Bird community of upper-montane rupestrian fields in South of Minas Gerais State, Southeastern Brazil

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The rupestrian fields are located at altitudes of 900 meters above sea level in Brazil. The mountains present rocks from the pre-Cambrian age, directly related to quartzite, sandstone and iron ore outcrops (Eiten, 1992; Alves & Kolbek, 1994; Giulietti, Pirani, & Harley, 1997; Caiafa & Silva, 2005; Alves, Cardin, & Kropf, 2007; Vasconcellos, 2011).

This vegetation type is distributed along the Espinhaço Range, but isolated areas of this kind of landscape are located in Central Brazil, for example: Chapada dos Veadeiros and Serra dos Pirineus in Goiás State. We also found this vegetation in the west of Minas Gerais State in Serra da Canastra and in the South in the cities of São João Del Rei (Serra do Lenheiro), Tiradentes (Serra de São José), Carrancas (Serra de Carrancas), Minduri (Chapada das Perdizes), Luminárias (Serra Grande), São Tomé das Letras (Serra do Cruzeiro do Canta Galo), Itumirim (Serra de Itumirim), Ingaí (Serra do Boqueirão) and Itutinga. The last nine cities are in Serra da Mantiqueira, with similar geology and floristic compositions to the Espinhaço Range (Eiten, 1992; Alves & Kolbek, 1994; 2009; 2010; Gavilanes, Brandão, Laca-Buendia, & Araujo, 1995; Harley, 1995; Giulietti et al., 1997; Alves et al., 2007; Rapini, Ribeiro, Lambert, & Pirani, 2008; Vasconcellos, 2011).

The bird community in the south of Minas Gerais State in Southeastern Brazil has been well studied (D’Angelo Neto, Venturin, Oliveira Filho, & Costa, 1998; Ribon, 2000; Vasconcelos et al., 2002; Lopes, 2006; Vasconcelos, D’Angelo-Neto, & Nemesio, 2005; Lombardi, Vasconcelos, & D’Angelo Neto, 2007; Vasconcelos, 2008; Corrêa & Moura, 2009; Braga, Zanzini, Cerboncini, Miguel, & Moura, 2010; Moura & Soares-Junior, 2010; Corrêa & Moura, 2010; Moura, Corrêa, & Santos, 2010; Moura & Corrêa, 2011; Santos, Lombardi, D’Ângelo-Neto, Miguel, & Faeti, 2011; Mazzoni & Perillo, 2011; Moura & Corrêa, 2012; Santos, 2012; Corrêa, Louzada, & Moura 2012; Lombardi et al., 2012; Rezende et al., 2013; Moura, 2014;Moura, Camargo, & Correa, 2014; Santos, Miguel, & Lombardi, 2014; Moura, Correa, & Machado, 2015; Moura, Mariano, Machado, Cerboncini, & Fontes, 2017). Papers focusing on bird communities in rupestrian fields are incomplete, despite these communities being threatened with a high risk of extinction (Machado, Fonseca, Machado, Aguiar, & Lins, 1998; Lopes et al., 2009). In this article we present a bird list in rupestrian fields of seven cities in the south of Minas Gerais State, Southeastern Brazil, and analyze the birds’ distribution, the endangered species (and its conservation status), and generate bases for future conservation actions.

The observations were conducted in rupestrian field areas (Figure 1) (Table 1), located in seven cities in the south of Minas Gerais State: Ingaí, Luminárias, São Thomé das Letras, Carrancas, Minduri, Itumirim and Tiradentes (Figure 2), during 2012 and 2018, in seasonal observations (winter and summer) to obtain occurrence data, with 10 hours (from 6 AM to 4 PM) of sampling effort of in each sampling collection point (similar to Braga et al., 2010). We used Nikon 08x40 and 10x50 binoculars, and Sony H 50, Canon EOS REBEL T1i and Canon Power Shot SX50 HS cameras to help record/sight the birds. The nomenclature follows Piacentini et al. (2015). The climate in the cities and in the studied area is Cwa according to the Köppen classification, with annual average precipitation of 1,529.7 mm concentrated in September to March, and annual average temperature of 19.4ºC (Alvares, Stape, Sentelhas, Gonçalves, & Sparovek, 2013). However, the climate in the Chapada das Perdizes between the cities of Carrancas and Minduri is Cwb, common for mountain tops (Alvares et al., 2013).

Figure 1.
A = Serra das Broas, Chapada das Perdizes region, between Carrancas and Minduri cities, B = rupestrian fields in the Chapada das Perdizes region, between Carrancas and Minduri cities, C = rupestrian fields in Cruzeiro do Canta Galo, São Thomé das Letras cities, D = Serra de Carrancas, Carrancas city (Source: Moura, A. S., personal archive).

Table 1.
Georeferenced points of the observation areas.

Figure 2.
Study area in grey. Observed cities are Ingaí, Luminárias, São Thomé das Letras, Carrancas, Mindurí, Itumirim and Tiradentes, South of Minas Gerais State, Southeastern Brazil.

We made cumulative species curves with Jackknife of first order estimator to analyze the richness, abundance and sampling sufficiency. These curves were obtained with 1000 randomizations using the EstimateS program version 9.10 (Colwell et al., 2012). The similarity and the groups between the sampling collection points were performed by the Jaccard index (Valentin, 2000), using the UPGMA method to create groups of vegetation types according to species composition. These groups were made in the Primer 6 + Permanova program (Clarke & Gorey, 2006; Anderson, Gorley, & Clarke, 2008).

We recorded 107 bird species (Table 2) of 29 families in a total of 280 hours of sampling effort. The more representative families in the rupestrian fields were: Thraupidae (N=26), Tyrannidae (N=15) and Trochilidae (N=11). Thraupidae was the more representative family because it presents a great species number in Brazil (n= 157) (Piacentini et al., 2015). Moreover, the floristic compositions of these areas were composed of grass and herbaceous species which commonly produce fruits, and are used by the frugivorous birds as food (Sick, 1997), for example plants of the Miconia genus (Gavilanes et al., 1995; Baumgratz & Chiavegatto, 2006; Nunes, Landau, & Veloso, 2008).

The Tyrannidae and Trochilidae families were expected to be abundant, because previous studies conducted in the south of Minas Gerais State found similar results (Lombardi et al., 2007; Moura et al., 2015). The representativity of the Trochilidae family (nectarivorous birds popularly called hummingbirds) can also be highlighted due to the abundance of food in the rupestrian fields, as they have a variety of rupiculous flowers of the Bromeliaceae, Orchidaceae and Cactaceae families (Gavilanes et al., 1995; Oliveira-Filho & Fluminhan-Filho, 1999).

From the records of this study, 6.54% are threatened species (n=7): Amazona vinacea (Kuhl, 1820), Geositta poeciloptera (Wied, 1830), Alectrurus tricolor (Vieillot, 1816), Anthus nattereri Sclater, 1878, Coryphaspiza melanotis (Temminck, 1822), (International Union for Conservation of Nature and Natural Resources [IUCN], 2019), Brasil, 2014), Culicivora caudacuta (Vieillot, 1818), and Polystictus superciliaris (Wied, 1831) (IUCN, 2019). With the exception of the Vinaceous-breasted amazon (A. vinacea), the other recorded threatened species are birds which are closely related to fields, and these species are among the most threatened birds of the Cerrado domain (Machado et al., 1998; Lopes et al., 2009).

As a result, we emphasize the importance of preserving this vegetation type for bird communities. In addition, Oliveira-Filho & Fluminhan-Filho (1999) mention the importance of preserving rupestrian fields due to its specific flora, the high species richness with restricted ecological and geographic distribution, and the presence of floristic endemic elements in the mountains, which together evidence that this type of vegetation and its bird communities deserve high conservation priority.

Table 2
Birds species recorded in the study. Ing= Ingaí, Lum= Luminárias, Stl= São Thomé das Letras, Car= Carrancas, Min= Minduri, Itu= Itumirim and Tir= Tiradentes.

The species accumulation curve did not reach the asymptote, and the Jackknife of first order estimator curve presented a small slope at the curve end (Figure 3). The estimator presented a richness of 96.87% of the total diversity, with 109.43 species. This high value demonstrates that the sampling effort was satisfied. The number of records, the representativity and the threatened species show that the rupestrian fields are of extreme importance in order to preserve and conserve the bird fauna which are more specific to these fields.

Figure 3
Cumulative species curve, confidence interval and Jackknife of first order estimator of the studied areas.

The cluster demonstrated a similarity between the bird community of rupestrian fields from the counties of Tiradentes and Luminárias; Minduri and Carrancas, Itumirim and Ingaí. The community from São Thomé das Letras city is the most different when compared among the other communities (Figure 3). The similarity is related to geographical proximity, considering that the sampling areas are continuous from a mountain range, and also the similarities are explained to their disturbance degree. In contrast, although the sampled vegetation type from São Thomé das Letras city is in good condition (Figure 1C), the landscape contains the presence of mining companies and has a great number of mining tailings (see Chiodi Filho, Artur, & Rodrigues, 2005), and therefore natural vegetation is absent in several areas, in turn presenting a human effect on the bird fauna (Figure 5).

Figure 4
Bird community cluster between sampling areas. Cities: Stl= São Thomé das Letras, Ing= Ingaí, Itu= Itumirim, Car= Carrancas, Min= Minduri, Lum= Luminárias and Tir= Tiradentes.

Despite the rupestrian fields being considered components of the Cerrado domain (Oliveira-Filho & Fluminhan-Filho, 1999), we recorded five species commonly found in the Atlantic Forest (Silva, 1995; Silva & Santos, 2005): Thalurania glaucopis (Gmelin, 1788), Primolius maracana (Vieillot, 1816), Knipolegus nigerrimus (Vieillot, 1818), Tachyphonus coronatus (Vieillot, 1822) and Sporophila ardesiaca (Dubois, 1894). The sampling areas (Figure 2) presented high influence of Atlantic Forest due to its location near to an ecotonal region between both domains, which may have altered the bird community.

Figure 5.
Photo of rupestrian fields from São Thomé das Letras city, highlighting the mining area and mining tailings, and the absence of natural vegetation
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Despite expressive richness recorded for the bird communities of the rupestrian fields in the south of Minas Gerais State, the species list presented herein needs to be completed because this fauna group is dynamic. We also need to consider that Rodrigues et al. (2011) recorded 151 bird species in the rupestrian fields in Serra do Cipó National Park, in central Minas Gerais State, thus suggesting that our sampling area can present higher richness because they are identical vegetation types and present a larger area than that presented by Rodrigues et al. (2011).

Part of the sampled areas is considered a priority for biological conservation (Chapada das Perdizes, bordering the cities of Carrancas/Minduri) (Drummond, Martins, Machado, Sebaio, & Antonini, 2005), not only presenting rare, endangered and endemic species of birds, but also other species (Oliveira-Filho et al., 2004) which are present in these rupestrian fields such as mammals (Machado, Gregorin, & Mouallem, 2013; Pecora et al., 2016; Machado et al., 2017), and plants (Oliveira-Filho et al., 2004). Lawton (1996) mentions that the knowledge about vertebrate composition in different areas and comparisons between them are important for conservationist projects. Therefore, the characteristics of the area, the large dimensions, its location, and the vegetation type make the area relevant for creating a conservation unit (wildlife protected area – Brasil, 2000) in the region. In addition, this (or these) conservation unit(s) will create an ecological corridor of rupestrian fields in association with other areas, such as the Serra de São José Environmental Protection Area (APA Serra de São José).

Our study found a high richness in relation to other open areas, with the Tyrannidae and Trochilidae families being the most representative. We highlight the endangered species in the Cerrado domain which of these species are closely linked to rupestrian fields. The composition is similar to closer areas, with exception to São Thomé das Letras city because it suffers an influence of mining areas. We suggest creating a wildlife protected area to preserve and conserve a great area of rupestrian fields and consequently the associated biota, especially the bird communities.