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NORTH-WESTERN JOURNAL OF ZOOLOGY 12 (2): 373-376 ©NwjZ, Oradea, Romania, 2016 Article No.: e152601 http://biozoojournals.ro/nwjz/index.html

The patchy distribution of the Pale-throated Serra-Finch longicauda (Aves: Thraupidae) in the eastern Brazilian mountaintops: the overlooked campos rupestres of the Rio Doce valley

Leonardo Esteves LOPES*, Bráulio de Freitas MARÇAL and Anderson Vieira CHAVES

Laboratório de Biologia , Universidade Federal de Viçosa - Campus , Rodovia LMG-818, km 6, Florestal, , Brazil, 35690-000. *Corresponding author, L.E. Lopes, E-mail: [email protected]

Received: 15. November 2014 / Accepted: 29. May 2015 / Available online: 22. July 2015 / Printed: December 2016

Abstract. The Pale-throated Serra-Finch lives in the unique vegetation types known as campos rupestres, campos gerais and campos de altitude, which are found on the mountaintops of Eastern Brazil. In this paper, we present the first records of disjunct populations of the Pale-throated Serra-Finch in the Rio Doce valley, municipality of Alvarenga, Minas Gerais, Brazil. The Atlantic Forest formerly covered this region, with open grasslands floristically related to the campos rupestres vegetation found at higher elevations. We highlight the importance of conducting botanical and faunal inventories on these mountaintops, which are currently not granted legal protection and might harbor other threatened and/or undescribed endemic species.

Key words: Brazilian mountaintops, , disjunct populations, Neotropics.

Given that appropriate knowledge of the geo- covery to be formally published (O’Brien 1968), graphic distribution of a species is required for and although the publication communicated many aspects of environmental research, resource Kampfer’s findings, and did it so without any ac- management, and conservation planning (Franklin companying natural history data of the Pale- 2010), it becomes evident that the current under- throated Serra-Finch. Additional records of the standing of the range of Neotropical species is species were published few years later. These re- fragmentary (e.g. Lopes et al. 2010, 2012). A good cords were based on the observations made and example is the Pale-throated Serra-Finch, Ember- the specimens collected in the southern portion of nagra longicauda Strickland, 1844, a Neotropical the Espinhaço Range, Minas Gerais, Southeastern that, in spite of being described more Brazil (Carnevalli 1980, 1982), but again they than a century and a half ago, has its geographic lacked critical natural history data of the species. range still poorly understood. The Pale-throated Natural history data for the Pale-throated Serra-Finch is endemic to the eastern Brazilian Serra-finch are still scarce (Hoffmann et al. 2009). mountaintops (Vasconcelos 2008), and although Mattos and Sick (1985) presented the first detailed considered a Least Concern species (BirdLife In- data of its habitat, which includes the campos ternational, 2015), its geographic range is pre- rupestres and campos gerais that are found in the dicted to dramatically decrease during the next eastern Brazilian mountaintops. The campos rupest- decades due to climate changes (Marini et al. res is an azonal vegetation complex that occurs 2009). In this paper we summarize the knowledge above 900 m a.s.l. on the highest elevations of the about the range of the Pale-throated Serra-finch, Espinhaço Range and other outlier ranges with the present new records of the species on the isolated same lithology, where rocky outcrops intermixed mountain peaks in Eastern Brazil, and comment with patches of pure sand and gravel provide a on the distinct local landscape. rich and complex mosaic of micro-habitats (Giuli- The Pale-throated Serra-Finch was first de- etti et al. 1997, Alves et al. 2014). The vegetation is scribed from an unspecified number of specimens composed of an herbaceous stratum with sclero- obtained at an unknown locality in “South Amer- phyllous evergreen small shrubs and subshrubs, ica” (Strickland 1844). The geographic range of the and is particularly rich in endemic and threatened Pale-throated Serra-finch remained a mystery for plant species, including many species of Vel- more than a century, until 1926 when it was col- loziaceae, Eriocaulaceae and Xyridaceae (Giulietti lected by Emilie Snethlage in Mariana, Minas et al. 1997). Campos gerais occurs in the northern Gerais, and independently by Emil Kaempfer in portion of the Espinhaço Range and presents a 1928 in Chapada Diamantina, Bahia. Remarkably, treeless ground stratum rich in stemless palms it took an additional four decades for this redis- and with fewer grasses (Giulietti et al. 1997). 374 L.E. Lopes et al.

Machado et al. (1998) presented the first re- cords of the Pale-throated Serra-Finch in the Man- tiqueira Range, where it was recorded in the high elevation natural grasslands, as well as on the iso- lated mountains along the Rio Doce valley. Given that these later records were obtained in disturbed areas formerly covered by the Atlantic Forest, it was suggested that the species is expanding its geographic range due to deforestation (Machado et al. 1998, Vasconcelos 2000). Vasconcelos et al. (2003) presented the first re- cord of the Pale-throated Serra-Finch in the campos de altitude found on the Caparaó Range, Espírito Figure 1. Location of the study area (A) and detail (B) of Santo. The campos de altitude is a cool-humid grass- the southern portion of the range of the Pale-throated dominated formation restricted to the highest Serra-Finch Embernagra longicauda in the states of Minas mountain summits in Southeastern Brazil (Safford Gerais (MG) and Espírito Santo (ES). Circles indicate occurrences in the Espinhaço Range, triangles indicate 1999). Vasconcelos et al. (2003) suggested that past previously known occurrences out of the Espinhaço connections between some of the open vegetation Range and stars indicate new occurrences presented in formations currently isolated on the southeastern this paper. Darker tones indicate higher elevations. Brazilian mountaintops might explain the current Digital elevation model are from ASTER GDEM, a disjunct populations of the Pale-throated Serra- product of METI and NASA (http://gdem.ersdac. Finch. Moreover, the additional records of the spe- jspacesystems.or.jp/index.jsp). Previous records of the cies in the Rio Doce valley (Alves et al. 2009) sug- Pale-throated Serra-Finch are from Vasconcelos et al. (2003), Vasconcelos et al. (2008) and Vasconcelos and gest that natural open grasslands associated with Rodrigues (2010). Map by LEL. the rocky outcrops on the isolated mountain peaks above 800 m provide a suitable habitat for the spe- cies in the region. Brazilian municipality of . We observed three In this paper we present the first records of the birds in a degraded pasture with some small trees and patches of invasive ferns (Fig. 2). Forests once composed Pale-throated Serra-Finch in the municipality of the original vegetation of this site, but were cleared for Alvarenga, Rio Doce valley, eastern Minas Gerais coffee plantations more than a century ago; and although, (Fig. 1). This is a mountainous region with eleva- these plantations were abandoned 20 years ago and tions ranging from about 300 to almost 1600 m largely replaced by planted Brachiaria (Poaceae) pastures, a.s.l., and a complex lithology, including quartzite many dead coffee trees remain on the site. One bird was outcrops and granite inselbergs. Although the At- photographed (photograph deposited in the web portal lantic Forest formerly covered the entire region www.wikiaves.com under the number WA806003) and collected together with a second individual. Both speci- (Ribeiro et al. 2009), natural grasslands can be mens were deposited in the Center for Taxonomic Collec- found at the upper elevations, above the tree line. tions at the Universidade Federal de Minas Gerais, Belo The records summarized here demonstrate that Horizonte (DZUFMG 7178 and 7179). small populations of the Pale-throated Serra-Finch The second record of the species was obtained on the are patchily distributed along the intervening low- Pico da Aliança (19°23’43’’S, 41°40’09’’W, ca. 1455 m lands that separate the Espinhaço, Caparaó and a.s.l.), the second highest peak in the region, only lower the southern Mantiqueira Ranges, restricted to the than the Pico do Padre Ângelo (19°19’12’’S, 41°34’45’’W, ca. 1547 m a.s.l.), which we did not visit. We observed summits of these isolated mountain peaks. two birds on 26 December 2012 during our first visit to

the Pico da Aliança. Although we were able to attract The first record of the Pale-throated Serra-Finch consisted these birds by using playback recording (recording made of three adult birds observed on 20 November 2012 in ) of their typical song, we failed to collect (19°25’20’’S, 41°41’27’’W, 830 m a.s.l.; WGS84 datum) at them. We returned to the Pico da Aliança on 22 October about 1.5 km from the Pedreira do Zé Bertino (Fig. 2), a 2014 and successfully collected two specimens (DZUFMG mountain rich in quartzite outcrops intermixed with her- 7194 and 7195) on a site (19°23’44’’S, 41°40’21’’W, 1215 m baceous and shrubby vegetation, like the campos rupestres a.s.l.) about 3.7 km from where the species was previ- found in the Espinhaço Range. This mountain contains ously collected in Alvarenga. the Pico do Itacolomi (19°24’42’’S, 41°42’20’’W, 1048 m The vegetation of the Pico da Aliança, which is rich a.s.l.), a peak that the reader should not confound with in quartzite outcrops, is physiognomically and maybe flo- the homonymous and well-known peak located in the ristically similar to the campos rupestres vegetation (Fig. 3). The patchy distribution of Embernagra longicauda 375

Figure 2. The Pedreira do Zé Bertino (A) and the nearby Figure 3. The Pico da Aliança vegetation (A and B) and site (B) where the Pale-throated Serra-finch was first the local landscape (C). Note the large size of Vellozia collected in the municipality of Alvarenga, Rio Doce found at the peak. Photos by AVC. valley, Minas Gerais. Note the dead coffee trees amidst artificial pastures. Photos by AVC and BFM. from two syntypes (Benson 1999), both without any indication of the place of origin. Benson (1999) For example, we noted large populations of Vellozia sp. stated that Strickland obtained each specimen (Velloziaceae) growing on rock outcrops, including a very “apparently through a different medium (yet both large Vellozia species, with some individuals reaching al- most 4 m tall (Fig. 3B). Nevertheless, given the lack of ex- in 1838), the actual collector and locality might be tensive botanical data, we prefer to wait for additional one and the same”. Strickland purchased the first data before drawing any conclusion about the bio- specimen, which would later be examined by geographic affinities of the local vegetation. Hellmayr (1938), from his cousin, Nathaniel Con- stantine Strickland. Nathaniel’s collection in- The recent discoveries of allopatric populations of cluded about 1,200 specimens obtained from deal- the Pale-throated Serra-finch reinforce Vasconce- ers in England and Scotland, and included speci- los et al.’s (2003) assertion that there is a great mens from all around the world, many of them need to analyze the geographic variation of this without any data on their labels (Salvin 1882). The species. This is particularly important if we con- second specimen, which apparently was not ex- sider the morphological differences between the amined by any other authors before Benson (1999), specimens obtained in the northern and southern bears a label marked by Strickland “bought at portions of the Espinhaço Range (O'Brien 1968, Aberystwith [sic] 1838” and on the reverse “Dup Mattos and Sick 1985). Moreover, recent phy- type of E. longicauda” (Benson 1999). The town of logeographic, vocal and morphological research Aberystwyth is located on the West Coast of suggests a strong geographic structuring of the Wales. Our research found no information about species (Chaves and Freitas, unpub.). Aberystwyth’s local natural history dealers or The geographical variation observed in the about any other specimens bought together with species highlight the necessity of fixing the type the second specimen that could shed light on the locality of the species. We tried to trace back the type locality of the Pale-throated Serra-Finch. Fur- type locality of this taxon, but we failed on this thermore, since “the mode of preparation of the task. Long supposed to have been described from type specimen [number 1] offers no clew as to its a single specimen, this taxon was in fact described origin” (Hellmayr 1938), the same is probably true 376 L.E. Lopes et al. of specimen number 2, because the two specimens and prediction. Cambridge University Press, Cambridge. Giulietti, A.M., Pirani, J.R., Harley, R.M. (1997): Espinhaço Range showed “no obvious difference in the make-up” region: eastern Brazil. pp. 397-404. In: Davis, S.D., Heywood, (Benson 1999). V.H., Herrera-MacBryde, O., Villa-Lobos, J. Hamilton, A.C. We conclude this paper by noting that the iso- (eds.) Centres of plant diversity: a guide and strategies for their conservation. Vol. 3, The Americas. Oxford Information Press. lated mountain peaks of the Rio Doce valley are Gonella, P.M., Rivadavia, F., Fleischmann, A. (2015): Drosera on private lands and as such are not afforded legal magnifica (Droseraceae): the largest New World sundew, protection. The main threats to this distinctive and discovered on Facebook. Phytotaxa 220: 257-267. Hellmayr, C.E. (1938): Catalogue of birds of the Americas and the sensitive habitat include frequent human set fires adjacent islands in Field Museum of Natural History, part XI, and cattle grazing and/or trampling. The collec- Ploceidae, Catamblyrhynchidae, Fringillidae. Field Museum of tion of firewood on the mountains and its poten- Natural History Publication, Zoological Series 13: 1-662. Hoffmann, D., Lopes, L.E. Vasconcelos, M.F. (2009): Natural history tially devastating impact on the Vellozia species, notes on the Pale-throated Serra-finch (Embernagra longicauda) in often used for lighting wood burning stoves is of eastern Brazil. Ornitologia Neotropical 20: 597-607. particular concern. Therefore, given the severe Lopes, L.E., Malacco, G.B., Alteff, E.F., Vasconcelos, M.F., Hoffmann, D., Silveira, L.F. (2010): Range extensions and threats to sensitive mountainous region, the high conservation of some threatened and little known Brazilian levels of endemicity observed in the campos rupest- grassland birds. Bird Conservation International 20: 84-94. res, and the potentiality of discovering unde- Lopes, L.E., Pinho, J.B., Gaiotti, M.G., Evangelista, M.M., Vasconcelos, M.F. (2012): Range and natural history of seven scribed and/or threatened species, we urge for poorly-known Neotropical rails. Waterbirds 35: 470-478. continued botanical and faunal inventories to be Machado, R.B., Rigueira, S.E., Lins, L.V. (1998): Expansão made in the region. The recent description of geográfica do canário-rabudo (Embernagra longicauda - Aves, Emberizidae) em Minas Gerais. Ararajuba 6: 42-45. Drosera magnifica, a microendemic sundew (Drose- Marini, M.Â., Barbet-Massin, M., Lopes, L.E., Jiguet, F. (2009): raceae) from the Pico do Padre Ângelo, corrobo- Major current and future gaps of Brazilian reserves to protect rates our suspicions (Gonella et al. 2015). Neotropical savanna birds. Biological Conservation 142: 3039- 3050.

Mattos, G.T., Sick, H. (1985): Sobre a distribuição e a ecologia de duas espécies crípticas: Embernagra longicauda Strickland, 1844, e Embernagra plantesis, (Gmelin, 1789). Emberizidae, Aves. Revista Acknowledgments. LEL benefited from grants from Brasileira de Biologia 45: 201-206. Fundação Arthur Bernardes (FUNARPEX 2010–2011, O'Brien, C.E. (1968): Rediscovery of Embernagra longicauda 2014; FUNARPEQ 2012). AVC was supported by PNPD- Strickland. The Auk 85: 323. Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J., Hirota, CAPES postdoctoral scholarship. This study received M.M. (2009): The Brazilian Atlantic Forest: how much is left, and research grants from FAPEMIG and Vale SA. ICMBio how is the remaining forest distributed? Implications for provided collecting permits. Miguel Ângelo Marini conservation. Biological Conservation 142: 1141-1153. helped us with hard to find references. Marcos Rodrigues Safford, H.D. (1999): Brazilian páramos I. An introduction to the (DZUFMG) kindly allowed us to study material under his physical environment and vegetation of the campos de altitude. care. Gumercindo de Freitas, Brasilina de Freitas and Journal of Biogeography 26: 693-712. Salvin, O. (1882): A catalogue of the collection of birds formed by Cléber Marçal provided logistic support during our the late Hugh Edwin Strickland, M.A. Cambridge University studies in the region. Press, Cambridge. Strickland, M.A. (1844): Descriptions of several new or imperfectly- defined genera and species of birds. The Annals and Magazine of Natural History 86: 409-421. References Vasconcelos, M.F. (2000): Ocorrência simpátrica de herbicola, Embernagra platensis e Embernagra longicauda Alves, A.C.F., Vasconcelos, M.F., Loures-Ribeiro, A. (2009): Novo (Passeriformes: Emberizidae) na região da Serra do Caraça, registro de Embernagra longicauda na Serra do Jacroá, leste de Minas Gerais. Melopsittacus 3: 3-5. Minas Gerais, reforça a hipótese de conexões paleoecológicas Vasconcelos, M.F. (2008): Mountaintop endemism in eastern Brazil: entre as montanhas do sudeste do Brasil. Atualidades why some bird species from campos rupestres of the Espinhaço Ornitológicas 148: 10-11. Range are not endemic to the Cerrado region? Revista Brasileira Alves, R.J.V., Silva, N.G., Oliveira, J.A., Medeiros, D. (2014): de Ornitologia 16: 348-362. Circumscribing campo rupestre - megadiverse Brazilian rocky Vasconcelos, M.F., Maldonado-Coelho, M. Buzzetti, D.R.C. (2003): montane savanas. Brazilian Journal of Biology 74: 355-362. Range extensions for the Gray-backed Tachuri (Polystictus Benson, C.W. (1999): Type specimens of bird skins in the University superciliaris) and the Pale-throated Serra-Finch (Embernagra Museum of Zoology, Cambridge, United Kingdom: Cambridge longicauda) with a revision on their geographic distribution. University Museum of Zoology, Cambridge. Ornitología Neotropical 14: 477-489. BirdLife International (2015): Species factsheet: Embernagra Vasconcelos, M.F., Lopes, L.E., Machado, C.G., Rodrigues, M. longicauda. , accessed on: 2015.03.11. (2008): As aves dos campos rupestres da Cadeia do Espinhaço: Carnevalli, N. (1980): Contribuição ao estudo da ornitofauna da diversidade, endemismo e conservação. Megadiversidade 4: Serra do Caraça, Minas Gerais. Lundiana 1: 89-98. 197-217. Carnevalli, N. (1982): Embernagra longicauda Strikiland [sic], 1844: Vasconcelos, M.F., Rodrigues, M. (2010): Patterns of geographic sua ocorrência em Minas Gerais - Brasil (Aves, Fringillidae). distribution and conservation of the open-habitat avifauna of Lundiana 2: 85-88. southeastern Brazilian mountaintops (campos rupestres and Franklin, J. (2010): Mapping species distributions: spatial inference campos de altitude). Papéis Avulsos de Zoologia 50: 1-29.