Is the Chestnut-Capped Foliage-Gleaner Clibanornis

Is the Chestnut-capped Foliage-gleaner ISSN 1981-8874

Clibanornis rectirostris (Wied, 1831) 9 77198188700350 0 1 8 (Passeriformes: Furnariidae) a typical gallery forest species endemic to the Cerrado region?

Marcelo Ferreira de Vasconcelos1,2, Luiz Gabriel Mazzoni2, Alyne Perillo2, Thiago Oliveira e Almeida3, Filipe Cristovão Ribeiro da Cunha4, Christian Regis da Silva5, Eduardo José Gazzinelli6 & Santos D’Angelo Neto7

The Chestnut-capped Foliage-gleaner (Clibanornis rectirostris) is considered an endemic species of the Cerrado region, having a strong association with gallery forests occurring in this mor- phoclimatic domain (Silva 1995, Betini et al. 1998, Silva & Vielliard 2000, Fa- ria et al. 2012). Despite the finding of Marini (2001) that the Chestnut-capped Foliage-gleaner is not sensitive to forest fragmentation and probably has the capacity to cross unfavorable landscape matrices, recent studies have suggested the species’ vulnerability based on its depen- dence on the highly impacted gallery forests (Faria et al. 2012). Furthermore, future range loss and shifts are expec- ted due climate change (Marini et al. 2009). Here, we present records of C. rectirostris in habitats not represented by gallery forests of the Cerrado, including the first observations in the Atlantic Forest region. We also comment on the species’ conservation based on these new records. Our records were made opportunisti- cally while conducting several avifaunal surveys in the states of Minas Ge- rais and São Paulo, between the years of 2001 and 2015. Whenever possible, records were documented by photographs, recordings of vocalizations and specimen collecting. Vocalizations were deposited in the Arquivo Sonoro Elias Coelho (ASEC), Rio de Janeiro, Figure 1. General aspect of two areas of arboreal caatinga where the Chestnut-capped Foliage-gleaner and in the online database Xeno-canto was recorded at Riacho dos Machados, Minas Gerais. Photos: Thiago Oliveira e Almeida.

40 Atualidades Ornitológicas, 185, maio e junho de 2015 - www.ao.com.br 02015.000518/2011-71; and SISBio per- manent permit number 28301-1).

Records in other habitats not represented by gallery forests in the Cerrado region

Arboreal caatinga In January and July 2013, during an avifaunal survey conducted at Riacho dos Machados municipality, northern Mi- nas Gerais, in a transitional zone between the Caatinga and the Cerrado, MFV, TOA and CRS found C. rectirostris in typical dry arboreal caatinga, without any watercourse or gallery forests (Figure 1). Four specimens, two males and two females (MCNA-2753, 3583, 3584, 3587 - Figu- re 2), were collected in two fragments of arboreal caatinga (16o03’S, 43o08’W and 16o04’S, 43o07’W). The closest watercourse in the region is dry during the major part of the year (usually betwe- Figure 2. Specimens of Clibanornis rectirostris deposited in the Museu de Ciências Naturais, Pontifícia Universidade Católica de Minas Gerais, from the following municipalities, from left en March and November), with running to right: Riacho dos Machados (MCNA-2753, 3583, 3584, 3587); Rifaina (MCNA-4230); water only in the rainy season, and it is Belo Horizonte (MCNA-2441); Almenara (MCNA-1550, 1551). Photo: Letícia Ferreira Pedroso. located c. 1.5 km from our record sites. Nevertheless, both areas were represented by ravines, locally named barrancos.

Cerradão woodland On 19 January 2004, MFV collected a female specimen (DZUFMG-4101 - Fi- gure 3) in a cerradão woodland at Fazen- da Jacaré-Riachão (18o38’S, 45o05’W), Felixlândia municipality, Minas Gerais state. This area was represented by tall typical cerradão trees of c. 8 m with dense tangles of vines. Despite not being close to any gallery forest, a small vere- da palm grove occurred 500 m from the collecting site. On 10 January 2015, another female (MCNA-4230 - Figure 2) was obtained by MFV in a cerradão habitat in Rifai- na municipality (20°00’S, 47°25’W), São Paulo state. This site is physiognomically very similar to that in Felixlândia and lacks any watercourse in its interior (Figu- re 4), despite being located near second- -growth gallery forests of Rio Grande, c. Figure 3. Specimen of Clibanornis rectirostris (DZUFMG-4101) from Felixlândia, deposited in the 350 m from the collecting site. Departamento de Zoologia da Universidade Federal de Minas Gerais. Photo: Letícia Ferreira Pedroso. (http://www.xeno-canto.org). Specimens were deposited in Urban areas the ornithological collection of Departamento de Zoologia On 17 December 2003, MFV observed and heard an indivi- da Universidade Federal de Minas Gerais (DZUFMG, under dual of the Chestnut-capped Foliage-gleaner in an urbanized IBAMA permit number 228/2003, process 02015.020098/02) site of Montes Claros municipality (16°44’S, 43°52’W). The and of the Museu de Ciências Naturais, Pontifícia Universi- bird was recorded in the margin of a polluted river along dade Católica de Minas Gerais (MCNA, under IBAMA per- one of the most important avenues of the city. Vegetation is mits 126/2014, process 02001.002573/1999-42; 518/2012, represented by sparse trees, and the matrix is represented by process 02015.004288/2011-19; and 089/2011, process urban areas with asphalt roads and buildings.

Atualidades Ornitológicas, 185, maio e junho de 2015 - www.ao.com.br 41 The species was also recorded during several months between 2010 and 2012 in an avifaunal inventory conducted at the campus of the Pontifícia Universida- de Católica de Minas Gerais (19°55’S, 43°59’W), isolated in an urban matrix of the large city of Belo Horizonte, in the state of Minas Gerais (Vasconcelos et al. 2013). We estimated three individuals li- ving in a small forest fragment of less than 7 ha inside the campus. Vegetation cover of this urban forest fragment is represented by semideciduous forest and lacks riverine habitats. Nevertheless, there are some natural barrancos in its interior and a small artificial lake (Figu- re 5). In the MCNA there is a specimen obtained from this area (MCNA-2441 - Figure 2). Despite the majority of records having come from the forest fragment, in a single occasion one individual was observed when singing in the canopy of a “castanheira” tree (Terminalia catappa) in the urbanized area of the campus, 250 m away from the forest fragment. This Figure 4. General aspect of the cerradão where the Chestnut-capped Foliage-gleaner bird was chasing a Rufous Hornero (Fur- was recorded at Rifaina, São Paulo. Photo: Luiz Gabriel Mazzoni. narius rufus) that was perched in the same tree.

Atlantic Forest fragments Vocalizations of one individual of the Chestnut-capped Foliage-gleaner were heard by MFV and I. R. Lamas on 14 January 2001 in second-growth forest on the left bank of Rio Suaçuí Grande (18°21’S, 42°31’W), São Pedro do Su- açuí municipality, Minas Gerais. The area was very degraded by selective lo- gging and the presence of cattle, with a very open understory. Nevertheless, there were several ravines on the river margin. The bird was vocalizing from a dense clump of exotic bamboo (Bambusa sp.). Between 22 and 30 December 2003, SDN and MFV observed and heard an individual of C. rectirostris in the pro- perty of Mr. Onofre Sandinha (17°08’S, 42°44’W), Leme do Prado municipality, near the limits of the Acauã Ecological Station. The area is represented by typical semideciduous Atlantic Forest (Ka- Figure 5. General aspect of the semideciduous forest fragment where the Chestnut-capped Foliage- mino et al. 2008) holding several bird gleaner was recorded at Belo Horizonte, Minas Gerais. Photo: Marcelo Ferreira de Vasconcelos. species endemic to this domain (Vasconcelos & D’Angelo On 10 July 2008, LGM and AP observed and heard an Neto 2007, Carrara et al. 2013). The bird was seen fora- individual on the left bank of the Rio Piracicaba (19°58’S, ging in the mid-stratum of the forest and on the ground. An 43°13’W), Rio Piracicaba municipality. The bird was fora- additional specimen (complete skeleton) of C. rectirostris ging in the understory of a narrow strip of riparian vegeta- (MCNA-1673) was collected close to this area by B. Garzon tion. The surroundings of the area were composed by semide- on 15 January 2006 in a nearby area at José Gonçalves de ciduous forests on slopes and pastures (Figure 6). Barrancos Minas municipality, although there is no indication of geo- were present in the banks of the Rio Piracicaba, and also graphic coordinates on its label. along trails located within forested slopes.

42 Atualidades Ornitológicas, 185, maio e junho de 2015 - www.ao.com.br 42°57’W). The region possesses typical semideciduous Atlantic Forest fragments (Figure 7) interspersed with pastures and second growth habitats. Barrancos were very common in this area, either within the forests or in forest edges and pastures. On 17 March 2011 the species was recorded in a fragment of Atlantic Forest in the municipality of Carlos Chagas, eastern Minas Gerais. EJG heard the vocalizations of four individuals in a riverine forest on the right bank of the Rio Mucuri (17°36’S, 41°02’W). The forest area was very narrow, with open understory and a small flooded area that was soaked with the accumulated rain of the past days. The surroundings of this forest were composed of a dirt road and deforested slopes with isolated shrubs. On 13 April 2011, FCRC collected two females, an adult and a juvenile (MCNA 1550, 1551 - Figure 2), in a fragment of semideciduous forest in the municipality of Almenara, Minas Gerais (16°00’S, Figure 6. General aspect of the riparian degraded vegetation where the Chestnut-capped Foliage- 40°36’W). This fragment is bordered by gleaner was recorded at Rio Piracicaba, Minas Gerais. Photo: Luiz Gabriel Mazzoni. pastures except on its southern portion, where the area adjoins a dense formation of Atlantic Forest with a small stream. The site where the birds were collected is approximately 800 m from a watercourse. On 18 and 19 March 2014, CRS observed and heard the vocalizations of two individuals in an Atlantic Forest fragment on the left bank of Rio Preto, municipality of Morro do Pilar, Minas Ge- rais (19°16’S, 43°33’W). This fragment is characterized as semideciduous forest surrounded by second growth and pastures (Figure 8).

Concluding remarks Our records show that the Chestnut- -capped Foliage-gleaner is not a specialist of the gallery forests of the Cerrado region. Records from Carlos Chagas and Almenara extend the species’ range eastward, almost to the boundaries of southern Bahia and northern Espírito Santo states (Figure 9). Records conducted in areas of arboreal Figure 7. General aspect of the Atlantic Forest fragment where the Chestnut-capped Foliage-gleaner caatinga, far away from any watercour- was recorded at Dores de Guanhães, Minas Gerais. Photo: Luiz Gabriel Mazzoni. se, but represented by barrancos, suggest On 20 July 2010, LGM and AP observed and audio-recor- that this should be the most important resource for habitat ded (ASEC 17036 and 17037, XC215506) two individuals in selection by this species, since it depends on barrancos for a clump of exotic bamboo (Bambusa sp.) in the left bank of nesting (Faria et al. 2008). Another observation made in den- the Rio Guanhães (19°03’S, 42°52’W), in the municipality se caatinga scrub (carrasco) was presented by Vasconcelos of Dores de Guanhães, Minas Gerais. The species was also et al. (2012) in the state of Bahia. It is also important to men- regularly recorded in this region between 12 and 16 Janua- tion that the four specimens collected at Riacho dos Macha- ry 2011 and between 29 July and 3 August 2011, including dos represent topotypes of Opetiorynchus rectirostris (ba- another locality on the right bank of the same river (18°59’S, sonym of Clibanornis rectirostris), since the area is located

Atualidades Ornitológicas, 185, maio e junho de 2015 - www.ao.com.br 43 in the northern Minas Gerais state, close to the Bahia border, named “Campos Ge- raës” by Wied (1831). The holotype, a female housed in the American Museum of Natural History (AMNH 5223), was collected in the nearby Serra Geral (15o25’S, 42o48’W) (LeCroy & Sloss 2000). The species’ records in cerradão woodland, but close to gallery forests or ve- reda palm groves, two habitat types known to be used by this species (Silva & Vielliard 2000, Tubelis 2009), show that the Chestnut-capped Foliage-gleaner can also use this kind of woodland typical of the Cerrado region. Other typical forest birds, including one which is also considered restricted to the gallery forests from the Cerrado region, the Helmeted Manakin (Antilophia galeata), were recorded in a cerradão woodland in the state of São Paulo (Cavarzere et al. 2011). Detailed studies should be conducted in this habitat type to check if these forest Figure 8. General aspect of the Atlantic Forest fragment where the Chestnut-capped Foliage-gleaner dependent species can use it sporadically was recorded at Morro do Pilar, Minas Gerais. Photo: Thiago Oliveira e Almeida. or if they are resident. The species’ records in urbanized sites, including a small fragment of semideciduous (not gallery) forest isolated for at least 40 years, reinforces Marini’s (2001) observations that it has low sensitivity to forest fragmentation and/or a reasonable capacity for dispersion. Other records of this species in urban parks were previous- ly reported by Franchin & Marçal (2004) and Valadão et al. (2006a, b). In this con- text, some observations in urbanized sites are probably related to dispersing individuals. On the other hand, the species’ presence in degraded areas or second-growth in the Atlantic Forest region probably represents a recent range expansion related to habitat modification or climate change. Marini et al. (2009), using the Maxent algorithm, modeled future distribution ranges for 26 bird species endemic to the Cerrado (including C. rectirostris), predicting a general trend for range shift toward southeastern Brazil. The same research group also presented another model, using GARP algorithm, which predicted a present-day potential distribution of C. rectirostris Figure 9. Map showing the records of Clibanornis rectirostris in the present study (red dots). in the same region of the Atlantic Forest Municipalities are numbered as follows: 1 and 2 - Riacho dos Machados; 3 - Felixlândia; 4 - Rifaina; where we made our records, but the au- 5 - Montes Claros; 6 - Belo Horizonte; 7 - São Pedro do Suaçuí; 8 - Leme do Prado; 9 - Rio Piracicaba; thors interpreted these results as a possible 10 and 11 - Dores de Guanhães; 12 - Carlos Chagas; 13 – Almenara; 14 – Morro do Pilar. error of their model, based on its unknown occurrence in this tant to point out that a previous record of the Chestnut-capped area (Corrêa et al. 2010). Thus, the present records in eastern Foliage-gleaner from Serra dos Órgãos, in the Atlantic Forest Minas Gerais can be related or not to climate change or defo- of Rio de Janeiro state (Sick 1985: 515) was rectified as based restation, but it is noteworthy that all records in the Atlantic on a mislabeled specimen probably collected in western São Forest were also represented by barrancos. It is also impor- Paulo by Heinrich Reinisch (Pacheco 1992).

44 Atualidades Ornitológicas, 185, maio e junho de 2015 - www.ao.com.br Finally, based on the present records and on the evident Sick, H. (1985) Ornitologia brasileira: uma introdução, v. 2. Brasília: recent range expansion of C. rectirostris eastward, we show Editora Universidade de Brasília. that the species is not a specialist of gallery forests. The spe- Silva, J.M.C. (1995) Birds of the Cerrado region, South America. Ste- cies’ vulnerability, estimated by population size occurring enstrupia 21(1): 69-92. only in gallery forests of the Cerrado region (Faria et al. Silva, W.R. & J. Vielliard (2000) Avifauna de mata ciliar, p. 169-185. In: 2012), is erroneous and can lead to misdirected conservation Rodrigues, R.R. & H.F. Leitão-Filho (eds.). Matas ciliares: con- efforts that should be directed to species that really deserve servação e recuperação. São Paulo: Editora da Universidade de threatened status. São Paulo. Tubelis, D.P. (2009) Veredas and their use by birds in the Cerrado, South Acknowledgments America: a review. Biota Neotropica 9(3): 363-374. FCRC thanks CAPES for a research grant (“Ciência sem Valadão, R.M., A.G. Franchin & O. Marçal-Júnior (2006a) A avifauna no Fronteiras”) during his Ph.D. work. Mr. Onofre Sandinha Parque Municipal Victorio Siquierolli, zona urbana de Uberlândia allowed us to conduct surveys in his lands. Ivana Reis Lamas (MG). Biotemas 19(1): 81-91. accompanied MFV in São Pedro do Suaçuí. Letícia Ferreira Valadão, R.M., O. Marçal-Júnior & A.G. Franchin (2006b) A avifauna no Pedroso took photographs of specimens deposited in DZU- Parque Municipal Santa Luzia, zona urbana de Uberlândia, Minas FMG and MCNA. Fernando Augusto Valério prepared the Gerais. Bioscience Journal 22(2): 97-108. map that illustrates Figure 9. Vasconcelos, M.F. & S. 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