Birds of rural landscape in the Midwest region of the state of Minas Gerais , Brazil Aves de paisagem rural na região Centro-oeste do estado de Minas Gerais , Brasil

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0), which permits reproduction, adaptation, and distribution provided the original author and source are credited. 1 Universidade do Estado de Mato Grosso, campus Cáceres. Centro de Pesquisa em Limnologia, Biodiversidade e Etnobiologia do Pantanal. Av. Santos Dumont, Bloco II, Cidade Universitária, 78200-000, Cáceres, MT, Brazil. 2 Faculdade de Filosofia Ciências e Letras do Alto São Francisco, campus Luz. Av. Guarin Caetano, 188, 35595000, Luz, MG, Brazil. 3 Centro Universitário Una, campus Betim. Av. Governador Valadares, 640, Centro, 32510-010, Betim, MG, Brazil. 4 BH Hawking Club. Rua Siderose, 1041, Alto dos Caiçaras, 30775-120, Belo Horizonte, MG, Brazil. Abstract


Introduction
Brazil is one of the countries with the greatest richness of birds in the world.Currently a total of 1919 species is known for its territory (Piacentini et al., 2015).The group is considered excellent bioindicator (Stotz et al., 1996), besides promoting environmental services such as pollination, seed dispersal and population control of several species (Sick, 1997).
A large number of the Brazilian birds are found in the Cerrado.This Biome contains 837 bird species, of which 29 are endemic (Silva, 1995), being the second Biome with the highest number of threatened birds in Brazil (Marini and Garcia, 2005).This high number of endemic and threatened species, together with the strong threat that the Cerrado suffers, make it a world biodiversity Hotspot (Myers et al., 2000).
Fragmentation and habitat loss are among the main causes of high rates of decline in biodiversity (Fahrig, 1997).Advances in the occupation of natural environments by human activities affect habitats of various species and exert great pressure on biodiversity.These impacts may lead to reduction and even extinction of local populations dependent on these habitats if no compensatory measures are adopted (Turner, 1996), including best practices in the agricultural production system (Machado et al., 2008).
Land tenure in tropical regions is a critical factor that determines both land use change and conservation strategies.Priority attention is given to the areas that are in the Hotspot Cerrado, a biome that is not designated as a National Heritage and the lands are predominantly private.Fact that implies in many areas that are not legally protected (Lahsen et al., 2016).This reduction in vegetation cover has negative consequences for avifauna.Among the most affected are those with a certain degree of endemism, habitat specificity and sensitive species (Mendonça et al., 2009).Because of these changes, there is a decrease in the number of more specialized species, mostly retaining only generalists (Saunders et al., 1991;D'Angelo Neto et al., 1998).
Environmental legislation appears as a conservation measure to protect native areas and their biodiversity.Like the Brazilian Forest Code (Law 12.651/2012) used in rural landscapes.This law establishes standards for the protection of native areas, including for example Permanent Protection Areas (PPA) that protect marginal environments to watercourses and Legal Reserve Areas (LRA) geared towards maintenance of vegetation with sustainable use, not covered by the PPA (Brasil, 2012).
Ornithological inventories constitute the first step to work on conservation actions aimed at the maintenance of bird diversity (Sutherland, 2000;Vasconcelos et al., 2002).Such inventories may supply information on the occurrence of rare, inconspicuous and migrant species, besides provide subsidies for the knowledge of distribution pat-terns and seasonality (Vitorino et al., 2016).Although, due to the vast territorial extension of the Brazilian country, great diversity of habitats of the Neotropical region, and the small number of researchers working in the area, the distribution of birds in Brazil is still poorly known (Lopes and Marçal, 2016).The aim of the paper was to characterize the rural landscape birds, evidencing dependent species from a protection area in private properties in the Cerrado Biome in the Midwest of the state of Minas Gerais.

Study area
The study area is in Midwest region of the state of Minas Gerais, Luz municipality, which has an area of about 1,171.659km 2 , where about 80,000 ha are destined to agricultural activities, according to the Instituto Brasileiro de Geografia e Estatística (IBGE, 2006).The main water courses in the municipality are São Francisco, Limoeiro, Bambuí, Jorge Grande, Jorge Pequeno and Córrego da Velha River.The region is located in the Cerrado Biome, a Neotropical Savanna hotspot (Figure 1).The climate is classified as Aw (tropical rainy) (Kottek et al., 2006).The research was developed in a rural area of about 200 continuous hectares, comprising two farms, which is situated 8.5 km far from the urban perimeter.This rural landscape is composed of patches of Cerrado sensu stricto and a Riparian Forest that composes the Permanent Protection Areas and Legal Reserve, here denominated as Protected Areas.These phytophysiognomies are inserted in a pasture matrix.

Data collection and analysis
The ornithological inventory was held from May 2011 to May 2012, through 15 incursions, between rainy and dry season.Systematic data were collected through two complementary methods: Direct observation census and mist-net captures.
The direct observation census consisted of walks made in preexisting tracks, carried out in different habitats from the sunrise to register the species (Rodrigues et al., 2005).In some occasions the route was performed at dusk in order to find species of nocturnal crepuscular habits.The sample effort for this method was 75 hours.All the visual and auditory contacts were considered for identification of the species.Visual contacts were aided in the field with use of a Bushnell® 10x50 binocular and a digital camera SX-30is Canon®.The auditory contacts were aided by a RR-US551Panasonic® digital recorder and a HT-81 Yoga® directional microphone.Recordings obtained in the field that were not immediately identified were evaluated a posteriori from sound banks: (www.xeno-canto.organd www.wikiaves.com.br) to identify the species.
To check inventory efficiency, we constructed a rarefaction curve of the species along the samples.The richness of the birds was estimated by Jackknife 1, using Estimates 9.0 software (Colwell et al., 2012).Occurrence Frequency (OF) of the species was stipulated through the total number of campaigns in which the species was recorded as a function of the total number of incursions (D' Angelo Neto et al., 1998).Species that presented OF between 75% and 100%, were considered as Highly Frequent (Hf), from 50% to 74% as Frequent (Fe), 25% to 49% as Less Frequent (Lf), and less than 25% as Infrequent (If).
Species recorded outside of the methods adopted were considered as random.These species were included in the analysis of the composition of the bird assemblages with a frequency lower than the observed frequency in relation to the systematic data, classified as Occasional (Oc).All registered species were grouped into trophic guilds: Insectivo-rous, Omnivorous, Frugivorous, Granivorous, Carnivorous, Piscivorous, Detritivorous and Nectarivorous according to Motta-Júnior (1990) andSick (1997).The threat level of the species follows evaluation of the World Conservation Union, Red list of Threatened Species -IUCN (BirdLife International 2016) and Brazil Red Book of Threatened Species of Fauna (Brasil, 2016).The classification of a species as endemics followed Silva (1995), Stotz et al. (1996), Sick (1997) and Piacentini et al. (2015).The nomenclature adopted follows the Comitê Brasileiro de Registros Ornitológicos (Piacentini et al., 2015).

Results
The survey revealed a total of 143 bird species, 134 were recorded by the Direct Observation Census, 10 captured in mist-nets and eight recorded exclusively in a random manner (Table 1).The registered species are distributed in 46 families and 20 orders.The most representative family of the survey was Tyrannidae, with 18 species.The rarefaction curve showed a tendency for stability.The richness estimated for the area was 155 species (SD = 5.61), indicating a sample efficiency of 91.61% (Figure 2).

Discussion
The data presented here, compiled to the study carried out in the Environmental Protection Area of the Córrego da Velha Basin (Gonçalvez and Andrade, 2015), records a total of 177 bird species for the Luz municipality.This number represents 28.83% of the recorded birds for the São Francisco Basin, in the portion comprising the state of Minas Gerais (Diniz et al., 2013), 22.87% of the richness found for the entire state (Mattos et al., 1993) and 21.15% of the birds found in the Cerrado Biome (Silva, 1995).
The large representativeness of the family Tyrannidae was expected, since this is the richest family of birds of the Neotropical region (Sick, 1997).Some authors have already hypothesized that species of this family are more tolerant to anthropically altered environments (Motta-Júnior, 1990;Krugel and Anjos, 2000).According to Ponço et al. (2013), this fact may be related to the generalist feeding  Birds rural landscape in the Midwest region of the state of Minas Gerais, Brazil habit of most of the species of this family, which adapt to a wide variety of food, as well as to use the most different spaces for nesting.
The evaluation of frequency in which the species were recorded during the study, indicated that about 65% of the avifauna in the rural landscape are classified as Less Frequent and Infrequent.This result may be related to presence of migratory species, such as Myiodynastes maculatus (Statius Muller, 1776), Pyrocephalus rubinus (Boddaert 1783) and Tyrannus melancholicus Vieillot (1819), which are recorded only at certain periods of the year.According to Anjos (1990), the low frequency of some species may also be associated with the presence of small fragments that do not support many birds, causing some species to use neighboring areas.A greater proportion of species Infrequent in relation to Frequent species may also be observed in several anthropically affected environments (Morante-Filho and Silveira, 2012;Mencato and Treco 2016;Vitorino et al., 2017).Some birds classified as Highly Frequent or Frequent may be considered typical elements of rural landscape, such as Vanellus chilensis (Molina 1782), Columbina talpacoti (Temminck 1810), Gnorimopsar chopi (Vieillot 1819) Furnarius rufus (Gmelin 1788).In addition, other species with low frequencies may also benefit in rural environments, for example: Bubulcus ibis (Linnaeus 1758), Guira guira (Gmelin 1788), and Progne tapera (Vieillot 1817) due to their adaptation to these environments.
A higher proportion of insectivorous followed by omnivorous, is reported for altered environments (Silva et al., 2014;Godoi et al., 2016;Ruiz-Esparza et al., 2016;Cosac and Silvano, 2016;Vitorino et al., 2017).In rural landscapes, groups composed mostly of generalist species benefit from open areas, such as pasture and border of small forest fragments that are kept as preservation areas.
Sick (1997) indicates insectivorous birds as abundant and commonly found in tropical regions.We observed a low number of insectivorous birds with specialized diet, such as species of the families Dendrocolaptidae and Picidae.According to Almeida (1982), insectivorous birds tend to decrease in more structured habitats, whereas the number of species with more specialized diet increases.
A trophic group of great relevance for anthropically affected areas is that of the frugivorous birds, which may be potential seed dispersals.This group is classified according to Lundberg and Moberg (2003) as mobile links, which are species that move actively in the landscape, and become a connecting element between fragments or small biotopes that are separated.Some species, such as Tangara sayaca (Linnaeus 1766), Tangara palmarum (Wied 1821) and Euphonia chlorotica (Linnaeus 1766), mentioned by Gonçalves and Vitorino (2014), act on seed dispersal process in anthropically affected environments, being of great importance for propagation of propagules in habitats with low number of specialized frugivores.
Among the endemic species of the Cerrado, A. galeata shows a distribution restricted to riparian areas (Sick, 1997).Due to their ecological importance, Riparian Forests are considered Permanent Protection Areas, with legal support in Brazil.However, according to Aquino et al. (2012), such areas are threatened in rural landscapes by the cutting and felling of trees, cattle trampling, intensive traffic of agricultural machinery, occupation of areas unfit for cultivation, indiscriminate use of pesticides, among others.
In relation to the endemism of the Atlantic Forest, both B. ruficapillus and H. ruficapilla were recorded in small forest remnants in the study area, which can be considered Atlantic Forest enclaves still present in the Luz municipality.These fragments are part of the Legal Reserve of the evaluated rural landscape, evidencing the importance of the legally protected areas for the maintenance of species dependent on natural areas.
Aratinga auricapillus is the only species classified by the IUCN as Near Threatened (NT).Willis (1979) evidences the sensitivity of frugivorous birds, including representatives of the family Psittacidae.According to the author, this group is quickly extinct in small fragments, because they need different species of trees that bear fruit in different seasons of the year.As observed by Gimenes and Anjos (2000) for other Psittacidae, A. auricapillus is certainly not restricted to the study area, but it explores it in different periods to obtaining certain resources.
Another species worth mentioning is Orthopsittaca manilatus (Boddaert 1783).This bird has a close relationship with areas of Veredas, which are areas with hydromorphic soils and prevalence of herbaceous vegetation, usually with the occurrence of Mauritia flexuosa L.f.Orthopsittaca manilatus feeds almost exclusively on the fruits of M. flexuosa, besides using this vegetation for nesting, rest and shelter (Roth, 1984).Veredas, as well as Riparian Forest, are also classified as permanent preservation ecosystems and ecological reserves.However, this environment in rural landscapes also suffers from anthropic pressures, such as pasture formation and latter cattle occupation, which cause soil compaction and suppresses herbaceous vegetation, triggering degradation processes (Bahia et al., 2009).Due to the absence of Veredas in the evaluated rural landscape, it is believed that O. manilatus only moves through it to make use of Veredas located nearby.
The present study raises important information about the composition of bird assemblages in rural landscape in the Hotspot Cerrado, with a community composed mostly by generalist species, but with some elements sensitive to anthropogenic processes.Private areas that are legally protected in altered environments become unique refuges for species dependent on natural areas.We highlight the importance of public policies that involve landowners for the preservation of these environments, in the domains of the Cerrado Biome.

Figure 1 .
Figure 1.Location of the study area in state of Minas Gerais, Brazil.Source: Adapted from IEDE-MG (2016) by Angélica Vilas Boas da Frota and Breno Dias Vitorino.

Figure 2 .
Figure 2. Species accumulation curve and estimated richness for the birds registered in a rural landscape, between May 2011 to May 2012, in the state of Minas Gerais, Brazil.

Figure 3 .
Figure 3. Frequency of occurrence of birds registered in a rural landscape, between May 2011 to May 2012, in the state of Minas Gerais, Brazil.

Table 1 .
Species of birds registered in a rural landscape, between May 2011 to May 2012, in the state of Minas Gerais, Brazil.At = Endemic of Atlantic Forest; Br = Endemic of Brazil; Ce = Endemic of Cerrado; Fe = Frequent; Hf = Highly Frequent; If = Infrequent; Lf = Less Frequent; Nt = Near Threatened; Oc = without standard.