Bird communities in different phytophysiognomies of the cerrado biome

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Bird communities in different phytophysiognomies of

the cerrado biome

Thiago Orsi Laranjeiras a , Nárgila Gomes de Moura c , Ludgero Cardoso Galli Vieira e , Ronaldo Angelini d & Adriana Rosa Carvalho b

a

Instituto Chico Mendes para Conservação da Biodiversidade, Parque Nacional do Viruá, Boa Vista, RR, Brazil

b

Departamento de Botânica, Ecologia e Zoologia, Universidade Federal do Rio Grande do Norte, UFRN, Natal, RN, Brazil

c

Museu Paraense Emilio Goeldi, Belém, PA, Brazil d

Departamento de Engenharia Civil, Universidade Federal do Rio Grande do Norte, UFRN, Natal, RN, Brazil

e

Universidade de Brasília, Planaltina, (DF), Brazil Version of record first published: 05 Mar 2012.

To cite this article: Thiago Orsi Laranjeiras , Nárgila Gomes de Moura , Ludgero Cardoso Galli Vieira , Ronaldo Angelini & Adriana Rosa Carvalho (2012): Bird communities in different phytophysiognomies of the cerrado biome, Studies on Neotropical Fauna and Environment, 47:1, 41-51

To link to this article: http://dx.doi.org/10.1080/01650521.2012.660779

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Vol. 47, No. 1, April 2012, 41–51

ORIGINAL ARTICLE

Bird communities in different phytophysiognomies of the cerrado biome

Thiago Orsi Laranjeirasa_{, Nárgila Gomes de Moura}c_{, Ludgero Cardoso Galli Vieira}e_{, Ronaldo Angelini}d_*

& Adriana Rosa Carvalhob

a_{Instituto Chico Mendes para Conservação da Biodiversidade, Parque Nacional do Viruá, Boa Vista, RR, Brazil;}b_Departamento de Botânica, Ecologia e Zoologia, Universidade Federal do Rio Grande do Norte, UFRN, Natal, RN, Brazil;c_{Museu Paraense} Emilio Goeldi, Belém, PA, Brazil;d_{Departamento de Engenharia Civil, Universidade Federal do Rio Grande do Norte, UFRN,} Natal, RN, Brazil;e_{Universidade de Brasília, Planaltina, (DF), Brazil}

(Received 29 April 2010; accepted 23 January 2012)

The Brazilian cerrado is a global biodiversity hotspot and one of the most poorly sampled regions in the Neotropics. We describe the bird community structure among the distinct cerrado phytophysiognomies and among different periods of the day, in five environments of this biome. Bird observations were carried out from October 2003 to March 2005, by visual and acoustical records, using transect and point-count surveys. We found a total of 128 species in the area, including six species endemic to the cerrado biome, and found evidence of breeding in nine species. The bird community differed significantly among phytophysiognomies. Our data show that, even at a small spatial scale, high richness, endemism and nesting are likely to be found in the cerrado. The variation in species occurrence also reveals the unique community structure of each cerrado habitat type over time, even if the same vegetal formations were considered between habitats. Our results support the decision to convert the study site into the first university cerrado conservation unit, since this will protect a broad range of species and will guarantee habitats for some endemic birds.

Keywords: hot spot; Neotropical birds; community structure; Brazilian savanna; cerrado; Nature Conservation Unit

Introduction

Cerrado (Brazilian savanna) is a biome consisting of habitat types which range from dense savanna forests to areas of open vegetation (Ribeiro & Walter 1998) and is a global biodiversity hotspot in South America. The biome is exposed to high rates of primary habitat conversion due to agriculture, principally a recent expansion of soybean cultures and pasturelands (Myers et al. 2000; Klink & Moreira 2002; Blamires et al. 2008). The species richness in the cerrado has been estimated to be around 320,000 species (Silva & Bates 2002; Klink & Machado 2005), which are dis-tributed in no more than 5% of its original area of 2.5 million km2 _{(Marris 2005; Silva et al. 2006). The}

cerrado avifauna is made of approximately 837 species, of which about 36 are endemic (Cavalcanti 1999; Silva & Bates 2002; Marini & Garcia 2005; CBRO 2011) and 48 are nationally or globally threatened (IBAMA 2003; Borges & Marini 2010; IUCN 2011). This biome has traditionally been considered to be one of the most poorly sampled regions in the Neotropics (Colli et al. 2002) despite its increasing fragmentation and loss of natural habitats, which implies a rapid loss of many

*Corresponding author. Email: angelini@ct.ufrn.br; ronangelini@yahoo.com.br

endemic and rare species (Myers et al. 2000; Brooks et al. 2002).

Habitat fragmentation is currently considered to be one of the most important threats to global biodiversity (Vitousek et al. 1997), and is followed by the loss of bird species by isolation, inbreeding, local and/or regional extinction, nest predation and parasitism (Findlay & Bourdages 2000; Marini 2001; Santos & Tabarelli 2002; Herkert et al. 2003; Borges & Marini 2010). In addition, fragmentation may lead to a simplified community structure, with a reduction in the number of specialist and an increase in the number of generalist species (D’Ângelo-Neto et al. 1998).

In spite of the importance of habitat fragmenta-tion, there have only been a small number of studies on the structure of bird communities in different cerrado phytophysiognomies (with the exceptions being: Monteiro & Brandão 1995; Blamires et al. 2001, 2002). This information gap makes it difficult to estab-lish effective strategies for conservation, which require information on the richness, abundance, endemism and spatial distribution of species (Cavalcanti 1999).

http://dx.doi.org/10.1080/01650521.2012.660779 http://www.tandfonline.com

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Therefore, the objective of this study was to deter-mine whether bird community structure varies among the cerrado’s habitat types and among different obser-vation periods. Our assumption is that the bird com-position is similar in environments of the same habitat type; thus, the bird species composition is expected to be distinct according to either different vegetational types or periods of the day.

Materials and methods

Study area

This study was performed in an ecological reserve at the campus of the Universidade Estadual de Goiás (UEG), in the city of Anápolis (GO). This area is in the process of becoming a Nature Conservation Unit (UCN), named as “Area of Relevant Ecological Interest” (Área de Relevante Interesse Ecológico – ARIE). This UCN will encompass 41% of the total campus area (134 ha) and consists of three different phytophysiognomies (Figure 1).

The university campus is situated at the mar-gins of highway BR-153, centered at the coordinates 16◦2034S, 48◦5251W and is surrounded by farms and the Anápolis Agro-Industrial District. Elevation varies between 1040 and 1100 m. Their lowest por-tions are the Barreiro and Urubu streams, which cut transversally across the area. The region has a semi-humid tropical climate (Nimer 1989) with two very well defined seasons, a rainy season in summer (October to March) and a dry season in winter (April to September).

To construct a bird inventory, the campus area was divided into five environments, according to their phytophysiognomy and location. These areas include open cerrado sensu stricto and mesophyllous semideciduous forests associated with gallery forest on the edge of the two streams (Table 1, Figure 1).

Data collection

Bird observations were carried out from October 2003 to March 2005. In order to qualitatively describe the bird fauna, all sightings in all environments were considered. For the quantitative analysis of the bird assemblage, the method of observation through visual and/or audible records (Bibby et al. 1992) was used at 18 points distributed through the different environ-ments according to their size (Table 1). The sampling points were located inside the vegetated area and at least 200 m apart from each other. All birds within a radius of 50 m around each point were counted. Nests were also counted and were visually inspected whenever possible.

All of the 18 points were sampled once a month for three days at two different time periods in the morning (06:00–09:00 and 09:00–12:00 h) and in the afternoon (12:00–15:00 and 15:00–18:15 h). Observations were conducted for 20 minutes at each point and both the visual or auditory species observations were recorded. Species recorded in transit between point counts were only used in the qualitative survey.

Each environment had a total number of sam-pling periods and a samsam-pling effort that reflected the number of points on each environment (Table 1). The total sampling effort included 288 effective hours of observations. When both the observations of move-ment and the qualitative survey were considered, the sampling effort totaled more than 400 h of observation.

The taxonomic identification of species was car-ried out according to Ridgely & Tudor (1989, 1994), Andrade (1997), Sick (1997) and Souza (2004). Visual and vocal recognition were done with the help of 10× 25 binoculars and an amateur mini-recorder used to record unknown vocalizations for later identifica-tion. The scientific nomenclature and taxonomic order follow those established by the Comitê Brasileiro para Registro Ornitológico (CBRO 2011).

Species recorded during qualitative surveys were reliably identified at the level of the genera, but had uncertain detection at the level of species and none of these species were included in the following statistical analysis.

Data analysis

The data were used to estimate the species frequency of occurrence (FO), considering only the samples taken during the two first blocks of time (06:00–09:00; 09:00–12:00 h). The FO is the proportion of sam-ples per environment (in %) where the species were observed.

In order to determine the sampling sufficiency (SS), richness was estimated through a second-order Jackknife estimator. This estimator takes into consid-eration the number of rare species and the number of samples used to estimate the total richness in the area and considers the samples taken during all of the time blocks (Krebs 1989).

To evaluate the difference in the structure of bird communities in the five studied environments, a mul-tiple response permutation procedure (MRPP) and a classification strength (CS) analysis were used.

The MRPP is a non-parametric analysis that tests whether there are differences among two or more sam-ple groups. In this analysis, a distance template is first calculated among all samples. The analysis then becomes very similar to a variance analysis, in which

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Urubu Stream MU MU Scale 1/10.000 300m CA CSS2 MB MB CSS1 N Barreiro Stream Campus UEG 16°23′47″ 42°56′55″ 16°22′36″ _{42°56′05″}

Figure 1. Location of the UEG campus indicating the study sites. CSS1 and CSS2: cerrado sensu stricto patches; MB: mesophyllous semideciduous and gallery forest of Barreiro Stream; MU: semideciduous forest and gallery forest of Urubu Stream; CA: grassland with sparse trees.

the dissimilarities are compared inside and among groups. The statistic of the MRPP is A, which equals: (i) 1, the maximum value, when all of the items in the groups are identical; (ii) 0 when the heterogeneity inside the groups is equal to that expected by chance; and (iii) less than 0 when there is a higher heterogene-ity inside the groups than would be expected by chance (McCune & Grace 2002).

CS is an analysis that measures the classification force by calculating the difference in the average similarity inside the groups (W) and the average sim-ilarity among groups (B). Thus, high CS values indi-cate a strong classification, with a high similarity inside groups (W) and a low similarity among the groups (Van Sickle & Hughes 2000; Heino & Mykra 2006).

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Table 1. Description of vegetation type and sample design for the environments studied.

Surveys

Code Environment Vegetation characteristics Sample points n Hours

CSS1 Cerrado sensu stricto (5.6 ha)

Sparse trees with low density of herb and shrub layers and high density of Brachiaria decumbens (Poaceae), an invasive species introduced in 1960.

2 96 32

CSS2 Cerrado sensu stricto (22 ha)

Medium size trees, isolated or in dense stands, shrub and herb layers less dense than at CSS1, B. decumbens absent.

8 384 128

MB Mesophyllous semideciduous forest, gallery forest along Barreiro Stream

(14 ha)

Riparian vegetation with high trees (15–20 m) along Barreiro Stream and two springs. Semi-deciduous forest next to a gallery forest (mean height 8 m).

5 240 80

MU Semideciduous forest, gallery forest along Urubu Stream

(6.5 ha)

Riparian vegetation with high trees (15–20 m) along Urubu Stream. Semi-deciduous forest next to a gallery forest (mean height 8 m).

2 96 32

CA Grassland with trees (2.5 ha)

Anthropic pasture covered by emerald grass with high trees and few fruit trees (guava, mango).

1 48 16

The MRPP and the CS were calculated using the Bray–Curtis distance between the sampling units after the bird density was log-transformed. The significance of both metrics was calculated from 10,000 randomizations. The bird community struc-ture patterns were visualized by classifying the sam-pling units using non-metric multidimensional scaling (NMDS), an analysis which is also based on the Bray–Curtis distance template (Legendre & Legendre 1998).

Results

Composition of the bird fauna

During the qualitative survey, 128 bird species in 40 families and 14 orders were observed (Table 2). The family with the highest number of bird species was Tyrannidae (21 species), followed by Thraupidae (nine) and Trochilidae (seven).

During the quantitative survey, the most fre-quent species seen in the CA was Furnarius rufus (FO = 45.8%), followed by Tyrannus melancholicus (41.7%), Columbina talpacoti (37.5%) and Elaenia flavogaster (31.3%). Basileuterus hypoleucus (32.1%) and Turdus leucomelas (30.8%) were the most fre-quently observed species in MB. Conversely, at MU T. leucomelas was the most frequently observed species (54.2%) followed by B. hypoleucus (40.6%). In the cerrado environments, no species dominated to the same extent. In CSS2 the most frequently observed species were Colaptes campestris (22.1%) and Coragyps atratus (17.2%), whereas in CSS1, the most frequently observed species were Elaenia chiriquensis (28.1%) and Volatinia jacarina (25%).

Six species considered to be endemic to the cerrado region were observed in the area: Hylocryptus rec-tirostris, Antilophia galeata, Cyanocorax cristatellus, Neothraupis fasciata, Cypsnagra hirundinacea, and Charitospiza eucosma. The two first species occurred in MB and MU and the remaining species were found in CSS2.

In the entire study area, 12 species occurred in only one sample (e.g. Zenaida auriculata, Chloroceryle ama-zona, Myiarchus tyrannulus). On the other hand, a few species occurred in more than 20% of the samples and these species were not repeated among environments. As many as 23 bird species occurred in only one of the environments sampled (Table 1). Nesting evidence was found for nine species (Table 3), including Falco femoralis in CSS2.

Spatial and temporal patterns in the bird community

Altogether, 109 species were counted, 34 of which only occurred in the CSS1. The highest richness occurred in the MB. However, the observed richness of the studied environment was lower than that estimated for each of the environments individually (Table 2). Only six species were recorded in all physiognomies: Columbina talpacoti, Rupornis magnirostris, T. melan-cholicus, Pitangus sulphuratus, Megarhynchus pitangua and C. campestris. The CSS2 environment showed the highest exclusive richness (n= 13), followed by the MB environment (n= 12).

The sorting results and the classification strength suggested that the sampling units inside the same kind of environment showed a similar species composition (B = 0.255; W = 0.655; CS = 0.400; p < 0.001),

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Table 2. Frequencies of bird species occurrence observed in different cerrado environments, Brazil. CSS1 and CSS2: Cerrado sensu stricto; MB: mesophyllous semideciduous and gallery forest of Barreiro Stream; MU: semideciduous forest and gallery forest of Urubu Stream; CA: grassland with sparse trees (‘?’: uncertainty on species identification but not in genera).

Frequency of occurrence (FO)

Species CA CSS1 CSS2 MB MU n Tinamidae Crypturellus undulatus2 _6.7 ₁₆ Rhynchotus rufescens 2.1 1.8 9 Nothura maculosa2 _0.3 ₁ Ardeidae Butorides striata1 Bubulcus ibis2 _0.3 ₁ Syrigma sibilatrix 2.1 1.0 0.3 3 Threskiornithidae Mesembrinibis cayennensis 4.2 2.1 7 Theristicus caudatus 4.2 3.1 16 Cathartidae Coragyps atratus 6.3 18.8 17.2 0.8 89 Accipitridae Elanus leucurus 4.2 2.1 12 Rupornis magnirostris 10.4 2.1 2.6 2.5 1.0 24 Geranoaetus albicaudatus2 _0.5 ₂ Falconidae Caracara plancus 2.1 3.1 6.3 1.0 29 Milvago chimachima 3.1 1.8 10 Herpetotheres cachinnans2 _0.3 ₁ Falco sparverius 2.1 4.4 19 Falco femoralis 1.0 4.2 17 Rallidae Aramides cajanea1 Cariamidae Cariama cristata2 _3.4 ₁₃ Charadriidae Vanellus chilensis 20.8 3.1 10.4 53 Columbidae Columbina talpacoti 37.5 3.1 1.8 2.1 2.1 35 Columbina squammata 10.4 2.1 0.3 0.8 10 Patagioenas picazuro 10.4 25.0 16.9 0.8 96 Zenaida auriculata2 _0.3 ₁ Leptotila verreauxi 2.1 2.1 1.0 7 Psittacidae Diopsittaca nobilis 2.1 1.0 1.3 7 Aratinga leucophthalma 6.3 8.3 1.8 0.4 19 Aratinga aurea1 Forpus xanthopterygius2 _2.1 ₁ Brotogeris chiriri 2.1 2.1 2.6 13 Cuculidae Piaya cayana 0.5 3.8 5.2 16 Coccyzus sp.2 _0.4 ₁ Crotophaga ani 2.1 13.5 0.3 0.4 16 Guira guira 4.2 12.5 12.0 60 Tapera naevia 2.1 1.3 4 Strigidae Athene cunicularia2 _8.1 ₃₁ Rhinoptynx clamator1 Caprimulgidae Antrostomus rufus1 Trochilidae Phaethornis pretrei (?)2 _0.8 ₂ Eupetomena macroura 1.0 1.3 6 Colibri serrirostris 2.1 0.3 3 Anthracothorax nigricollis1 (Continued)

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Table 2. (Continued).

Species CA CSS1 CSS2 MB MU n Leucochloris albicollis 0.3 0.4 2 Amazilia fimbriata 2.1 1.0 6 Amazilia lactea (?) 0.5 0.4 3 Alcedinidae 4.17 Chloroceryle amazona2 _2.1 ₁ Momotidae Momotus momota 5.0 5.2 17 Galbulidae Galbula ruficauda 14.6 12.5 13.5 50 Bucconidae Monasa nigrifrons 8.3 7.5 3.1 25 Ramphastidae Ramphastos toco 0.8 0.4 4 Picidae Picumnus albosquamatus 2.1 0.3 0.4 2.1 5 Melanerpes candidus2 _1.8 ₇ Veniliornis passerinus (?) 4.2 1.7 1.0 7 Colaptes melanochloros 6.3 0.3 2.5 1.0 11 Colaptes campestris 6.3 10.4 22.1 0.4 1.0 100 Dryocopus lineatus 0.3 0.8 3 Thamnophilidae Herpsilochmus sp.2 (atricapillus/longirostris) 1.0 1 Thamnophilus doliatus 2.1 5.4 2.1 16 Thamnophilus caerulescens (?) 1.7 4 Taraba major2 _0.8 ₂ Dendrocolaptidae Lepidocolaptes angustirostris2 _0.8 ₂ Furnariidae Furnarius rufus2 _45.8 ₂₂ Lochmias nematura 6.7 4.2 20 Hylocryptus rectirostris 1.3 1.0 4 Synallaxis frontalis 2.1 0.3 1.3 14.6 19 Synallaxis scutata 3.8 1.0 10 Pipridae Antilophia galeata 20.8 11.5 61 Rhynchocyclidae Mionectes rufiventris (?)1 Leptopogon amaurocephalus (?) 5.4 2.1 15 Todirostrum cinereum 2.1 0.4 2 Tyrannidae Elaenia flavogaster 31.3 0.5 2.1 22 Elaenia chiriquensis 28.1 7.6 0.8 58 Serpophaga subcristata (?)1 Legatus leucophaius 27.1 0.5 0.8 1.0 18 Myiarchus tyrannulus2 _1.0 ₁ Casiornis rufus (?)1 Pitangus sulphuratus 27.1 7.3 0.8 17.1 15.6 79 Machetornis rixosa Myiodynastes maculatus2 _1.3 ₃ Megarynchus pitangua 8.3 1.0 0.3 3.8 10.4 25 Myiozetetes similis 10.4 0.3 3.8 2.1 17 Tyrannus melancholicus 41.7 20.8 6.8 13.3 11.5 109 Tyrannus savanna 2.1 14.6 5.2 35 Griseotyrannus aurantioatrocristatus 6.3 3 Colonia colonus 8.3 2.5 10 Xolmis cinereus 1.0 4.4 18 (Continued)

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Table 2. (Continued).

Species CA CSS1 CSS2 MB MU n Xolmis velatus1 Vireonidae Cyclarhis gujanensis 10.4 0.5 15.8 9.4 54 Hylophilus pectoralis (?)1 Corvidae Cyanocorax cristatellus2 6.8 26 Hirundinidae Alopochelidon fucata1 Stelgidopteryx ruficollis1 Progne chalybea1 Troglodytidae Pheugopedius genibarbis 23.3 8.3 64 Cantorchilus leucotis 20.4 5.2 54 Polioptilidae Polioptila dumicola 16.7 5.4 2.1 23 Turdidae Turdus rufiventris 1.7 2.1 6 Turdus leucomelas 22.9 0.3 30.8 54.2 138 Turdus amaurochalinus 4.2 1.3 5 Turdus albicollis 1.0 1 Mimidae Mimus saturninus2 _0.8 ₃ Coerebidae Coereba flaveola 10.4 7.1 3.1 25 Thraupidae Saltator maximus 2.5 3.1 9 Saltator similis 8.8 4.2 25 Cypsnagra hirundinacea2 _1.3 ₅ Lanio cucullatus 4.2 0.5 0.4 2.1 7 Lanio penicillatus 3.1 3 Tangara sayaca 8.3 0.3 2.1 3.1 13 Tangara cayana 6.3 2.5 3.1 12 Neothraupis fasciata 1.6 6 Tersina viridis 10.4 3.3 1.0 14 Dacnis cayana 0.8 2 Hemithraupis guira 2.1 1.3 3.1 7 Conirostrum speciosum Emberizidae Ammodramus humeralis 3.1 10.4 43 Volatinia jacarina 25.0 0.5 26 Sporophila nigricollis 10.4 4.2 9 Arremon taciturnus Charitospiza eucosma2 _1.0 ₄ Parulidae Basileuterus hypoleucus 32.1 40.6 116 Basileuterus flaveolus 12.1 2.1 31 Icteridae Icterus pyrrhopterus1 Gnorimopsar chopi 4.2 2 Molothrus bonariensis 4.2 0.3 3 Fringillidae Euphonia chlorotica 0.4 1 Euphonia violacea 10.4 0.8 7

Richness per habitat 51 34 60 65 43

Estimated richness (Jackknife 2)

73.4 42.9 89.9 75.9 57.9

1_{Species were recorded during qualitative surveys only.}

2_{Species were recorded in single environment from the five ones sampled.}

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Table 3. Birds species nesting in the cerrado fragments between October 2003 and March 2005. CSS1 and CSS2: Cerrado sensu stricto; MB: mesophyllous semideciduous and gallery forest of Barreiro Stream; CA: grassland with sparse trees.

Species Observation Fragment

Rhynchotus rufescens Nest with eggs CSS1 Volatinia jacarina Nest with eggs CSS1 Columbina talpacoti Nest with eggs and

nestlings

CSS2

Falco femoralis Nest with nestlings under parental care

CSS2

Molothrus bonariensis Nestling under nidoparasitism

CSS2

Patagioenas picazuro Display and copulation

MB

Furnarius rufus Nest CA

Colonia colonus Nest with nestlings under parental care

CA

Tyrannus melancholicus Nest and nestlings CA

and the bird community structure was not different between time periods (Figure 2; CS = –0.007 and p = 0.513) given that sample units of distinct ronments were not grouped, revealing that these envi-ronments were different in bird species composition. Additionally bird species composition was not simi-lar by time period evaluated, given that sample units for the same time period were not grouped together (Figure 2). This result was confirmed by the MRPP for the different kinds of environment (A = 0.49, p< 0.001) and for the observation periods (A = – 0.08, p= 0.999).

When the five sampling units were grouped into the following three environments: (a) grassland, (b) cerrado sensu stricto environment and (c) forests (mesophyllous and gallery) they still differed in their bird communities, but the grouping factor evaluated by the A statistic of MRPP (A= 0.36, p < 0.001) and by CS (B= 0.203; W = 0.556; CS = 0.352; p < 0.001)

Stress = 5.26

CSS1

CSS2

CA

MU

MB

PC 1

PC 2

Figure 2. Sampling units sorted according to the NMDS. Symbols of same color indicate the same period of the day, as follows: white: 06:00–09:00 h; light grey: 09:00–12:00 h; dark grey: 12:00–15:00 h; and black: 15:00–18:15 h. CSS1 and CSS2: cerrado sensu stricto patches; MB: mesophyllous semideciduous and gallery forest of Barreiro Stream; MU: semideciduous forest and gallery forest of Urubu Stream; CA: grassland with sparse trees.

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was slightly lower than that produced when the five groups were considered. Grouped environments did not show differences in bird community structure through time periods (CS= –0.005 and p = 0.421).

Discussion

Bird composition and distribution

The frequency of occurrence of bird species was gen-erally low in each environment, probably due to the fact that the mosaic of different cerrado habitat types is indeed under intensive human use and occupation. Even though some species use the area for repro-duction, the low occurrence of bird species reveal a prevailing pattern of use for other activities, such as feeding and/or resting instead of living in the area. Therefore, the area is used as a refuge by many species that are locally displaced by human activities and may work as a source–sink system for surrounding fragments with the same habitat types given that it provides nesting habitats and food for some species. This seems to be true especially for the smaller envi-ronment of the cerrado (CSS1), which is contiguous to the environment of the mesophyllous semideciduous forest and the gallery forest of the Barreiro Stream (MB). Even though species composition in CSS1 was distinctive and constant through time, it presented the lowest richness. This is due to the proximity with university campus buildings and associated negative impacts from the university’s ongoing construction. Most likely CSS1 has been used by some generalist bird species from MB as feeding habitat on a daily basis. CSS1 has many fruiting cerrado trees (Marques-Alves & Carvalho 2008), is close to areas of human activity, which supply an additional source of food and artificial materials for nesting (Borges & Marini 2010) and is contiguous to MB, which had the higher richness and frequency of tyrannid species occur-rence. In fact, a number of tyrannid (tyrant flycatcher) species can be generalists, partially migratory (Sick 1997), nomadic or even residents of cerrado areas throughout the year (Marini et al. 2009), support-ing the probability of their migration between these environments.

The trends of distinct bird species distribution and composition across the study environments dur-ing different times revealed the unique spatio-temporal patterns of the bird community living at each envi-ronment. This is true even when comparing cerrado CSS1 to cerrado CSS2 or between both gallery forests (MU and MB). Further, many species were restricted to a single environment, implying that the preservation of all phytophysiognomies is essential for maintaining cerrado bird species richness.

Suitability for the establishment of a conservation area

The main driver for the research was the threatened status of cerrado, its potential for biodiversity con-servation and the risk of university expansion on the studied environments. These areas host several restricted-range and endemic species of special con-cern for conservation (see Costa et al. 2010). It is not clear where nest habitats for the endemic birds are, but the conservation unit under consideration at the study site will be essential for the preservation of these endemic species by providing them with a shelter habitat.

Even though the other species observed were not endemic, a number of local species are threatened by diverse pressures and this supports the idea for the establishment of a conservation unit at the study site. One of them, Falco femoralis, sometimes abandons its nest before the chicks hatch if disturbed by humans (Sick 1997; Granzinolli et al. 2002) and, therefore, needs protected environments to carry out its brood care and to complete its reproductive cycle. Currently, F. femoralis is quoted in the Red List of Threatened Species for Brazil as “least concern” (IUCN 2011). In addition, Elaenia chiriquensis, a key species for seed dispersal in the cerrado (Medeiros & Marini 2007), was more frequently recorded in CSS1, the smaller and more disturbed environment of cerrado. The protec-tion of CSS1 would help to preserve this important seed disperser and thus contribute to the restoration of natural vegetation in the surrounding cerrado areas.

Given that at regional and local scales, spatial patterns tend to be driven by a more complex inter-action of past and current ecological and evolution-ary processes (Blamires et al. 2008), local intrinsic associations, which determine nest success, settle-ment and conservation status for many species are likely to remain undescribed in areas unprotected and under intense pressure. Such ecological associa-tions have already been described for Elaenia cristata exclusively using the climax tree species Davilla elliptica (Dilleniaceae) as a nesting habitat (Marini et al. 2009). Therefore, nesting success for E. cristata depends on a cerrado tree which can be found in approximately 2% of the study site (Marques-Alves & Carvalho 2008), highlighting the importance of its conservation for this species.

Additionally, half of the endemic species observed in the study site are from the Emberizidae or Thraupidae, and one third of the species nesting in the area are in the Emberizidae or Columbidae fam-ilies, whose species are likely to have lower daily nest survival rates than species from Tyrannidae (Borges & Marini 2010), which is the most frequently observed family in the site.

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Given the species richness, endemism, and human threats in the cerrado, it is important not to neglect available species occurrence information (Costa et al. 2010). The conservation value of small patches should not be underestimated, because fragmented landscapes might arise as promising sites to invest resource management and conservation funds (Armstrong et al. 2008). Indeed, the data pre-sented show that, even at a small spatial scale, high richness and endemism are likely to be found in the cerrado. Overall, these data highlight the potential benefit in conservation of small patches of cerrado habitat and the ecological value of creating conser-vation units in both large and small cerrado areas. Our results support the decision to convert the study site into the first university cerrado conservation unit, since it will protect a broad range of species and will guarantee habitats for some endemic birds. However, to increase its effectiveness for preserving the bird fauna, further management strategies should be imple-mented such as decreasing the anthropogenic modifi-cations and reducing garbage disposal, livestock graz-ing and controllgraz-ing human use for leisure, which is currently unregulated in the area.

Acknowledgments

To the colleagues at the Laboratório de Biodiversidade do Cerrado for their support in the field. To Nilton C. do Valle, Daniel Blamires, Carlos E. Sant’Ana and José Hidasi for the ornithological arguments. Laranjeiras T.O. and Moura N.G. had a scholarship during the work (PBIC-UEG). We are grateful to B. Quartarolo and Alex Lees for English review and to an anonymous referee for valuable recommendations.

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