Pernambuco Endemism Center Research Articles

Endemic and threatened birds as surrogates for identifying conservation priority areas and ecological corridors in the America’s most endangered habitat

Investigating multi-taxa macroecological patterns can provide critical insights for spatial conservation planning and landscape management across biodiversity hotspots. The Pernambuco Endemism Center (PEC) is a biogeographic region of the Brazilian Atlantic Forest known to harbor the most threatened habitats in the Americas and a considerable number of recent bird extinctions. Here, we modeled the distribution of 30 threatened forest-dependent birds, 29 of which endemic to the PEC, to reveal key habitats/resources for their survival, identify conservation priority areas, and design ecological corridors. We found variations in the responses of the taxa to landscape characteristics when we addressed these organisms separately and when we grouped them by conservation status. Overall, the environmental variables related to forest quality (e.g., distance to large fragments, distance to the forest edge, percentage of tree cover, percentage of older forests) were important predictors of habitat suitability for the regional threatened avifauna. Additionally, we revealed forest fragments of high ecological importance for the PEC’s threatened birds, and we propose the creation of the Pernambuco Endemism Center Restoration Arc (PEC-ARC) that may maximize the investments in conservation and guarantee the connectivity of crucial areas for long-term species survival.

Minor loss or huge threat? Assessment of potential infrastructure projects reveals drastic landscape degradation in the Atlantic forest

Projects demanding deforestation to expand urban infrastructure and road networks put pressure on the Atlantic Forest − a hyper-fragmented global conservation hotspot known for its high biodiversity and endemism. To support decision-making, we applied a scientific approach to analyse the immediate and long-term impacts of two major planned projects in the most threatened Atlantic Forest region – the Pernambuco Endemism Center, a crucial area for the survival of many endemic species. A Metropolitan Road Arch and a Training School for Career Sergeants are expected in the Environmental Protection Area Aldeia-Beberibe (31,634 ha) in the next few years. The area has 198 protected forest remnants, including one larger than 10,000 ha. Our analysis shows that the projects’ implementation may deforest 189 ha, increase fragment number by 3.5 % and decrease the average patch area by 4 %. The largest fragment will be divided into two. We may lose 335,307 trees and 44,655.59 Mg of carbon. Approximately 112.67 ha of watershed protection will be damaged. Thus, in the medium to long term, habitat quality will worsen, and the probability of connectivity will decrease, restricting forest-dependent species’ mobility considerably. To date, alternative areas have been proposed in meetings, working groups, and environmental advisory bodies for the analysed projects.We strongly oppose further deforestation and suggest that science-based approaches must be immediately considered for any project that requires forest suppression in highly fragmented landscapes. This is crucial to mitigate the alarming scenarios of extreme climate and biodiversity loss that we are currently witnessing in Brazil and worldwide.

Mammal surveys and vertical strata use in an Atlantic Forest patch in the Pernambuco Endemism Center, Northeastern Brazil

Surveys are a key tool for the assessment of conservation strategies. We evaluated the relative abundance and vertical strata used by mammals in an Atlantic Forest patch in Igarassu (PE), Northeastern Brazil. We walked a total of 145.25 km on transects from December 2018 to June 2019, recording 105 sightings of eight species. Callithrix jacchus presented the highest relative abundance and Cuniculus paca the lowest. There was variation in the forest strata used by mammals. The records of rare and large-bodied mammals indicate the importance of this area for the maintenance of the mammalian fauna of the Pernambuco Endemism Center.

Massive Bird Nest Losses: A Neglected Threat for Passerine Birds in Atlantic Forest Fragments from the Pernambuco Endemism Center

Understanding the mechanisms by which tropical forest fragmentation can affect the persistence of species and populations is of scientific and practical interest. However, nest survival has been one the least addressed of the potentially harmful effects associated with habitat fragmentation, and studies involving nest predator’s identification are still underdeveloped. The Pernambuco Endemism Center (PEC) is the part of the Atlantic Forest located north of the São Francisco River, in northeastern Brazil, where large forest tracts no longer exist and a wave of bird extinctions has occurred recently. Here, we investigated the nest survival of forest understory birds from three PEC fragments (690, 979, and 1036 ha), and we used infra-red camera traps for predators’ identification. Overall, the apparent nest survival was 15.5%, and nest-day-based survival probability for the four more representative species (including two endemic and threatened taxa) were 2.6, 4.4, 6.9, and 18.9%, being 2.7 to 8.5 times smaller than populations or related taxa from the Atlantic Forest of southeastern Brazil. Predators were marmosets (25%), opossums (25%), tegu (19.4%), coati (16.7%), snakes (8.3%), and hawks (5.5%). Jackknife2 model-predicted nest predator’s richness was 20.7 (SD = 1.6). We reinforce the evidence that nest predation associated with fragmentation can affect negatively the bird populations from tropical forests.

First record of Dermanura gnoma for the threatened Pernambuco Endemism Center, northern Atlantic Forest, with phylogenetic insights.

Dermanura gnoma (Handley, 1987) is a phyllostomid bat that occurs in South America. In Brazil, most of the records are concentrated in the Amazon Forest, with sparse data from Cerrado and Atlantic Forest. This study presents the first record of D. gnoma for Alagoas state, and for the Pernambuco Endemism Center (PEC), the most threatened region of the Brazilian Atlantic Forest, characterized by its high rate of endemism, habitat loss, and fragmentation. The species was surveyed at Murici Ecological Station and its identification was supported by morphological and molecular data. We provide the first COI and CYTB gene sequences for this species in the entire Atlantic Forest. Phylogenetic analyses reveal that the generated sequences were recovered in the same clade as the published sequences of D. gnoma from the Amazonian Forest, corroborating the disjunct distribution pattern between Amazonia and PEC, as already reported for other vertebrate taxa. Also, this record increases the number of bat species to 71 for the PEC and extends the geographic distribution of D. gnoma by 758 kilometers to the northeast of its range.

Spatiotemporal dynamics reveals forest rejuvenation, fragmentation, and edge effects in an Atlantic Forest hotspot, the Pernambuco Endemism Center, northeastern Brazil.

Large forested tracts are increasingly rare in the tropics, where conservation managers are often presented with the challenge of preserving biodiversity in small and isolated fragments. The Atlantic Forest is one of the world's most important biodiversity hotspots, jeopardized by habitat loss and fragmentation. The Pernambuco Endemism Center (PEC) is the most degraded of the Atlantic Forest regions and because of the dramatic levels of deforestation, fragmentation, and ongoing species losses, studies on the distribution and configuration of the PEC's forest cover are necessary. However, across dynamic tropical landscapes, investigating changes over time is essential because it may reveal trends in forest quality attributes. Here, we used Google Earth Engine to assess land use and land cover data from MapBiomas ranging from 1985 to 2020 to calculate current landscape metrics and to reveal for the first time the spatiotemporal dynamics of the PEC's forests. We identified a forest cover area that ranged from 571,661 ha in 1985 to 539,877 ha in 2020, and about 90% of the fragments were smaller than 10 ha. The average fragment size was about 11 ha, and only four fragments had more than 5,000 ha. Deforestation was mostly concentrated in northern Alagoas, southern Pernambuco, and non-coastal Paraíba and Rio Grande do Norte. On average, borders represented 53.6% of the forests from 1985 to 2020, and younger forests covered 52.3% of the area in 2017, revealing a vegetation rejuvenation process 2.5 times higher than in total Atlantic Forest. In 2017, older forest cores in fragments larger than 1000 ha (i.e., higher-quality habitats) represented only 12% of the remaining forests. We recommend that the amount of forest cover alone may poorly assist conservation managers, and our results indicate that ensuring legal protection and increasing surveillance of the PEC's few last higher-quality habitats is urgently needed.

AVIFAUNA OF THE ECOTOURISM PARK CACHOEIRA DO URUBU: A FRAGMENT OF ATLANTIC FOREST IN THE PERNAMBUCO ENDEMISM CENTER, NORTHEASTERN BRAZIL

The forest fragments that persist within a landscape formed by sugarcane matrix are fundamental for the faunal maintenance. Here, we present the list of bird species found in the Ecotourism Park Cachoeira do Urubu (PECUB), an Atlantic Forest fragment inserted in a landscape consisted by a sugarcane matrix in northeastern Brazil. Our consolidated list includes 117 bird species, of which 106 were recorded during our systematic surveys and other 11 species from a preliminary survey and an online database. When compared to larger fragments located in the same region (Atlantic Forest of Pernambuco), PECUB stands out for its species richness in such a small area (30 ha), with just over 40% of the number of species found in fragments 20 times larger, such as Dois Irmãos State Park. PECUB has three endemic taxa to the Pernambuco Endemism Center ( Picumnus pernambucensis , Hemitriccus griseipectus naumburgae , and Tangara cyanocephala corallina ) and one endemic to the Atlantic Forest ( Chrysuronia leucogaster bahiae ). Our study demonstrated the importance of PECUB as a suitable habitat for birds in a region threatened by forest fragmentation.

Estimativas de densidade populacional em três táxons de aves ameaçados de extinção do Centro de Endemismo Pernambuco, nordeste do Brasil

Abstract Determining the relative risks of extinction of declining taxa is important to delineate conservation priorities and to guide the investments in conservation. Brazil concentrates the greatest number of endangered avian taxa on Earth, yet demographic information is lacking for most of them. Here we present distance-sampling population density estimates for three endangered bird taxa endemic to the Pernambuco Endemism Center (PEC), the most critically disturbed Atlantic Forest region. The analyzed taxa were the White-shouldered Antshrike Thamnophilus aetiops distans (Endangered), the Brown-winged Mourner Schiffornis turdina intermedia (Vulnerable), and the White-bellied Tody-tyrant Hemitriccus griseipectus naumburgae (Vulnerable). The estimated numbers of individuals/ha in an approximately 1,000 ha forest fragment were 0.21, 0.14, and 0.73, respectively. Our findings corroborated the premise that even taxa classified in similar threat categories based on habitat characteristics alone can have different population densities and consequently, divergent risks of extinction. Although population densities can vary among fragments, the extrapolation of our data to the whole PEC confirmed the Vulnerable status of the Brown-winged Mourner, and indicated the Vulnerable and Least Concern categories for the White-shouldered Antshrike and for the White-bellied Tody-tyrant, suggesting that for the two later taxa, the current classifications (Endangered and Vulnerable) based on their Areas of Occupancy must prevail.

The snake fauna of the most threatened region of the Atlantic Forest: natural history, distribution, species richness and a complement to the Atlas of Brazilian Snakes

The Atlantic Forest is one of the richest tropical forests in the world, with a high endemism rate of vertebrates, including several snakes. The snake fauna of the Atlantic Forest is rich and complex, presenting differences in fauna composition along its extension. The existence of at least four endemism centers along this forest is well documented and supported by data of vertebrates, invertebrates and plants. The Pernambuco Endemism Center (PEC) is the most septentrional region of the Atlantic Forest, and it contacts areas with transitional forests and arid landscapes (Caatinga) which along with altitudinal variation enable a unique snake fauna for this region. In this study we provide: (i) an updated list of species, detailed information about natural history, as well as a detailed geographic distribution for all species recorded in the PEC; (ii) a comparison between the snake fauna of the PEC with other regions of the Atlantic Forest. The snake fauna of the PEC is composed by 86 species of 8 families. The results showed that most of the species recorded in the PEC are distributed close to the coast, probably due to the proximity of the research centers, but also due to the present distribution of the remnants close to the coast. The forest remnants in the highlands (Brejos de Altitude) harbors a high diversity of species with high similarity with the coastal forests. We found a strong separation between the snake fauna of assemblages located in southwestern and northeastern Brazil, indicating clear characteristics of the snake fauna of the PEC.

New record of Ocelot, Leopardus pardalis (Linnaeus, 1758) (Felidae), in an Atlantic Forest fragment in the Pernambuco Endemism Center, northeastern Brazil

The Pernambuco Endemism Center is a key region for the maintenance of biodiversity of the Brazilian Atlantic Forest. Inventories of the medium-sized terrestrial mammals in this region are scarce, and several information gaps still remain. We conducted a camera trap survey at the Tapacurá Ecological Station, São Lourenço da Mata, Pernambuco. We obtained new records of at least four females and three male individuals of Ocelot, Leopardus pardalis (Linnaeus, 1758). The records provide important data about occurrence and distribution of a threatened population of this mesocarnivore in northeastern Brazil.

Environmental heterogeneity and sampling relevance areas in an Atlantic forest endemism region

The knowledge of the diversity, richness, and distribution of tropical organisms are poorly understood, and a plethora of new species are still being described even among groups considered well-known. As a result, this inadequate knowledge of the biodiversity has hampered the species’ conservation. Thus, sampling efforts must be urgently optimized to survey important and unique areas and to better allocated the scarce conservation resources, especially in the tropical and developing countries that harbor much of the world biodiversity. We assessed the most relevant regions in terms of environmental dissimilarity for sampling vertebrates (amphibians, birds, and mammals) in the Pernambuco Endemism Center (PEC), located in Atlantic forest and the most threatened region in South America, where only about 1% of remaining forests are protected. We found that 8–41% of the PEC areas showed high sampling relevance for all vertebrate groups, with the non-coastal areas of the PEC presenting the highest sampling relevance in terms of environmental dissimilarity. For all vertebrate groups, the sites with the highest sampling relevance are threatened by fragmentation, and sampling efforts must be allocated to these areas before they are totally converted into human-modified landscapes.

A New Species of the Genus Adelophryne (Anura: Eleutherodactylidae: Phyzelaphryninae) from the Atlantic Forest of Northeastern Brazil

Species in the Adelophryne genus consist of diminutive, agile, and secretive frogs that inhabit forest leaf litter and have direct development. Species richness within Adelophryne was previously underestimated, and several new species have recently been described. Here, we describe a new species of Adelophryne from the Atlantic Forest in the Brazilian states of Alagoas, Pernambuco, and Paraiba. The new species is characterized by its small body size, small and distinct tympanum, toes with subarticular tubercles, fingers mucronate, three phalanges in the Finger IV, and an advertisement call composed of one single pulsed note with a high dominant frequency. The new species is phylogenetically related to other Adelophryne species of the Northern Atlantic Forest Clade and is endemic to the “Pernambuco Endemism Center” in the Atlantic Forest biodiversity hotspot.

Foraging behavior and association with mixed flocks by the Critically Endangered Alagoas Tyrannulet Phylloscartes ceciliae (Aves: Passeriformes: Tyrannidae)

The Alagoas Tyrannulet Phylloscartes ceciliae is a Critically Endangered species with a restricted distribution to the Atlantic Forest of the Pernambuco Endemism Center. It seems to specialize in using the sally-strike maneuver (68.85%) to catch prey on green foliage (50.82%) and in the air (34.42%). We calculated a catch rate of 2.93 catches/minute, identified a new food item for this species (caterpillars), and included 12 species in the list of birds recorded in mixed flocks with the species. Our results show that majority of the prey capture events by Alagoas Tyrannulet occurred inside tree canopies, thus we can infer that this species needs a more advanced stage of forest sucession, with higher trees, emphasizing the urgency for restoration programs in the region.

New records of two cladoceran species (Branchiopoda: Anomopoda) from Northeastern Brazil: the importance of studies in temporary ponds

Abstract Temporary ponds are heterogeneous aquatic environments, in which hydrodynamics and richness of macrophytes may increase the diversity of zooplankton and other invertebrate communities. Cladocerans are common residents of these ecosystems, showing great variability of forms. During a faunistic survey in temporary ponds under the influence of riparian vegetation, in the Camucim Forest Protected Area, Pernambuco Endemism Center, Brazil, the cladocerans Moina dumonti Kotov, Elias-Gutierrez and Granado-Ramirez, 2005 and Chydorus nitidulus (Sars, 1901) were found. These are their first records in the Oriental Northeast Atlantic hydrographic region, and the second record of M. dumonti in Brazil. The present study raises Cladocera species richness in Pernambuco State to 73 and also 16 in the Pernambuco Endemism Center.

Lizards and snakes of Refúgio de Vida Silvestre Matas do Siriji, an Atlantic Forest hotspot of the Pernambuco Endemism Center, Northeastern Brazil

Abstract: The Atlantic Forest north of the São Francisco River, known as the Pernambuco Endemism Center (PEC), comprises small, poorly-known and, consequently, highly threatened forest remnants, such as Refúgio de Vida Silvestre (RVS) Matas do Siriji, a montane forest located in the municipality of São Vicente Férrer, state of Pernambuco, Northeast Brazil. We provide the results of the first inventory of the squamate fauna of the region with comments on the conservation status of some species, comparisons with other locations in Northeast Brazil and a brief discussion of biogeography. Time-constrained transects, pit-fall traps, occasional encounters and third-party records registered 18 lizard species and 25 snake species, with the rarefaction curve of the former tending to stability. The RVS Matas do Siriji possesses 39.81 % of the lizard and snake species known for the state of de Pernambuco, being the third richest area in species in the State, with a composition similar to that of other areas within PEC. Based on the lists of SEMAS, ICMBio and IUCN, some of the registered species are considered vulnerable to extinction while others have yet to be evaluated. The RVS Matas do Siriji includes a rich, threatened and underestimated fauna of squamate reptiles, indicating that more restrictive protection measures must be adopted in this Conservation Unit.

Snakes of the Pernambuco Endemism Center, Brazil: diversity, natural history and conservation.

The Atlantic Forest is one of the largest and richest tropical rainforests on the planet, being one of the 25 world priorities for conservation. The Atlantic Forest portion located north of the São Francisco River corresponds to the Pernambuco Endemism Center (PEC). We describe the snake composition of the PEC, providing information about the diversity, natural history and geographical distribution of the species, based on records from five scientific collections and additional information from the literature. A total of 78 species of snakes distributed in eight families was registered in the Pernambuco Endemism Center. The Caatinga is the Brazilian biome that most shares species with the PEC, followed by Cerrado. On the other hand, seven species are considered endemic of this region. Most of the snake species in the PEC have been registered in forest (94.8%), followed by “Brejos Nordestinos” (46.1%), Tabuleiros (43.5%), Restingas (14.1%) and Mangroves (5.1%). The PEC snake fauna includes mainly terrestrial species (60.2%) and cryptozoic and/or fossorial species (21.7%), but also presents a high richness of semi-arboreal and arboreal species (29.5%). Vertebrates are the main food item consumed by the species (78% of species), among the main prey are mammals, lizards, and amphibians. Most species show a strictly nocturnal activity period (50%), followed by strictly diurnal (38%). The PEC is the most degraded and least known region of the Atlantic Forest, yet it has revealed a high richness of snake species, including seven endemic species. It is emphasized that regional conservation efforts need to be intensified, because few forests in the region are formally protected, and the majority consist of small and poorly protected fragments, which means that many species in the region may be in risk of extinction.

The advertisement call of Physalaemus caete Pombal & Madureira, 1997 (Anura: Leptodactylidae: Leiuperinae), an endangered species endemic to Brazil’s northern Atlantic Forest

Foam-nesting frogs of the genus Physalaemus Fitzinger, 1826 have been long known for their diverse acoustic patterns (e.g., Barrio 1965; Bokermann 1966). Of the 49 species, the vocalizations of only three remain unknown to date (see Table 1 of Hepp Pombal 2020): P. caete Pombal Madureira, 1997, P. deimaticus Sazima Caramaschi, 1988, and P. insperatus Cruz, Cassini Caramaschi, 2008. Physalaemus caete is rare and narrowly distributed in Brazil's northern Atlantic Forest (Santos et al. 2016; Bernardo et al. 2017; Haddad et al. 2018), and an explosive breeder (EMS pers. obs.). For those reasons the species is classified in the endangered category of Brazil's red list of threatened species (ICMBio, 2018). Physalaemus caete was described in the late 1990s from the coastal region of the Brazilian state of Alagoas (Passo do Camaragibe) and reported for a second locality in Alagoas (Murici; Pombal Madureira 1997). Recently, the distribution was extended to a third locality (Paulista, state of Pernambuco; Santos et al. 2016). The distribution range of P. caete coincides with the "Pernambuco endemism center", a biogeographic subregion of coastal Atlantic Forest north of the São Francisco River (sensu Silva Casteli 2003). Here we describe the advertisement call of the Pernambuco population of P. caete and make comparisons with calls of congeners.

State of knowledge and conservation of the snake fauna of the “Brejos de Altitude” in the Pernambuco Endemism Center, Northeastern Brazil

The Atlantic Forest is originally distributed along the Brazilian coast from the states of Rio Grande do Norte to Rio Grande do Sul, and it presents many different vegetal physiognomies. Brejos de Altitude is a set of relict altitudinal forests in northeastern Brazil with a distinct and poorly studied biota representing special areas within the Atlantic Forest. The snake fauna of these forests is still poorly understood despite the increasing amount of information available. The aim of this study was to furnish the current state of knowledge and conservation of the snake fauna at the Brejos in the Pernambuco Endemism Center. The database used here is based on the materials housed at Museu de Zoologia da Universidade de Sao Paulo and the herpetological collections of Universidade Federal da Paraiba and Universidade Federal Rural de Pernambuco, in addition to literature records. Out of 7 families, 37 genera and 63 species were found in Brejos de Altitude, and no species appeared in the list of endangered fauna of Brazil. The results showed species with strong dependence on forest and species distributed in open areas, such as Caatinga and Cerrado, although, many Brejos showed no data on snake fauna. In conclusion, Brejos de Altitude is a threatened region of the Atlantic Forest with a small number of protected areas and high rates of deforestation, thus needing urgent conservation actions.

Reconsidering mammal extinctions in the Pernambuco Endemism Center of the Brazilian Atlantic Forest: a critique

espanolSe ha calculado que, en los ultimos 500 anos, se han extinguido 21 mamiferos en el Centro de Endemismo Pernambuco. En el presente estudio, realizamos un examen critico de los datos aportados en las publicaciones cientificas historicas y recientes, y concluimos que el numero real de mamiferos extintos es de siete, lo que indica que la cifra anterior de 21 especies extintas es una sobrestimacion de aproximadamente 30%. Nuestra lista difiere de las publicaciones previas en que incluye especies aun existentes (n = 5) y excluye otras que nunca habian sido registradas en el Centro de Endemismo Pernambuco (n = 8). Asimismo, senalamos que, al elaborar listas de fauna extinta a escala regional, es necesario adoptar un planteamiento mas riguroso en relacion con los registros historicos y recientes, dado que las identificaciones erroneas y las suposiciones falsas podrian conducir a la perdida de credibilidad ante las partes interesadas y, en ultima instancia, ser negativas para la conservacion de especies. EnglishIn the last 500 years, there have been an estimated 21 mammal extinctions in the Pernambuco Endemism Center. We critically reviewed the published historical and recent literature records and concluded that the actual number of mammal species extinction was seven, indicating that the previous figure of 21 species lost is an overestimation of approximately 30%. Our checklist differs from previous publications by including species that are still extant (n = 5), and removing species that have never been recorded in the Pernambuco Endemism Center (n = 8). We point out that a more rigorous approach towards historical and recent records is needed when producing lists of regionally extinct fauna, given that the implications of misidentifications and false assumptions can potentially lead to loss of credibility by stakeholders and ultimately have a negative effect on species conservation.

Recording of relict ocelot (Leopardus pardalis) and South American coati (Nasua nasua) populations in the biodiversity hotspot Pernambuco Endemism Center, Northern Atlantic Forest, Brazil

Abstract The northern portion of the Atlantic Forest, namely Pernambuco Endemism Center (PEC), faces an extreme level of forest loss, with only 2% of its original forest remaining. In the PEC, mesocarnivores are the only remaining carnivores and, among them, the ocelot and South American coati present a poorly known or even ignored distribution. Our goal is to provide an overview of the current distribution and conservation status of both species in the PEC through camera trap survey, review of published scientific literature and a search for voucher specimens in mammal collections. Our data confirm the presence of the ocelot and the South America coati in the PEC. The ocelots were mainly recorded in fragments smaller than 12 km2, suggesting they might access the monoculture matrix and anthropogenic areas. The few recent records of coatis suggest a worse scenario, predicting an imminent local extinction. The PEC has witnessed a historical continued deforestation, which has reduced the remaining fragments and contributed to the accentuated decline of both species populations. Nevertheless, these Atlantic Forest remnants are paramount to supporting relict populations of mesocarnivores in the PEC, and their maintenance and connectivity should be a conservation priority.