An overlooked hotspot for birds in the Atlantic Forest

Montane and submontane forest patches in the state of Bahia, Brazil, are among the few large and preserved Atlantic Forests remnants. They are strongholds of an almost complete elevational gradient, which harbor both lowland and highland bird taxa. Despite being considered a biodiversity hotspot, few ornithologists have surveyed these forests, especially along elevational gradients. Here we compile bird records acquired from systematic surveys and random observations carried out since the 1980s in a 7,500 ha private protected area: Serra Bonita private reserve. We recorded 368 species, of which 143 are Atlantic Forest endemic taxa. Some 16 and 13 species are threatened at the global and national levels, respectively. If one accounts for subspecies, the number of Brazilian threatened taxa raises to 21. Species composition differs between lower and higher elevations, in which case lowlands harbor Amazonia-related taxa, whereas highlands are the home of Atlantic Forestrelated taxa. Key-Words. Aves; Bahia; Elevational gradient; Serra Bonita.


INTRODUCTION
The Atlantic Forest originally comprised 150 million hectares of vegetation in highly heterogeneous environmental conditions.Its forests (the predominant type of vegetation within the domain) extend into tropical and subtropical regions due to a wide latitudinal range (ca.30°).The structure of these forests is quite distinct as one leaves Brazilian eastern shores into the interior of the country mostly because of the decreased rainfall away from the coasts.Coastal areas receive as much as 4,000 mm of rain year-round, while inland forests receive ca. 1,000 mm/year (Câmara, 2005).These features, combined with elevational gradients, resulted in high diversity and endemism for several groups of plants and animals (Goerck, 1997;Myers et al., 2000;Silva & Casteleti, 2005).Currently, most of the remaining lowland (below about 500 meters elevation) Atlantic Forest is represented by small (< 50 ha) and isolated fragments composed predominantly by secondary growth in early to medium stages of succession (Ribeiro et al., 2009).Large fragments almost entirely remained in locations where steep terrains made human occupation particularly difficult (Silva et al., 2007).
Among the largest and best-preserved blocks of Atlantic Forests are montane and submontane forests in northern Espírito Santo and southern Bahia, Brazil (Ribeiro et al., 2009).Land cover in the region is a mosaic of native forest patches and areas of shade cocoa plantations interspersed with low-yield pastures, small farms and large forestry properties, the latter established mainly in the last three decades.Southern Bahia is the country's main cocoa (Theobroma cacao) production area (Alger & Caldas, 1996;May & Rocha, 1996;Cerqueira Neto, 2012).Nearly 70% of its cocoa production originates from the agroforestry system locally known as cabruca (Araújo et al., 1998), in which the cocoa trees, introduced from the Brazilian Amazon in 1746 (see Pacheco et al., 1996) replace the original understory and grow under the shade of a layer of native canopy species.This scenario is alarming since cabruca these poorly studied systems harbor great numbers of forest specialists (Pardini et al., 2009), including the Pink-legged Graveteiro (Acrobatornis fonsecai), a new genus and species unknown to science until the 1990s (Pacheco et al., 1996).
However, both the cocoa agroforests as forest remnants are still under intense threat.A severe socioeconomic crisis, caused by the devastation of cocoa farming by the Witches' Broom Disease and the falling price of cocoa on the international market, has triggered a sharp rise in pressure on these areas.This has led to the clearing of forest remnants and the replacement of cabruca areas for crops that interrupted the landscape connectivity, such as coffee and pasture.The region also became a major focus of illegal trade in native wood of the Central Atlantic Forest Corridor leading to serious erosion of biodiversity of forest areas that have not been cleared.In addition to habitat loss, high levels of hunting and illegal extraction of palm heart result in loss of biodiversity (Fonseca et al., 2004).
The remaining forests of southern Bahia, although small, fragmented and inserted into a mosaic of secondary vegetation, harbor some of the highest levels of biodiversity and endemism on the planet (Silva & Casteleti, 2005).It is also unique in sharing lowland Amazonia-related taxa such as the Cinereous Antshrike Thamnomanes caesius and the Screaming Piha Lipaugus vociferans (Aguiar et al., 2005).Although vegetation of this region is still poorly known from a floristic viewpoint, recent studies demonstrate extraordinary biological richness and species endemism (Thomas et al., 1998;Thomas, 2003).For this reason, it is one of the areas of highest priority within the Central Corridor of the Atlantic Forest.To reinforce its biological importance and high rates of endemism, the scientific crew created by the Ministry of the Environment to identify and propose areas for the creation of new protected areas recommended the creation of the Wildlife Refuge Serra do Baixão-Serra Bonita with an area of 33,000 hectares (Timmers, 2006).
According to the Instituto de Estudos Socioambientais do Sul da Bahia, Una-Serra do Baixão, which encompass the Serra Bonita complex, has a total area of 330,295 hectares.There are only two federal protected areas within this forest continuum: Una Biological Reserve (recently expanded to 18,500 ha) and the Una Wildlife Refuge (23,400 ha).However, in its current form, the public system of protected areas is not enough to reverse this situation nor to ensure the conservation and sustainable use of biodiversity in the long term.The main factors are two-fold: (1) the absolute area of the integral protected region is inadequate and (2) the distribution of protected areas through geographic and biological viewpoints is irregular and are concentrated in the region of Una (Descobrimento, Monte Pascoal and Pau-Brasil national parks).Thus, there are significant gaps in the remaining mountains, particularly in sub montane rainforests.Current protected areas suffer severe staff and financial resources limitations to ensure their effective management and supervision and despite its expan-sion into 7,100 ha, the land tenure of more than 50% of the Una Biological Reserve is not regularized (Diniz da Cruz, pers. com.).
Considering that southern Bahia suffered a severe forest clearing in the state between 2015and 2016(SOS Mata Atlântica & INPE, 2017), protected areas are of paramount importance to biodiversity.Within this context, Private Natural Heritage Reserves (PNHR) become crucial to strengthen the public protected areas system by filling gaps, increasing absolute areas under protection, conserving unique unprotected habitats and increasing connectivity in the landscape (Pinto et al., 2004).Within the Serra do Baixão, Serra Bonita PNHR is a key core area that has a significant role in increasing the absolute area of the region under full protection including a significant portion of sub montane and montane forests, a unique habitat still not represented by public protected areas.Serra Bonita is also exceptionally important for bird conservation, considered an Important Bird Area (BA 23, BR 111), with globally threatened and range-restricted species (Bencke et al., 2006;IUCN, 2016).This is the third largest number of endangered and endemic species out of the 31 Important Bird Areas (IBA) in Bahia (Bencke et al., 2006).Serra Bonita represents > 50% of the total area of the protected PNHR in southern Bahia and the incorporation of 725 ha of land already acquired by third parties as well as the acquisition of 1,045 ha through the Instituto Uiraçu will eventually expand it area to 2,700 ha (V.Becker, pers.com.).Hellmayr's (1929) andPinto's (1935) are still the main authorities regarding the Bahian ornithological state of the art.Few recent studies have gathered significant information on birds from this state, including southern Bahia (Gonzaga et al., 1995;Silveira et al., 2005).The absence of a state-level threatened species list is a consequence of the lack of studies within this region.Despite its biological representativeness, there are still significant gaps in knowledge of faunal groups, particularly regarding terrestrial vertebrates.Since the knowledge of composition of groups of vertebrates in any given area is a prime factor to define measures for their conservation (Heyer et al., 1994), the implementation of targeted and applied studies on amphibians, mammals and birds of the Serra Bonita and its surroundings proves decisive for the success of the area to conserve biodiversity in the long term.We surveyed the birds of Serra Bonita to provide basic elements for defining and monitoring measures to significantly enhance the ornithological knowledge of this PNHR.

MATERIAL AND METHODS
Serra Bonita PNHR is located south of Una-Serra do Baixão, in the municipalities of Camacan and Pau Brasil, southeastern Bahia, northeastern Brazil (Fig. 1).A significant part of this IBA, which has ca.7,500 ha, is included in PNHR Serra Bonita I, II, III and IV, forming a 2,700 ha forest block.Well-preserved forests cover the elevational gradient (from 200 to 950 m) of the mountains with rainforests richly covered in epiphytes.Above 600 m, there is frequent formation of dense fog, which renders montane forests a wetter aspect than the adjacent lowlands (BirdLife International, 2016).The latter include semideciduous forests whereas montane rainforests are typically found on higher elevations.This whole area is part of a mountain range that stands out in the landscape of south-eastern Bahia, contiguous to Serra das Lontras (currently a National Park), Serra do Javi and Serra do Teimoso (BA 20 and BA 22, BirdLife International, 2016).
Since 1980, authors have unsystematically surveyed birds at several farms that compose the Serra Bonita PNHR.We performed more concentrated efforts between 12-22 December 2010, when we visited two trails in Serra Bonita I (15°23'30"S, 39°34'06"W, alt.930 m, and 15°23'44"S, 39°24'25"W, alt.890 m) and two sites in Serra Bonita III (15°25'29" S, 39°32'31"W, alt.174 m, and 15°25'06"S, 39°32'38"W, alt.208 m).Lower elevations include Fazenda Paris and Santo Antônio (15°25'07"S, 39°32'44"W, alt.268 m), part of the reserve.For five months (June-October 2017), one of us (CA) also walked all trails of all farms on a weekly basis.In those areas, we walked randomly at a constant speed of about 1.5 km/h on several environments to record the largest number of species possible.We visually identified birds with the aid of binoculars and recorded vocalizations with a TASCAM DR-40 and shotgun microphones.These are deposited at Seção de Aves do Museu de Zoologia da Universidade de São Paulo (MZUSP), where we also deposited some collected specimens.We included non-systematic crepuscular observations to register nocturnal species.We began transect counts ca. 15 minutes before sunrise and lingered, at the minimum, for 2 hours when weather conditions permitted, i.e., when there was no rain or intense winds.It allowed us to ensure that the detectability of the birds would not be significantly affected.We conducted surveys along trails, secondary growth and forest edges.The total number of census resulted in over 100 days.In addition, in 2010 we used 20-30 mist nets (12 m × 3 m, mesh 36 mm) along the same trails used for surveys.We opened mist nets, mounted at ground level, at 06h00 and closed them around 17h00 or earlier in accordance with climatic conditions.Standardization of capture effort is in accordance with the following equation: E=area.h.n (1), where E is capture effort, area corresponds to the area of each net (height multiplied by width), h is exposure time (number of hours multiplied by the number of days) and n is the number of nets.We expressed results in h.m² (Roos, 2010) and accumulated 19,584 h.m² of net effort.We followed Straube's et al. (2010) suggestions for the standardization of environmental impact studies surveys, which also apply for our own objectives.Hence, database (rather than secondary data) are records from literature and museums (and in this case, previous visits by CA, LFS, JFP and BMW to Serra Bonita).In addition, we searched and critically revised Wikiaves (http://wikiaves.com.br)database from Serra Bonita private reserve and Camacan and Pau Brasil municipalities as of 12 December 2018 which resulted in some additions to the species list.We obtained field data, synonymous with primary data, in situ.
We used a Jaccard similarity index to compare species richness similarity between highlands and lowlands based on species present on both environments, as follows: (2), where J' is the actual index, a equals the number of exclusive species on a given site, b equals the number of exclusive species on a different given site and c equals the number of shared species between sites (Krebs, 1999).Taxonomic arrangements follow the most recent list of the Comitê Brasileiro de Registros Ornitológicos (Piacentini et al., 2015).

RESULTS
We recorded a total of 368 species, 276 at Serra Bonita (I and III) and 244 at Fazenda Paris (as well as another 56 only on surroundings).This corresponds to 45% of all bird species of the state of Bahia (Souza & Borges, 2008).As of 12 December 2018, the Wikiaves site reported one species from Pau Brasil and 258 species from Camacan, including three species we had not recorded in situ: Pseudoseisura cristata, Progne chalybea and Tangara brasiliensis.Combined with colleagues' records, Serra Bonita is the stronghold for 371 species of birds.Of this total, 13 species are under threat categories in Brazil (ICMBio, 2016), and as many as 16 species are either globally vulnerable or endangered (Appendix; IUCN, 2016).Some 67 (18%) species recorded at Serra Bonita PNHR are Atlantic Forest endemic species according to Bencke et al. (2006;Appendix).If one includes subspecies, then another 143 are Atlantic forest endemic taxa, in which case Serra Bonita harbors 108 taxa exclusive to this domain.Of these, the Olivaceous Woodcreeper Sittasomus griseicapillus olivaceus, inhabits southern Bahia only, and another six subspecies are threatened in Brazil.Because IUCN does not yet denote global extinction risk at the subspecies level, we call attention for a major gap in the knowledge of such taxa, which should be the objective of future taxonomic revisions.
We detected 93 (25%) species exclusively in the highlands (above 500 m), while 61 (22%) were only recorded in lowlands.The similarity index between the bird community in distinct elevational ranges was J' = 0.54, with 183 shared species.

DISCUSSION
Serra Bonita PNHR is the single locality with the highest species richness in all available inventories in Bahia.Not only the absolute number of species is remarkable, but also the percentage of endemic and threatened species has no parallel in the state (see Pinto, 1993;Gonzaga et al., 1995;Parrini et al., 1999;Silveira et al., 2005;Laps, 2006;Vasconcelos et al., 2012;Morante-Filho et al., 2015, 2016, 2018).From southern Bahia south to northern Rio de Janeiro, the lowlands harbor Amazonia-related taxa, whereas, in the highlands, Atlantic Forest-related elements are typically found (e.g., Willis & Oniki 2002;Silveira et al., 2005;Mallet-Rodrigues et al., 2010).Serra Bonita is no exception.Lowland Amazonian taxa include Thamnomanes caesius and Lipaugus vociferans.Like Serra das Lontras (Silveira et al., 2005), the entire elevational gradient, which in Serra Bonita is largely preserved, is necessary to maintain this biodiversity.
Due to the continuity and preservation of these forests, Serra Bonita PNHR may be a promising location to find some rare and threatened Atlantic Forest endemic taxa not yet recorded.In Bahia such species can be found almost exclusively at Una Biological Reserve or Pau-Brasil/Trancoso, Monte Pascoal and Descobrimento National Parks, situated within a 100 km radius (e.g., Laps, 2006), such as the Red-billed Curassow Crax blumenbachii.At Serra Bonita NHPR recent records of the Harpy Eagle Harpia harpyja, with breeding pairs and still relatively common in Amazonia but now very rare in the Atlantic forest (Galetti et al., 1997) also indicate the pristine conditions of local forests.There are a few recent records from southern Bahia as well, such as Serra das Lontras (Silveira et al., 2005) (Silveira et al., 2005) and is only found at higher elevations.This isolated population is currently under description and will be endemic to these southern Bahian mountains.
For harboring the greatest species richness, Atlantic Forest endemic species and globally threatened birds in Bahia, and because even more endemic and threatened species are likely to be found with increasing surveys, we urge that unprotected areas surrounding Serra Bonita be immediately incorporated into a permanent protection conservation unit.This act will enhance the survival of this entire ecosystem, already almost completely extirpated and fragmented, found nowhere else on Earth.In addition, cabrucas support high species richness of birds but do not act as surrogates for intact forests.The presence and representativeness of some forest species seem to depend on the existence of nearby native forests (Faria et al., 2006(Faria et al., , 2007;;Pardini et al., 2009).Pacheco et al. (1996) recognized the dire interface of cocoa growers in southern Bahia being forced to abandon their livelihoods in favor of cutting old cabruca canopies and planting other crops (such as bananas and coffee) with preservation of forests.To the point, they called for the immediate preservation of two blocks of land covering the elevational range from the lowlands to the tops of the highest peaks, one in the Serra das Lontras and the other in the Serra Bonita.As integral parts of the conservation plan, they recommended inclusion of extensive blocks of cabruca canopies; removal of the introduced cocoa trees; and planting of native seedling trees while ancient native "shade" trees were still present and dropping seeds annually.They further recommended that local people, especially large land owners, be integrally involved in the creation and maintenance of these forest reserves.Now, some 20 years later, good progress has been made in both the Serra das Lontras and Serra Bonita, and we still have the chance to follow through with these important directives.

APPENDIX
List of bird taxa recorded within Serra Bonita.Subspecific nomenclature are tentatively placed according to location and follow Piacentini et al. (2015) and MZUSP data when specimens are available.An asterisk indicates a taxa endemic of Atlantic Forest (n = 143).Paris and Santo Antônio Farms (< 500 m) and Serra Bonita I and III (> 500 m); S stands for surroundings.Acronyms refer to authors who recorded some species during initial observations.WA indicates records deposited online.The last two columns refer to endangered taxa globally (IUCN) and in Brazil (ICMBio).

Figure 1 .
Figure 1.Location of Serra Bonita NHPR in northeast Brazil.
, Estação Experimental Pau-Brasil, municipality of Porto Seguro, and a photograph of a young Harpy Eagle at Serra Bonita I (Sánchez-Lalinde et al., 2011).At Serra Bonita, V. Becker sighted a couple on forest border August 2015, and saw one individual close to the research facility August 2016.LFS also heard one individual calling at Fazenda Santa Antônio in May 2016 and an active nest was discovered in February 2018 (V.Becker, pers.comm.).We found as fairly common in the highlands a treehunter Heliobletus sp. which is being scientifically described (Whitney et al. in prep.).The taxon Cavarzere, V. et al.: A hotspot for birds Pap.Avulsos Zool., 2019; v.59: e20195905 4/14 also occurs at Serra das Lontras Cavarzere, V. et al.:A hotspot for birdsPap.Avulsos Zool., 2019; v.59: e20195905  12/14