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Spatial segregation between the native Tropical mockingbird and the invader Chalk-browed mockingbird (Passeriformes: Mimidae) along a Neotropical natural-urban gradient

ABSTRACT

Congeneric species have similarities in phenotypic and ecological traits. The sympatry of congeneric species constitutes an opportunity for studies on coexistence. Two bird species of Mimidae, the native Tropical mockingbird, Mimus gilvus Oberholser, 1919, and the restinga invader Chalk-browed mockingbird, Mimus saturninus (Lichtenstein, 1823), currently occur in sympatry across the sandy-coastal ecosystem (restinga) of Espírito Santo state, Southeastern Brazil. We studied the spatial distribution of Tropical mockingbird and Chalk-browed mockingbird to understand the degree of competition across a preserved and urban gradient. We sampled 1,451 sampling units across a preserved and urban landscape in a coastal area of southeastern Brazil. The best-fitting model for abundance (Punctual Abundance Index) included urbanization index, distance from the coast, and distance from the closest protected area, which explained 63% and 97% of the abundance of Tropical mockingbird and Chalk-browed mockingbird, respectively. The species exhibited a segregated spatial pattern at small scale, indicating that both species are avoiding one another. Chalk-browed mockingbird showed ecological plasticity in modified environments, whereas Tropical mockingbird was more sensitive to urbanization. We suggested that the coexistence of these species is associated with resource partitioning. Monitoring Tropical mockingbird populations may be a proxy for the assessment of habitat quality and restoration success in the highly threatened restinga ecosystem.

KEY WORDS:
Interspecific competition; Mimus gilvus; Mimus saturninus; restinga; syntopy; urbanization

INTRODUCTION

Invader species may establish populations in novel landscapes due to invasion or expansion of their original distribution (Lockwood et al. 2013Lockwood JL, Hoope MF, Marchetti MP (2013) Invasion ecology. John Wiley & Sons, Blackwell Publishing, Chichester, 456 pp., Chen et al. 2022Chen K-H, Lin W-L, Lin S-M (2022) Competition between the black-winged kite and Eurasian kestrel led to population turnover at a subtropical sympatric site. Journal of Avian Biology 8: e03040. https://doi.org/10.1111/jav.03040
https://doi.org/10.1111/jav.03040...
). Invasion is generally related to human-induced alterations of the natural landscape (Grarock et al. 2014Grarock K, Tidemann CR, Wood JT, Lindenmayer DB (2014) Are invasive species drivers of native species decline or passengers of habitat modification? A case study of the impact of the common myna (Acridotheres tristis) on Australian bird species. Austral Ecology 39: 106-114. https://doi.org/10.1111/aec.12049
https://doi.org/10.1111/aec.12049...
, Zorzal et al. 2021Zorzal R, Diniz P, Oliveira R, Duca C (2021) Drivers of avian diversity in urban greenspaces in the Atlantic Florest. Urban Forestry & Urban Greening 59: e126908. https://doi.org/10.1016/j.ufug.2020.126908
https://doi.org/10.1016/j.ufug.2020.1269...
). Landscape alteration can promote native species to colonize new habitats within their native range (Carey et al. 2012Carey MP, Sanderson BL, Barnas KA, Olden JD (2012) Native invaders - challenges for science, management, policy, and society. Frontiers in Ecology and the Environment 10: 373-381. https://doi.org/10.1890/110060
https://doi.org/10.1890/110060...
). The effects of habitat modification and invasive species are interrelated, and thus useful to investigate native species decline (Grarock et al. 2014Grarock K, Tidemann CR, Wood JT, Lindenmayer DB (2014) Are invasive species drivers of native species decline or passengers of habitat modification? A case study of the impact of the common myna (Acridotheres tristis) on Australian bird species. Austral Ecology 39: 106-114. https://doi.org/10.1111/aec.12049
https://doi.org/10.1111/aec.12049...
). Invasion is context-dependent, and factors associated with invasion success are not uniform across time (Catford et al. 2019Catford JA, Smith AL, Wragg PD, Clark AT, Kosmala M, Cavender-Bares J, Reich PB, Tilman D (2019) Traits linked with species invasiveness and community invasibility vary with time, stage and indicator of invasion in long-term grassland experimente. Ecology Letters 22: 593-604. https://doi.org/10.1111/ele.13220
https://doi.org/10.1111/ele.13220...
).

Congeneric species may have similar phenotypic and ecological attributes, which provides an opportunity to study coexistence. The Tropical mockingbird, Mimus gilvus antelius Oberholser, 1919 and the Chalk-browed mockingbird, Mimus saturninus (Lichtenstein, 1823), currently occur in sympatry in the coast of Southeastern Brazil (Argel-de-Oliveira and Pacheco 1998Argel-de-Oliveira MM, Pacheco JF (1998) Um resumo da situação: Mimus saturninus e M. gilvus no litoral sudeste brasileiro. Boletim FBCN 25: 53-69.), whereas co-occurrence records are lacking on historical publications (e.g., Bell et al. 1841Bell T, Eyton TC, Scharf G, Hawkins BW (1841) The Zoology of the Voyage of HMS Beagle, Under the Command of Captain Fitzroy, RN, During the Years 1832 to 1836. Smith, Elder and Company, London, 275 pp., Hussey 1916Hussey RF (1916) Notes on some spring birds of La Plata. The Auk 33: 384-399. https://doi.org/10.2307/4072634
https://doi.org/10.2307/4072634...
, Arribálzaga 1920Arribálzaga EL (1920) Las aves del Chaco. El Hornero 2: 85-98., Willis 1992Willis EO (1992) Zoogeographical origins of eastern Brazilian birds. Ornitologia Neotropical 3: 1-15.). Regarding niche theory, competition through resource exploitation is the most important determinant of ecological segregation (Levins 1968Levins R (1968) Evolution in changing environments. Princeton University Press, Princeton, 132 pp.). However, interference competition may also be decisive for characterizing species distribution and abundance (Case and Gilpin 1974Case TJ, Gilpin ME (1974) Interference competition and niche theory. Proceedings of the National Academy of Sciences 71: 3073-3077. https://doi.org/10.1073/pnas.71.8.3073
https://doi.org/10.1073/pnas.71.8.3073...
). Species with high niche overlap are generally involved in territorial competition (Louarn et al. 2016Louarn ML, Couillens B, Deschamos-Cottin M, Clergeau P (2016) Interference competition between an invasive parakeet and native bird species at feeding sites. Journal of Ethology 34: 291-298. https://doi.org/10.1007/s10164-016-0474-8
https://doi.org/10.1007/s10164-016-0474-...
), which may have a significant impact when native species have temporal niche overlap with an invasive species.

Mimus gilvus antelius is restricted to the Brazilian coast (Cody 2005Cody M (2005) Family Mimidae (Mockinbird and Thrashers). In: del Hoyo J, Elliot A, Christie DA (Eds) Handbook of the birds of the world: Cuckoos-shrikes to Thrushers. Lynx Editions, Barcelona, vol. 10, 895 pp.), where it has close dietary relationship with plants of the restinga ecosystem (i.e., sandy-coastal plains) (Sick 1997Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro, 862 pp.). The Tropical mockingbird is a key species on dispersing restinga plants (Naranjo et al. 2003Naranjo ME, C Rengifo, PJ Soriano (2003) Effect of ingestion by bats and birds on seed germination of Stenocereus griseus and Subpilocereus repandus (Cactaceae). Journal of Tropical Ecology 19: 19-25. https://doi.org/10.1017/S0266467403003031
https://doi.org/10.1017/S026646740300303...
, Gomes et al. 2007Gomes VSM, Correia MCR, Lima HAL, Alves MAS (2007) Potential role of frugivorous birds (Passeriformes) on seed dispersal of six plant species of a restinga habitat, southeastern Brazil. Revista de Biología Tropical 56: 205-216. https://www.scielo.sa.cr/pdf/rbt/v56n1/art15v56n1.pdf
https://www.scielo.sa.cr/pdf/rbt/v56n1/a...
), but it is Endangered in the states of Espírito Santo (Chaves et al. 2019Chaves FG, Duca C, Pinto GO, Rosa GAB, Magnago GR, Daros-Filho HJ, Passamani JA, Silva JN, Silva JP, Bissoli LB, Mathias LB, Alves MAS, Ribon R, Betzel RL, Vanstreels RET, Hurtado R (2019) Aves ameaçadas de extinção no estado do Espírito Santo. In: Fraga CN, Formigoni H, Chaves FG (Eds) Fauna e flora ameaçada de extinção no estado do Espírito Santo. Instituto Nacional da Mata Atlântica, Santa Teresa, 432 pp.) and Rio de Janeiro (Alves et al. 2000Alves MAS, Pacheco JF, Gonzaga LAP, Cavalcanti RB, Raposo M, Yamashita C, Maciel NC, Castanheira M (2000) Aves. In: Bergallo HG, Rocha CFD, Alves MAS, Van-Sluys M (Eds) A fauna ameaçada de extinção do estado do Rio de Janeiro. Editora UERJ, Rio de Janeiro, 166 pp.). Whereas, M. saturninus is common in semi-open natural areas, and also inhabits rural and urban areas from northern Bolivia to Midwest and Northeastern Brazil (Ridgely and Tudor 1989Ridgely RS, Tudor G (1989) The birds of South America. University of Texas Press, Austin, vol. 1, 516 pp., Argel-de-Oliveira 1994Argel-de-Oliveira MM (1994) A Família Mimidae. Boletim CEO 10: 3-15. http://www.ceo.org.br/bolet/bolceo10.pdf
http://www.ceo.org.br/bolet/bolceo10.pdf...
). The Chalk-browed mockingbird is expanding its geographical distribution to deforested areas along the Atlantic coast (Ridgely and Tudor 1989Ridgely RS, Tudor G (1989) The birds of South America. University of Texas Press, Austin, vol. 1, 516 pp.), colonizing the restinga ecosystem of the southeastern region. At the coast of southeastern and northeastern Brazil, Tropical mockingbird is confined to patches of restinga, whereas Chalk-browed mockingbird was originally associated with inland xerophytic vegetation (Lamm 1948Lamm DW (1948) Notes on the birds of the states of Pernambuco and Paraiba, Brazil. The Auk 65: 261-283. https://doi.org/10.2307/4080302
https://doi.org/10.2307/4080302...
).

The first published record of the Chalk-browed mockingbird in the Cerrado Biome was in 1926 (Rogers 2016Rogers S (2016) CM Birds Collection. Carnegie Museums, Occurrence Dataset, v. 9.1. https://doi.org/10.15468/dv1ojv [Accessed: 26/12/2017]
https://doi.org/10.15468/dv1ojv...
), 715 km distant from our study site. In 1930, the Chalk-browed mockingbird was recorded in the Atlantic Forest biome (Cicero 2017Cicero C (2017) MVZ Bird Collection (Arctos). Museum of Vertebrate Zoology, occurrence dataset, v. 43.8. https://doi.org/10.15468/r1woj3 [Accessed: 26/12/2017]
https://doi.org/10.15468/r1woj3...
) at 238 km from our study site. In 1941, it was recorded in an urbanized area 70 km from our study site (GBIF 2022GBIF (2022) GBIF Backbone Taxonomy. Checklist data set, Checklist data set, https://www.gbif.org/occurrence/1324004822 [Accessed: 02/08/2018]
https://www.gbif.org/occurrence/13240048...
). Currently, Chalk-browed mockingbird occurs in sympatry with Tropical mockingbird. Contrarily, Tropical mockingbird is endemic to restinga ecosystem (Gonzaga et al. 2000Gonzaga LP, Castiglioni GDA, Reis HBR (2000) Avifauna das restingas do sudeste: estado do conhecimento e potencial para futuros estudos. In: Esteves FA, Lacerda LD (Eds) Ecologia de restingas e lagoas costeiras. Macaé, NUPEM/UFRJ, 151-163.), whereas Chalk-browed mockingbird is a habitat generalist using open and mountainous regions, but absent from forested regions of southeastern Brazil (Ridgely and Tudor 1989Ridgely RS, Tudor G (1989) The birds of South America. University of Texas Press, Austin, vol. 1, 516 pp.). Thus, Chalk-browed mockingbird is an invader of restinga, leading to the current sympatry of these two congeneric species.

The presence of Chalk-browed mockingbird in the restinga is likely detrimental to the Tropical mockingbird due to its novel competitive effect (Argel-de-Oliveira 1994Argel-de-Oliveira MM (1994) A Família Mimidae. Boletim CEO 10: 3-15. http://www.ceo.org.br/bolet/bolceo10.pdf
http://www.ceo.org.br/bolet/bolceo10.pdf...
). Chalk-browed mockingbird has been observed expelling a pair of Tropical mockingbird from a constructed nest for egg laying (R. Morais, pers. com.) and we have also recorded other agonistic interactions between these species (C. Duca pers. obs.). Tropical mockingbird is not highly sensitive to habitat disturbance (Parker III et al. 1996Parker III TA, Stotz DK, Fitzpatrick JW (1996) Database A: zoogeography and ecological attributes of bird species breeding in the Neotropics. In: Stoltz DF, Fitzpatrick JW, Parker III TA, Moskivits DK (Eds) Neotropical birds: ecology and conservation. University of Chicago Press, Chicago, 502 pp.), but Chalk-browed mockingbird inhabits coastal urban environments where Tropical mockingbird is absent or uncommon. However, the interaction between these two congeneric species may expose the Tropical mockingbird to further selection pressure in its native habitat.

Considering that the concept of ecological tolerance includes the acclimatization to physical conditions and the behavioral indifference of one species towards another (Begon et al. 2007Begon M, Townsend CR, Harper JL (2007) Ecologia: de indivíduos a ecossistemas. Artmed, Porto Alegre, 4th ed., 740 pp.), our goal was to compare the abundance and spatial distribution of the Tropical mockingbird and the Chalk-browed mockingbird to understand their recent coexistence. We studied a gradient from preserved to urban sites of Southeastern Brazil to determine: the landscape features related to the presence and abundance of the two species; the patterns of association between the species; and the role of space and environment in explaining these patterns.

MATERIAL AND METHODS

Study site

The study site is located in the municipalities of Vila Velha and Guarapari, state of Espírito Santo, southeastern Brazil (Fig. 1). It is in the Atlantic Forest biome, and it was originally covered by restinga vegetation (Pereira 2003Pereira OJ (2003) Restinga: origem, estrutura e diversidade. In: Jardim MAG, Bastos NNC, Santos JUM (Eds) Desafios da botânica brasileira no novo milênio: inventário, sistematização e conservação da diversidade vegetal. Sociedade Brasileira de Botânica, Belém, 177-179.), which has rocky outcrop, open herbaceous vegetation, flood-meadow, and forest (Fabris and Cesar 1996Fabris LC, Cesar O (1996) Estudos florísticos em uma mata litorânea do sul do estado do Espírito Santo, Brasil. Boletim do Museu de Biologia Mello Leitão 5: 15-46.). The study site comprises a gradient from preserved to urban areas. In the south of the sampled site, data were collected in the Setiba Environmental Protection Area (APA-Setiba, 12,960 ha) (Lausche 2011Lausche B (2011) Guidelines for protected areas legislation. IUCN, Gland, 370 pp.), which includes the Paulo César Vinha State Park (PEPCV, 1,500 ha) located inside the APA-Setiba. In the north of the sampled site, there are urban areas in the municipality of Vila Velha, which is a highly urbanized city with 210 km2. This region has an Am tropical monsoon climate (Köppen) (Alvares et al. 2013Alvares CA, Stape JL, Sentelhas C, Moraes GJL, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728. https://doi.org/10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0...
).

Figure 1
Sampling design (transects) in the municipalities of Vila Velha and Guarapari, state of Espírito Santo, southeastern Brazil.

Sampling design

Data were collected from November 2015 to April 2017. The sampling design had 30 transects perpendicular to the coast, each 5,000 m long and placed 1,000 m apart from each other (Fig. 1). Each transect had up to 50 sampling units, which was a circle of 50 m radius (area 7,854 m2). A pilot study showed that both species were reliably identified and counted up to 50 m without recounting by the observer using Tasco 10 × 50 binoculars. The total sampling area is about 1,140 ha. Each sampling unit was surveyed twice for five minutes using the point count method (Bibby et al. 2000Bibby CJ, Burgess ND, Hill DA, Mustoe SH (2000) Bird census techniques. Academic Press, London, 2nd ed., 55 pp.) between dawn and 10:00 in the morning, which is the highest activity period of both species and consequently has a higher probability of detection (Anjos et al. 2010Anjos LD, Volpato GH, Mendonça LB, Serafini P, Lopes EV, Boçon R, Bisheimer MV (2010) Técnicas de levantamento quantitativo de aves em ambiente florestal: uma análise comparativa baseada em dados empíricos. In: Von-Matter S, Straube FC, Accordi I, Piacentini V, Cândido-Jr JF (Eds) Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Technical Books, Rio de Janeiro, 516 pp.). A pilot study using plastic color bands showed an individual was not counted twice due to the distance between our sampling units and the time reserved for detection (see Morais et al. 2019Morais R, Araújo LC, Silva GR, Duca C (2019) Multiple nesting attempts and long breeding seasons of Mimus gilvus (Aves: Mimidae) in southeastern Brazil. Zoologia 36: e25717. https://doi.org/10.3897/zoologia.36.e25717
https://doi.org/10.3897/zoologia.36.e257...
).

Predictive variables

The predictive variables were the distance from each site to the coast (hereafter ‘coast distance’) and to the protected area (hereafter ‘protected area distance’) and the Normalized Difference Built-up Index (hereafter ‘NDBI”; see description below). Coast distance and protected area distance were calculated based on aerial imagery from the Integrated System of Geospatial Bases of the State of Espírito Santo (GEOBASES) using the QGIS program (QGIS 2016QGIS Development Team (2016) QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org [Acessed: 17/08/2018]
http://qgis.osgeo.org...
) and validated by in situ observation. The NDBI was developed mainly for Landsat TM satellite data by analyzing the spectral response of built-up areas in different image bands, indicating the degree of urbanization (Zha et al. 2010Zha Y, Gao J, Ni S (2010) Use of normalized difference built-up index in automatically mapping urban areas from TM imagery. International Journal of Remote Sensing 24: 583-594. https://doi.org/10.1080/01431160304987
https://doi.org/10.1080/01431160304987...
). Landsat-8 OLI images were used in this predictive variable, following four main steps: pre-processing and satellite data analysis; image enhancement by resolution fusion; development of the built-up area extraction method; and precision evaluation (Zha et al. 2010Zha Y, Gao J, Ni S (2010) Use of normalized difference built-up index in automatically mapping urban areas from TM imagery. International Journal of Remote Sensing 24: 583-594. https://doi.org/10.1080/01431160304987
https://doi.org/10.1080/01431160304987...
). The file format and data type of the Landsat-8 OLI images were the ESRI ASCII (American Standard Code), a raster file format for digital imaging. In order to resize the NDBI to values between zero and one, each element of the set was logarithm transformed, and the maximum value of the set was used as the base of the logarithm. The resized NDBI value (hereafter ‘urbanization index’) resulted in values close to zero indicating areas of higher vegetation coverage and values close to one indicating higher amount of construction.

Response variables

The response variables were frequency of occurrence and abundance. The frequency of occurrence (FO) and total abundance of Tropical mockingbird and Chalk-browed mockingbird were based on the presence and absence and number of individuals recorded at each site. The FO was the ratio between the number of sampling units where each species was recorded (presence) relating to total sampling unit. The total abundance was the maximum number of individuals recorded in each sampling unit. Total abundance was used to estimate the Punctual Abundance Index (hereafter “abundance”), which is the ratio between the total number of individuals of each species and the total number of sampling units. It indicates species abundance as a function of their detection coefficient (Bibby et al. 2000Bibby CJ, Burgess ND, Hill DA, Mustoe SH (2000) Bird census techniques. Academic Press, London, 2nd ed., 55 pp.). To estimate the abundance regarding the urbanization index, the number of individuals of each species recorded in the sampling units with an equal urbanization index value was divided by the number of sampling units with this value of the urbanization index. The abundance estimates for coast distance and protected area distance were determined at intervals of 200 m, based on the mean area of Tropical mockingbird territory (3.4 ha; L.C. Araujo, unpublished data); for example, the abundance-200 m comprised the ratio between the total number of individuals of each species and the total number of sampling units between zero and 200 m, and so on.

Statistical analyses

Prior to analysis, there was a weak correlation between the three predictive variables (Pearson correlation coefficient r < 0.75) (Bland and Altman 1990Bland JM, Altman DG (1990) A note on the use of the intraclass correlation coefficient in the evaluation of agreement between two methods of measurement. Computers in biology and medicine 20: 337-340. https://doi.org/10.1016/0010-4825(90)90013-F
https://doi.org/10.1016/0010-4825(90)900...
). The Chi-square Adherence test (χ2) was applied to determine if there was a difference between the two species regarding total FO and total abundance. The individual relationship between each species’ abundance and the predictive variables was assessed by simple linear regression (Zar 1984Zar JH (1984) Biostatistical analysis. Prentice-Hall, Engewood Cliffs, New Jersey, 2nd ed, 718 pp.), using the BioEstat version 5.0 program (Ayres and Ayres 2000Ayres M, Ayres-Jr M (2000) BioEstat 2.0: Aplicações estatísticas nas áreas das ciências biológicas e médicas. Sociedade Civil Mamirauá, Belém, 364 pp.), at a significance level of α = 0.05.

Generalized Linear Models (GLMs) were used to test how the numbers of individuals of each species varied in relation to the predictive variables (Gotelli and Ellison 2013Gotelli NJE, Ellison AM (2013) A primer of ecological statistics. Sinauer Associates, Sunderland, 614 pp.). Eight models were generated for each species, and model selection followed Akaike Information Criteria (ΔAIC) values, where models with ΔAIC ≤ 2 were considered to have similar ability to explain the variation in the data (Burnham and Anderson 2002Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer Verlag, New York, 2nd ed., 488 pp.). The best models had lower ΔAIC values and higher strength of evidence (high values of wi). Null models were also included (Zuur et al. 2009Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, 574 pp.). The GLM with Poisson distribution was employed using the glm() package in version 3.0.3 of R (R Core Team 2015R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org [Accessed: 17/08/2018]
http://www.R-project.org...
).

Partial redundancy analysis (pRDA), spatial filtering using Moran’s auto vector mapping (Moran’s eigenvector maps [MEMs] - see Dray et al. 2006Dray S, Legendre P, Peres-Neto PR (2006) Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecological Modelling 196: 483-493. https://doi.org/10.1016/j.ecolmodel.2006.02.015
https://doi.org/10.1016/j.ecolmodel.2006...
, Griffith and Peres-Neto 2006Griffith DA, Peres-Neto PR (2006) Spatial modeling in ecology: the flexibility of eigenfunction spatial analyses. Ecology 87: 2603-2613. https://www.jstor.org/stable/20069270
https://www.jstor.org/stable/20069270...
), and spline correlograms were utilized to partition the abundance of the two species into spatial MEM and environmental components and to quantify univariate and bivariate species patterns. The MEMs were designed to detect spatial structures of variable scale in response data. These structures, understood as scale measures, were then decomposed into a new set of independent spatial variables, which were incorporated into the analysis of variance partitioning (Legendre and Legendre 2013Legendre P, Legendre LF (2013) Numerical ecology. Elsevier, Amsterdam, 715 pp.). The species abundance matrix (‘A’) per sample unit was used in this analysis. Another matrix (X) was elaborated using local spatial coordinates, longitude (x) and latitude (y) of each sampling unit, which, after being expanded to Moran’s auto vector predictors, resulted in a ‘M’ matrix and a third ‘E’ matrix, representing a gradient with the three predictive variables. Prior to partitioning, a forward selection of variables was run on these explanatory matrices.

Spline-type Moran’s I and univariate and cross-correlation functions were calculated using an abundance matrix of the species per sample unit and a matrix of geographic coordinates (x, y) (Bjørnstad and Falck 2001Bjørnstad ON, Falck W (2001) Nonparametric spatial covariance functions: estimation and testing. Environmental and Ecological Statistics 8: 53-70. https://doi.org/10.1023/A:1009601932481
https://doi.org/10.1023/A:1009601932481...
, Fortin and Dale 2005Fortin MJ, Dale MR (2005) Spatial Analysis: a guide for ecologists. Cambridge University Press, Cambridge, 365 pp., Borcard et al. 2018Borcard D, Gillet F, Legendre P (2018) Numerical ecology with R. Springer International Publishing, New York, 435 pp. https://doi.org/10.1007/978-3-319-71404-2
https://doi.org/10.1007/978-3-319-71404-...
). They were used to determine the autocorrelation scale (univariate analysis) and the cross-correlation (bivariate analysis) between the species Tropical mockingbird and Chalk-browed mockingbird. Spatial autocorrelation is obtained from mean deviations and provides evidence of autocorrelation intensity, influence zone size, and the type of spatial pattern of the studied variable (Legendre and Fortin 1989Legendre P, Fortin MJ (1989) Spatial pattern and ecological analysis. Vegetatio 80: 107-138. https://doi.org/10.1007/BF00048036
https://doi.org/10.1007/BF00048036...
). Differently from the commonly used discrete correlograms, the spline correlogram is a continuous estimator (Bjørnstad and Falck 2001Bjørnstad ON, Falck W (2001) Nonparametric spatial covariance functions: estimation and testing. Environmental and Ecological Statistics 8: 53-70. https://doi.org/10.1023/A:1009601932481
https://doi.org/10.1023/A:1009601932481...
). For univariate correlograms, values close to zero indicate randomness in species abundances, whereas values above zero indicate an aggregate distribution pattern. For the cross-correlograms, values below zero indicate a segregated pattern among the individuals of both species. This segregation can be used as an indicator of competitive interactions between the two species. The uncertainty of the cross-spline correlograms was estimated using the bootstrapping method (10 thousand iterations) with 95% confidence intervals. The correlograms were created at a distance of 6,665 m, approximately one-third of the maximum amplitude. All analyses were performed in R (R Core Team 2015R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org [Accessed: 17/08/2018]
http://www.R-project.org...
). MEMs were created using the PCNM package (Legendre et al. 2013Legendre P, Borcard D, Blanchet FG, Dray S (2013) PCMN: MEN spatial eigenfunction and principal coordinate analyses [R package version 2.1-2/r109] http://r-forge.r-project.org/R/?group_id=195
http://r-forge.r-project.org/R/?group_id...
), variable selection was carried out using the ordistep function from the vegan package (Oksanen et al. 2017Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) vegan: Community Ecology Package. R package version 2.4-3. https://CRAN.R-project.org/package=vegan [Acessed: 17/08/2018]
https://CRAN.R-project.org/package=vegan...
), and the univariate and cross-correlograms were run with the ncf package (Bjørnstad 2017Bjørnstad ON (2017) ncf: spatial nonparametric covariance functions. R package version 1.1-5. http://CRAN.R-project.org/package=ncf [Accessed: 10/04/2020]
http://CRAN.R-project.org/package=ncf...
).

RESULTS

At least one species (Tropical mockingbird and/or Chalk-browed mockingbird) was present in 64% (n = 933) of the sampling units. The frequency of occurrence of Tropical mockingbird (FO = 73%) was significantly higher than Chalk-browed mockingbird (FO = 39%) (χ2 = 97.94; df = 1; p < 0.001). Tropical mockingbird (n = 1019; 0.91 ind.ha-1) had 1.9 times more individuals than Chalk-browed mockingbird (n = 543; 0.49 ind.ha-1) (χ2 = 128.82; df = 1; p < 0.001).

The abundance of the Tropical mockingbird was negatively correlated with the urbanization index (r2 = 0.42; p < 0.001), whereas the Chalk-browed mockingbird showed a weak correlation with the urbanization index (r2 = 0.01; p = 0.67) (Fig. 2). The abundance of Tropical mockingbird decreased with increasing coast distance (r2 = 0.46; p < 0.001), whereas Chalk-browed mockingbird showed a weak correlation with coast distance (r2 = 0.01; p = 0.73). The abundance of Tropical mockingbird showed a weak correlation with protected area distance (r2 = 0.01; p = 0.21), whereas Chalk-browed mockingbird increased with protected area distance (r2 = 0.19; p < 0.001).

Figure 2
Abundance (Punctual Abundance Index) of Tropical mockingbird (Mimus gilvus, closed circle and continuous line) and Chalk-browed mockingbird (M. saturninus, open circle and dashed line) regarding urbanization index (Normalized Difference Built-up Index) in a coastal region of southeastern Brazil. Urbanization increases toward a higher urbanization index.

The model with all three predictive variables was the best fit to the abundance of both species, explaining 63% of the abundance variation of the Tropical mockingbird and 97% of the Chalk-browed mockingbird (Table 1). For the Tropical mockingbird, the second best-fitting model had the urbanization index and coast distance explaining 37% of the data. These two models explained 100% of the abundance of the Tropical mockingbird and the Chalk-browed mockingbird (Table 1).

Table 1
Model selection of abundance of Tropical mockingbird and Chalk-browed mockingbird regarding the predictive variables (Normalized Difference Built-up Index - NDBI, coast distance - CD, and protected area distance - PAD) based on Akaike’s Information Criteria (AIC). Total AIC, the difference of AIC of each model relative to the top model (∆AIC), Akaike model weight (wi).

The partitioning between environment and space explained 22% of the variation (p = 0.001). The greater proportion (11%; p = 0.001) of the abundance variation of Tropical mockingbird and Chalk-browed mockingbird was associated with the spatial component (MEMs), whereas the environment explained a relatively lower fraction (6%, p = 0.001). The shared variation between both components was 5%.

The spatial pattern analysis (univariate spline correlograms) of each species showed positive spatial autocorrelation for Tropical mockingbird until ca. 2,000 to 3,000 m (Fig. 3A), while Chalk-browed mockingbird (Fig. 3B) is aggregated up to a 3,500 m spatial scale. The cross-spline correlogram indicated segregation of the two species at scales up to 5,000 m. At greater distances, the test value and its confidence interval were at the zero line, denoting a random spatial distribution pattern (Fig. 3C).

Figure 3
(A,B) Univariate spline correlogram: (A) Tropical mockingbird; (B) Chalk-browed mockingbird. Superior and inferior lines represent a 95% confidence interval. The confidence intervals below or above zero in splines indicate negative and positive spatial structures, respectively. (C) Cross-spline correlogram of the two species denoting spatial segregation between the two species (negative values) regarding distances of up 1,000 m.

DISCUSSION

The native restinga specialist Tropical mockingbird is more abundant than the invader Chalk-browed mockingbird in the study area. Considering the closest relationship between the Tropical mockingbird and the restinga ecosystem, this result corroborates the hypothesis of higher abundance at the center of species distribution (Brown 1984Brown JH (1984) On the relationship between abundance and distribution of species. The American Naturalist 124: 255-279. https://www.jstor.org/stable/2461494
https://www.jstor.org/stable/2461494...
). Restinga patches still remain around higher urbanization centers and near the coastline. Thus, the specialization of Tropical mockingbird on restinga may influence its presence and abundance in the coastal-urban region (Crates et al. 2011Crates RA, French K, McLean CM (2011) The abundance and distribution of two species of fairy-wren in suburban and natural habitats. Emu 111: 341-349. https://doi.org/10.1071/MU10057
https://doi.org/10.1071/MU10057...
), explaining the decreasing abundance of the Tropical mockingbird with coast distance and the weak relationship of Chalk-browed mockingbird abundance with this variable. However, habitat loss in restinga may be influencing the historical reduction of Tropical mockingbird abundance (i.e., 30% and 46% in a 10-year period; see Zanon et al. 2015Zanon MS, Valeand MM, Alves MAS (2015) Missing for the last twenty years: the case of the southernmost populations of the Tropical mokingbird Mimus gilvus (Passeriformes: Mimidae). Zoologia 32: 1-8. https://doi.org/10.1590/S1984-46702015000100001
https://doi.org/10.1590/S1984-4670201500...
) and the expansion of Chalk-browed mockingbird.

Apparently, the Tropical mockingbird is more sensitive to urbanization than the Chalk-browed mockingbird. The sensitivity of the Tropical mockingbird to urbanization has also been reported for other populations (Zanon et al. 2015Zanon MS, Valeand MM, Alves MAS (2015) Missing for the last twenty years: the case of the southernmost populations of the Tropical mokingbird Mimus gilvus (Passeriformes: Mimidae). Zoologia 32: 1-8. https://doi.org/10.1590/S1984-46702015000100001
https://doi.org/10.1590/S1984-4670201500...
), suggesting the need for conservation of the remaining restinga to maintain viable populations. Urbanization may be the main threat affecting the reduction of the Tropical mockingbird abundance across the Brazilian coast. The Tropical mockingbird is a threatened species in the coastal region of Southeastern Brazil (Alves et al. 2000Alves MAS, Pacheco JF, Gonzaga LAP, Cavalcanti RB, Raposo M, Yamashita C, Maciel NC, Castanheira M (2000) Aves. In: Bergallo HG, Rocha CFD, Alves MAS, Van-Sluys M (Eds) A fauna ameaçada de extinção do estado do Rio de Janeiro. Editora UERJ, Rio de Janeiro, 166 pp., Chaves et al. 2019Chaves FG, Duca C, Pinto GO, Rosa GAB, Magnago GR, Daros-Filho HJ, Passamani JA, Silva JN, Silva JP, Bissoli LB, Mathias LB, Alves MAS, Ribon R, Betzel RL, Vanstreels RET, Hurtado R (2019) Aves ameaçadas de extinção no estado do Espírito Santo. In: Fraga CN, Formigoni H, Chaves FG (Eds) Fauna e flora ameaçada de extinção no estado do Espírito Santo. Instituto Nacional da Mata Atlântica, Santa Teresa, 432 pp.). It is also considered a key species due to its seed dispersal function in restinga ecosystem (Naranjo et al. 2003Naranjo ME, C Rengifo, PJ Soriano (2003) Effect of ingestion by bats and birds on seed germination of Stenocereus griseus and Subpilocereus repandus (Cactaceae). Journal of Tropical Ecology 19: 19-25. https://doi.org/10.1017/S0266467403003031
https://doi.org/10.1017/S026646740300303...
, Gomes et al. 2007Gomes VSM, Correia MCR, Lima HAL, Alves MAS (2007) Potential role of frugivorous birds (Passeriformes) on seed dispersal of six plant species of a restinga habitat, southeastern Brazil. Revista de Biología Tropical 56: 205-216. https://www.scielo.sa.cr/pdf/rbt/v56n1/art15v56n1.pdf
https://www.scielo.sa.cr/pdf/rbt/v56n1/a...
), being essential in the conservation and recovery of degraded areas in coastal environments (Gomes et al. 2008). To safeguard the long-term presence of the Tropical mockingbird, a sustainable land use plan for the coastal region is required by combining urbanization and protection of restinga remnants (Rocha et al. 2007Rocha CFD, Bergallo HG, Van Sluys M, Alves MAS, Jamel CE (2007) The remnants of restinga habitats in the Brazilian Atlantic Forest of Rio de Janeiro state, Brazil: habitat loss and risk of disappearance. Brazilian Journal of Biology 67: 263-273. https://doi.org/10.1590/S1519-69842007000200011
https://doi.org/10.1590/S1519-6984200700...
). We highlight the importance of the restinga strip as a permanent preservation area (Brasil 2012Brasil (2012) Lei n. 12.651, de 25 de maio de 2012. Dispõe sobre a proteção da vegetação nativa; altera as Leis nos 6.938, de 31 de agosto de 1981, 9.393, de 19 de dezembro de 1996, e 11.428, de 22 de dezembro de 2006; revoga as Leis nos 4.771, de 15 de setembro de 1965, e 7.754, de 14 de abril de 1989, e a Medida Provisória no 2.166-67, de 24 de agosto de 2001; e dá outras providências. 2012. Diário Oficial da União, Brasília, Ano CXLIX, n. 102, 28/05/2012, Seção 1, p. 1. http://portal.in.gov.br [Accessed: 10/03/2018]
http://portal.in.gov.br...
) on the coast as a way to mitigate the impacts of urbanization on the Tropical mockingbird population. We also suggest restinga restoration could be useful for the Tropical mockingbird recovery and Chalk-browed mockingbird control.

The Tropical mockingbird and the Chalk-browed mockingbird showed different responses to coast distance. The abundance of Tropical mockingbird decreased toward the inland and Chalk-browed mockingbird did not show any trend. These spatial distributions are corroborated by the literature for both species (Ridgely and Tudor 1989Ridgely RS, Tudor G (1989) The birds of South America. University of Texas Press, Austin, vol. 1, 516 pp., Argel-de-Oliveira 1994Argel-de-Oliveira MM (1994) A Família Mimidae. Boletim CEO 10: 3-15. http://www.ceo.org.br/bolet/bolceo10.pdf
http://www.ceo.org.br/bolet/bolceo10.pdf...
). The Chalk-browed mockingbird is less selective regarding coast distance due to its behavioral plasticity to use different habitats (see Argel-de-Oliveira 1994, Rodrigues et al. 2017Rodrigues SS, Lopes LE, Marini MÂ (2017) Breeding biology of Chalk-browed mokingbird Mimus saturninus in a natural savanna of central Brazil. Revista Brasilieira de Ornitologia 25: 237-244. https://doi.org/10.1007/BF03544402
https://doi.org/10.1007/BF03544402...
). Invader species are usually benefited by urbanization and increase their presence in suburban and urban areas (e.g., van Rensburg et al. 2009van Rensburg BJ, Peacock DS, Robertson MP (2009) Biotic homogenization and alien bird species along an urban gradient in South Africa. Landscape Urban Planning 92: 233-241. https://doi.org/10.1016/j.landurbplan.2009.05.002
https://doi.org/10.1016/j.landurbplan.20...
, Grarock et al. 2014Grarock K, Tidemann CR, Wood JT, Lindenmayer DB (2014) Are invasive species drivers of native species decline or passengers of habitat modification? A case study of the impact of the common myna (Acridotheres tristis) on Australian bird species. Austral Ecology 39: 106-114. https://doi.org/10.1111/aec.12049
https://doi.org/10.1111/aec.12049...
).

The Tropical mockingbird had similar abundance in relation to the protected area distance, whereas the Chalk-browed mockingbird had an increase toward urban areas. There are patches of restinga between the protected and urban areas that could increase habitat connectivity, mainly near the coast. Nonetheless, these remaining restinga patches are private properties under continuous human modification, which may promote the isolation of the Tropical mockingbird population. So, it is possible that Tropical mockingbird is not subjected to fragmentation effects on the study area yet, due to the still high restinga vegetation cover of the landscape, but it is also possible that it will be affected by restinga fragmentation in short to middle term.

The urbanization and the isolation of populations may influence the absence of Tropical mockingbird in some restinga patches. In other two populations, the Tropical mockingbird has also been absent in preserved areas (Zanon et al. 2015Zanon MS, Valeand MM, Alves MAS (2015) Missing for the last twenty years: the case of the southernmost populations of the Tropical mokingbird Mimus gilvus (Passeriformes: Mimidae). Zoologia 32: 1-8. https://doi.org/10.1590/S1984-46702015000100001
https://doi.org/10.1590/S1984-4670201500...
, C. Duca pers. obs.). Apparently, Tropical mockingbird is sensitive to high-density urbanization, leading to population isolation (Zanon et al. 2015), which would impede the recolonization of metapopulation dynamics (McDonnell et al. 1997McDonnell MJ, Pickett ST, Groffman P, Bohlen P, Pouyat RV, Zipperer WC, Medley K (1997) Ecosystem processes along an urban-to-rural gradient. Urban Ecosystem 1: 21-36. https://doi.org/10.1023/A:1014359024275
https://doi.org/10.1023/A:1014359024275...
). The fragmentation of the restinga may reduce displacement between sites and consequently recolonization (Rocha et al. 2007Rocha CFD, Bergallo HG, Van Sluys M, Alves MAS, Jamel CE (2007) The remnants of restinga habitats in the Brazilian Atlantic Forest of Rio de Janeiro state, Brazil: habitat loss and risk of disappearance. Brazilian Journal of Biology 67: 263-273. https://doi.org/10.1590/S1519-69842007000200011
https://doi.org/10.1590/S1519-6984200700...
). On the other hand, the Chalk-browed mockingbird is likely more resistant to the effects of fragmentation, showing good adaptive plasticity in altered environments.

The Chalk-browed mockingbird does not occur only in developed urban areas nor it is restricted to regions occupied by exotic or native vegetation, showing that this species can inhabit both natural and altered environments (Vallejos et al. 2016Vallejos MAV, Padial AA, Vitule JRS (2016) Human-induced landscape changes homogenize Atlantic Forest bird assemblages through nested species loss. PloS One 11: e0147058. https://doi.org/10.1371/journal.pone.0147058
https://doi.org/10.1371/journal.pone.014...
). Low levels of urban development (e.g., areas with empty lots, small houses, squares, and gardens) increase the variety and quantity of resources available for birds (Blair 1996Blair RB (1996) Land use and avian species diversity along an urban gradient. Ecological Applications 6: 506-519. https://doi.org/10.2307/2269387
https://doi.org/10.2307/2269387...
). Therefore, low rates of urbanization alter the environment less significantly compared to large urban centers. This low-intensity modification may occur through changes in the composition of the plant community, the introduction of ornamental species, and changes in structure (e.g., replacement of tree species with herbaceous plants) (Rudnicky and McDonnell 1989Rudnicky JL, McDonnell MJ (1989) Forty-eight years of canopy change in a hardwood-hemlock forest in New York City. Bulletin of the Torrey Botanical Club 116: 52-64. https://doi.org/10.2307/2997109
https://doi.org/10.2307/2997109...
). These alterations may be associated with increased water sources, primary productivity, and habitat fragmentation (Kark et al. 2007Kark S, Iwaniuk A, Schalimtzek A, Banker E (2007) Living in the city: can anyone become an ‘urban exploiter’? Journal of Biogeography 34: 638-651. https://doi.org/10.1111/j.1365-2699.2006.01638.x
https://doi.org/10.1111/j.1365-2699.2006...
). Alterations in resource availability may also alter community patterns, interfering with species composition as well as abundance (Blair 1996Blair RB (1996) Land use and avian species diversity along an urban gradient. Ecological Applications 6: 506-519. https://doi.org/10.2307/2269387
https://doi.org/10.2307/2269387...
).

Habitat variability can lead to spatial segregation or species grouping. The results showed that at small scales (0 to 3,500 m), Tropical Mockingbirds and Chalk-browed Mockingbirds displayed individual aggregated spatial patterns, showing that the spatial variable explains the abundance variance of the two species. Apparently, the two species exhibited segregated spatial patterns in response to competition, suggesting that they would be potential competitors in syntopy. Congeneric species with similar niches tend to reduce competition by segregating in space, as discussed in the Principle of Competitive Exclusion (Gause 1932Gause GF (1932) Experimental Studies on the Struggle for Existence - I. Mixed Population of Two Species of Yeast. Journal of Experimental Biology 9: 389-402. https://doi.org/10.1242/jeb.9.4.389
https://doi.org/10.1242/jeb.9.4.389...
, Bringloe et al. 2016Bringloe TT, Adamowicz SJ, Harvey VF, Jackson JK, Cotteni K (2016) Detecting signatures of competition from observational data: a combined approach using DNA barcoding, diversity partitioning and checkerboards at small spatial scales. Freshwater Biology 61: 646-657. https://doi.org/10.1111/fwb.12732
https://doi.org/10.1111/fwb.12732...
). It is known that niche overlap can affect populations of both species (Chen et al. 2022Chen K-H, Lin W-L, Lin S-M (2022) Competition between the black-winged kite and Eurasian kestrel led to population turnover at a subtropical sympatric site. Journal of Avian Biology 8: e03040. https://doi.org/10.1111/jav.03040
https://doi.org/10.1111/jav.03040...
) and this seems to be the ecological scenario for Tropical mokingbird and Chalk-browed mokingbird in the study area. The observed spatial differentiation may also be a result of past competition, a principle known as the “ghost of competition past” (Connell 1980Connell JH (1980) Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 35: 131-138. https://doi.org/10.2307/3544421
https://doi.org/10.2307/3544421...
). Future studies on habitat selection may provide important insights into how these species are segregating in space.

Our study showed that the Chalk-browed mokingbird has ecological plasticity in altered environments and is possibly benefiting from habitat modification, thus increasing its geographical distribution. The results corroborate studies showing that the Tropical mokingbird is susceptible to urbanization and fragmentation of the restinga (Alves et al. 2000Alves MAS, Pacheco JF, Gonzaga LAP, Cavalcanti RB, Raposo M, Yamashita C, Maciel NC, Castanheira M (2000) Aves. In: Bergallo HG, Rocha CFD, Alves MAS, Van-Sluys M (Eds) A fauna ameaçada de extinção do estado do Rio de Janeiro. Editora UERJ, Rio de Janeiro, 166 pp., Zanon et al. 2015Zanon MS, Valeand MM, Alves MAS (2015) Missing for the last twenty years: the case of the southernmost populations of the Tropical mokingbird Mimus gilvus (Passeriformes: Mimidae). Zoologia 32: 1-8. https://doi.org/10.1590/S1984-46702015000100001
https://doi.org/10.1590/S1984-4670201500...
). Because the Tropical mokingbird is a threatened species in southeastern Brazil (Alves et al. 2000Alves MAS, Pacheco JF, Gonzaga LAP, Cavalcanti RB, Raposo M, Yamashita C, Maciel NC, Castanheira M (2000) Aves. In: Bergallo HG, Rocha CFD, Alves MAS, Van-Sluys M (Eds) A fauna ameaçada de extinção do estado do Rio de Janeiro. Editora UERJ, Rio de Janeiro, 166 pp., Chaves et al. 2019Chaves FG, Duca C, Pinto GO, Rosa GAB, Magnago GR, Daros-Filho HJ, Passamani JA, Silva JN, Silva JP, Bissoli LB, Mathias LB, Alves MAS, Ribon R, Betzel RL, Vanstreels RET, Hurtado R (2019) Aves ameaçadas de extinção no estado do Espírito Santo. In: Fraga CN, Formigoni H, Chaves FG (Eds) Fauna e flora ameaçada de extinção no estado do Espírito Santo. Instituto Nacional da Mata Atlântica, Santa Teresa, 432 pp.) and also plays a critical role in the restinga ecosystem (Gomes et al. 2008Gomes VSM, Loiselle BA, Alves MAS (2008) Birds foraging for fruits and insects in shrubby restinga vegetation, southeastern Brazil. Biota Neotropica 7: 21-31. https://doi.org/10.1590/S1676-06032008000400001
https://doi.org/10.1590/S1676-0603200800...
), it can be a useful bioindicator of environmental quality in these areas. The monitoring of Tropical mokingbird populations can be considered a suitable tool for assessing the conservation status of restinga at local (remnant) and regional (landscape) scales and also to evaluate the efficiency of restoration of degraded areas in the restinga ecosystem.

ACKNOWLEDGEMENTS

This study received support from the Concessionária Rodovia do Sol (RODOSOL) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, grant 45.6446/2014-1). The Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, grant 23038.004514/2018-40) funded a PhD scholarship to VAL, and Fundação de Amparo à Pesquisa e Inovação do Espírito Santo (FAPES) a post-doctoral fellowship to RBF (grant 0823/2015), Master’s scholarship to RSO (grant 8887.285553/2018-00). MLG is grateful to CNPq (“Bolsa de Produtividade em Pesquisa”, grant 311522/2022-0”), and FAPES for the research grants (grant 299/2021). Authors declare that any impropriety of language proficiency is our responsibility.

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ADDITIONAL NOTES

  • ZooBank register

    https://zoobank.org/C98EE011-747B-4F89-897A-8E876BF22F38
  • How to cite this article

    Araujo-Lima V, Ferreira RB, Oliveira RS, Ferreira-Santos K, Garbin ML, Duca C (2023) Spatial segregation between the native Tropical mockingbird and the invader Chalk-browed mockingbird (Passeriformes: Mimidae) along a Neotropical natural-urban gradient. Zoologia 40: e22061. https://doi.org/10.1590/S1984-4689.v40.e22061
  • Published by

    Sociedade Brasileira de Zoologia at Scientific Electronic Library Online (https://www.scielo.br/zool

Edited by

Editorial responsibility

Luís Fábio Silveira

Data availability

Data citations

Cicero C (2017) MVZ Bird Collection (Arctos). Museum of Vertebrate Zoology, occurrence dataset, v. 43.8. https://doi.org/10.15468/r1woj3 [Accessed: 26/12/2017]

GBIF (2022) GBIF Backbone Taxonomy. Checklist data set, Checklist data set, https://www.gbif.org/occurrence/1324004822 [Accessed: 02/08/2018]

Rogers S (2016) CM Birds Collection. Carnegie Museums, Occurrence Dataset, v. 9.1. https://doi.org/10.15468/dv1ojv [Accessed: 26/12/2017]

Publication Dates

  • Publication in this collection
    18 Sept 2023
  • Date of issue
    2023

History

  • Received
    30 Dec 2022
  • Accepted
    08 May 2023
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