Sains Malaysiana 52(2)(2023): 321-331

http://doi.org/10.17576/jsm-2023-5202-01

 

Monitoring Heavy Metal Bioaccumulation in Rivers Using Damselflies (Insecta: Odonata, Zygoptera) as Biological Indicator

(Memantau Bioakumulasi Logam Berat di dalam Sungai menggunakan Pepatung Jarum (Insecta: Odonata, Zygoptera) sebagai Penunjuk Biologi)

 

AHMAD HADRI JUMAAT & SUHAILA AB HAMID*


School of Biological Sciences, Universiti Sains Malaysia, 11800 Minden, Penang, Malaysia

 

Received: 1 June 2022/Accepted: 27 November 2022

 

Abstract

Contamination by pollutants in freshwater ecosystem has been identified extensively in river, sediments, and freshwater biota. Pollutants may have incorporated into the sediments and accumulated in tissue of aquatic organisms which persist as difficult to degrade matter in upper trophic level. Therefore, few selected heavy metals were measured from the river sediment and tissue of damselflies larvae collected from the selected rivers using inductively coupled plasma optical emission spectrometry (ICP-OES). The results showed metals in damselflies tissue were higher than in the sediments. Mn and Zn were found in greatest concentrations both in sediment and damselflies’s tissue. Biota-sediment accumulation factors (BSAF) were computed based on these data, and it was discovered that all values of BSAF for Cd, Cu, Mn, and Zn were typically high (BSAF >1). In conclusion, the rivers contamination induced accumulation of heavy metal in the river sediments and damselflies larvae (Pseudagrion microcephalum, Pruinosum fraseri, and Copera marginipes). The highest concentration value was calculated as 29.23 for Cd in the C. marginipes.  The high concentrations of this element in the insect body tissue has shown a trace of bioaccumulation and may pose biomagnification to organisms in the upper trophic level. The results of this study indicated that damselfly is reliable to become a bioindicator for heavy metals particularly pollution in the river.

 

Keywords: Aquatic insects; bioaccumulation; heavy metals; sediments

 

Abstrak

Pencemaran oleh bahan pencemar dalam ekosistem air tawar telah dikenal pasti secara meluas dalam sungai, sedimen dan biota air tawar. Bahan pencemar mungkin telah meresap ke dalam sedimen dan terkumpul di dalam tisu organisma akuatik yang berterusan sebagai sukar untuk diuraikan pada aras trofik teratas. Oleh itu, beberapa logam berat terpilih diukur daripada sedimen sungai dan tisu larva pepatung jarum yang dikumpul daripada sungai terpilih menggunakan spektrometri pelepasan optik plasma (ICP-OES) yang digabungkan secara induktif. Keputusan menunjukkan logam dalam tisu pepatung jarum lebih tinggi daripada dalam sedimen. Mn dan Zn didapati dalam kepekatan terbesar untuk sedimen dan tisu pepatung jarum. Faktor pengumpulan biota-sedimen (BSAF) telah dihitung berdasarkan data ini dan didapati bahawa semua nilai BSAF untuk Cd, Cu, Mn dan Zn adalah tinggi (BSAF >1). Kesimpulannya, pencemaran sungai menyebabkan pengumpulan logam berat dalam sedimen sungai dan larva pepatung jarum (Pseudagrion microcephalum, Pruinosum fraseri dan Copera marginipes). Nilai kepekatan tertinggi dihitung sebagai 29.23 untuk Cd dalam tisu C. marginipes. Kepekatan tinggi unsur ini dalam tisu badan serangga telah menunjukkan kesan bioakumulasi dan mungkin menimbulkan pembesaran biologi kepada organisma pada aras trofik atas. Hasil kajian ini menunjukkan bahawa pepatung jarum boleh digunakan sebagai penunjuk biologi bagi logam berat khususnya pencemaran di sungai.

 

Kata kunci: Bioakumulasi; logam berat; sedimen; serangga akuatik

 

REFERENCES

Addo-Bediako, A. & Malakane, K. 2020. Preliminary assessment of chemical elements in sediments and larvae of Gomphidae (Odonata) from the Blyde River of the Olifants River System, South Africa. International Journal of Environmental Research and Public Health 17(21): 8135.

Ben-Shahar, Y. 2018. The impact of environmental Mn exposure on insect biology. Frontier Genetics 9: 70.

Bhat, R.A., Shafiq-ur-Rehman, M.M.A., Dervash, M.A., Mushtaq, N., Bhat, J.I.A. & Dar, G.H. 2017. Current status of nutrient load in Dal Lake of Kashmir Himalaya. Journal Pharmacognosy Phytochemistry 6(6): 165-169.

Bouchelouche, D. & Abdeslem, A. 2019. Bioaccumulation of heavy metals in an aquatic insect (Baetis pavidus; Baetidae; Ephemeroptera) in the El Harrach Wadi (Algeria). Arabian Journal of Geosciences 13: 672-686.

Božanić, M., Todorović, D., Živić, M., Perić-Mataruga, V., Marković, Z. & Živić, I. 2018. Influence of a trout farm on antioxidant defense in larvae of Ephemera danica (Insecta: Ephemeroptera). Knowledge and Management Aquatic Ecology 47: 419-447.

Briffa, J., Sinagra, E. & Blundell, R. 2020. Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon6(9): 1-26.

Buchwalter, D.B., Cain, D.J., Clements, W.H. & Luoma, S.N. 2007. Using biodynamic modelsto reconcile differences between laboratory toxicity tests and field biomonitoring with aquatic insects. Environmental Science Technology 41(13): 4821-4828.

César Dos Santos Lima, J., Gazonato Neto, A.J., de Pádua Andrade, D., Freitas, E.C., Moreira, R.A., Miguel, M., Daam, M.A. & Rocha, O. 2019. Acute toxicity of four metals to three tropical aquatic invertebrates: The dragonfly Tramea cophysa and the ostracods Chlamydotheca sp. and Strandesia trispinosa. Ecotoxicology and Environmental Safety 180: 535-541.

Cezário, R.R., Firme, P.P., Pestana, G.C., Vilela, D.S. & Juen, L. 2020. Sampling methods for dragonflies and damselflies. In Measuring Arthropod Biodiversity, edited by Santos, J.C. & Fernandes, G.W. Springer Nature Switzerland. pp. 223-240.

Cham, S. 2012. Field Guide to the Larvae and Exuviae of British Dragonflies: Damselflies (Zygoptera) and Dragonflies (Anisoptera). British Dragonfly Society.

Cid, N., Ibánez, C., Palanques, A. & Prat, N. 2010. Patterns of metal bioaccumulation in two filter-feeding macroinvertebrates: Exposure distribution, inter-species differences and variability across developmental stages. Science Total Environment 408: 2795-2806.

de Barros, C.M., da Fonte Carvalho Martins, D., Mello, A.D.A., Salgado, L.T. & Allodi, S. 2017. Nitric-oxide generation induced by metals plays a role in their accumulation by Phallusia nigra hemocytes. Marine Pollution Bulletin 124: 441-448.

Dittman, E.K. & Buchwalter, D.B. 2010. Manganese bioconcentration in aquatic insects: Mn oxide coatings, molting loss, and Mn (II) thiol scavenging. Environment Sciences Technology 44: 9182-9188.

Ekubo, A.J. & Abowel, J.F.N. 2011. Aspects of aquatic pollution in Nigeria. Researches of Journal Environmental Earth Science 3: 673-693.

Gheorghe, S., Catalina, S., Gabriela, G.V., Mihai, N., Elena, S. & Irina, E.L. 2017. Metals toxic effects in aquatic ecosystems: Modulators of water quality. Water Quality 87: 59-89.

Girardin, V., Grung, M. & Meland, S. 2020. Polycyclic aromatic hydrocarbons: Bioaccumulation in dragonfly nymphs (Anisoptera), and determination of alkylated forms in sediment for an improved environmental assessment. Scientific Reports 10(1): 1-14.

Golovanova, I.L. 2008. Effects of heavy metals on the physiological and biochemical status of fishes and aquatic invertebrates. Inland Water Biology 1: 93.

Guimarães, S.R.D.M., Corbi, J.J. & Giuliano, B.J. 2019. Aquatic insects as bio-indicators of heavy metals in sediments in Cerrado streams. Limnetica 38(2): 575-586.

Hampel, M., Blasco, J. & Segner, H. 2015. Molecular and cellular effects of contamination in aquatic ecosystems. Environmetal Science and Pollution Research 22: 17261-17266.

Harguinteguy, C.A., Cirelli, A.F. & Pignata, M.I. 2014. Heavy metal accumulation in leaves of aquatic plant Stuckenia filiformis and its relationship with sediment and water in the Suquía River (Argentina). Microchemical Journal 114: 111-118.

Huang, L., Rad, S., Xu, L., Gui, L., Song, X., Li, Y., Wu, Z. & Chen, Z. 2020. Heavy metals distribution, sources, and ecological risk assessment in Huixian Wetland, South China. Water 12: 431.

Iqra Azam, Sumera, A., Ahmed, Z., Muqaddas, J., Rashid, S., Muhammad, K.S. & Bushra, M. 2015. Evaluating insects as bioindicators of heavy metal contamination and accumulation near industrial area of Gujrat, Pakistan. Journal of Biomedicine and Biotechnology 2015: 942751.

Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B.B. & Beeregowda, K.N. 2014. Toxicity, mechanism and health effects of some heavy metals. Interdiscipline Toxicology 7(2): 60-72.

Jones, J.I., Davy-Bowker, J., Murphy, J.F. & Pretty, J.L. 2010. Ecological monitoring and assessment of pollution in rivers. In Ecology of Industrial Pollution, edited by Batty, L.C. & Hallberg, K.B. Cambridge: Cambridge University Press. pp. 126-146.

Kouidri, M., Youcef, N.D., Benabdellah, I., Ghoubali, R., Bernoussi, A. & Lagha, A. 2016. Enrichment and geoaccumulation of heavy metals and risk assessment of sediments from coast of Ain Temouchent (Algeria). Arab Journal Geoscience 9: 354.

Krång, A.S. & Rosenqvist, G. 2006. Effects of manganese on chemically induced food search behaviour of the Norway lobster, Nephrops norvegicus (L.). Aquatic Toxicology 78(3): 284-291.

Kraus, J.M., Schmidt, T.S., Walters, D.M., Wanty, R.B., Zuellig, R.E. & Wolf, R.E. 2014. Cross-ecosystem impacts of stream pollution reduce resource and contaminant flux to riparian food webs. Ecological Applications 24(2): 235-243.

Kula, E., Martinek, P., Chromcová, L. & Hedbávný, J. 2014. Development of Lymantria dispar affected by manganese in food. Environmental Science Pollution Research 21: 11987-11997.

Lavilla, I., Rodriguez-Linares, G., Garrido, J. & Bendicho, C.A. 2010. Biogeochemical approach to understanding the accumulation patterns of trace elements in three species of dragonfly larvae: Evaluation as biomonitors. Journal Environmental Monitoring 12: 724-730.

Liu, M., Zhong, J., Zheng, X., Yu, J., Liu, D. & Fan, C. 2018. Fraction distribution and leaching behavior of heavy metals in dredged sediment disposal sites around Meiliang Bay, Lake Taihu (China). Environmental Science Pollution Research 25: 9737-9744.

Luo, M., Finet, C., Cong, H., Wei, H. & Chung, H. 2020. The evolution of insect metallothioneins. Proceedings of the Royal Society B: Biological Sciences 287: 1937.

Martinek, P., Kula, E. & Hedbávný, J. 2018. Reactions of Melolontha hippocastani adults to high manganese content in food. Ecotoxicology Environmental Safety 148: 37-43.

Mendes, T.M., Benone, N.L. & Juen, L. 2019. To what extent can oil palm plantations in the Amazon support assemblages of Odonata larvae? Insect Conservation Diversity 12(5): 448-558.

Nasirian, H. & Irvine, K.N. 2017. Odonata larvae as a bioindicator of metal contamination in aquatic environments: Application to ecologically important wetlands in Iran. Environmental Monitoring Assessment 189: 436.

Nenciu, M., Oros, A., Roşioru, D., Galatchi, M., Filimon, A., Tiganov, G., Danilov, C. & Roşoiu, N. 2016. Heavy metal bioaccumulation in marine organisms from the Romanian Black Sea coast. Academy of Romanian Scientists 5(1): 38-52.

Nenciu, I.M., Coatua, V., Orosa, A., Rosiorua, D., Tiganus, D. & Rosoiub, N. 2014. Pollutant bioaccumulation in the long-snouted seahorse at the Romanian coast. Journal of Environmental Protection and Ecology 15(4): 1650-1659.

Oweson, C., Sköld, H., Pinsino, A., Matranga, V. & Hernroth, B. 2008. Manganese effects on haematopoietic cells and circulating coelomocytes of Asterias rubens (Linnaeus). Aquatic Toxicology 89: 75-81.

Petrova, S., Yurukova, L. & Velcheva, I. 2013. Taraxacum officinale as a biomonitor of metals and toxic elements (Plovdiv, Bulgaria). Bulgarian Journal of Agricultural Science 19(2): 241-247.

Poteat, M.D., Díaz-Jaramillo, M. & Buchwalter, D.B. 2012. Divalent metal (Ca, Cd, Mn, Zn) uptake and interactions in the aquatic insect Hydropsyche sparna. Journal Experimental Biology 215: 1575-1583.

Prommi, T.O. & Payakka, A. 2018. Monitoring cadmium concentrations in sediments and aquatic insects (Hydropsychidae: Trichoptera) in a stream near a zinc mining area. Polish Journal of Environmental Studies 27(5): 2237-2243.

Reda, A.H. & Ayu, A.A. 2016. Accumulation and distribution of some selected heavy metals in both water and some vital tissues of two fish species from Lake Chamo Ethiopia. International Journal Fisheries Aquatic Studies 4: 6-12.

Rokytova, L., Kula, E., Kodarova, L. & Peslova, A. 2004. Feeding of the willow leaf beetle Lochmaea capreae L. (Coleoptera, Chrysomelidae) on leaves of birch (Betula pendula Roth) contaminated by heavy metals. Journal Forest Sciences 50: 109-117.

Rosado, D., Usero, J. & Morillo, J. 2016. Assessment of heavy metals bioavailability and toxicity toward Vibrio fischeri in sediment of the Huelva estuary. Chemosphere 153: 10-17.

Shahbaz, M., Hashmi, M.Z., Malik, R.N. & Yasmin, A. 2013. Relationship between heavy metals concentrations in egret species, their environment and food chain differences from two headworks of Pakistan. Chemosphere 93: 274-282.

Simon, E., Kisb, O., Jakabc, T., Kolozsvárid, I., Málnáse, K., Harangia, S. & Baranyaif. 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.

Simon, E., Tóthmérész, B., Kis, O., Jakab, T., Éva Szalay, P., Vincze, A., Baranyai, E., Harangi, S., Miskolczi, M. & Dévai, G. 2019. Environmental-friendly contamination assessment of habitats based on the trace element content of dragonfly exuviae. Water 11(11): 2200. 

Theischinger, G. & Endersby, I. 2014Australian Dragonfly (Odonata) larvae: Descriptive history and identification. Memoirs of Museum Victoria 72: 73-120.

Triquet-Amiard, C., Amiard, J.C. & Rainbow, P.S. 2013. Ecological Biomarkers: Indicators of Ecotoxicological Effects. CRC Press, Taylor & Francis Group. p. 450.

Villalobos-Jiménez, G., Alison, M.D. & Christopher, H. 2016. Dragonflies and damselflies (Odonata) in urban ecosystems: A review. European Journal Entomology 113: 217-232.

Wesner, J.S., Kraus, J.M., Schmidt, T.S., Walters, D.M. & Clements, W.H. 2014. Metamorphosis enhances the effects of metal exposure on the mayfly, Centroptilum triangulifer. Environmental Science & Technology 48: 10415-10422.

Wojtkowska, M., Bogacki, J. & Witeska, A. 2016. Assessment of the hazard posed by metal forms in water and sediments. Science Total Environment 551-552: 387-392.

Zaghloul, A., Saber, M., Gadow, S. & Awad, F. 2020. Biological indicators for pollution detection in terrestrial and aquatic ecosystems. Bulletin of the National Research Centre 44: 127.

Ziyaadini, M., Yousefiyanpour, Z. & Ghasemzadeh, J. 2017. Biota-sediment accumulation factor and concentration of heavy metals (Hg, Cd, As, Ni, Pb and Cu) in sediments and tissues of Chiton lamyi (Mollusca: Polyplacophora: Chitonidae) in Chabahar Bay, Iran. Iran Journal Fish Sciences 16(4): 1123-1134.

 

*Corresponding author; email: ahsuhaila@usm.my