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Papéis Avulsos de Zoologia

Print version ISSN 0031-1049

Pap. Avulsos Zool. (São Paulo) vol.54 no.14 São Paulo  2014

http://dx.doi.org/10.1590/0031-1049.2014.54.14 

Status of the globally threatened forest birds of northeast Brazil

 

 

Glauco Alves PereiraI; Sidnei de Melo DantasII; Luís Fábio SilveiraIII; Sônia Aline RodaIV; Ciro AlbanoV; Frederico Acaz SonntagVI; Sergio LealVII; Mauricio Cabral PeriquitoIV; Gustavo Bernardino MalaccoVIII; Alexander Charles LeesIX

IUniversidade Federal Rural de Pernambuco (UFRPE), Programa de Pós-Graduação em Etnobiologia e Conservação da Natureza. Rua Manoel de Medeiros, s/n, Dois Irmãos, CEP 52171-900, Recife, PE, Brasil and Observadores de Aves de Pernambuco (OAP). E-mail for correspondence: glaucoapereira@yahoo.com.br
IICoordenação de Zoologia, Museu Paraense Emílio Goeldi. Caixa Postal 399, CEP 66040-170, Belém, Pará, Brasil and Observadores de Aves de Pernambuco (OAP)
IIICurador das coleções ornitológicas, Museu de Zoologia da Universidade de São Paulo, Caixa Postal 42.494, CEP 04218-970, São Paulo, SP, Brasil
IVObservadores de Aves de Pernambuco (OAP). Rua Agamenon Magalhães, 28, QC13, Engenho Maranguape, CEP 53423-440, Paulista, PE, Brasil
VNE Brazil Birding. Rua das Laranjeiras, 485, Lagoa Redonda, CEP 60831-620, Fortaleza, CE, Brasil
VIRua David Ferreira Luna, 151, Apartamento 1002, Brisamar, CEP 58033-090, João Pessoa, PB, Brasil
VIIOrganização de Preservação Ambiental (OPA). Loteamento Valparaíso, Rua 02, Quadra D, 281, CEP 57043-015, Feitosa, Maceió, AL, Brasil
VIIIAssociação para a Gestão Socioambiental do Triângulo Mineiro (ANGÁ), Av. Anselmo Alves dos Santos, 119, sala 04, Saraiva, CEP 38408-008, Uberlândia, MG, Brasil
IXCoordenação de Zoologia, Museu Paraense Emílio Goeldi. Caixa Postal 399, CEP 66040-170, Belém, Pará, Brasil

 

 


ABSTRACT

The Atlantic Forest of northeast Brazil hosts a unique biota which is among the most threatened in the Neotropics. Near-total conversion of forest habitat to sugar cane monocultures has left the region's endemic forest-dependent avifauna marooned in a few highly-fragmented and degraded forest remnants. Here we summarise the current status of 16 globally threatened species based on surveys conducted over the last 11 years. We found a bleak situation for most of these species and consider that three endemics: Glaucidium mooreorum (Pernambuco Pygmy- owl), Cichlocolaptes mazarbarnetti (Cryptic Treehunter) and Philydor novaesi (Alagoas Foliage-gleaner) are most likely globally extinct. Some positive news can, however, be reported for both Leptodon forbesi (White-collared Kite) and Synallaxis infuscata (Pinto's Spinetail) which may warrant re-evaluation of their respective red list statuses. We outline a road map to prioritise conservation interventions in the region directed at preventing the extinction of this suite of threatened bird species and their companion biota.

Key-Words: Fragmentation; Species-area relationship; Conservation intervention; Protected areas.


RESUMO

A Floresta Atlântica do Nordeste do Brasil abriga uma biota única que está entre as mais ameaçadas na região Neotropical. A quase total conversão dos habitats florestais em áreas de plantação de cana-de-açúcar deixou a avifauna florestal endêmica da região isolada em poucos remanescentes florestais altamente fragmentados e degradados. Aqui, resumimos o status atual de 16 espécies globalmente ameaçadas baseado em pesquisas conduzidas nos últimos 11 anos. Encontramos uma situação desanimadora para a maioria dessas espécies e consideramos que três espécies endêmicas: Glaucidium mooreorum (caburé-de-pernambuco), Cichlocolaptes mazarbarnetti (gritador-do-nordeste) e Philydor novaesi (limpa-folha-do-nordeste) estejam provavelmente extintas. Algumas notícias positivas podem, no entanto, ser reportadas para Leptodon forbesi (gavião-de-pescoço-branco) e Synallaxis infuscata (tatac), do qual necessitam de uma reavaliação de seus respectivos status na lista vermelha. Descrevemos em linhas gerais um planejamento para priorizar as intervenções conservacionistas na região direcionadas na prevenção da extinção do conjunto das espécies de aves ameaçadas e sua biota associada.

Palavras-Chave: Fragmentação; Relação espécie-área; Intervenção conservacionista; Áreas protegidas.


 

 

INTRODUCTION

The Atlantic Forest stretches across eastern Brazil, eastern Paraguay and northeastern Argentina (Rizzini, 1997). It is subdivided into regional biogeographic provinces or centres of endemism with their own unique biotas (Silva & Casteletti, 2003; Silva et al., 2004). The most threatened of these endemic areas is the Pernambuco Centre of Endemism (henceforth PCE) in northeastern Brazil, a strip of Atlantic Forest north of the São Francisco River, encompassing the states of Alagoas, Pernambuco, Paraíba and Rio Grande do Norte (Brown, 1982; Prance, 1982).

This region has suffered from both the first (dating back to the 16th century) and the most severe waves of forest loss observed in any Brazilian ecoregion. Deforestation rates accelerated during the late 1970s and early 1980s (Silveira et al., 2003a) when the last remaining large tracts of lowland forest were lost. This pulse of forest loss was driven by a Brazilian government program (with the support of the World Bank) called PROALCOOL which was launched in 1975 and aimed to increase ethanol production as a substitute for gasoline, helping Brazil to reduce its dependence on oil following the global petroleum crisis of the early 1970s (Teixeira, 1986; Cavalcanti, 1992; Silveira et al., 2003a; Martinelli & Filoso, 2008). This drive for energy independence came at a cost of most remaining forest, leaving the regional landscape dominated by sugar-cane monocultures (Silveira et al., 2003a; Tabarelli et al., 2010). Regional forest cover is now reduced to 12.1% of its original pre-Columbian extent (Ribeiro et al., 2009).

The legacy of this assault on the region's forests is that 48% of the remaining fragments are smaller than 10 ha and very few are larger than 1,000 ha, moreover all are embedded in a hostile matrix of sugar cane plantations (Ranta et al., 1998). Remaining forest patches are threatened by on-going degradation from fire, selective-logging and firewood removal and the large-bodied vertebrate fauna is threatened by hunting (Silveira et al., 2003a).

Of the 434 bird species recorded in the PCE, 65% are strongly associated with forest habitats (Roda, 2003). Fifteen of these are currently listed on the International IUCN Red List (IUCN, 2013), making the PCE the Brazilian ecosystem with the highest relative number of threatened birds (Olmos, 2005) and probably one of the most threatened in the world (see the list of endemic and threatened species in Silveira et al., 2003a). Distributional data for these threatened taxa is critical for effective conservation planning, to revise threat assessments and more pessimistically to document the likely imminent extinction of some of these bird species. Here we present new records for globally threatened species, synthesise knowledge on their tolerance to habitat loss and fragmentation, and assess their future conservation prospects.

 

METHODS

Study area and bird surveys

The PCE is divided into three geographical subunits: the coastal plain, the São Franciscana depression and the Planalto da Borborema (IBGE, 1985), this last stretching across the entire PCE over 900 m asl (Moreira, 1977). The regional climate is hot and humid (Nimer, 1972), with the rainfall decreasing from the coastal plain to the interior, and increasing again at the highest altitudes (Annel, 1998 apud Roda, 2003). On the coast, annual rainfall varies from 1,750 to 2,000 mm, with a dry season lasting from October to January. In the interior annual rainfall varies from 1,250 to 1,750 mm, with a longer dry season extending between October and March (Coutinho et al., 1998; IBGE, 1985). Broadly interpreted, the Atlantic Forest in the PCE includes mangroves, restingas, semideciduous and ombrophilous forests, and their contact zones (IBGE, 2004; Tabarelli et al., 2006). Ombrophilous forests are dominated by trees in the families Leguminosae, Lauraceae, Sapotaceae, Chrysobalanaceae, and Lecythidaceae (Grillo et al., 2006).

We compiled data from both intensive targeted bird surveys and opportunistic observations in the PCE over the course of the last 11 years, accumulating data for many globally-threatened bird species. These surveys were undertaken in Atlantic Forest fragments of varying size, from 6 to 1,200 hectares, all with little, if any, connectivity to other fragments (Table 1). Our surveys took place in six localities in Paraíba, 35 in Pernambuco and seven in Alagoas states. An additional site outside the PCE range (in Sergipe) was included given records of two threatened birds widely regarded as endemic to the PCE sensu strictu (Fig. 1).

Species accounts are provided for taxa currently classified as threatened on the IUCN Red List and restricted to the PCE in addition to two recently described or 'upgraded' species and we also indicate the current national threat status as judged by the Brazilian Ministry of the Environment (Ministério do Meio Ambiente: MMA, 2003). Scientific names of the species follow those of the Comitê Brasileiro de Registros Ornitológicos (CBRO, 2014). Geographic coordinates of survey sites, patch area, and habitat type are listed in Table 1. Given the importance of providing objective documentation for rare species (see e.g., Lees et al. 2014b), we present links to digital vouchers (sound-recordings or photographs) deposited on the Brazilian avian photo archive Wikiaves (www.wikiaves.com.br) and/or the global avian sound library xeno-canto (www.xenocanto.org). Recordings on both sites are searchable by the catalogue number provided in the species accounts.

In addition to our own fieldwork we also compiled presence/absence data for all threatened species recorded in the last 11 years from 99 variable-sized forest fragments within the PCE, published both in the primary ornithological literature and in the 'grey' literature – e.g., unpublished consultancy reports (for additional data sources see Appendix). With this information we created a species-by-site matrix with binary presence/absence data. Using this matrix we assessed the species-area relationship between forest fragment area (log10 ha) and number of threatened bird species, performing a linear regression model considering all 99 forest fragments for which we could find bird data. The R2 value that we report is the adjusted R2. We also constructed a horizontal point plot illustrating species presence/absence in all forest fragments.

 

RESULTS

Our surveys amassed 97 new records of 11 threatened bird species (see Table 2). Richness of threatened species per fragment increased over the range of observed fragment sizes in the PCE (mean: 3.22 threatened species per fragment, SD: 2.72 range 1-14), generating a significant semi-log species-area relationship (r2 = 0.236, P < 0.001, N = 99, Fig. 2). Threatened species varied in their responses to habitat fragmentation even among respective IUCN threat classes (Fig. 3) in a highly species-specific manner. Both the well-inventoried 6,116 ha Estação Ecológica de Murici (ESEC Murici) and the 500 ha Mata do Quengo (RPPN Frei Caneca) held all the threatened species at least up until 2007 (see accounts for Philydor novaesi and Myrmotherula snowi) but extinctions of these species have been subsequently documented at these sites. Some globally threatened species were not encountered despite our searches, and these nega-tive results are also presented to highlight the critical situation of some threatened birds in the PCE.

Species accounts

Pauxi mitu (linnaeus, 1766), Alagoas Curassow
(IUCN and MMA: EW; Fig. 4)

 

 

The last observations of this species from the wild were made in lowland forest fragments at Roteiro, Barra de São Miguel, Pilar, and Marechal Deodoro in the mid 1980s (Teixeira, 1986; Silveira et al., 2004). There have been no subsequent sightings by ornithologists in the region and semi-structured interviews with local people living around suitable forest fragments failed to indicate any recent sightings (Silveira et al., 2004, GAP unpublished data). However, prior to this species' extinction in the wild, a few individuals were captured and a captive breeding program was launched. This program is now composed of both hybrids (with Razor-billed Currasow Pauxi tuberosa) and pure-bred individuals, and is currently run by two aviculturists in Minas Gerais, Brazil (see Silveira et al., 2004). This captive population, now numbering over 100 pure-bred individuals, is subject to genetic management (Francisco et al., in prep.) with a reintroduction program scheduled to start in 2015 in Alagoas.

Leptodon forbesi (Swann, 1922),
White-collared Kite (IUCN: CR)

Considered one of the world's most threatened raptors, this species was recently "rediscovered" (Pereira et al., 2006; Dénes et al., 2011), when recorded from 12 localities in the states of Alagoas and Pernambuco (Seipke et al., 2011). This species was considered a PCE endemic, but there is now a single recent record south of the São Francisco river in Sergipe outside of the PCE which may be a vagrant individual – perhaps unsurprising as a river is unlikely to form a major barrier for a large soaring forest raptor. We recorded this species from another 16 sites in Pernambuco, Alagoas and Paraíba states (Table 2). This series of new records (including the first for the state of Paraíba) suggests that this species is more widespread in the PCE than formerly thought. The persistence of some individuals in small and degraded forest fragments (and likely an ability to move between different forest patches) coupled with an apparent absence of hunting pressure, suggest a degree of resilience to land-use change in the region, although quantitative studies should be undertaken to assess this assumption. Nevertheless, we suggest that this species also ought to be the target of a captive breeding program given the relative ease at which raptors can be maintained and bred in captivity.

Touit surdus (Kuhl, 1820),
Golden-tailed Parrotlet (IUCN: VU)

Despite its relatively ample distribution in the Atlantic Forest – stretching from Paraíba to São Paulo (Collar, 1997; Forshaw, 2010), this species is only known from only 12 localities in the PCE (Roda, 2003) with Silveira et al. (2003a) finding this parrotlet in 5 of 15 surveyed forest fragments (Fig. 3). Our fieldwork produced additional records from 13 localities in Pernambuco, Paraíba and Alagoas (Table 2). As with the preceding species, this parrotlet may be preadapted to life in fragmented landscapes as these and other psittacids have to track spatio-temporally variable fruit resources (e.g., Lees & Peres, 2009). Parrotlets in the genus Touit have very poor survivorship in captivity and are thus not highly sought after by bird traffickers (Collar, 2000). A pair was observed attending a nest in an arboreal termitarium in the RPPN Fazenda Pacatuba, municipality of Sapé, Paraíba. The preference for nesting in arboreal termitaria frees members of this genus from dependence on tree hollows, required by many parrot species.These may be a population-limiting factor in degraded and regenerating forests with few large old trees (e.g., Cockle et al., 2010).

Glaucidium mooreorum
Silva, Coelho & Gonzaga, 2002,
Pernambuco Pygmy-owl (IUCN: CR)

Documented records of this enigmatic species include just the type series of two individuals collected in November 1980 and a single sound-recording obtained in October 1990 from the Reserva Biológica (REBIO) de Saltinho, Pernambuco. Since its description, the species has been extensively sought-after by many different fieldworkers in forest fragments across the PCE using playback of the single vocal sample available (see Roda & Pereira, 2006; Roda et al., 2011). These searches have resulted in just one subsequent undocumented sight record of a single bird observed at Usina Trapiche in November 2001 (Silva et al., 2002). Our own playbacks elicited a mobbing response in small passerines (e.g., Red-headed Manakin Ceratopipra rubrocapilla, Olivaceous Woodcreeper Sittasomus griseicapillus, Variable Oriole Icterus pyrrhopterus) at Engenho Cachoeira Linda, Mata do Roncadorzinho, and other fragments e.g., the Usina Trapiche (Mata do Dêra, Mata do Sá and Engenho Jaguaré) which we may interpret as evidence of the historic occurrence of G. mooreorum in these localities. Given the absence of records for a minimum period of 12 years, we consider that this species may be potentially extinct. Galileu Coelho (pers. comm.) regularly heard one or more individuals of this species singing near the main house of the Saltinho research station until the start of the 1990's. Pygmy-owls belonging to the Glaucidium minutissimum species complex (which also includes G. hardyi) (Marks et al., 1999) occur at low densities in well-preserved forest physiognomies, so there is now very little suitable habitat left for this species in the PCE. However, there are several precedents for the rediscovery of cryptic night birds (e.g., Halleux & Goodman, 1994; King & Rasmussen, 1998) and we encourage observers to keep looking, just in case.

Philydor novaesi Teixeira & Gonzaga, 1983,
Alagoas Foliage-gleaner (IUCN and MMA: CR)

Discovered at Murici, Alagoas in 1979 (Teixeira & Gonzaga, 1983), this species has only ever been found at this type locality and the RPPN Frei Caneca, Pernambuco (Roda, 2008; Roda et al., 2011, Fig. 5). This is one of the most highly sought-after species (by both visiting birders and professional ornithologists alike), and ourselves and others have searched extensively for this species in forest fragments across the PCE (even in forest patches outside of the 'known'altitudinal range) but with no success. Playback of vocalisations of the Alagoas Foliage-gleaner – a nuclear species in mixed-species flocks (acting to aggregate, and orientate other flock members), attracted facultative flock-following heterospecifics (Mazar-Barnett et al., 2005; Roda, 2008; Roda et al., 2011), such as the Long-billed Gnatwren Ramphocaenus melanurus (at Murici and Bonito), Rufous-winged Antwren Herpsilochmus rufimarginatus and White-flanked Antwren Myrmotherula axillaris (at Mata do Estado). We interpret the reaction of these flock-following species as expressing interest in joining a flock and evidence for the historic occurrence of this species at Mata do Estado, EngenhoÁgua Azul, Bonito and Gravatá. This species was last recorded from Murici in 2007 (sound-recording in Minns et al., 2009 and image here: http://ibc.lynxeds.com/photo/alagoas-foliage-gleaner-philydor-novaesi/perched-adult) and last recorded from Frei Caneca in September 2011 (CA, video-recording) despite subsequent intensive searches at both these localities. Along with Pernambuco Pygmy-owl, we consider the Alagoas Foliage-gleaner likely extinct following forest loss, fragmentation and degradation. The disappearance of these species represent the first evidence for extinctions of endemic Brazilian birds in modern times (see Lees et al., 2014a).

 

 

Cichlocolaptes mazarbarnetti
Barnett & Buzzetti, 2014,
Cryptic Treehunter (Not Evaluated)

This recently-described taxon (Mazar-Barnett & Buzzetti, 2014), was formerly confused with the preceding species with which it is cryptically similar but differs subtly in morphology, plumage, behaviour and vocalizations (see also Claramunt, 2014). Like Philydor novaesi it is only known from Murici and RPPN Frei Caneca and was apparently a specialist in foraging in arboreal bromeliads. Mazar-Barnett & Buzzetti (2014) suggest that it should be listed as Critically Endangered both nationally and internationally. Realistically however this species is also likely extinct, there have been no records from other sites in the region and the last records from Frei Caneca were obtained in February 2005 (D. Buzzetti: XC#180936) and the last records from Murici was in April 2007 (D. Buzzetti: XC#180893). The disappearance of these two Furnarids and the Glaucidium pygmy-owl represent the first evidence for extinctions of endemic Brazilian birds in modern times.

Synallaxis infuscata Pinto, 1950,
Pinto's Spinetail (IUCN and MMA: EN)

This PCE endemic is inferred to be in decline due to forest loss and fragmentation (Remsen, 2003) although we found it to be locally common, occupying edge habitats and exhibiting a greater tolerance to habitat fragmentation than other endemic birds in the PCE, potentially warranting a re-evaluation of its status (Fig. 3). Roda et al. (2011) were able to compile records in 53 localities in the PCE. We recorded this species from nine sites in Pernambuco and Paraíba states (Table 2, Fig. 6).

 

 

Automolus lammi Zimmer, 1947,
Pernambuco Foliage-gleaner (Not Evaluated)

Zimmer (2008) advocated splitting this taxon from its putative sister-species, the White-eyed Foliage-gleaner (Automolus leucophthalmus) a change subsequently adopted by the South American Classification Committee (Remsen et al., 2013) which means a formal conservation assessment by the IUCN is due. We consider this species to be globally threatened given that it is only known from 16 localities in Pernambuco, Paraíba and Alagoas (Roda, 2003; Silveira et al., 2003a; Farias et al., 2007) and we present records from five new sites (Table 2). This species was also found south of the São Francisco river, in Sergipe (beyond the PCE as usually delimited) at the Mata do Crasto, in the municipality of Santa Luzia do Itanhy by A. Grosset & J. Minns. It is hoped that the belated recognition of species status for this distinctive taxon may afford it a higher conservation profile (e.g., Mace, 2004).

Myrmotherula snowi Teixeira & Gonzaga, 1985,
Alagoas Antwren (IUCN and MMA: CR)

This species is known from just four disjunct localities: ESEC Murici (Alagoas), RPPN Frei Caneca, Mata do Estado and Engenho Jussará (Pernambuco) (Mazar-Barnett et al., 2005; Roda et al., 2011). There have been no recent records from RPPN Frei Caneca, where the last report concerns a single female photographed in 2007 (WA#92572; 13/12/2007). Despite extensive searching using playback (e.g., at Engenho Jussará, Bonito, Gravatá, Maraial and Brejo dos Cavalos), we were unable to find any additional sites for this species. This species requires urgent conservation intervention to prevent its imminent extinction; less than 30 individuals are thought to survive and the species shares life history traits (such as area sensitivity and obligatory flock-following behaviour) with the Alagoas Foliage-gleaner (see Lees et al., 2014a).

Myrmoderus ruficaudus soror (Pinto, 1940),
Scalloped Antbird (IUCN and MMA: EN)

This species is represented in the PCE by the endemic subspecies M. r. soror, which is confined to humid forests in the states of Paraíba, Pernambuco and Alagoas (Zimmer & Isler, 2003; Grantsau, 2010). This taxon is known in the PCE from 29 localities (Farias et al., 2002; Roda, 2003; Silveira et al., 2003a; Farias et al., 2007, 2010) and currently persists in forest fragments of varying sizes and in varying states of degradation. We recorded this species from an additional four sites in Pernambuco (Table 2).

Terenura sicki Teixeira & Gonzaga, 1983,
Orange-bellied Antwren (IUCN and MMA: EN)

Roda et al. (2011) reported this PCE endemic in 14 forest fragments in upland forest (between 300 and 700 m asl) in the states of Pernambuco and Alagoas. Albano (2009) also reported this species in lowland forest (c. 80 m asl) at Usina Trapiche. We add two new localities in Pernambuco (Table 2, Fig. 7). This species is typically seen accompanying mixed-species flocks: at the Parque Natural Municipal Mucuri-Himalaya it was observed foraging with Veniliornis sp., Sittasomus griseicapillus, Herpsilochmus atricapillus, Phylloscartes ceciliae, Basileuterus culicivorus and Lanio cristatus, and at the Engenho Brejão was observed in a mixed species flock including Myrmotherula axillaris, Herpsilochmus atricapillus and Phylloscartes ceciliae. This species is still recorded with some frequency at the Mata do Estado and Engenho Água Azul (GAP), and six territories were located at the 630 ha RPPN Frei Caneca in November 2012 (ACL: WA#814109, XC#113530; November/2012). It has apparently declined to a handful of pairs (perhaps now a single pair) at the ESEC Murici, Alagoas (Albano 2009, A. Whittaker pers. comm.). The causes of this nearextinction at the latter site are unknown, but given that the ESEC Murici is the largest remaining forest patchin the PCE this is a very worrying trend, and we consider that this species now qualifies for Critically Endangered status based on a total population now estimated at fewer than 250 mature individuals in a few disparate forest fragments.

 

 

Xipholena atropurpurea (Wied, 1820),
White-winged Cotinga (IUCN and MMA: EN)

Restricted to primary lowland and adjacent foothill Atlantic forest (up to 900 m asl), between Paraíba and Rio de Janeiro (Snow, 2004), it has been reported from 13 protected areas (BirdLife International, 2013). This species has been recorded from 25 localities in the PCE between 1961 and 2003 (Roda, 2003). Our fieldwork produced records from an additional four sites in Pernambuco (Table 2, Fig. 8).

 

 

Phylloscartes ceciliae Teixeira, 1987,
Alagoas Tyrannulet (IUCN and MMA: EN)

This PCE endemic is known from 17 localities in the states of Pernambuco and Alagoas (Roda et al., 2011) and was found in just one of 15 fragments inventoried by Silveira et al. (2003a). We found this species in another four sites in Pernambuco (Table 2, Fig. 9). Although still highly imperilled, this species' conservation prospects are slightly brighter than those of the other four 'Murici endemics' – Philydor novaesi, Cichlocolaptes mazarbarnetti, Myrmotherula snowi and Terenura sicki, occurring in more forest patches albeit always at low densities (Fig. 3).

 

 

Tangara fastuosa (lesson, 1831),
Seven-colored Tanager (IUCN and MMA: VU)

Silveira et al. (2003b) summarized the conservation status and distribution of this species. Here, we report 18 additional records across three states (Table 2, Fig. 10). Of the endemic and threatened birds of the PCE, this tanager is among the most tolerant to habitat disturbance, occupying forest edges and orchards where breeding behaviour has been observed (Fig. 3, Silveira et al., 2003b). Capture for the illegal bird trade remains a threat, with individuals traded in illegal street markets around Recife, Pernambuco between June 2000 and June 2005, and between August 2010 and April 2011 (Pereira & Brito, 2005; Regueira & Bernard, 2012).

 

 

Curaeus forbesi (Sclater, 1886),
Forbes Blackbird (IUCN and MMA: EN)

This cryptic and thus often overlooked species has two disjunct populations, one found in the PCE and the other in the state of Minas Gerais, south-east Brazil (Jaramillo & Burke, 1999; Fraga, 2011; Mazzoni et al., 2012). Here, we report records from a further 13 sites in Pernambuco (Table 2, Fig. 11). The observation in Escada, Pernambuco involved a flock forag-ing in association with Molothrus bonariensis. Nests of Curaeus forbesi are parasitised by Molothrus bonariensis which may represent cause declines in anthropogenic landscapes with elevated cowbird densities (Jaramillo & Burke, 1999; Fraga, 2011) but this behaviour has yet to be recorded in the PCE. The pre-Columbian habitat of Forbe's Blackird in PCE is not known. Most of our records came from forest edges associated with sugar cane plantations, with many nests were found in mango trees, near houses. Autecological studies are needed to understand the ecology of this species in anthropogenic landscapes.

 

 

Sporagra yarrellii (Audubon, 1839),
Yellow-faced Siskin (IUCN and MMA: EN)

Formerly widespread in north-eastern Brazil, now all populations are very reduced and fragmented following decades of intense illegal trapping (Fernandes-Ferreira et al., 2012). Here, we found this species in seven new sites in Pernambuco (Table 2). This species is still often encountered for sale in some places in north-east Brazil.

 

DISCUSSION

Our surveys produced many additional records of globally threatened bird species. We reveal that the conservation situation for some poorly known species such as Leptodon forbesi and Synallaxis infuscata is more positive than previously thought, given their apparent higher tolerance to habitat loss and disturbance (Fig. 3). However, the situation for most threatened species is very bleak; for example, we failed to find new records or localities for Philydor novaesi, Cichlocolaptes mazarbarnetti and Glaucidium mooreorum, which may be globally extinct. Many other species such as the Alagoas Antwren Myrmotherula snowi are in precipitous decline and their continued survival is dependent on immediate conservation intervention, if is not already too late. Fragment size (Fig. 2) was a strong predictor of threatened species richness in forest fragments of the PCE (even considering variable survey effort between fragments), reinforcing the need to protect all large forest remnants. This species-area relationship was likely mediated by significant unmeasured variation in habitat quality, with logged, burned and secondary forest patches likely harbouring fewer threatened species (e.g., Moura et al., 2013). However, it is also likely that variation in occupancy in some of the larger forest patches with low threatened species richness may reflect Pre-Columbian differences in distribution patterns; for which several of the patches in the north of the region may lie outside of their respective bioclimatic distributional envelopes.

Declines and local extinctions of many guilds (Silveira et al., 2003a) even in protected areas (e.g., ESEC Murici) indicate that these remaining forest fragments may now be suboptimal for these species following changes to the biophysical characteristics of the fragments themselves. Small forest patches are especially vulnerable to fire, especially after selective logging events and this sensitivity is exacerbated by climatic edge effects such as exposure to drying winds, which may result in tree and bromeliad mortality (Siqueira-Filho & Tabarelli, 2006; Loarie et al., 2011).

Proposed conservation actions

1) Consolidate existing fragments into larger blocks

The largest remaining forest patches as ESEC Murici are likely too small to hold viable populations of many species in the long-term, and even fragments as large as 10,000 ha are expected to owe extinction debts in the long-term (e.g., Ferraz et al., 2003; Lees & Peres, 2008b). Land purchases for afforestation with native tree communities (by governments or major NGOs) should be directed at areas buffering existing large fragments, perhaps within the remit of the Project for the Conservation and Sustainable Use of Brazilian Biological Diversity (PROBIO, see Tabarelli et al., 2005). The resultant secondary forests will dampen edge effects on existing primary forest remnants and eventually facilitate inter-patch movements for species (such as small insectivorous passerines) behaviourally reticent or physically incapable of crossing extensive sugar cane plantations (Moore et al., 2008; Lees & Peres 2009).

2) Conferral of legal protection on existing large unprotected forest fragments

Many of the largest fragments in the region (e.g., around Bonito, Pernambuco) have no legal protection and efforts should be maintained to at least achieve private legal reserve (RPPN: Reserva Particulare do Patrimônio Natural) status for these areas. Landowner benefits could also include additional income from responsible ecotourism (Şekercioğlu, 2002) or participation in REDD+ carbon-trading schemes prioritising biodiversity (Gardner et al., 2011).

3) Ensuring private landholder compliance with the Brazilian Forest Code

Fulfilment of existing Brazilian Forest Code requirements, which will require effective law enforcement, is needed to ensure that streams are buffered by the requisite minimum amount of riparian forest (APPs) and that existing legal reserve (RL) requirements are met. This would increase the size of and connectivity between existing forest patches and facilitate rescue effects in small patches (Alger & Lima, 2003; Lees & Peres, 2008a).

4) Consider captive breeding programs for critically endangered species

For species such as Myrmotherula snowi, extreme ex-situ conservation measures such as captive breeding may have to be considered (see e.g., Groombridge et al., 2004; Lees et al., 2014a). Existing populations may become extinct with one or two decades without intervention and are unlikely to persist long-enough to benefit from the effects of any (hypothetical) reforestation plans. However, there are few precedents for the animal husbandry and captive breeding of suboscine passerines (although see Touchton et al., 2014), so appropriate 'practice' species (e.g., Myrmotherula axillaris as a surrogate for M. snowi) should be selected first to assess the viability of such an approach before the lives of individuals of the rarer species are risked.

5) Survey any remaining un-surveyed forest patches and consider the merit of translocation of 'stranded' individuals of rare species to larger patches

Not all patches within the PCE have been surveyed, and their remains the chance that individuals of species of high conservation priority may still be found in relatively small forest patches for which long term population survival is inviable. If this is the case then translocation of individuals to larger forest patches may be desirable to maintain genetic diversity of such populations (e.g., VanderWerf et al., 2006).

 

CONCLUSION

Without significant, government and NGO action, we anticipate imminent extinctions of more threatened endemic birds from the PCE and the reduction of the regional forest avifaunal poor to a handful of disturbance and fragmentation-tolerant species. These extinctions will also likely include a number of PCE endemic subspecies, many of which may be the subject of future taxonomic upgrades e.g., Xiphorhynchus (fuscus) atlanticus (already split by the CBRO, 2011).

 

ACKNOWLEGEMENTS

We thank the Centro de Pesquisas Ambientais do Nordeste and Fundação O Boticário de Proteção a Natureza for supporting some of our expeditions in the PCE (GAP, MCP and SAR). We thank all collaborating private landowners and local government officials for their support and members of the Observadores de Aves de Pernambuco (OAP) for help in the field. LFS and ACL are supported by CNPq (the latter by a Bolsa Jovem Talento). We thank Marco Antônio Rego for producing the map, Edson Endrigo and Airton Cruz for the help with the images, Bruno Ehlers for the constant support and Galileu Coelho, Jeremy Minns and Arthur Grosset for kindly sharing their records.

 

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Aceito em: 21/07/2014
Publicado em: 31/07/2014

 

 

APPENDIX

Additional references used to construct species by site matrix.

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Collar, N.J.; Gonzaga, L.P.; Krabbe, N.; Madroño-Nieto, A.; Naranjo, L.G.; Parker, T.A. & Wege, D.C. 2000. Aves amenazadas de las Americas (Libro Rojo de CIPA/UICN). Quito, BirdLife International.

Collar, N.J.; Wege, D.C. & Long, A.J. 1997. Patterns and causes of endangerment in the new world avifauna. Ornithological Monographs, 48: 237-260.

Daher, M.R.M.; Pereira, G.A.; Leal, S.R.M. & Souza, D.S. 2013. Aves. In: Bagetti, W.S. (Org.). Restauração do Rio Coruripe: um projeto de resgate socioambiental. Maceió, Graziella Helena Fritscher. p. 79-115.

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Leal, S. 2010. Guia das Aves do Parque Municipal de Maceió. Maceió, Poligraf.

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