Abstract
Free-living birds play an important role as bioindicators in natural environments. In this study, we used the micronucleus test and nuclear erythrocyte abnormalities to investigate the difference in the genotoxic damage frequency between animals in agricultural areas (soybean planting) in relation to the conserved area. It was also discussed the bird’s eating habits, which are important for ecotoxicological analysis. The results point to a difference between the insectivorous, granivorous, and omnivorous guilds. The omnivore Gnorimopsar chopi was the species that most exhibited micronucleus frequency in the protected area. In the agricultural area, the animals did not differ in the genotoxic damage frequency. In the comparison between common species in both environments, G. chopi from the agricultural area showed a micronuclei frequency almost three times higher in relation to specimens collected in the conserved area. Based on these results, this study adds to the efforts of using the micronucleus test as a simple and accessible tool for biomonitoring the wild fauna. It can be concluded that the passerine, G. chopi, due to its higher genotoxic damage frequency may be a strong candidate to indicate environmental health.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
References
Adam ML, Torres RA, Kiska M, Oliveira FF, Lacerda O, Sponchiado G, Ribas CMO, Correia MTS (2013) Assessment of genome damage in bird and mammal species as a tool for improvements in ex-situ conservation at zoos. Nat Conserv 11:59–64. https://doi.org/10.4322/natcon.2013.010
Assis RA, Rezende WR, Dos Santos CGA, Benvindo-Souza M, Amorim NPL, Borges RE, Franco-Belussi L, De Oliveira C, de Souza Santos LR (2021) Habitat differences affect the nuclear morphology of the erythrocytes and the hepatic melanin in Leptodactylus fuscus (Anura) in the Brazilian Cerrado savanna. Environ Sci Pollut Res 24. https://doi.org/10.1007/s11356-021-14974-4
Baesse CQ, Tolentino VCD, da Silva AM, Silva AD, Ferreira GA, Paniago LPM, Nepomuceno JC, de Melo C (2015) Micronucleus as biomarker of genotoxicity in birds from Brazilian Cerrado. Ecotox Environ Safe 115:223–228. https://doi.org/10.1016/j.ecoenv.2015.02.024
Baesse CQ, Tolentino VCD, Morelli S, Melo C (2019) Effect of urbanization on the micronucleus frequency in birds from forest fragments. Ecotox Environ Saf 171:631–637. https://doi.org/10.1016/j.ecoenv.2019.01.026
Barbosa A, De Mas E, Benzal J, Diaz JI, Motas M, Jerez S, Pertierra L, Benayas J, Justel A, Lauzurica P, Garcia-Pena FJ, Serrano T (2013) Pollution and physiological variability in gentoo penguins at two rookeries with different levels of human visitation. Antarct Sci 25:329–338. https://doi.org/10.1017/S0954102012000739
Benvindo-Souza M, Borges RE, Pacheco SM, Santos LRD (2019a) Genotoxicological analyses of insectivorous bats (Mammalia: Chiroptera) in central Brazil: The oral epithelium as an indicator of environmental quality. Environ Pollut 245:504–509. https://doi.org/10.1016/j.envpol.2018.11.015
Benvindo-Souza M, Borges RE, Pacheco SM, Santos LRS (2019b) Micronucleus and other nuclear abnormalities in exfoliated cells of buccal mucosa of bats at different trophic levels. Ecotox Environ Saf 172:120–127. https://doi.org/10.1016/j.ecoenv.2019.01.051
Benvindo-Souza M, Oliveira EAS, Assis RA, Santos CGA, Borges RE, Silva DM, Santos LRS (2020) Micronucleus test in tadpole erythrocytes: trends in studies and new paths. Chemosphere 240:124910. https://doi.org/10.1016/j.chemosphere.2019.124910
Bichsel D, De Marco P, Bispo AA, Ilg C, Dias-Silva K, Vieira TB, Correa CC, Oertli B (2016) Water quality of rural ponds in the extensive agricultural landscape of the Cerrado (Brazil). Limnology 17:239–246. https://doi.org/10.1007/s10201-016-0478-7
Bouam I, Bachir ASI, Katayama N (2017) Variation in bird assemblages along an agricultural intensification gradient: a case study of olive orchards in north-eastern Algeria. Ornithol Sci 16:147–157. https://doi.org/10.2326/osj.16.147
Borges RE, Santos LRD, Benvindo-Souza M, Modesto RS, Assis RA, de Oliveira C (2019a) Genotoxic Evaluation in Tadpoles Associated with Agriculture in the Central Cerrado. Brazil Arch Environ Contam Toxicol 77:22–28. https://doi.org/10.1007/s00244-019-00623-y
Borges FJA, Ribeiro BR, Lopes LE, Loyola R (2019b) Bird vulnerability to climate and land use changes in the Brazilian Cerrado. Biol Conserv 236:347–355. https://doi.org/10.1016/j.biocon.2019.05.055
Bosch B, Gorla N, Aiassa D (2011) Micronucleus test in post metamorphic Odontophrynus cordobae and Rhinella arenarum (Amphibia: Anura) for environmental monitoring. J Toxicol Environ Health Sci 3:155–163
BLI (2020) Bird Life International. Available in: http://www.birdlife.org/. Accessed 3 Aug 2020
Bhunya SP, Jena GB (1992) Genotoxic potential of the organochlorine insecticide lindane (gamma-BHC): an in vivo study in chicks. Mutat Res 272:175–181. https://doi.org/10.1016/0165-1161(92)90045-N
Bhunya SP, Jena GB (1993) Studies on the genotoxicity of monocrotophos, an organophosphate insecticide, in the chick in vivo test system. Mutat Res 292:231–239. https://doi.org/10.1016/0165-1161(93)90026-V
de Faria DBG, Montalvao MF, de Souza JM, Mendes BD, Malafaia G, Rodrigues ASD (2018) Analysis of various effects of abamectin on erythrocyte morphology in Japanese quails (Coturnix japonica). Environ Sci Pollut Re 25:2450–2456. https://doi.org/10.1007/s11356-017-0677-8
Ceyca-Contreras JP, Cortés-Gutiérrez EI, García-Salas JA, Dávila-Rodríguez MI, García-Hernández J (2020) Evaluation of the genotoxic effect of heavy metals in pigeons from urban and rural habitat in Monterrey, Mexico, using the chromatin dispersion assay. Biomarkers 25:670–676. https://doi.org/10.1080/1354750X.2020.1825811
de Mas E, Benzal J, Merino S, Valera F, Palacios MJ, Cuervo JJ, Barbosa A (2015) Erythrocytic abnormalities in three Antarctic penguin species along the Antarctic Peninsula: biomonitoring of genomic damage. Polar Biol 38:1067–1074. https://doi.org/10.1007/s00300-015-1667-2
de Lima MG (2003) Ecologia da paisagem e cenários para a conservação da aviifauna na região do Parque Nacional das Emas. GO. Diss. Doctoral thesis, Postgraduate Program in Ecology, Department of Ecology, Institute of Biology, University of Brasilia
de Oliveira JSP, Vieira LG, Carvalho WF, de Souza MB, de Lima Rodrigues AS, Simões K, de Melo e Silva D, dos Santos Mendonça J, Hirano LQL, Santos ALQ, Malafaia G (2020) Mutagenic, genotoxic and morphotoxic potential of different pesticides in the erythrocytes of Podocnemis expansa neonates. Sci Total Environ 737:140304. https://doi.org/10.1016/j.scitotenv.2020.140304
Eiten G (1993) Vegetação do cerrado. Pp. 17–73 in Pinto, M. N. (ed.). Cerrado: caracterização, ocupação e perspectivas. Ed. Univ. Brasília, Brasília
Fenech M (2000) The in vitro micronucleus technique. Mutat Res 455:81–95. https://doi.org/10.1016/s0027-5107(00)00065-8
Ferreira ME, Ferreira LG, Miziara F, Soares-Filho BS (2013) Modeling landscape dynamics in the central Brazilian savanna biome: future scenarios and perspectives for conservation. J Land Use Sci 8:403–421. https://doi.org/10.1080/1747423X.2012.675363
Gomes MP, Cruz FVD, Bicalho EM, Borges FV, Fonseca MB, Juneau P, Garcia QS (2017) Effects of glyphosate acid and the glyphosate-commercial formulation (Roundup) on Dimorphandra wilsonii seed germination: Interference of seed respiratory metabolisme. Environ Pollut 220:452–459. https://doi.org/10.1016/j.envpol.2016.09.087
Gonçalves MW, Vieira TB, Maciel NM, Carvalho WF, Lima LSF, Gambale PG, Cruz AD, Nomura F, Bastos RP, Silva DM (2015) Detecting genomic damages in the frog Dendropsophus minutus: preserved versus perturbed areas. Environ Sci Pollut Res 22:3947–3954. https://doi.org/10.1007/s11356-014-3682-1
Gonçalves VF, Ribeiro PVA, Oliveira CFD, Pires LP, Baesse CQ, Paniago LPM, Toletino VCG, de Melo C (2020) Effects of urban proximity and the occurrence of erythroplastids in Antilophia galeata. Environ Sci Pollut Res 27:44650–44655. https://doi.org/10.1007/s11356-020-10057-y
González-Acevedo A, García-Salas JA, Gosálvez J, Fernández JL, Dávila-Rodríguez MI, Cerda-Flores RM, Méndez-Lopez LF, Cortés-Gutiérrez EI (2016) Evaluation of environmental genotoxicity by comet assay in Columba livia. Toxicol Mech Methods 26:61–66. https://doi.org/10.3109/15376516.2015.1114059
Ghaffar A, Hussain R, Khan A, Abbas RZ, Aslam S, Mehreen M, Rani K (2015) Hemato-biochemical and testicular changes induced by subchronic doses of triazophos in male Japanese quail. Pak J Agric Sci 52:801–807
Grecchi RC, Gwyn QHJ, Bénié GB, Formaggio AR, Fahl FC (2014) Land use and land cover changes in the Brazilian Cerrado: A multidisciplinary approach to assess the impacts of agricultural expansion. Appl Geogr 55:300–312. https://doi.org/10.1016/j.apgeog.2014.09.014
Hussain R, Mahmood F, Khan A, Javed MT, Rehan S, Mehdi T (2012) Cellular and biochemical effects induced by atrazine on blood of male Japanese quail (Coturnix japonica). Pestic Biochem Physiol 103:38–42. https://doi.org/10.1016/j.pestbp.2012.03.001
Hussain R, Mahmood F, Khan A (2015) Genotoxic and pathological effects of malathion in male japanese quail (Coturnix japonica). Pak J Agri Sci 52:1149–1156
Hussain R, Ghaffar A, Ali HM, Abbas RZ, Khan JA, Khan IA, Ahmad I, Iqbal Z (2017) Analysis of different toxic impacts of Fipronil on growth, hemato-biochemistry, protoplasm and reproduction in adult cockerels. Toxin Reviews. https://doi.org/10.1080/15569543.2017.1366921
IMB (2018) Instituto Mauro Borges de estatística e estudos socieconómicos. Available in: http://www.imb.go.gov.br/viewrele.asp?cd_assunto=5&cd_anomes=20140000. Accessed 14 Jul 2018
ICMBio (2019) Instituto Chico Mendes do Ministério do Meio Ambiente. Parque Nacional das Emas. Available in: https://assiste.icmbio.gov.br/portal/visitacao1/unidades-abertas-a-visitacao/204-parque-nacional-das-emas. Accessed 5 Dec 2019
Kontas S, Bostanci D (2020) Genotoxic Effects of Environmental Pollutant Heavy Metals on Alburnuschalcoides (Pisces: Cyprinidae) Inhabiting Lower Melet River (Ordu, Turkey). Bull Environ Contam Toxicol 104:763–769. https://doi.org/10.1007/s00128-020-02857-2
Krebs CJ (1989) Ecological Methodology. Harper and Row Publications, New York
Osman A, Hamed M, Sayed A (2019) Protective role of Spirulina platensis against UVA-induced haemato-biochemical and cellular alterations in Clarias gariepinus. J Photoch Photobio B 191:59–64. https://doi.org/10.1016/j.jphotobiol.2018.12.013
Pignati WA, Lima FANDS, Lara SSD, Correa MLM, Barbosa JR, Leão LHDC, Pignatti MG (2017) Spatial distribution of pesticide use in Brazil: a strategy for Health Surveillance. Cien Saude Colet 22:3281–3293. https://doi.org/10.1590/1413-812320172210.17742017
Pinhatti VR, da Costa AM, Breyer AS, Pereira RA, da Silva J (2006) Determinação de danos basais no DNA de araras canindé (Ara ararauna) através do Teste de Micronúcleos: uma ferramenta na avaliação da saúde animal e seu uso no biomonitoramento da poluição ambiental. Acta Sci Vet 34:313–317
Quero AAM, Ferre DM, Zarco A, Cuervo PF, Gorla NBM (2016) Erythrocyte micronucleus cytome assay of 17 wild bird species from the central Monte desert, Argentina. Environ Sci Pollut Res 23:25224–25231. https://doi.org/10.1007/s11356-016-7638-5
Rocha C, Matia R, Aguiar LM, Melo-Silva C, Gonçalves BB, Mesquita-Neto JN (2015) Caracterização da avifauna em áreas de cerrado no Brasil Central. Acta Biol Catarin 2:49–63
Salek M, Brlik V, Kadava L, Praus L, Studecky J, Vrana J, Gamero A (2020) Year-round relevance of manureheaps and its conservation potential for declining farmland birds in agricultural landscape. Agr Ecosyst Environ 301:107032. https://doi.org/10.1016/j.agee.2020.107032
Santos CSA, Brandão R, Monteiro MS, Bastos AC, Soares AMVM, Loureiro S (2017) Assesment of DNA damage in Ardea cinerea and Ciconia ciconia: A 5-year study in Portuguese birds retrieved for rehabilitation. Ecotoxicol Environ Saf 136:104–110. https://doi.org/10.1016/j.ecoenv.2016.10.039
Sandoval-Herrera N, Castillo JP, Montalvo LGH, Welch KC (2021) Micronucleus Test Reveals Genotoxic Effects in Bats Associated with Agricultural Activity. Environ Toxicol Chem 40:202–207. https://doi.org/10.1002/etc.4907
Silva FC, Silva GG, Chagas MO, Jung DMH (2014) Bird community composition in an urban area in southern Brazil. Neotrop Biol Conserv 9:78–90. https://doi.org/10.4013/nbc.2014.92.02
Simonyan A, Hovhannisyan G, Sargsyan A, Arakelyan M, Minasyan S, Aroutiounian R (2018) DNA damage and micronuclei in parthenogenetic and bisexual Darevskia rock lizards from the areas with different levels of soil pollution. Ecotoxicol Environ Saf 154:13–18. https://doi.org/10.1016/j.ecoenv.2018.02.025
Souto HN, Campos Júnior EO, Campos CF, Rodrigues TS, Pereira BB, Morelli S (2018) Biomonitoring birds: the use of a micronuclei test as a tool to assess environmental pollutants on coffee farms in southeast Brazil. Environ Sci Pollut Res 25:24084–24092. https://doi.org/10.1007/s11356-018-2466-4
Shake CS, Moorman CE, Riddle JD, Burchell MR (2012) Influence of Patch Sizeand Shape on Occupancy by Shrubl and Birds. Condor 114:268–278
Sharaf S, Khan A, Khan MZ, Aslam F, Saleemi MK, Mahmood F (2010) Clinico-hematological and micronuclear changes induced by cypermethrin in broiler chicks: their attenuation with vitamin E and selenium. Exp Toxicol Pathol 62:333–341. https://doi.org/10.1016/j.etp.2009.05.002
Shepherd GL, Somers CM (2012) Adapting the Buccal Micronucleus Cytome Assay for Use inWild Birds: Age and Sex Affect Background Frequency in Pigeons. Environ Mol Mutagen 53:136–144. https://doi.org/10.1002/em.21673
Tubelis DP, Cavalcanti RB (2001) Community similarity and abundance of bird species in open habitats of a central Brazilian Cerrado. Ornitol Neotrop 12:57–73
Tsarpali V, Kassara C, Barboutis C, Papadimitraki M, Kloukinioti M, Giokas S, Dailianis S (2020) Assessing the seasonal and intrinsic variability of neurotoxic and cyto-genotoxic biomarkers in blood of free-living Eleonoras’ falcons. Sci Total Environ 711:135101. https://doi.org/10.1016/j.scitotenv.2019.135101
Vitorino BD, Rodrigues MB, da Frota AVB, de Avelar DM, Rodrigues WL, Castrillon SKI, da Silva Nunes JR (2018) Birds of rural landscape in the Midwest region of the state of Minas Gerais, Brazil. Neotrop Biol Conserv 13:62–73. https://doi.org/10.4013/nbc.2018.131.08
Acknowledgements
Although the study was not funded, some authors thank their research grants, such as the Coordination for the Improvement of Higher Education Personnel—Brazil (CAPES) and the Brazilian Fund for Biodiversity. We would like to thank Instituto Federal Goiano, campus Rio Verde for research support. We would also like to thank Marcos da Silva Cunha, manager of the Parque Nacional das Emas for his support in the unit.
Author information
Authors and Affiliations
Contributions
Elaine Divina Rodrigues Silveira Oliveira: writing (original draft), conceptualization, methodology, formal analysis. Marcelino Benvindo Souza: writing (original draft), conceptualization, methodology, formal analysis. Rhayane Alves Assis: conceptualization, methodology. Cirley Gomes Araújo dos Santos: conceptualization, methodology. Nathan Pereira de Lima Amorim: conceptualization, methodology. Rinneu Elias Borges: supervision, writing (original draft). Celine de Melo: supervision. Lia Raquel Souza Santos: conceptualization, methodology, supervision, writing (original draft).
Corresponding author
Ethics declarations
Ethical approval
This study was approved by the Ethics Committee on the Use of Animals of the Instituto Federal Goiano (n. 2295300119) and by the Chico Mendes Institute for Biodiversity Conservation (n. 67504–1).
Consent to participate
All authors participated in this work.
Consent to publish
All authors agree to publish.
Conflict of interest
The authors declare 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
About this article
Cite this article
Silveira, E.D.R., Benvindo-Souza, M., Assis, R.A. et al. Micronucleus and different nuclear abnormalities in wild birds in the Cerrado, Brazil. Environ Sci Pollut Res 29, 14279–14287 (2022). https://doi.org/10.1007/s11356-021-16845-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16845-4