Abstract
Stressing agents can cause morphophysiological and behavioural changes in several animals, including birds, which are good study models for environmental biomonitoring. The heterophil/lymphocyte ratio (H/L) is an efficient indicator of chronic stresses in birds. In this study, we aimed to compare the H/L ratio of birds between the areas with different levels of urbanisation, anthropogenic noise and carbon monoxide (CO) emission rates. A total of 1288 birds were captured in six Cerrado forest fragments between 2013 and 2019, from which we took blood samples to produce blood smears. In each of these fragments, the noise level was measured with a sound pressure level metre. The CO rates were obtained from the National Institute for Space Research database (INPE-Brazil). There was a higher H/L ratio in individuals captured in urban areas or close to urbanisation with high anthropogenic noise levels and high CO rates, and a lower H/L ratio in individuals from preserved areas, far from urban environments with low noise levels and low CO rates. Six species (Antilophia galeata, Leoptopogon amaurocephalus, Cnemotriccus fuscatus, Lathrotriccus euleri, Turdus leucomelas and Eucometis penicillata) showed a significant difference between the areas and followed the pattern shown by the individuals. The present study showed that birds living in the urban and peri-urban sites have higher values of H/L ratio than birds from rural sites. These results suggest that the H/L ratio can be used as an environmental biomonitoring tool and an efficient parameter to assess chronic stress in birds in degraded environments.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analysed during this study are included in this published article.
References
Baesse CQ, Tolentino VCM, Silva AM, Silva AA, Ferreira GÂ, Paniago LPM, Melo C (2015) Micronucleus as biomarker of genotoxicity in birds from Brazilian Cerrado. Ecotoxicol Environ Saf 115:223–228. https://doi.org/10.1016/j.ecoenv.2015.02.024
Baesse CQ, Tolentino VCM, Morelli S, Melo C (2019) Effect of urbanization on the micronucleus frequency in birds from forest fragments. Ecotoxicol Environ Saf 171:631–637. https://doi.org/10.1016/j.ecoenv.2019.01.026
Baesse CQ (2019) Análise de micronúcleos em aves como ferramenta de biomonitoramento do efeito da poluição em ambientes florestais e urbanos. PhD Thesis, Universidade Federal de Uberlândia. https://doi.org/10.14393/ufu.te.2019.2450
Bauerová P, Vinklerová J, Hraníček J, Čorba V, Vojtek L, Svobodová J, Vinkler M (2017) Associations of urban environmental pollution with health-related physiological traits in a free-living bird species. Sci Total Environ 601:1556–1565. https://doi.org/10.1016/j.scitotenv.2017.05.276
Bauerová P, Krajzingrová T, Těšický M, Velová H, Hraníček JM, S, Albrecht T, Vinkler M, (2020) Longitudinally monitored lifetime changes in blood heavy metal concentrations and their health effects in urban birds. Sci Total Environ 723:138002. https://doi.org/10.1016/j.scitotenv.2020.138002
Bedanova I, Chloupek J, Chloupek P, Knotkova Z, Voslarova E, Pistekova V, Vecerek V (2010) Responses of peripheral blood leukocytes to chronic intermittent noise exposure in broilers. Berliner und Münchener Tierärztliche Wochenschrift 123(5):186–191. https://pubmed.ncbi.nlm.nih.gov/20496823/. Accessed 20 Jan 2022
Bodziach K, Staniszewska M, Falkowska L, Nehring I, Ożarowska A, Zaniewicz G, Meissner W (2021) Gastrointestinal and respiratory exposure of water birds to endocrine disrupting phenolic compounds. Sci Total Environ 754:142435. https://doi.org/10.1016/j.scitotenv.2020.142435
Brown RE, Brain JD, Wang N (1997) The avian respiratory system: a unique model for studies of respiratory toxicosis and for monitoring air quality. Environ Health Perspect 105(2):188–200. https://doi.org/10.1289/ehp.97105188
Campbell T (2015) Exotic animal hematology and cytology. John Wiley & Sons, New Jersey. https://doi.org/10.1002/9781118993705
Campo JL, Gil MG, Davila SG (2005) Effects of specific noise and music stimuli on stress and fear levels of laying hens of several breeds. Appl Anim Behav Sci 91(1):75–84. https://doi.org/10.1016/j.applanim.2004.08.028
Capllonch P, Zelaya P (2006) Sobre la distribución y migración de la Mosqueta parda (Lathrotriccus euleri argentinus) en Sudamérica. Ornitología Neotropical 17:501–513. https://www.researchgate.net/publication/267413805. Accessed 20 Jan 2022
Carbó‐Ramírez P, Zuria I (2017) Leukocyte profile and body condition of the house finch (Haemorhous mexicanus) in two sites with different levels of urbanization in Central Mexico. Ornitología Neotropical 28:1–10. https://journals.sfu.ca/ornneo/index.php/ornneo/article/view/218. Accessed 20 Jan 2022
Cavalli M, Baladrón AV, Isacch JP, D’Amico V, Bó MS (2018) Leukocyte profiles and body condition of free-living burrowing owls (Athene cunicularia) from rural and urban areas in the Argentinean Pampas. Ornithol Res 26:45–51. https://doi.org/10.1007/BF03544414
Cid FD, Fernández NC, Pérez-Chaca MV, Pardo R, Caviedes-Vidal E, Chediack JG (2018) House sparrow biomarkers as lead pollution bioindicators. Evaluation of dose and exposition length on hematological and oxidative stress parameters. Ecotoxicol Environ Saf 154:154–161. https://doi.org/10.1016/j.ecoenv.2018.02.040
Clark P, Boardman W, Raidal S (2009) Atlas of clinical avian hematology. John Wiley & Sons, New Jersey
Costa A, Galvão A, Gonçalves da Silva L (2019) Mata Atlântica brasileira: análise do efeito de borda em fragmentos florestais remanescentes de um hotspot para conservação da biodiversidade. Revista de Geografia, Meio Ambiente e Ensino 10(1):112–123. http://rpem.unespar.edu.br/index.php/geomae/article/view/415/0. Accessed 20 Jan 2022
Davis AK, Maney DL (2018) The use of glucocorticoid hormones or leucocyte profiles to measure stress in vertebrates: what’s the difference? Methods Ecol Evol 9(6):1556–1568. https://doi.org/10.1111/2041-210X.13020
Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22(5):760–772. https://doi.org/10.1111/j.1365-2435.2008.01467.x
Deikumah JP, McAlpine CA, Maron M (2015) Matrix intensification affects body and physiological condition of tropical forest-dependent passerines. PLoS ONE 10(6):e0128521. https://doi.org/10.1371/journal.pone.0128521
Fränzle O (2003) Bioindicators and environmental stress assessment. In: Markert BA, Breure AM, Zeehmeister, HG (ed) Trace metals and other contaminants in the environment. Vol. 6. Elsevier Science, Oxford, pp 41–84. https://doi.org/10.1016/S0927-5215(03)80132-7
Gaiotti MG, Pinho JB (2013) Diet of the fuscous flycatcher Cnemotriccus fuscatus (Wied, 1831)–Aves, Tyrannidae-in three habitats of the northern Pantanal, Mato Grosso, Brazil. Braz J Biol 73:841–845. https://doi.org/10.1590/S1519-69842013000400021
Godoy FI, Gabriel V (2019) Provável híbrido entre Myiothlypis flaveola (Baird, 1865) e M. leucophrys (Pelzeln, 1868) (Passeriformes: Parulidae). Boletim Do Museu Paraense Emílio Goeldi - Ciências Naturais 14(1):111–117. https://boletimcn.museu-goeldi.br/bcnaturais/article/view/145. Accessed 20 Jan 2022
Goessling JM, Kennedy H, Mendonça MT, Wilson AE (2015) A meta-analysis of plasma corticosterone and heterophil: lymphocyte ratios–is there conservation of physiological stress responses over time? Funct Ecol 29(9):1189–1196. https://doi.org/10.1111/1365-2435.12442
Gonçalves VF, Ribeiro PVA, Souza OCF, Pires LP, Baesse CQ, Paniago LPM, Toletino VCG, 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
Grilli PG, Jensen RF, Navajas, SCE (2016) La expansión de la Mosqueta de Corona Parda Leptopogon amaurocephalus sobre el corredor del Río Uruguay. Nuestras Aves 61:30–32. https://ri.conicet.gov.ar/handle/11336/115027. Accessed 20 Jan 2022
Gross WB, Siegel HS (1983) Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis 27(4):972–979. https://doi.org/10.2307/1590198
Gwynne JA, Ridgely RS, Argel M, Tudor G (2010) Guia Aves do Brasil: Pantanal e Cerrado. Horizonte Geográfico, São Paulo
INPE. Instituto Nacional de Pesquisas Espaciais (2020) http://meioambiente.cptec.inpe.br/index.php?lang=pt. Accessed 26 May 2020
Isaksson C (2018) Impact of urbanization on birds. In: Tietze D (ed) Bird species. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-319-91689-7_13
Keller RH, Xie L, Buchwalter DB, Franzreb KE, Simons TR (2014) Mercury bioaccumulation in Southern Appalachian birds, assessed through feather concentrations. Ecotoxicology 23(2):304–316. https://doi.org/10.1007/s10646-013-1174-6
Lopes FM, Carvalho ST, Santos MPD (2007) Extensão de distribuição da pipira-da-taoca (Eucometis penicillata) para o estado do Piauí e leste do Maranhão, Brasil. Atualidades Ornitológicas 137:40–41. https://www.researchgate.net/publication/290020641. Accessed 20 Jan 2022
Marini MA, Cavalcanti RB (1993) Habitat and foraging substrate use of three Basileuterus warblers from central Brazil. Ornitologia Neotropical 4(2):69–76. https://sora.unm.edu/sites/default/files/journals/on/v004n02/p0069-p0076.pdf. Accessed 20 Jan 2022
Markert BA, Breure AM, Zechmeister HG (2003) Definitions, strategies and principles for bioindication/biomonitoring of the environment. Markert BA, Breure AM, Zeehmeister, HG (ed) Trace Metals and other Contaminants in the Environment. Vol. 6. Elsevier Science, Oxford, pp 3–39. https://doi.org/10.1016/S0927-5215(03)80131-5
Meissner W, Binkowski ŁJ, Barker J, Hahn A, Trzeciak M (2020) Relationship between blood lead levels and physiological stress in mute swans (Cygnus olor) in municipal beaches of the southern Baltic. Sci Total Environ 710:136292. https://doi.org/10.1016/j.scitotenv.2019.136292
Minias P (2019) Evolution of heterophil/lymphocyte ratios in response to ecological and life-history traits: a comparative analysis across the avian tree of life. J Anim Ecol 88(4):554–565. https://doi.org/10.1111/1365-2656.12941
MMA - Ministério do Meio Ambiente (2020) https://antigo.mma.gov.br/images/arquivo/80060/Diagnostico_Rede_de_Monitoramento_da_Qualidade_do_Ar.pdf Accessed 23 March 2021
Nicodemos RM, Assis AJ, Barrozo SMA (2010) Estudo sobre qualidade do ar na cidade de Uberlândia: análise da influência de variáveis. Horizonte Científico 4:1–25. http://www.seer.ufu.br/index.php/horizontecientifico/article/view/4367. Accessed 20 Jan 2022
Petrucci E, Oliveira LA (2019) Relações entre intensidade, duração e frequência das precipitações máximas de 24 horas e equação de chuvas intensas para a cidade de Uberlândia-MG. Rev Bras Climatol 25:337–354. https://doi.org/10.5380/abclima.v25i0.57767
Piacentini VQ et al (2015) Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee/Lista comentada das aves do Brasil pelo Comitê Brasileiro de Registros Ornitológicos. Ornithol Res 23(2):91–298. https://doi.org/10.1007/BF03544294
Pires LP, Melo C (2020) Individual–resource networks reveal distinct fruit preferences of selective individuals from a generalist population of the Helmeted Manakin. Ibis 162(3):713–722. https://doi.org/10.1111/ibi.12794
Rezende PS, Souza JDR, Silva GO, Ramos RR, Santos DG (2012) Qualidade ambiental em parques urbanos: levantamento e análises de aspectos positivos e negativos do Parque Municipal Victório Siquierolli-Uberlândia-MG. Observatorium: Revista Eletrônica de Geografia 4(10):53–73. http://www.seer.ufu.br/index.php/Observatorium/article/view/45452. Accessed 20 Jan 2022
Ribeiro PVA, Baesse CQ, Cury MC, Melo C (2020) Leukocyte profile of the helmeted manakin, Antilophia galeata (Passeriformes: Pipridae) in a Cerrado forest fragment. Zoologia 37:1–9. https://doi.org/10.3897/zoologia.37.e46441
Ruus A, Øverjordet IB, Braaten HFV, Evenset A, Christensen G, Heimstad ES, Gabrielsen GW, Borgå K (2015) Methylmercury biomagnification in an Arctic pelagic food web. Environ Toxicol Chem 34(11):2636–2643. https://doi.org/10.1002/etc.3143
Schilderman PA, Hoogewerff JA, Van Schooten FJ, Maas LM, Moonen EJ, Van Os BJ, Van Wijnen JH, Kleinjans JC (1997) Possible relevance of pigeons as an indicator species for monitoring air pollution. Environ Health Perspect 105(3):322–330. https://doi.org/10.1289/ehp.97105322
Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro
Sigrist T (2009) Guia de campo Avis Brasilis - Avifauna Brasileira: Pranchas e mapas. Avis Brasilis, São Paulo
Silva DP, Barbieri LR, Ferreira IJ, Ferreira JHD, Couto EVD (2017) Efeitos da fragmentação florestal no município de Japurá–Paraná. Revista de Geografia, Meio Ambiente e Ensino 8(3):186–195. http://www.fecilcam.br/revista/index.php/geomae/article/view/1757. Accessed 20 Jan 2022
Silva JMC (1995) Birds of the cerrado region, South America. Steenstrupia 21:69–92. https://www.researchgate.net/publication/260591911. Accessed 20 Jan 2022
Tolentino VCM, Baesse CQ, Melo C (2018) Dominant frequency of songs in tropical bird species is higher in sites with high noise pollution. Environ Pollut 235:983–992. https://doi.org/10.1016/j.envpol.2018.01.045
Tolentino VCM (2019) Bioacústica como ferramenta para estudo da influência do ruído antrópico nas aves. PhD Thesis, Universidade Federal de Uberlândia. https://doi.org/10.14393/ufu.te.2019.1232
Valadão RM, Franchin AG, Silva GBM, Pioli D, Júnior OM (2013) Riqueza e distribuição de Acciptriformes e Falconiformes em uma unidade de conservação no Triângulo Mineiro, MG, Brasil. Ornithologia 6:70–77. http://ornithologia.cemave.gov.br/index.php/ornithologia/article/view/155. Accessed 20 Jan 2022
Vogel HF, Zawadzki CH, Metri R (2011) Coexistência entre Turdus leucomelas Vieillot, 1818 e Turdus rufiventris Vieillot, 1818 (Aves: Passeriformes) em um fragmento urbano de floresta com araucárias, Sul do Brasil. Biota Neotrop 11:35–45. https://doi.org/10.1590/S1676-06032011000300002
Walthers AR, Barber CA (2020) Traffic noise as a potential stressor to offspring of an urban bird, the European Starling. J Ornithol 161:459–467. https://doi.org/10.1007/s10336-019-01733-z
Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15(8):711–724. https://doi.org/10.1046/j.1365-2826.2003.01033.x
Zollinger SA, Dorado-Correa A, Goymann W, Forstmeier W, Knief U, BastidasUrrutia AM, Brumm H (2019) Traffic noise exposure depresses plasma corticosterone and delays offspring growth in breeding zebra finches. Conserv Physiol 7:coz056. https://doi.org/10.1093/conphys/coz056
Acknowledgements
We thank the Companhia Energética de Minas Gerais S.A. (CEMIG) and Postgraduate Program in Ecology, Conservation and Biodiversity, Federal University of Uberlândia for providing the infrastructure services and support.
Funding
This work was supported by Conselho Nacional de Desenvolvimento Científico (CNPQ—PELD 403733/2012–0) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES—Finance Code 001).
Author information
Authors and Affiliations
Contributions
PVAR and CM contributed to the study conception and design. Material preparation and data collection were performed by all authors. PVAR analysed the data. The first draft of the manuscript was written by PVAR. All authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
All bird captures and handling were approved by the Ethical Committee on Animal Experiments, Federal University of Uberlândia, Brazil (CEUA/UFU—Authorization: 038/18) and the Brazilian Biodiversity Information and Authorization System (SISBIO/ICMBio—Authorization: 44901) in compliance with Brazilian laws and regulations.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Philippe Garrigues
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ribeiro, P.V.A., Gonçalves, V.F., de Magalhães Tolentino, V.C. et al. Effects of urbanisation and pollution on the heterophil/lymphocyte ratio in birds from Brazilian Cerrado. Environ Sci Pollut Res 29, 40204–40212 (2022). https://doi.org/10.1007/s11356-022-19037-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-19037-w