Effects of urbanisation and pollution on the heterophil/lymphocyte ratio in birds from Brazilian Cerrado.

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.

Effects of urban proximity and the occurrence of erythroplastids in Antilophia galeata.

Air pollution can generate changes in the morphology, physiology, and behavior of several animals, including birds, which, when responding to such environmental changes, can be used as biomonitors. Quantitative and qualitative analyses of erythrocyte nuclear anomalies comprise a useful tool for biomonitoring, with anucleated erythrocytes, called erythroplastids, being particularly significant. The objectives of the present study were to quantify the presence of erythroplastids in Antilophia galeata and relate their presence to distance from the nearest urban environment. Blood smears were analyzed for 80 individuals of A. galeata captured between June 2013 and October 2018 in five Cerrado forest fragments of different sizes and with different influences from urbanization. The quantity of erythroplastids differed among areas, with it being greater in fragments within a proximity with urban, and less in highly preserved areas far from an urban environment. Quantification of erythroplastids in A. galeata proved to be a useful tool for monitoring air quality.

Effect of urbanization on the micronucleus frequency in birds from forest fragments.

The urbanization contributes to environment contamination, mainly by the increased vehicle traffic. This intense traffic releases in the air chemical compounds with mutagenic properties that can affect the entire ecosystem. The birds for the flight accumulate air, absorbing gases or particles. The absorption of this polluted air may be causative agent responsible for micronucleus (MN) induction in bird erythrocytes. The quantitative analysis of MN in birds can assists in the monitoring environmental quality of various places. The study aimed to quantify the MN frequency in birds and compare their variation: I) among forest fragments distant from and near to urbanization, II) among species and populations of birds and III) to find if there is a relation between vehicle traffic and MN induction. The capture of the birds took place in four forest fragments in central Brazil (two distant and two near the city) using mist nets. Blood smears were prepared with blood collected from the tarso-metatarsal vein. A total of 354 individuals were analyzed and MN were found in 52% of the individuals analyzed. All sampled birds were identified and resulted to belong to 50 different species, only 4 of which were captured in all the 4 forest fragments. The average MN frequency, regardless of bird species and sampling area, was 1.04/10,000 erythrocytes. From an overall analysis carried out on all birds, the MN frequencies were found to vary among forest fragments distant from and near to urbanization (x2 =15.513; p < 0.001) and demonstrated positive correlation between vehicle traffic intensity and the MN frequency (r = 0.988; df=2; p = 0.011). The species of birds presented variation in the amount of MN (x2 = 84.64; df=49; p = 0.001). Therefore, a restricted analysis carried out on the 4 species of birds present in all the forest fragments showed that the populations of Antilophia galeata (x2 =6.029; p = 0.014), Basileuterus culicivorus (x2 =9.53; p = 0.002), Eucometis penicillata (x2 =8.067; p = 0.005) and Myiothlypis flaveola (x2 =4.771; p = 0.029) showed difference in the MN frequency, when compared between forest fragments distant from and near to cities. The analysis demonstrated that birds living in forest areas near to the city presented higher MN frequency, probably because pollutants generated by urbanization affect birds and that the larger the vehicle traffic the greater the induced MN in the birds.

Dominant frequency of songs in tropical bird species is higher in sites with high noise pollution.

The structure and organization of acoustic signals arise through evolutionary processes and adaptive pressures on each species. During learning, natural or anthropogenic factors, such as high noise levels in urban areas, pose challenges to acoustic communication in birds. Many species adjust their acoustic signals to higher noise levels by increasing the frequency of vocalizations. The objectives of this study were to compare the dominant frequency of songs among birds dwelling in forest fragments distant from and near to urban areas, establish correlations between the dominant frequency of song and noise levels in these environments and verified the difference of response between oscines, suboscines and non-passerines. We recorded vocalizations of birds between July/2013 and November/2014 in four forest fragments, two of them near and two distant from urban areas. We used Audacity software to measure the dominant frequency. We measured the ambient noise by a calibrated sound pressure level meter in decibels (dBA) in each of the forest fragments. We analyzed 3740 vocalizations of nine tropical bird species. Forest fragments near to urban areas have higher noise levels than more distant forest fragments. Eight of nine studied species presented higher dominant frequencies of songs in forest fragments near to urban areas. Only one species, Myiothlypis flaveola, did not change the dominant frequency of song between the four analyzed forest fragments. The difference in dominant frequency between the forest fragments distant and closer to the urban areas did not vary between oscines, suboscines and non-passerines. Eight tropical birds exhibited higher dominant frequencies of song in forest fragments near urban areas with high level of ambient noise. Oscine, suboscine and non-passerine showed song variations. Bird species that have differences in the vocalization dominant frequency can be used in environmental monitoring and in ethological studies, as they are sensitive to high noise levels. Noise pollution caused by the vehicular traffic and urbanization are correlates with changes in the vocalization of tropical birds in forest fragments.

Micronucleus as biomarker of genotoxicity in birds from Brazilian Cerrado.

Birds are considered efficient bioindicators, by their behavioral characteristics, diversified diet, and use of several vegetation layers, including in contaminated environments. The accumulation of contaminants can harm the reproductive process and survival of species, in addition to causing severe metabolic disorders. Air pollution can also affect the birds' health. Micronucleus analysis, a technique able to evaluate the organisms' sensitivity to contaminant agents, has been regarded as a practical tool for evaluating and monitoring the clastogenic and aneugenic effects caused by pollutants. The purpose of this study was to evaluate the presence of micronuclei in bird species that use forest environments and their surroundings; and to verify if the frequency and amount of micronuclei varies between species, areas and populations. Birds transiting between the Brazilian Cerrado forest and open formations were analyzed, coming from four forest fragments of Triângulo Mineiro, two close to urban areas and two more distant. Birds were captured with mist-nets for collecting blood extensions, which were used for counting micronuclei. In total, 103 individuals of 21 species were captured, and the micronucleus rate for every 5000 erythrocytes analyzed was 1.30. Only six populations had sampling sufficiency. There was no difference between the number of individuals with and without micronuclei (χ²=3.18, df=1, p=0.08). In areas closer to the urban perimeter, the micronuclei averages in birds were greater compared to the most isolated areas (H=27.534, df=3, p<0,001). In São José, the individuals of Myiothlypis flaveola presented a number of micronuclei significantly greater than the Galheiro and Água Fria (H=9.601, df=2, p=0.008). M. flaveola clearly reflected the area quality. The micronuclei analysis in birds was effective for evaluating the area quality as well as the intensity with which the birds respond to impacts caused by the surrounding matrix.