Long-term avifaunaL survey in an urban ecosystem from southeastern braziL , with comments on range extensions , new and disappearing species

Urban avifaunal surveys in Brazil have been increasing in recent years, despite none of them consisting of long-term studies indicating events of regional colonization and/or missing species. Here, we present an avifaunal survey of an urbanized ecosystem in southeastern Brazil, carried out along 30 years, on the campus of the Pontifícia Universidade Católica de Minas Gerais, municipality of Belo Horizonte, Minas Gerais state. Inside the campus there is a forest reserve adjacent to a small lake. The inventory was mainly based on opportunistic records from the years 1982-2013. We recorded 134 bird species along the past 30 years. However, the present avifauna is composed of 123 species. A total of 97 species was recorded in the reserve, including the forest fragment and the adjacent lake, of which 44 were exclusive to this area. Nevertheless, the majority of the current species found in the study area is forest independent (N = 51) or semi-dependent (N = 46). There is a predominance of insectivorous (N = 43) and omnivorous (N = 29) species. The current avifauna is represented by 15 migratory species, which can be found both in the urbanized area and in the forest remnant. However, the majority of the species (N = 75) is resident in the area, including three invasive species, whereas few others 1. Museu de Ciências Naturais, Pontifícia Universidade Católica de Minas Gerais. Avenida Dom José Gaspar, 290, Bairro Coração Eucarístico, Campus PUC Minas, CEP 30535‐901, Belo Horizonte, MG, Brasil. 2. Pós‐Graduação em Zoologia de Vertebrados, Pontifícia Universidade Católica de Minas Gerais. Avenida Dom José Gaspar, 500, Bairro Coração Eucarístico, Campus PUC Minas, CEP 30535‐610, Belo Horizonte, MG, Brasil. 3. Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais. Caixa Postal 486, CEP 30161‐970, Belo Horizonte, MG, Brasil. 4. Pós‐Graduação em Biologia Animal, Museu de Zoologia João Moojen, Universidade Federal de Viçosa. Vila Gianetti, 32, CEP 36570‐000, Viçosa, MG, Brasil. 5. E‐mail corresponding author: mfvasconcelos@gmail.com Volume 53(25):327‐344, 2013 (N = 28) are occasional visitors. The remaining species were probably introduced in the area. There were 11 cases of disappearing species, which include typical forest birds, and also species typical of wetlands and rural environments. We also comment on recent colonization and on the possible effects of isolation on birds. Probably, the majority of forest-dependents are on the brink of extinction in the forest fragment. Thus, the species’ list provided here can be useful as a database for monitoring long-term effects of urbanization on this bird community. Key‐Words: Avifauna; Colonization; Disappearing species; Urban environment. Valadão et al., 2006a, b; Torga et al., 2007; Vascon‐ celos, 2007; Vasconcelos et  al., 2007; Paetzold & Querol, 2008; Pinheiro et al., 2008; Pereira & Silva, 2009; Fontana et al., 2011; Rosa & Blamires, 2011; Dario, 2012; Franco & Prado, 2012; Mafia et  al., 2012; Reis et  al., 2012; Scherer‐Neto et  al., 2012; Teles et  al., 2012). However, none of these surveys consist of long‐term studies that indicate events of re‐ gional colonization and/or missing species. In this paper we present an avifaunal survey of an urbanized ecosystem in southeastern Brazil, car‐ ried out along 30 years. Bird species were classified according to occurrence in urban habitats and in the reserve, which includes a native forest remnant and an adjacent lake located within the area. We describe the current bird community in terms of species rich‐ ness, composition, trophic structure, and the patterns of movement. We also report and comment on range extensions, regional colonization and disappearing species in the bird community during this period.


IntroductIon
In the past century urban ecosystems became the main landscape for billions of people around the world, and concentration of urban population is rising fast (Grimm et al., 2008).In those ecosystems dominated by human activities, biodiversity exerts an important role on human health and welfare and should be managed for improving the quality of life of citizens and the conservation of wildlife (Savard et al., 2000).Birds are important drivers of processes that regulate and support ecosystem function, including pest control, carcass and waste disposal, nutrient deposition, seed dispersal, pollination, and ecosystem engineering by burrow and cavity diggers (Sekercioglu, 2006).Besides the recreational, aesthetic and educational significance of urban birds (Sick, 1997), this highly mobile group is of major importance concerning air traffic collisions (Kitowski, 2011) and the spread of disease (Reed et al., 2003).Urbanization negatively affects bird species richness and composition, selecting against specialized species and favoring synanthropic ones (Chace & Walsh, 2006;Carvalho & Marini, 2007;Ortega-Álvarez & MacGregor-Fors, 2009;Reis et al., 2012).However, even in urban ecosystems, bird species comprise remarkable elements of the biodiversity, and information on community composition can be an important tool for monitoring environmental changes (Fernández-Juricic & Jokimäki, 2001;Chace & Walsh, 2006;Ortega-Álvarez & MacGregor-Fors, 2009, 2011;Fontana et al., 2011;Reis et al., 2012).
Based on old aerial photographs available at the university library, it was found that the forest fragment was completely isolated from other forest patches since 1960; part of it, currently covered by secondary forest, was cleared in the past (Fig. 2).This area was reforested with native and exotic trees in the 1970s and the vegetation regenerated (Mata da PUC Minas, 2011).Nevertheless, in the 1960s the entire area of the campus was on the outskirts of Belo Horizonte, in a predominantly rural matrix where pastures and swampy areas dominated (B.J. Teixeira, pers. com.).Currently, however, this area is completely inserted in an urban matrix, which prevents or impairs the dispersal of several bird species to other city parks and reserves.Furthermore, a small airport (Aeroporto de Carlos Prates), in activity since 1944, is located c. 500 m from the campus.
Adjacent to the PUC forest is a small lake of about 1,280 m², which was formed by damming a small stream (Landa & Landa, 2001).Upstream, there is another temporary lake, which presents water only during the rainy season (October-March) and becomes a marsh during the dry season (April-September).The rest of the campus is characterized by several buildings and gardens, represented by various tree species, most of them exotic.
Despite the importance of the PUC forest as a training site for the undergraduate and graduate students of this institution, there are only three published studies on its fauna: a checklist of butterflies (Silva et al., 2007), a study on the use of space by the Whiteeared Opossum (Didelphis albiventris -Almeida et al.,

2008
) and a behavioral study of the Flavescent Warbler (Basileuterus flaveolus - Perillo et al., 2010).With respect to the campus, the only published paper refers to the behavior of the Burrowing Owl (Athene cunicularia - Perillo et al., 2011).

Avifaunal survey
The general survey of the campus avifauna was conducted between 1982 and 2013.Most of the authors' records were opportunistic, without systematic survey techniques.J.E.S. and B.G. initiated fortuitous bird observations in 1982, working from then until the present as teachers of this institution.
Later, L.G.M., A.P. and R.M. conducted a systematic survey of the avifauna of the PUC forest between 2005 and 2007 using point counts.In that study, 11 points were established in the PUC forest (50 m apart from each other), which were sampled for eight minutes in fortnight campaigns, totaling 160 h of sampling effort.
Another systematic study in this forest fragment was conducted by F.A.V. and D.P. based on MacKinnon lists of 10 species (MacKinnon & Phillips, 1993;Herzog et al., 2002;Ribon, 2010) during monthly observations conducted in the morning (06:00 h-08:00 h) between 2 March 2012 and 8 June 2012, totaling 30 h of sampling effort.
Since April 2010, M.F.V. has taught several field classes in the PUC forest and other areas of the campus, including bird observations (c.250 h of sampling effort) and capture with mist-nets (c.20,000 m².h, following Straube & Bianconi, 2002).In those recent surveys, the vocalizations of several species have been recorded with a Sony TCM-5000EV tape recorder and Sennheiser ME-66 microphone.Copies of these vocalizations will be deposited in the Arquivo Sonoro Prof. Elias Coelho (ASEC), at the Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.Between 2006 and 2012, C.E.R.T.B., J.E.M.D. and B.P.R. also documented the avifauna with photographs, which have been kept in their personal archives.
Additionally, for the general survey of the avifauna, we also checked the bird collection of the Museu de Ciências Naturais da PUC Minas (MCNA), where there are several bird specimens (study skins and skeletons) from the study area and its vicinities.
The systematic order and scientific names follow the Brazilian Committee of Ornithological Records (CBRO, 2011).Classification of endemic birds of the Atlantic Forest was based on Brooks et al. (1999b), while those endemic to the Cerrado followed Silva (1995).Species were classified by forest dependency according to Silva (1995).Birds were also classified in trophic guilds according to Motta Junior (1990), Stotz et al. (1996), Sick (1997) and Lopes et al. (2005), and according to their migratory status following Sick (1984Sick ( , 1997) ) and Chesser (1994).Exotic species were considered invasive, occupying the area with human assistance and, later, establishing populations followed by range expansion (sensu Simberloff, 2010).We treated those invasive species differently than introduced species, considering native species that were released in the area; the majority of them common in the pet trade.
In relation to the pattern of movements and dispersal, the current avifauna is represented by 15 migratory species (see below), nine from Tyrannidae and the remaining distributed among other five families (Appendix).These migratory species can be found both in the urbanized area and in the forest remnant, but few species exclusively used the reserve (Fig. 5).However, most species recorded (N = 75, 61%) can be considered as resident in the area, including three invasive species, whereas few others (N = 28, 22.8%) are occasional visitors.The remaining species were probably introduced in the area, and the majority of them have been recorded in the reserve (Fig. 5).
Also noteworthy are those species of aquatic habitats, which are restricted to the small permanent lake adjacent to the PUC forest.Examples are: Neotropic Cormorant (Phalacrocorax brasilianus), Black-crowned Night-Heron (Nycticorax nycticorax), Striated Heron (Butorides striata), Great Egret (Ardea alba), Gray-necked Wood-Rail (Aramides cajanea), Paint-billed Crake (Neocrex erythrops), Ringed Kingfisher (Megaceryle torquata) and Amazon Kingfisher (Chloroceryle amazona).The piscivorous species are occasional visitors in the study area and feed mainly on Nile Tilapias (Oreochromis niloticus) that were introduced in this lake.In the specific case of the Paintbilled Crake, the only species record in the study area is based on a specimen found dead near the Museu de Ciências Naturais, not far from the lake, on 28 September 2010 (Lopes et al., 2012).Its skeleton was prepared and deposited in the bird collection of this institution (MCNA 1757).Sick (1997) reports another record of this species for the city of Belo Horizonte, possibly based on a skin deposited in the collection of the Museu de História Natural and Jardim Botânico da Universidade Federal de Minas Gerais, which was checked by M.F.V.
Those missing species can be divided into three different groups according to their habitats: species typical of forests and forest edges, species typical of wetlands with cattails (Typha sp.), and species typical of rural environments.The first group includes E. forficatus and H. albicollis, which probably disappeared due to the rapid urbanization of the region, which led to the reduction of fragments needed for foraging and perching (E.forficatus) or because of the strong pressure of ground-nest predation by domestic cats and dogs (H.albicollis), a well known impact on the avifauna of urban areas (Woods et al., 2003;Galetti & Sazima, 2006).Even though both species are absent at PUC Forest currently, they apparently present different extinction levels.Hydropsalis albicollis should be considered locally extinct, as it can still be found in larger forest fragments around the city (Vasconcelos et al., 2003;Vasconcelos, 2007).However, E. forficatus should be considered regionally extinct, as there are no longer known records of the species in Belo Horizonte, nor in its surroundings (Carvalho & Marini, 2007; L.G.M., M.F.V. and C.E.R.T.B., pers.obs.).Birds of the second group include C. cinnamomeus, A. leucocephala and D. atricapilla, occurring in wetlands with cattails until the 1990s.Subsequently, most of this vegetation was harvested and these three species had no longer been recorded.The third group includes the remaining species, C. parvirostris, P. rufifrons, T. leucorrhoa, L. pileatus, Z. capensis and G. chopi, which are very common in rural habitats of central and southeastern Brazil (farms, orchards, plantations) that until the late 1970s represented the dominant landscape of the region where the campus was located.With rapid urbanization in the region after the 1980s, it is possible that these species were no longer able to maintain viable populations in the campus area surrounded by inappropriate urban matrix.
The Picazuro Pigeon (Patagioenas picazuro) was rarely recorded in the campus area in the 1980s, as well as in the surroundings of Belo Horizonte city, until the mid-1990s.Currently, it is widespread throughout the city and very common on the campus.This species has also expanded its range in the state of São Paulo (Willis & Oniki, 1987;Alvarenga, 1990).Willis (1991) suggested that it would be important to collect specimens of P. picazuro in the state of São Paulo in order to determine if the subspecies expanding there was the southern form (P. p. picazuro) or the northeastern subspecies (P.p. marginalis).Seven specimens that were found dead in the study area (MCNA 726, 1881(MCNA 726, , 2361(MCNA 726, , 2362(MCNA 726, , 2363(MCNA 726, , 2364(MCNA 726, , 2922) ) were identified as the subspecies P. p. marginalis (following Pinto, 1949), suggesting that colonization of Belo Horizonte should be occurring from north to south.
The Band-winged Nightjar (Hydropsalis longirostris) was previously recorded on the campus in 1995 (L.F.Silveira, pers.com.).Recently, on 13 October 2011, a young male was found dead near the campus.This specimen was prepared as a study skin and has been deposited in MCNA (under the registration number MCNA 1796).Since it is known that H. longirostris has the ability to colonize large and mediumsized cities, such as Rio de Janeiro, Porto Alegre and Santo Amaro (Sick, 1959(Sick, , 1963(Sick, , 1997;;Ingels et al., 1999), it is very possible that this species is colonizing urban areas of Belo Horizonte.In this city, it has also been recorded in recent years in regions where it had not been detected until the last 20 years, such as the districts of Anchieta, Funcionários, Gutierrez, Luxemburgo, Mangabeiras, Santa Lúcia, Santo Antônio and Serra (L.G.M., M.F.V., C.E.R.T.B. and L.P.S.S., pers.obs.).
Finally, the record of the Masked Gnatcatcher (Polioptila dumicola) on the campus represents a range extension of almost 300 km to the east, based on current literature.In Minas Gerais, its known range is concentrated in the extreme west of the state, in the regions of Triângulo Mineiro and northwestern Minas Gerais (Ridgely & Tudor, 1989;Ridgely et al., 2007;Lopes et al., 2008;Faria et al., 2009).Although unpublished, four specimens collected in 2004 by M.F.V. at Fazenda Buriti Grande (18°44'S, 45°20'W), municipality of Morada Nova de Minas, are deposited in the Coleção Ornitológica do Departamento de Ornitologia da Universidade Federal de Minas Gerais (DZUFMG 4182,4183,4248,5188), which extends the species' range to the central region of the state.Anyway, the record on the campus still represents the southeastern border of the range of P. dumicola (c.200 km southeast of Fazenda Buriti Grande).The species was first recorded in the study area in 2010.Since P. dumicola was not detected during other surveys conducted in other areas of Belo Horizonte (Carnevalli & Rigueira, 1982;Rigueira et al., 1982;Faggioli, 1991;Vasconcelos, 2007;Pedersoli et al., 2010;Mafia et al., 2012), it is possible that the species has been expanding its range as a result of recent environmental changes.

Introduced and invasive species
Some species recorded on the campus are commonly appreciated by the human population as pets and can be considered as introduced.Some of them have sporadic records in the study area, but do not appear to establish populations there, including Duskylegged Guan (Penelope obscura -Fig.6), Blue-fronted Parrot (Amazona aestiva), Green-winged Saltator (Saltator similis) and Hooded Siskin (Sporagra magellanica).Probably, these birds escaped from captivity or    have been released.All individuals of the above mentioned species were recorded only once on the campus, were not shy (an indication that it is used to humans) and were represented by a single individual.
On the other hand, the introduced Saffron Finch (Sicalis flaveola), which has been recently released by the Brazilian environmental agency (IBAMA) and the forest police in Belo Horizonte and several other cities of Minas Gerais state, has a stable and reasonable population in the campus area.
Three other common and abundant species, the Rock Pigeon (Columba livia), the Common Waxbill (Estrilda astrild) and the House Sparrow (Passer domesticus) are exotic and considered invasive in Brazil, commonly found in urbanized ecosystems (Sick, 1997).

Migratory species
Despite the fact that we did not attempt to record specific dates of arrival and departure of some migratory species on the campus, we were able to note some patterns of occurrence for some of them.The migratory species found were mostly passerines (including several tyrant-flycatchers) and have been generally recorded in the study area between August and December, including: Streaked Flycatcher (Myiodynastes maculatus), White-throated Kingbird (Tyrannus albogularis), Tropical Kingbird (T.melancholicus), Fork-tailed Flycatcher (T.savana), Crowned Slaty Flycatcher (Griseotyrannus aurantioatrocristatus), Variegated Flycatcher (Empidonomus varius), Red-eyed Vireo (Vireo olivaceus) and Eastern Slaty Thrush (Turdus subalaris).
On the other hand, our records for the Brownchested Martin (Progne tapera) are concentrated during the first months of the year, between January and April.Nevertheless, more detailed investigations are needed to understand the patterns of temporal occurrence of those species in the study area.An example is the Gray Monjita (Xolmis cinereus), for which we could not find any clear pattern of seasonal occurrence on the campus.

Possible effects of isolation on birds
The campus population of the Chalk-browed Mockingbird (Mimus saturninus) consists of several individuals possessing a distinct phenotype from the original form.Some of them exhibit, to a greater or lesser extent, a blackish-brown throat, sometimes expanding to the breast (Fig. 7).Probably, this atypical plumage pattern is related to a mutation established in the campus population, isolated from others by the urban matrix, where the species is rarely recorded.However, other individuals showing the same atypical plumage pattern have been observed by M.F.V. in two squares of Belo Horizonte city: the Praça do Papa (19°57'22"S, 43°54'54"W) and the Praça Professor Alberto Mazzoni (19°54'31"S, 43°56'11"W).Rapid changes in plumage color and morphology (over a few decades) have been suggested or documented for isolated bird populations (e.g., Fitzpatrick, 1980;Remsen Jr., 1984;Rasner et al., 2004).Thus, detailed genetic studies should be conducted to test whether this mutation is related to the possible isolation of urban populations of this species.

conclusIon
The campus avifauna is relatively rich and still harbors many native bird species from different functional guilds that must contribute considerably to the health of this urban ecosystem.Nevertheless, the bird community comprises mostly widespread generalists.Yet the forest remnant increases habitat heterogeneity on the campus, favoring more specialized species than urbanized areas, and increasing functional diversity of birds on a small scale.Nevertheless, several species have disappeared from the area in a few years, whereas others have been introduced or have invaded this ecosystem, highlighting the pervasive effects of urbanization on bird community turnover.The cases of disappearing species suggest that isolated bird populations are likely to be extirpated in the urban matrix, especially because metapopulations of various species should not be able to recolonize these areas.For example, in the Brazilian Amazon, Borges & Guilherme (2000) found that the loss of understory bird species in an urban fragment of the city of Manaus was stronger than in forest fragments located in rural matrices, such as pastures and plantations.In this respect, within the study area, a single event of harvesting cattails led to the disappearance of three species (see above).
In addition, most forest-dependent species found are represented by small populations in the forest fragment and they are isolated from other populations at least since the 1960s, when the PUC forest was already isolated from other forest fragments (see Fig. 2).Therefore, it is possible that species with small populations are on the brink of extinction in this fragment (Brooks et al., 1999a), since they probably do not present potential abilities for dispersal to other urban or suburban forested areas.Moreover, the gene flow of these populations is probably interrupted for decades.This isolation of small populations of forestdependent birds, combined with the risk of predation by domestic cats and dogs that roam in the area, makes it possible to foresee that, in a few decades, the PUC forest will face local extinctions of some bird species (see Christiansen & Pitter, 1997;Willis & Oniki, 2002;Ribon et al., 2003), the last testimonies of the still little known forest avifauna of the municipality of Belo Horizonte.
The species list provided here will be useful as a database for monitoring long term effects of urbanization on this bird community.The continuous effort in surveying the campus avifauna will allow us to document new colonization and future local extinctions, especially in the case of forest-dependent species.

AcknowledgeMents
Prof. Bonifácio José Teixeira and Prof. Miguel Ângelo Andrade facilitated our field work in the PUC forest and provided all the institutional support for the conclusion of this study.The taxidermist and biologist Leandro de Oliveira Marques assisted in the preparation of some specimens found dead inside the campus.Ivana Gabriela Schork and Mariane da Cruz Kaizer collected a specimen of the Band-winged Nightjar, which was found dead near the campus.Marcela Fortes de Oliveira Passos, Eduardo José Gazzinelli, Igor Soares, Diego Hoffmann, Thais Augusta Maia, Vinícius Ferreira de Abreu, Ingred Rose Resende, Gefferson Guilherme Rodrigues Silva and Paula Cabral Eterovick accompanied us while doing some field work.We are also grateful to the Centro de Memória of the Library "Pe.Alberto Antoniazzi" for providing aerial photographs of the study area.

FIgure 1 :FIgure 2 :
FIgure 1: Map showing the study area of the campus of the Pontifícia Universidade Católica de Minas Gerais (yellow) in the municipality of Belo Horizonte, Minas Gerais, southeastern Brazil.The municipality is in a transitional zone between the Atlantic Forest and the Cerrado.

FIgure 5 :
FIgure 5: Distribution of bird species according to habitat use and patterns of movements and dispersal on the campus of the Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte, Minas Gerais, southeastern Brazil.

FIgure 6 :
FIgure 6: Individual of Dusky-legged Guan (Penelope obscura) in the edge of PUC forest and the garden of Museu de Ciências Naturais.Photo: D. Hoffmann.