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Gentil Alves Pereira Filho
Frederico Gustavo Rodrigues França
Rômulo Romeu Nóbrega Alves · Alexandre Vasconcellos
Editors

Animal Biodiversity
and Conservation
in Brazil’s Northern
Atlantic Forest
 Composition, Species Richness,
and Conservation of the Reptiles 11
of the Highly Threatened Northern
Brazilian Atlantic Forest

Gentil Alves Pereira Filho, Thais Barreto Guedes,
Rafaela Candido de França, Marco Antônio de Freitas,
Ricardo Lourenço-de-Moraes, Daniel Oliveira Mesquita,
Pedro Murilo Sales Nunes, Fagner Ribeiro Delfim,
Marcos Jorge Matias Dubeux,
and Frederico Gustavo Rodrigues França

Abstract
The northern Brazilian Atlantic Forest comprising the
states of Alagoas, Pernambuco, Paraíba, and Rio Grande
do Norte is considered a distinct biogeographic unity, also
known as Pernambuco Endemism Center (PEC). This
unique area harbors a high biodiversity with threatened,
rare, and endemic species and is considered of high rele-
vance for the preservation of the whole biome. In this
chapter, we present for the first time a complete list of all
reptile species found in PEC, composed by 6 species of
amphisbaenians, 38 lizards (3 endemics), 88 snakes (7
endemics), 5 chelonians, and 2 crocodilians. The numbers
can be considered high but can increase once many areas
remain unexplored. We also present beta diversity analy-
ses showing that the south of Pernambuco and Alagoas
state are the richest regions; on the other hand, the north
of Rio Grande do Norte presents low numbers of species
and can be considered the poorest area. A possible expla-
nation for these differences in richness and species com-
position possibly relies on floristic distinctiveness and
differences in the moisture along the area. We also
detected the insufficient number of conservation units in
PEC denoting a worrying panorama for the most threat-
ened sector of the entire Atlantic Forest. Conservation
measures combined with scientific research are urgent to
protect such unique and important forests.
Keywords
Herpetofauna · Endemic species · Habitat loss · Protected
areas

G. A. P. Filho (*)
Departamento de Biologia, Universidade Estadual da Paraíba,
Campina Grande, Paraíba, Brazil
T. B. Guedes
Centro de Estudos Superiores de Caxias, Universidade Estadual do
Maranhão, Caxias, MA, Brazil
Department of Biological and Environmental Sciences,
Gothenburg Global Biodiversity Center, University of Gothenburg,
Göteborg, Sweden
R. C. de França
Programa de Pós-graduação em Ecologia e Conservação da
Biodiversidade, Universidade Estadual de Santa Cruz,
Ilhéus, Bahia, Brazil
M. A. de Freitas
Instituto Chico Mendes de Conservação da Biodiversidade
(ICMBIO), ESEC Murici, Murici, Alagoas, Brazil
R. Lourenço-de-Moraes · F. G. R. França
Programa de Pós-Graduação em Ecologia e Monitoramento
Ambiental (PPGEMA), Universidade Federal da Paraíba,
Rio Tinto, Paraiba, Brazil
D. O. Mesquita · F. R. Delfim
Departamento de Sistemática e Ecologia, Centro de Ciências
Exatas e da Natureza, Universidade Federal da Paraíba,
João Pessoa, Paraíba, Brazil
P. M. S. Nunes
Laboratório de Herpetologia, Departamento de Zoologia, Centro
de Biociências, Universidade Federal de Pernambuco,
Recife, Brazil
M. J. M. Dubeux
Programa de Pós-Gradução em Biologia Animal, Departamento de
Zoologia, Centro de Biociências, Universidade Federal de
Pernambuco, Recife, Pernambuco, Brazil

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 169
G. A. Pereira Filho et al. (eds.), Animal Biodiversity and Conservation in Brazil’s Northern Atlantic Forest,
https://doi.org/10.1007/978-3-031-21287-1_11
170
11.1 Introduction
The Atlantic northernmost Brazilian Atlantic Forest, also
known as the Forest of the Pernambuco Endemism Center
(PEC), is distributed in the states of Alagoas, Pernambuco,
Paraíba, and Rio Grande do Norte, comprehending coastal
fragments and inland forests (“Brejos de Altitude”) (Tabarelli
and Santos 2004). These forests harbor a huge reptile diver-
sity, and even with the increasing of researches being devel-
oped in the area, the discovery of new species has become
more often in the last decades (e.g., Freire 1999; Ferrarezzi
and Freire 2001; Passos et  al. 2010; Freire et  al. 2010;
Gonçalves et al. 2012; Pires et al. 2014; Graboski et al. 2015;
Montingelli et al. 2020). Despite the discovery of new spe-
cies, there is a lack of information about the composition of
reptile species in the PEC. The herpetofaunistic inventories
and studies on reptile diversity in this specific area of the
northeastern Atlantic Forest are still scanty with many gaps
of knowledge and several regions without any zoological
information.
The first data about the reptile fauna of the region nowa-
days recognized as PEC comes from a historical source.
During the 1600s, the Dutch naturalist Guilherme Piso in his
historical compendium, Historia Naturalis Brasiliae (1648),
with additional information of the German naturalist George
Marcgrave, traveled by the northeast Brazilian states of
Alagoas, Pernambuco, Paraíba, Rio Grande do Norte, and
Ceará, making natural observations about the fauna of the
Atlantic Forest and Caatinga. Some snakes such as
“Surucucu” (Lachesis muta), “Caninana” (Spilotes pullatus),
and “Ibiboboca” (Micrurus ibiboboca) are mentioned,
together with other reptiles such as the lizards “Iguana”
(Iguana iguana), the “Teiú” (Salvator merianae), and
“Caimans” (probably Caiman latirostris).
The main reason for the lack of information about the rep-
tile fauna of the PEC probably was the absence, until the
2000s, of professional herpetologists working in the univer-
sities in most states of northeast Brazil. This panorama is
completely changed nowadays, with well-developed research
centers in all states. More than 100 papers have been pub-
lished about the reptiles of PEC, emphasizing many aspects
such as taxonomy, ecology, biogeography, and conservation.
However, considering the reptile surveys (the mains focus
herein), the literature is still scarce, and the geographical
coverage is insufficient. The first reptile surveys conducted
in the PEC region were coordinated by Dr. Eliza Xavier
Freire in the restingas of Paraíba and Rio Grande do Norte
states and focused exclusively on lizards (Freire 1996). A
few years later, Dr. Freire coordinated a new survey in the
forest remnants of Alagoas state, precisely in Murici, Catolé,
G. A. P. Filho et al.
and Cedro, involving all Squamate reptiles (Freire 2001).
These surveys furnished important information about the
reptiles of the area. The second published reptile survey in
the PEC region was published more than a decade later by
Santana et al. (2008), with a comprehensive list of amphibi-
ans and reptiles of a forest remnant of Paraíba state.
After the establishment of herpetologists in the
Universidade Federal da Paraiba and Universidade Federal
de Pernambuco, in the second decade of the twenty-first cen-
tury, some specific papers on snake distribution and natural
history were published (França et al. 2012, 2020; França and
França 2019; Pereira-Filho et al. 2017, 2020; Marques et al.
2021). However, the third comprehensive reptile survey in a
PEC locality was published only in 2016 for an urban forest
remnant in Pernambuco state (Oliveira et al. 2016). Lately,
other comprehensive surveys have been published, and the
amount of information has increased significantly. Recently,
Mesquita et al. (2018) described the herpetofauna of Guaribas
Biological Reserve, in Paraíba state, and four important stud-
ies were published in areas of Pernambuco state: the reptiles
of Pedra Talhada Biological Reserve (Roberto et al. 2015),
the herpetofauna of Serra do Urubu mountain range (Roberto
et al. 2017), the very recent inventories for the reptile fauna
of the forest remnants of Siriji (Andrade-Lima et al. 2021),
and for the herpetofauna of the Serra do Mascarenhas and
Wildlife Refuge Matas de Água Azul (Oliveira et al. 2021).
Finally, for the Alagoas state, inventories of reptiles were
published for the Environmental Protection Area and
Ecological Station of Murici (Dubeux et al. 2022). Regarding
the highland humid forest remnants scattered throughout the
semiarid lowlands, known as “Brejos de Altitude,” only three
studies were published. The first was about the snakes of the
Brejos de Altitude of Paraíba and Pernambuco (Pereira-Filho
and Montingelli 2011), the second approached the herpeto-
fauna of three Brejos in Pernambuco (Freitas et  al. 2019),
and finally, Pereira-Filho et al. (2020) published a compre-
hensive list of the snakes of the inland forests of PEC.
Considering the relevance of the region as endemism
center and the constant and high deforestation rates in the
region, we understand that a document compiling the avail-
able information on the reptile diversity in the PEC region,
including data available in literature and in some of the
main Brazilian zoological collections with representative-
ness to the region, was urgently needed. Therefore, the
aims of this chapter are (a) to provide an updated list of the
reptile species recorded in PEC for coastal and inland for-
ests; (b) to define patterns of richness and endemisms to the
region; (c) to examine the origin and diversification of rep-
tile fauna of the PEC; and finally (d) discuss aspects about
conservation.
11  Composition, Species Richness, and Conservation of the Reptiles of the Highly Threatened Northern Brazilian Atlantic Forest
11.2 Methods
11.2.1 Reptile Species List
We create a database composed of reptiles specimens housed
in three herpetological collections: the Herpetological
Collection of Universidade Federal da Paraíba (CHUFPB),
the Herpetological Collection of Universidade Federal Rural
de Pernambuco (CHUFRPE), and the Herpetological collec-
tion of Museu de Zoologia da Universidade de São Paulo
(MZUSP). In addition, unpublished data of some of the
authors and literature data were added to the database (e.g.,
Freire 1996; Santana et  al. 2008; Pereira-Filho and
Montingelli 2011; Roberto et al. 2015, 2017; Oliveira et al.
2016, 2021; Pereira-Filho et al. 2017, 2020; Mesquita et al.
2018; Freitas et al. 2019; França et al. 2020; Andrade-Lima
et al. 2021).
11.2.2 Taxonomic Richness Patterns
We mapped the distribution of taxonomic richness for all
reptiles, as well as in detail for the three most diverse groups
(snakes, lizards, and worm-lizards) along PEC area. To do
this, we downloaded the polygons provided by Roll et  al.
(2017) and calculated the number of species per grid (0.2°)
superimposed on the PEC area. We drew the maps on QGIS
software version 3.16.3-Hannover (QGIS Development
Team 2022).
11.2.3 Beta Diversity and Conservation
We delimitated the studied sites considering the political
divisions and separated each one in the North and South
regions. The delimitation in political divisions is because
each state has different environmental laws (e.g., IMA-­
Instituto Ambiental do Meio Ambiente de Alagoas—Alagoas
state; SUDEMA—Superintendência de Administração do
Meio Ambiente, Paraíba state; SEMAS—A Secretaria de
Meio Ambiente e Sustentabilidade, Pernambuco state; and
IDEMA—Instituto de Desenvolvimento Sustentável e Meio
Ambiente, Rio Grande do Norte state). Thus, we provided
spatial data that allow to help each state’s conservation strat-
egies (Lourenço-de-Moraes et al. 2020). The divisions fol-
low: NRN (North of Rio Grande do Norte state), SRN (South
of Rio Grande do Norte state), NPB (North of Paraíba state),
SPB (South of Paraíba state), NPE (North of Pernambuco
state), SPE (South of Pernambuco state), NAL (North
Alagoas state), and SAL (South Alagoas state). In total, we
analyzed eight territories (Fig. 11.1).
171
We included the species occurrences records available of
the database species through occurrence polygons available
in Roll et al. (2017). We used ArcGIS 10.1 software (ESRI
2019) to build presence/absence matrices from the species
distribution data by superimposing a grid system with cells
of 0.02 latitude/longitude degrees, creating a network with
10,739 grid cells.
We used two complementary metrics for beta diversity
analysis by considering species presence and absence
(Lourenço-de-Moraes et  al. 2020). First, we calculated a
nestedness metric based on the overlap and decreasing fill
(index NODF) across the eight territories (Almeida-Neto
et al. 2008; Ulrich et al. 2009). In reducing both columns and
rows, the matrix are ranking the areas according to their spe-
cies richness and ordering the species in lines, the most fre-
quent to the less frequent. We performed this analysis for all
localities with 1000 simulations using the package “vegan”
(Oksanen et  al. 2013) in the R software (R Development
Core Team 2021).
Second, following the sequence provided by NODF, we
conducted beta diversity partitioning and computed distance
matrices using pairwise dissimilarities βsor (i.e., measure
total beta diversity), βsim (i.e., measure spatial turnover),
and βnes (i.e., measure nesting) (Baselga 2010). We com-
puted these analyses among the eight territories to show the
directions of the species distributions. We considered high
nesting values mean more species similar to the area of high-
est species richness, and increased numbers of turnover
mean less similar species composition. We performed these
tests using the package “betapart” (Baselga and Orme 2012)
in the R software (R Development Core Team 2021).
11.3 Results
11.3.1 Reptile Species Composition
In the PEC, including coastal and inland forests remnants,
many regions lack information about reptile diversity.
Although, with the increasing number of research centers in
the area, the knowledge about the reptiles has been improved
in the last decades (Pereira-Filho et al. 2020). According to
our database, the PEC harbors 143 reptile species, divided
into 7 amphisbaenians (worm-lizards), 38 lizards, 91 snakes,
5 chelonians, and 2 crocodilians (Table 11.1).
The numbers mentioned are very impressive when com-
pared with the total number of species found in the Atlantic
Forest. In terms of percentage, the forests of PEC harbor
17.5% of the amphisbaenians (one endemic species), 21.8%
of lizards (three endemic species), 40% of snakes (seven
endemic species), 23.8% of the chelonians, and 50% of the
172
Fig. 11.1  Map of the Pernambuco Endemism Center (PEC) location,
with the original coverage of Atlantic Forest with study sites considered
in nestedness metric based on overlap and decreasing fill analysis
crocodilians, found in the whole Atlantic Forest. For croco-
dilians and chelonians, there is no endemism in the area.
Despite the high number of reptiles known for the PEC,
this singular region has presented a continuous rate of
description of new species in the last 20  years (e.g.,
Echinanthera cephalomaculata, Coleodactylus natalensis,
Bothrops muriciensis, Coleodactylus elizae, Dendrophidion
atlantica, Micrurus potyguara, Amerotyphlops arenensis,
Caaeteboia gaeli, and Phyllopezus selmae) (Fig. 11.2).There
is still a diversity of reptiles not described for the area, indi-
cating that the richness may be underestimated for this par-
ticular sector of the Atlantic Forest. Besides the descriptions
of new species, the reptile fauna of PEC presents a strong
influence of the Caatinga domain. Many species such as
Bothrops erythromelas, Dryophylax almae, Acratosaura
mentalis, Phyllopezus pollicaris, Polychrus acutirostris, and
Gymnodactylus geckoides can be found in the PEC, espe-
cially in the inland mountain forests (“Brejos de Altitude”).
The forest patches that compose the “Brejos de Altitude” are
G. A. P. Filho et al.
(NODF) and the actual forest remnants. Integral protection Conservation
units are evidenced on the map
immersed in the Caatinga domain, and due to the proximity
with the xeric vegetation of the Caatinga harbors a reptile
fauna with elements of this xeric biome (Guedes et al. 2014;
Pereira-Filho et al. 2020). However, even in the coastal frag-
ments of PEC, we can find some species commonly found in
open areas. These species are mainly related to tabuleiros,
characteristic environment of northeast Atlantic Forest that
present phytophysiognomy of savannah, and coastal restin-
gas, characterized by medium-sized trees and shrubs over
sand dunes (Thomas and Barbosa 2008).
11.3.2 Taxonomic Richness Patterns
The taxonomic richness showed a pattern in which the rich-
est areas (>86 spp.) are located in the south of PEC, precisely
between south of Pernambuco and along Alagoas states
(Fig.  11.3), both in the countryside. Intermediate values
11  Composition, Species Richness, and Conservation of the Reptiles of the Highly Threatened Northern Brazilian Atlantic Forest 173

Table 11.1  List of reptiles recorded for Pernambuco Endemism Table 11.1 (continued)
Center (PEC)
Species EPEC EAF DD LAD WD
Species EPEC EAF DD LAD WD Coleodactylus meridionalis X
SQUAMATA (Boulenger, 1888)
Lizards Coleodactylus natalensis (Freire, X
Worm-Lizards 1999)
Amphisbaenidae Anguidae
Amphisbaena alba (Linnaeus, 1758) X Ophiodes sp. X◊
Amphisbaena heathi (Schmidt, Diploglossidae
1963) Diploglossus fasciatus (Gray, 1831) X
Amphisbaena littoralis (Roberto, X #
Brito & Ávila, 2014) Diploglossus lessonae (Peracca, X
Amphisbaena lumbricalis X* 1890)
(Vanzolini, 1996) Teiidae
Amphisbaena pretrei (Duméril & X Ameiva ameiva (Linnaeus, 1758) X
Bibron, 1839) Ameivula ocellifera (Spix, 1825) X
Amphisbaena vermicularis (Wagler X Kentropyx calcarata (Spix, 1825) X▲
in Spix, 1824)
Salvator merianae (Duméril & X
Leposternon polystegum (Duméril in X
Bibron, 1839)
Bibron & Duméril, 1851)
Gymnophthalmidae
Lizards
Acratosaura mentalis (Amaral, X*
Iguanidae
1933)
Iguana iguana (Linnaeus, 1758) X
Cercosaura olivacea (Gray, 1845) X◊
Dactyloidae
Dryadosaura nordestina (Rodrigues, X
Norops fuscoauratus (D’Orbigny, X▲ Freire, Pellegrino & Sites, 2005)
1837 in Duméril & Bibron, 1837)
Micrablepharus maximiliani X
Norops ortonii (Cope, 1868) X+ (Reinhardt & Lütken, 1862)
Dactyloa punctata (Daudin, 1802) X+ Stenolepis ridleyi (Boulenger, 1887) X
Polichrotidae Vanzosaura multiscutata (Amaral, X*
Polychrus acutirostris (Spix, 1825) X 1933)
Polychrus marmoratus (Linnaeus, X▲ Mabuyidae
1758) Brasiliscincus heathi (Schimdt & X
Leiossauridae Inger, 1951)
Enyalius bibronii (Boulenger, 1885) X Copeoglossum nigropunctatum X
Enyalius aff. bibronii X (Spix, 1825)
Tropiduridae Psychosaura agmosticha X*
Strobilurus torquatus (Wiegmann, X (Rodrigues, 2000)
1834) Psychosaura macrorhyncha (Hoge, X
Tropidurus hispidus (Spix, 1825) X 1946)
Tropidurus semitaeniatus (Spix, X* Snakes
1825) Anomalepididae
Gekkonidae Liothyphlops trefauti (Freire, X
Hemidactylus agrius (Vanzolini, X* Caramaschi & Argôlo, 2007)
1978) Typhlopidae
Hemidactylus mabouia (Moreau de X Amerotyphlops amoipira (Rodrigues X*
Jonnès, 1818) & Juncá, 2002)
Phyllodactylidae Amerotyphlops arenensis (Graboski, X×
Gymnodactylus darwinii (Gray, X Pereira-Filho, Silva, Prudente &
1845) Zaher, 2015)
Gymnodactylus geckoides (Spix, X* Amerotyphlops brongersmianus X
1825) (Vanzolini, 1976)
Phyllopezus lutzae (Loveridge, X Amerotyphlops paucisquamus X+
1941) (Dixon & Hendricks, 1979)
Phyllopezus pollicaris (Spix, 1825) X* X Leptotyphlpidae
Phyllopezus selmae (Dubeux, X Epictia borapeliotes (Vanzolini, X*
Gonçalves, Palmeira, Nunes, 1996)
Cassimiro, Gamble, Werneck, Trilepida salgueiroi (Amaral, 1955) X
Rodrigues & Mott, 2022) Boidae
Sphaerodactylidae Boa constrictor (Linnaeus, 1758) X
Coleodactylus elizae (Gonçalves, X Corallus hortulana (Linnaeus, 1758) X
Torquato, Skuk, & Sena, 2012)
(continued) (continued)
174 G. A. P. Filho et al.

Table 11.1 (continued) Table 11.1 (continued)

Species EPEC EAF DD LAD WD Species EPEC EAF DD LAD WD
Epicrates assisi (Machado, 1945) X Cercophis auratus (Schlegel, 1837) X+
Epicrates cenchria (Linnaeus, 1758) X+ Clelia plumbea (Wied-Neuwied, X+
Viperidae 1820)
Bothrops bilineatus (Wied-Neuwied, X+ Dibernardia affinis (Günther, 1858) X
1821) Dipsas indica (Laurenti, 1768) X+
Bothrops erythromelas (Amaral, X* Dipsas mikanii (Schlegel, 1837) X
1923) Dipsas aff. neuwiedi X
Bothrops leucurus (Wagler in Spix, X Dipsas sazimai (Fernandes, Marques X
1824) & Argôlo, 2010)
Bothrops muriciensis (Ferrarezzi & X Dipsas variegata (Duméril, Bibron X+
Freire, 2001) & Duméril, 1854)
Crotalus durissus (Linnaeus, 1758) X Dryophylax almae (Franco & X*
Lachesis muta (Linnaeus, 1766) X+ Ferreira, 2003)
Elapidae Dryophylax hypoconia (Cope, 1860) X
Micrurus aff. ibiboboca X Dryophylax phoenix (Franco, X*
Micrurus corallinus (Merrem, 1820) X Trevine, Montingelli & Zaher, 2017)
Micrurus lemniscatus (Linnaeus, X Echinanthera cephalomaculata X
1758) (Di-Bernardo, 1994)
Micrurus potyguara (Pires, Silva-Jr., X Echinanthera cephalostriata X
Feitosa, Prudente, Pereira-Filho & (Di-Bernardo, 1996)
Zaher, 2014) Erythrolamprus aesculapii X
Micrurus sp. X (Linnaeus, 1758)
Colubridae Erythrolamprus almadensis (Wagler, X
Chironius bicarinatus (Wied, 1820) X 1824)
Chironius carinatus (Linnaeus, X+ Erythrolamprus miliaris (Linnaeus, X
1758) 1758)
Chironius exoletus (Linnaeus, 1758) X Erythrolamprus mossoroensis (Hoge X*
Chironius flavolineatus (Jan, 1863) X & Lima-Verde, 1973)
Dendrophidion atlantica (Freire, X Erythrolamprus poecilogyrus X
Caramaschi & Gonçalves, 2010) (Wied-Neuwied, 1824)
Drymarchon corais (Boie, 1827) X Erythrolamprus reginae (Linnaeus, X+
1758)
Drymoluber brazili (Gomes, 1918) X§
Erythrolamprus taeniogaster (Jan, X+
Drymoluber dichrous (Peters, 1863) X+
1863)
Leptophis dibernardoi X X
Erythrolamprus viridis (Günther, X*
(Albuquerque, Santos, Borges-­
1862)
Nojosa & Ávila, 2022)
Helicops angulatus (Linnaeus, X
Leptophis liocercus (Wied, 1824) X
1758)
Oxybelis aeneus (Wagler in Spix, X
Helicops leopardinus (Schlegel, X
1824)
1837)
Palusophis bifossatus (Raddi, 1820) X
Hydrodynastes gigas (Duméril, X≠
Spilotes pullatus (Linnaeus, 1758) X Bibron & Duméril, 1854)
Spilotes sulphureus (Wagler in Spix, X+ Imantodes cenchoa (Linnaeus, X
1824) 1758)
Tantilla melanocephala (Linnaeus, X Leptodeira annulata (Linnaeus, X+
1758) 1758)
Dipsadidae Leptodeira tarairiu (Costa, X
Adelphostigma occipitalis (Jan, X Graboski, Grazziotin, Zaher,
1863) Rodrigues & Prudente, 2022)
Apostolepis cearensis (Gomes, X Lioheterophis iheringi (Amaral, X*
1915) 1935)
Apostolepis longicaudata (Gomes in X! Lygophis dilepis (Cope, 1862) X*
Amaral, 1921) Oxyrhopus guibei (Hoge & X
Atractus caete (Passos, Fernandes, X Romano, 1977)
Bérnils & Moura-Leite, 2010) Oxyrhopus petolarius (Linnaeus, X
Atractus maculatus (Günther, 1858) X 1758)
Atractus potschi (Fernandes, 1995) X Oxyrhopus trigeminus (Duméril, X
Boiruna sertaneja (Zaher, 1996) X* Bibron & Duméril, 1854)
Caaeteboia gaeli (Montingelli, X Philodryas nattereri (Steindachner, X
Barbo, Pereira-Filho, Santana, 1870)
França, Grazziotin & Zaher, 2020) (continued)
(continued)
11  Composition, Species Richness, and Conservation of the Reptiles of the Highly Threatened Northern Brazilian Atlantic Forest 175

Table 11.1 (continued) (70–86  spp.) are found in the coast of Alagoas and
Species EPEC EAF DD LAD WD Pernambuco, and in the countryside and Brejos de Altitude
Philodryas olfersii (Linchtenstein, X of Paraíba state. The lowest values (37–69  spp.) are in the
1823) north of PEC along the whole Rio Grande do Norte state and
Phimophis guerini (Duméril, Bibron X coast of Paraíba.
& Duméril, 1854)
Pseudablabes patagoniensis (Girard, X
When considering different groups of reptiles, the taxo-
1858) nomic richness pattern changes for some of them in compari-
Pseudoboa nigra (Duméril, Bibron X son with the reptile pattern. For snakes, the taxonomic
& Duméril, 1854) pattern is similar to reptile: richest areas (>53 spp.) between
Psomophis joberti (Sauvage, 1884) X south of Pernambuco and along Alagoas states; intermediate
Sibon nebulatus (Linnaeus, 1758) X+ richness values (40–52 spp.) are found in the coast of Alagoas
Siphlophis compressus (Daudin, X+
and Pernambuco, and in the countryside and Brejos de
1803)
Thamnodynastes pallidus (Linnaeus, X+ Altitude of Paraíba state; and lowest values (14–39 spp.) in
1758) the north of PEC. Regarding lizards, the richest areas
Thamnodynastes sertanejo (Bailey, X* (>30 spp.) are in the countryside and Brejos de Altitude in
Thomas & Silva-Jr., 2005) Pernambuco state, intermediate values (26–29  spp.) in the
Xenodon merremii (Wagler in Spix, X countryside of Pernambuco and Alagoas and in the Brejos de
1824)
Altitude in Paraíba state, lowest values (<22 spp.) along the
Xenodon rhabdocephalus (Wied-­ X+
Neuwied, 1824) whole coast of PEC. For the worm-lizards, the richest area
Xenopholis scalaris (Wucherer, X+ (= 6 spp.) is a small spot in the north of Rio Grande do Norte
1861) state, intermediate richness (= 5 spp.) is mostly in the state of
Xenopholis undulatus (Jensen, 1900) X Pernambuco and Brejos de Altitude of Paraíba, lowest values
TESTUDINATA (<4  spp.) are in most of the area of Rio Grande do Norte,
Kinosternidae Paraíba, and Alagoas.
Kinosternon scorpioides (Linnaeus,
1766)
Since we are considering the polygons range of the spe-
Testudinidae cies to calculate taxonomic richness, it prevents us from
Chelonoides carbonarius (Spix, X viewing in detail the sampling gaps that exist along the PEC
1824) area. However, since there is a strong relationship between
Chelidae sampling effort and species richness (Guedes et al. 2018), we
Acanthochelys radiolata (Mikan, X could assume some areas reported as poor in species could
1820)
highlight poorly sampled regions that need attention in future
Mesoclemmys tuberculata X*
(Luederwaldt, 1926) surveys.
Phrynops tuberosus (Peters, 1870) X In the southern portion of PEC, precisely, the forests
CROCODYLIA between Alagoas and the south of Pernambuco states are
Aligatoridae considered ombrophilous forests, thus, presenting more
Caiman latirostris (Daudin, 1801) X moisture and a higher forest size (Thomas and Barbosa
Paleosochus palpebrosus (Cuvier, X 2008). They also present a better conservation condition,
1807)
including the two most representative remnants in terms of
Notes: * Species with distribution core area in the Caatinga Domain; × size of the PEC, the Murici Ecological Station (6.131  ha)
Species with distribution core area in the northern Atlantic Forest; ▲
Species with disjunct distribution between Amazon domain/Cerrado and and the Biological Reserve of Pedra Talhada (4.469  ha).
Atlantic Forest; + Species with disjunct distribution between Amazon These two factors can be responsible for the higher number
domain and Atlantic Forest; ■ This species is treated by most authors as of species in this specific portion. The northern portion of
E. catenatus; however, Rodrigues et al. (2014), in phylogenetic analysis, PEC presents two different types of phytophysiognomy, the
show that its relationship is direct with E. bibronii; ◊ Species with distri-
bution related to the Cerrado and discontinuous occurrences in the “Florestas de Tabuleiro” and the “Restinga Forests”
Atlantic Forest; # There is only one record to this species in the PEC, (Thomas and Barbosa 2008). These forests are very differ-
precisely in the Atlantic Forest of Alagoas state; § There is only one ent from the ombrophilous forests found in Alagoas and
record of Drymoluber brazili in one Brejo de Altitude (Pico do Jabre, south Pernambuco, as they present a smaller size, sandy
Paraíba), although this “Brejo” presents a complex vegetation physiog-
nomy with elements of the Atlantic Forest, Caatinga, and Cerrado; ≠: soil, and a smaller amount of rain annually (Thomas and
Hydrodynastes gigas presents its distribution linked to the hydrography Barbosa 2008). The variable sampling efforts can also influ-
and presents few records in the region of PEC precisely to Paraíba and ence the richness pattern along the regions of PEC.
Rio Grande do Norte states; ! Apostolepis longicaudata is a rare species Unfortunately, the data about reptile diversity in the north-
with disjunct distribution between Cerrado, Caatinga, and Atlantic Forest
EPEC Endemic of Pernambuco Endemism Center, EAF Endemic of the ern portion are scanty, which need to be reinforced to
Atlantic Forest, DD Disjunct Distribution, LAD Linked to adjacent enhance the effect of sampling in the region and also gather
domains, WD Wide distribution more refined comparisons.
176 G. A. P. Filho et al.

Fig. 11.2  Some of the

endemic species of the
northern Atlantic Forest. (a)
Phyllopezus selmae; (b)
Coleodactylus elizae; (c)
Coleodactylus natalensis; (d)
Bothrops muriciensis; (e)
Micrurus potyguara; (f)
Dendrophidion atlantica; (g)
Atractus caete; (h) Atractus
maculatus; (i) Caaeteboia
gaeli; (j) Echinanthera
cephalomaculata. Photos, (a):
Marcos Dubeux; (b), (g):
Grabriel Skuk; (c): Raul
Sales; (e): Claudio Sampaio;
(f), (h), and (j): Marco
Freitas; (i): Gentil Filho

The central part of PEC comprising the north of
Pernambuco and almost the whole coast of Paraiba presents
an intermediary richness with numbers varying for more
than 70 species in specific locations. The “Tabuleiro Forest”
that covers these areas is significantly more humid than the
forests of the northernmost portion.
In a general view, all these factors can be responsible for
the decreasing of species richness from south to north as a
general pattern, although many areas still need to be sur-
veyed, especially the “Brejos de Altitude.” With the investi-
gation of more areas, the richness patterns of the reptiles of
PEC would be better understood.
 177

-5

Snakes
66
40
14

Lizards
33
-10 Reptiles
26
102
18
70
0 75 150 km
37

-40 -35 Worm lizards

6
5
3

Fig. 11.3  Map of richness patterns of the reptiles of PEC. In detail, richness patterns for snakes, lizards, and amphisbaenians (worm-lizards)

11.3.3 Beta Diversity Table 11.2  The Betapart results showed the partitioning of beta diver-
sity, turnover, nestedness, and Soerensen index for reptiles from
The reptiles from PEC, present strong nestedness Pernambuco Endemism Center, Atlantic Forest north of São Francisco
River
(NODF = 77.4; P < 0.0001), indicating that study sites share
Turnover Nestedness Sorensen
many species among them, promoting a solid identity to PEC
NAL 0 0 0
(Fig. 11.3). The nestedness metric based on the overlap and
SAL 0.01 0 0.25
decreasing fill (NODF) indicates that PEC from Alagoas, SPE 0.03 0.01 0.14
Pernambuco, and South of Paraíba (NAL, SAL, SPE, SPB, SPB 0.12 0.01 0.47
and NPE) are the richest sites, acting as species source to NPE 0.09 0.01 0.46
other sites. This pattern could be related to the quality of NPB 0.12 0.09 0.45
inventories in these areas (Roberto et al. 2015, 2017; Freire SRN 0.11 0.24 0.51
et al. 2018; França et al. 2020), or also could be a simple pat- NRN 0.13 0.34 0.48
tern of species richness following the moisture gradient, NAL Northern Alagoas State, SAL Southern Alagoas, SPE Southern
which decreases according with the distance from São Pernambuco, SPB Southern Paraíba, NPE Northern Pernambuco, NPB
Northern Paraíba, SRN Southern Rio Grande do Norte, NRN Northern
Francisco River to the north (Pianka 1966; Hijmans et  al. Rio Grande do Norte
2005).
The areas with the highest nestedness are SRN and NRN
(Table 11.2), indicating that these two sites share more spe- ferent species, compared to NAL, the richest site in PEC.
cies within them. Otherwise, the sites that present more The beta diversity (Sorensen index) indicates that SRN,
considerable turnover are the Rio Grande do Norte (NRN, NRN, SPB, NPB, and NPE are the most distinct areas to
SRN) and Paraíba states (NPB and SPB), offering more dif- SPE, NAL, and SAL.
178
Our data show that most humid areas from PEC, such as
Alagoas and Pernambuco states, act as species sources to dri-
est areas, such as Paraíba and Rio Grande do Norte states.
However, moisture could limit the distribution of some taxa,
such as the snakes Atractus maculatus (Abegg et al. 2017),
Epicrates cenchria (Passos and Fernandes 2008), and
Xenodon rabdocephalus (Lima et  al. 2020) and the lizard
Phyllopezus lutzae (Albuquerque et al. 2019), which could
occur below São Francisco River in Southeast Brazil, but do
not cross in the Atlantic Forest sites from the north of
Pernambuco/South of Paraíba.
11.3.4 Origin, Diversification, and Distribution
Patterns of Reptiles from PEC
The PEC is recognized as a natural biogeographical unit for
several groups of organisms in the Atlantic Forest hotspot,
including reptiles (e.g., Vasconcelos et al. 2014; Xavier et al.
2015; Moura et al. 2016; DaSilva et al. 2017). To explain in
detail the origin, the diversification, and the drives of region-
alization of the reptile fauna from this region is challenging,
especially because there is a lack of data (molecular, distri-
bution, and ecological) for several taxa, which hamper a
more comprehensive understanding of biogeographical his-
tory over evolutionary timescales (Guedes et al. 2018; Tonini
et al. 2021). However, the few studies conducted until now
show that PEC has a complex history, which evolves jointly
ecological drivers and historical events acting in the origin
and diversification, as well as shaping the distribution of the
biota in the region (e.g., Moura et al. 2016; Prates et al. 2016;
Barbo et al. 2021).
The PEC is recognized as a biogeographical unit regard-
ing to snake fauna, although some discrepancy in the extent
of the area is still unsolved (Moura et al. 2016; Barbo et al.
2021). The regionalization of snakes in the PEC is explained
by current climate (temperature, energy input, and precipita-
tion), along with the historical legacy of climate (historical
difference in temperature), which is strongly related to the
role of topography (Moura et al. 2016). Although there are
no comprehensive regionalization studies including lizards
of the Atlantic Forest, the presence of endemic species to the
northern portion also suggests the PEC as a putative biogeo-
graphic unit for this group (Enyalius aff. bibronii,
Coleodactylus elizae, C. natalensis, and Phyllopezus
selmae).
The effect of quaternary climate changes, related to diver-
sification and high endemism rates of other organisms, also
explains the distribution of narrow-range species of snakes.
It allows persistence of endemic snakes (e.g., Caaeteboia
gaeli Montingelli et al. 2020) species, especially in montane
areas (Moura et al. 2016). Some endemic lizard species that
can be mentioned to PEC area are the Coleodactylus elizae
G. A. P. Filho et al.
and C. natalensis, both restricted to forested fragments in the
states of Alagoas and Rio Grande do Norte. Vicariance-based
events (e.g., combination of uplifts of mountain ranges and
abrupt changes in vegetation physiognomies acting breaking
ancestral areas) must also have an important role in shaping
the distribution patterns of snakes in the PEC (Barbo et al.
2021).
It is known that high diversity areas in the neotropical
region experienced an unprecedented level of biotic inter-
change of several organisms along major natural regions,
with predominant directionality from forested (especially the
Amazon) to open landscapes (Antonelli et  al. 2018).
Although little is known about the reptiles from PEC, former
biogeographical connections through historical bridges are
known to occur between other natural landscapes and the
Atlantic Forest for other group of organisms (Costa 2003). If
better investigated, these connections could provide evidence
to explain diversity and endemism of reptiles from PEC. For
instance, Azevedo et  al. (2020) reported both ancient and
recent diverged lineages of narrow range snakes explaining
phylogenetic endemism of PEC. While explaining demo-
graphic history of the green jararaca (also occurring on
PEC), Dal Vechio et al. (2018) revealed multiple connection
events between Amazonia and Atlantic Forest populations in
the last 2 million years. The biogeographical history of other
two jararaca species, Bothrops leucurus (B. atrox clade) and
B. muriciencis (B. jararacussu clade), are also related to the
PEC, and their current distribution are explained by the
appearance of the dispersal corridors among forested areas
(Hamdan et  al. 2020). Additionally, the results of our beta
diversity analysis show that the biotic interchange is still
complex, and it is also occurring inside PEC limits since rep-
tiles from more humid areas used to act as species sources to
the driest areas.
The relatively recent and consistently documented
Amazonian influence in the PEC fauna (e.g., Carvalho et al.
2003; Costa 2003; Batalha-Filho et al. 2013) is also present
in lizards, as demonstrated by Prates et al. (2016) for three
anole species codistributed in both Amazonia and Atlantic
Forest (Dactyloa punctata, Norops ortonii, and Polychrus
marmoratus). Their results revealed the synchronous coloni-
zation of the northern Atlantic Forest from eastern Amazonia
in mid-Pleistocene, agreeing with patterns already recorded
for other vertebrates (e.g., Costa 2003; Batalha-Filho et al.
2013), including viperid snakes of the jararacussu group of
the genus Bothrops (Dal Vechio et al. 2020). Similar faunal
exchange related to the quaternary climate fluctuations is
reported for the teiid lizard Kentropyx calcarata (Werneck
et al. 2009). This historical event also is the probable expla-
nation for the reduced divergence observed between
Amazonian and Atlantic Forest populations of the bushmas-
ter Lachesis muta (Zamudio and Greene 1997; Fernandes
et al. 2004).
 179

The PEC is a high-diverse biogeographic area of the natural Municipal da Cidade do Natal Dom Nivaldo Monte
Atlantic Forest regarding reptile fauna. However, a historical (148 ha) (Fig. 11.5).
combination of insufficient investments and low regional We found nine endemic reptile species from PEC: the liz-
research capacity have made the diversification history of its ards Coleodactylus natalensis and C. elizae and the snakes
reptiles a neglected chapter in the biogeographical studies of Bothrops muriciensis, Micrurus potyguara, Dendrophidion
the Neotropical region. We should now focus to include atlantica, Atractus caete, Atractus maculatus, Caaeteboia
more reptile taxa of this area while investigating biogeo- gaeli, and Echinanthera cephalomaculata. An exciting and
graphical connections among other South American ecosys- very positive pattern is that endemic species are well distrib-
tems. Certainly, the biota of this area is crucial to understanduted throughout PEC. However, only a few species could be
the complex evolutionary dynamic of origin of the neotropi- found in ICUs: Dendrophidion atlantica and Bothrops muri-
cal region diversity. ciensis in ESEC Muruci, Atractus caete in REBIO Pedra
Talhada, and Micrurus potyguara in REBIO Guaribas
(Fig.  11.3). In addition, four of these species (the lizard
11.3.5 Conservation Coleodactylus natalensis and the snakes Bothrops muriciensis,
Atractus caete, and Echinanthera cephalomaculata) are listed
The best way to protect biodiversity is the creation and effec- on the Brazilian Red List of Endangered Species (ICMBio
tiveness of Integral Conservation Units (ICUs). These pro- 2018). Other reptiles are very rare in PEC, with less than ten
tected areas (IUCN I-IV) are expected to maintain the natural individuals found in this northern portion of the Atlantic
ecosystem without human interference (Gonçalves-Souza Forest, such as the snakes Palusophis bifossatus, Hydrodynastes
et  al. 2021). The PEC is considered a climate refuge with gigas, and Caaeteboia gaeli and the lizard Cercosaura oliva-
high ecological and evolutionary values (Lourenço-de-­ cea. Although these species are not listed on the Brazilian Red
Moraes et  al. 2019, 2021); the establishment of ICUs is List, they deserve to be highlighted in conservation strategies
essential for its conservation. According to Fig.  11.4, the for PEC and may be threatened locally or regionally.
almost absence of ICUs in the natural remnants in the The maintenance of the ICUs and the creation of new
Atlantic Forest of PEC is evident. However, considering the ones are very important measures to assure the biodiversity
distribution of species throughout the PEC, this absence of of such a threatened sector of the Atlantic Forest. Unlike the
ICUs is even more alarming since the areas that harbor more southeastern portion of the Atlantic Forest, the region of PEC
species and share them with other regions almost do not have is flat and easy to access, which makes the region suitable to
ICUs, such as SAL and SPE. The only significant ICUs are the plantation of sugar cane. The monoculture of sugar cane
REBIO Pedra Talhada and ESEC Murici. On the other side, is not recent in the Brazilian coast; in the eighteenth century,
the sites with more exclusive species, Rio Grande do Norte with the establishment of the sugarcane mills, many areas of
and Paraíba, present only one significant ICUs, the REBIO the Atlantic Forest were devastated, which is considered the
Guaribas (4.052 ha) in NPB. Rio Grande do Norte only has a first cycle of this monoculture (Dean 1996). Still, stimulated
very small ICU in the Atlantic forest fragment, the Parque by the Brazilian government through the National Alcohol

Fig. 11.4  Matrix of presence

(filled cells) and absence
(empty cells) of reptiles from
Pernambuco Endemism
Center (PEC), Atlantic Forest
north of São Francisco River,
indicating strong nestedness
(NODF = 77.4; P < 0.0001).
The line represents the
isocline of differences in
species richness among sites
(NAL Northern Alagoas State,
SAL Southern Alagoas, SPE
Southern Pernambuco, SPB
Southern Paraíba, NPE
Northern Pernambuco, NPB
Northern Paraíba, SRN
Southern Rio Grande do
Norte, NRN Northern Rio
Grande do Norte)
180 G. A. P. Filho et al.

Fig. 11.5  Map of the location of the Pernambuco Endemism Center (PEC), with the distribution of all endemic reptile species

Program (Proálcool) in 1975, the remnant areas of the first
cycle were deforested, which made the situation much worse
(Coimbra-Filho and Câmara 1996; Dean 1996). Nowadays,
the fragments of the forests of PEC are isolated by large cit-
ies or mainly by sugarcane plantations (Tabarelli et al. 2006).
Even with an extremely worrying panorama, the PEC still
harbors a high animal diversity with an urgent need to be
known and preserved, which depends on scientific research,
awareness of the population, and the will of the government
to implement public policies to protect the area.
11  Composition, Species Richness, and Conservation of the Reptiles of the Highly Threatened Northern Brazilian Atlantic Forest
11.4 Conclusions
The global environmental crisis is perhaps the most urgent
problem that mankind faces nowadays, where uncountable
species are affected by loss of habitat, hunting, among other
problems. The northern part of the Brazilian Atlantic Forest
due to its high biodiversity can be considered a hotspot
within a hotspot, but unfortunately, this special sector faces
relentless destruction since Brazil’s colonial time, where the
forest was replaced by sugarcane fields based on a short-
sighted production system. Even with a mass destruction
process, the biodiversity of this region still survives but asks
for urgent help. The entire region must be considered propri-
etary for conservation, and long-term researches must be
developed in order to know its biodiversity. Our analysis
showed that along this center of endemism, the composition
and richness of the species present variation, with more spe-
cies in the southern portion than in the northern. This is the
first time this pattern is recognized for reptiles of the region,
and this evidence highlights that there is so much to discover
about these northern forests. At the same time, the whole
situation of this part of the Atlantic Forest is catastrophic
with a high heterogeneity among the forest remnants. The
remnants, accounting to 41%, of the region are smaller than
1  ha, and only 896 remnants are larger than 100  ha (see
Chap. 2). These numbers indicate that the time to save the
remaining northern forests is now once we do not know how
much time the Northern Atlantic Forest will survive facing
this extreme environmental crisis.
References
Abegg AD, Freitas MA, Moura GJB (2017) First confirmed record
of Atractus maculatus (Serpentes, Dipsadidae) from the state of
Pernambuco, northeastern Brazil. Check List 13(2):1–3. https://doi.
org/10.15560/13.2.CL2080
Albuquerque PRA, Morais MSR, Moura PTS et al (2019) Phyllopezus
lutzae (Loveridge, 1941) (Squamata, Phyllodactylidae): new records
from the Brazilian state of Paraíba. Check List 15(1):49–53. https://
doi.org/10.15560/15.1.49
Almeida-Neto M, Guimarães P, Guimarães PR Jr et al (2008) A consis-
tent metric for nestedness analysis in ecological systems: reconcil-
ing concept and measurement. Oikos 117:1227–1239. https://doi.
org/10.1111/j.0030-­1299.2008.16644.x
Andrade-Lima JH, Dias EG, Costa RDL et  al (2021) Lizards
and snakes of Refúgio de Vida Silvestre Matas do Siriji, an
Atlantic Forest hotspot of the Pernambuco Endemism Center,
Northeastern Brazil. Biota Neotrop 21(2):e20201106. https://doi.
org/10.1590/1676-­0611-­BN-­2020-­1106
Antonelli A, Zizka A, Carvalho FA et al (2018) Amazonia is the pri-
mary source of neotropical biodiversity. Proc Natl Acad Sci
115(23):6034–6039. https://doi.org/10.1073/pnas.1713819115
Azevedo JAR, Guedes TB, Nogueira CC et  al (2020) Museums and
cradles of diversity are geographically coincident for narrowly dis-
tributed neotropical snakes. Ecography 43:328–339. https://doi.
org/10.1111/ecog.04815
181
Barbo FE, Nogueira CC, Sawaya RJ (2021) Vicariance and regionaliza-
tion patterns in snakes of the South American Atlantic Forest mega-
diverse hotspot. J Biogeogr 48(4):823–832. https://doi.org/10.1111/
jbi.14040
Baselga A (2010) Partitioning the turnover and nestedness compo-
nents of beta diversity. Glob Ecol Biogeogr 19:134–143. https://doi.
org/10.1111/j.1466-­8238.2009.00490.x
Baselga A, Orme CDL (2012) Betapart: an R package for the study
of beta diversity. Methods Ecol Evol 3:808–812. https://doi.
org/10.1111/j.2041-­210X.2012.00224.x
Batalha-Filho H, Fjeldså J, Fabre PH, Miyaki CY (2013) Connections
between the Atlantic and the Amazonian forest avifaunas ­represent
distinct historical events. J Ornithol 154:41–50. https://doi.
org/10.1007/s10336-­012-­0866-­7
Carvalho CJB, Bortolanza MCC, Soares EDG (2003) Distributional
patterns of neotropical Muscidae (Diptera). In: Morrone JJ, Llorent
B (eds) Una perspective latinoamericana de la Biogeografia.
Universidade Autônoma do México, Ciudad del México,
pp 236–274
Coimbra-Filho AF, Câmara IG (1996) Os limites originais do bioma
Mata Atlântica na região Nordeste do Brasil. Fundação Brasileira
para a Conservação da Natureza, Rio de Janeiro
Costa LP (2003) The historical bridge between the Amazon and
the Atlantic Forest of Brazil: a study of molecular phylogeog-
raphy with small mammals. J Biogeogr 30:71–86. https://doi.
org/10.1046/j.1365-­2699.2003.00792.x
Dal Vechio F, Prates I, Grazziotin FG et al (2018) Phylogeography and
historical demography of the arboreal pit viper Bothrops bilinea-
tus (Serpentes, Crotalinae) reveal multiple connections between
Amazonian and Atlantic rain Forests. J Biogeogr 45(10):2415–
2426. https://doi.org/10.1111/jbi.13421
Dal Vechio F, Prates I, Grazziotin FG et al (2020) Molecular and pheno-
typic data reveal a new Amazonian species of pit vipers (Serpentes:
Viperidae: Bothrops). J Nat Hist 54:37–38. https://doi.org/10.1080/
00222933.2020.1845835
DaSilva MB, Pinto-da-Rocha R, Morrone J (2017) Historical relation-
ships of areas of endemism of the Brazilian Atlantic rain forest: a
cladistic biogeographic analysis of havertsman taxa (Arachnida:
Opiliones). Current Zool 63(3):525–535. https://doi.org/10.1093/
cz/zow092
Dean WA (1996) Ferro e fogo: a história e a devastação da Mata
Atlântica Brasileira. Companhia das Letras, São Paulo
Dubeux MJM, Araujo Neto JV, Tiburcio ICS et  al (2022) A hotspot
whin a hotspot: the reptiles of the Estaão Ecológica and Área de
Proteão Ambiental de Murici, Atlantic Forest of Northeastern
Brazil. Biota Neotrop 22(2):e20221337
ESRI (2019) Arcgis software. Version 10.1 edn., www.esri.com/prod-
ucts/index.html
Fernandes DS, Franco FL, Fernandes R (2004) Systematic revi-
sion of the genus Lachesis Daudin, 1803 (Serpentes, Viperidae).
Herpetologica 60(2):245–260
Ferrarezzi H, Freire EMX (2001) New species of Bothrops Wagler,
1824 from the Atlantic Forest of northeastern Brazil (Serpentes,
Viperidae, Crotalinae). Bol Mus Nac 440:1–10
França RC, França FGR (2019) Spatial patterns of snake diversity in an
urban area of north-east Brazil. Herpetol J 29:274–281. https://doi.
org/10.33256/hj29.4.274281
França RC, Germano CES, França FGR (2012) Composition of a snake
assemblage inhabiting an urbanized area in the Atlantic Forest of
Paraíba State, Northeast Brazil. Biota Neotrop 2:183–195. https://
doi.org/10.1590/S1676-­06032012000300019
França RC, Morais M, França FGR et  al (2020) Snakes of the
Pernambuco Endemism Center, Brazil: diversity, natural history
and conservation. Zookeys 1002:115–158. https://doi.org/10.3897/
zookeys.1002.50997
182
Freire EMX (1996) Estudo ecológico e zoogeográfico sobre a fauna
de lagartos (Sauria) das dunas de Natal, Rio Grande do Norte e da
restinga de Ponta de Campina, Cabedelo, Paraíba, Brasil. Rev Bras
Zool 13(4):903–921
Freire EMX (1999) Espécie nova de Coleodactylus Parker, 1926 das
dunas de Natal, Rio Grande do Norte, Brasil, com notas sobre suas
relações e dicromatismo sexual no gênero (Squamata, Gekkonidae).
Bol Mus Nac 399:1–14
Freire EMX (2001) Composição, Taxonomia, Diversidade e consid-
erações zoogeográficas sobre a fauna de lagartos e serpentes de
remanescentes da Mata Atlântica do estado de Alagoas, Brasil.
Dissertation, Universidade Federal do Rio de Janeiro
Freire EMX, Caramaschi U, Gonçalves U (2010) A new species of
Dendrophidion (Serpentes: Colubridae) from the Atlantic Rain
Forest of northeastern Brazil. Zootaxa 2719:62–68. https://doi.
org/10.11646/zootaxa.2719.1.5
Freire EMX, Silva ST, Gonçalves U et  al (2018) Mata Atlântica de
Alagoas: Herpetofauna Ameaçada e Estratégias de Conservação. In:
Plano de ação nacional para a conservação da herpetofauna da mata
Atlântica nordestina. ICMBio, Brasília, pp 113–132
Freitas MA, Abegg AD, Araujo DS et al (2019) Herpetofauna of three
“Brejos de Altitude” in the interior of the State of Pernambuco,
northeastern Brazil. Herpetol Notes 12:591–602
Gonçalves U, Silva ST, Skuk G, Sena GAB (2012) A new species of
Coleodactylus Parker, 1926 (Squamata: Sphaerodactylidae) from
the Atlantic Forest of northeast Brazil. Zootaxa 3204:20–30. https://
doi.org/10.11646/zootaxa.3204.1.2
Gonçalves-Souza D, Vilela B, Phalan B, Dobrovolski R (2021) The role
of protected areas in maintaining natural vegetation in Brazil. Sci
Adv 7(38):1–9. https://doi.org/10.1126/sciadv.abh2932
Graboski R, Pereira-Filho GP, Da-Silva AAA et al (2015) A new spe-
cies of Amerotyphlops from Northeastern Brazil, with comments on
distribution of related species. Zootaxa 3920:443–452. https://doi.
org/10.11646/zootaxa.3920.3.3
Guedes TB, Nogueira CC, Marques OAV (2014) Diversity, natural
history, and geographic distribution of snakes in the Caatinga,
Northeastern Brazil. Zootaxa 3863, 1:–93. https://doi.org/10.11646/
zootaxa.3863.1.1
Guedes TB, Sawaya RJ, Zizka A et  al (2018) Patterns, biases
and ­ prospects in the distribution and diversity of Neotropical
snakes. Glob Ecol Biogeog 27:14–21. https://doi.org/10.1111/
geb.12679
Hamdan B, Guedes TB, Carrasco P, Melville J (2020) A complex bio-
geographic history of diversification in neotropical lancehead pit-
vipers (Serpentes, Viperidae). Zool Scr 49:145–158. https://doi.
org/10.1111/zsc.12398
Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution
interpolated climate surfaces for global land areas. Int J Climatol
25(15):1965–1978. https://doi.org/10.1002/joc.1276
ICMBio (2018) Livro Vermelho da Fauna Brasileira Ameaçada de
Extinção, vol 1–6. Instituto Chico Mendes de Conservação da
Biodiversidade, Brasilia
Lima JHA, Freitas MA, Dubeux MJM et  al (2020) New records
of Xenodon rabdocephalus (Wied-Neuwied, 1824) (Serpentes:
Dipsadidae) in the Pernambuco Endemism Center, Northeastern
Brazil. Herpetol Notes 13:517–522
Lourenço-de-Moraes R, Lansak-Tohâ FM, Schwind LTF et  al
(2019) Climate change will decrease the range size of snake
species under negligible protection in the Brazilian Atlantic
Forest hotspot. Sci Rep 9(1):8523. https://doi.org/10.1038/
s41598-­019-­44732-­z
Lourenço-de-Moraes R, Campos FS, Ferreira RB et al (2020) Functional
traits explain amphibian distribution in the Brazilian Atlantic Forest.
J Biogeogr 47:275–287. https://doi.org/10.1111/jbi.13727
Lourenço-de-Moraes R, Campos FS, Carnaval AC et  al (2021) No
more trouble: an economic strategy to protect taxonomic, functional
G. A. P. Filho et al.
and phylogenetic diversity of continental turtles. Biol Conserv
261:109241. https://doi.org/10.1016/j.biocon.2021.109241
Marcgrave GL (1648) Historia Naturalis Brasiliae. Franciscum
Hackium; Lud. Elzevirium, Batavorum; Amstelodami
Marques R, Guedes TB, Lanna FM et al (2021) Species richness and
distribution patterns of the snake fauna of Rio Grande do Norte
state, northeastern Brazil. An Acad Bras Cienc 93:e20191265.
https://doi.org/10.1590/0001-­3765202120191265
Mesquita DO, Alves BCF, Pedro CKB et  al (2018) Herpetofauna of
Reserva Biológica Guaribas: a complex of Atlantic Forest and
isolated Cerrado patches in Northeastern Brazil. Herpetol Notes
11:455–474
Montingelli GG, Barbo F, Pereira-Filho GA et al (2020) A second new
species for the rare dipsadid genus Caaeteboia Zaher et  al. 2009
(Serpentes: Dipsadidae) from the Atlantic Forest of ­northeastern
Brazil. Cuad Herpetol 34:219–230. https://doi.org/10.31017/
CdH.2020.(2020-­003)
Moura MR, Argôlo AJ, Costa HC (2016) Historical and contem­
porary correlates of snake biogeographical subregions in the
Atlantic Forest. J Biogeogr 44(3):640–650. https://doi.org/10.1111/
jbi.12900
Oksanen J, Blanchet FG, Kindt R et al (2013) Vegan: community ecol-
ogy package. R package version 2.0-10
Oliveira CN, Muniz SLS, Moura GJB (2016) Reptiles of an urban
Atlantic rainforest fragment in the state of Pernambuco, northeast-
ern Brazil. Herpetol Notes 9:1–9
Oliveira PMA, Mello AVA, Dubeux MJM et  al (2021) Herpetofauna
of Matas de Água Azul, an Atlantic Forest remnant in Serra do
Mascarenhas, Pernambuco state, Brazil. Biota Neotrop 21:1–13.
https://doi.org/10.1590/1676-­0611-­BN-­2020-­1063
Passos P, Fernandes R (2008) Revision of the Epicrates cenchria com-
plex (Serpentes: Boidae). Herpetol Monogr 22(1):1–30
Passos P, Fernandes R, Bérnils RS, Moura-Leite JC (2010) Taxonomic
revision of the Brazilian Atlantic Forest Atractus (Reptilia:
Serpentes: Dipsadidae). Zootaxa 2364:1–63
Pereira-Filho GA, Montingelli GG (2011) Check list of snakes from the
brejos de altitude of Paraíba and Pernambuco. Brazil Biota Neotrop
11:145. https://doi.org/10.1590/S1676-­06032011000300011
Pereira-Filho GA, Vieira WLS, Montingelli GG et  al (2017)
Diversidade. In: Pereira-Filho GA, Vieira WLS, Alves RRN, França
FGR (eds) Serpentes da Paraíba. Diversidade e Conservação, João
Pessoa, pp 55–269
Pereira-Filho GA, Freitas MA, Vieira WLS et al (2020) State of knowl-
edge and conservation of the snake fauna of the Brejos de Altitude in
the Pernambuco Endemism Center, Northeastern Brazil. Ethnobiol
Conserv 9:1–15
Pianka ER (1966) Latitudinal gradients in species diversity: a review of
concepts. Am Nat 100(910):33–46
Pires MG, Da-Silva NJ Jr, Feitosa DT et  al (2014) A new species of
triadal coral snake of the genus Micrurus Wagler, 1824 (Serpentes:
Elapidae) from northeastern Brazil. Zootaxa 3811:569–584. https://
doi.org/10.11646/zootaxa.3811.4.8
Prates I, Rivera D, Rodrigues MT, Carnaval AC (2016) A mid-­
Pleistocene rainforest corridor enabled synchronous invasions
of the Atlantic Forest by amazonian anole lizards. Mol Ecol
2016(25):5174–5186. https://doi.org/10.1111/mec.13821
QGIS Development Team (2022) QGIS geographic information sys-
tem. Open source geospatial foundation project. https://qgis.org/en/
site/
R Development Core Team (2021) A language and enviroment for sta-
tistical computing. Viena, Austria
Roberto IJ, Ávila RW, Melgarejo AR (2015) Répteis (Testudines,
Squamata, Crocodylia) da Reserva Biológica de Pedra Talhada.
In: Studer A, Nusbaumer L, Spichiger R (eds) Biodiversidade da
Reserva Biológica de Pedra Talhada (Alagoas-Pernambuco, Brasil),
Boissiera, vol 68, pp 357–375
11  Composition, Species Richness, and Conservation of the Reptiles of the Highly Threatened Northern Brazilian Atlantic Forest
Roberto IJ, Oliveira CR, Araujo Filho JA et  al (2017) The herpeto-
fauna of The Serra do Urubu mountain range: a key ­biodiversity
area for conservation in the brazilian Atlantic Forest. Pap Av Zool
57(27):347–373. https://doi.org/10.11606/0031-­1049.2017.57.27
Rodrigue MT, Bertolloto CEV, Amaro RC et al (2014) Molecular phy-
logeny, species limits, and biogeography of the Brazilian endemic
lizards genius Enyalius (Squamata: Leiosauridae): An example of
the historical relationship between Atlantic Forest and Amazonia.
Mol Phyl Evol 81(2014):137–146. https://doi.org/10.1016/j.
ympev.2014.07.019
Roll U, Feldman A, Novosolov M et al (2017) The global distribution of
tetrapods reveals a need for targeted reptile conservation. Nat Ecol
Evol 1:1677–1682. https://doi.org/10.1038/s41559-­017-­0332-­2
Santana GG, Vieira WLS, Pereira-Filho GA et al (2008) Herpetofauna
em um fragmento de Floresta Atlântica no estado da Paraíba,
região nordeste do Brasil. Biotemas 21:75–84. https://doi.
org/10.5007/2175-­7925.2008v21n1p75
Tabarelli M, Santos AMM (2004) Uma breve descrição sobre a história
natural dos brejos nordestinos. In: Pôrto KC, Cabral JJP, Tabarelli
M (eds) Brejos de altitude em Pernambuco e Paraíba: História natu-
ral, ecologia e conservação. Ministério do Meio Ambiente, Brasília,
pp 99–110
Tabarelli M, Siqueira-Filho JA, Santos AMM (2006) A floresta Atlântica
ao norte do Rio São Francisco. In: Pôrto KC, Cortez JA, Tabarelli M
(eds) Diversidade biológica e conservação da Floresta Atlântica ao
norte do Rio São Francisco. Ministério do Meio Ambiente: Coleção
Biodiversidade, Brasília, pp 21–35
View publication stats
183
Thomas WW, Barbosa MR (2008) Natural vegetation types in the
Atlantic Coastal Forest of northeastern Brazil. Mem NY Bot Gard
100:6–20
Tonini JFR, Ferrari TB, Fenker J et  al (2021) Os determinantes da
diversidade biológica da herpetofauna neotropical. In: Toledo LF
(ed) Herpetologia Brasileira Contemporânea. Sociedade Brasileira
de Herpetologia, São Paulo, pp 159–172
Ulrich W, Almeida-Neto M, Gotelli NJ (2009) A consumer’s
guide to nestedness analysis. Oikos 118:3–17. https://doi.
org/10.1111/j.1600-­0706.2008.17053.x
Vasconcelos TS, Prado VHM, da Silva FR, Haddad CFB (2014)
Biogeographic distribution patterns and their correlates in the
diverse frog fauna of the Atlantic Hotspot. PLoS One 9(8):e104130.
https://doi.org/10.1371/journal.pone.0104130
Werneck FP, Giugliano L, Collevatti RG et al (2009) Phyllogeny, bio-
geography and evolution of clutch size in south American lizards of
the genus Kentropyx (Squamata: Teiidae). Molec Ecol 18:262–278.
https://doi.org/10.1111/j.1365-­294X.2008.03999.x
Xavier AL, Guedes TB, Napoli MF (2015) Biogeography of anurans
from the poorly known and threatened coastal sandplains of eastern
Brazil. PLoS One 10(6):e0128268. https://doi.org/10.1371/journal.
pone.0128268
Zamudio KR, Greene HW (1997) Phylogeography of the bush-
master (Lachesis muta: Viperidae): implications for neotropi-
cal bio­geography, systematics, and conservation. Biol J Linn Soc
62:421–442