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ORNITOLOGIA NEOTROPICAL 24: 279–297, 2013© The Neotropical Ornithological Society

RELATIONSHIP BETWEEN HABITAT TRAITS AND BIRD DIVERSITY AND COMPOSITION IN SELECTED URBAN GREEN

AREAS OF MEXICO CITY

Grégory M. Charre1, J. Alejandro Zavala Hurtado2, Gabriel Néve3, Alejandro Ponce-Mendoza4,5, & Pablo Corcuera2,6

1Programa del Doctorado en Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana. Departamento de Biología, Laboratorio de Ecología Animal, UAM-Iztapalapa,

A.P. 55-535, C.P. 09340, México, D.F., México.2Universidad Autónoma Metropolitana-Iztapalapa, Departamento de Biología. A.P. 55-535,

C.P. 09340, México, D.F., México.3IMEP, case 36, Université de Provence, 3 Place Victor Hugo, 13331 Marseille cedex 3,

France.4Departamento el Hombre y su Ambiente, Universidad Autónoma Metropolitana Xochimilco,

Calz. del Hueso 1100, Colonia Villa Quietud, C. P. 04960, México, D.F., México.5Centro Nacional de Investigaciones Disciplinarias en Conservación y Mejoramiento de Sistemas Forestales, INIFAP, Av. Progreso num. 5, Barrio Sta. Catarina, Del. Coyoacan,

C.P. 04010, Mexico, D.F., México.6Corresponding author. E-mail: pcmr@xanum.uam.mx

Resumen. – Relación entre aspectos del hábitat y la composición y diversidad de aves enáreas verdes selectas de la Ciudad de México. – Los espacios verdes de las ciudades contrarrestanla pérdida de la diversidad de aves debida a la urbanización, ya que proporcionan alimento, sitios deanidación y protección contra depredadores. Sin embargo, la influencia de la vegetación, el área,y superficies impermeables sobre la distribución de las especies silvestres todavía no es bien conociday puede variar entre estaciones e incluso de ciudad en ciudad en diferentes partes del mundo. En elpresente estudio se estimó la abundancia de aves en 12 parques de la Ciudad de México durantedos temporadas del 2008. Encontramos 96 especies de aves canoras y las agrupamos según susafinidades urbanas y estado migratorio. El número de especies aumentó con respecto al área en latemporada de reproducción, pero no durante la época migratoria. En contra de lo esperado, la riquezade aves migratorias aumentó en parques lejanos a las áreas naturales. Además, siete especies deParulinae invernales fueron comunes en todos los parques, por lo que podrían ser consideradas comosuburbanas. Por otra parte, las especies que utilizan recursos urbanos y toleran las condiciones creadaspor los seres humanos en las ciudades, fueron más abundantes en los parques con mayor superficiede áreas impermeables y/o situados lejos de las áreas naturales. En ambas estaciones, lo contrariofue cierto para las especies insectívoro-frugívoras, las cuales evitan las zonas urbanas por lo general.Este último grupo además fue más abundante en los parques más grandes. La mayoría de las espe-cies ampliamente distribuidas fueron insectívoro-granívoras del suelo y varias fueron gregarias. Análisisde especies indicadoras seleccionaron 22 especies en invierno y 17 en la temporada de reproducción.La distribución de estas aves estuvo asociada con la distancia a las áreas naturales y superficiesimpermeables en ambas temporadas, y con la cobertura de árboles micrófilos en la temporada invernal

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y la de Fraxinus uhdei en la época de reproducción. Nuestros resultados pueden ser útiles para estrate-gias de manejo encaminadas a la conservación de aves canoras en parques urbanos.

Abstract. – Green spaces within cities counteract the loss of bird diversity due to urbanization becausethey provide food, nesting sites, and protection against predators. Nevertheless, the influence of vegeta-tion, area, and impervious surfaces on the distribution of wild species is not well understood and can varybetween seasons and even from city to city in different parts of the world. In this study we estimated birdabundances in 12 parks of Mexico City during two seasons in 2008. We found 96 songbirds and groupedthem according to their urban affinities and migratory status. The number of species increased in relationto park area in the breeding season, but not during the migratory season. Unexpectedly, migratory birdrichness increased in relation to distance from natural woodlands. Furthermore, seven winter transientparulines were common in all parks and could therefore be considered as suburban adaptable. On theother hand, species that use urban resources and tolerate the conditions created by human beings intowns and cities were more abundant in parks with a high impervious cover and/or located far from natu-ral areas. In both seasons, the opposite was true for insectivore-frugivorous species, which generallyavoid urban areas. The latter group was more abundant in larger parks as well. Widely distributed spe-cies tended to be ground insectivore-granivores and many were gregarious. Indicator value analysesselected 22 species in winter and 17 in the breeding season. The distribution of these birds was associ-ated with distance to natural areas and impervious surfaces cover in both seasons, and with the cover ofsmall-leaved trees in the wintering season and the cover of Fraxinus uhdei in the breeding season.These results may be useful for future management actions focused on the conservation of songbirds inurban parks. Accepted 12 September 2013.

Key words: Bird diversity, urban parks, urbanization, vegetation, Mexico.

INTRODUCTION

Green spaces within cities mitigate the loss ofnatural habitats and the potential disappear-ance of species caused by the growth of urbanareas (Brawn et al. 2001, Fernández-Juricic2003, Chace & Walsh 2004, Yeoman & Mac-Nally 2005, Clergeau et al. 2006, McKinney2006). Recreational parks and other forestedareas within cities also help to counteract thebiotic homogenization represented by cosmo-politan species, which thrive in many built-upenvironments (Fernández-Juricic & Jokimäki2001, Renjifo 2001, MacGregor-Fors et al.2010). This is partly explained by vegetationcover which provides nesting sites, increasesfood availability, and offers protection againstpredators (cats, dogs and rodents) for manybird species (Park & Lee 2000, Sandström etal. 2005). Large parks with high foliage heightdiversity (sensu MacArthur & MacArthur1961) are particularly valuable to support alarge number of species (Park & Lee 2000,Ortega-Álvarez & MacGregor-Fors 2010,

Zuria 2010, Carbó-Ramírez & Zuria 2011,González-Oreja et al. 2012). Moreover, greenareas close to natural vegetation can alsoencourage bird colonization of parks that aremore isolated (Savard et al. 1999, Hess & Fi-scher 2001).

In general terms, the degree of urbaniza-tion within and around green areas can deter-mine the type of birds found in cities (Blair1996, Hostetler & Knowles-Yanes 2003). Theso-called urban exploiters, capable of usingman-made structures and urban resources(Blair 1996), are more abundant in highlyurbanized parks. These birds are mainly non-territorial omnivores or insectivore-granivores(Crooks et al. 2004, González-Ortega et al.2007, Shwartz et al. 2008). Inversely, wood-land insectivorous species, which tend toavoid cities, are more common in suburbanand better-preserved areas (Clergeau et al.2001, McKinney 2006). Nevertheless, addi-tional information concerning species diver-sity and distribution, as well as seasonalvariations in green areas is necessary to

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understand urban bird communities and torecommend strategies for their conservation.With this in mind, we analyzed the possibleinfluence of size, distance to the nearest natu-ral location, and cover of impervious surfaces(proportion of paved roads and constructionswithin each park), as well as of vegetationstructure on the diversity and distribution ofthe birds found in 12 parks in Mexico Cityduring the breeding and non-breeding sea-sons. The cover of all trees and shrubs in eachsite was also estimated, and species weregrouped according to foliage type. In additionto regression analyses between variables andcommunity parameters, birds were groupedaccording to habitat specificity and fidelity inorder to explore if foraging strategies, socia-bility (gregarious/solitary), and main foodtype differed between habitat specialists andgeneralists. Finally, indicator value analyseswere used to determine which birds wereassociated with particular parks or groups ofparks.

Our results were used to test the followinghypotheses: 1. Species richness would behigher in large parks, particularly in thosecloser to natural habitats. 2. Dominancewould be higher in parks with a high percent-age of impervious surfaces and in those beingmost distant from natural areas due to the rel-atively high abundance of a few opportunisticspecies. 3. Non-territorial omnivores/grani-vores would be dominant in parks with a highcover of impervious surfaces farther fromnatural areas. 4. Woodland insectivores wouldbe mainly present in large parks with a highvegetation cover and closer to natural areas.

METHODS

Study area. Mexico City is located between19°03’–19°36’N and 98°57’–99°22’W at 2240m a.s.l. Mean temperature fluctuates between12.5°C (January) and 20°C (August) (Varona-Graniel 2001). Mean annual precipitations

vary between 700 and 800 mm (Sanchez et al.1979), and there are two well-defined periods:the rainy season from June to September, andthe dry season from October to May.

The metropolitan area of Mexico City isapproximately 7854 km2, with a population of20,137,152 inhabitants (INEGI 2010). It isone of the largest human concentrations inthe world. The city includes 33.1 km2 of greenareas, including parks, gardens, arboreta, eco-logical reserves, and national parks (Benavides1992). From these, we selected 12 sites (parksfrom here on) which included four reserves,one arboretum, one area dedicated to sports,and seven recreational parks: Aragón (Ara),Ciudad Deportiva (Cdd), Cerro de la Estrella(Cer), Primera Sección de Chapultepec (Ch1),Tercera Sección de Chapultepec (Ch3),Parque Hundido (Hun), Jardín BotánicoUNAM (Jab), Parque Lira (Lir), Naucalli(Nau), Remedios (Rem), Tezozomoc (Tez),and Viveros de Coyoacán (Viv). The sites dif-fered in area, proximity to natural areas, coverof impervious surfaces, and vegetation struc-ture and composition.

Habitat characterization. We used 60 m in diam-eter circular plots in which we counted thenumber of tree species and estimated the fol-lowing variables: 1) cover of all trees andshrubs, 2) total plant cover, 3) total vegetationdensity, 4) foliage height diversity, 5) cover ofCupressus spp., 6) cover of needle shaped-leaved trees, 7) cover of small-leaved trees, 8)cover of broad-leaved trees. In addition, wemeasured the distance to the nearest naturalforested area, park area, and the proportion ofthe impervious surfaces cover.

Plant cover was estimated with an opticalsquare or periscope marked with two perpen-dicular axes (Montaña & Ezcurra 1980). Theapparatus has three mirrors arranged so that aperson looking horizontally can see theobjects found above. In each plot we countedthe number of foliage contacts with the point

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of intersection of the perpendicular lines.This procedure was repeated every meter anda half in two 60 m perpendicular transects(N–S and E–W) within each circular plot.Cover was assessed by the frequency of con-tacts or presence of vegetation in each point.Foraging preferences of many insectivorousbirds strongly depend on vegetation physiog-nomy (Holmes & Robinson 1981). Therefore,trees were grouped according to their foliagetype (small-leaved, broad-leaved, needle-shaped, scale-shaped of cover of Cupressusspp.), and the sum of their cover was obtainedfor each type. The foliage height diversity(sensu MacArthur & MacArthur 1961) wasestimated with the Shannon-Wiener indexusing the number of all contacts at 1 m inter-vals regardless of plant species (Corcuera &Zavala-Hurtado 2006).

The proportion of impervious areas,including roads, pathways, and buildings withrespect to the vegetation cover (all permeablesurfaces which included tree, shrub, and grasscover), was calculated using digital maps fromGoogle Earth (http://www.google.es/intl/es_es/earth/download/ge/agree. html). Wealso measured the minimal distance of parksfrom the nearest natural forested area usingthe same maps. Bird surveys. From January to August 2008, wedetermined the composition of all songbirdsseen or heard in the 12 parks. The observa-tions were conducted between sunrise (06:00h in late spring–early summer, and 07:00 h inwinter) and no later than 11:30 h. The lengthof the visits depended on the number of plotsin each park.

We used 8x40 binoculars and the Peterson& Chalif (1998) and Kaufman (2005) guidesto identify the bird species in the field. A cir-cular point count protocol (Hutto 1985) witha fixed radius of 30 m was used for the birdcounts. This radius has been used to reason-ably detect birds in sites with varying vegeta-tion densities (Hutto 1985, Corcuera &

Zavala-Hurtado 2006). The number of pointcounts ranged from 5 to 20, and was based onthe size and the accessibility of each park. Wecalculated the relative abundance by dividingthe total number of individuals of each spe-cies by the number of plots in each location.All parks were visited four times before thefinal counts in order to gain familiarity withthe bird songs and calls. Final relative abun-dances were obtained in February to earlyMarch 2008, which includes the dry seasonand migrants are still present (wintering sea-son) and in June 2008, when the rains havealready started and birds are breeding (breed-ing season). All individuals seen or heardwithin a 10 min period at each point countwere recorded. This interval is long enough inorder to count most birds present, includingrare species, and short enough so that theprobability of counting the same bird morethan once is minimized (Hutto 1985).

The conservation status was definedaccording to the list of Mexican threatenedspecies in the NOM-059-SEMARNAT-2010(SEMARNAT 2010).

Finally, we searched for the main foodtype (insect/seed, insect/fruit, insects, nectar,broad), foraging strategy (hovering, gleaning,fly-catching), and main foraging substrate(foliage, bark, ground, flower, bark), grouping(solitary, flock) of each species included in theliterature (Howell & Webb 1995, Del OlmoLinares & Roldán Velasco 2007, Grosselet &Ruiz 2008), the internet (http://neotropi-cal.birds.cornell.edu/portal/home), and per-sonal observations.

STATISTICAL ANALYSISDiversity. Since the sample size was differentbetween parks, we used rarefaction analyses(James & Rathbun 1981, Colwell et al. 2004)to compare the number of bird speciesamong sites. We used the first Jackknife andthe second Chao order estimators with Esti-mateS (version 8, Colwell 2006) to assess the

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comprehensiveness of the bird species survey.These non-parametric species richness esti-mators have been found to give reasonableapproximations at small grain size sampleunits (Hortal et al. 2006, González-Oreja et al.2011). Empirical studies have also shown thatthey are relatively insensitive to samplingintensity (Colwell & Coddington 1994, Gotelli& Colwell 2001, Brose 2002, Witman et al.2004, Hortal et al. 2006, González-Oreja et al.2011). Species dominance was estimated withthe Simpson index (Magurran 1988).

Simple linear regressions were used toanalyze the relationship between rarefied spe-cies richness, relative abundance and domi-nance, and the independent variables. Wepreviously confirmed that the data compliedwith the normality and homoscedasticityassumptions with the Number Cruncher Sta-tistical System software (Hinze 2001).

Habitat specificity and fidelity. Bird species wereclassified according to their habitat breadth(percentage of sites where the species waspresent) and fidelity or incidence (percentageof plots in sites where the bird species waspresent) following González-Oreja et al.(2007). We selected an unweighted pair groupaverage method (UPGMA) with the Bray-Curtis dissimilarity coefficient (Orlóci 1978)using MVSP (Kovach 1999), and comparedthe main food type, foraging strategy, sub-strate, and grouping between the resultinggroups (e.g., low specificity vs high specificityand fidelity).

We used indicator value analyses (IndVal)to select species that were associated with oneor a combination of two or more parks. Arandomization procedure (Dûfrene & Legen-dre 1997) was used to obtain the value foreach species. Specificity was estimated as:Aij= N individualsij/ N individuali, where N indi-vidualsij is the mean number of species i on sitej, and N individuali the sum of the meannumbers of individuals of species i over all

sites. Fidelity was estimated as follows: B ij =N sites ij/ N sites j, where N sites ij is the numberof sites in habitat j where species i is present,and N site j the total number of sites in thehabitat. The indicator value for species i in thehabitat j is defined as: IndVal ij = v (A ij * B ij).The resulting values have an associated statis-tical significance and those species with anIndVal value > 70% were regarded as habitatindicators (Van Rensburg et al. 1999). TheIndVal analyses were performed with thefunction “multipat” (with this code: func ="Indval.g", duleg = TRUE, nperm = 9999)with the package “indicspecies” (De Cáceres& Legendre 2009) in R 2.14.0 (http://cran.r-project.org/).

The relationship between the indicatorspecies distribution and the independent vari-ables was analyzed with a canonical corre-spondence analysis (CCA) with MVSP(Kovach 1999). This technique is used toobtain synthetic environmental gradients ofgroups of ecological data and to detect speciesdistribution patterns that can be explained bya group of environmental variables (Ter Braak& Verdonshot 1995).

RESULTS

Independent variables. We registered 59 treeand shrub species. Non-native species, such asthe gum tree or eucalypt (Eucalyptus spp.),sheoak (Casuarina equisetifolia), Australiansilver-oak (Grevillea robusta), and Peruvianpeppertree (Schinus molle) were dominant inmost parks. The native vegetation was wellrepresented by the Mexican white cedar(Cupressus lusitanica) and the tropical ash(Fraxinus uhdei). Park size varied from 11 to1100 ha. Foliage cover ranged from 12.50contacts per plot in Cer to 27.62 in Hun.Some parks consisted mainly of green areas(Cer, Ch3, and Rem with 12, 11.4, and 11.8%impermeable surfaces) while others, such asCdd (52% impermeable surfaces) had a high

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percentage of paved roads and constructions(Table 1).

Bird species composition and diversity. During thestudy period, we registered a total of 1742individuals, representing 96 species and 24families (Appendix 1). According to the Mex-ican official standards for threatened species,NOM-059-SEMARNAT-2010 (SEMARNAT2010), the Brown-backed Solitaire (Myadestesoccidentalis, Turdidae) is under special protec-tion.

In average, the estimated percentage ofspecies for the wintering season ranged from76%, according to Jackknife 1, to 81%, asindicated by Chao 2. The values were higherfor the breeding season, and ranged from84% as predicted by Jackknife 1, to 93%,according to Chao 2. Ciudad Deportiva, Viv,Ch1, and Ch3 had the highest rarefied rich-ness in the migratory season (Table 2), andCer and Rem in the breeding period (Table 3).

In the migratory season, the total birdabundance (R2 = 0.4024, F10 = 8.57, P =0.015), dominance (R2 = 0.3441, F10 = 5.24, P= 0.045), and the number of migratory indi-viduals (R2 = 0.3504, F10 = 5.39, P = 0.045)showed a negative relationship with distanceto natural areas. The same variable had a posi-tive relationship with the abundance of resi-dent species (R2 = 0.3820, F10 = 6.18, P =0.033) and the migratory rarefied richness (R2

= 0.6581, F10 = 19.25, P = 0.001). The abun-dance of migratory species presented a posi-tive relationship with total foliage cover (R2 =0.5562, F10 = 12.53, P = 0.005), and the dom-inance of the total bird community was posi-tively related to foliage height diversity in thewintering season (R2 = 0.5957, F10 = 14.84, P= 0.003).

During the breeding season, rarefied spe-cies richness was higher in larger parks (R2 =0.3587, F10 = 5.59, P = 0.039) and the propor-tion of impervious surfaces had a positiverelationship with the number of birds (R2 =

0.5163, F10 = 10.67, P = 0.008). We did notfind any significant relationships between thebird community characteristics and the treesgrouped according to their leaf types.

Indicator species. On first inspection, all specieswere classified according to their specificityand fidelity (or incidence) percentages. Weobtained three clusters for each season. Dur-ing the migratory season (Fig. 1a), the widthof the distribution was 13.5 ± 4.0% for thefirst cluster and 21.3 ± 11.9% for the secondone. Fidelity was higher in the first cluster(37.1 ± 16.2% v 10.9 ± 3.5%). Specificity andincidence in the third group were 73.7 ±23.4% and 39 ± 15.1% respectively. In thebreeding season (Fig. 1b), the first two groupsincluded narrowly distributed species (10.7 ±5.1% and 13.3 ± 7.5%), but incidence waslow in the first group (12.7 ± 4.7%) in com-parison with the second one (46.2% ±15.8%). In the third group, birds were foundin a wider range of parks (75.0 ± 23.4%) andhad intermediate incidence values in compari-son with the other clusters (19.2 ± 7.9).

During the migratory months, the firstcluster (narrowly distributed birds) included50% of foliage frugivores-insectivores (Fig. 1,species codes in Appendix 1). Most of themwere gleaners (63%) but 38% used aerial for-aging tactics. The second cluster included86% gleaning species. Most were insectivo-rous (44%) and foraged in the foliage oftrees and shrubs (41%). An additional 26% ofthe species were frugivore-insectivores. Mostspecies from the third group (widely distrib-uted birds) were ground gleaners (92%) thatfeed on seeds and insects, and 46% were gre-garious.

The first cluster (narrow distribution, lowincidence) for the reproductive seasonincluded 14 species (Fig. 2). Most of themwere frugivore-insectivores (50%), solitary(86%), and foraged in the foliage of trees andshrubs (57%). The second group (narrow

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distribution, high incidence) consisted of onlyfive species (Fig. 2). Three were flycatchers:Cassin’s Kingbird (Tyrannus vociferans), North-ern Beardless Tyrannulet (Camptostomaimberbe), and Vermilion Flycatcher (Pyro-cephalus rubinus), one was nectarivore (Cinna-mon-bellied Flowerpiercer) and the other anunderstory insectivore (Carolina Wren,Thryothorus ludovicianus). The most-repre-sented species corresponding to the thirdgroup (wide distribution) were granivore-insectivores (47%), and most foraged onthe ground (65%). Many were gregarious(47%).

According to the indicator value analysis,22 species in the migratory season and 17 inthe breeding season were significantly associ-ated to one park or to a combination of parks.The wintering season included seven speciesthat were indicators of a single park, and sixthat were widely distributed and indicators of≥ five parks (low habitat specificity but highfidelity). In the breeding season, there were 17indicator species. Six species were associatedto a single park, and another six had a wide

distribution and were indicators of ≥ fiveparks.

During migration, the first axis of theCCA (Eigenvalue = 0.152) explained 17.36%of the variance and was significantlycorrelated with impervious surfaces (Urb,r = - 0.660, P < 0.02) and the cover of small-leaved trees (Smal, r = 0.731, P < 0.01) (Fig.3). The second axis (Eigenvalue = 0.103)accounted for a further 11.71% of the vari-ance and was correlated with the cover ofsmall-leaved trees and distance to the nearestnatural area (Dist) (r = 0.665, P < 0.02 and r =0.775, P < 0.005 respectively). Besides theGreat-tailed Grackle (qm), House Finch (cm),House Sparrow (pd), Rufous-backed Robin(tr), Bushtit (pmi), and Inca Dove (ci), whichtend to be gregarious, solitary foliage insecti-vorous as Orange-crowned Warbler (Oreothly-pis celata) (oc), Ruby-crowned Kinglet (rc), andTownsend’s Warbler (Setophaga townsendi) (st),together with the Vermilion Flycatcher (pr)were associated to parks with high impervioussurfaces (Urb) that were far from natural areas(Dist). Cassin’s Kingbird (tv), Baltimore Oriole

TABLE 1. Number of count points, area size, distance to nearest natural area, percentage of impervioussurfaces, number of tree species, total foliage cover, foliage height diversity, cover of Cupressus spp., needleshaped-leaved, broad-leaved, and small-leaved trees in twelve parks of Mexico City. Cover is expressed innumber of contacts per plot (see text). Ara = Bosques de Aragón, Cdd = Ciudad Deportiva, Cer = Cerrode la Estrella, Ch1 = Primera Sección de Chapultepec, Ch3 = Tercera Sección de Chapultepec, Hun =Parque Hundido, Jab = Jardín Botánico de la UNAM, Lir = Parque Lira, Nau = Naucalli, Rem = LosRemedios, Tez = Tezozomoc, Viv = Viveros de Coyoacán.

Park Ara Cdd Cer Ch1 Ch3 Hun Jab Lir Nau Rem Tez VivPoint count numberArea (ha)Distance to natural area (km)Impervious surfaces (%)Tree species numberTotal foliage coverFoliage height diversity (H´)Cypress coverNeedle shaped-leaved coverBroad-leaved coverSmall-leaved cover

1011424.030.011

13.11.60.41.19.42.0

715017.552.020

15.11.20.17.04.82.2

10110010.912.010

12.51.50.51.47.63.0

1823012.324.718

18.21.491.60.48.90.7

1828612.311.415

17.71.70.40.314.70.3

815

11.330.022

27.61.44.73.518.50.8

62374.618.520

19.11.40.65.111.32.0

5119.536.415

24.01.23.01.016.40.2

6433.529.911

19.51.51.55.112.00.6

74002.611.815

24.51.72.50.119.72.1

10285.632.127

12.71.50.92.15.62.3

2040

10.540.712

19.11.33.21.722.61.2

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(ig), Grey Silky-flycatcher (pc), and AmericanRobin (tm) are solitary frugivore-insectivoresand, together with House Wren (Troglodytesaedon) (ta) and Lesser Goldfinch (Spinus psal-tria) (sps), were found in parks nearest to nat-ural areas with a low cover of impervioussurfaces and a high cover of small-leaved trees(Smal). The distribution of these species wasnarrow during this season. To a lesser extent,Yellow-rumped Warbler (sc), Bewick’s WrenThryomanes bewickii (tb), and Canyon Towhee(pf) were also more abundant in this type ofparks.

During the breeding season (Fig. 4), thefirst axis (Eigenvalue = 0.094) explained

15.59% of the variation and was positivelycorrelated with the cover of impervious sur-faces (Urb, r = 0.691, P < 0.02). The secondaxis (Eigenvalue = 0.072) explained a further12% of the variation) and was significantlycorrelated with the cover of Tropical Ash(Fra) (r = 0.898, P < 0.001). Great-tailedGrackle, Inca Dove, Vermilion Flycatcher,Rufous-backed Robin, and House Sparrow,together with Curve-billed Trasher (tc) andNorthern Beardless Tyrannulet (cai), wereagain related with parks with a high cover ofimpervious surfaces. With the exception ofthe Vermilion Flycatcher all had wide distri-butions. Three frugivore-insectivores, Scott’s

TABLE 2. Observed specific richness, rarefied richness, mean abundance, abundance standard deviation(SD), and dominance (Simpson index) of birds found in 12 parks in Mexico City during the winteringseason of 2008. The Jackknife1 and Chao2 estimators are also shown.

Parks Ara Cdd Cer Ch1 Ch3 Hun Jab Lir Nau Rem Tez VivObserved richnessRarefied richnessChao2 Chao2 (%)Jackknife1 Jackknife1 (%)Mean abundanceAbundance SDSimpson index

188.524.374

24.374

24.515.20.20

1513.116.292

17.685

13.13.90.09

169.622.371

22.371

15.410.00.21

2011.723.983

26.675

10.911.00.15

1811.020.388

22.779

12.016.80.30

189.819.890

23.377

22.210.40.17

1710.522.874

23.774

23.011.70.33

1414.016.485

18.874

10.42.30.10

137.818.869

19.766

17.69.60.39

127.712.694

14.682

24.016.50.46

97.69.396

10.8839.57.20.27

2312.934.466

31.672

10.710.90.03

TABLE 3. Observed specific richness, rarefied richness, mean abundance, abundance standard deviation(SD), and dominance (Simpson index) of birds found in 12 parks in Mexico City during the breedingseason of 2008. The Jackknife1 and Chao2 estimators are also shown.

Parks Ara Cdd Cer Ch1 Ch3 Hun Jab Lir Nau Rem Tez VivObserved richnessRarefied richnessChao2 Chao2 (%)Jackknife1 Jackknife1 (%)Mean abundanceAbundance SDSimpson index

1410.914.298

15.888

13.97.50.13

1310.113.010013.010024.210.60.16

2316.728.481

31.174

10.35.80.13

1610.116.199

17.989

15.919.10.07

1913.819.597

21.8878.98.20.18

1310.613.894

15.683

14.07.10.17

1312.413.894

16.3799.83.40.14

1414.016.088

18.874

10.02.60.11

119.911.893

13.581

11.84.10.14

1715.523.074

23.0739.02.50.07

1310.813.010013.993

14.07.70.13

1611

16.398

17.989

11.212.40.12

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Oriole (ip), Cassin’s Kingbird, and Black-headed Grosbeak (pm), and two nectarivores,an unidentified species (hum) and Cinnamon-bellied Flowerpiercer (db), were negativelyrelated with cover of impervious surfaces andpositively with the cover of tropical ash.

DISCUSSION

The bird species distribution followed a non-random pattern. In general, birds that useman-made structures, also known as urbanexploiters, were more common in parks withhigh cover of impervious surfaces. They weremainly omnivorous or insectivore-granivores,gregarious, and ground gleaners. Migratoryfoliage insectivores, which generally avoidurban areas, were more abundant in largeparks close to natural areas. Nevertheless,some species of this guild were widespreadthroughout the study sites. Frugivore-insecti-

vores that use an aerial strategy to catch preywere mainly found in the largest parks and/orin parks with low impervious surfaces thatwere relatively close to natural areas.

We found 96 species of resident andmigratory songbirds. The species richnessestimators showed that most of them wereincluded in the counts. The number of specieswas similar to that reported by Varona-Graniel (2001) for seven parks in Mexico City.Species composition, on the other hand, var-ied considerably between the two studies.Fifty species were present in both reports,while 38 were observed only in the presentstudy. Compositional changes of migratoryspecies are common in urban areas (Husté &Boulinier 2007) and the difference betweenthe species lists of both studies may be due tochanges in the habitats used during stopoverto the final destination (Griffis-Kyle & Beier2005).

FIG. 1. Classification of the bird species found in 12 parks of Mexico City based on habitat specificity andincidence during the wintering season of 2008. The Bray Curtis distance with the UPGMA clusteringmethod was used. Species codes are in Appendix 1.

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As shown in other studies (Fernández-Juricic 2003, Crooks et al. 2004, Husté et al.2006, MacGregor-Fors 2008), the regressionbetween rarefied richness and park area wassignificant in the breeding season, as pre-dicted by the island biogeography theory(MacArthur & Wilson 1967). This partiallysupports our first hypothesis because thesame relationship did not hold for the winter-ing season. The lack of significance betweenarea and number of migrant species is notunexpected. Askins et al. (1992), for example,found more species on the island of St. Johnthan on St. Thomas, despite the former beingsmaller. This was because St. John had amuch higher proportion of forest cover. Fur-thermore, the theory does not take intoaccount factors, such as edge effect, sur-rounding matrix nature, and anthropogenicdisturbance (Laurance 2008), and this couldalso explain the lack of a significant relation-ship between species richness and area for thebirds that visit the parks during migration.

We expected to find high numbers of afew urban exploiter species in the parks withthe highest cover of impervious surfaces, andfurthest from the natural areas. This would bereflected in high dominance values, as pre-dicted by our second hypothesis. During themigratory season we found that the oppositewas true. Dominance was higher in parks nearnatural areas and with a low percentage ofpaved areas and constructions. This was dueto large flocks of Yellow-rumped Warblersand it explains the negative correlationbetween the number of migratory individualsand distance and impervious surfaces. On theother hand, we observed high numbers ofspecies typically found in urban areas (i.e.,Rock Dove, Great-tailed Grackle) in neigh-borhood squares that were not included inour study. Furthermore, in the breeding sea-son parks far from natural areas supported ahigher number of birds. Abundance was alsohigher in those parks with a high cover ofimpervious surfaces. The positive relation

FIG. 2. Classification of the bird species found in 12 parks of Mexico City based on habitat specificity andincidence during the breeding season of 2008. The Bray Curtis distance with the UPGMA clusteringmethod was used. Species codes are in Appendix 1.

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between urban residents and urbanization hasbeen reported elsewhere (Jokimäki et al. 1996,Ortega-Alvárez & MacGregor-Fors 2009) andit is the result of large populations of gregari-ous birds adapted to urban conditions. It hasalso been argued that during stopover, resi-dent birds may be confined to central andhighly urbanized areas to avoid competitionwith migrants which are more abundant infragments close to woodlands (Rodewald &Brittingham 2002, Crooks et al. 2004, Piper &Catterral 2006).

The number of migrants was positivelycorrelated with foliage height diverstiy andtotal plant cover. These results support addi-tional studies showing that insectivorousmigratory species are more abundant in areaswith a high plant structural complexity(Holmes et al. 1979, Holmes & Robinson

1981, Strong 2000, Corcuera & Zavala-Hur-tado 2006, Carbó-Ramírez & Zuria 2011).There is also evidence suggesting that proxi-mate factors, such as branch arrangement andvertical foliage arquitecture, may have a directinfluence on species richness, abundance, anddominance (Marzluff & Rodewald 2008,Müller et al. 2010).

The positive relationship between distanceand migratory species richness was unex-pected and could be explained by the pres-ence of relatively large water bodies and/orwell irrigated gardens with luxuriant vegeta-tion that are closer to some of the parkslocated far from natural areas (Ara, Ch1, Lir).

In the incidence/habitat breadth classifi-cations, most species with low habitat speci-ficity were granivorous, ground gleaners, andgregarious in the two seasons, supporting our

FIG. 3. Distribution of 22 indicator bird species in 12 parks of Mexico City according to a Canonical Cor-respondence Analysis (wintering season). Distance to the nearest natural area = Dist, small-leaved treecover = Smal, impervious cover surfaces = Urb. Species codes are in Appendix 1.

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third hypothesis. The indicator value analysisshowed that generalist birds adapted to citiesare typical of parks with the highest cover ofimpervious cities according with other studies(Mills et al. 1989, Blair 1996, González-Orejaet al. 2007, Carbó-Ramírez & Zuria 2011).These species include House Sparrow, Great-tailed Grackle, Inca Dove, and Rock Dove.They occur in all large cities in Mexico andillustrate the biotic homogenization tendencyworldwide (Clergeau et al. 2006, McKinney2006).

Even though migrant insectivores are usu-ally rare in urban areas (McKinney 2006), thenumber of transient species responded posi-tively to distance from natural areas in ourstudy.

Moreover, three migrants (Ruby-crownedKinglet, Townsend’s Warbler, and Orange-

crowned Warbler) were associated to parkswith high impervious cover and far from nat-ural areas, and five more: Yellow-rumpedWarbler, Nashville Warbler (Oreothlypis rufica-pilla), Wilson’s Warbler, Blue-gray Gnat-catcher, and Least Flycatcher (Empidonaxminimus) were abundant in all parks.González-Oreja (2011) also found an unex-pected high number of Nearctic warbler spe-cies in urban sites throughout Mexico. Thissuggests that some of these birds may havethe flexibility to exploit urban environmentsto a certain degree (González-Oreja 2011)and could be included in the suburbanadapter category according to the classifica-tion used by Blair (1996). However, there islittle information about habitat selection andforaging behavior of these parulines in urbanareas, and further study is necessary to under-

FIG. 4. Distribution of 17 indicator bird species in 12 parks of Mexico City according to a Canonical Cor-respondence Analysis (breeding season). Distance to the nearest natural area = Dist, Tropical Ash cover =Fra, impervious cover surfaces = Urb. Species codes are in Appendix 1.

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stand their habitat preferences in urbanareas.

Specialist birds usually have higher abun-dances and richness in larger parks (Blair1996, Rodewald & Brittingham 2002, Crookset al. 2004, González-Oreja et al. 2007,MacGregor-Fors 2008), and our last hypothe-sis predicted that these species would be foli-age-foraging solitary territorial birds. Eventhough species richness was correlated witharea in the breeding season, park size was notsignificantly correlated with any of the mainaxes in the bird species ordination. On theother hand, we found that insectivores thatinclude fruit as an important part of their dietduring part of the year were negatively corre-lated with impervious surfaces. These in-cluded Western Kingbird in both seasons,Baltimore Oriole, Grey Silky-flycatcher, andAmerican Robin in the wintering season, andScott’s Oriole and Black-Headed Grosbeak inthe breeding season. The Cinnamon-belliedFlowerpiercer in the reproductive season andthe House Wren during migration respondedin the same way to this variable. It has beensuggested that, for some species, shrub coverand vegetation physiognomy are more impor-tant than tree species composition (Park &Lee 2000, Carbó-Ramírez & Zuria 2011), andthis may explain the presence in these parksof at least some of these birds (i.e., CarolinaWren, Northern Beardless Tyrannulet).

Our study confirmed what other studieshave demonstrated regarding the ubiquitouspresence of urban exploiters within city parks.On the other hand, some migrant foliageinsectivores were present in all sites or wereassociated with urbanized parks, and thissuggests that many species, at least duringstopover, are more flexible in their habitatrequirements than expected and/or thaturban parks represent adequate habitats fora wide variety of birds. However, in bothseasons a group of birds had a narrow distri-bution and were associated to the largest

parks. These were mainly territorial fly-catch-ing frugivore-insectivores, which may be moresusceptible to the fragmentation of theirhabitats.

In addition to presenting recent informa-tion on the composition and diversity of birdsin parks of Mexico City, our results could beincorporated into conservation and wildlifemanagement plans in urban areas in otherlarge cities elsewhere.

ACKNOWLEDGMENTS

We wish to thank the Ministry of the Envi-ronment and Natural Resources (SEMAR-NAT) and all the political delegations thatgranted us permission to use the city parks toconduct the fieldwork. A special acknowl-edgement is due to the administration staff ofthe Viveros de Coyoacán, Tezozomoc, andBosque de Chapultepec. GC would like toacknowledge the National Council for Scienceand Technology (CONACYT), Mexico, forsupporting his Ph.D. studies.

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APPENDIX 1. Bird species found in 12 parks within Mexico City, including the two seasons censes. Thecodes used in multivariate analyses are also shown.

Species Code Ara Cdd Cer Ch1 Ch3 Hun Jab Lir Nau Rem Tez VivAegithalidaePsaltriparus minimusBombycillidaeBombycilla cedrorumCardinalidaeCardinalis cardinalisPasserina caeruleaPasserina cyanaea Pheucticus melanocephalusCorvidaeAphelocoma ultramarinaCyanocorax yncasColumbidaeColumbia liviaColumbina incaZenaida macrouraEmberizidaeAimophila ruficepsAtlapetes pileatusDiglossa baritulaMelospiza georgianaMelospiza lincolniMelospiza melodiaOriturus superciliosusPipilo fuscusSpizella passerinaSpizella pusillaFringillidaeCarpodacus mexicanusSpinus psaltria

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APPENDIX 1. Continuation.

Family/species Code Ara Cdd Cer Ch1 Ch3 Hun Jab Lir Nau Rem Tez VivIcteridaeEuphagus cyanocephalusIcterus abeilleiIcterus bullockiiIcterus cucullatusIcterus galbulaIcterus parisorumMolothrus aeneusMolothrus aterQuiscalus mexicanusLaniidaeLanius ludovicianusMimidaeDumetella carolinenisToxostoma curvirostreToxostoma longirostreMelanotis caerulescensParidaePoecile sclateriParulidaeBasileuterus rufifronsCardellina pusillaGeothlypis nelsoniGeothlypis tolmieiIcteria virensMniotilta variaMyioborus miniatusMyioborus pictusOreothlypis celataOreothlypis ruficapillaPeucedramus taeniatusSeiurus noveboracensisSetophaga coronataSetophaga magnoliaSetophaga nigrescensSetophaga occidentalisSetophaga petechiaSetophaga townsendiSetophaga virensPasseridaePasser domesticusPicidaeColaptes auratusPicoides scalarisSphyrapicus varius

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297

SONGBIRDS OF MEXICO CITY PARKS

APPENDIX 1. Continuation.

Family/species Code Ara Cdd Cer Ch1 Ch3 Hun Jab Lir Nau Rem Tez VivPtiligonatidaePtilogonys cinereusRegulidaeRegulus calendulaSturnidaeSturnus vulgarisSylviidaePolioptila caeruleaThraupidaePiranga ludovicianaPiranga olivaceaPiranga rubraTrochilidaeAmazilia beryllinaCynanthus latirostrisHylocharis leucotisTroglodytidaeCatherpes mexicanusThryomanes bewickiiTroglodytes aedonThryothorus ludovicianus TurdidaeCatharus guttatusMyadestes occidentalisTurdus migratoriusTurdus rufopalliatusTyrannidaeCamptostoma imberbeContopus cooperiContopus pertinaxContopus sordidulusEmpidonax flaviventrisEmpidonax minimusMitrephanes phaeocercusMyiarchus tuberculiferPyrocephalus rubinusSayornis sayaTyrannus vociferansTyrannus tyrannusVireonidaeVireo cassiniVireo flavifronsVireo gilvusVireo huttoniVireo solitarius

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