First record of the characteristics of the nest of Glaucis dohrnii (: Trochilidae): biometry of the and environmental aspects of the nesting site

Pedro Cerqueira Lima¹, Josafá Sampaio de Almeida², Josafá Sampaio de Almeida Filho², Ricardo Lustosa¹, Jamerson Monteiro Rodrigues Viana³

Abstract. The article describes the nest of Glaucis dohrnii (Bourcier & Mulsant, 1852 - Passeriformes: Trochilidae) and characteristics of the “vine forest” (mata de cipó) in the municipality of Boa Nova, Bahia, where the bird and its nest were evaluated. The area is considered a transition zone between the biomes of the Caatinga and Atlantic Forest, rich in the biodiversity of bromeliad , whose inflorescences are the principal food source of this species. The nest of Glaucis dohrnii was recorded on a bro- meliad leaf (Bromelia sp). The munici- pality of Boa Nova is 80 kilometers from Jequié, the locale where the G. dohrnii Figure 1. Actual occurrences and records of Glaucis dohrnii in Brazil. was observed by Oliveiro Pinto in 1932, and both of these municipalities are composed of the Caatinga and Atlantic Forest biomes and ecotonal areas.

Introduction The Hook-billed , Glaucis dohrnii (Bourcier & Mulsant, 1852) is considered to be one of the rarest spe- cies of Brazilian fauna (Grantsau 2010). Historically, G. dohrnii is recorded from the north of Rio de Janeiro to the south of Bahia, passing through the state of Espírito Santo and the eastern corner of Minas Gerais (Birdlife 2017) (Figure 1). G. dohrnii occurs in the tropical forests of the Atlantic Rainfor- est (Mata Atlantica) particularly along rivers with flowering , and is seen within the forest as well as in ar- eas adjacent to the forest visiting orna- mental flowers (Ruschi 1982). There is Figure 2. Nest registration region of Glaucis dohrnii. a historic record of G. dohrnii made in the southern region pality of Itagibá (Pinto 1935), near the Gongogi River basin, of the state of Bahia in 1932 by Oliveira Pinto in the munici- where the nest of the G. dohrnii was recorded in the current

Atualidades Ornitológicas, 204, julho e agosto de 2018 - www.ao.com.br 49 study ( Figure 2). The Gongogi river ba- sin encompasses the municipalities of Gongogi, Nova Canaã, Iguaí, Itagibá, Dário Meira, Ibicui and Aurelino Leal. A specimen of Glaucis hirsuta hunted in Espirito Santo and described as G. dohrnii was deposited in the Paulista Museum by E. Gaber in January 1906 (Pinto 1935, 1964, 1978, Collar et al. 1992). Sick (1985, 1997) reported that the G. dohrnii is restricted to the prima- ry forests of Espírito Santo and located a population in the Monte Pascoal Na- tional Park (Bahia) in 1977. Historic records also occur from the eastern corner of Minas Gerais (Sick 1997). In Bahia, there are recent reports in three localities: Estação Vera Cruz, Monte Pascoal National Park and Serra de Itamaraju (Birdlife 2017). G. dohr- nii appears on the red list of extinction (Birdlife 2016), and due to deforesta- tion throughout all its distribution area it has been reduced to some fragmented sub-populations, probably in decline, as Figure 3. Vine Forest in the municipality of Boa Nova (BA), the habitat a result of this continual loss of habitat. of Glaucis dohrnii, rich in bromeliad species. Photo: Pedro Lima G. dohrnii suffers from settlements pressures, fires, road tics of the nest of Glaucis dohrnii, and there are few des- construction and very little protection of waterways which criptions of the biometry of this bird (Rushi 1982, Grantsau reduces suitable habitat for this species (Brasil 2008, Bir- 1989), as well as scarce information on the aspects of the dLife 2017). G. dohrnii lives in virgin forests, over-flying nesting site of this species.The objective of this study was streams and rivers looking for nesting sites; it reproduces to describe the characteristics of the G. dohrnii nest found from September to February (Ruschi 1982, 1986). Accor- in the municipality of Boa Nova, Bahia, the biometry of the ding to our knowledge there is no record of the characteris- bird and environmental aspects of the nesting site.

Figure 4. (A) The nest of G. dohrnii constructed on a Bromelia sp leaf (B) G. dohrnii registered in Boa Nova, Bahia on 04/07/2014, latitude: -14 21’ 38,58398’’ and longitude: -40 11’ 24,47571’’. Photos: Pedro Lima.

50 Atualidades Ornitológicas, 204, julho e agosto de 2018 - www.ao.com.br tural corridors to establish genetic flow between populations of plants and ani- mals, which assures the conservation in situ of several species of flora from the northeast of Brazil (Figure 3). The current study is part of research on the reproductive behavior of in Bahia that has been ongoing since 1989. From 1989 to 2017, more than 200 species of birds have been evalua- ted and the nests of 12 specimens des- cribed. The study occurred in the Boa Nova National Park (12,065 hectares) and was created in June of 2010 toge- ther with the Wildlife Refuge (15,024 hectares) with the goal of protecting an important area of transition between the Caatinga and Atlantic Rainforest (Bra- sil 2017). The high altitude forest whe- re the nest was located is between the- se two important biomes and is locally known as “vine forest” (mata de cipó).

Data collection Figura 5. Glaucis dohrnii nest built on a bromeliad leaf and containing two eggs. Almeida (2012b). Observations were made with the naked eye, binoculars, playback and audio recognition. Mist nets measuring 12 meters in length 2.5 meters in height and with 10 mm mesh size were used to capture the specimens/ They were pla- ced in areas of the bird’s potential food sources in order to increase capture ra- tes. Ten nets were set up in each of the forested areas of the Caatinga biome, the Atlantic Forest biome and the Vine Forest. Each net remained set up for ap- proximately 11 hours (from 5:30 a.m. 5:00 p.m.) for three consecutive days, with the total sample time of 330 hours per net. The nets were inspected at in- tervals of 20 to 30 minutes in order to minimize the amount of time birds were in the net and therefore stressed. The captured birds were identified, placed in cloth sacks and weighed, ban- ded and measured to gather standard biometric data. The birds were subse- quently released in the same places they Figure 6. Glaucis dohrnii nest with two chicks close to fledging, had been captured. Individual records photographed on December 16, 2012. Photo: Josafá Almeida. were made, specifying the name of the Material and methods species, sex, age (when possible), measurements of beak, Study area tarsus, wing and tail, verification of the reproductive period Fieldwork was carried out in the municipality of Boa through the presence of brood patches, the presence of ecto- Nova, which is composed of two biomes: the Caatinga and parasites and anomalies. Colored metallic bands of a diame- the Atlantic Rainforest. The transition zone between the ter suitable for each species were attached to each captured biomes is where the Vine Forest occurs. Macedo (2009) bird. The methodology proposed in the Banding Manual of reports that this vine forest has a large number of species the National Center for Research for Conservation of Wild from both the Atlantic Forest and the Caatinga as well as Birds – Cemave (Brasil 1994) was followed in all banding its own species. This fact qualifies these vine forests as na- activity.

Atualidades Ornitológicas, 204, julho e agosto de 2018 - www.ao.com.br 51 Figure 7. (A, B, C) The Glaucis hirsutus nest has an elongated shape ending in a long caudal appendage suspended from a palm leaf. On the outer walls are attached some lichens and plant detritus. The caudal appendage provides balance to the nest which is built quite loose. Measurements of the birds, the eggs and the nests were the other ona leaf of a Shrub species in December 2013 and made using millimetric and pachymetric rulers. Dynanome- December 2016 in Poções and Porto Seguro, Bahia, respec- ters of 0.5 kg, 1.0 kg and 5.0 kg and spring scales of 10.0g, tively. The records of these G. dohrnii nests in the state of 30g, 100g and 300g were used. Material was collected from Bahia, as well as those recorded by Josafá Almeida (Almei- the nests after the birds had abandoned them to identify their da 2012a, 2012b, 2012c), were entered into the WikiAves compostion, and the plants, fruits and inflorescences which database, which is the most important source for consulta- are part of the bird’s diet were identified by specialists. A Garmin Etrex-H GPS was used (Datum: WGS84) to geo-reference the locale of the G. dohrnii nest in the muni- cipality of Boa Nova, Bahia. Geographical information on the historic occurrence of G. dohrnii fwas gathered from Pinto (1935, 1964, 1978), Ruschi (1982, 1986), Collar et al. (1992), Sick (1997), Brasil (2008), Grantsau (2010), Birdli- fe (2017), Fnjv (2017) and the Encyclopedia of the Birds of Brazil, WikiAves. photographic records of G. dohrnii came from Dias (2017) and Santos (2013). The delimitation of the watershed of the Gongogi River was digitalized by Teixeira et al. (2012), using the app. Arcgis 10.1. for cartographic production.

Results and discussion Characteristics of the nest of Glaucis dohrnii On July 4, 2014 we located a nest of G. dohrnii which had been abandoned on the same clump of Bromelia sp where the first nest had been observed. The construction of the nest starts at around 150 mm from the tip of the drooping leaf (which has an average width of 35 mm) and extends down vertically to the tip of the leaf. It is built around the leaf, taking advantage of its concave shape (Figure 4). Small pieces of leaves are affixed to the external walls. It has the general form of a funnel or coffee filter, with a small caudal appendage, distinguishing it from the nest of the G. hirsutus (Figure 5) in that it is relatively short and has neither leaves nor lichens affixed. Grantsau (1989) reports that the nests of the Glaucis ge- nus are affixed to the underside of a palm leaf and are very Figure 8. Nest of the Glaucis dohrnii drawn by Augusto Ruschi loose. Santos (2013) and Dias (2017) recorded G. dohrnii taken from his book of the State of Espírito Santo nests on two occasions, one built on a bromeliad leaf and (Beija-flores do Estado do Espírito Santo) (Ruschi 1982).

52 Atualidades Ornitológicas, 204, julho e agosto de 2018 - www.ao.com.br tion due to the absence of photographic records of G. dohr- Biometry of Glaucis dohrnii nii nests in the scientific literature. The egg of the G. dohrnii weighs 0.75 g and measures 16 On November 26, 2012, G. dohrnii was observed in the mm x 10 mm, and incubation is performed over 14-15 days. vine Forest of Boa Nova, Bahia, during a bird watching The young fledge at between 20-22 days old (Ruschi 1982, expedition led by Josafá Almeida for Pedro Ávila, Marcus 1986). Another report of G. dohrnii describes two eggs wei- Mello and Rafael Furtado (Almeida 2012a). On December ghing an average of 0.75g, measuring 17 mm x 10 mm and 1, 2012, Josafá Almeida discovered a nest containing two incubated by the female for 15 days, with the chicks fled- eggs built on a bromeliad leaf (Almeida 2012b) (Figure 5). ging at between 20-27 days of age (Del Hoyo et al. 1999), On December 16, 2012 there were two feathered chicks and 27 days (Grantsau 1989). On December 1, 2012, a nest which were almost ready to fledge (Almeida 2012c) (Figure of G. dohrnii was found containing two eggs and on De- 6). cember 16 there were two feathered chicks (Almeida 2012b) In this study, it was observed that the nest of G. dohrnii is (Figure 5) which fledged a few days later. Assuming that affixed to bromeliads’ leaves taking advantage of the plants’ the chicks were born on December 2, it would have been 14 form, and the nest material is woven around the leaf which days later when they were photographed and fledged in less provides rigidity and balance, so that a long caudal appen- than 18 days. dage as seen in the nests of G. hirsutus and the genera of Table 1 shows the biometric differences between Glaucis Ramphodon and Therenetes (Figure 7) is not necessary. dohinii captured on July 4, 2014 in the municipality of Boa The nest structure of Ramphodon, Glaucis and Therene- Nova, Bahia, with the acknowledgments other authors. Ac- tes is elongated in form, ending in an appendage like tail. cording to Grantsau (1989) the female Glaucis dohrnii is a The nests hangfrom a palm tree leaf, or etc. Some little smaller and the male’s beak is more curved. lichens and plant debris are affixed to the external walls of the nest, and the caudal appendage provides equilibrium Environmental aspects of the nesting site of Glaucis dohr- and stability. It is composed of fibers taken from palm tree nii pinnules which allows it to be seen through its fork (Ruschi Between 2006 and 2017 an inventory of the bromeliad 1982) (Figure 8). Ruschi (1982, 1986) reports that G. dohr- species of the vine forest in the municipality of Boa Nova nii reproduces from September to February and that it lives was performed, and six species which are visited by the in virgin forests, over-flying streams and rivers looking for G. dohrnii were identified: Aechemea alba (Mez.,1894), nesting sites which always occur in the pinnule of palm leaf, Aechmea multiflora (L.B.Sm. 1970) a species endemic to and they affix the nest on the extremity of the pinnule. Ho- Bahia whose inflorescence is heavily used (Figure 9), Bil- wever, in the present study the characteristics of the nest of bergia saundersii (L.B.Sm. & Reitz.,1964), Bilbergia saun- G. dohrnii were different from Ruschi’s (1982) description. dersii saundersii (Bull 1874), Vriesea sp, and Bromelia sp., Specifically,it was much smaller than the nest of G. hirsutus all considered Atlantic Rainforest species (Martinelli et al. and was built on the dorsal tip of a Bromelia sp leaf at a 2008) (Figure 10) and (Cryptanthus boanovensis Leme., height of 1.5 meters from the ground. 2015), a species described as endemic to the vine forest in Table 1. Biometric data of the Glaucis dohrnii gathered by different authors. Weight (g) Total length (mm) Tail (mm) Wing (mm) Beak (mm) Source 6.5 145 46.6 73.11 20,5 The author 6.5 122 43 70 28 Ruschi (1982) 9 137 39 68 29 Grantsau (1989)

Figure 9. (A) Aechmea multiflora. The flowers of this species are heavily relied upon by Glaucis dohrnii. It is the most abundant species in the vine forest, and locales with high density of this bromeliad are the preferred habitat of the Slender Antbird (Rhopornis ardesiaca) and (B) Bilbergia saundersii. Photos: Pedro Lima.

Atualidades Ornitológicas, 204, julho e agosto de 2018 - www.ao.com.br 53 Figure 10. (A) Aechemea alba and (B) Bilbegia porteana, bromeliad species whose inflorescences are visited by Glaucis dohrnii. Photos: Pedro Lima.

Figure 11. (A) Bromelia sp., the genus on which Glaucis dohrnii constructs their nests and (B) Cryptanthus boanovensis by Leme (2015), a species described in 2015 and endemic to the vine forest of Boa Nova; the flowers of this species are also visited by the Glaucis dohrnii. Photos: Pedro Lima. the municipality of Boa Nova (Leme 2015) (Figure 11). The relevance of the vine forest in the municipality of Boa Nova where the G. dohrnii was recorded is heightened by the fact that the Slender Antbird (Rho- pornis ardesiaca) (Wied, 1831) occurs there, a species endemic to the Vine Forest and more frequently observed in locales with the bromeliads from the Bromelia genus. The Slender Antbird (Figure 12) is on the red list of Brazil- ian birds and is threatened with extinc- tion (Brasil 2008). The transition or vine forest in the municipality of Boa Nova, Bahia, has acted as a refuge for endangered spe- cies of birds, and larger studies about the forest’s extension and the risk of Figure 12. Rhopornis ardesiaca perched on a bromeliad leaf (Aechmea multiflora). This species is endemic degradation in the municipality and the to the vine forest and prefers forests with large densities of bromeliads of this species. Photo: Pedro Lima.

54 Atualidades Ornitológicas, 204, julho e agosto de 2018 - www.ao.com.br region are needed, as are programs that bolster its mainte- Brasil (Ministério do meio Ambiente) (2017) Unidades abertas a visita- nance and expansion in order to preserve and multiply areas ção. Parque Nacional de Boa Nova. Brasília: Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio. favorable to species such as Rhopornis ardesiaca and Glau- Brasil (Ministério do Meio Ambiente - MMA e Fundação Biodiversitas) cis dohrnii. (2008) Livro vermelho da fauna brasileira ameaçada de extinção. Figure 2 shows the watershed of the Gongogi River, the 1ª ed. Brasília: MMA e Fundação Biodiversitas. v. II region where the nest of G. dohrnii described in this study CBRO - Comitê Brasileiro de Registros Ornitológicos (2014) Listas das Aves do Brasil. 11ª ed. Brasília: Comitê Brasileiro de Registros Or- was found (the red dot on the map). Teixeira et al. (2012) nitológicos. characterize the river basin of the Gongogi River both phys- Collar, N.J., L.A.P. Gonzaga, N. Krabbe, A. Madroño Nieto, L.G. Naranjo, ically and socio-economically and concluded that the land T.A. Parker & D.C. Wege (1992) Threatened birds of the Américas: use in the river basin correlates directly with its climatic the ICBP/IUCN Red Data Book. Cambridge: International Council for Bird Preservation conditions since the area where cacao is cultivated closer to del Hoyo, J.A. Elliott, A. & J. Sargatal (eds) (1999) Handbook of the the river has a more humid climate, while pastures are drier birds of the world. Vol. 5. Barcelona: Lynx Edicions. areas. The substitution of cacao areas and forests closer to Dias, A.C. (2016) Registro fotográfico de ninho de Glaucis dohrnii (Bour- the river with drier pastures needs to be monitored in the cier & Mulsant, 1852) em Poções, Bahia, em dezembro de 2016 [WA2433025]. Wiki Aves - A Enciclopédia das Aves do Brasil. Dis- river basin so that the refuges of G. dohrnii will not be fur- ponível em: . Acesso em: 17 ther degraded. jun. 2017. The nest of G. dohrnii offers good camuflauge in the for- FNJV (Fonoteca Neotropical Jacques Vielliard) (2017) Fonoteca neotro- est and difficult access for predators. However, since it is pical Jacques Vielliard, pesquisa G. dohrnii. Brasília: rede species- Link. built on the leaves of palm trees, bromeliads and bushes, it Grantsau, R (1989) Os beija-flores do Brasil. São Paulo: Exped. depends on the occurrence cycles of these plant species with Grantsau, R. (2010) Guia completo para identificação das aves do bra- these characteristics and is vulnerable to the environmental sil. 1ª ed. São Paulo: Vento Verde. degradations of the Atlantic Rainforest, the forests near riv- Leme, E.M.C. (2015) Cryptanthus boanovensis. J. Bromeliad Soc. 65(2). ers as well as ecotone regions of the biomes of the Caatinga Macedo, G.E.L (2009) Florestas Estacionais Interioranas do Nordeste – O Brejo Novo. In: III CLAE e IXCEB, São Lourenço - MG. Anais... and Atlantic Rainforest, such as the locale where the nest of São Lourenço - MG. the G. dohrnii for this study was located (Figure 2). More Martinelli, G., C.M. Vieira, M. Gonzalez, P. Leitman, A. Piratininga, A.F. research and preservation of ecotone areas and river basins, Costa & R.C. Forzza (2008) Bromeliaceae da Mata Atlântica brasilei- such as those suggested for the Gongogi River basin, favor ra: lista de espécies, distribuição e conservação. Rodriguésia 59(1): 209-258. the preservation of the G. dohrnii. Pinto, O.M.O. (1935) Aves da Bahia notas críticas e observações sobre uma coleção feita no recôncavo e na parte meridional do estado. Acknowledgments Separata. São Paulo: Museu Paulista da Universidade de São Paulo. We thank the Foundation for the Support of Research Pinto, O.M.O. (1964) Ornitologia brasiliense. Catálogo descritivo e ilus- trado das aves do brasil. São Paulo: Depto. de Zoologia e Secret. do from the State of Bahia (Fundação de Amparo à Pesquisa estado de São Paulo. do Estado da Bahia – Fapesb) for its support of this study Pinto, O.M.O. (1978) Novo catálogo das aves do Brasil. Primeira Parte. and our friend Elton Leme, who has contributed more than São Paulo: Museu de Zoologia, Universidade de São Paulo. a decade to the inventorying of the bromeliads of Bahia in Ruschi, A. (1982) Beija-flores do estado do Espírito Santo. São Paulo: Editora Rios. regions like Boa Nova where we perform studies of birds, Ruschi, A. (1986) Aves do Brasil. Rio de Janeiro: Expansão Editora. Vol: for his generosity in allowing us to participate in some of IV. his field studies. Santos, J.S. 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