsvári, I., Málnás, K., Harangi, S., et al. (2017). Assessment of contamination based on trace element concentrations in Gomphus flavipes (Odonata: insect) larvae of the Upper Tisza Region. Ecotoxicology and Environmental Safety, 136, 55–61.

    Article  CAS  Google Scholar 

  • Sow, A. Y., Ismail, A., & Zulkifli, S. Z. (2013). An assessment of heavy metal bioaccumulation in Asian Swamp Eel, Monopterus albus, during plowing stages of a paddy cycle. Bulletin Environmental Contamination and Toxicology, 91(1), 6–12.

    Article  CAS  Google Scholar 

  • Takamura, K., Hatakeyama, S., & Shiraishi, H. (1991). Odonate larvae as an indicator of pesticide contamination. Applied Entomology and Zoology, 26(3), 321–326.

    Google Scholar 

  • Tollett, V. D., Benvenutti, E. L., Deer, L. A., & Rice, T. M. (2009). Differential toxicity to Cd, Pb, and Cu in dragonfly larvae (Insecta: Odonata). Archives of Environmental Contamination and Toxicology, 56(1), 77.

    Article  CAS  Google Scholar 

  • Tulonen, T., Pihlström, M., Arvola, L., & Rask, M. (2006). Concentrations of heavy metals in food web components of small, boreal lakes. Boreal Environment Research, 11(3), 185–194.

    CAS  Google Scholar 

  • Turner, K. R., Georgio, S., & Fisher, B. (2011). Valuing ecosystem services, the case of multi-functional wetlands. Washington, D.C.: Earthscan.

    Google Scholar 

  • U.S.EPA. (2000). Bioaccumulation testing and interpretation for the purpose of sediment quality assessment, status and needs. U.S. EPA Report EPA-823-R-00-001. Washington, D.C.

  • Visoth, T., Yim, M., Vathna, S., Irvine, K., & Koottatep, T. (2010). Efficiency of Phnom Penh’s natural wetlands in treating wastewater discharges. Asian Journal of Water, Environment and Pollution, 7(3), 39–48.

    CAS  Google Scholar 

  • Wade, T. J., Pai, N., Eisenberg, J. N. S., & Colford, J. M. (2003). Do U.S. Environmental Protection Agency water quality guidelines for recreational waters prevent gastrointestinal illness? A systematic review and meta-analysis. Environmental Health Perspectives, 111(8), 1102–1109.

    Article  Google Scholar 

  • Watson, J. A. L., Arthington, A. H., & Conrick, D. L. (1982). Effect of sewage effluent on dragonflies (Odonata) of Bulimba Creek, Brisbane. Marine & Freshwater Research, 33(3), 517–528.

    Article  Google Scholar 

  • Weisberg, S. P., Ranasinghe, J. A., Dauer, D. M., Schaffner, L. C., Diaz, R. J., & Frithsen, J. B. (1997). An estuarine Benthic Index of Biotic Integrity (B-BI) for Cheasapeake Bay. Estuaries, 20(1), 149–158.

    Article  Google Scholar 

  • Widianarko, B., Van Gestel, C. A., Verweij, R. A., & Van Straalen, N. M. (2000). Associations between trace metals in sediment, water, and guppy, Poecilia reticulata (Peters), from urban streams of Semarang, Indonesia. Ecotoxicology and Environmental Safety, 46(1), 101–107.

    Article  CAS  Google Scholar 

  • Wong, P. T. S., Chau, Y. K., & Luxon, P. L. (1978). Toxicity of a mixture of metals on freshwater algae. Journal of the Fisheries Board of Canada, 35(4), 479–481.

    Article  CAS  Google Scholar 

  • Zarasvandi, A., Carranza, E. J. M., Moore, F., & Rastmanesh, F. (2011). Spatio-temporal occurrences and mineralogical-geochemical characteristics of airborne dusts in Khuzestan Province (southwestern Iran). Journal of Geochemical Exploration, 111, 138–151.

    Article  CAS  Google Scholar 

  • Zarghami, M. (2011). Effective watershed management; case study of Urmia Lake, Iran. Lake and Reservoir Management, 27, 87–94.

    Article  Google Scholar 

  • Zedler, J. B., & Kercher, S. (2005). Wetland resources: status, trends, ecosystem services, and restorability. Annual Review of Environmental Resources, 30, 39–74.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hassan Nasirian.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nasirian, H., Irvine, K. Odonata larvae as a bioindicator of metal contamination in aquatic environments: application to ecologically important wetlands in Iran. Environ Monit Assess 189, 436 (2017). https://doi.org/10.1007/s10661-017-6145-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-017-6145-6

Keywords

Navigation