Volume 12 Issue 1
Jul.  2021
Turn off MathJax
Article Contents
Abstract
Background
Methods
Results
Discussion
Conclusion
Authors' contributions
Acknowledgements
Competing interests
References
Related Articles
Hani Amir Aouissi, Mostefa Ababsa, Aissam Gaagai, Zihad Bouslama, Yassine Farhi, Haroun Chenchouni. 2021: Does melanin-based plumage coloration reflect health status of free-living birds in urban environments?. Avian Research, 12(1): 45. DOI: 10.1186/s40657-021-00280-7
Citation: Hani Amir Aouissi, Mostefa Ababsa, Aissam Gaagai, Zihad Bouslama, Yassine Farhi, Haroun Chenchouni. 2021: Does melanin-based plumage coloration reflect health status of free-living birds in urban environments?. Avian Research, 12(1): 45. DOI: 10.1186/s40657-021-00280-7
shu

Does melanin-based plumage coloration reflect health status of free-living birds in urban environments?

  • 1.

    Scientific and Technical Research Center on Arid Regions (CRSTRA), 07000, Biskra, Algeria

  • 2.

    Faculty of Sciences, Department of Biology, Badji-Mokhtar Annaba University, 23000, Annaba, Algeria

  • 3.

    Environmental Research Center (CRE), Badji-Mokhtar Annaba University, 23000, Annaba, Algeria

  • 4.

    Department of Nature and Life Sciences, Faculty of Exact Sciences and Nature and Life Sciences, University of Larbi Tebessi, 12002, Tebessa, Algeria

  • 5.

    Laboratory of Natural Resources and Management of Sensitive Environments 'RNAMS', University of Larbi Ben M'hidi, 04000, Oum-El-Bouaghi, Algeria

Funds: 

the DGRSDT and MESRS Ministry of Higher Education and Scientific Research of Algeria

More Information
  • Corresponding author:

    Haroun Chenchouni, chenchouni@gmail.com

  • Received Date: 18 Oct 2020
  • Accepted Date: 01 Sep 2021
  • Available Online: 24 Apr 2022
  • Publish Date: 13 Sep 2021
    Graphical Abstract
    • Abstract
  • Background 

    Ecological functions and processes in urban ecosystems are governed by various human activities. City-adapted and city-exploiting animal species are expected to present certain specific behavioral and physiological traits in comparison to city-avoiders or conspecific individual frequenting less urbanized or rural environments. A trait of high importance, the plumage color polymorphism has been selected as the main study model and was correlated with different morphological and physiological parameters to highlight its importance in determining the possible health status of urban Feral Pigeons (Columba livia) in North African urban habitats.

    Methods 

    Different body morphometrics, hematological and hemoparasitic parameters were quantified on free-living Feral Pigeons in urban environments of northern Algeria. Moreover, plumage melanin-based coloration (MBC) was measured and the data collected at the individual scale was correlated with the previous parameters using linear and non-linear modeling approaches.

    Results 

    Plumage MBC scores of the sampled Feral Pigeons ranged between 0.3% and 74.8%. Among the 12 morphological traits measured, body weight, tail length and total length were deemed to be positively correlated with MBC. Darker morphs appeared to have more hemoparasites compared to lighter pigeons. Quite the same observation goes with the immunity but with non-linear trends. The number of monocytes and granulocytes increased with the increase in MBC levels in lighter morphs, while pigeons with high MBC scores exhibited negative relationships between MBC levels and the number of white blood cells.

    Conclusions 

    Despite the existence of a number of studies demonstrating phenotypic directional selection, further studies are undoubtedly necessary to understand in detail the underlying mechanisms in species life-history strategies between differently colored individuals. Findings of this correlative study open exciting perspectives revealing that MBC can be considered a good indicator of and health status and adaptation strategies to changes in urban environments.

    • FullText(HTML)

  • Integumentary coloration is essential in avian communication: signalers use coloration to provide information, such as the bearer's physical condition or genetic quality, to receivers (Hill 2006; Senar 2006). Melanins, mainly responsible for black (eumelanins) or reddish and brown (pheomelanin) colors, are considered one of the main pigment classes associated with variations in the physiological and behavioral traits that are typical targets in animal communication. It has been shown that vertebrates with melanin-richer coloration are more aggressive, sexually attractive and resistant to stress than those with melanin-lesser ones (Ducrest et al. 2008). However, compared with the well-studied carotenoid-based coloration, the function of melanin-based traits to their bearers is less understood.

    Animals can synthesize melanins from the aromatic amino acids, phenylalanine and tyrosine. Melanization can be highly heritable (Hill and McGraw 2006; Jawor and Breitwisch 2003). In the past, variations in melanin-based traits were believed mainly to be genetically controlled (Bize et al. 2006). However, later studies suggest that these traits could be condition-dependent: factors such as parasitic infections and diet quality can also influence the level of expression of melanin-based signals (e.g., Fargallo et al. 2007; Jacquin et al. 2011). In particular, oxidative stress could play a critical role in regulating melanization (e.g., Roulin et al. 2008). High oxidative stress, which results from the imbalance between the rate of production of reactive oxygen species (including free radicals) by cell metabolism and the state of repair and antioxidant machinery, can induce ageing and reduce life span (Finkel and Holbrook 2000). The process of melanization could reduce the concentration of free radicals, making melanin an important antioxidant (Ducrest et al. 2008). However, the correlation between oxidative stress levels and the coloration of melanin-based traits is still controversial in birds (e.g., Ducrest et al. 2008; Galván and Alonso-Alvarez 2009). In the current study, we examined the correlation between the brightness of black plumage (defined in materials and methods below) and individuals' oxidative stress levels in Himalayan Black Bulbuls (Hypsipetes leucocephalus nigerrimus) to test whether melanin-based plumage could be an indicator of the individuals' physical condition.

    To human eyes, melanin-based ornaments are usually just dull colored (i.e. black or brown), and are less varied within and between species than carotenoid-based ornaments (Badyaev and Hill 2000). However, the extra cones and oil drops that birds have make them have better at color discrimination than humans (Griffith et al. 2006; Jawor and Breitwisch 2003; McGraw 2006). Traditionally, avian melanin-based plumage patterns are characterized by patch size or darkness ranked by human eyes (e.g., Bize et al. 2006), but such methods may highly underestimate variations in brightness, and severely hamper our understanding of the functions of melanin-based traits. Fortunately, with the aid of a spectrometer, subtle differences in brightness of melanin-based pigments can be quantified, and results indicate that the variation in melanin-based coloration within and between species can be huge (McGraw et al. 2005).

    The Himalayan Black Bulbul is widely distributed in Taiwan's broad-leaf forests at elevations from 100 to 1500 m. Their plumage coloration is entirely melanin-based; black plumage with grey patches on the scapular feathers and remige. It makes the Himalayan Black Bulbul a perfect system to investigate the function of melanin-based signaling. In theory, the process of melanin production should reduce the sensitivity of the stress-regulation processes and result in lower oxidative stress (Ducrest et al. 2008); therefore, we expected a negative correlation between an individual's oxidative stress levels and its black plumage coloration, with brighter individuals (i.e. more melanins) under lower oxidative stress. The results of this study should enhance our knowledge of the role of melanin-based coloration in avian communication.

    Study species and captive setting

    In total, 18 and 48 Himalayan Black Bulbuls were bought from a pet-shop in Taipei in 2010 and 2011 respectively. Each bird was housed individually in the laboratory. We collected 150 μL blood from each individual for molecular sex typing. A drop of blood, approximately 5 μL, from each bird was used as the blood smear for the oxidative stress test. Each bird's brightness measurement and oxidative stress test were carried out in March of 2010 or 2011, which was the beginning of the breeding season.

    Molecular sex typing

    Gross DNA was extracted from blood samples with traditional proteinase K digestion followed by LiCl extraction [modified from the procedure of Gemmell and Akiyama (1996)]. Extracted DNA was re-suspended in ddH2O and stored at −20 ℃. Less than 100 ng of genomic DNA was added to 12.5 μL of PCR (polymerase chain reaction) mix containing 0.5 mmol/L of each of the dNTPs, 0.3 μmol/L of each PCR primer (2550F/2718R, Fridolfsson and Ellegren 1999), 10 mmol/L Tric-HCL, 50 mmol/L KCL, 1.5 mmol/L of MgCl2 and 0.4 U of Taq DNA polymerase (Amersham Biosciences). The PCR profile was 94 ℃ for 3 min, followed by 40 cycles of 95 ℃ for 20 s, 46 ℃ for 30 s and 72 ℃ for 40 s, finishing at 72 ℃ for 2 min. The PCR reactions were carried out in iCyclers (Bio-Rad, Hercules, CA, USA). After the PCR reactions, we conducted electrophoresis with 1.2 % agarose gel to determine the birds' sex. We identified eight females and ten males in 2010 and 18 females and 30 males in 2011.

    Brightness measurements

    For each individual, the reflectance of eight regions of melanin-based plumage- including the forehead, nape, back, breast, belly, tail, remige and scapular feathers—was measured using an USB2000 spectrometer (Ocean Optics) with a HL2000 deuterium-halogen light source (Ocean Optics). A R600-7-UV/125F probe (Ocean Optics) was held perpendicular to the surface of the feathers with a cylindrical cap at the end to standardize the distance (5 mm) measured and to shield ambient light. To calculate relative reflectance, a white standard (Labsphere) was used. To collect the dark reference, the light source was capped by a black plastic plate. Each part was measured three times to calculate repeatability (repeatability > 90 %, Lessells and Boag 1987). The brightness of each region was defined as the average of total reflectance within the range of 300–700 nm. McGraw et al. (2005) demonstrated that the concentrations of both eumelain and phaeomelanin in feathers were significantly and positively correlated with brightness: a brighter measurement indicates more melanin in the feathers.

    Oxidative stress test

    We calculated the ratio of lymphocytes (L) to heterocytes (H) in total of 100 leukocytes as a measure of oxidative stress for each individual bulbul following the methods used by Vleck et al. (2000). The blood smear was first dyed with a Wright-Giemsa stain for 3 min and then with 5 % PBS for 70 s. After drying, the numbers of lymphocytes and heterocytes were counted under a microscope at a magnification of 100× with oil immersion, and the H/L ratio calculated. The H/L ratio has been proved to be a good indicator of oxidative stress: higher levels of corticosterones can cause higher oxidative stress and also increase the number of heterocytes in the blood (Davis et al. 2008; Gross and Siegel 1983). Because leukocyte numbers change more slowly in response to stress than corticosterone does (Maxwell 1993), H/L ratios provide a more useful and accurate measure of long-term stress than a single measure of plasma corticosterone (McFarlane and Curtis 1989; Vleck et al. 2000).

    Statistical analysis

    Two-way ANOVA was conducted to test whether each individual's oxidative stress level and the brightness of each its body parts differed significantly between years. In these tests, sex, year and the interaction between sex and year were taken into account. Multiple regression was used to test whether the brightness of each body part correlated with oxidative stress (H/L ratio) while taking into account the birds' sex and the interaction between sex and oxidative stress. In the tests, the H/L ratio was log transformed to fit the normal distribution.

    Ethics statement

    Live birds were housed in the Animal Care House of the National Taiwan Normal University and cared for using procedures approved by the Institutional Animal Care and Use Committee of the Department of Life Science (IACUC Approval No 96026).

    The average H/L ratio in 2010 was 0.35 ± 0.05 and ranged from 0.1 to 0.4, while the average H/L ratio in 2011 was 1.05 ± 0.13 and ranged from 0.2 to 4.6. Individuals in the 2010 group were under significantly lower oxidative stress (lower H/L ratio) than those in the 2011 group (Fig. 1, two-way ANOVA, F = 15.36, p = 0.0002). The females' average H/L ratio was 0.76 ± 0.15 and the males' was 0.92 ± 0.14; there was no significant difference in the two sexes' H/L ratios (Fig. 1, two-way ANOVA, F = 0.73, p = 0.72).

    Figure  1.  The Log (H/L ratio) of two sexes in different years. The circles indicate the average Log (H/L) ratios for 2011 and the triangles indicate those for 2010. The lines indicate the standard error. The solid symbols represent the females and the hollow ones represent the males. Two-way ANOVA, factor year includes 2010 and 2011. df = 1, *p < 0.05
    DownLoad: Full-Size Img PowerPoint

    The brightness of melanin-based colors differed significantly between Himalayan Black Bulbuls in the 2010 and 2011 groups. Members of the 2011 group were brighter (i.e. more melanins) than those of the 2010 group, mainly in belly (two-way ANOVA, Table 1; Ls mean ± SE, 2010 group 4.45 ± 0.31 %, 2011 group 5.34 ± 0.19 %, post hoc (student's t) test, CL −1.61; −0.1) and breast (Table 1; 2010 group 3.22 ± 0.21 %, 2011 group 3.82 ± 0.13 %, post hoc (student's t) test, CL −1.10; −0.11). The same tendencies were observed at the remige and scapulars, although there were significant interactions with two factors, sex and year (two-way ANONA Table 1).

    Table  1.  Two-way ANOVA tests of brightness in eight body parts
    Parts Source F Ratio p
    Back Sex 0.50 0.483
    Yeara 0.47 0.495
    Year × sex 0.10 0.759
    Belly Sex 0.01 0.921
    Year 5.84 0.019*
    Year × sex 3.58 0.063
    Breast Sex 0.89 0.350
    Year 6.05 0.017*
    Year × sex 0.11 0.738
    Forehead Sex 1.84 0.181
    Year 0.80 0.375
    Year × sex 1.71 0.196
    Nape Sex 0.39 0.533
    Year 1.01 0.319
    Year × sex 0.61 0.439
    Remige Sex 2.61 0.112
    Year 7.95 0.007*
    Year × sex 5.27 0.025*
    Scapulars Sex 3.75 0.057
    Year 13.58 0.001*
    Year × sex 4.68 0.035*
    Tail Sex 1.95 0.168
    Year 2.18 0.145
    Year × sex 0.70 0.406
    df = 1
    * p < 0.05
    aFactor year: including 2010 and 2011
     | Show Table
    DownLoad: CSV

    The results of multiple regression indicate that brighter breast and scapular feathers might be related to lower oxidative stress: there was a significant negative correlation between the brightness of breast and scapulars and oxidative stress (multiple regressions, Table 2; linear correlation coefficients in breast, rfemale = −0.23, rmale = −0.47; correlations in scapulars, rfemale = −0.54, rmale = −0.23), but not between oxidative stress and the brightness of the other six body parts. However, this relationship only applied in 2011 and not in 2010: the 2010 H/L ratio was not significantly correlated with the brightness of any melanin-based parts (multiple regressions, Table 2).

    Table  2.  Multiple regressions of brightness in different body parts in 2010 and 2011
    Parts Terms 2010 2011
    t ratio p t ratio p
    Back Intercept 7.25 < .0001 29.49 < .0001
    Sex(F) 0.25 0.808 0.83 0.413
    Log(H/L ratio)a −0.05 0.964 −1.14 0.262
    Sex(F) × Log(H/L ratio) −1.46 0.166 −1.49 0.144
    Belly Intercept 6.09 < .0001 24.15 < .0001
    Sex(F) −1.37 0.194 1.53 0.134
    Log(H/L ratio) 0.78 0.447 −1.35 0.183
    Sex(F) × Log(H/L ratio) −0.85 0.409 0.35 0.728
    Breast Intercept 9.00 < .0001 24.53 < .0001
    Sex(F) 0.65 0.525 0.93 0.358
    Log(H/L ratio) 0.19 0.853 −2.43 0.019*
    Sex(F) × Log(H/L ratio) −1.44 0.172 −0.46 0.645
    Forehead Intercept 3.85 0.002 17.16 < .0001
    Sex(F) 1.52 0.150 −0.02 0.984
    Log(H/L ratio) −0.49 0.635 −0.39 0.696
    Sex(F) × Log(H/L ratio) −0.43 0.675 0.18 0.858
    Nape Intercept 7.03 < .0001 30.95 < .0001
    Sex(F) −0.75 0.465 0.01 0.995
    Log(H/L ratio) 0.70 0.497 −0.62 0.539
    Sex(F) × Log(H/L ratio) 0.18 0.858 −1.2 0.238
    Scapulars Intercept 8.07 < .0001 40.47 < .0001
    Sex(F) −2.22 0.043* 0.03 0.976
    Log(H/L ratio) −1.01 0.329 −2.37 0.022*
    Sex(F) × Log(H/L ratio) −0.76 0.461 −0.93 0.358
    Remige Intercept 5.70 < .0001 49.39 < .0001
    Sex(F) −2.41 0.032* 0.59 0.555
    Log(H/L ratio) −0.67 0.515 −0.28 0.782
    Sex(F) × Log(H/L ratio) −1.60 0.133 −0.78 0.440
    Tail Intercept 6.23 < .0001 27.93 < .0001
    Sex(F) 0.31 0.759 2.1 0.042*
    Log (H/L ratio) 0.13 0.899 0.34 0.739
    Sex(F) × Log(H/L ratio) 1.01 0.330 −0.36 0.724
    * p < 0.05
    aHeterocyte/lymphocyte ratio log transformed to normalize the distribution
     | Show Table
    DownLoad: CSV

    Our regression analysis for the 2011 sample shows that melanin-based characteristics could be brighter (i.e. more melanin) in individuals that suffered lower oxidative stress. This result is consistent with the work of Ducrest et al. (2008). They reviewed six studies and discovered a significantly negative correlation between the expression of melanin-based characteristics and the level of oxidative stress. This implies that expression of melanin-based traits is condition-dependent and could be a quality cue reflecting an individual's physical condition (Hill and McGraw 2006).

    However, individuals in our 2011 sample suffered higher oxidative stress than those in the 2010 sample but had brighter plumage (i.e. more melanins)—a positive correlation, contrasting with the negative correlation found within the 2011 group. Several recent studies also report similar, positive, correlations between oxidative stress and melanin-based coloration (Galván and Alonso-Alvarez 2008; Galván and Alonso-Alvarez 2009; Hõrak et al. 2010), suggesting that an alternative hypothesis about a different interaction between melanin coloration and oxidative stress should be considered in the role of melanin-based signaling.

    Glutathione (GSH), another key intracellular antioxidant, has been suggested to inhibit eumelanogenesis and eumelanin-based black ornaments, and might be crucial to the expression of melanin-based traits (Benedetto et al. 1982). GSH is a tripeptide thiol found in virtually all animal cells, and often considered as a vital antioxidant. It functions in the reduction of the disulfide linkages of proteins, in the synthesis of the deoxyribonucleotide precursors of DNA and in the protection of cells against free radicals (Meister 1983). GSH also serves as an agent regulating the process of melanogenesis. Low GSH levels have been associated with the deposition of melanin in bird feathers, whereas high GSH levels inhibit melanogenesis (Galván and Alonso-Alvarez 2008; Galván and Alonso-Alvarez 2009; Hõrak et al. 2010). Hence, GSH might be involved in a trade-off between antioxidants and melanogenesis. We suspect this might be the case in the Black Bulbuls: individuals in 2011 might have had lower GSH than those in 2010, therefore having brighter plumage but higher oxidative stress.

    The fact that we only discovered a significant relationship in the 2011 group, not in the 2010 group, might also provide support for the GSH hypothesis. A study in rats suggested that corticosterone could decrease glutathione levels (Patel et al. 2002). In our study, individuals in 2011 suffered higher oxidative stress of those in 2010, a relatively lower level of GSH might be expected in 2011 than in 2010. A lower level of GSH could enhance the melanin concentration or the patch size of individuals' melanin-based ornaments (Galván and Alonso-Alvarez 2008; Galván and Alonso-Alvarez 2009; Hõrak et al. 2010). Therefore the positive correlation between oxidative stress and brightness of melanin-based traits in the 2 years would be expected.

    In our study, individuals in 2011 suffered almost three times the oxidative stress of those in 2010; and variations in oxidative stress were larger within the 2011 group. Previous studies have shown that individuals' H/L ratio usually keeps steady until it moves on to a different life-history stage: the individual's H/L ratio could be higher at times during migration (Work et al. 1999), and parasitic infection or oil pollution can raise H/L ratios to four to six times those of controls (Davis et al. 2008). Since we collected all data at the beginning of breeding seasons of 2010 or 2011 and after molting, individuals should been in the same stage of life-history in the 2 years. But unpublished data showed that there were different rates of parasitic infection in the 2 years (Hung collected): a higher percentage of malarial infection in 2011 (37 %) than in 2010 (26 %). Therefore, besides the level of GSH, the rate of malarial infection might be another factor causing different levels of oxidative stress in our study between 2 years. But this requires further investigation.

    The status of oxidative stress we test here should not reflect the physical condition in real time or during molting, but is rather the long-term condition of an individual. Such long-term oxidative stress could be affected by many factors: genetic, environmental or different life-history stages (Monaghan et al. 2009). Therefore, Black Bulbuls might be able to use melanin-based coloration to evaluate individual's long-term physical condition. Consequently, the traits might be important in sexual selection or individual assessment in animal aggressive behavior in the Himalayan Black Bulbul. This hypothesis, however, requires further verification.

    In summary, we examined the relationship between individuals' oxidative stress levels and expression of melanin-based plumage in Himalayan Black Bulbuls. Our data suggest that melanin-based plumage can reflect individuals' long-term physical condition in certain situations. Therefore we propose that the brightness of melanin-based plumage could have a role in Himalayan Black Bulbuls' communication.

    HYH and SHL conceived and designed the experiments, and HYH performed the experiments. All the authors participated in the data analysis and paper writing. Both authors read and approved the final manuscript.

    The project was founded by the Population Genetics Lab, Department of Life Science, National Taiwan Normal University. We thank the following for laboratory assistance: C-F Yen, R-W Chu and R–C Lin. We also thank Y-Z Yi and Z-R Hung for helping care for the birds. Specially, we thank A. Watson who provided English editing.

    The authors declare that they have no competing interests

    • References (140)
  • Almasi B, Jenni L, Jenni-Eiermann S, Roulin A. Regulation of stress response is heritable and functionally linked to melanin-based coloration. J Evol Biol. 2010;23: 987–96.
    Aouissi HA, Belabed AI, Bouslama Z. Doves' mapping and inventory into the urban sites of Annaba (Northeastern of Algeria). Adv Environ Biol. 2015;12: 328–38.
    Aouissi HA, Gasparini J, Belabed AI, Bouslama Z. Impact of greenspaces in city on avian species richness and abundance in Northern Africa. CR Biol. 2017;340: 394–400.
    Aouissi HA, Petrişor AI, Ababsa M, Boştenaru-Dan M, Tourki M, Bouslama Z. Influence of land use on avian diversity in North African urban environments. Land. 2021;10: 434.
    Aouissi HA. Écologie des espèces aviaires dans le tissu urbain de la ville de Annaba. Doctoral Thesis. Annaba: University of Annaba; 2016.
    Barber I, Dingemanse NJ. Parasitism and the evolutionary ecology of animal personality. Philos Trans R Soc B. 2010;365: 4077–88.
    Barcia JJ. The Giemsa stain: its history and applications. Int J Surg Pathol. 2007;15: 292–6.
    Belabed AI, Aouissi HA, Zediri H, Djemadi I, Driss K, Houhamdi M, et al. The effect of urbanization on the phenotype of the Collared Dove (Streptopelia decaocto) in northeastern Algeria. Bull Inst Sci Rabat. 2013;35: 155–64.
    Belabed BE, Meddour A, Samraoui B, Chenchouni H. Modeling seasonal and spatial contamination of surface waters and upper sediments with trace metal elements across industrialized urban areas of the Seybouse watershed in North Africa. Environ Monit Assess. 2017;189: 265.
    Bendjoudi D, Chenchouni H, Doumandji S, Voisin JF. Bird species diversity of the Mitidja Plain (Northern Algeria) with emphasis on the dynamics of invasive and expanding species. Acrocephalus. 2013;34: 13–26.
    Bendjoudi D, Voisin JF, Doumandji S, Merabet A, Benyounes N, Chenchouni H. Rapid increase in numbers and change of land-use in two expanding Columbidae species (Columba palumbus and Streptopelia decaocto) in Algeria. Avian Res. 2015;6: 18.
    Berry JL. Urbanization. The earth as transformed by human action. In: Turner II BL, Clark WC, Kates RW, Richards JF, Mathews JT, Meyer WB, editors. The earth as transformed by human action: global and regional changes in the biosphere over the past 300 years. Cambridge: Cambridge University Press, UK; 1990. p. 103–19.
    Blair R. The effects of urban sprawl on birds at multiple levels of biological organization. Ecol Soc. 2004;9: 2.
    Blanchet S, Méjean L, Bourque JF, Lek S, Thomas F, Marcogliese DJ, et al. Why do parasitized hosts look different? Resolving the "chicken-egg" dilemma. Oecologia. 2009;160: 37.
    Borras A, Pascual J, Senar JC. What do different bill measures measure and what is the best method to use in granivorous birds? J Field Ornithol. 2000;71: 606–11.
    Bradley CA, Altizer S. Urbanization and the ecology of wildlife diseases. Trends Ecol Evol. 2007;22: 95–102.
    Brazil M. Birds of east Asia: China, Taiwan, Korea, Japan, and Russia. Princeton, New Jersey: Princeton University Press; 2009.
    Campbell TW. Avian hematology and cytology. 2nd ed. Ames, IA: Iowa State University Press; 1995.
    Chakarov N, Boerner M, Krüger O. Fitness in common buzzards at the cross-point of opposite melanin–parasite interactions. Funct Ecol. 2008;22: 1062–9.
    Chanarin I. Hematology: principles and procedures. J Clin Pathol. 1984;37: 1419.
    Chatelain M, Gasparini J, Frantz A. Do trace metals select for darker birds in urban areas? An experimental exposure to lead and zinc. Glob Chang Biol. 2016;22: 2380–91.
    Chatelain M, Gasparini J, Jacquin L, Frantz A. The adaptive function of melanin-based plumage coloration to trace metals. Biol Lett. 2014;10: 20140164.
    Chatelain M, Pessato A, Frantz A, Gasparini J, Leclaire S. Do trace metals influence visual signals? Effects of trace metals on iridescent and melanic feather colouration in the feral pigeon. Oikos. 2017;126: 1542–53.
    Chedad A, Bendjoudi D, Beladis I, Guezoul O, Chenchouni H. A comprehensive monograph on the ecology and distribution of the House bunting (Emberiza sahari) in Algeria. Front Biogeogr. 2021;13: e47727.
    Chenchouni H. Contribution à l'étude de la bio-écologie de la Cigogne blanche (Ciconia ciconia) dans la région de Batna (Nord-est algérien). Doctoral Thesis. Algeria: University of Batna; 2017a.
    Chenchouni H. Variation in White Stork (Ciconia ciconia) diet along a climatic gradient and across rural-to-urban landscapes in North Africa. Int J Biometeorol. 2017;61: 549–64.
    Clavel J, Julliard R, Devictor V. Worldwide decline of specialist species: toward a global functional homogenization? Front Ecol Environ. 2011;9: 222–8.
    Combes C. Parasitism: the ecology and evolution of intimate interactions. Chicago: University of Chicago Press; 2001.
    Comer JA, Paddock CD, Childs JE. Urban zoonoses caused by Bartonella, Coxiella, Ehrlichia, and Rickettsia species. Vector Borne Zoonotic Dis. 2001;1: 91–118.
    Corbel H, Legros A, Haussy C, Jacquin L, Gasparini J, Karimi B, Frantz A. Stress response varies with plumage colour and local habitat in feral pigeons. J Ornithol. 2016;157: 825–37.
    Côte J, Boniface A, Blanchet S, Hendry AP, Gasparini J, Jacquin L. Melanin-based coloration and host–parasite interactions under global change. Proc R Soc Lond B Biol. 2018;285: 20180285.
    Davey JW, Cezard T, Fuentes-Utrilla P, Eland C, Gharbi K, Blaxter ML. Special features of RAD Sequencing data: implications for genotyping. Mol Ecol. 2013;22: 3151–64.
    Davidsohn I, Henry JB. Clinical diagnosis by laboratory methods. 15th ed. Philadelphia, Pa: W. B. Saunders Co; 1974.
    Davis AK, Maney DL, Maerz JC. The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol. 2008;22: 760–72.
    de Godoi FSL, Nishi SM, de Jesus Pena HF, Gennari SM. Toxoplasma gondii: diagnosis of experimental and natural infection in pigeons (Columba livia) by serological, biological and molecular techniques. Rev Bras Parasitol Vet. 2010;19: 238–43.
    Devictor V, Julliard R, Clavel J, Jiguet F, Lee A, Couvet D. Functional biotic homogenization of bird communities in disturbed landscapes. Glob Ecol Biogeogr. 2008a;17: 252–61.
    Devictor V, Julliard R, Couvet D, Lee A, Jiguet F. Functional homogenization effect of urbanization on bird communities. Conserv Biol. 2007;21: 741–51.
    Devictor V, Julliard R, Jiguet F. Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos. 2008b;117: 507–14.
    Dreiss A, Henry I, Ruppli C, Almasi B, Roulin A. Darker eumelanic barn owls better withstand food depletion through resistance to food deprivation and lower appetite. Oecologia. 2010;164: 65–71.
    Ducatez S, Giraudeau M, Thébaud C, Jacquin L. Colour polymorphism is associated with lower extinction risk in birds. Glob Chang Biol. 2017;23: 3030–9.
    Ducrest AL, Keller L, Roulin A. Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol. 2008;23: 502–10.
    Eck S, Fiebig J, Fiedler W, Heynen I, Nicolai B, Töpfer T, et al. Measuring birds/vögel vermessen. Germany: Deutsche Ornithologen-Gesellschaft; 2011.
    Emaresi G, Henry I, Gonzalez E, Roulin A, Bize P. Sexand melanism-specific variations in the oxidative status of adult tawny owls in response to manipulated reproductive effort. J Exp Biol. 2016;219: 73–9.
    Ermert D, Niemiec MJ, Röhm M, Glenthøj A, Borregaard N, Urban CF. Candida albicans escapes from mouse neutrophils. J Leukocyte Biol. 2013;94: 223–36.
    Evans KL, Gaston KJ, Sharp SP, McGowan A, Simeoni M, Hatchwell BJ. Effects of urbanisation on disease prevalence and age structure in blackbird Turdus merula populations. Oikos. 2009;118: 774–82.
    Fallon SM, Ricklefs RE. Parasitemia in PCR-detected Plasmodium and Haemoproteus infections in birds. J Avian Biol. 2008;39: 514–22.
    Farhi Y, Aouissi HA, Nouidjem Y, Belhamra M. Spur-winged Lapwing at Djamaa, Algeria, in June 2011. Dutch Birding. 2020;42: 186–7.
    Fokidis HB, Greiner EC, Deviche P. Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. J Avian Biol. 2008;39: 300–10.
    French SS, Fokidis HB, Moore MC. Variation in stress and innate immunity in the tree lizard (Urosaurus ornatus) across an urban–rural gradient. J Comp Physiol B. 2008;178: 997–1005.
    Gaagai A, Boudoukha A, Boumezbeur A, Benaabidate L. Hydrochemical characterization of surface water in the Babar watershed (Algeria) using environmetric techniques and time series analysis. Int J River Basin Manag. 2017;15: 361–72.
    Galeotti P, Sacchi R. Differential parasitaemia in the tawny owl (Strix aluco): effects of colour morph and habitat. J Zool. 2003;261: 91–9.
    Galván I, Solano F. Melanin chemistry and the ecology of stress. Physiol Biochem Zool. 2015;88: 352–5.
    Galván I, Solano F. The evolution of euand pheomelanic traits may respond to an economy of pigments related to environmental oxidative stress. Pigment Cell Melanoma Res. 2009;22: 339–42.
    Gasparini J, Bize P, Piault R, Wakamatsu K, Blount JD, Ducrest AL, et al. Strength and cost of an induced immune response are associated with a heritable melanin-based colour trait in female tawny owls. J Anim Ecol. 2009;78: 608–16.
    George EL, Panos A. Does a high WBC count signal infection? Nursing. 2005;35: 20–1.
    Germaine SS, Rosenstock SS, Schweinsburg RE, Richardson WS. Relationships among breeding birds, habitat, and residential development in greater Tucson, Arizona. Ecol Appl. 1998;8: 680–91.
    Gilot-Fromont E, Jégo M, Bonenfant C, Gibert P, Rannou B, Klein F, et al. Immune phenotype and body condition in roe deer: individuals with high body condition have different, not stronger immunity. PLoS ONE. 2012;7: e45576.
    Godfrey PS, Toone BK, Carney MW, Flynn TG, Bottiglieri T, Laundy M, et al. Enhancement of recovery from psychiatric illness by methylfolate. Lancet. 1990;336: 392–5.
    Graczyk TK, Cranfield MR, Shiff CJ. Extraction of Haemoproteus columbae (Haemosporina: Haemoproteidae) antigen from rock dove pigeons (Columba livia) and its use in an antibody ELISA. J Parasitol. 1994;80: 713–8.
    Gregoire A, Faivre B, Heeb P, Cezilly F. A comparison of infestation patterns by Ixodes ticks in urban and rural populations of the Common Blackbird Turdus merula. Ibis. 2002;144: 640–5.
    Grimm NB, Grove JG, Pickett ST, Redman CL. Integrated approaches to long-term studies of urban ecological systems. Bioscience. 2000;50: 571–84.
    Haase E, Ito S, Sell A, Wakamatsu K. Melanin concentrations in feathers from wild and domestic pigeons. J Hered. 1992;83: 64–7.
    Hanson HE, Koussayer B, Kilvitis HJ, Schrey AW, Maddox JD, Martin LB. Epigenetic potential in native and introduced populations of house sparrows (Passer domesticus). Integr Comp Biol. 2020;60: 1458–68.
    Hart BL. Behavioural defence. In: Clayton DH, Moore J, editors. Host-parasite evolution: general principle and avian models. Oxford: Oxford University Press; 1997. p. 59–77.
    Hawkey CM, Dennett TB. A colour atlas of comparative veterinary haematology. London: Wolfe Publishing; 1989.
    Hill GE, McGraw KJ. Bird colouration: function and evolution. Cambridge: Harvard University Press; 2006.
    Ishtiaq F, Rao M, Huang X, Bensch S. Estimating prevalence of avian haemosporidians in natural populations: a comparative study on screening protocols. Parasite Vectors. 2017;10: 127.
    Jacquin L, Haussy C, Bertin C, Laroucau K, Gasparini J. Darker female pigeons transmit more specific antibodies to their eggs than do paler ones. Biol J Linn Soc. 2013a;108: 647–57.
    Jacquin L, Lenouvel P, Haussy C, Ducatez S, Gasparini J. Melanin-based coloration is related to parasite intensity and cellular immune response in an urban free living bird: the feral pigeon Columba livia. J Avian Biol. 2011;42: 11–5.
    Jacquin L, Récapet C, Bouche P, Leboucher G, Gasparini J. Melanin-based coloration reflects alternative strategies to cope with food limitation in pigeons. Behav Ecol. 2012;23: 907–15.
    Jacquin L, Récapet C, Prévot-Julliard AC, Leboucher G, Lenouvel P, Erin N, et al. A potential role for parasites in the maintenance of color polymorphism in urban birds. Oecologia. 2013b;173: 1089–99.
    Jacquin L. Coloration mélanique et stratégies d'histoire de vie chez le pigeon biset urbain. Doctoral Thesis. University of Paris 6; 2011.
    Jarry G, Baillon F. Hivernage de la tourterelle des bois (Streptopelia turtur) au Sénégal: étude d'une population dans la région de Nianing. Paris: Report of CRBPO; 1991.
    Jiguet F, Sunnen L, Prévot AC, Princé K. Urban pigeons losing toes due to human activities. Biol Conserv. 2019;240: 108241.
    Johnston RF, Janiga M. Feral pigeons. Vol. 4. Oxford: Oxford University Press; 1995.
    Karell P, Ahola K, Karstinen T, Kolunen H, Siitari H, Brommer JE. Blood parasites mediate morph-specific maintenance costs in a colour polymorphic wild bird. J Evol Biol. 2011;24: 1783–92.
    Kark S, Iwaniuk A, Schalimtzek A, Banker E. Living in the city: can anyone become an 'urban exploiter'? J Biogeogr. 2007;34: 638–51.
    Kilvitis HJ, Hanson H, Schrey AW, Martin LB. Epigenetic potential as a mechanism of phenotypic plasticity in vertebrate range expansions. Integr Comp Biol. 2017;57: 385–95.
    Kittilsen S, Schjolden J, Beitnes-Johansen I, Shaw JC, Pottinger TG, Sørensen C, et al. Melanin-based skin spots reflect stress responsiveness in salmonid fish. Horm Behav. 2009;56: 292–8.
    Kolomak IO, Berdnyk VP, Kyrychko OB, Nedosekov VV. Analysis of ultrastructural morphometric changes of pigeon kidneys affected by colibacteriosis. Transl Res Vet Sci. 2019;2: 37–49.
    Kramar DE, Carstensen B, Prisley S, Campbell J. Mercury concentrations in blood and feathers of nestling Bald Eagles in coastal and inland Virginia. Avian Res. 2019;10: 3.
    Krause ET, Krüger O, Hoffman JI. The influence of inherited plumage colour morph on morphometric traits and breeding investment in zebra finches (Taeniopygia guttata). PLoS ONE. 2017;12: e0188582.
    Krüger O, Lindström J. Lifetime reproductive success in common buzzard, Buteo buteo: from individual variation to population demography. Oikos. 2001;93: 260–73.
    Law GRJ. Blood samples from jugular vein of turkeys. Poult Sci. 1960;39: 1450–2.
    Le Viol I, Jiguet F, Brotons L, Herrando S, LindströmPearce-Higgins ÅJW, et al. More and more generalists: two decades of changes in the European avifauna. Biol Lett. 2012;8: 780–2.
    Leclaire S, Chatelain M, Pessato A, Buatois B, Frantz A, Gasparini J. Pigeon odor varies with experimental exposure to trace metal pollution. Ecotoxicology. 2019;28: 76–85.
    Luniak M. Synurbization – adaptation of animal wildlife to urban development. In: Shaw WW, Harris K, Vandruff L, editors. Proceedings of the 4th international symposium on urban wildlife conservation. Tucson, Arizona: University of Arizona; 2004. p. 50–5.
    Madans JH, Webster KM. Health surveys. In: Wright JD, editor. International encyclopedia of the social and behavioral sciences. 2nd ed. Orlando: University of Central Florida; 2015. p. 725–30.
    Martin LB. Stress and immunity in wild vertebrates: timing is everything. Gen Comp Endocrinol. 2009;163: 70–6.
    Martínez J, Vásquez RA, Venegas C, Merino S. Molecular characterisation of haemoparasites in forest birds from Robinson Crusoe Island: is the Austral Thrush a potential threat to endemic birds? Bird Conserv Int. 2015;25: 139–52.
    Martinossi-Allibert I, Clavel J, Ducatez S, Viol IL, Teplitsky C. Does habitat specialization shape the evolutionary potential of wild bird populations? J Avian Biol. 2017;48: 1158–65.
    Marzluff JM. Worldwide urbanization and its effects on birds. In: Marzluff JM, Bowman R, Donnelly R, editors. Avian ecology and conservation in an urbanizing world. Boston: Springer; 2001. p. 19–47.
    McCarren S, Sumasgutner P, Tate G, Koeslag A, Amar A. Clinal variation in the polymorphic Black Sparrowhawk Accipiter melanoleucus is unrelated to infection by the blood parasite Haemoproteus nisi. J Ornithol. 2021;162: 231–41.
    Miller LK, Brooks R. The effects of genotype, age, and social environment on male ornamentation, mating behavior, and attractiveness. Evolution. 2005;59: 2414–25.
    Møller AP. Interspecific variation in fear responses predicts urbanization in birds. Behav Ecol. 2010;21: 365–71.
    Møller AP. Successful city dwellers: a comparative study of the ecological characteristics of urban birds in the Western Palearctic. Oecologia. 2009;159: 849–58.
    Moreno J, Møller AP. Are melanin ornaments signals of antioxydant and immune capacity in birds? Acta Zool Sin. 2006;52: 202–8.
    Nebel C, Harl J, Pajot A, Weissenböck H, Amar A, Sumasgutner P. High prevalence and genetic diversity of Haemoproteus columbae (Haemosporida: Haemoproteidae) in feral pigeons Columbae livia in Cape Town. South Africa Parasitol Res. 2020;119: 447–63.
    Obukhova NY. Geographic variation of color in the synanthropic Blue Rock Pigeon. Russ J Genet. 2001;37: 649–58.
    Ouali N, Belabed BE, Chenchouni H. Modelling environment contamination with heavy metals in flathead grey mullet Mugil cephalus and upper sediments from north African coasts of the Mediterranean Sea. Sci Total Environ. 2018;639: 156–74.
    Oxnard CE. One biologist's view of morphometrics. Annu Rev Ecol Evol Syst. 1978;9: 219–41.
    Pal M, Pop P, Mahapatra A, Bhagat R, Hore U. Diversity and structure of bird assemblages along urban-rural gradient in Kolkata, India. Urban Forest Urban Green. 2019;38: 84–96.
    Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature. 2003;421: 37–42.
    Pellegrino I, Cucco M, Calà E, Boano G, Pavia M. Plumage coloration and morphometrics of the Little Owl Athene noctua in the Western Palearctic. J Ornithol. 2020;161: 1071–81.
    Pérez JE, Nirchio M, Alfonsi C, Muñoz C. The biology of invasions: the genetic adaptation paradox. Biol Invas. 2006;8: 1115–21.
    Périquet JC. Le Pigeon: races, élevage et utilisation, reproduction, hygiène et santé. Collection Les cahiers de l'élevage, Ed. Rustica, Paris; 1998.
    Pickett ST, Cadenasso ML, Grove JM, Boone CG, Groffman PM, Irwin E, et al. Urban ecological systems: scientific foundations and a decade of progress. J Environ Manage. 2011;92: 331–62.
    Pinheiro J, Bates D, DebRoy S, Sarkar D and R Core Team. nlme: linear and nonlinear mixed effects models. R package version 3.1–131. 2017. .
    Pollack L, Ondrasek NR, Calisi R. Urban health and ecology: the promise of an avian biomonitoring tool. Curr Zool. 2017;63: 205–12.
    Quesada J, Senar JC. The role of melaninand carotenoid-based plumage coloration in nest defence in the Great Tit. Ethology. 2007;113: 640–7.
    R Core Team. R: a language and environment for statistical computing. R foundation for statistical computing. 2020. .
    Rasmussen PC, Anderton JC. Birds of south Asia: the Ripley guide: attributes and status. 1st Edn, Vol. 2. Washington and Barcelona: Smithsonian Institution and Lynx Edicions; 2005.
    Récapet C, Dauphin L, Jacquin L, Gasparini J, Prévot-Julliard AC. Eumelanin-based colouration reflects local survival of juvenile feral pigeons in an urban pigeon house. J Avian Biol. 2013;44: 583–90.
    Reyer HU, Fischer W, Steck P, Nabulon T, Kessler P. Sex-specific nest defense in house sparrows (Passer domesticus) varies with badge size of males. Behav Ecol Sociobiol. 1998;42: 93–9.
    Roulin A, Almasi B, MeichtryStier KS, Jenni L. Eumelaninand pheomelanin-based colour advertise resistance to oxidative stress in opposite ways. J Evol Biol. 2011;24: 2241–7.
    Roulin A, Altwegg R, Jensen H, Steinsland I, Schaub M. Sex-dependent selection on an autosomal melanic female ornament promotes the evolution of sex ratio bias. Ecol Lett. 2010;13: 616–26.
    Roulin A, Altwegg R. Breeding rate is associated with pheomelanism in male and with eumelanism in female barn owls. Behav Ecol. 2007;18: 563–70.
    Roulin A, Gasparini J, Bize P, Ritschard M, Richner H. Melanin-based colorations signal strategies to cope with poor and rich environments. Behav Ecol Sociobiol. 2008;62: 507–19.
    Roulin A, Jungi TW, Pfister H, Dijkstra C. Female barn owls (Tyto alba) advertise good genes. Proc R Soc Lond B Biol. 2000;267: 937–41.
    Roulin A, Riols C, Dijkstra C, Ducrest AL. Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behav Ecol. 2001;12: 103–10.
    Roulin A. The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol Rev. 2004;79: 815–48.
    Rumsfeld JS. Health status and clinical practice: when will they meet? Circulation. 2002;106: 5–7.
    Saino N, Romano M, Rubolini D, Ambrosini R, Caprioli M, Milzani A, et al. Viability is associated with melanin-based coloration in the barn swallow (Hirundo rustica). PLoS ONE. 2013;8: e60426.
    Samuel MD, Woodworth BL, Atkinson CT, Hart PJ, LaPointe DA. Avian malaria in Hawaiian forest birds: infection and population impacts across species and elevations. Ecosphere. 2015;6: 104.
    Schultz PW, Gouveia VV, Cameron LD, Tankha G, Schmuck P, Franěk M. Values and their relationship to environmental concern and conservation behavior. J Cross-Cult Psychol. 2005;36: 457–75.
    Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D. From patterns to emerging processes in mechanistic urban ecology. Trend Ecol Evol. 2006;21: 186–91.
    Sol D, Jovani R, Torres J. Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography. 2000;23: 307–14.
    Stevens RWC, Ridgway GJ. A technique for bleeding chickens from the jugular vein. Poultry Sci. 1966;45: 204–5.
    Stone KD, Prussin C, Metcalfe DD. IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol. 2010;125: S73-80.
    Stöppler MC, Shiel WC, Credo Reference (Firm), WebMD (Firm). Webster's new world medical dictionary, 3rd ed.; Redo Reference: Boston, MA, USA; Wiley: Hoboken, NJ, USA. 2014; 480 p.
    Sumasgutner P, Rose S, Koeslag A, Amar A. Exploring the influence of urbanization on morph distribution and morph-specific breeding performance in a polymorphic African raptor. J Raptor Res. 2018;52: 19–30.
    The GIMP team. GIMP 2.8.10. 2014. .
    Tostes R, Vashist U, Scopel KKG, Massard CL, Daemon E, D'Agosto M. Plasmodium spp. and Haemoproteus spp. infection in birds of the Brazilian Atlantic Forest detected by microscopy and polymerase chain reaction. Pesq Vet Bras. 2015;35: 67–74.
    Uhm TG, Kim BS, Chung IY. Eosinophil development, regulation of eosinophil-specific genes, and role of eosinophils in the pathogenesis of asthma. Allergy Asthma Immunol Res. 2012;4: 68–79.
    Valkiūnas G, Palinauskas V, Ilgūnas M, Bukauskaitė D, Dimitrov D, Bernotienė R, et al. Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitol Res. 2014;113: 2251–63.
    Van den Brink V, Dreiss AN, Roulin A. Melanin-based coloration predicts natal dispersal in the barn owl Tyto Alba. Anim Behav. 2012;84: 805–12.
    Vignieri SN, Larson JG, Hoekstra HE. The selective advantage of crypsis in mice. Evolution. 2010;64: 2153–8.
    Vlahov D, Freudenberg N, Proietti F, Ompad D, Quinn A, Nandi V, et al. Urban as a determinant of health. J Urban Health. 2007;84: 16–26.
    Wei T, Simko V. R package "corrplot": Visualization of a Correlation Matrix (Version 0.84). 2017. .
    Yeh PJ. Rapid evolution of a sexually selected trait following population establishment in a novel habitat. Evolution. 2004;58: 166–74.
    • Related Articles

  • Related Articles

    Shangmingyu Zhang, Shane DuBay, Yuwen Cheng, Zhehan Dong, Zhengwei Liu, Yongjie Wu. 2025: Inter- and intraspecific variation in flight muscle fibers is associated with migratory timing. Avian Research, 16(1): 100223. DOI: 10.1016/j.avrs.2025.100223
    Dmitry Shitikov, Tatiana Vaytina, Polina Lebedyanskaya. 2024: Conspecific cues and breeding territory selection in Whinchat on abandoned fields. Avian Research, 15(1): 100212. DOI: 10.1016/j.avrs.2024.100212
    Lin Sun, Chunhong Liang, Shidi Qin, Ying Zhu, Ke He. 2024: Exploring the interplay of T cell receptor-V gene copy numbers and major histocompatibility complex selection pressure in avian species: Insights into immune system evolution and reproductive investment. Avian Research, 15(1): 100204. DOI: 10.1016/j.avrs.2024.100204
    Yue Wang, Qian Hu, Jiliang Xu, Jianqiang Li. 2023: Sex-specific selective effect of winter weather on morphological traits in a small passerine bird. Avian Research, 14(1): 100093. DOI: 10.1016/j.avrs.2023.100093
    Kevin B. Briggs, Mark C. Mainwaring. 2022: Habitat selection by nestbox-breeding birds and Roe Deer are incongruent within a heterogeneous woodland landscape. Avian Research, 13(1): 100012. DOI: 10.1016/j.avrs.2022.100012
    Ning Li, Zheng Wang, Yao Cai, Lin Zhang. 2020: Importance of microhabitat selection by birds for the early recruitment of endangered trees in a fragmented forest. Avian Research, 11(1): 46. DOI: 10.1186/s40657-020-00232-7
    Alexander M. Myrka, Tooba Shah, Jason T. Weir, Kenneth C. Welch Jr.. 2020: No signature of selection on the C-terminal region of glucose transporter 2 with the evolution of avian nectarivory. Avian Research, 11(1): 44. DOI: 10.1186/s40657-020-00231-8
    Roel May, Jens Åström, Øyvind Hamre, Espen Lie Dahl. 2017: Do birds in flight respond to (ultra)violet lighting?. Avian Research, 8(1): 33. DOI: 10.1186/s40657-017-0092-3
    K. M. Aarif, Aymen Nefla, S. B. Muzaffar, K. K. Musammilu, P. K. Prasadan. 2017: Traditional fishing activities enhance the abundance of selected waterbird species in a wetland in India. Avian Research, 8(1): 16. DOI: 10.1186/s40657-017-0073-6
    Junhua HU, Zhigang JIANG, Daode YANG, Huijian HU. 2010: Nest-site selection by Purple Swamphen in Haifeng, China. Avian Research, 1(4): 230-235. DOI: 10.5122/cbirds.2010.0018

Catalog

    Figures(5)  /  Tables(4)

    Get Citation
    PDF
    XML

    Article Metrics

    Article has an altmetric score of 3
    Article has an altmetric score of 3
    Article views (380) PDF downloads (7) Cited by()
    Supported by: Beijing Renhe Information Technology Co. Ltd.   Technical support: info@rhhz.net

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return