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
Animal Biodiversity and Conservation in Brazil’s
Northern Atlantic Forest
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
Editors
Gentil Alves Pereira Filho Frederico Gustavo Rodrigues França
Departamento de Biologia Departamento de Engenharia e Meio Ambiente
Universidade Estadual da Paraíba Universidade Federal da Paraíba
Campina Grande, Paraíba, Brazil Rio Tinto, Brazil

Rômulo Romeu Nóbrega Alves Alexandre Vasconcellos

Departamento de Biologia Departamento de Sistemática e Ecologia
Universidade Estadual da Paraíba Universidade Federal da Paraíba
Campina Grande, Paraíba, Brazil João Pessoa, Brazil

ISBN 978-3-031-21286-4    ISBN 978-3-031-21287-1 (eBook)

https://doi.org/10.1007/978-3-031-21287-1

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Preface

The Atlantic forest biome stretches over 3000 km from the state of Rio Grande do Norte south
to Rio Grande do Sul. This huge distance spans great latitudinal, climatic, and economic dif-
ferences, from only 8° south of the equator to the subtropics in the south. Thus, the Araucaria
forests in the south, and the forests of the Serra do Mar in the states of Rio de Janeiro and São
Paulo are cooler, better protected, and much better studied than the northeastern forests in
Alagoas, Pernambuco and Paraíba. The northeastern Atlantic forests formed a narrow fringe
extending only 50–100 km inland, over terrain that is relatively flat. Thus, they were easily
cleared for farming and especially for huge sugarcane plantations. The remaining fragments
are critically endangered as are their flora and fauna.
Studies of the plants and animals have been ongoing in northeastern Brazil, but with several
differences. Collections of plants, regardless of the taxonomic order, are grouped together
while those of animals are usually held separately, in part because they require different meth-
ods of storage. Also, although plants are more difficult to identify than most groups of verte-
brates, they are much easier to identify than the incredibly diverse invertebrate fauna. Over the
last 20 years, there has been significant progress in digitizing animal and plant specimen data,
and images of the specimens themselves. In part, because plant specimens are flat and grouped
together, great progress has been made in making Brazilian plant specimen data available
online through SpeciesLink and the REFLORA program. Although the Brazilian zoological
community is making great strides now to digitize their specimen data (almost 2  million
records available on SpeciesLink), the amount of data currently available is roughly only 20%
of the data available for plants. The data provided in this book, therefore, are both timely and
unavailable elsewhere.
The first chapter puts the remaining chapters in context by describing the vegetation, forest
fragmentation, endemism, and protected areas in the region. Ten chapters detail the diversity,
biogeography, and endemism of different animal groups in the Atlantic forest of northeastern
Brazil, especially within the Pernambuco Center of Endemism. While the chapters on mam-
mals, birds, and reptiles are to be expected, the data they contain on species diversity, numbers
of endemic and endangered species, and biogeography are new and up to date. The Amphibia
are less well-known in the region, but the analysis of literature and specimen records also pro-
vides the most current information available on this threatened group. Of the animals discussed
in the chapters of this book, the fish are unique in that they do not inhabit forests, but are found
in the streams that flow through, or used to flow through, the forests. They are under heavy
threat and pressure from fishing and from agricultural runoff.
One of the unique features of this book are the five chapters on invertebrate groups. Two
chapters are on conspicuous insects, butterflies and scarab beetles. These chapters detail the
numbers of species, their biogeographic patterns, and their conservation requirements. A less
well-understood group of insects, the termites are also discussed, including details of their
diversity, urban ecology, and conservation. Although everyone knows of spiders, few under-
stand their diversity and ecological impact. These are discussed here along with their high level
of endemism in the region. The most mysterious and least well-known group of animals dis-
cussed here are the harvestmen (Opiliones). They are evolutionarily ancient and spider-like in
appearance, with many in the northeastern Atlantic forest still undescribed today.

v
vi Preface

Two chapters discuss the anthropic pressure on the terrestrial vertebrates and fishes. The
hunting pressure on large terrestrial animals is intense and has led to at least seven species
being included on the IUCN Red List. Fishing pressure is high, as is the effect of agricultural
runoff, leading to 17 fish species being included in the Brazilian Red List of endangered spe-
cies. The last chapter summarizes the region’s rich diversity and the environmental pressures
leading to erosion of forest integrity and species diversity. It ends with recommendations for
governmental actions required to preserve what is left of this amazing forest.
This is an enormous contribution to our knowledge of the fauna in the northeastern Atlantic
forest area and unites a huge amount of previously unavailable data.

The New York Botanical Garden William Wayt Thomas

New York City, NY, USA
Acknowledgements

We are grateful to the authors for accepted writing high-quality chapters in a short amount of
time as well as for sharing their knowledge and information of the northern Atlantic Forest
along the 15 chapters of this book. We are also in debt with the important contribution made
by all reviewers who worked to help the quality of this book. We thank Springer Press for
believing in our idea and giving us all the support during the whole process, specially to Mr.
Zachary Romano, Mr. Vinesh Vinayagam and Mr. Ragavendar Mohan. We are grateful to the
Universidade Federal da Paraiba (UFPB), Universidade Estadual da Paraiba (UEPB) and
Conselho Nacional de Desenvolvimento e Pesquisa (CNPq) and Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for support and the productivity grant
awarded to Rômulo RN Alves and Alexandre Vasconcellos.

vii
Contents

1 An
 Introduction to the Knowledge of Animal Diversity and Conservation
in the Most Threatened Forests of Brazil�����������������������������������������������������������������   1
Frederico Gustavo Rodrigues França, Alexandre Vasconcellos,
Rômulo Romeu Nóbrega Alves, and Gentil Alves Pereira Filho
2 Northern
 Atlantic Forest: Conservation Status and Perspectives �������������������������   7
Adriana M. Almeida and Alexandre F. Souza
3 Ants
 (Hymenoptera: Formicidae) in the Pernambuco Endemism Center
of the Brazilian Atlantic Forest���������������������������������������������������������������������������������  23
Rogério R. Silva, Joudellys Andrade-Silva, Lívia Pires do Prado,
Jacques Hubert C. Delabie, Inara Roberta Leal, and Rodrigo M. Feitosa
4 The
 Butterfly Fauna of the Northern Atlantic Forest���������������������������������������������  33
André Victor Lucci Freitas, Jessie Pereira Santos,
Augusto Henrique Batista Rosa, Douglas Henrique Alves Melo,
Carlos Eduardo Beserra Nobre, Larissa Nascimento dos Santos,
and Márcio Zikán Cardoso
5 Dung
 Beetles from the Atlantic Forest North of the São Francisco River: An
Overview of a Fragile Fauna�������������������������������������������������������������������������������������  47
Luciana Iannuzzi, Carolina N. Liberal, André B. Reis, João Paulo Nunes,
Thamyrys B. Souza, Fábio C. Costa, João Carlos da S. Regueira,
Mario Jardim Cupello, Bruno K. C. Filgueiras, Fredy Alvarado,
Renato P. Salomão, Mateus S. E. C. Lima, and Priscila P. Lopes
6 The
 Most Endemic Taxon of an Area of Endemism: Harvestmen (Opiliones)
Fauna of NAF and Its Contribution to Biogeography and Conservation�������������  85
Adriano Medeiros DeSouza and Marcio Bernardino DaSilva
7 The
 Spider Fauna of the Northern Brazilian Atlantic Forest: Effect
of Sampling Bias on Diversity Patterns and Conservation������������������������������������� 103
Leonardo Sousa Carvalho, Philip Russo, Antonio Domingos Brescovit,
Márcia Oliveira-Tomasi, Ubirajara de Oliveira, and Adalberto José dos Santos
8 Termites
 from the Northern Atlantic Forest, Brazil: Ecology
and Conservation ������������������������������������������������������������������������������������������������������� 121
Alexandre Vasconcellos, Eliana Marques Cancello,
Flávia Maria da Silva Moura, Joice Paulo Constantini,
Matilde Vasconcelos Ernesto, Alane Ayana Vieira de Oliveira Couto,
and Antônio Carvalho da Silva Neto
9 Fishes
 from the Northern Atlantic Forest and Their Conservation����������������������� 133
Manoela M. F. Marinho, Sergio M. Q. Lima, Roney E. C. de Paiva,
and Telton P. A. Ramos

ix
x Contents

10 Species
 Richness, Distribution Pattern, and Conservation of Amphibians
in the Northern Portion of the Brazilian Atlantic Forest ��������������������������������������� 147
Washington Luiz Silva Vieira, Geraldo Jorge Barbosa de Moura,
Francisco Vicente Macedo Júnior, Gindomar Gomes Santana, Tamí Mott,
Marcos Jorge Matias Dubeux, Filipe Augusto Cavalcanti do Nascimento,
and Kleber Silva Vieira
11 Composition,
 Species Richness, and Conservation of the Reptiles
of the Highly Threatened Northern Brazilian Atlantic Forest������������������������������� 169
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
12 Bird
 Diversity and Conservation of the Northern Atlantic Forest������������������������� 185
Helder F. P. Araujo, Hermínio A. L. S. Vilela, Benjamin Phalan,
and Pedro F. Develey
13 Mammals
 of the Pernambuco Endemism Center: Diversity, Biogeography,
Research Gaps, and Conservation Concerns����������������������������������������������������������� 201
Anderson Feijó, Mayara Beltrão, Anna Ludmilla da Costa-­Pinto,
Patrício Adriano da Rocha, Marco Antônio de Freitas,
Bruno Augusto Torres Parahyba Campos, Diego Astúa,
and Pedro Cordeiro-Estrela
14 Fisheries
 and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian
Atlantic Forest������������������������������������������������������������������������������������������������������������� 229
Rômulo Romeu Nóbrega Alves, Márcia Freire Pinto,
Anna Karolina Martins Borges, and Tacyana Pereira Ribeiro Oliveira
15 Hunting
 and Uses of Terrestrial Vertebrates in the Northernmost Region
in the Atlantic Forest in Brazil����������������������������������������������������������������������������������� 257
Rômulo Romeu Nóbrega Alves, José Aécio Alves Barbosa,
and Anna Karolina Martins Borges
Index������������������������������������������������������������������������������������������������������������������������������������� 275
Contributors

Fredy  Alvarado Instituto Potosino de Investigación Científica y Tecnológica, Divison de

Ciencias Ambientales, San Luis Potosí, México
Joudellys  Andrade-Silva  Coordenação de Ciências da Terra e Ecologia, Museu Paraense
Emílio Goeldi, Belém, PA, Brazil
Diego Astúa  Laboratório de Mastozoologia, Departamento de Zoologia, CB, Universidade
Federal de Pernambuco, Recife, PE, Brazil
José Aécio Alves Barbosa  Universidade Federal de Campina Grande, Campina Grande, PB,
Brazil
Mayara Beltrão  Museu de Zoologia, Universidade de São Paulo, São Paulo, SP, Brazil
Anna  Karolina  Martins  Borges  Universidade Estadual da Paraíba, Campina Grande, PB,
Brazil
Antonio  Domingos  Brescovit Laboratório Especial de Coleções Zoológicas, Instituto
Butantan, São Paulo, SP, Brazil
Bruno Augusto Torres Parahyba Campos  Programa de Pós-graduação em Biodiversidade
Meio Ambiente e Saúde, Universidade Estadual do Maranhão, Caxias, MA, Brazil
Eliana Marques Cancello  Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil
Márcio Zikán Cardoso  Departamento de Ecologia, Universidade Federal do Rio de Janeiro,
Rio de Janeiro, RJ, Brazil
Leonardo Sousa Carvalho  Campus Amílcar Ferreira Sobral, Universidade Federal do Piauí,
Floriano, PI, Brazil
Joice Paulo Constantini  Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil
Pedro Cordeiro-Estrela  Laboratório de Mamíferos, Departamento de Sistemática e Ecologia,
CCEN, Universidade Federal da Paraíba, João Pessoa, PB, Brazil
Fábio  C.  Costa  Departamento de Zoologia, Universidade Federal de Pernambuco, Recife,
PE, Brazil
Mário Jardim Cupello  Departamento de Zoologia, Universidade Federal do Paraná, Curitiba,
PR, Brazil
Anna  Ludmilla  da Costa-Pinto Museu de História Natural, Universidade Federal de
Alagoas, Maceió, AL, Brazil
Rômulo  Romeu  Nóbrega  Alves Departamento de Biologia, Universidade Estadual da
Paraíba, Campina Grande, PB, Brazil
Patrício  Adriano  da Rocha Programa de Pós-Graduação em Ciências Biológicas,
Universidade Federal da Paraíba, João Pessoa, PB, Brazil

xi
xii Contributors

Flávia Maria da Silva Moura  Laboratório de Pesquisa em Ensino, Zoologia e Conservação,

CSTR, Universidade Federal de Campina Grande, Campina Grande, PB, Brazil
Antônio Carvalho da Silva Neto  Laboratório de Termitologia, Departamento de Sistemática
e Ecologia, CCEN, Universidade Federal da Paraíba, João Pessoa, PB, Brazil
Marcio Bernardino da Silva  Universidade Federal da Paraíba, João Pessoa, PB, Brazil
Adriana  M.  de Almeida Departamento de Ecologia, CB, Universidade Federal do Rio
Grande do Norte, Campus Universitário, Natal, RN, Brazil
Helder  Farias  Pereira  de Araújo Departamento de Biociência, Universidade Federal da
Paraíba, Areia, PB, Brazil
Rafaela  Candido  de França  Programa de Pós-graduação em Ecologia e Conservação da
Biodiversidade, Universidade Estadual de Santa Cruz, Ilhéus, BA, Brazil
Marco  Antônio  de Freitas Instituto Chico Mendes de Conservação da Biodiversidade
(ICMBio), ESEC Murici, Murici, AL, Brazil
Jacques Hubert C. Delabie  Laboratório de Mirmecologia, Centro de Pesquisas do Cacau,
Comissão Executiva do Plano da Lavoura Cacaueira, Ilhéus, BA, Brazil
Universidade Estadual de Santa Cruz, Ilhéus, BA, Brazil
Fagner Ribeiro Delfim  Departamento de Sistemática e Ecologia, Centro de Ciências Exatas
e da Natureza, Universidade Federal da Paraíba, João Pessoa, PB, Brazil
Geraldo  Jorge  Barbosa  de Moura  Laboratório de Estudos Herpetológicos e
Paleoherpetológicos, Universidade Federal Rural de Pernambuco, Recife, PE, Brazil
Alane Ayana Vieira de Oliveira Couto  Estação Experimental de Cana-de-açúcar do Carpina,
Universidade Federal Rural de Pernambuco, Recife, PE, Brazil
Tacyana Pereira Ribeiro de Oliveira  Universidade Estadual da Paraíba, João Pessoa, PB,
Brazil
Ubirajara  de Oliveira Centro de Sensoriamento Remoto, Instituto de Geociências,
Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
Roney E. C. de Paiva  Laboratório de Ictiologia Sistemática e Evolutiva, Departamento de
Botânica e Zoologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte,
Natal, RN, Brazil
Adriano Medeiros de Souza  Universidade Federal da Paraíba, João Pessoa, PB, Brazil
Alexandre F. de Souza  Departamento de Ecologia, CB, Universidade Federal do Rio Grande
do Norte, Natal, RN, Brazil
Pedro  F.  Develey  Sociedade para a Conservação das Aves do Brasil  – SAVE Brasil, São
Paulo, SP, Brazil
Filipe Augusto Cavalcanti do Nascimento  Laboratório de Biologia Integrativa, Instituto de
Ciências Biológicas e da Saúde, Universidade Federal de Alagoas, Maceió, AL, Brazil
Lívia Pires do Prado  Laboratório de Hymenoptera, Museu de Zoologia da Universidade de
São Paulo, Ipiranga, São Paulo, SP, Brazil
Adalberto  José  dos Santos Departamento de Zoologia, Instituto de Ciências Biológicas,
Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
Larissa Nascimento dos Santos  Programa de Pós-Graduação em Ecologia, Departamento de
Ecologia, Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil
Contributors xiii

Marcos  Jorge  Matias  Dubeux Programa de Pós-Graduação em Biologia Animal,

Departamento de Zoologia, Instituto de Biociências, Universidade Federal de Pernambuco,
Recife, PE, Brazil
Matilde Vasconcelos Ernesto  Laboratório de Termitologia, Departamento de Sistemática e
Ecologia, CCEN, Universidade Federal da Paraíba, João Pessoa, PB, Brazil
Anderson  Feijó Key Laboratory of Zoological Systematics and Evolution, Institute of
Zoology, Chinese Academy of Sciences, Beijing, China
Rodrigo M. Feitosa  Departamento de Zoologia, Universidade Federal do Paraná, Curitiba,
PR, Brazil
Bruno K. C. Filgueiras  Departamento de Zoologia, Universidade Federal de Pernambuco,
Recife, PE, Brazil
Gentil  Alves  Pereira  Filho  Departamento de Biologia, Universidade Estadual da Paraíba,
Campina Grande, Paraíba, Brazil
Frederico  Gustavo  Rodrigues  França Departamento de Engenharia e Meio Ambiente,
Centro de Ciências Aplicadas e Educação, Universidade Federal da Paraíba UFPB, Rio Tinto,
PB, Brazil
André Victor Lucci Freitas  Departamento de Biologia Animal and Museu de Diversidade
Biológica, Instituto de Biologia, Unicamp, Campinas, SP, Brazil
Thais Barreto Guedes  Centro de Estudos Superiores de Caxias, Universidade Estadual do
Maranhão, Caxias, MA, Brazil
Luciana Iannuzzi  Departamento de Zoologia, Universidade Federal de Pernambuco, Recife,
PE, Brazil
Francisco Vicente Macedo Júnior  Programa de Pós-Graduação em Biodiversidade, Centro
de Ciências Agrárias, Universidade Federal da Paraíba, Areia, PB, Brazil
Inara  Roberta  Leal Departamento de Botânica, Universidade Federal de Pernambuco,
Recife, PE, Brazil
Carolina N. Liberal  Departamento de Biologia, Universidade Federal Rural de Pernamuco,
Recife, PE, Brazil
Mateus S. E. C. Lima  Departamento de Biologia, Universidade Federal Rural de Pernamuco,
Recife, PE, Brazil
Sergio  M.  Q.  Lima Laboratório de Ictiologia Sistemática e Evolutiva, Departamento de
Botânica e Zoologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte,
Natal, RN, Brazil
Priscila P. Lopes  Departamento de Ciências Biológicas, Universidade Estadual de Feira de
Santana, Feira de Santana, BA, Brazil
Manoela M. F. Marinho  Laboratório de Sistemática e Morfologia de Peixes, Departamento
de Sistemática e Ecologia/CCEN, Universidade Federal da Paraíba, João Pessoa, PB, Brazil
Douglas  Henrique  Alves  Melo Programa de Pós-Graduação em Biologia Animal,
Departamento de Zoologia, Universidade Federal de Pernambuco, Recife, PE, Brazil
Daniel  Oliveira  Mesquita Departamento de Sistemática e Ecologia, Centro de Ciências
Exatas e da Natureza, Universidade Federal da Paraíba, João Pessoa, PB, Brazil
Tamí Mott  Laboratório de Biologia Integrativa, Instituto de Ciências Biológicas e da Saúde,
Universidade Federal de Alagoas, Maceió, AL, Brazil
xiv Contributors

Carlos  Eduardo  Beserra  Nobre Programa de Pós-Graduação em Biologia Animal,

Departamento de Zoologia, Universidade Federal de Pernambuco, Recife, PE, Brazil
Pedro  Salles  Nunes Laborratório de Herpetologia, Departamento de Zoologia, Centro de
Biociências, Universidade Federal de Pernambuco, Recife, PE, Brazil
Márcia  Oliveira-Tomasi Pós-Graduação em Zoologia, Instituto de Ciências Biológicas,
Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
João  Paulo  N.  A.  Pereira Departamento de Biologia, Universidade Federal Rural de
Pernamuco, Recife, PE, Brazil
Benjamin Phalan  Parque das Aves, Foz do Iguaçu, PR, Brazil
Márcia Freire Pinto  Universidade Estadual do Ceará, Limoeiro do Norte, CE, Brazil
Telton  P.  A.  Ramos  Laboratório de Sistemática e Morfologia de Peixes, Departamento de
Sistemática e Ecologia/CCEN, Universidade Federal da Paraíba, João Pessoa, PB, Brazil
João Carlos da S. Regueira  Departamento de Zoologia, Universidade Federal de Pernambuco,
Recife, PE, Brazil
André B. Reis  Departamento de Biologia, Universidade Federal Rural de Pernamuco, Recife,
PE, Brazil
Augusto  Henrique  Batista  Rosa Departamento de Biologia Animal and Museu de
Diversidade Biológica, Instituto de Biologia, Unicamp, Campinas, SP, Brazil
Philip  Russo  Pós-Graduação em Zoologia, Instituto de Ciências Biológicas, Universidade
Federal de Minas Gerais, Belo Horizonte, MG, Brazil
Renato P. Salomão  Programa de Pós Graduação em Ecologia, Instituto Nacional de Pesquisas
da Amazônia, Manaus, AM, Brazil
Gindomar  Gomes  Santana Laboratório de Herpetologia (Integrado ao Laboratório de
Etnoecologia), Departamento de Biologia, Centro de Ciências Biológicas e da Saúde,
Universidade Estadual da Paraíba, Campina Grande, PB, Brazil
Jessie  Pereira  Santos Departamento de Biologia Animal and Museu de Diversidade
Biológica, Instituto de Biologia, Unicamp, Campinas, SP, Brazil
Rogério  R.  Silva Coordenação de Ciências da Terra e Ecologia, Museu Paraense Emílio
Goeldi, Belém, PA, Brazil
Thamyrys B. Souza  Instituto Nacional da Mata Atlântica, Santa Teresa, ES, Brazil
Alexandre  Vasconcellos Laboratorio de Termitologia, Departamento de Sistemática e
Ecologia, CCEN, Universidade Federal da Paraíba, João Pessoa, PB, Brazil
Kleber  Silva  Vieira Bolsista CNPq pelo Programa de Desenvolvimento Científico e
Tecnológico Regional, Universidade Estadual da Paraíba, Campina Grande, PB, Brazil
Washington  Luiz  Silva  Vieira Laboratório de Ecofisiologia Animal, Departamento de
Sistemática e Ecologia da Universidade Federal da Paraíba, João Pessoa, PB, Brazil
Hermínio A. L. S. Vilela  Sociedade para a Conservação das Aves do Brasil – SAVE Brasil,
São Paulo, SP, Brazil
 An Introduction to the Knowledge
of Animal Diversity and Conservation
in the Most Threatened Forests of Brazil
Frederico Gustavo Rodrigues França,
Alexandre Vasconcellos, Rômulo Romeu Nóbrega Alves,
and Gentil Alves Pereira Filho
Abstract
This chapter provides a brief overview on the following
chapters and highlights the relevance of research focusing
on the current animal knowledge in the Northern Atlantic
Forest. The book was written by more than 70 researchers
from more than 20 universities and institutes from Brazil,
China, and Sweden and sought to provide a comprehensive
update on biodiversity, biogeography, and the conservation
status of a sector that presents high anthropogenic pressure
and that has the lower original cover of the Atlantic Forest.
Keywords
Anthropogenic pressures · Atlantic Forest · Biodiversity ·
Biogeography · Conservation status
1.1 Introduction
The importance of the Atlantic Forest, both biologically and
economically, is already widely known and published
(Galindo Leal and Câmara 2003; Scarano and Ceotto 2015;
Rezende et al. 2018). This biome harbors stupendous biodi-
F. G. R. França (*)
Departamento de Engenharia e Meio Ambiente, CCAE,
Universidade Federal da Paraíba, João Pessoa, Paraíba, Brazil
e-mail: frederico.franca@academico.ufpb.br
A. Vasconcellos
Laboratório de Termitologia, Departamento de Sistemática e
Ecologia, CCEN, Universidade Federal da Paraíba,
João Pessoa, Paraiba, Brazil
R. R. Nóbrega Alves
Departamento de Biologia, Universidade Estadual de Campina
Grande, Campina Grande, Paraiba, Brazil
G. A. P. Filho
Departamento de Biologia, Universidade Estadual da Paraíba,
Campina Grande, Paraíba, Brazil
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
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_1
1
versity and an enormous rate of endemism, even though it
has been facing massive impacts from exploitation and frag-
mentation (Ribeiro et al. 2009; Scarano 2014). Endemic spe-
cies with geographic distribution restricted to different
portions of the Atlantic Forest were fundamental for the
comprehension and recognition of regions with different bio-
geographic histories known as centers of endemism (Silva
and Casteleti 2003). The Northern Atlantic Forest (NAF),
also called by several authors as the Pernambuco Endemism
Center (PEC) or Pernambuco Center of Endemism, is  the
section of the Atlantic Forest located in Northeast Brazil
northern from São Francisco River and distributed through
the states of Alagoas, Pernambuco, Paraíba, and Rio Grande
do Norte (Silva and Casteleti 2003; Tabarelli and Roda 2005;
Chap. 2).
The “Pernambuco” was one of the “Centers of Rainforest
Endemism” first suggested by the British botanist Ghillean
Tolmie Prance (1982). Prance found floristic similarities and
endemic species in distinct regions, defining them as 26 dis-
tinct “Centers of Rainforest Endemism.” For the Atlantic
Coastal Brazil, Prance recognized three well-defined areas:
Pernambuco, the most northern area; Bahia and northern
Espírito Santo, located in the middle range of the biome; and
Rio de Janeiro and Espírito Santo south of the Rio Doce, the
southernmost area (Prance 1982).
Although these “Centers of Endemism” have been
reviewed in subsequent papers, the Pernambuco Endemism
Center (or Northern Atlantic Forest) has remained as a dis-
tinct unit through several different works (Silva and Casteleti
2003; Tabarelli and Roda 2005; Tabarelli et  al. 2010;
Carvalho et al. 2021). Despite its importance, the NAF rep-
resents less than 5% of the original Atlantic Forest, and the
remaining forest is now comprised of small forest fragments
scattered in urban and agricultural matrices throughout its
distribution (Silva and Tabarelli 2001).
Human impact on the NAF has been taking place since
before the European occupation of the Brazilian Northeast in
the beginning of the sixteenth century (Dean 2004). However,
1
2 F. G. R. França et al.
the arrival of the Portuguese and the successive cycles of
colonization of the northeastern coast intensified the damage
in this region. The exploitation started with the extraction of
timber of Pau-Brasil (Paubrasilia echinata), then land clear-
ing for pastures, and culminated in the establishment of large
sugar cane plantations, for sugar production and, more
recently, for production of fuel alcohol (Coimbra-Filho and
Câmara 1996) (Fig. 1.1). The history of occupation and frag-
mentation of the Brazilian Atlantic Forest, especially the
NAF, has been documented by several authors (Freyre 1985;
Dean 2004; Siqueira Filho and Leme 2006; Scarano 2014).
Nevertheless, we can consider that the ecological history of
the NAF has been characterized by strong resistance and
high resilience. Even after centuries of intensive occupation
and use resulting in this high degree of fragmentation (see
Chap. 2), the region still has high biodiversity in various ani-
mal groups, high heterogeneity throughout its geographical
range (Fig. 1.2), and high rates of endemism, as can be seen
in all the chapters in this book.
All forest patches found in different ecoregions through
the extension of the NAF still provide a glimpse of the bio-
logical magnitude that this area contained in the past.
Nowadays, this environmental diversity extending from
tropical moist forests (Pernambuco coastal forest and
Pernambuco interior forest or “brejos de altitude”) to
Mangrove forests and tropical semideciduous forests
(Tabuleiro), still forms a background for the emergence and
recognition of new species such as the frog Adelophryne nor-
destina (Lourenço-de-Moraes et  al. 2021), the snake
Caaeteboia gaeli (Montingelli et al. 2020), or the bird Trogon
muriciensis (Dickens et al. 2021). On the other hand, local
extinction and population decline of vertebrate species have
been recorded throughout the Atlantic Forest and a long and
consistent history of hunting pressure, habitat conversion
and fragmentation, or a synergistic combination of both
(Canale et al. 2012).
As the human pressure on these NAF fragments remains
high, we are looking at the countdown to extinction for many
endemic species (Brooks and Rylands 2003). Undeniably,
the NAF is one of the regions on the planet where conserva-
tion efforts are most needed. It should be considered a
hotspot within one of the most important and threatened
hotspots—the Atlantic Forest (Tabarelli and Roda 2005).
1.2 Why This Book?
The publications about the animal diversity of the NAF
reflect a phenomenal effort, but there is an absence of a sin-
gle literature source gathering general information of the ani-
mal diversity of the region. We decided to write this book
with the collaboration of experts on the vertebrate and inver-
tebrate fauna. This was a hard task and demanded a massive
effort of 81 scientists from more than 20 universities and
institutions from Brazil, China and Sweden.
This book presents the first synthesis of the knowledge of
animal ecology and conservation of NAF.  Although work
has already been published about some groups, for example,
mammals (Asfora and Pontes 2009; Garbino et  al. 2018),
snakes (França et al. 2020; Pereira Filho et al. 2021), birds
(Silva et al. 2004), and bees (Nemesio and Santos Jr 2014),
all chapters of this book present new and detailed informa-
tion and are far from a simple species list, since many eco-
logical and biogeographical analyses were performed.
Dealing with such a highly diverse region, some questions
easily come to mind, such as: How much forest is left in this
region? How is the richness, diversity, and endemism of each
studied group? Where are the gaps of knowledge and what
areas are the most surveyed? Are there new species to be
described, and are there species that are disappearing? Is
there a congruence for the richest areas or those with fewer
species when comparing different animal groups? Which
animal groups are facing the countdown to extinction? Each
of these questions is answered in detail in all chapters of this
book.
The book is organized into 15 chapters. Following this
introduction, Chap. 2 presents an overview of the landscape,
fragmentation, vegetation cover, and the distribution of pro-
tected areas in the NAF.  This chapter provides a reviewed
base-map of the area that will be referred to in all the follow-
ing chapters. An analysis of more than 2000 native forest
satellite images gives approximately 750,000  ha of native
Atlantic Forest remnants. Most of the patches are small, with
41% smaller than 1 ha, and only 11% of the PEC region is
within Protected Areas.
Chapters 3, 4, 5, 6, 7, and 8 deal with the invertebrate
diversity of the NAF. Taxonomy, ecology, biodiversity short-
falls, biogeographical patterns, and conservation data of ants
(Hymenoptera), butterflies (Lepidoptera), beetles
(Coleoptera, Scarabaeinae), harvestmen’s (Opiliones), spi-
ders (Aranae), and termites (Isoptera) are investigated,
described, and summarized. Chapters 9, 10, 11, 12, and 13
focus on vertebrate diversity of the NAF.  The authors
explored the richness and endemism, biogeographical
dynamics, and conservation status for freshwater fishes
(Osteichthyes), frogs, toads, and caecilians (Lissamphibia),
turtles, lizards, snakes, and caimans (Reptilia), birds (Aves),
and mammals (Mammalia). Finally, Chaps. 14 and 15 pro-
vide an overview of the ethnozoology studies in the
NAF. Chapter 14 discusses the importance of fishery activi-
ties in the region. Chapter 15 finishes the book’s information
about vertebrates of NAF used by human population,
With the vast amount of information distributed in all 15
chapters, we do hope the Northern Atlantic Forest can be
considered as an emergency area for conservation and bio-
logical research. This is not the first time this sector of the
1  An Introduction to the Knowledge of Animal Diversity and Conservation in the Most Threatened Forests of Brazil 3

Fig. 1.1  Sugarcane fields (a) and pastures (b) cleared from the Northern Atlantic Forest in Paraiba and Alagoas, respectively

Atlantic Forest has been considered fundamental for conser- and hunting are still scarce. Considering the coastal frag-
vation, although efforts like the creation of new protected ments and the inland remnants (Brejos de Altitude), the pan-
areas and environmental inspection to combat deforestation orama is more severe in the inland forests, once these regions
4 F. G. R. França et al.

Fig. 1.2  Examples of environmental heterogeinity in the Northern Atlantic Forest. (a) Restinga forest and coastal cliffs (Rio Grande do Norte) (b)
Coastal Mangrove forest (Pernambuco)
1  An Introduction to the Knowledge of Animal Diversity and Conservation in the Most Threatened Forests of Brazil
are less protected by the actions of the environmental inspec-
tions and now face an accelerated rhythm of deforestation for
housing purposes and water exploitation (Pereira-Filho et al.
2021). The fact is that one of the richest portions of the
Brazilian Atlantic Forest is under permanent threat and in
need of more scientific research and creation of protected
areas. Certainly, the tipping point for the Atlantic Forest is
closer than we thought, and the statistics of deforested area
and extinction rates are strong evidence of this panorama.
We are facing an imminent risk of losing this forest if serious
measurements are not taken in a short amount of time.
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 Northern Atlantic Forest: Conservation
Status and Perspectives
Adriana M. Almeida and Alexandre F. Souza
Abstract
The Atlantic Forest is a biodiversity hotspot and is widely
known both for its high species richness, including many
endemics, and also by its high degradation, with few forested
areas left. The Northern Atlantic Forest (NAF) lies in the
northernmost part of the biome, suffering from an old frag-
mentation process and with little remaining forest. In
Northeastern Brazil, we also find some areas called “Brejos
Nordestinos” that are enclaves of high-altitude humid forests
embedded in the Caatinga semiarid region. A careful analy-
sis of a 2019 forest cover map revealed a total of 747,926 ha
of remaining forest (18.8%) distributed in 63,048 fragments
(41% are smaller than 1 ha). There are only 896 forest frag-
ments larger than 100 ha, covering an area of 437,434.6 ha.
The NAF region has a few large fragments with large interior
(core) forests. When considering a 90-m-edge influence,
core area drops to 216,628.0  ha (30% of the area in frag-
ments larger than 1 ha and 5.4% of the NAF area). A total of
10.5% of the NAF region is composed of Protected Areas
(PA), from which 9.7% is under sustainable use and 0.8% is
under strictly protection. More protected areas are needed to
achieve the global goal of 17% of protected areas, and their
placement should be considered in order to efficiently con-
serve the NAF biodiversity and its ecosystem services, creat-
ing a landscape with high connectivity. Protected Areas also
must have efficient management plans, so that biodiversity
protection will be effective.
Keywords
Centro de Endemismo de Pernambuco · Pernambuco
Endemism Center · Brejos Nordestinos · Brejos de
A. M. Almeida (*) · A. F. Souza
Departamento de Ecologia, CB, Universidade Federal do Rio
Grande do Norte, Campus Universitário, Natal, RN, Brazil
e-mail: adriana.almeida@ufrn.br
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
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_2
2
Altitude · Rain forest · Habitat fragmentation ·
Landscape analysis
2.1 The Brazilian Atlantic Forest
The Atlantic Forest occurs along most of the Brazilian coast
and the beautiful view of the forest landscape may be the first
image of Brazil to most foreign visitors. Already inhabited
by various indigenous groups, in the sixteenth century, it was
colonized by Europeans (Solórzano et al. 2021). The Atlantic
Forest is home to more than 125 million people (ca. 60% of
Brazil’s population and 35% of the South American popula-
tion) (Scarano and Ceotto 2015; Lima et al. 2020), contrib-
utes to 70% of the gross domestic product (GDP), two-thirds
of the industrial economy, and has some of Brazil’s most
productive land (more than half of the national land dedi-
cated to horticulture) (Joly et al. 2014; Rezende et al. 2018).
Metropolises like São Paulo and Rio de Janeiro are situated
within Atlantic Forest domain. The Atlantic Forest is world-
wide known both for its high species diversity and degrada-
tion. With little forested area left, and divided into small and
isolated fragments, it is considered one of the most frag-
mented tropical/subtropical forests in the world (Laurance
2009; Metzger 2009; Ribeiro et  al. 2009; Rezende et  al.
2018; Lima et al. 2020).
The original Atlantic Forest spanned a latitudinal gradient
from 3°S to 31°S, and from 35°W to 60°W, covering 3300 km
of Brazilian coastline and 148,194,638  ha (approximately
17.4% of the Brazilian territory) (Metzger 2009; Ribeiro
et al. 2009). It also spans into Paraguay and Argentina, com-
prising mostly evergreen and seasonally dry forests (Metzger
2009; Ribeiro et al. 2009). With both a long latitudinal gradi-
ent and a great altitudinal variation (from sea level to ca.
2800  m), the Brazilian Atlantic Forest encompasses many
diverse climates, soils, and reliefs (Metzger 2009).
The Atlantic Forest climate is highly heterogeneous,
including many Köppen climate zones, with a strong north-­
7
8 A. M. Almeida and A. F. Souza
south temperature gradient (Alvares et al. 2013). Most of the
climate in this Atlantic region is tropical, varying from humid
tropical climates in the north to temperate climates with
moderate summer in the south (Alvares et  al. 2013). In its
southeastern and southernmost portions, the Atlantic Forest
covers a rough topography that includes major mountain
ranges along the coastline, such as “Serra do Mar,” “Serra da
Mantiqueira,” and “Serra Geral,” where altitudes reach up to
ca. 2800  m (Metzger 2009, Cantidio and Souza 2019). In
Northeastern Brazil, with one exception, topography has no
major accidents, and altitude variations are restricted to
smaller mountain ranges with well-marked limits in relation
to the surrounding lowlands. The exception is “Chapada
Diamantina,” in Bahia state, with altitudes that reach up to
2000 m. Further north, the Borborema highlands (“Serra da
Boborema”) runs in a north-south direction for about 400 km,
spanning Alagoas, Pernambuco, Paraíba, and Rio Grande do
Norte states. In Northeastern Brazil, we can also find moun-
tainous refuges known as “Brejos Nordestinos” or “Brejos
de Altitude” (Northeastern Forest islands), which are moun-
tains with tropical wetter climate located further west, repre-
senting enclaves inserted in semiarid regional climates (the
Brazilian biome called Caatinga) (Porto et al. 2004; Alvares
et al. 2013).
Being home to native pre-Colombian populations since
Late Pleistocene, a period in which it was subjected to little
anthropogenic changes (Lira et  al. 2021; Solórzano et  al.
2021), the Atlantic Forest has suffered extensive deforesta-
tion since the sixteenth century, with European arrival. First
with logging and hunting, and lately with deforestation to
agriculture and human settlements (e.g., Dean 1997; Cabral
and Cesco 2008; Lins-e-Silva et al. 2021; Lira et al. 2021;
Solórzano et al. 2021).
Recent studies accessed the remaining Atlantic Forest
cover. Ribeiro et al. (2009), considering patches larger than
3 ha, estimated that native forest cover ranges from 11.4% to
16%. A more recent study based on 5-m-high-resolution
imagery showed that native vegetation cover in 2013 had a
28% coverage, from which 26% was forest cover and 2%
was nonforest native formations (Rezende et al. 2018). Rosa
et al. (2021) studied the Atlantic Forest native forest cover
dynamic (gains and losses) from 1990 to 2017. They showed
that the apparent stability of vegetation cover hides the fact
that older forests are being replaced by younger ones, result-
ing in a “rejuvenation” of the forest. This observation is
alarming, since not all species are able to live in young for-
ests, and such forests may not provide all ecosystem ser-
vices, in comparison to mature forests (Rosa et  al. 2021).
Atlantic Forest fragments’ size and isolation are also a prob-
lem, since few fragments are really large, undisturbed, and
really protected from human influences (Ribeiro et al. 2009;
Lima et al. 2020).
In the Atlantic Forest, a multitude of productive and
diverse environments are home to a huge number of species,
many endemics. The Atlantic Forest is globally recognized
for its high species diversity, accounting from 1% to 8% of
the world’s plant and vertebrate species (Myers et al. 2000).
Studies suggest that there are at least 20,000 species distrib-
uted through vascular plants, amphibians, reptiles, birds, and
mammals (Figueiredo et al. 2021). Endemism is also high,
accounting for 57% of its vascular flora and 77% of its epi-
phytic vascular flora (Freitas et al. 2016). Animals also pres-
ent high endemism, with 16% bird, 27% mammal, 31%
reptile, and 60% amphibian fauna only found there
(Mittermeier et  al. 2005; Metzger 2009; Figueiredo et  al.
2021). Taking into consideration Atlantic Forest’s high deg-
radation and high levels of species richness and endemism, it
is considered a biodiversity hotspot (Myers et al. 2000), and
maybe even “the hottest hotspot” (Laurance 2009). Hotspot
areas concentrate half of the species in the planet, within 1%
of its area and are key points for conservation (Myers et al.
2000; Laurance 2009).
A recent study (Lima et al. 2020) estimated that human-­
induced impacts on forest biodiversity and biomass are
pervasive across the Atlantic Forest fragments, with
impacts that can be 42% higher if compared to the pre-
dicted for a human-free scenario. Human-induced losses
are stronger in the abundance of endemic tree species, sug-
gesting that endemics are being replaced by generalist spe-
cies. They also found that late-successional tree species
abundance is also strongly impacted by humans. Important
to remember that large trees are ecosystem engineers and
play a fundamental role in community structure (Lima
et al. 2020).
With its past and present impacts, humans now have a
chance to turn the Atlantic Forest’s trajectory of degradation
into a new path of nature protection and restoration, warrant-
ing a sustainable future, where society’s vulnerability to cli-
mate change is reduced. Some initiatives such as restoration
programs and payment for ecosystem services are reasons
for optimism (Scarano and Ceotto 2015). Atlantic Forest still
has a chance to be transformed from a hotspot to a hopespot
(Scarano and Ceotto 2015; Rezende et al. 2018; Lira et al.
2021).
Species composition in the Atlantic Forest is not distrib-
uted homogenously and presents some “Endemism Centers”
(Andrade-Lima 1982; Silva and Casteleti 2003, 2005).
Considering endemic species of birds, primates and butter-
flies, Silva and Casteleti (2003, 2005) identified five ende-
mism centers and three transition zones. With one exception
to “Serra do Mar,” in southeastern Brazil, all other four cen-
ters are in Northeastern Brazil. They are all composed of
humid forests and are called: Pernambuco, Diamantina,
Bahia and “Brejos Nordestinos” centers. Since the
2  Northern Atlantic Forest: Conservation Status and Perspectives
“Pernambuco Endemism Center” spans four Brazilian states,
in this text it will be called “Northern Atlantic Forest”
(NAF) from now on. The term is synonym to “Pernambuco
Endemism Center” (Andrade-Lima 1982; Silva and Casteleti
2003) and “Pernambuco biogeographical sub-region” (Lins-­
e-­Silva et al. 2021) in previous studies.
The Northeastern Brazilian coast is cut by a large river, the
São Francisco River, which separates Alagoas and Sergipe
states. North of São Francisco River we can find two Brazilian
endemism centers, the Northern Atlantic Forest and “Brejos
Nordestinos” (Andrade-Lima 1982; Silva and Casteleti 2003;
Porto et al. 2004; Tabarelli et al. 2005). The Northern Atlantic
Forest (NAF) is a subset of Atlantic Forest in its most northern
part, occurring from latitudes 5.0°S to 10.5°S, in Northeastern
Brazil, encompassing four Brazilian states: Rio Grande do
Norte (RN), Paraíba (PB), Pernambuco (PE), and Alagoas
(AL) (Fig. 2.1). The “Brejos Nordestinos” are found in eleva-
tions covered by semideciduous forest vegetation. Also known
as “Brejos de Altitude,” they occur in altitudes and present
vegetation that differs from the smaller, deciduous predomi-
nant one on the drier lowlands (Fig. 2.2) (Lopes et al. 2017).
The “Brejos Nordestinos” enclaves occur mainly in
Fig. 2.1  Northern Atlantic Forest and “Brejos Nordestinos” (black dots), in Brazil. Numerals in Brejos refer to Table 2.1. RN—Rio Grande do
Norte state, PB—Paraíba state, PE—Pernambuco state and AL—Alagoas state
9
Pernambuco and Paraiba, but also in Rio Grande do Norte and
Ceará states. Although all are important, here we consider
only the “Brejos” in the east of Borborema highlands, in
Pernambuco and Paraíba states (Table 2.1).
2.2 The Northern Atlantic Forest
The region occurs mainly through Barreiras Formation
and Borborema highlands. Barreiras is a sedimentary geo-
logical formation widespread along the Brazilian coast,
occurring throughout the Northeastern and Southeastern
regions up to Rio de Janeiro State, being particularly well
represented along numerous but discontinuous coastal
cliffs (Rossetti and Goes 2009). The NAF relief is mostly
plain with maximum altitude ca. 1000  m in Borborema
Highlands, in Pernambuco and Paraíba States. NAF has a
humid tropical climate (Köppen’s As’), with dry summer
and autumn-­winter rains, rainfall ranging from 750 to
1500  mm per year, and monthly-average temperatures
above 18  °C (Tabarelli et  al. 2006;  Alvares et  al. 2013).
Vegetation is composed mainly of humid tropical forests
10 A. M. Almeida and A. F. Souza

Fig. 2.2  “Brejos Nordestinos” are enclaves of high-altitude humid forests embedded in the semiarid climate. (a) Areia, Paraiba state (point 3 in
Fig. 2.1 and Table 2.1). (b) Bonito, Pernambuco state (point 12 in Fig. 2.1 and Table 2.1). (Credit photos to: Flávia Maria da Silva Moura)
2  Northern Atlantic Forest: Conservation Status and Perspectives 11

Table 2.1  Geographical and administrative information on the “Brejos Nordestinos” considered (code numbers refer to Fig. 2.1)
Code Name State Municipality Latitude (°W) Longitude (°S) Altitude (m)
1 Araruna PB Araruna 6.55 35.73 532
2 Bananeiras PB Bananeiras 6.75 35.62 500
3 Areia PB Areia 6.95 35.67 540
4 Alagoa Nova PB Alagoa Nova 7.07 35.75 531
5 Taquaritinga PE Taquaritinga 7.90 36.02 765
6 Bezerros PE Bezerros 8.32 36.42 671
7 Brejo dos Cavalos PE Caruaru 8.27 35.97 550
8 Serra Negra PE Bezerros 8.22 35.77 560
9 Gravatá PE Gravata 8.20 35.53 518
10 Camocim de São Felix PE Camocim de São Felix 8.35 35.75 656
11 Agrestina PE Agrestina 8.45 35.93 560
12 Bonito PE Bonito 8.47 35.72 655

in a mosaic of ombrophilous and semideciduous forests,
encompassing also “restingas,” “tabuleiros,” and man-
groves (the Atlantic Forest lato-sensu) (Tabarelli et  al.
2006).
Although the Northern Atlantic Forest encompasses only a
small portion of Atlantic Forest’s original geographical range,
it is home to many species. Roda (2003) estimated that two-
thirds of all bird species and subspecies of Atlantic Forest are
found there, with 417 endemic bird species occurring only in
NAF. In a recent biogeographical analysis of the Atlantic Forest
flora, the NAF has been confirmed as having a distinctive flora
of tree, shrub, and palm species (Cantidio and Souza 2019).
Two Brazilian states (Rio Grande do Norte and Paraíba)
are sometimes excluded from Atlantic Forest studies in the
NAF area (e.g., Tabarelli et  al. 2005; Ribeiro et  al. 2011).
Occurring in a narrow and small area and covered by many
clouds, being situated in the intertropical convergence zone,
this region is difficult to visualize in satellite images. In the
present study, the entire scope of the NAF area is considered,
covering all the four Brazilian states.
2.3 “Brejos Nordestinos” or “Brejos de
Altitude”
The geomorphology of the Brazilian northeastern region is
marked by the occurrence of mountain ranges and plateaus
with local climates that are more humid and rainier than the
average of the surrounding plains. Regionally these eleva-
tions were, and to a large extent still are, covered by semide-
ciduous forest vegetation known as “Brejos de Altitude”
occurring in altitudes mostly above 500 m, with greater bio-
mass and complexity than the smaller, deciduous vegetation
predominant on the drier lowlands (Lopes et al. 2017). These
areas have thus functioned as refugia for tree and shrub spe-
cies adapted to less stressful thermal and hydric conditions,
including many Myrtaceae, and many species that occur in
the neighboring vegetational domains of the Atlantic Forest,
the Amazon, and the Cerrado savanna (Diogo 2017).
In Northeastern Brazil, most of the Atlantic Forest is
inserted in a relatively narrow strip of lowland broadleaved
semideciduous and rain forests along the coastline. Further
inland the Atlantic Forest occurs as several disjunct broad-
leaved forest islands embedded in the drier lowlands domi-
nated by seasonally dry forests and woodlands (Queiroz
et  al. 2017). Overall, the different lowland seasonally dry
Caatinga vegetation types are strongly limited by rainfall
(Salimon and Anderson 2017), and forest islands are located
on the windward slopes of highlands that receive orographic
rainfall able to sustain semideciduous or evergreen forests
mainly in Pernambuco and Paraiba, but also in Rio Grande
do Norte and Ceará states.
Orographic rainfall produces resource gradients running
from hotter and drier climates in lowlands to cooler and wet-
ter climates upland. Data from two sites in Paraíba pointed to
changes in vegetation and soil properties accompanying ele-
vational changes in temperature and rainfall (Ramos et  al.
2020). The increase in productivity with altitude led to
changes in vegetation structure: tree density declines but
total aerial biomass increases with altitude, indicating habitat
change from lowland vegetation dominated by many thin
and branched trees to submontane vegetation with fewer but
larger trees. Increases in elevation are accompanied by
increased soil clay content, acidity, aluminum, and organic
matter, and reduced base saturation. Drought stress reduction
with increased elevation is the likely cause in the increased
species diversity in higher altitudes (Silva et al. 2014; Lopes
et  al. 2017; Ramos et  al. 2020). Few studies have investi-
gated vegetation response to different topographic positions
and terrain exposures like top, windward, and leeward slopes.
However, available evidence indicates significant effects on
stem density, basal area, species richness, and dominance
12
(Silvera et  al. 2020; Diogo et  al. 2021), with species like
Senegalia polyphilla, associated with drier leeward slopes
and species like Cupania impressinervia, associated with
windward slopes (Diogo et al. 2021). Mountain tops seem to
be less affected by tree fall and display higher basal area
while rainier windward slopes may show increased stem
density. This suggests increased natural mortality in wind-
ward slopes, perhaps by increased treefall gaps.
There is evidence that species composition follows the
diminishing stress conditions with increased altitude, segre-
gating species groups at different altitudinal belts (Lopes
et  al. 2017). The issue, however, of which mechanisms
exactly determine species sorting between different moun-
tain ranges and between sectors within each mountain range
remains debated. It has been shown that niche differences
between dry forest species produce spatial segregation along
soil nutrient, disturbance history, and wetness gradients
(López-Martínez et  al. 2013; Ramos et  al. 2020). Other
results, however, indicate broad niche overlap between spe-
cies across environmental gradients (Pulla et al. 2017). In the
lack of more conclusive studies, the issue of the relative
importance of ecological factors like changing temperature,
rainfall, soil texture, soil nutrients, and anthropogenic distur-
bance on the species community assembly of the Caatinga
mountain ranges remains to be fully resolved. A confound-
ing factor that accompanies the changes in productivity with
elevation is human disturbance. Lowland dry forest sites
usually suffer from chronic anthropogenic disturbance by
removal of firewood and grazing by goats and cattle, and
these impacts tend to reduce with altitude (Silva et al. 2014).
Chronic anthropogenic disturbance is believed to favor pio-
neer species like Cenostygma pyramidale, Croton heliotropi-
ifolius, and Croton blanquetianus (Ribeiro et al. 2015; Rito
et al. 2017), which have been found to be abundant in lower
altitudes of the mountain ranges (Ramos et al. 2020).
In several mountainous forests of northeastern Brazil,
Myrtaceae is the most abundant botanical family, and Myrcia
splendens is frequently one of the most dominant species
(Silvera et al. 2020; Diogo et al. 2021). A macroecological
comparison of 24 broadleaved semideciduous forests in
northeastern Brazil, many of them located in mountainous
localities, found a broad division between windward and lee-
ward slopes. Forests located on the windward and wetter
slopes of the Borborema mountain range had greater floristic
affinity with the Atlantic Forest. To the west, we find those
species located on the drier leeward slopes of the Borborema
plateau and isolated eroded peaks that punctuate the semi-
arid Caatinga lowlands (Rodal et al. 2008). This second and
drier mountainous group includes a more heterogeneous
mixture of genera originating in the Caatinga lowlands like
Myracroduon and Schinopsis, and genera originating in wet-
ter more forested areas like Rollinia and Diospyros.
Comparisons spanning geographically more scattered sites
A. M. Almeida and A. F. Souza
have revealed that the floristic composition of the Caatinga
mountain forests is considered as a mixture of species with
Amazon, Atlantic Forest, and Caatinga distributions, and
suggested that western forest enclaves like Baturité in Ceará
State have closer affinities with the Amazon flora than with
other enclaves within the Caatinga (Santos et al. 2007). The
largest macroecological comparison of the “Brejos
Nordestinos,” however, has been carried out by Diogo
(2017), using thousands of localities scattered across the
entire Amazon, Caatinga, Cerrado, and Atlantic Forest
biomes. Contrary to the conception that mountain enclaves
would be floristically more similar to the Atlantic Forest to
the east, to the Caatinga seasonally dry forest to the west, and
to the Amazon flora in the north (Queiroz et  al. 2017), he
found a great number of exclusive trees and shrubs in the
enclaves, characterized the composition of the mountainous
enclaves as distinct from that of all studied biomes, and iden-
tified the Brazilian Northeast Mountain Forests (BNMF) as a
new bioregion with its exclusive species and characteristics.
Diogo (2017) identified that the most common species in
BNMF were Manilkara rufula, Wedelia villosa, and
Guettarda angelica, and the most indicative species were
Guettarda angelica and Manilkara rufula.
During parts of its geological past, Northeastern Brazil
was under wetter climates, which have been associated with
the southward displacement of the Intertropical Convergence
Zone (Wang et  al. 2004). The isolated mountain forests
embedded in the seasonally dry Caatinga vegetation are
regarded as interglacial microrefugia, or relics of a past
expansion of forested connections between the Amazon and
the Atlantic Forest (Santos et al. 2007; Montade et al. 2014).
This conclusion has received support from the macroeco-
logical analyses of floristic relationships between the moun-
tainous enclaves (Diogo 2017), palynological reconstructions
(Montade et al. 2014), niche modeling (Silveira et al. 2019),
and cladistic aerogram analyses (Santos et  al. 2007).
Projection of abiotic niche envelopes of 13 species represen-
tative of the semideciduous to humid Northern Atlantic
Forest suggests an expansion of wetter forests into what is
currently seasonally dry forest and woodland during the Last
Glacial Maximum, with enclaves in Paraiba and Pernambuco
having moderate connectivity with coastal Atlantic Forest
(Silveira et al. 2019).
2.4 Northern Atlantic Forest History
The region occupied by the NAF is the nearest to Europe and
was heavily visited for brazilwood extraction (pau-brasil:
Paubrasilia echinata (Lam.) Gagnon, H.  C. Lima & G.  P.
Lewis) in the first years of the sixteenth century (Dean 1997;
Lira et al. 2021; Solórzano et al. 2021). Pernambuco state is
situated in the middle of NAF and was an important point of
2  Northern Atlantic Forest: Conservation Status and Perspectives
brazilwood extraction since the beginning of colonization
(Dean 1997; Lins-e-Silva et  al. 2021; Lira et  al. 2021;
Solórzano et  al. 2021). Brazilwood extraction was quickly
added to sugarcane agriculture. The sugarcane cycle (“ciclo
da cana”) started very early in 1516 in Itamaracá island (PE),
only 16  years after Brazil’s discovery. Soon, in 1549,
Pernambuco state had already 30 sugar farms and was con-
sidered the richest region in Brazil (Dean 1997). Sugarcane
farms spread to the coasts of all states of NAF, with a strong
impact in its Atlantic Forest (Dean 1997; Lins-e-Silva et al.
2021; Lira et al. 2021; Solórzano et al. 2021). The Atlantic
Forest degradation took some steps. First of all, came defor-
estation to clean the area for sugarcane. Sugarcane planting
was also based on burning the areas, so that it is easier to
plant again. Such burning practice impoverished the soil in a
few years, and more deforestation for new planting areas
were needed. Sugarcane farms also used firewood in its sugar
production process, which impacted surrounding forests
even more (Dean 1997; Lins-e-Silva et al. 2021; Lira et al.
2021; Solórzano et al. 2021).
For five centuries, NAF was converted mostly for sugar-
cane plantations, but also for other human uses, such as set-
tlements, cattle, and mining (Lins-e-Silva et  al. 2021; Lira
et al. 2021; Solórzano et al. 2021). More recently, from the
1970s, Brazil implemented a sugarcane agriculture stimulus
called “Pró-álcool,” with many incentives to alcohol produc-
tion as a green fuel as a substitute to gas fuel (Lins-e-Silva
et  al. 2021; Lira et  al. 2021; Solórzano et  al. 2021). This
stimulus has reinforced sugarcane farms in the area.
Nowadays, the Atlantic Forest in NAF is considered the least
protected and the most endangered region in all Atlantic
Forest (Ranta et al. 1998; Silva and Casteletti 2005; Tabarelli
et al. 2006).
2.5 Northern Atlantic Forest Landscape
Analysis
A forest cover map of the year 2019 was obtained from the
MapBiomas Project, version 5.0. The MapBiomas Project is
a multi-institutional initiative to generate annual land-use
and land-cover maps from automatic classification processes
applied to satellite images with a 30  m resolution (http://
mapbiomas.org) (Souza et al. 2020). We considered only the
“Forest formation” class (“Florestas Nativas,” classes 1 and
2) inside the NAF shape. This image has 87.1% accuracy.
Since our objective was to analyze forest formations, the
classes “restingas,” sand dunes and mangroves, mostly com-
posed of shrubs, were not considered here. The “Brejos
Nordestinos” enclaves outside NAF were not considered in
the landscape analysis, because of the unavailability of their
border’s delimitation.
13
To obtain a recent land use and land cover assessment of
NAF, we first defined its external limits (shape). We used the
recent Atlantic Forest shapefile definition created by INPE
(“Instituto Nacional de Pesquisas Espaciais”—Brazilian
National Institute for Space Research). This shapefile is
recent (2019) and is very accurate with both the Brazilian
Atlantic Forest Law (Law 11428/2006) and Brazilian coast-
line (Assis et al. 2019). This shape is the one used nowadays
to monitor deforestation in the area (Assis et al. 2019). The
Atlantic Forest shape was then cut by the São Francisco
River, to create a Northern Atlantic Forest polygon delimita-
tion in QGIS (2021).
The Mapbiomas map was then used to access the NAF
current situation in relation to forest cover and fragmenta-
tion. Fragmentation occurs when a continuous area is “bro-
ken” into smaller and isolated parts, called fragments (Fahrig
2003, 2017). Fragments of different sizes, degrees of isola-
tion and shapes tend to present distinct influences on the spe-
cies that will be able to inhabit it. In general, larger, more
regular-shaped, and more heterogeneously filled fragments
support more species (McGarigal 2015; Turner and Gardner
2015 and references therein).
Fragmentation creates edges. Forests near the edge suffer
changes in abiotic conditions and, consequently, on species
and ecological process when compared to patch interiors
(called core areas). Forest edges in general have increased
light availability, are warmer, with drier microclimates than
the forest’s core. Forest edges are also in constant contact
with the surrounding  matrix, and susceptible to external
influences, such as fire, exotic species, pesticides, and even
increased human impacts (selective logging and hunting)
(Gascon et  al. 2000; Cochrane and Laurance 2002; Ewers
and Didham 2006; Lima et al. 2020). The core area is espe-
cially important to interior species and is not directly related
to area, but to fragment’s shape, since large fragments may
not have large core areas to support interior species if they
are simultaneously long and narrow, for example (McGarigal
2015). It is important to note that the relative amount of edge
versus interior habitat varies with patch size and shape.
Considering fragments of regular shapes, smaller ones will
have a greater portion of edge area than larger fragments
(Turner and Gardner 2015). The edge’s extension varies
greatly among fragments and regions, and different species
respond differently, with some effects being deeper than oth-
ers, and changing under the influence of factors such as edge
age, number of nearby edges, and the adjoining matrix of
modified vegetation surrounding fragments (Laurance et al.
2011).
Fragment area is of great importance to biodiversity.
When considering fragments of regular shape, larger frag-
ments support more species and more individuals when com-
pared to smaller ones in the same region (Turner and Gardner
14
2015). Larger fragments may have a higher local environ-
mental heterogeneity, with more food and habitat resources.
Larger areas also support larger populations, which assures a
high genetic diversity, with increased adaptive potential
(Reed and Frankham 2003; Dixo et al. 2009). Larger areas
also support larger-sized species, mostly top-predator ones,
that control herbivores and warrant a high diversity of plant
species (e.g., Estes et  al. 2011). Fragment shape is also of
crucial importance, and fragments of the same size can pres-
ent diverse shapes. Shape refers to the form of the fragment.
For the same area, a circular shape will have the least edge
area, and a long narrow shape (riparian forests, for example)
may present an only-edge habitat (depending on the width)
(Turner and Gardner 2015). Complex, irregular shapes trans-
late into strong edge effects (Ewers and Didham 2006;
McGarigal 2015; Turner and Gardner 2015).
Finally, isolation must also be considered. Species need
minimum size areas to keep a population. In a fragmented
habitat, connectedness is necessary to sum small areas and
keep the minimum viable population size. Different species
present distinct dispersal abilities, and isolation may be a
very important factor. In this context, small fragments
(stepping-­stones) and corridors may be crucial in facilitating
connectedness and mitigating isolation deleterious effects
(Villard and Metzger 2014; Siqueira et al. 2021).
To access the landscape configuration within NAF, some
landscape metrics were calculated, considering the
8-­neighbor rule, in Fragstats v. 4.0 (McGarigal et al. 2012)
and analyzed in R (2021). First, metrics related to area and
perimeter were obtained to all existing fragments (ca.
60,000 fragments). Then, some specific metrics were applied
to the subset of fragments larger than 1 ha (ca. 37,400 frag-
ments). Fragments smaller than 1 ha are very numerous and
may not be adequate to keep populations of most species. On
the other hand, they have high conservation value as stepping
stones, being important in connectivity, and considered as
“small landscape elements” (SLE) by Siqueira et al. (2021).
The calculated metrics were fragment size (AREA), shape
(SHAPE) and Euclidean nearest neighbor distance (ENN).
The area index (AREA) gives the area of each patch (in ha).
The Shape index (SHAPE) compares the fragment form to a
square of the same area and varies from 1 when shape is a
square and increases without limit as fragment shape
becomes more irregular (McGarigal 2015). The Euclidean
nearest neighbor distance (ENN) is the shortest straight-line
distance between the focal patch and its nearest neighbor,
based on the distance between the cell centers of the two
closest cells from the respective patches (McGarigal 2015).
To access the amount of edge effect and core area, we also
applied the metrics: core area (CORE), number of core areas
in each patch (NCORE), and core area index (CAI) to the
subset of fragments larger than 1  ha. The core area index
(CORE) is the area within a patch that is not influenced by
A. M. Almeida and A. F. Souza
edge effect. To obtain CORE, first, we must define the edge
size, or how far edge effects penetrate the fragments. CORE
is zero when the whole fragment is under edge influence, and
value grows as more interior area remains. Core area was
calculated considering an edge effect of 90  m (3  pixels).
Previous studies have shown that 90–100 m is a good estima-
tor of edge influence to tropical forests (Cochrane and
Laurance 2002; Paula et  al. 2016) and more specifically
Atlantic Forest (Lima et al. 2020). At least one study showed
that the 100 m is a good estimator of edge effect for trees in
NAF (Oliveira et al. 2004). The number of core areas in each
patch (NCORE) gives the number of disjunct interior core
areas in each patch after the influence of the edge effect is
applied. The core area index (CAI) quantifies the percentage
of the patch that comprises the core area (McGarigal 2015).
To analyze the area under protection in NAF, we obtained
data from State and Federal Protected Areas (PAs). Brazilian
law considers protected areas under strictly protection (IUCN
categories I–IV) or sustainable use ones (IUCN categories
V–VI) (National System of Conservation Units—SNUC,
Law 9.985/2000). Protected areas shapefiles were obtained in
the official database on protected areas of the Ministry of
Environment (MMA 2021). In Brazil, government-­managed
protected areas can be federal, state, or municipal, depending
on the hierarchical level of its creation and administration.
Protected Areas under municipal administration were not
considered here since it is difficult to obtain their data. Private
Natural Heritage Reserves (RPPN, “Reserva Particular do
Patrimônio Natural”) are sustainable use PAs and were also
considered. Their shapefiles and data were obtained also in
the official database on protected areas of the Ministry of
Environment (MMA 2021) and complemented with
SIMRPPN database (“Sistema Informatizado de Monitoria
de RPPN,” RPPN Monitoring System) (ICMBio 2021). A
total of 10 RPPNs did not have available shapefiles. In this
case, the UC area was obtained from the SIMRPPN site.
A total of 17 small, protected areas are situated inside the
limits of seven larger APAs (locally known as “Environmental
Protection Areas,” a class of sustainable use PA) in NAF:
APA Aldeia-Beberibe, APA Barra do Rio Mamanguape,
APA Bonfim-Guaraíra, APA do Catolé e Fernão Velho, APA
Guadalupe, APA Murici, and APA Santa Cruz. These 17
small PAs sum 68,567.52 ha, and their overlapping area was
not considered in the sum of PA area in NAF. The APA defi-
nition allows for the existence of nested private lands inside
their limits. This class of PA may be the one with the least
protection in Brazil, and Lima et al. (2020), analyzing biodi-
versity and biomass erosion on Atlantic Forest, observed that
this class performed worse than both strictly protection and
sustainable use PAs. Silva et al. (2022) found that an impor-
tant portion of the functional diversity of the Atlantic Forest
is only weakly protected because they are found mostly
within APAs.
2  Northern Atlantic Forest: Conservation Status and Perspectives
2.6 Current Status of Vegetation Cover
The Northern Atlantic Forest (NAF) encompasses an area
of almost 4,000,000 ha (3,986,988.10 ha). This area corre-
sponds to a very small portion of 2.70% of all the Atlantic
Forest area. In NAF, we detected 747,926.73  ha of forest
cover (18.76%), distributed in 63,048  fragments, varying
from 0.09  ha (the pixel size) to 25,175.43  ha (but see
below). The amount of forest cover in NAF is a little more
than the 11–16% cover detected by Ribeiro et  al. (2009)
(but they did not consider fragments smaller than 3 ha), but
lower than the 28% cover detected by Rezende et al. (2018)
(but they considered also nonforest natural formations).
Species loss is expected under a fragmentation threshold of
10–30%, since habitat loss may be fatal for most species
(Fahrig 1997; Villard and Metzger 2014). Forest cover in
NAF is thus in a critical condition and deserves careful
attention.
In the NAF, fragment size distribution is strongly influ-
enced by very small fragments, which are very numerous,
but sum a small area. Only 37,397 fragments are larger than
1 ha, showing a worrisome value of almost half (40.7%) of
fragments of tiny size (less than 1 ha). There are only 896
fragments larger than 100 ha and they represent 1.42% of the
total number (Fig. 2.3). When considering larger than 1 ha
fragments, their area is 705,144.8 ha, representing 17.69% of
Fig. 2.3  Forest coverage in Northern Atlantic Forest, Brazil, distrib-
uted per fragments class size. Bars are divided into core (interior)
(darker green) and edge areas, considering a 90 m of edge influence.
15
the total NAF area, while larger than 100 ha fragments span
an area of 437,434.6 ha and represent 10.97% of NAF area.
Fragments larger than 100  ha represent 58.49% of the
remaining forest (Fig. 2.3).
Other regions in the Brazilian Atlantic Forest present a
better situation than found in NAF, with much larger forest
remnants. In all the Atlantic Forest, only one remnant has an
area of more than 1 million ha of continuous forest and is
situated in “Serra do Mar,” along the coastal mountains of
São Paulo. This mountain range, in fact, has many forest
fragments larger than 50,000 ha (Ribeiro et al. 2009). Few
other remnants larger than 50,000 can be also found in Santa
Catarina and Iguaçu National Park (both southern Brazil)
(Ribeiro et al. 2009). In Bahia region (Northeastern Brazil,
but south of NAF), the largest one is 29,000 ha large (Ribeiro
et al. 2009).
A careful inspection of the fragments’ size results detected
that the mapping resolution (30 m pixel) generated a coarse
map that resulted in the fusion of smaller patches and created
artificial patches that seemed to be very large. In the NAF,
when observing the three fragments larger than 10,000 ha in
a finer resolution in Google Earth Pro 7.3.4.8248 (64-bit)
(November 2021), we detected that what seemed to be a
large fragment is in fact a group of fragments. One example
is the third “largest fragment,” situated in Rio Grande do
Norte state (RN). It is in fact a group of fragments connected
Values above columns are the number of fragments in each class. Note
that the x-axis is log-transformed
16
Fig. 2.4  Atlantic Forest fragment in Northern Atlantic Forest, Rio
Grande do Norte. This is an example of a fragment that seems to be
large, but, in fact, is an artifact of the use of the 8-neighbor-rule and a
30 m pixel. This fragment is almost totally inserted in a sugarcane farm,
and windbreaks connected some small fragments, mistakenly creating a
nonexisting large remnant in the area (see Fig  2.5). (Map generated
by windbreaks (most of them composed of Eucalyptus, but
also by degraded secondary forest) and are mostly inside a
sugarcane farm (Figs. 2.4 and 2.5). This is a clear example of
what seemed to be a good forest fragment, but, in fact, is a
group of smaller ones of poor quality. Important to note that
we used the same map and method to all NAF analysis, and
this “resolution artifact” could also  have occurred in frag-
ments of all sizes.
Fragment size should not be used singly as an estimator of
good habitat condition. In Fig. 2.6, it is possible to compare
two large fragments found in the area. The first one is in APA
Aldeia Beberibe (Pernambuco state, PE), with 18,604.9  ha
but with an irregular size and 61% of core area (Fig. 2.6a,
Table 2.2). The second one is in REBIO Serra Talhada (also
in PE) with 6261.8  ha but with a more regular shape and
72.4% of core area (Fig. 2.6b, Table 2.2).
Taking into consideration that the fragments’ size may
not be the best surrogate for native forest health in NAF, we
decided to rank fragments by core area, instead of fragment
area. When considering an edge influence of 90 m in frag-
ments larger than 1 ha in the NAF, only 8186 fragments pres-
ent core area with at least 0.09 ha (one pixel) (only 21.9% of
the fragments larger than 1 ha). Also, the interior (core) area
falls to a worrisome value of 216,628.0 ha (only 30.72% of
the area of remnants above 1 ha) (Figs. 2.2 and 2.7a). The
smallest fragment with 0.09 ha core area is 3.3 ha large. Only
two fragments had core areas summing more than 10,000 ha,
but they are also a junction of smaller ones. The largest core
area was found in Santa Rita (Paraíba state, PB) in the largest
A. M. Almeida and A. F. Souza
using Google Earth. Google Earth Pro 7.3.4.8248 (64-bit) (November.
2021). Usina Estivas. Rio Grande do Norte. Brazil. 06°12′36″S.
35°14′04″W. Eye alt 42 km. Borders and labels; places layers. Images:
SIO. NOAA. USNavy. NGA. GEBCO. 2020. http://www.google.com/
earth/index.html (Accessed November 21, 2021))
remnant, with a core area of 12,711.96 ha, but divided in 582
small parts. The second largest remnant, considering core
area, is in Pernambuco state with a core area of 11,384.82 ha,
but divided into 251 parts (Table 2.2). The high number of
core areas reflects the irregular shape of the fragments and
reinforces the observation that functionally such fragments
may correspond to fragmented habitats for the subset of late-­
successional plant and animal species.
Most fragments larger than one ha in NAF presented
irregular shapes, observed by the SHAPE metrics. Shape
values varied from 1 (a square shape) to 38.43 (very irregular
shape) (Fig 2.7c). Only 277 fragments with more than 1 ha
(less than 1%) had a shape value of 1.0 (square shape)
(Fig.  2.7c). All square-shaped fragments are small, and do
not exceed 4 ha, showing that regular shapes are more easily
found in small fragments. In contrast, four fragments had a
shape index value above 25.0, and all of them are among the
five largest remnants (with disjunct core areas, see discus-
sion above) (Table 2.2). Shape is correlated to fragment area
(rs = 0.683; p < 0.001), core area (rs = 0.435; p < 0.001) and
consequently to edge effect. Core area, together with shape,
can also be a good estimator of fragment health, since the
more irregular the shape, the more the edge influence in the
fragment.
Both shape and edge influence will indicate the amount of
good interior forest (core). In the NAF, the percentage of
core area per fragment varied from 0% to 81% as shown by
the CAI index (Fig. 2.7b). A total of 29,210 fragments larger
than 1 ha (78.1%) present no core area. Taking into consider-
2  Northern Atlantic Forest: Conservation Status and Perspectives 17

Fig. 2.5  Northern Atlantic Forest fragments in Usina Estivas, Rio In this sugarcane farm, windbreaks and small fragments all connected
Grande do Norte. (a) Sugarcane in foreground and a forest fragment. and formed a large, unique fragment in analysis (see Fig. 2.4 and text).
(b) A windbreak composed of degraded forest in the foreground, a (Credit photos to: A. M. Almeida)
small fragment and farther a larger fragment in a matrix of sugarcane.
18 A. M. Almeida and A. F. Souza

Fig. 2.6  Two of the largest Northern Atlantic Forest fragments. The shape. (b) REBIO Serra Talhada (PE) (36,428°W, 9.228°S, 6261.84 ha)
forest fragment (green) is presented in contrast to the Protected Area has a fragment of smaller size than the previous one but has a more
delimitation (yellow). (a) APA Aldeia Beberibe (PE) (35.023°W, regular shape and a better percentage of good interior forest (core area).
7.893°S, 18,604.89  ha) has a large fragment, but with an irregular See Table 2.1 for the main landscape metrics for these two fragments

Table 2.2  Landscape metrics of six fragments in the Northern Atlantic Forest ordered by interior forest area (CORE), considering 90-m depth of
edge
Protected area State Area (ha) Core (ha) NCORE CAI Shape
– PB (Usina Agroval, Fazenda Pacatuba) 25,175.43 12,711.96 582 50.49 38.43
APA Aldeia Beberibe PE 18,604.89 11,384.82 251 61.19 26.32
APA Murici AL 8927.73 6320.07 60 70.79 12.34
– RN (Usina Estivas) 11,528.55 5399.19 253 46.83 24.63
REBIO Serra Talhada PE/AL 6261.84 4535.10 56 72.42 8.48
APA Piquiri-Una RN 6621.39 3631.14 97 54.84 16.47
Metrics are fragment area in ha (AREA), core area in ha (CORE), number of core areas in the fragment after the 90-m-edge effect is considered
(NCORE), proportion of core area in relation to edge (CAI), shape index (SHAPE, varies from 1 if square shape and increases without limit as
form is more irregular). (See Sect. 2.5 for more details). The Protected Area in which the fragment is inserted is also given, with the State to help
localize the area. The two fragments that are not inserted in a Protected Area are identified by the sugarcane farm name

ation fragments with at least 0.09  ha of core area, we
observed that 6043 (73.8%) of them have less than 20% of its
area as interior forests. Only 192 fragments (2.3% of frag-
ments with core areas) have interior forests with more than
50% of its area (Fig. 2.7b).
Isolation is also important. Distance, and consequently
isolation among fragments is also crucial for species pop-
ulation’s maintenance. Living in small, irregular frag-
ments, most animal species will need to transit among
them to find food, refugia and even reproductive sites. In
NAF, the average distance to the nearest neighbor, when
considering fragments larger than 1  ha, is 178.10  m
(±191.72  sd). Distance values ranged from 60  m to
3766.16 m (Fig. 2.7d). However, when all fragments are
considered (even smaller than 1  ha), average distance to
the nearest neighbor falls by its half, to 90.0 m (±142.23).
2  Northern Atlantic Forest: Conservation Status and Perspectives
Fig. 2.7  Number of fragments in the Northern Atlantic Forest distrib-
uted in classes according to each metrics. (a) Core size (ha) considering
90-m-edge. (b) Core Area (%) or CAI index (CAI gives the proportion
This shows the importance of small fragments (even less
than 1  ha) in reducing isolation, as already pointed by
Siqueira et al. (2021).
Landscapes are complex structures, and the NAF is not an
exception. Comprehension of landscape ecology needs the
observation of more than one landscape metric to better
understand the situation. In NAF, the core areas found in the
larger fragments are divided into more than 250 small cores
and in one case, more than 580 core areas (Table 2.2). Larger
fragments also presented irregular shapes, allied to a small
proportion of the core area (varying from 46% to 61%,
Table 2.2). So, fragment size must be observed with caution
and interpreted together with more information. With this in
mind, some fragments presented good structure. The first
one is in APA Murici (AL) completely inserted in Murici
Ecological Station (ESEC, Ecological Station, “Estação
Ecológica” in Portuguese, a strictly protection class) but
expands to APA Murici in its west portion (Table 2.2). This
remnant is 8927.73 ha large, but its core is 6320.07 ha (con-
sidering 90 m edge). It also has a low shape value when com-
pared to the largest ones (Table 2.2). The second one is in the
Biological Reserve Serra Talhada (PE/AL) (REBIO,
“Reserva Biológica” in Portuguese, a strictly protection
19
of area per fragment that is composed of interior forest (core) area). (c)
SHAPE index (Shape varies from 1.0 (a square) without limit, accord-
ing to more irregular shapes). (d) Distance to nearest neighbor (m)
class) (Table 2.2). The fragment is 6261.8 ha large and has
4535.1 ha of core forest, showing 72.4% of its area as good
interior forest (Table 2.2, Fig. 2.7b).
We should highlight here that our results present struc-
tural analyses based on a classified map that was obtained
from satellite images. Fragments health includes a myriad of
ecological information and should also take into consider-
ation species composition (native/endemics/exotics), pres-
ence of late successional species, large-seeded species, etc.,
as considered in Lima et al. (2020). So, remote sensing-based
map analysis brings important information, but must be
complemented with field data.
2.7 Conservation
A small fraction in the Northern Atlantic Forest is under fed-
eral, state, or private protection, totaling 418,319.29 ha. The
area in protected areas is equivalent to 10.5% of the NAF
area (overlapping PAs were not considered, see methods),
from which 9.7% is under sustainable use and only 0.8% is
under strictly protection (Table 2.3). Protected Areas are 103
altogether (municipal areas were not considered, see
20
Table 2.3  Area (ha) in Protected Areas (PAs) in Northern Atlantic
Forest. Numbers in parentheses indicate the number of PAs
Strict protection Sustainable use Total
State 17,034.01 (37) 345,949.51 (14) 362,983.53 (51)
Federal 15,127.70 (4) 32,038.98 (8) 47,166.68 (12)
Private – 8169.08 (40) 8169.08 (40)
Total 32,161.72 (41) 386,157.57 (62) 418,319.29a (103)
a
A total of 17 PAs are inserted into larger ones summing an area of
15,161.59 ha. The overlapping areas were considered only once in the
table
­ ethods), distributed in 41 strictly Protected Areas and 62
m (40%) are small structures, with less than 1 ha. More than
sustainable use ones. Almost 40% of protected areas
(40  areas, 38.8%) are Private Natural Heritage Reserves,
(RPPN) spanning an area of 8169.08 ha (Table 2.3). The area
under Government managed Sustainable Use Protected
Areas is ca. 10× larger than under strictly protection: while
Sustainable Use Protected Areas span an area of
386,157.57 ha (not considering overlapping PA), strictly pro-
tected areas cover only 32,161.72 ha (Table 2.3). Many sus-
tainable use protected areas in the region are large, with the
largest one spanning 129,523.21  ha (APA Murici, Alagoas
State). The smaller protected area has one ha (RPPN, Reserva
Particular do Patrimônio Natural Tobogã, inserted into “APA
do Catolé e Fernão Velho,” Maceió, Alagoas State).
In NAF, the area under state protection is much larger
than the federal ones, with 362,983.53 ha (87.8% of the area
in Protected Areas). Much of this area is under sustainable
use protected areas (345,949.51 ha, 95.4%), leaving less than
5% of state Protected Areas under strictly protection
(Table 2.3). Note that the strictly Protected Areas are more
numerous (37) but their total area is small.
Brejos Nordestinos are inserted in few Protected Areas. In
Pernambuco state, The APA Brejos do Capiberibe contains
one “Brejo” area called Taquaritinga. One Brejo called
Bezerros is far 3.5 km from the same APA. One Brejo area in
Paraiba state, called Bananeiras, is equally 1.5 km far from
APA do Roncador and ARIE Goiamunduba.
A recent study using high-resolution images observed that
30% of vegetation cover in the Atlantic Forest is located
inside Protected Areas, from which 9% are under strictly pro-
tection and 21% under sustainable use (Rezende et al. 2018).
In NAF, Protected Areas span a coverage of only 10.5%, and
this value should be even lower since most PAs are not
entirely filled with native forests. In NAF, the area under pro-
tection is lower than the found in the Atlantic Forest, and the
area under strictly protection is small (only 8% of the area
under protection is inside strictly protection PAs).
Protected Areas may be an ultimate refuge for wild spe-
cies in the Northern Atlantic Forest. Being a region with an
old fragmentation process, some good quality Atlantic Forest
fragments still exist because they are inside Protected Areas.
A. M. Almeida and A. F. Souza
Although Protected Areas in NAF may be effective in con-
servation of forest cover and animal species, they cover an
area of only 10.5%, which is less than the 17% target of
inland Protected Areas to the world (IUCN 2021).
2.8 Conclusion
Northern Atlantic Forest presents a total of 18.8% of the
original forest cover, distributed mostly in many isolated
fragments of small size and irregular shape. Many fragments
two-thirds of fragments have no core area, considering a
90 m edge effect. Protected Areas are responsible for 10.5%
of the NAF area, but strictly protected areas are less than 1%.
Most “Brejos Nordestinos” areas are not under formal pro-
tection. Forest loss must be stopped in NAF, and efforts must
be directed in order to improve landscape health, managing
forest quality, improving connectivity, and matrix quality.
Fragments must be managed to size augmentation, and also
connectivity expansion through corridors creation and main-
tenance (and creation) of stepping stones. More Protected
Areas must be created in NAF, and strictly protection ones
must be considered with urgency. Finally, we must do our
best to ensure that sustainable use protected areas have effi-
cient management plans, establishing adequate zoning, set-
ting aside for low-impact activities in their best-conserved
ecosystems.
Acknowledgments  We thank Lourdes M. M. Villavicencio and Maria
Izabelle C. Dantas for help in analysis with QGis and figures creation.
Rafael Leandro V. F da Silva and Diego Vinícius M. de Carvalho orga-
nized the protected areas data. We thank Flávia Maria da Silva Moura
for the “Brejos Nordestinos” photographs. We are thankful to Paula
K. Lira and José Luiz Alves da Silva for valuable and constructive sug-
gestions during the revision process, improving a lot the chapter’s qual-
ity. We also thank Alexandre Vasconcellos, Gentil A.  Pereira Filho,
Rômulo R. N. Alves, and Frederico G. R. França for the invitation to
produce the chapter.
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 Ants (Hymenoptera: Formicidae)
in the Pernambuco Endemism Center
of the Brazilian Atlantic Forest
Rogério R. Silva, Joudellys Andrade-Silva,
Lívia Pires do Prado, Jacques Hubert C. Delabie,
Inara Roberta Leal, and Rodrigo M. Feitosa
Abstract
We revised the literature on ant records in the Pernambuco
Endemism Center  – the Biogeographical Sub-Region
Pernambuco in the Atlantic Forest  – to synthesize the
information regarding the diversity and distribution of
ants in this important endemism area of the biome. We
gathered 3769 ant records, encompassing over 10 sub-
families, 71 genera, and 247 nominal species. We further
provide up-to-date information regarding the state of
knowledge, distribution gaps, and prospects for ant diver-
sity in this key region for the maintenance of biodiversity
of the Brazilian Atlantic Forest.
Keywords
Northern Atlantic Forest · Conservation · Endemism
Supplementary Information The online version contains supplemen-
tary material available at https://doi.org/10.1007/978-­3-­031-­21287-
­1_3.
R. R. Silva (*) · J. Andrade-Silva
Coordenação de Ciências da Terra e Ecologia, Museu Paraense
Emílio Goeldi, Belém, Pará, Brazil
L. P. do Prado
Laboratório de Hymenoptera, Museu de Zoologia da Universidade
de São Paulo, São Paulo, São Paulo, Brazil
J. H. C. Delabie
Laboratório de Mirmecologia, Centro de Pesquisas do Cacau,
Comissão Executiva do Plano da Lavoura Cacaueira,
Ilhéus, Bahia, Brazil
Universidade Estadual de Santa Cruz, Ilhéus, Bahia, Brazil
I. R. Leal
Departamento de Botânica, Universidade Federal de Pernambuco,
Recife, Pernambuco, Brazil
R. M. Feitosa
Departamento de Zoologia, Universidade Federal do Paraná,
Curitiba, Paraná, Brazil
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
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_3
3
3.1 Introduction
Ants (Hymenoptera: Formicidae) are an ecologically suc-
cessful and numerically dominant group of animals, playing
key ecological roles as soil engineers, predators, nutrient
recyclers, and regulators of plant growth and reproduction in
most terrestrial ecosystems (Hölldobler and Wilson 1990;
Lach et al. 2010; Parker and Kronauer 2021). Ants are also
widely used as bioindicators of the ecological impact of land
use (Andersen and Majer 2004), including several studies
performed in the Atlantic Forest areas (reviewed in Ribas
et al. 2012; Silva et al. 2022).
The Brazilian Atlantic Forest is a hotspot of biodiversity
(Myers et  al. 2000) and is recognized as one of the most
diverse rain forests in the world (Marques and Grelle 2021),
holding an impressive number of eusocial insect species,
such as ants, bees, wasps (Hymenoptera), and termites
(Blattodea, Isoptera) (Feitosa et  al. 2021). Particularly for
ants, a recent compilation of ant records across the entire
Atlantic Forests of Brazil, Paraguay, and Argentina identified
1114 ant species representing 10 subfamilies and 99 genera
(Feitosa et al. 2021; Silva et al. 2022).
In Atlantic Forest, the Pernambuco Endemism Center
(PEC) – the biogeographical subregion (BSR) Pernambuco
(Silva and Casteleti 2005; Peres et al. 2020) – is an important
endemism center in South America. With a long history of
habitat fragmentation, which began in 1500 with the eco-
nomic cycle of brazilwood, PEC currently presents one of
the highest deforestation rates among Brazilian biomes, at
the same time it is one of the least studied regions in the
Atlantic Forest, especially regarding invertebrates. This is of
particular concern for ants, given that this region is seen as a
global hotspot of discovery, with the potential to host at least
20 new records of ant genera (Guénard et al. 2012).
Despite the importance of ants as indicator of biodiversity
(Leal et al. 2010) and of habitat quality (Leal et al. 2012) in
the Pernambuco Endemism Center, there are very few check-
lists and distributional analyses for this biogeographical
23
24
subregion. Here, we organized a list of the ant species of this
region aiming to describe its species richness and distribu-
tion in the PEC.
3.2 Methods
The complete data set comprises historical and current ant
records (ranging from 1803 to 2021), most of them extracted
from the Atlantic Ants data set (Silva et al. 2022). We updated
this data set by incorporating published literature in 2021,
especially by including data sets from recent taxonomic revi-
sions of Neotropical ants, as those of the genera Cephalotes
(Oliveira et al. 2021), Dinoponera (Dias and Lattke 2021),
and Hylomyrma (Ulysséa and Brandão 2021). When coordi-
nates were not available, we georeferenced the records using
the GeoNames geographical database (geonames.org) and
secondly Google Maps (www.google.com.br/maps/).
Regarding the source of the occurrence data available in the
Atlantic Ants dataset, 3041 records were compiled from pub-
lished literature, 212 from collections databases, and 516
come from unpublished data (i.e., ant surveys carried out by
coauthors, including undergraduate and graduate studies;
Silva et al. 2022). The data set includes occurrence data from
the following Brazilian museums and institutions: Museu de
Zoologia da Universidade de São Paulo (MZSP), São Paulo;
Museu Paraense Emílio Goeldi (MPEG), Belém, Pará;
Coleção Entomológica Padre Jesus Santiago Moure (DZUP),
Universidade Federal do Paraná, Curitiba, Paraná. Further, ant
records from online specimen repositories such as AntWeb.org
as implemented by the California Academy of Sciences, San
Francisco, California, United States, and GBIF (https://www.
gbfi.org/). Finally, 1481 ant records in the BRC Pernambuco
were gathered from the Global Ant Biodiversity Informatics
(GABI) Project (Guénard et al. 2017).
We prepared a map based on kernel density estimation
(KDE) with a bandwidth of 15 km to describe the ant sam-
pling distribution in the Pernambuco Endemism Center.
Further, we extracted the relative sampling coverage by
counting points (geographic coordinates) inside and outside
of protected areas, Atlantic Forest remnants, and priority
areas for conservation to describe sampling efforts inside the
PEC. We considered ant records in the Pernambuco
Endemism Center when they were within its boundaries as
defined by the shapefile, including the so-called “brejos de
altitude” (remnants of wet forest in a Caatinga landscape) in
the states of Pernambuco and Paraíba. We defined the bound-
aries of the biogeographical Sub-Region Pernambuco using
shapefiles from the Instituto Nacional de Pesquisas Espaciais
(INPE) to the Brazilian States of Rio Grande do Norte,
Paraíba, Pernambuco, and Alagoas, available online (http://
terrabrasilis.dpi.inpe.br/downloads/). Shapefiles from both
R. R. Silva et al.
protected and priority areas were provided by Ministério do
Meio Ambiente (MMA; https://www.mma.gov.br).
We organized the entire data set in a single database, com-
bining assemblage information and occurrence information.
The data set can be accessed on GitHub Inc. repository
(https://github.com/LEEClab/Atlantic_series) as a new
release of the Atlantic Ants dataset. The literature used to
compile the ant records (110  references in alphabetical
order) can be consulted in a supplementary data
(Supplementary Table 1).
3.3 Results
We identified 3769 records in the Pernambuco Endemism
Center (Fig.  3.1a), encompassing over 10 subfamilies, 71
genera, and 247 species (Supplementary Table 1). The distri-
bution of ant records by State is highly uneven
(Alagoas = 1798; Paraíba = 968, Pernambuco = 812, and Rio
Grande do Norte = 191). Over the 236 municipalities within
the PEC (Alagoas = 71; Pernambuco = 99; Paraíba = 38; Rio
Grande do Norte = 28), we recorded ant occurrences in 62
first-order administrative divisions (i.e., 25% of the munici-
palities). Further, sampling is strongly biased to the ten com-
monest municipalities that together include 82% of records
(N = 3103; Figs. 3.1b and 3.2) and, in general, is represented
by sampling sites close to the capitals or larger cities in the
Pernambuco Endemism Center.
We characterized 1731 records (about 46% of records)
inside protected areas, representing 18 conservation units in
the PEC. The Reserva Biológica Guaribas (n = 635), Área de
Proteção Ambiental Aldeia Beberibe (n  =  283), Área de
Proteção Ambiental de Muricí (n  =  276), Parque Estadual
Dois Irmãos (n = 203), and the Refúgio de Vida Silvestre da
Mata do Buraquinho (n  =  184) had the highest number of
occurrences among the protected areas found in the PEC. In
total, there were 150 nominal ant species recorded in pro-
tected areas (61% of species). According to the priority areas
for conservation in the PEC, we determined 1187 ant occur-
rences (31% of the records), but site records are obviously
aggregated (Fig. 3.1c).
Regarding Atlantic Forest remnants in the PEC, we found
1999 occurrences (53% of the records) representing 156
nominal ant species. However, remnants at north of Rio
Grande do Norte, south of Paraíba, and north of Pernambuco,
as well a large area at south of Alagoas, remain largely
unsampled (Fig. 3.1d).
We gathered 20 records of a vulnerable species
(Lachnomyrmex nordestinus Feitosa & Brandão, 2008) accord-
ing to the Brazilian Red List of Threatened Species (ICMBio
2018) (Fig.  3.3). There were 27 records for exotic species
throughout the Pernambuco Endemism Center – an unidenti-
3  Ants (Hymenoptera: Formicidae) in the Pernambuco Endemism Center of the Brazilian Atlantic Forest
Fig. 3.1  Distribution of the 3769  ant records in the Pernambuco
Endemism Center of the Atlantic Forest, compiled from 1803 to 2021
(a), density of records as estimated by KDE functions (b), ant sampling
fied species of Cardiocondyla (1), Monomorium floricola
(Jerdon, 1851) (5), Paratrechina longicornis (Latreille, 1802)
(9), Tapinoma melanocephalum (Fabricius, 1793) (8) (Fig. 3.3),
as well as Tetramorium simillimum (Smith, 1851) (4).
In terms of species richness (not including morphospe-
cies), Myrmicinae was the richest subfamily (119 species),
followed by Ponerinae (31), Formicinae (27), Dorylinae
(22), Pseudomyrmecinae (20), Dolichoderinae (14),
Ectatomminae (13), Proceratiinae (2 species), and
Amblyoponinae (1 species). Among the genera recorded
(morphospecies excluded), the richest genera in the PEC
were Pheidole and Pseudomyrmex with 20 recorded species
each, followed by Camponotus (19), Strumigenys (17),
Neivamyrmex (12), Cephalotes (10), Crematogaster (9),
25
distribution in priority areas for conservation (c), and distribution of ant
records in remnants (d)
Solenopsis and Dolichoderus (8 species each), Neoponera
(7), Atta, Acromyrmex, Ectatomma, Gnamptogenys, and
Odontomachus (5 species each) (Fig. 3.4). There are 12 gen-
era currently represented by one or two nominal species. The
number of ant records represented by morphospecies (i.e.,
nonnominal species) is high (51% of the data set) (Fig. 3.5).
Indeed, this scaled up to the genus level in the Biogeographical
Sub-Region Pernambuco, ten genera were recorded only at
morphospecies level, as Acanthognathus, Acanthoponera,
Cardiocondyla, Linepithema, Myrmicocrypta, Prionopelta,
Typhlomyrmex, Probolomyrmex, Myrmelachista, and Mycet
omoellerius/Paratrachymyrmex (in this case, it is currently
impossible to determine to which of these genera the species
belongs without examined the specimens).
26 R. R. Silva et al.

Fig. 3.2  Number of ant records per sampling site and municipality in of total number of records). AL Alagoas, PE Pernambuco, PB Paraíba,
the Pernambuco Endemism Center of the Atlantic Forest (only the 15 RN Rio Grande do Norte
most frequently sampled municipalities are included, summing up 95%

Fig. 3.3  Lachnomyrmex

nordestinus, classified as a
vulnerable species according
to the Brazilian Red List of
Threatened Species of the
Instituto Chico Mendes de
Conservação da
Biodiversidade/ICMBio.
(ICMBio 2018). Tapinoma
melanocephalum, species
classified as exotic and
recorded at the Pernambuco
Endemism Center. (Image:
César Favacho). Ectatomma
tuberculatum, considered one
of the most frequently
recorded species in the
Pernambuco Endemism
Center as well as in Brejos de
altitude. (Image: César
Favacho)
3  Ants (Hymenoptera: Formicidae) in the Pernambuco Endemism Center of the Brazilian Atlantic Forest
Fig. 3.4  The top 20 most species-rich ant genera in the Pernambuco Endemism Center of the Atlantic Forest
Regarding the nominal species, there were 1207 species
occurrences (i.e., discarding duplicate records) (Fig.  3.6),
where site locations were defined by coordinates (based on
six decimal places). The ten most frequently recorded ant
species in the PEC were Dinoponera quadriceps Kempf,
1971 (n = 59 localities), Atta sexdens (Linnaeus, 1758) (56),
Ectatomma tuberculatum (Olivier, 1792) (n = 33) (Fig. 3.3),
Strumigenys denticulata Mayr, 1887 (30), Odontomachus
meinerti Forel, 1905 (n = 27), Pachycondyla harpax
(Fabricius, 1804) (n  =  27), Mayaponera constricta (Mayr,
1884) (n = 24), Atta cephalotes (Linnaeus, 1758) (20),
Odontomachus brunneus (Patton, 1894) (n = 20), and
Cephalotes pusillus (Klug, 1824) (19). On the other hand,
there were 72 species recorded from a single locality
(Supplementary Table 1).
We found only 35  ant records in “brejos” or “brejos de
altitude” or “brejos nordestinos” (Rizzini 1997, p.  381).
These records represented 13 ant species  – Acromyrmex
27
landolti (Forel, 1885), A. rugosus (Smith, 1858), Acropyga
goeldii Forel, 1893, Atta laevigata (Smith, 1858),
Camponotus atriceps (Smith, 1858), C. crassus Mayr, 1862,
Dinoponera quadriceps Kempf, 1971, Ectatomma brunneum
Smith, 1858, E. edentatum Roger, 1863, E. tuberculatum
(Olivier, 1792), Odontomachus haematodus (Linnaeus,
1758), Tetramorium simillimum (Smith, 1851) (exotic), and
Wasmannia auropunctata (Roger, 1863).
3.4 Discussion
It is well known that, although ants are among the best-­
studied taxa among invertebrates, the knowledge on their
occurrence and diversity in the Atlantic Forest is uneven dis-
tributed across the biome and understanding fine-scale distri-
bution of each species remains challenging (Feitosa et  al.
2021; Silva et al. 2022). Our analysis of ant records in the
28
Fig. 3.5  The top 20 most recorded species and morphospecies per ant genus in the Pernambuco Endemism Center of the Atlantic Forest. Mycet./
Parat. = Mycetomoellerius/Paratrachymyrmex
Pernambuco Endemism Center also suggests such draw-
backs because large gaps in ant sampling are too much evi-
dent in this subregion of the Atlantic Forest, including
fragment remnants and priority areas for conservation.
Ant surveys have been concentrated around urban
centers and a few conservation units or protection areas, such
as the Área de Proteção Ambiental de Murici (Alagoas),
Reserva Biológica Guaribas and Mata do Buraquinho
(Paraíba), APA Aldeia Beberibe, and Parque Estadual Dois
Irmãos (Pernambuco). The aggregated distribution of sam-
pling density in Brazilian ecoregions is well known (Oliveira
et  al. 2016) and strategies that incorporate both sampling
density and habitat loss are important for identifying the
highest priority areas for new ant surveys (Divieso et  al.
2020).
R. R. Silva et al.
Most of the available ant records in the PEC only can be
retrieved from examined material in taxonomic studies (e.g.,
Wheeler 1907–1925, Borgmeier 1923–1959, Santschi 1925–
1930, Kempf 1951–1978; Supplementary Table 1 references)
or taxonomic catalogues (Carvalho and Freitas 1960; Kempf
1972; Brandão 1991; Scott-Santos et al. 2008; Esteves et al.
2011). Biogeographical studies in the PEC are largely incipi-
ent and limited to fungus farming-ants (e.g., Barbosa 2018).
Further, research on ant biology or population biology is
focused on leaf-cutter ants of the genus Atta (e.g., Wirth
et al. 2007; Meyer et al. 2009; Correa et al. 2016; Farias et al.
2018) or large-sized ants (e.g., Dinoponera quadriceps;
Araújo and Rodrigues 2006).
In terms of species richness, we recorded 247 ant species
in the PEC and this number strongly underestimates the true
3  Ants (Hymenoptera: Formicidae) in the Pernambuco Endemism Center of the Brazilian Atlantic Forest 29

Fig. 3.6  Number of records per ant species in the Pernambuco Endemism Center of the Atlantic Forest (the top five most recorded species per
subfamily are included)

number of species in this region of the Atlantic Forest.
Considering the list of ant species recorded for the entire
Atlantic Forest (Silva et  al. 2022), the ant fauna of the
Pernambuco Endemism Center seems to be a subset of the
Atlantic Forest ant fauna. Indeed, for leaf-litter ants, north-
eastern sites showed higher similarity in species composition
than intermediate latitude areas or low and high southeastern-­
south Atlantic Forest areas (Silva and Brandão 2014).
Interestingly, Dorylinae, the army ants and their relatives
(Brady et al. 2014), is the third richest subfamily in number
of species (22 species). Army ants are keystone species in
Neotropical forests because of their major role as top preda-
tors, as well as numerous vertebrate- and invertebrate-­
associated species that depend upon their colonies for
survival (Pérez-Espona 2021). Such high species richness in
the PEC is in part related to the occurrence of 12 species of
Neivamyrmex. Those records of nominal species of
Neivamyrmex date back from classical taxonomic studies by
Borgmeier, Kempf and Watkins in the twentieth century (see
Supplementary Table 1). However, eight recent records for
this genus published in the ecological literature are based on
unidentified specimens. Army ants and their relatives are
30
very sensitive to habitat loss and modification (Pérez-Espona
2021). Given the current conservation status of the Atlantic
Forest of the PEC, with no single fragment larger than
10,000  ha, low functional connectivity, and only 1% pro-
tected in nature reserves (Ribeiro et  al. 2009; Lins-e-Silva
et al. 2021), studies on army ants distribution can be impor-
tant to understand the consequences of habitat loss and frag-
mentation for biodiversity maintenance of invertebrates.
Among the ant genera exclusively found within the
Atlantic Forest domain (Anillidris, Phalacromyrmex, and
Diaphoromyrma), there are no records for them in the PEC,
probably because the leaf-litter and subterranean stratum
remains largely undersampled in this region. Information on
endemism or biogeography of Atlantic Forest ants is scant,
and therefore, the extent to which endemism within the
Atlantic Forest ant fauna is related to environments or regions
is uncertain (Feitosa et al. 2021). Over the 1114 ant species
recorded in the Atlantic Forest, we found that only three spe-
cies are endemic of the PEC (Hylomyrma lopesi Ulysséa,
2021, Pheidole deima Wilson, 2003 and Pheidole impressa
Mayr, 1870). On the other hand, there are currently 866 addi-
tional ant species occurring in the Atlantic Forest but not
recorded in the PEC.
The pervasive presence of morphospecies in ant commu-
nity studies of the Neotropical region (Delabie et al. 2012),
representing 50% of the ant records in the PEC data set, is
one of the main impediments to comparative analyses on
assemblage structure in the Atlantic Forest (Silva et al. 2022).
Particularly for the Pernambuco Endemism Center, we found
ten ant genera currently known only at morphospecies level
(Acanthognathus, Acanthoponera, Cardiocondyla,
Linepithema, Myrmicocrypta, Prionopelta, Typhlomyrmex,
Probolomyrmex, Myrmelachista, and Mycetomoellerius or
Paratrachymyrmex). However, if the original samples cannot
be tracked (Turney et al. 2015), the presence of these genera
cannot be confirmed.
The recent synthesis of ants across the Atlantic Forests of
South America, a collaborative database of species occur-
rences (Silva et  al. 2022), indicated that one of the main
knowledge gaps regarding ant distribution in the Atlantic
Forest is the poor sampling along mountain sites, since most
records in the biome are concentrated in low altitudes. We
identified a very low sampling coverage in the “brejos” (alti-
tude swamps) and an incipient list of ant species (12 native
species, most of them very common and widely distributed
in Brazil). Therefore, enclaves of dense forests in the semi-
arid Northeast (in the Caatinga domain), in regions of high
altitude and humidity (Marques et al. 2021), represent large
gaps in sampling effort for ants and, although not inside the
PEC, should be a priority for further inventories.
Our data provide a comprehensive analysis on the regional
richness and distribution of an important insect group in the
Atlantic Forest north of the São Francisco River, combining
R. R. Silva et al.
available quantitative and qualitative data on ant species
occurrences. We found large sampling gaps in the
Pernambuco Endemism Center and thus, new guided sam-
pling expeditions may provide additional useful data to esti-
mate distributions of rare and endemic species as well as
reveal new species (e.g., Hylomyrma lopesi; Ulysséa and
Brandão 2021).
Acknowledgments  L.P. Prado acknowledges the São Paulo Research
Foundation (FAPESP) for the postdoctoral fellowship (grant n°
2022/01974-8). JAS, IRL, and RMF are grateful for the financial sup-
port provided by Conselho Nacional de Desenvolvimento Científico e
Tecnológico  – CNPq (grants 300981/2022-8, 308300/2018-1, and
301495/2019-0).
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 The Butterfly Fauna of the Northern
Atlantic Forest
André Victor Lucci Freitas, Jessie Pereira Santos,
Augusto Henrique Batista Rosa,
Douglas Henrique Alves Melo,
Carlos Eduardo Beserra Nobre, Larissa Nascimento dos
Santos, and Márcio Zikán Cardoso
Abstract
The coastal forests north of the Sao Francisco River lie on
mostly gentle terrain, spanning four states in the Brazilian
Northeast. Since colonial times, these landscapes have
endured severe impacts due to the extensive scale of sug-
arcane plantations and urban expansion. Nowadays, the
forest survives in mostly mid-sized forest fragments.
Nevertheless, these forests harbor a unique butterfly fauna,
influenced by a distinct climate environment than the more
southerly portions of the Atlantic Forest. This unique
fauna of the Northern Atlantic Forest (NAF) (also known
as the “Pernambuco Center of Endemism”) has been his-
torically understudied. With renewed interest in butterfly
ecology and trained personnel, several studies have begun
to uncover patterns of diversity and ecological dynamics in
the region in the last decade. In this chapter, a review of
these studies is provided, together with an up-­to-­date view
of the biology of butterflies in the region. Regardless of the
low number of surveys precluding precise estimates of
A. V. L. Freitas (*) · J. P. Santos · A. H. B. Rosa
Departamento de Biologia Animal and Museu de Diversidade
Biológica, Instituto de Biologia, Unicamp, Campinas, São Paulo,
Brazil
e-mail: baku@unicamp.br
D. H. A. Melo · C. E. B. Nobre
Programa de Pós-Graduação em Biologia Animal, Departamento
de Zoologia, Universidade Federal de Pernambuco, Recife,
Pernambuco, Brazil
L. N. dos Santos
Programa de Pós-Graduação em Ecologia, Departamento de
Ecologia, Universidade Federal do Rio Grande do Norte, Natal,
Rio Grande do Norte, Brazil
M. Z. Cardoso
Programa de Pós-Graduação em Ecologia, Departamento de
Ecologia, Universidade Federal do Rio Grande do Norte, Natal,
Rio Grande do Norte, Brazil
Departamento de Ecologia, Universidade Federal do Rio de
Janeiro, Rio de Janeiro, Brazil
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
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_4
4
species diversity, available evidence points to lower global
and local species richness than in the central sectors of the
Atlantic Forest. The relative isolation of the NAF is
reflected in the endemic subspecies found in the region
and in the possibility of unveiling additional endemisms as
further surveys are conducted. Biogeographical related-
ness to Amazonian and Bahia is evident, and phylogeo-
graphical work, including the humid enclaves in the
otherwise semiarid Caatinga, is needed to elucidate the
history of this unique fauna. The present review identified
knowledge gaps that range from basic natural history and
local surveys to broader macroecological studies. Priority
research lists inventories, natural history, comparative
ecology, landscape analyses, monitoring with bait traps,
molecular work, and citizen science as open questions that
can be tackled by those interested in the butterfly fauna of
the NAF. We also urge research training in the many public
research institutions located within the NAF realm.
Keywords
Atlantic Forest · Endemism · Conservation
4.1 Introduction
The Atlantic Forest was once a continuous stripe of humid
forests and associated physiognomies (as sand forests, dunes,
mangroves, high altitude highlands, and other minor physi-
ognomies) from sea level up to 2800 m a.s.l., extending for
more than 3000  km between the Brazilian states of Rio
Grande do Sul (30°S) and Rio Grande do Norte (5°S),
spreading to the interior as semideciduous forests as far as
Northern Argentina and Paraguay and the Brazilian states of
Goiás and Mato Grosso do Sul, and as wet enclaves of humid
forest within the semiarid (Andrade-Lima 1982; Morellato
and Haddad 2000; see also Iserhard et al. 2018). In more than
500 years of European occupation, a large part of the Atlantic
33
34
Forest has been replaced by anthropogenic environments.
Nowadays, the Atlantic Forest is restricted to less than 16%
of its original cover, with most of the remnants comprising
patches smaller than 50 ha (Ribeiro et al. 2009). In addition,
the entire region shows a high level of endemism, which
makes the Atlantic Forest one of the global biodiversity
hotspots for conservation (Myers et al. 2000).
As could be expected, the Atlantic Forest is not homoge-
neous over its enormous geographical extension, and differ-
ent species of organisms present distinct limits of distribution
(e.g., Brown et  al. 2020), a result of past and present pro-
cesses such as climatic changes and stability, orography,
variations in the sea level and biotic interactions (Carnaval
et  al. 2014; Santos et  al. 2020; Paz et  al. 2021). For some
widely distributed species, distinct molecular groups have
been identified along the Atlantic Forest (Pellegrino et  al.
2005; Palma-Silva et al. 2009; Amaral et al. 2013; Carnaval
et al. 2009, 2014; Pablos et al. 2021 and references therein),
suggesting the presence of biogeographical barriers possibly
related to past and/or present climatic discontinuities
(Carnaval et al. 2014; Pablos et al. 2021). For butterflies, in
particular, these discontinuities are visually expressed in
their wing color patterns, in many cases defining different
subspecies along the Atlantic Forest. The recognition and
mapping of these subspecies in the different sectors of the
Atlantic Forest (and ultimately in all tropical Americas) were
used to define the known centers of endemism in the
Neotropical region (Haffer 1969; Vanzolini 1970; Brown Jr
1977, 1979, 1987 and references therein).
In the northern limits of the Atlantic Forest, the area
extending from the mouth of the São Francisco River through
the dunes of the Brazilian state of Rio Grande do Norte is
defined as the Northern Atlantic Forest (hereafter NAF) (also
known as “Pernambuco Center of Endemism” sensu Brown
Jr 1979) (Fig. 4.1). In this region, the forests are restricted to
a narrow stripe extending over the low tablelands near the
coast, and also in the top of some plateaus in the semiarid
interior, where wet forests are maintained by orographic
rains (locally known as “brejos” or “brejos de altitude”)
(Andrade-Lima 1982; Oliveira-Filho and Fontes 2000)
(examples of representative forests are presented in Fig. 4.2).
The NAF is the most threatened sector of the Atlantic Forest,
harboring several endemic and threatened taxa of plants and
animals, including butterflies (Freitas and Marini-Filho
2011; Martinelli and Moraes 2013; ICMBio 2018).
Besides the degree of threat and high levels of endemism,
the NAF is one of the least known regions of the Atlantic
Forest (Santos et al. 2008; Shirai et al. 2019). Early studies
include a few inventories that served as a basis for the knowl-
edge in the region for many decades (Cardoso 1949; Ebert
1969; Kesselring 1976a; Kesselring and Ebert 1982), and
apart for specific studies focusing on taxonomy and insect
pests, three decades passed before some new butterfly inven-
A. V. L. Freitas et al.
tories appeared in the scientific literature (Paluch et al. 2011;
Godé and Nobre 2015; Melo et  al. 2019a; Medeiros et  al.
2021). Apart from these, additional distribution data for but-
terflies of the NAF have recently been compiled (from muse-
ums and fieldwork) and are available in databases and
published studies, including fruit-feeding butterflies
(Filgueiras et  al. 2016; Oliveira et  al. 2018; Santos et  al.
2018, 2020; Melo et al. 2019b; Brito et al. 2021), Brassolini
(Nymphalidae: Satyrinae) (Matos-Maravi et  al. 2013),
Ithomiini (Nymphalidae: Danainae) (Chazot et  al. 2016;
Brown et  al. 2020), and for all butterflies (Brown Jr and
Freitas 2000a) among other minor sources of scattered data.
Given this scenario, this chapter presents the state of the
art of knowledge about the butterflies from the NAF, describ-
ing patterns of species richness, community composition,
biogeography, and conservation in this restricted and threat-
ened sector of the Brazilian Atlantic Forest.
4.2 Species Richness and Taxonomic
Composition
Butterfly species richness peaks in the central sector of the
Atlantic Forest, around the southeastern coastal mountains
near the Tropic of Capricorn, where the complex orography,
milder temperatures, and abundant rainfall create a plethora
of habitat heterogeneity. The range from wet and warm low-
land forests to cold open habitats in the mountain tops and
dry valleys in the west slopes in the interior promotes
increased butterfly richness (Brown Jr and Freitas 2000a, b;
Brown Jr 2005). Species richness decreases gradually toward
the south and north limits, a pattern reported for several but-
terfly groups (Brown Jr and Freitas 2000a; Brown et al. 2020;
Santos et al. 2020). Despite the low number of existing fau-
nistic surveys in the NAF, available data show that species
richness is lower in this region when compared to localities
near the central sector of the Atlantic Forest.
Comparing some near-complete inventories along the
Atlantic Forest, local lists range from 500 to as high as 900
species in localities of the central sector, while the lists in the
NAF have around 200 to just above 300 species (Brown Jr
and Freitas 2000a, b; Francini et al. 2011; Paluch et al. 2011;
Melo et al. 2019a) (Table 4.1). This pattern is mirrored by
most subgroups, such as Heliconiini (Rosser et  al. 2012),
Ithomiini (Brown et  al. 2020; Paz et  al. 2021), and fruit-­
feeding butterflies (Santos et al. 2020). An unpublished list
reported more than 500 species for the Atlantic Forest in the
state of Pernambuco (data from H. Ebert notes, published in
Brown Jr and Freitas 2000a). This number is higher than any
maximum estimates reported in local lists, suggesting a high
level of spatial turnover in butterfly species in the NAF (see
in the next sections), a characteristic with important conse-
quences for conservation actions (see in the final section).
4  The Butterfly Fauna of the Northern Atlantic Forest
Fig. 4.1  Map showing the ecoregions (limits combined from Silva &
Casteleti 2003 and Fundação SOS Mata Atlântica 2005), the major riv-
ers and river basins (blue lines), and the main studied sites mentioned in
the text and on Table 4.1 (black centered open circles) in the Northern
Given the low number of well-sampled localities in the
NAF, it is difficult to point general patterns of taxonomic
composition for the entire region. For example, studies sug-
gest that Hesperiidae is usually the most species-rich butter-
fly family in well-sampled localities (Francini et al. 2011), a
condition satisfied only in two out of the five available local
lists (Table 4.1). On the other hand, because the Nymphalidae
are easy to sample and most species of this family are rela-
tively constant and conspicuous, species accumulation is
rapid after a few sample occasions and, consequently, com-
prehensive local lists for this family can be achieved with
relatively low effort (Francini et  al. 2011; Iserhard et  al.
2013). Based on this premise, the figures around 80 species
of Nymphalidae present in a given locality in the NAF are
likely a confident estimate of the actual species richness for
any given site in the region, a figure well below those reported
in the southernmost localities (from about 150 to more than
200 species; Brown Jr and Freitas 2000a; Brown Jr 2005;
Francini et al. 2011). A second interesting pattern emerging
35
Atlantic Forest. In the regional map (upper left corner), Northeastern
Brazil is shown in black. Acronyms for Brazilian States: AL Alagoas,
BA Bahia, CE Ceará, PB Paraíba, PE Pernambuco, PI Piauí, RN Rio
Grande do Norte, SE Sergipe
from these few lists is related to the total numbers of
Riodinidae and Lycaenidae in each locality. The family
Lycaenidae is usually richer than Riodinidae in most of the
southern Atlantic Forest sites; in colder montane forests,
Lycaenidae are found in a proportion of 2:1 or higher
(Francini et al. 2011). Although the reasons for these biases
are unknown, the richness of Riodinidae at a given site has
been positively correlated with the average temperature of
the site (Brown Jr 2005). In line with this observation, in the
five well-sampled sites in the NAF, Riodinidae and
Lycaenidae are virtually equivalent in the number of species,
a pattern congruent with the tropical warm climate all year
round in this region.
Considering the Ithomiini, a well-known group easy to
sample (Brown Jr 1972; Brown Jr and Freitas 2000a), a total
of 14 well-sampled lists are available, including ten in the
Atlantic Forest and three in the “brejos” (data available in
Doré et al. in press). Based on these lists, a total of 25 ithomi-
ine species have been reported for the entire NAF, with local
36
Fig. 4.2 Overview of representative landscapes in the Northern
Atlantic Forest. (a) View near a waterfall, Usina Frei Caneca, Jaqueira,
PE; (b) Forest interior in the urban park “Dois Irmãos,” Recife, PE; (c)
Estação Ecológica do Tapacurá, São Lourenço da Mata, PE; (d) Usina
Serra Grande, Ibateguara and São José da Laje, AL; (e) Forest fragment
A. V. L. Freitas et al.
adjacent to a sugarcane plantation, Usina Trapiche, Sirinhaém, PE; (f)
Reserva Biológica de Pedra Talhada, Quebrangulo, AL; (g) Mata do
Buraquinho, João Pessoa, PB. (Photo by Alexandre Vasconcellos); (h)
Trail inside the “Mata do Jiqui,” Parnamirim, RN.  Acronyms for
Brazilian States: AL Alagoas, PB Paraíba, PE Pernambuco, RN Rio
Grande do Norte
4  The Butterfly Fauna of the Northern Atlantic Forest
Table 4.1  Diversity and species richness of butterflies recorded in five sites in the Northern Atlantic Forest (first five rows) and a compilation of
the Atlantic Forest in Pernambuco (last row)
Hesperiidae Lycaenidae
Maceió1 55 29
João Pessoa2 110* 42
Caruaru3 59 17
Recife4 108* 43
Tiuma, São Lourenço da Mata5 25 11
East Pernambuco6 194* 102
Asterisks indicate the richest butterfly family in each site. Superscript numbers indicate the source of data. All sites are shown on Fig. 4.1
Sources for the site data: 1 – Cardoso 1949; 2 – Kesselring and Ebert 1982; 3 – Paluch et al. 2011; 4 – Melo et al. 2019a; 5 – Brown & Ebert,
unpublished field lists, Kesselring 1976a and data from the collections at UFPE; 6 – H. Ebert, unpublished data, based on more than three decades
of collecting in several distinct sites of Atlantic Forest in the state of Pernambuco (after Brown and Freitas 2000a, b)
richness ranging from a minimum of five species (in a
“brejo” near the northern limits of the wet forests), and maxi-
mums of 16 to 17 species (in three sites near the geographi-
cal center of the NAF, in the inlands of Pernambuco); for
comparison, lists of 20 species or more (some reaching 34
species) are common in southernmost localities (Brown Jr
and Freitas 2000a, b; Doré et al. in press).
4.3 Faunistic Affinities of the Butterflies
of the NAF
The butterfly assemblages in the NAF present several faunis-
tic elements that make them quite distinct from those reported
in other sectors of the Atlantic Forest, not only by the pres-
ence of several endemic subspecies but also by the presence
of many species exclusive to the region. In addition, the NAF
presents several species that are related to the Amazon fauna,
many of them shared with localities in the immediate south,
in the “Bahia Center of Endemism” (hereafter BCE, limited
north by a region with open vegetation in northern Bahia
state and south by the Doce River, in the state of Espírito
Santo, see Brown Jr 1979, 1987). Accordingly, although the
localities of these two centers of endemism appear as distinct
groups, they sometimes appeared as neighbor groups in anal-
yses of species composition similarity and occasionally
related to localities in the Amazon region (Fig. 4.3; Brown Jr
and Freitas 2000a; Brown Jr 2005). The close affinities of the
butterfly assemblages of the NAF and BEC are obvious in
multivariate analyses for two well-sampled butterfly groups
in the Atlantic Forest, the Ithomiini (199 sites), and the fruit-­
feeding butterflies (93 sites) (primary data available in Doré
et al. in press and Santos et al. 2018, respectively) (Fig. 4.3).
For ithomiines, the 13 sites in the NAF form a distinct group
and with low overlap with sites of the BCE (Fig. 4.3a). For
fruit-feeding butterflies, the six sites are still organized as a
distinct group, but less isolated and overlap with a few BCE
sites (Fig. 4.3b).
Several species are shared by the NAF and BCE and also
with the Amazon region but are absent or only occasionally
37
Riodinidae Nymphalidae Pieridae Papilionidae Total
28 86* 17 3 218
46 86 18 5 307
12 87* 18 4 197
37 80 16 4 288
27 100 17 4 184
76 139 21 6 538
reported in other regions of the Atlantic Forest. Good exam-
ples are the ithomiines Napeogenes inachia and Scada reckia
(Brown Jr 1979), the satyrines Chloreuptychia chlorimene,
Taygetis echo, Nhambikuara mima, and Pierella hyalinus
(Freitas et al. 2018; Santos et al. 2018), the morphine Morpho
telemachus (Blandin 2007), and Adelpha mesentina
(Nymphalidae: Limenitidinae) (Willmott 2003). No endemic
species for the NAF were reported in the tribe Heliconiini
(Nymphalidae) and the families Pieridae and Papilionidae.
Many additional examples of endemic species of the NAF or
species that are also shared with the Amazon region will
eventually appear as knowledge about the geographical dis-
tribution of Neotropical butterflies increases. Promising
groups to find those examples are the families Hesperiidae,
Lycaenidae, and Riodinidae (e.g., the description of the rio-
dinid endemic to the NAF, Eurybia gonzaga, Dolibaina et al.
2014).
4.4 Biogeography
The Atlantic Forest north of the mouth of the São Francisco
River was shaped by a combination of several factors includ-
ing historic occupation, geology, and climate, among others.
The climatic stability in the region associated with fertile
soils allowed the persistence of forests in the NAF even dur-
ing past events of dry climate that reduced the area of the
Atlantic Forest in the past (Brown Jr 1979; Brown Jr and
Ab’Sáber 1979; Paz et  al. 2021). Currently, these forests
reach the southern limits in the state of Alagoas, north of the
São Francisco River, and they are replaced by open forma-
tions dominated by small trees and shrubs that extend from
the north of the state of Sergipe to northern Bahia. This
makes the NAF the most isolated sector of the Atlantic
Forest, a condition that shaped its unique biota, leaving clear
marks of this isolation in populations of several forest ani-
mals and plants. For butterflies, this paleo-legacy can be eas-
ily observed in the wing patterns of some groups of mimetic
butterflies (subspecies), especially the ithomiines and
heliconiines.
38 A. V. L. Freitas et al.

Fig. 4.3 Nonmetric
multidimensional scaling
(NMDS) comparing the
composition of the
assemblages of (a) Ithomiini
species and subspecies
(Jaccard; Stress = 0.25); and
(b) fruit-­feeding butterfly
species (Jaccard;
Stress = 0.19) in the Atlantic
Forest Domain. Each data
point is a locality and the
symbols correspond to
different sectors: solid
circles = Northern Atlantic
Forest; open circles = “Bahia
Center of Endemism”; solid
diamonds = Serra do Mar;
open diamonds = Central
plateau and cerrado savannas;
gray
diamonds = Semideciduous
Forests; solid
triangles = semiarid Chaco;
open triangles = Southern
Atlantic Forest. Sites located
in the Northern Atlantic
Forest are with delimitated
with a dashed elipse

For example, considering the Ithomiini reported for the
NAF, by excluding the clearwing (with transparent wings)
and those species widely distributed and presenting a low
level of geographic differentiation (see Brown Jr 1979), a
total of 10 species belonging to two mimicry rings are pres-
ent. Four of them are represented by subspecies endemic to
the NAF (Fig. 4.4, see also Freitas 2020; Freitas et al. 2021)
and two that are shared with the BCE (Mechanitis lysimnia
nesaea and Scada reckia reckia). In the Heliconiini, how-
ever, a single subspecies, Heliconius ethilla flavomaculatus
is endemic to the NAF (Fig. 4.4a). With the pattern of rich-
ness decreasing toward the northern limits of the Atlantic
Forest, the number of endemic subspecies also decreases,
and the poorer Ithomiini assemblages are mostly represented
by widespread species, which are more tolerant to sunny
habitats and forest edges  – a single endemic subspecies
(Hypothyris ninonia daetina) (Fig. 4.4b) is present in the two
northernmost sampled sites (Campina Grande and João
Pessoa, in the state of Paraíba). In a third group of apose-
matic butterflies, the endemic Actinote pellenea auloeda
(Nymphalidae: Heliconiinae, Fig. 4.4c) is the only represen-
tative of the tribe Acraeini in the NAF (Silva-Brandão et al.
2021; an old unpublished record of Actinote ca. pyrrha by
H.  Ebert needs confirmation). The troidini swallowtail
4  The Butterfly Fauna of the Northern Atlantic Forest 39

Fig. 4.4  Eight subspecies of

mimetic butterflies in the
Nymphalidae tribes
Heliconiini, Acraeini, and
Ithomiini (all in dorsal view)
endemic to the Northern
Atlantic Forest (top and
middle rows) and two shared
with the “Bahia Center of
Endemism” (bottom row). (a)
Heliconius ethilla
flavomaculatus (Heliconiini);
(b) Hypothyris ninonia
daetina (Ithomiini); (c)
Actinote pellenea auloeda
(Acraeini); (d) Napeogenes
inachia grazielae; (e) Aeria
olena tiuma; (f) Scada
karschina delicata; (g)
Mechanitis lysimnia nesaea;
(h) Scada reckia reckia (all
Ithomiini)

Fig. 4.5  The four subspecies

of Morpho butterflies
(Nymphalidae) present in the
Northern Atlantic
Forest (dorsal on the left,
ventral on the right) (a, b).
Morpho menelaus eberti
(male and female,
respectively); (c) Morpho
helenor anakreaon (male); (d)
Morpho epistrophus
nikolajewna (male); (e).
Morpho telemachus jorgei
(female)

Parides zacynthus polymetus (Papilionidae: Troidini), a sub-
species shared with the BCE, is present along the coastal for-
ests and in several “brejos” (Tyler et al. 1994; Paluch et al.
2011).
All four species of Morpho from the NAF are represented
by endemic subspecies, but each one with different charac-
teristics (Fig. 4.5). Two of them are included in the Brazilian
red list of threatened species (Freitas and Marini-Filho 2011;
ICMBio 2018): These are the large white Morpho epistro-
phus nikolajewna (Fig.  4.5d) and the bright blue Morpho
menelaus eberti (Fig. 4.5a, b), this last shared with the BCE
(additional information is presented in the section on threat-
ened butterflies). A third endemic Morpho, the common and
more tolerant to disturbance Morpho helenor anakreon
(Blandin 2007) (Fig.  4.5c) is very widespread in the NAF,
and in the words of Kesselring (1976a) this ever-present but-
terfly “…can be found in almost any piece of woodland in
the Coastal Zone, even secondary forests and scrub.” Finally,
a fourth endemic subspecies, Morpho telemachus jorgei
(Fig. 4.5e), is known from three localities, one of these not
far from the urban perimeter of Recife, the capital of
Pernambuco state (Kesselring 1976a; Blandin 2007; Nobre
CEB, unpublished).
In other nonmimetic butterfly groups, the identification of
subspecies is not well established due to its low level of geo-
graphic differentiation, but as detailed studies advance, sev-
eral new endemic subspecies eventually will be described for
the NAF. In addition to the formation of endemic subspecies,
the relative isolation of the Atlantic Forests in the NAF sector
left markings in the genetic structure of several forest species
of animal and plants (e.g., Pellegrino et al. 2005; Cabanne
et  al. 2008; Carnaval et  al. 2009; Pinheiro et  al. 2014).
40
However, there are few phylogeographic studies of species
of the Atlantic Forest that include samples from the NAF,
and only three focusing on butterflies: one with Morpho epi-
strophus (Pablos et al. 2021), a second with the heliconiine
Heliconius erato phyllis (Machado et al. unpublished data)
and a third with Actinote pellenea (Heliconiinae: Acraeini)
(Silva-Brandão et  al. 2021). The first two studies showed
congruent patterns, with the populations from the NAF quite
distinct from all remaining populations based on mtDNA
haplogroups. In the third study, the sampled population from
the NAF (assigned to A. pellenea auloeda) showed no clear
separation from other studied populations, but in this specific
case a high frequency of Wolbachia infection could be the
reason why the mtDNA mitochondrial gene COI failed to
delimit not only the population from the NAF but all other
studied subspecies of A. pellenea.
In brief, all available biological evidence at the infraspe-
cific level (subspecies and populations) reinforces the long
history of isolation of the biological assemblages in the NAF,
confirming the evidence that comes from geological and his-
torical data. Additional phylogeographic studies, focusing on
different species with variable levels of dependence on for-
ested habitats will help in understanding the evolution of this
highly endemic biota.
4.5 Threatened Species
Currently, only three butterflies occurring in the NAF are
listed as threatened in the latest Brazilian Red List (MMA
2014; Rosa et al. 2020). While the information on geographic
distribution is available for all the listed butterflies, knowl-
edge about immature stages, host plants, ecology, behavior,
and other natural history data are scarce or absent. Moreover,
several endemic subspecies are waiting to be described,
some of them certainly in the threatened status due to the
continuous habitat loss, such as the recently described
Morpho telemachus jorgei (Blandin 2007) (Fig.  4.5e) and
Aeria olena tiuma (Freitas et al. 2021) (Fig. 4.4e).
Previously known from several localities in the states of
Pernambuco and Paraíba, the large white Morpho epistrophus
nikolajewna (Fig. 4.5d) is currently known from a single pop-
ulation in an urban park in the city of João Pessoa, capital of
the state of Paraíba (Kesselring 1976b; Kesselring and Ebert
1982; Andrade et al. 2019). Based on wing color and pattern,
the individuals from this population are quite similar to those
known from other populations near the coast in the central
region of the Atlantic forest, to the point of some authors ques-
tioning the validity of this subspecies (Lamas 2004). This
population is isolated by a gap of more than 800  km to the
nearest known population of M. epistrophus, in central Bahia
(Blandin 2007). This isolation explains the high molecular
divergence reported in the NAF compared to all other popula-
A. V. L. Freitas et al.
tions in the Atlantic Forest (Pablos et al. 2021). Moreover, M.
epistrophus nikolajewna occurs in the warm lowland forests
(from sea level to 400 m), different from most of the remain-
ing populations that show a marked preference for the milder
climate present of montane forests, mountain slopes, and the
subtropical forests in southern Brazil through Uruguay and
Argentina (Blandin 2007). Larvae are grouped and feed on
Inga (Fabaceae), as reported to all other known populations of
M. epistrophus, and the adults are univoltine, flying from April
to May (Kesselring 1976a, b). This subspecies is considered
Critically Endangered (CR).
The large iridescent blue Morpho menelaus eberti
(Fig. 4.5a, b) presents a much wider distribution, occurring in
a large part of the BCE where it reaches its southern limits in
central Bahia (Blandin 2007; Freitas and Marini-Filho 2011;
Melo et  al. 2014; ICMBio 2018). This iconic butterfly has
been reported only from the larger and well-preserved frag-
ments in the NAF, usually in low densities (Kesselring 1976a;
Melo et al. 2014; but see Blandin 2007: 143). Adults fly all
year round; immature stages and hostplants are not known.
This subspecies is considered Critically Endangered (CR).
Knowledge about the small clearwing Scada karschina
delicata (Fig.  4.4f) increased considerably in recent years.
This subspecies was described by George Talbot in 1932
from a male and a female from an unspecified locality in
Brazil. Later, a pair of additional specimens from Pernambuco
were found by Dr. Keith S. Brown Jr. in a museum drawer,
including one with the specific locality “Água Azul” (name
of an old sugarcane farm near the cities of Timbaúba and
Vicência, Pernambuco) written in its label. This finding
resulted in a specific field trip by Keith Brown Jr. to the same
locality, which lead to the rediscovery of this butterfly in
1988 (Freitas et al. 2020). Today, additional searches found
four additional localities where the species is present, all far
from the coast and on altitudes ranging from 500 to 1000 m.
The hostplant, immature stages, habitat, and distribution, as
well as conservation status, were described and discussed in
Freitas et  al. (2020). This subspecies is considered
Endangered (EN).
One additional fourth threatened species, the swallowtail
Heraclides himeros baia (Papilionidae), occurs in a reserve
located in the semiarid Caatinga, in Paraíba (Kerpel et  al.
2014). This subspecies was also reported from wet coastal
forests in Bahia and could likely occur in the wet forests of
the NAF. This subspecies is considered Endangered (EN).
4.6 Comparative Studies with Fruit-­
Feeding Butterflies
The neotropical fruit-feeding butterflies include species of
four Nymphalidae subfamilies that obtain most of their nutri-
tional requirements from rotting fruits, plant sap, and other
4  The Butterfly Fauna of the Northern Atlantic Forest
decaying material (DeVries 1988; Freitas et al. 2014). Because
of their feeding habits, fruit-feeding butterflies can be easily
attracted and captured with traps baited with fermenting fruits,
allowing simultaneous sampling with standardized efforts at
different sites. Therefore, studies with fruit-feeding butterflies
have been widely used in ecological research in Brazil in the
last decade (Freitas et al. 2014; Santos et al. 2018 and refer-
ences therein), including in the NAF.
The region of “Usina Serra Grande” (Fig. 4.2d), a large
private sugarcane landholding in the State of Alagoas, main-
tain more than a hundred forest fragments of several sizes,
including a large remnant with 3500 ha (known as “Coimbra
forest”) that is the best-preserved fragment in the NAF (more
details in Silva and Tabarelli 2000). This region supports a
total of 61 species of fruit-feeding butterflies, including the
large blue Morpho menelaus eberti (Melo et al. 2019b) and a
recently described species of Yphthimoides (Nymphalidae:
Satyrinae) only known from this region (Barbosa et al. 2016).
A comparative study with bait traps in this region showed
that butterfly assemblages in the small fragments showed a
high dominance of species typical of forest edges, missing
most of the forest-dependent species. This difference in the
butterfly assemblages can be a result of both changes in the
vegetation caused by fragmentation or the intolerance of
some species to the sunny and hot habitats in the forest edges
and small fragments (Filgueiras et  al. 2016). For example,
both the small fragments and the edges of the large Coimbra
forest showed a marked dominance of species of Satyrini,
possibly a result of the increase in light levels in these habi-
tats, which promotes an increase in pioneer plant species,
including several species of grasses, their main larval host-
plants (Melo et al. 2019b). Indeed, the area of the fragment
and the proportion of pioneer tree species were two of the
most important characteristics associated with observed
changes in butterfly assemblages in the region (Filgueiras
et al. 2016).
As mentioned before, butterfly abundance and species
richness were both higher in the small fragments when com-
pared to the large 3500  ha forest (Melo et  al. 2019b). An
increase in abundance and species richness in disturbed habi-
tats when compared to more preserved habitats is a pattern
previously reported in other areas of the Atlantic forest (see
Gueratto et al. 2020 and references therein). However, this
increase in species richness and abundance hides negative
outcomes, including the loss of β-diversity in the small frag-
ments (that is, leads to biotic homogenization), with the
impoverishment of forest interior assemblages, increasing
the ecological redundancy and decreasing the ecological ser-
vices provided by forest-dependent butterfly species
(Filgueiras et al. 2019).
In the northern limits of the Atlantic Forest, in the state of
Rio Grande do Norte, the drier and lower forests are restricted
to a very narrow stripe near the coast and presented as a
41
mosaic of hundreds of small fragments (Ribeiro et al. 2009).
A recent study in this region (including the surroundings of
the city of Parnamirim, see Fig. 4.2h) sampled fruit-feeding
butterflies in 15 forest fragments aiming to understand the
patterns of the temporal and spatial distribution of the 33
known species in the local assemblages (Brito et al. 2021).
The results revealed that most fragments presented similar
species composition and that the local assemblages pre-
sented a nested pattern, that is, the assemblages with lower
species richness are usually a subset of the richer assem-
blages. In addition, distance to the water bodies was shown
to be the most important predictor of species richness and
abundance, with the assemblages near the water presenting
more species and more individuals when compared to those
more distant from water. Possibly, the scarce water supply
and the relatively short wet season (when compared to south-
ern sites in the NAF) explain the importance of distance from
water bodies on the structure and dynamics of fruit-feeding
butterfly assemblages in this region.
The standardized protocols provided by baiting traps have
also been used to compare butterfly diversity in urban areas
in the NAF. Comparing butterfly diversity in urban plazas to
sites located within a large, well-preserved urban park,
Oliveira et al. (2018) found that the plazas in the coastal cap-
ital city of Natal harbored a very poor species assemblage
when compared to the better-preserved urban park.
Although studies using bait traps are especially promising
in comparative ecological studies, in the NAF they have been
restricted to only two landscapes in two distinct regions (see
above), denying us the possibility of making more general
statements and establishing general assemblage patterns for
the region. Nevertheless, ongoing studies (Santos L, Kerpel
S, Cardoso MZ, unpublished data) should provide more data
on additional sites in the states of Rio Grande do Norte and
Pernambuco. Given the easiness and tractability of studies
focusing on fruit-feeding butterflies with the use of bait
traps, more initiatives using this method should be employed
in different localities on the NAF. Open questions that should
be addressed are local and regional patterns of species
assemblages. The climate in the NE sector of the Atlantic
forest is strongly related to the movement of the intertropical
convergence zone, with a hot and dry season and a more
moderate rainy season when compared to the southernmost
areas. Thus, seasonality should play a major role in species
dynamics in time. As the northern limit of the Atlantic Forest
is located in the NAF, one interesting scientific question to be
addressed is the potential for changes in species diversity as
a function of latitudinal position. Heliconiine diversity, for
instance, drops by more than half from sites in the state of
Pernambuco to sites in the state of Rio Grande do Norte,
roughly a 300 km distance. The ecotones between the wetter
coast and the drier Caatinga should also provide for interest-
ing work on potential ecological filters determining butterfly
42
assemblages. Priority approaches should also include the
investigation of vertical stratification, ecological restoration,
and temporal variation. Also, the simple description of fruit-­
feeding butterfly assemblages in different localities could
improve the understanding of patterns of species distribu-
tion, providing crucial information for future conservation
actions in the entire region.
4.7 Conservation of Butterflies and Their
Habitats: The Future of the Northern
Atlantic Forest
The butterfly fauna of the northernmost sector of the Atlantic
Forest has a long history of relative isolation, today expressed
as several endemic species and subspecies, or by segregated
molecular groups. The lack of comprehensive inventories
and ecological studies in the NAF, however, precludes the
identification of general patterns and processes in the region,
and the scenario is not positive concerning the current situa-
tion of the remaining forests. For example, differently from
the other sectors of the Atlantic Forest, the NAF lacks a for-
est continuum or a large forest block that could be a testi-
mony of the original ecological processes in the region
(Tabarelli et al. 2006a). The remaining forest remnants are
distributed in several small fragments (less than 50  ha)
mostly isolated from each other (Ribeiro et  al. 2009). For
plants, for example, this situation resulted in a general biotic
homogenization, with a loss of phylogenetic and functional
diversity (Silva and Tabarelli 2000; Lôbo et al. 2011). Not
surprisingly, butterflies, whose larvae feed mostly on plants,
are directly affected by this scenario. A similar biotic homog-
enization was reported for butterflies in the small forest frag-
ments as shown in previous sections.
A second condition noted for the butterfly fauna of the
NAF is the apparently high species replacement in space
(high β-diversity), although studies on small scale in the
northern limits of the NAF forests did not report significant
changes (Brito et  al. 2021). At a regional scale, however,
considering the clearwing ithomiines, although 25 species
are present in the NAF, not more than 17 species were
reported in a single locality. A similar situation applies to the
entire butterfly fauna: just over 300 species were reported in
an extremely well-sampled locality, well below the 538 spe-
cies reported by the entire Atlantic Forest in Pernambuco
(Table 4.1, see also Ebert 1969). In practical terms, this is a
challenge for conservation because this implies the necessity
of preserving many of the remaining fragments in each area
to sustain the regional butterfly fauna.
Contrary to our hopeful wishes, the last remaining forests
continue to suffer from anthropogenic disturbance such as
timber extraction, fire, and urban expansion (Tabarelli et al.
2006b). As a result, several butterfly populations have been
A. V. L. Freitas et al.
reported to be extinct since the second half of the twentieth
century. One well-documented example is the case of the
critically endangered M. epistrophus nikolajewna. As
reported by Kesselring (1976b), the species was extremely
common in several forest patches around the city of João
Pessoa in the 1940s, but as forests were gone, this species
disappeared except for one forest-disturbed fragment, where
a population persists nowadays (see previous sections). As
noted, several local endemic forms are still undescribed, and
some of them could be extinct before being named and with-
out even a chance that conservation actions could be pro-
posed or implemented.
Accordingly, major efforts should not be restricted to stop
deforestation and the proposal of new conservation areas. In
addition to these, effective plans of forest restoration and
implementation of ecological corridors connecting the forest
remnants should be implemented. Butterflies could be used
as a low-cost and easy-to-work bioindicator group for assess-
ing habitat quality and for long-term monitoring programs.
Therefore, suggestions of priority studies for the NAF are
here presented (see below) as advice for those students and
researchers interested in obtaining relevant biological data
that could also be used as subsidies for conservation actions.
1. Species lists: Obtaining comprehensive butterfly invento-
ries for several additional localities in the region of the
NAF including the “brejos” is extremely important. This
information is important since these are the primary data
used for several other studies such as distribution of rich-
ness and niche modeling, including impacts of future sce-
narios of climate change (e.g., Santos et al. 2020).
2. Natural history data: The lack of information on host-
plants, immature stages, and behavior are not exclusive
for the butterflies of the NAF. Obtaining natural history
information for any species in the NAF is extremely
important, even if similar data are available for the same
species in other sectors of the Atlantic Forest. Such stud-
ies may not only contribute to knowledge about their life
cycles but also reveal patterns of local adaptation to hosts.
Studies of population biology using mark-recapture tech-
nics can be added to this topic, since they are of low cost
and easy to conduct.
3. Monitoring habitat quality: Programs using bait traps to
sample fruit-feeding butterflies are especially useful both
for rapid diagnostics and long-term monitoring. Proposing
some sites to establish a program of long-term monitoring
using fruit-feeding butterflies can add important informa-
tion and help to unveil ecological patterns of diversity
distribution in the forests of the NAF.  Recommended
localities include the region of the “Usina Serra Grande”
(especially the large Coimbra forest), where some infor-
mation is already available (Fig. 4.2d), the region of the
“Reserva Biológica de Pedra Talhada” (Fig.  4.2f), and
4  The Butterfly Fauna of the Northern Atlantic Forest
even in urban landscapes (Oliveira et al. 2018). In addi-
tion, monitoring should also be employed in at least some
of the few established conservation areas in the NAF not
only to monitor changes but also help staff guide their
conservation actions, a task recently implemented in
some of them (L. N. Santos and M. Z. Cardoso, unpub-
lished data).
4. Molecular studies: Any study assessing molecular data
for butterflies of the NAF will provide relevant informa-
tion to understand the genesis and the evolution of its
unique biota (Pablos et  al. 2021), as well as they could
provide important ecological and demographic informa-
tion (de Moura et al. 2011).
5 . Science outreach, education, and citizen science: Actions
connecting the scientific community with society are
extremely important for several reasons, including chang-
ing the collective indifference toward nature. Accordingly,
scientists should include scientific outreach in their proj-
ects whenever possible. Butterflies are especially appro-
priate since they are diurnal, easy to observe, colorful,
charismatic, and usually appreciated by people (unlike
most insects). Moreover, the uniqueness of the butterfly
fauna of the NAF, if effectively presented to the popula-
tion of the region, can result in a sense of pride and a
desire to protect these butterflies (and even create new
economic opportunities, such as butterfly watching). So,
even simple actions as helping to give names to butterfly
pictures posted on social media (Facebook, Instagram,
iNaturalist) are important to create a culture of conserva-
tion of butterflies and their habitats.
It is obvious that there are many other avenues of investi-
gations not mentioned here, and all are welcome considering
the lack of information for the entire region. However, the
five emphasized areas could serve as a guide to those stu-
dents and scientists interested in butterflies in the region.
Moreover, the present chapter is not only useful as an attempt
to compile most scientific information available for butter-
flies of the NAF; it can be useful to financial agencies to
organize and prepare forthcoming calls and especially to
environmental organs when prioritizing research areas in the
region.
4.8 A Final Word: When Geography
Should Not Mean Destiny: Capacity
Building as a Means to End Inequality
Despite a long history of occupation by European colonists,
past boom-and-bust cycles of various commodities
(Brazilwood, sugarcane, coffee, and gold) have moved the
43
economical centers progressively to the south. Consequently,
most of the research centers in Brazil have been located in
the southeast and adequate training of scientists has lagged.
The past decade or so has seen an improvement in university
funding and many new graduate programs in Biology have
been created in the Northeast, be it in the coastal capitals or
in larger cities in the semiarid Caatinga realm. Thus, we are
optimistic as to the future of butterfly research in the NAF
and its neighboring Caatinga. Hopefully, the current genera-
tion of new scientists will engage in understanding this
unique and beautiful aspect of Neotropical biodiversity, not
only by studying them but also by training new researchers
and striving to protect and restore the Atlantic Forest of the
Brazilian Northeast.
4.9 In Memoriam
We would like to dedicate this chapter to the memory of two
pioneer lepidopterists, Heinz Ebert and Hans Jörg [= Jorge]
Kesselring; together, these two dedicated naturalists
immensely contributed to the knowledge of the butterfly fauna
of the Atlantic Forest of the so-called “Pernambuco Endemism
Center.” In addition to the huge contribution to the knowledge
of butterflies, they were among the first to rise in defense of the
conservation of the rich forests of the entire region.
Acknowledgments The authors thank Inara R.  Leal and Marcelo
Tabarelli (UFPE) for sharing information and for the excellent discus-
sions about NAF; Keith S.  Brown Jr. for sharing all his information
from field notes and other unpublished data; Solange Kerpel and an
anonymous referee for reading and making valuable suggestions on the
final version of the manuscript; and Anita Studer and Luis Freitas in the
name of Nordesta NGO. Alexandre Vasconcellos kindly sent us a pic-
ture of the urban park in João Pessoa. The authors also thank all stu-
dents and collaborators of LABBOR-UNICAMP, especially Luisa
Mota, Eduardo Barbosa, André Cesar, Simeão Moraes, Patrícia
Gueratto, and Junia Carreira, that visited Pedra Talhada, bringing
important biological information on the butterflies of that area. The
authors also thank many colleagues and students that have contributed
to the study of butterflies in the Brazilian Northeast, in special to Onildo
Marini-Filho, Rodrigo Vasconcellos, Elaine Cambuí Barbosa, José
Elieudo Dias Barbosa, Isabela Oliveira, Marcos Roberto Brito, Marília
Lion, Solange Kerpel and Adalberto Medeiros. The authors also thank
the ICMBio for the permits (#10438-1, #10802-24, #32853-10,
#10894). AVLF acknowledges support from Fundação de Amparo à
Pesquisa do Estado de São Paulo  – (FAPESP) (Biota-Fapesp grants
2011/50225-3, 2013/50297-0  and 2021/03868-8) and from the
Conselho Nacional de Desenvolvimento Científico e Tecnológico
(CNPq) (421248/2017-3 and 304291/2020-0). MZC thanks the col-
leagues at the Departamento de Ecologia (Universidade Federal do Rio
Grande do Norte) for logistical as well as intellectual support, and
CNPq (563332/2010, 400242/2014-1) and Fundação Boticário
(201810074) for grants. AHBR, CEBN, DHAM, and LNS thank the
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil
(CAPES) – Finance Code 001. This study is registered in the SISGEN
(AA9A2EA).
44 A. V. L. Freitas et al.

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 Dung Beetles from the Atlantic Forest
North of the São Francisco River: 5
An Overview of a Fragile Fauna

Luciana Iannuzzi, Carolina N. Liberal, André B. Reis,

João Paulo Nunes, Thamyrys B. Souza, Fábio C. Costa,
João Carlos da S. Regueira, Mario Jardim Cupello,
Bruno K. C. Filgueiras, Fredy Alvarado, Renato P. Salomão,
Mateus S. E. C. Lima, and Priscila P. Lopes

Abstract São Francisco River. We provide information on the diver-

Dung beetles are sensitive to environmental quality, there-
fore being excellent bioindicators and are being used to
assess the effects of habitat transformation. These beetles are
detritivores, thus contributing to the environment by cycling
soil nutrients, aerating the soil, and performing  secondary
seed dispersal. In this chapter, our primary goal is to compile
from the scattered literature information on the dung beetle
species already identified in the Atlantic Forest north of the
L. Iannuzzi (*) · F. C. Costa · João Carlos da S. Regueira ·
B. K. C. Filgueiras
Departamento de Zoologia, Universidade Federal de Pernambuco,
Recife, PE, Brazil
e-mail: luciana.iannuzzi@ufpe.br
C. N. Liberal
Departamento de Biologia, Universidade Federal Rural de
Pernamuco, Recife, PE, Brazil
A. B. Reis · J. P. Nunes · Mateus S. E. C. Lima
Departamento de Sistemática e Ecologia, Universidade Federal da
Paraíba, João Pessoa, PB, Brazil
T. B. Souza
Instituto Nacional da Mata Atlântica, Santa Teresa, ES, Brazil
M. J. Cupello
Departamento de Zoologia, Universidade Federal do Paraná,
Curitiba, PR, Brazil
F. Alvarado
Divison de Ciencias Ambientales, Instituto Potosino de
Investigación Científica y Tecnológica, San Luis Potosí, México
R. P. Salomão
Programa de Pós Graduação em Ecologia, Instituto Nacional de
Pesquisas da Amazônia, Manaus, AM, Brazil
Universidad Nacional Autónoma de México, Instituto de Ecología,
Coyoacán, Ciudad de México, México
P. P. Lopes
Departamento de Ciências Biológicas, Universidade Estadual de
Feira de Santana, Feira de Santana, BA, Brazil
sity, biology, and conservation status of dung beetle species
already evaluated, as well as point out the gaps in our knowl-
edge and regions that still lack surveys. Our literature review
found 6 tribes, 23 genera, and 89 species of dung beetles,
comprising data from Atlantic Forest, Restinga and Brejos
de Altitude ecosystems in the states of Rio Grande do Norte,
Paraíba, Pernambuco and Alagoas. Although information on
the diversity of dung beetle in the northern Atlantic Forest is
still limited in terms of territorial extension, its importance
and fragility are undeniable. The number of endemic species
is significant, thus making this area and its beetle fauna  a
priority for conservation.
Keywords
Scarabaeidae · Scarabaeinae distribution · Endemism ·
Brejo de Altitude · Restinga
5.1 Introduction
The Atlantic Forest is a megadiverse tropical forest and is
considered one of the 25 priority areas for conservation
worldwide (Myers et  al. 2000; Silva and Tabarelli 2000).
This hotspot covers around 15% of the total Brazilian terri-
tory, along the coast of 12 states, from Rio Grande do Norte
to Rio Grande do Sul, and penetrating farther inland into four
other states, namely Piauí, Minas Gerais, Goiás, and Mato
Grosso do Sul (Joly et al. 1991, 1999; Rizzini 1997; INPE
2019). Currently, the Atlantic Forest is highly fragmented,
and 80% of the forest fragments are less than 50  ha and
highly isolated (Ribeiro et al. 2009). Land-use changes were
particularly severe within large patches of previously con-
tinuous forests, which were converted to fragments of differ-
ent sizes and successional stages and inserted in a mosaic of

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 47

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_5
48
different monocultures, such as sugarcane and soybean
(Bernard et al. 2011; Melo et al. 2013). Due to its large lati-
tudinal span (circa 27°, Tabarelli et al. 2010) and variations
in vegetation structure, we can identify biogeographic units
in the distribution of the Atlantic Forest fauna (Silva and
Vaz-de-Mello 2020).
One of the biogeographic units of the Brazilian Atlantic
Forest is located north of the São Francisco River between
Alagoas and Rio Grande do Norte (Veloso et al. 1991). This
unit has been identified as an important center of endemism in
South America, the Pernambuco Endemism Center (Prance
1982, 1987), and an important climatic refugium for species,
the Pernambuco refugium (Carnaval et al. 2009). Part of the
northern Atlantic Forest is composed of a collection of small-
to  medium-sized patches of tropical moist forest that cover
the slopes of isolated plateaus rising above the dry forests of
the Caatinga. These are the “Caatinga moist forest enclaves”
or, as they are locally known, as “Brejos de Altitude” or
“Brejos Nordestinos” (Andrade-Lima 1982), and harbor
endemic species of several plants and animals (Andrade-
Lima 1982; Borges-Nojosa and Caramaschi 2003; França
et  al. 2020; Pessoa and Alves 2015). These moist forest
enclaves are very peculiar in biodiversity terms, especially
when compared to the rest of the Atlantic Forest, as their biota
shows a mixture of Amazonian elements as well as others
from the Atlantic Forest of southern and southeastern Brazil,
amidst a matrix of semiarid vegetation (Andrade-­Lima 1960,
1982; Prance 1982).
Despite a crescent number of studies in the Atlantic Forest
domain, there are still many areas that could be considered
“data deficient” concerning their insect fauna. The areas
north of the São Francisco River are a good example.
Nevertheless, some biological groups have been systemati-
cally studied from this area, such as dung beetles, allowing a
broader analysis of its diversity, composition, and conserva-
tion status.
Dung beetles of the subfamily Scarabaeinae are detritivo-
rous insects that, due to their feeding and reproductive hab-
its, provide several ecosystem functions, such as secondary
seed dispersal, nutrient recycling, soil aeration, and parasites
control (Nichols et  al. 2008). Previous studies with dung
beetles in Paraíba, Pernambuco, and Alagoas have addressed
their seasonality and period of activity (Endres et al. 2005;
Iannuzzi et  al. 2016), bait attractivity (Endres et  al. 2005;
Filgueiras et  al. 2009; Salomão et  al. 2014), diversity and
distribution (Costa et  al. 2009; Endres et  al. 2007; Gillett
et al. 2010), conservation status (Vieira et al. 2011), habitat
preference (Costa et  al. 2013), behavior (Salomão et  al.
2016), genetic structure (Amorim et al. 2018; Ferreira-Neto
et al. 2017), and have empirically demonstrated the negative
anthropogenic effects on dung beetle communities (Filgueiras
et al. 2011a; Salomão and Iannuzzi 2015).
L. Iannuzzi et al.
Dung beetles have been considered good habitat indica-
tors due to their well-understood ecological roles (Hanski
and Cambefort 1991), increasingly refined systematics (Vaz-­
de-­Mello et al. 2011a; Vaz-de-Mello and Cupello 2018), and
sensibility to habitat alteration (Larsen et al. 2005; Nichols
et al. 2007). The decrease in their abundance and diversity
may result in cascading effects on ecosystem functioning,
with important implications for forest regeneration and con-
servation (Andresen and Feer 2005; Lawson et  al. 2012;
Nichols et al. 2008). Sampling of dung beetles is more cost-­
effective than many other taxa (Gardner et al. 2008; Larsen
and Forsyth 2005), and sampling methodology is easily rep-
licable, thereby making dung beetles a model system for
evaluating impacts from human activities in the Atlantic
Forest (Filgueiras et al. 2015; Salomão and Iannuzzi 2015;
Souza et al. 2020).
In this chapter, our primary goal is to compile from the
scattered literature information on the dung beetle species
already identified in the Atlantic Forest north of the São
Francisco River. This is added by information on the ecology
and distribution of these species. Together, this data shall
contribute to the understanding of the importance and need
of conservation of this biogeographic unit.
5.2 Methods
5.2.1 Study Area
Published studies on the dung beetle communities of the
Northern Atlantic Forest (NAF) include fragments of Atlantic
Forest located in the states of Rio Grande do Norte, Paraíba,
Pernambuco, and Alagoas. In this region, there are highland
forests, locally known as “Brejos de Altitude,” located on the
eastern edge of the Borborema Plateau of the respective
Brazilian states. The studied sites ranged from 9°55′S to
6°70′S, and from 35°77′W to 34°84′W.  According to the
Köppen classification, the local climate is classified in some
areas as Tropical with dry summer (As) and in others as
Tropical without dry season (Af). Mean annual rainfall of the
studied sites ranges from 940  mm (Igarassu municipality,
Pernambuco) to 1304 mm (Maceió municipality, Alagoas),
and mean annual temperature ranges from 22.9 °C (Ibateguara
municipality, Alagoas) to 25.9  °C (Itamaracá municipality,
Pernambuco) (Climate-Data 2020). In all areas, dung beetle
samplings were performed in forest fragments, which had
different classifications regarding their conservation politics.
Most of them are conservation units (e.g., Amorim et  al.
2018; Costa et al. 2009; Iannuzzi et al. 2016), whether public
(e.g., Gillett et al. 2010; Salomão et al. 2020) or private (e.g.,
Hernández et al. 2014).
The Northern Atlantic Forest is highly heterogeneous,
both in vegetation types and soils, but mostly composed of
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna
semideciduous forests, open and closed rainforests (Carvalho
et  al. 2021), with trees varying from 8 to 15  m in height
(Santiago and Barros 2003). Other forest types found in eco-
tonal zones vary between grassland, savanna, and marine-­
influenced areas, such as restingas and mangroves. The soil
in the region has low fertility and it is classified as yellow
oxisol and red-yellow argisol (Souza et al. 2020).
Leading  to the alarming conservation status of Atlantic
Forest native vegetation, especially in northeastern Brazil
(Myers et al. 2000; Rezende et al. 2018), currently, there are no
continuous forests in the studied region. Most of the native
Atlantic Forest remnants in this region are in hilltops or sloping
terrains that are difficult for human occupation. Therefore, all
studied areas consist of forest fragments covering different
sizes, ranging from small forest patches (e.g., 8 ha, see Salomão
and Iannuzzi 2015) up to 3500 ha and 7324 ha (respectively,
Coimbra and Campo de Instrução Marechal Newton Cavalcanti
(CIMNC, the largest forest fragments of the region) (Costa
et al. 2013; Filgueiras et al. 2011a). Those forest fragments are
under different conservation status, being mostly secondary
vegetation and deforested sites, with almost no primary forests.
Sugarcane monoculture and urban expansion stand out as two
of the main activities that promote the substitution of native
land cover by anthropogenic land uses, and compose the main
matrix that surrounds the remnants (Filgueiras et  al. 2015;
Salomão et al. 2017), although other activities are also respon-
sible for important changes in the native vegetation of Northern
Atlantic Forest (e.g., mining, see Hernández et al. 2014).
5.2.2 Information About Taxa
A list of dung beetles found in the Atlantic Forest north of
the São Francisco River including Brejos de Altitude was
produced. We did two separate searches. The first was a
search for works presenting dung beetle records from the
region published between 2000 and 2021 and listed in online
databases (Scielo, Web of Science), web search engines
(Google Scholar, CAPES periodical portal, ScienceDirect),
and other resources such as SpringerLink and BioOne Online
Journals. We used the following key words to find these arti-
cles: Scarabaeidae, Scarabaeinae, rola-bosta, Dung beetle,
Scarab beetle, besouros escarabeíneos, besouros escara-
beídeos, Caatinga, Brejo de Altitude, Atlantic Forest, Floresta
Atlântica, Restinga, Nordeste, Maranhão, Piauí, Ceará, Rio
Grande do Norte, Paraíba, Pernambuco, and Alagoas. Gray
literature was not used.
The second search was done manually by checking all taxo-
nomic works on South American Scarabaeinae known to us to
have appeared  since the 1990s addressing South American
dung beetles as well as others published in the preceding
decades whose identifications were deemed reliable. These
taxonomic works were listed in Vaz-de-Mello and Cupello
(2018) as well as others published since then (Génier and
49
Cupello 2018; Valois et  al. 2018, 2020, 2022; González-­
Alvarado et al. 2019; Maldaner et al. 2019, 2021; Nunes and
Vaz-de-Mello 2019; Pacheco and Vaz-de-Mello 2019a, b;
Santana et  al., 2019; Sawaris et  al. 2019; Silva and Génier
2019; Silva and Valois 2019; Vieira et al. 2019; Cassenote et al.
2020; Cupello et  al. 2020, 2021; Lopera-Toro et  al. 2020;
Martínez-Revelo et al. 2020; Nunes et al. 2020; Rossini and
Vaz-de-Mello 2020; Silva et al. 2020, 2022; Chamorro et al.
2021; González-Alvarado and Vaz-de-Mello 2021; Moctezuma
and Halffter 2021; Montoya-Molina et  al. 2021; Montoya-
Molina and Vaz-de-Mello 2019a, b, 2021; Nazaré-Silva and
Silva 2021a, b; Costa-Silva et  al. 2022; Giraldo-Mendoza
2022; Maldaner and Vaz-de-Mello 2022). The 1990s, as
explained in Vaz-de-Mello and Cupello (2018), marked a rena-
scence in the taxonomic studies of the South American scara-
baeines, one that is still flourishing. Except for the commonest
and most easily identifiable species, identifications and geo-
graphic records appearing in papers published before then are
usually unreliable and, as such, not worth compiling here.
The tribe-level classification follows Tarasov and
Dimitrov (2016), whereas the genus- and species-level tax-
onomies are according to the most recent taxonomic revision
for each group. Taxa that suffered nomenclatural and taxo-
nomic changes since the publication of their records from
our studied area have these changes noted in “Remarks” sec-
tions. Species originally identified as “aff.” in groups whose
taxonomy is still to be revised remained listed as “aff.” here.
Species that were originally listed without a specific name,
but with the formula generic name + the “sp.” notation, con-
tinue to be listed here as such here unless we were able to
determine their correct identification.
Geographical data were taken from papers citing dung bee-
tles from localities in the Atlantic Forest north of São Francisco
River, in the states of Rio Grande do Norte, Alagoas,
Pernambuco, and Paraíba, all in the northeastern region of
Brazil (Appendices 5.1, 5.2, 5.3, and 5.4). A supervised clas-
sification of each land cover within our study region (tree
cover, shrubland, grassland, cropland, urban area, mangroves)
was obtained using worldwide land cover mapping from the
European Space Agency (ESA) (www.esa-­worldcover.org)
and ARCMAP 10.2 (ESRI 2016). The generated map was
used to plot the distribution of the dung beetle species.
5.2.3 Conservation Status
The species recorded were assessed in terms of their distri-
bution in the Atlantic Forest and in the focus area of this
work (north of the São Francisco River) for risk characteriza-
tion, as well as the IUCN Red List (2021) was consulted to
determine the threat level of each species. The areas were
evaluated in terms of their richness, similarity, and presence
of endemic species, or habitat specialists, to establish the
level needed for preservation.
50
5.3 Results
Our literature survey found 6 tribes, 23 genera, and 89 spe-
cies of dung beetles (Scarabaeidae, Scarabaeinae) present in
the Northern Atlantic Forest (Appendices 5.1, 5.2, 5.3, and
5.4). Records were found for 46 municipalities in the states
of Rio Grande do Norte, Paraíba, Pernambuco, and Alagoas,
in the Atlantic Forest and Brejos de Altitude north of the São
Francisco River (Figs. 5.1 and 5.2).
Scarabaeinae tribes have the following richness:
Deltochilini (formerly known as Canthonini), with six gen-
era and 29 species; Ateuchini, with four genera and eight
species; Phanaeini, with five genera and 12 species;
Onthophagini, with two genera and six species; Dichotomiini,
with a single genus and 16 species; Eurysternini, with a sin-
gle genus and five species. Four genera currently incertae
sedis at the tribal level have 14 species in the region.
The two richest genera in the region are Canthon and
Dichotomius, both with 16 species. Thirty-eight species were
recorded from only  one state  each (four in Paraíba, 22  in
Pernambuco and 12 in Alagoas), 21 occur in the three states,
and two occur in the four states (Fig. 5.3). No species have
been recorded from all 46 municipalities, with 16 being the
highest number. Only seven, however, have been recorded
from 16 to 10 municipalities. Most species had few records,
with an average of four per species (Appendices 5.1, 5.2, 5.3,
and 5.4; Fig. 5.4).
Considering only the distribution of the species within the
Atlantic Forest domain north of the São Francisco River, 75
species occurred in forests, 29 in restinga, and 47 in Brejos
de Altitude. Thirty-eight species were restricted to one loca-
tion, 11  in Ibateguara (Alagoas), one in Murici (Alagoas),
five in Caruaru (Pernambuco), four in Igarassu (Pernambuco),
two in Bezerros (Pernambuco), one in Ipojuca (Pernambuco),
one in Recife (Pernambuco), one in Areia (Paraíba), one in
Mataraca (Paraíba) and one in João Pessoa (Paraíba).
Pernambuco recorded 71 species, Alagoas 46, Paraíba 37,
and Rio Grande do Norte 9.
5.4 Taxonomy
Coleoptera Linnaeus, 1758
Scarabaeidae Latreille, 1802
Scarabaeinae Latreille, 1802
ATEUCHINI Perty, 1830
As defined by Vaz-de-Mello (2008), Ateuchini is most likely
a polyphyletic tribe (Tarasov and Génier 2015; Tarasov and
Dimitrov 2016). Thirty-one genera are currently classified in
it (Vaz-de-Mello 2008; see also the synonymies established
L. Iannuzzi et al.
in Vaz-de-Mello et  al. 2011a). Twenty-one of them are
arranged into two subtribes, Scatimina (17 genera), and
Ateuchina (four genera), the remaining ones deemed incer­
tae sedis in the tribe (Vaz-de-Mello 2008). Combined, these
genera have a mostly holotropical distribution (cf. Scholtz
et al. 2009).
ATEUCHINA Perty, 1830
Of the four genera constituting the exclusively New World
subtribe Ateuchina sensu Vaz-de-Mello (2008), only two are
present in the Pernambuco Endemism Center, Ateuchus
Weber, 1801 and Aphengium Harold, 1868.
Ateuchus Weber, 1801
Ateuchus is widely distributed in the Americas, from
New  York State (USA) to northern Argentina, including
the entire Brazilian territory and many of the Lesser
Antilles (Matthews 1966; Kohlmann 1984, 1997, 2000;
Vaz-de-­Mello et al. 2011a; M. Cupello, unpublished data).
As noted by Vaz-de-Mello (2007), as currently constituted,
the genus is most certainly merophyletic: On the one hand,
Aphengium and Deltorhinum are likely nested within it; on
the other, the so-called ovalis group (Martínez and
Martínez 1987) constitutes a separate clade apparently not
related to the true Ateuchina (M.  Cupello, unpublished
data). Including new species, Ateuchus comprises 133 spe-
cies and is currently under taxonomic revision by one of us
(Mario Cupello).
Ateuchus oblongus (Harold, 1883)
Biological and Ecological Data  The species has been col-
lected in pitfall traps baited with human feces and decaying
banana (M. Cupello, unpublished data). Recorded through-
out the northern half of the Brazilian Atlantic Forest, from
Alagoas to Rio de Janeiro (P. Lopes, Dec. 2021; M. Cupello,
unpublished data).
Records  Alagoas (Ibateguara).
Comments on Taxonomy  This species was identified as
Ateuchus aff. alipioi Pereira, 1954 in Filgueiras et al. (2015)
(M. Cupello, unpublished data). Originally described simply
as from Brazil (“Brasilien”; Harold 1883), we are the first to
record the presence of the species in a specific locality of the
country.
“Ateuchus” vigilans (Van Lansberge, 1874)
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna 51

Fig. 5.1  Distribution maps of

the localities where the
presence of dung beetles was
recorded in the Atlantic Forest
north of São Francisco River,
in Rio Grande do Norte,
Paraíba, Pernambuco, and
Alagoas states, Brazil. Red
circles – localities. Blue –
area of influence of the São
Francisco River basin

Biological and Ecological Data  They are crepuscular-­
nocturnal beetles that have coprophagous-feeding habits
(Genes et al. 2019; M. Cupello, unpublished data). The spe-
cies is widely distributed in the Brazilian Atlantic Forest,
ranging from Paraíba to São Paulo.
to a new genus in a forthcoming paper (M. Cupello, unpub-
lished data). This species was identified as Ateuchus aff. ovalis
in Iannuzzi et al. (2016). Agamopus convexus Balthasar, 1965,
a nominal species recently transferred to Ateuchus by Costa-
Silva et  al. (2022), is a likely junior subject synonym of
“Ateuchus” vigilans (M. Cupello, unpublished data).

Records  Paraíba (Mamanguape), Pernambuco (Abreu e

Lima, Araçoiaba, Igarassu, Recife), Alagoas (Ibateguara). Ateuchus semicribratus (Harold, 1868)

Remarks  Here, the generic name Ateuchus is given in quota- Biological and Ecological Data  This dark, matte species is
tion marks because the species belongs to the ovalis group a very common one in the semiarid Caatinga as well as in
(Martínez and Martínez 1987) and, as such, will be transferred adjacent habitats in northeastern Brazil (Hernandez et  al.
52 L. Iannuzzi et al.

Fig. 5.2  Distribution maps  of the dung beetles tribes in the Atlantic Forest north of São Francisco River, in Rio Grande do Norte, Paraíba,
Pernambuco, and Alagoas states, Brazil. Circles – localities of occurrence

Ateuchus volxemi (Preudhomme de Borre, 1886)

Biological and Ecological Data  Ateuchus volxemi has

coprophagous habits (Barretto et  al. 2021; M.  Cupello,
unpublished data) and ranges almost exclusively through the
Brazilian Atlantic Forest, from Paraíba to Mato Grosso do
Sul (M. Cupello, unpublished data). The only reliable record
from outside these forests is Brasília (De Oliveira Ribeiro
et al. 2022; M. Cupello, unpublished data).

Records  Paraíba (Mamanguape), Pernambuco (Araçoiaba,

Igarassu, Paudalho, Pesqueira – Serra do Ororubá, Recife),
Alagoas (Ibateguara).

Fig. 5.3  Venn diagram of the exclusive and shared dung beetles spe- Aphengium Harold, 1868
cies in the Atlantic Forest north of São Francisco River, from Rio Aphengium includes six species – two yet to be described –
Grande do Norte, Paraíba, Pernambuco, and Alagoas states, northeast-
that occur only in the Atlantic Forest of Brazil, from Alagoas
ern region of Brazil
to Santa Catarina (Silva and Vaz-de-Mello 2015; M. Cupello,
unpublished data).
2014; Vieira et  al. 2017; M. Cupello, unpublished data). It
shows coprophagous habits (Vieira and Silva 2012;
Aphengium ibateguara Silva & Vaz-de-Mello, 2015
M. Cupello, unpublished data).
Biological and Ecological Data  Collected from both human
feces and rotten meat, there are not enough data to establish
Records  Rio Grande do Norte (Canguaretama, Macaíba,
preferences (Silva and Vaz-de-Mello 2015). Only recorded
Natal, Parnamirim), Paraíba (Mamanguabe, Mataraca),
from Alagoas (Ibateguara) (Silva and Vaz-de-Mello 2015).
Pernambuco (Buíque – PARNA Catimbau, Gravatá, Ipojuca).
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna 53

Fig. 5.4  Histogram of the number of localities recorded for dung bee- region of Brazil. AL Alagoas, PE Pernambuco, PB Paraíba. Only spe-
tle species in the Atlantic Forest north of São Francisco River, from Rio cies with more than one occurrence
Grande do Norte, Paraíba, Pernambuco, and Alagoas states, northeast

Records  Alagoas (Ibateguara).
Remarks  This species was identified as Aphengium aff.
sordidum Harold, 1868 in Filgueiras et al. (2015), but it is
Aphengium ibateguara following the last revision of the
genus (Silva and Vaz-de-Mello 2015).
details). “Pery-Pery” seems to be the former name of the cur-
rent district of Pirituba (Paynter and Traylor 1991; Campaner
et  al. 2008; Collar and Kirwan 2018), in the Pernambuco
municipality of Vitória de Santo Antão. Pirituba lies about 50
southwest of Recife, Pernambuco’s capital city, and is part of
the Atlantic Forest region of the state, also known as “Zona
da Mata.”

SCATIMINA Vaz-de-Mello, 2008 Trichillum Harold, 1868

Of the 17 genera of this exclusively New World subtribe,
only two have been recorded from the Pernambuco
Endemism Center, Genieridium and Trichillum.
Genieridium Vaz-de-Mello, 2008
Genieridium presents a disjunct, amphiamazonian distribu-
tion (Vaz-de-Mello 2008). Seven species compose the genus
(Vaz-de-Mello 2008).
Genieridium margareteae (Génier & Vaz-de-Mello, 2002)
Trichillum is distributed throughout South America east of
the Andes (Vaz-de-Mello 2008; Vaz-de-Mello et al. 2011a).
It includes 11 described species and supposedly at least
another 30 awaiting description (Vaz-de-Mello 2008).
Trichillum sp.
Records  Pernambuco (Caruaru).

Trichillum externepunctatum Preudhomme de Borre, 1880

Biological and Ecological Data  Nothing is known about
the habits of this species. Its range seems to be mainly cen-
tered in the Caatinga, but there are at least two records from Biological and Ecological Data  This is a generalist species
Atlantic Forest localities in northeastern Brazil (Vaz-de-­ (Silva et al. 2014), considered as an indicator and is impor-
Mello 2008; listed below). tant for dung removal in Brazilian pastures (Tissiani et  al.
2017). This species has a crepuscular and nocturnal habit and
it can be found throughout the year in the state of Paraíba
Records  Rio Grande do Norte (Natal), Pernambuco (Vitória (Hernández and Endres 2011).
de Santo Antão).

Records  Rio Grande do Norte (Canguaretama, Natal,

Remarks  Génier and Vaz-de-Mello (2002) and Vaz-de-­ Parnamirim), Paraíba (Areia, João Pessoa, Mamanguape),
Mello (2008) examined three specimens of G. margareteae Pernambuco (Abreu e Lima, Bonito, Igarassu, Triunfo,
collected in 1892 by Pierre-Émile Gounelle at the locality of Vitória de Santo Antão), Alagoas (Ibateguara).
“Pery-Pery,” Pernambuco (see Gounelle 1909, for more
54 L. Iannuzzi et al.

Remarks  The record from Vitória de Santo Antão Records  Rio Grande do Norte (no more specific locality
(Pernambuco) is based on Vaz-de-Mello’s (2008) examina- known), Paraíba (Mataraca, Rio Tinto).
tion of material of the species labeled “Pery-Pery.” “Pery-­
Pery,” as explained in detail in the “remarks” under
Genieridium margareteae, is the former name of a district in Deltochilum (Calhyboma) verruciferum Felsche, 1911
the municipality of Vitória de Santo Antão.

Biological and Ecological Data  A large, mostly nocturnal

DELTOCHILINI Lacordaire, 1856 (= Canthonini) species. It is found abundantly in semiarid habitats, such as
Deltochilini (sensu Tarasov and Dimitrov 2016) is a mono- the Caatinga, but occurs also in adjacent more humid vegeta-
phyletic tribe, comprising 22 genera found exclusively in the tion (Salomão et  al. 2017; Silva et  al. 2007; Vieira et  al.
New World, with most species occurring in the Neotropics 2017). Attracted to both dung and rotten meat (Salomão
and some distributed in the Nearctic Region (Vulcano and et al. 2017; Vieira et al. 2017).
Pereira 1964; see many references cited in Cupello and Vaz-­
de-­Mello 2018).
Records  Pernambuco (Caruaru, Triunfo).
Deltochilum Eschscholtz, 1822
Deltochilum is a diverse genus with 114 named species
(Schoolmeesters 2022) and dozens of others to be described Deltochilum (Deltohyboma) calcaratum Bates, 1870
(González-Alvarado and Vaz-de-Mello 2021). They are
arranged into eight subgenera: Aganhyboma Kolbe, 1893,
Calhyboma Kolbe, 1893, Deltochilum s.tr., 1822, Bioogical and Ecological Data  This species has necropha-
Deltohyboma Lane, 1946, Euhyboma Kolbe, 1893, gous feeding habits (Vieira and Silva 2012). They are most
Hybomidium Shipp, 1897, Rubrohyboma Paulian, 1938, and often found in forest habitats and tend to benefit from the
Parahyboma Paulian, 1938. The genus is distributed from environmental conditions that are established by shade-­
the United States to Argentina (Vaz-de-Mello et al. 2011a). tolerant trees (Filgueiras et al. 2009, 2015).
Although the monophyly of the genus has not yet been
tested, it appears to one of us that the recent description of
Atlantemolanum González-Alvarado et  al. (2019) and its Records  Alagoas (Ibateguara).
ranking as a genus may have rendered Deltochilum paraphy-
letic (M. Cupello, personal observation).
Deltochilum (Deltohyboma) irroratum (Castelnau, 1840)
Deltochilum (Aganhyboma) alpercata Silva et al., 2015

Biological and Ecological Data  With generalist feeding

Biological and Ecological Data  The species is endemic to
northeastern Brazil (Silva et  al. 2015; Araújo et  al. 2020).
Like other members of the subgenus, it is a nocturnal preda-
tor of millipedes (Araújo et al. 2020).
Records  Pernambuco (Camaragibe, Paulista), Alagoas
(Murici).
Deltochilum (Aganhyboma) kolbei Paulian, 1938
habits, it is believed that this species feeds preferably on car-
casses, while dung is used as a complement (Medina and
Lopes 2014; Salomão and Iannuzzi 2017; Silva et al. 2007).
They display a form of thanatosis characterized by the action
of remaining immobile and opening their legs when they feel
threatened (Wuerges and Hernández 2013).
Records  Paraíba (Areia, João Pessoa), Pernambuco (Abreu
e Lima, Caruaru, Cabo de Santo Agostinho  – Paiva,
Sirinhaém), Alagoas (Ibateguara).

Biological and Ecological Data  The species is endemic to Deltochilum (Deltohyboma) sextuberculatum Bates, 1870
northeastern Brazil and is apparently an inhabitant of sandy species group
lowland Atlantic Forest (Silva et  al. 2015). Feeding habits
are unknown.
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna 55

Records  Pernambuco (Itamaracá, Cabo de Santo Agos­ and Figueroa 2013; Figueroa and Edmonds 2015; Cano
tinho – Paiva, Recife – Dois Irmãos, Goiana – Tabatinga). 2018; Valois et al. 2020; note that, with the synonymy estab-
lished by Vaz-de-Mello et  al. [2011a] between Hypo­
canthidium Balthasar, 1938 and Anomiopus, the type species
Remarks  This group of species was proposed for the sub- of the former, H. globulum Balthasar, 1938, became an
genus Deltohyboma by González-Alvarado and Vaz-de-­ Anomiopus. It is, therefore, included in our count. This has
Mello (2021) and is under revision. It is composed of escaped Schoolmeesters’s [2022] attention).
Deltochilum sextuberculatum Bates, 1870 and at least 10
undescribed species (González-Alvarado and Vaz-de-Mello Anomiopus nigricans Westwood, 1842
2021). In a previous study (Filgueiras et al. 2009), the speci-
mens belonging to the group were treated as Deltochilum
morbilosum (Burmeister, 1848). Species of this group occur Biological and Ecological Data  Feeding habits are
throughout Brazil, in both forest, Caatinga and cerrado envi- unknown, as the specimens were collected only in flight
ronments (González-Alvarado and Vaz-de-Mello 2021). All interception traps (Sampaio et  al. 2009). The species is
are reduced in size when compared to other Deltochilum known solely from Bahia and Pernambuco (Canhedo 2006;
(<10 mm) (González-Alvarado and Vaz-de-Mello 2021). Sampaio et al. 2009).

Deltochilum (Euhyboma) brasiliense (Castelnau, 1840) Records  Pernambuco (Igarassu).

Biological and Ecological Data  This large (>20 mm) roller
dung beetle, of the monospecific subgenus Euhyboma, is
considered common in the Atlantic Forest as well as in forest
enclaves in the Pampas grasslands (Araújo et  al. 2020;
Nazaré-Silva and Silva 2021a). The species is considered a
generalist (Almeida and Louzada 2009), being recorded
from carcasses, having forensic importance (Almeida et al.
2015).
Records  Pernambuco (Caruaru, Pesqueira  – Serra de
Ororuba), Alagoas (Murici).
Anomiopus parallelus (Harold, 1862)
Biological and Ecological Data  As reported by Canhedo
(2006), this species, widely distributed in the Amazon Basin,
is also known in the Atlantic Forest from a single specimen
supposedly collected by Moacyr Alvarenga in April 1972 at
Caruaru, Pernambuco. We wonder whether this disjunction
is real or whether the specimen may be mislabeled or even
misidentified.
Records  Pernambuco (Caruaru).

Deltochilum (Hybomidium) pseudoicarus Balthasar, 1939

Biological and Ecological Data  They are cupreous (or,
rarely, black) beetles with diurnal habits and generalist feed-
ing habits, with no significant preference for food  type
(González-Alvarado and Vaz-de-Mello 2014; Harada et  al.
2020).
Records  Paraíba (João Pessoa, Mamanguape, Mataraca),
Pernambuco (Abreu e Lima), Alagoas (Ibateguara).
Anomiopus Westwood, 1842
The genus Anomiopus is composed of 63 described species,
all endemic to the Neotropical region, being present from
Guatemala to Argentina (Canhedo 2004a, b, 2006; Edmonds
Canthon Hoffmannsegg, 1817
Canthon is a merophyletic genus distributed from Canada
to Argentina (Medina et al. 2003). Most of its 180 described
species (Vaz-de-Mello et  al. 2020; Schoolmeesters 2022)
are classified into nine subgenera – Bajacanthon Halffter,
2022, Canthon s.str., Francmonrosia Pereira & Martínez,
1959, Glaphyrocanthon Martínez, 1948, Goniocanthon
Pereira & Martínez, 1956, Nesocanthon Pereira & Martínez,
1956, Peltecanthon Pereira, 1953, Pseudepilissus Martínez,
1948, and Trichocanthon Pereira & Martínez, 1959  – ,
while others are incertae sedis in the genus (Halffter and
Martínez 1977). The microtaxonomy of the group is still
largely unexplored [cf. Cupello and Vaz-de-Mello 2018]
and most of the identification presented here are necessar-
ily tentative.
Canthon (Canthon) aff. juvencus Harold, 1868
56
Biological and Ecological Data  The feeding habits of this
species are still unknown. Broad distribution, from Costa
Rica to Bolivia and Brazil (Schoolmeesters 2022).
Records  Pernambuco (Igarassu).
Canthon (Canthon) lituratus (Germar, 1813)
Biological and Ecological Data  Diurnal beetles, this spe-
cies has coprophagous habits (Rodrigues and Flechtmann
1997). Widespread from Costa Rica to South America
(Vulcano and Pereira 1964; Howden and Young 1981; Solís
and Kohlmann 2002; but not in the Antilles as said by Harold
[1868], see Matthews [1966]), it tolerates conditions from a
wide variety of habitats, both forested and open ones as well
as anthropized environments (Vaz-de-Mello et al. 2014).
Records  Paraíba (Areia, Mamanguape), Pernambuco
(Caruaru, Igarassu, Itamaracá, Tamandaré).
Canthon (Canthon) mutabilis Lucas, 1859
Biological and Ecological Data  This species is, overall,
copronecrophagous, being attracted to both feces and rotten
meat, but shows a preference for carcasses (Silva et al. 2014;
Salomão and Iannuzzi 2017).
Records  Pernambuco (Abreu e Lima, Caruaru, Igarassu,
Itamaracá, Cabo de Santo Agostinho  – Paiva), Alagoas
(Ibateguara).
Canthon (Canthon) nigripennis Van Lansberge, 1874
Biological and Ecological Data  Measuring 0.61 ± 0.04 cm
(Hernández and Endres 2011), this small roller species is
diurnal (Costa et al. 2013; Medina and Lopes 2014; Iannuzzi
et  al. 2016). These beetles are often found in periods of
drought (Salomão and Iannuzzi 2015), and can occasionally
be seen in pastures close to forests and clearings (Tissiane
et  al. 2017). Their distribution is limited to northeastern
Brazil (Schoolmeesters 2022).
Records  Paraíba (João Pessoa), Pernambuco (Abreu e
Lima, Cabo de Santo Agostinho – Paiva, Goiana – Tabatinga,
L. Iannuzzi et al.
Igarassu, Ipojuca  – Maracaípe, Ipojuca  – Muro Alto,
Itamaracá, Recife  – Dois Irmãos, Sirinhaém, Tamandaré),
Alagoas (Ibateguara).
Canthon (Canthon) piluliformis Blanchard, 1846
Biological and Ecological Data  They have coprophagous
habits (Oliveira et al. 2021) and are known from Brazil and
Argentina (Schoolmeesters 2022). Small-bodied beetles,
they are more commonly found in more open, anthropized
environments, being abundant in sugarcane matrices and
pastures (Filgueiras et al. 2015). However, the species was
also considered an indicator of riparian forest in a Caatinga
matrix in Bahia state (Vieira et al. 2017).
Records  Pernambuco (Itamaracá), Alagoas (Ibateguara).
Canthon (Canthon) virens chalybaeus Blanchard, 1846
Biological and Ecological Data  They use both feces and
rotten meat (Costa et al. 2013). These beetles can also show
predatory behavior, being predators of leaf-cutting ant
queens, using their abdomens for oviposition (Hertel and
Colli 1998; Vaz-de-Mello et al. 1998; Forti et al. 2012). The
subspecies occurs from Venezuela and the Guianas to south-
ern Brazil (Schoolmeesters 2022).
Records  Paraíba (Areia, Mataraca); Pernambuco (Abreu e
Lima, Caruaru, Ibateguara, Igarassu, Itamaracá, Cabo de
Santo Agostinho  – Paiva, Sirinhaém, Goiana  – Tabatinga);
Alagoas (Ibateguara).
Canthon (Canthon) virens scrutator Balthasar, 1939
Biological and Ecological Data  Generalist beetles
(Salomão and Iannuzzi 2017). According to Vaz-de-Mello
et al. (2021), the subspecies scrutator may be a forest habitat
specialist, in which case habitat loss could become a pres-
sure for it.
Records  Pernambuco (Abreu e Lima, Sirinhaém).
Canthon (Francmonrosia) aff. carbonarius Harold, 1868
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna
Biological and Ecological Data  They have generalists
feeding habits (Silva et al. 2007). They may also act as either
predators or secondary disperses of myrmecochorous seeds
available in the environment (Iannuzzi et al. 2013).
Records  Pernambuco (Bezerros – Serra Negra, Caruaru).
Canthon (Glaphyrocanthon) oliverioi (Pereira & Martínez,
1956)
Biological and Ecological Data  They have coprophagous
habits, with special attractiveness to human feces (Silva et al.
2012). The species is present in Brazil, Paraguay, and
Argentina (Schoolmeesters 2022).
Records  Pernambuco (Sirinhaém), Alagoas (Ibateguara).
Canthon (Glaphyrocanthon) simulans (Martínez, 1950)
Biological and Ecological Data  The species has been
recorded from Venezuela, Peru, and Brazil (Schoolmeesters
2022) and is abundant in pastures (Silva et al. 2014). Feeding
habits are unknown.
Records  Pernambuco (Abreu e Lima, Sirinhaém).
Canthon (Goniocanthon) smaragdulus (Fabricius, 1781)
Biological and Ecological Data  The species has been
mostly collected in pitfall traps baited with human feces
(Nunes et  al. 2018). The populations from northeastern
Brazil were classified by Nunes et al. (2018) in the subspe-
cies C. smaragdulus subviridis Schmidt, 1922, which would
differ from the nominotypical subspecies in coloration.
Cupello et al. (2021), however, challenged this classification
and proposed the synonymy between the subspecific names,
deeming the species monotypic.
Records  Alagoas (Ibateguara).
Canthon (Peltecanthon) haroldi Nunes et al., 2020
57
Biological and Ecological Data  Coprophagous habits
(Nunes et al. 2020; P. Cerqueira, pers. comm., March 2022).
They are most often found in the driest period of the year
(Salomão and Iannuzzi 2015) and range exclusively in
Brazil, from Alagoas to Rio de Janeiro (Nunes et al. 2020).
Records  Pernambuco (Sirinhaém), Alagoas (Rio Largo).
Remarks  This species was identified as Canthon sulcatus
in works published previously to Nunes et  al. (2020)
(Salomão and Iannuzzi 2015; Salomão et al. 2016).
Canthon (Peltecanthon) staigi (Pereira, 1953)
Biological and Ecological Data  These medium-sized dung
beetles are diurnal (Medina and Lopes 2014) and coprone-
crophagous (Costa et al. 2013). They are confined to closed
canopy forests of the Atlantic Forest ecosystem (Halffter and
Martínez 1967; Hernández et  al. 2014), ranging from
Pernambuco, in Brazil, southward to Argentina and Paraguay
(Nunes et al. 2020).
Records  Pernambuco (Bonito – Colônia, Caruaru – Parque
Estadual João Vasconcelos), Alagoas (Ibateguara, União dos
Palmares).
Canthon (Peltecanthon) terciae Nunes et al., 2020
Biological and Ecological Data  Attracted to both dung and
rotten meat and endemic to the Atlantic Forest north of the
São Francisco River (Nunes et al. 2020).
Records  Rio Grande do Norte (Baia Formosa), Paraíba
(Areia, Caaporã, Mamanguape, Mataraca, João Pessoa, Rio
Tinto), Pernambuco (Abreu e Lima, Bonito, Camaragibe,
Caruaru – Terra Vermelha, Itamaracá, Paudalho, Pesqueira –
Serra do Ororubá, Tamandaré).
Remarks  This species had been identified as Canthon
staigi in studies published before the revision of Peltcanthon
by Nunes et al. (2020) (Endres et al. 2007; Costa et al. 2009,
2013; Hernández et al. 2014; Salomão et al. 2014; Salomão
and Iannuzzi 2015; Salomão et al. 2016; Iannuzzi et al. 2016;
58
Ferreira-Neto et al. 2017; Leite et al. 2018; Salomão et al.
2017; Barretto et al. 2021).
Canthon (incertae sedis) histrio (Le Peletier & Serville,
1828)
Biological and Ecological Data  Diurnal beetles with
coprophagous habits (Harada et al. 2020). The taxon varies
from being treated as a subspecies of Canthon septemmacu­
latus (Latreille, 1807) (e.g., Halffter and Martínez 1977) to
as a full species on its own right (e.g., Vaz-de-Mello and
Cupello 2018; Araújo et al. 2020). This matter, as well as the
distribution of the taxon, is yet to be settled.
Records  Pernambuco (Abreu e Lima, Igarassu).
Canthon (incertae sedis) machadoi (Martínez and Pereira,
1967)
Biological and Ecological Data  With unknown feeding
habits, this species is known exclusively from the type series
collected at a “brejo de altitude” in Bezerros, Pernambuco
(Cupello and Vaz-de-Mello 2018). Whether it is indeed a
microendemic of this place or if it is more widely distributed,
but rare, is still an open question.
Records  Pernambuco (Bezerros – Serra Negra).
Canthon (incertae sedis) aff. maldonadoi Martinez, 1951
Biological and Ecological Data  They have generalist
feeding habits, being attracted to both feces and rotten
meat (Hernández 2007). The true C. maldonadoi has been
recorded in Brazil from Mato Grosso do Sul (Vaz-de-
Mello et  al. 2017) as well as in Argentina (Vulcano and
Pereira 1964). Whether the Paraiba  species identified as
C. aff. maldonadoi by Hernández (2007) is the same is
still uncertain.
Records  Pernambuco (Caruaru, Igarassu).
Malagoniella Martínez, 1961
L. Iannuzzi et al.
Malagoniella has nine species organized into two subgenera:
Malagoniella s.str. and Megathopomima Martínez, 1961.
The genus ranges from southern Texas (USA) to northern
Argentina, being richest in South America south of the
Amazon (Halffter and Martínez 1966).
Malagoniella (Malagoniella) astyanax (Olivier, 1789)
Biological and Ecological Data  They are crepuscular-­
nocturnal beetles that present coprophagous feeding hab-
its (Halffter and Martínez 1966; Hernández 2007). Large
dung beetles, they occur in several biomes (Caatinga,
humid forests, and pastures) and are apparently organized
into four or five geographical isolates distributed from
southern Texas (USA) to northern Argentina (Halffter
et  al. 1960; Halffter and Martínez 1966). These isolates
are apparently slightly heteromorphic and each has been
classified as a separate subspecies (Halffter et  al. 1960;
Halffter and Martínez 1966). The nominotypical subspe-
cies is the one present in the states of the Pernambuco
Endemism Center (Halffter et  al. 1960; Halffter and
Martinez 1966).
Records  Rio Grande do Norte (unknown locality), Paraíba
(unknown locality), Pernambuco (Caruaru), Alagoas
(unknown locality).
Pseudocanthon Bates, 1887
Pseudocanthon is a small genus with 11 species and two
subspecies (Nazaré-Silva and Silva 2021b) and is distributed
through much of the New World, from the United States to
Argentina and the Antilles (Matthews 1966; Vaz-de-Mello
et al. 2011a; Nazaré-Silva and Silva 2021b).
Pseudocanthon xanthurus (Blanchard, 1846)
Biological and Ecological Data  They have coprophagous
habits (Silva et al. 2014) and are usually found in pastures,
clearings and natural fields, being important in excrement
removal in Brazil (Tissiani et al. 2017). The species is widely
distributed in South America and presents interesting pheno-
typic variation in coloration and the shape of the male geni-
talia (Nazaré-Silva and Silva 2021b).
Records  Rio Grande do Norte (Natal, Parnamirim),
Pernambuco (Abreu e Lima, Araçoiaba, Camaragibe,
Caruaru, Goiana  – Tabatinga, Igarassu, Recife), Alagoas
(Ibateguara).
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna 59

Nomenclatural Note  Nazaré-Silva and Silva (2021b) mis- Remarks  Sylvicanthon obscurus is part of the furvus sub-
takenly reported the publication year of Pseudocanthon xan­ group of the candezei group (Cupello and Vaz-de-Mello
thurus as 1847. The correct date is 1846. Canthon xanthurum 2018) and, before the revision of the genus, it was identified
[sic], the original combination (the gender of Canthon is as Sylvicanthon sp. (Costa et al. 2013; Salomão and Iannuzzi
actually masculine, not neuter; Cupello and Vaz-de-Mello 2015; Iannuzzi et  al. 2016), Sylvicanthon aff. machadoi
2018), first appeared on page 166 of Vol. VI, Part 2, of Alcide (Filgueiras et  al. 2015) and Sylvicanthon foveiventris
d’Orbigny’s Voyage dans l’Amérique méridionale. This page (Salomão and Iannuzzi 2015).
was part of livraison 79 (pp. 153–168), which was published
no later than 1846 and whose content was, as correctly
pointed out by Nazaré-Silva & Silva, authored by Blanchard DICHOTOMIINI Pereira, 1954
(Sherborn and Woodward 1901: 389; Evenhuis 1997: 573). Dichotomiini (sensu Tarasov and Dimitrov 2016) is a mono-
Here, like in Cupello et al. (2022), we adopt this date. Note, phyletic tribe, comprising four genera distributed in the
however, that the wrapper of livraison 79 is dated 1845 Neotropical Region, one of them, Dichotomius, also occur-
(Sherborn and Griffin 1934; Evenhuis 1997; Bousquet 2016), ring in the Nearctic.
but this should be disregarded as the Voyage dans l’Amérique
méridionale wrappers are not reliable sources for dating the Dichotomius Hope, 1838
corresponding livraisons (Evenhuis 1997). Dichotomius comprises 199 named species
(Schoolmeesters 2022) distributed throughout the
Americas, from the United States to Argentina. They com-
Sylvicanthon Halffter & Marttinez, 1977 prise four subgenera: Dichotomius s. str., Homocanthonides
Sylvicanthon is a Neotropical genus composed of 15 species Luederwaldt, 1929, Selenocopris Burmeister, 1846, and
organized into two species groups, the enkerlini group, with Cephagonus Luederwaldt, 1929 (Nunes and Vaz-de-Mello
one species, and the candezei group, including five sub- 2019). Traditionally, the name Luederwaldtinia Martínez
groups (Cupello and Vaz-de-Mello 2018). Except for a spe- 1951 was used for the subgenus now known as
cies living in Caatinga-Cerrado-Amazonia ecotones, the Selenocopris, with the latter being used for Cephagonus.
others are endemic to the rainforests of the Neotropical Corrections put forward by Nunes and Vaz-de-Mello
region, from Nicaragua to Colombia, in most of the Amazon, (2019) changed the nomenclature. Despite the recent
and in the Atlantic Forest, from Pernambuco to São Paulo stream of papers addressing the topic (e.g., Nunes and
(Cupello and Vaz-de-Mello 2018). Cupello and Vaz-de-­ Vaz-de-Mello 2013, 2019; Nunes et  al. 2016; Maldaner
Mello (2018) hypothesized that the genus is monophyletic et  al. 2015, 2018; Valois et  al. 2017, 2022; Montoya-
and originated in the Amazon, dispersing to the Atlantic Molina and Vaz-de-Mello 2019b, 2021; Pardo-­Díaz et al.
Forest twice independently during the Neogene or in the 2019; Cassenote et  al. 2020; Rossini and Vaz-de-­Mello
Quaternary. 2020; Silva et al. 2020; Chamorro et al. 2021; Maldaner
and Vaz-de-Mello 2022), the systematics of the
Sylvicanthon obscurus (Schmidt, 1920) Dichotomius is still largely unresolved, whether in terms
of micro- or macrotaxonomy. The number of undescribed
species appears to be high and the genus is likely paraphy-
Biological and Ecological Data  They have coprophagous letic by not including Isocopris, Chalcocopris, and
habits and are nocturnal (Cupello and Vaz-de-Mello 2018). Holocephalus (Cupello et al. 2020).
They are found most often in the spring and summer
(records from October, November, December, January, and Dichotomius (Dichotomius) bos (Blanchard, 1846)
July), and are restricted to closed forest areas from
Pernambuco to Espírito Santo, in Brazil (Silva et al. 2010;
Cupello and Vaz-­de-­Mello 2018). The species shows an Biological and Ecological Data  They are predominantly
interesting geographical variation in color (Cupello and coprophagous, frequently caught feeding on cattle dung
Vaz-de-Mello 2018). (Harada et  al. 2020). This species is mostly found in pas-
tures, with wide distribution in the grasslands of the South
American Dry Diagonal in Brazil, Bolivia, Paraguay, and
Records  Pernambuco (Abreu e Lima, Bezerros  – Serra Argentina (Luederwaldt 1929; Maldaner et al. 2021).
Negra, Igarassu, Sirinhaém), Alagoas (Ibateguara).
60
Records  Paraíba (Areia), Pernambuco (Caruaru, Igarassu,
Itamaracá, Recife).
Dichotomius (Cephagonus) fernandosilvai Nunes and Vaz-­
de-­Mello, 2019 Records  Pernambuco (Bonito), Alagoas (Ibateguara).
Biological and Ecological Data  Unknown. Known only
from Pernambuco (Nunes and Vaz-de-Mello 2019).
Records  Pernambuco (Caruaru).
Dichotomius (Cephagonus) filgueirasi Nunes & Vaz-de-­ generalist feeding habits, being attracted to both feces, rotten
Mello, 2019
Biological and Ecological Data  Habits of this species are
still unknown. It is endemic to the northern Atlantic Forest
(Nunes and Vaz-de-Mello 2019).
Records  Paraíba (Mamanguape), Pernambuco (Abreu e
Lima, Recife  – Dois Irmãos, Sirinhaém), Alagoas
(Ibateguara).
Remarks  Dichotomius filgueirasi was firstly described in
the revision of Dichotomius (Cephagonus) by Nunes and
Vaz-de-Mello (2019). This species had been previously iden-
tified as Dichotomius ascanius (Harold, 1869) in Salomão
and Iannuzzi (2015), as Dichotomius bicuspis (Germar,
1823) in Filgueiras et al. (2009) and Costa et al. (2013), and
as Dichotomius aff. fissus (Harold, 1867) in Filgueiras et al.
(2011a).
Dichotomius (Dichotomius) aff. depressicollis (Harold, 1867)
Biological and Ecological Data  The feeding habits of this
species are still unknown. They are nocturnal beetles
(Hernández et al. 2019).
Records  Paraíba (João Pessoa), Pernambuco (Abreu e
Lima, Sirinhaém), Alagoas (Ibateguara).
Dichotomius (Dichotomius) mormon (Ljungh, 1799)
L. Iannuzzi et al.
Biological and Ecological Data  These beetles seem to
have a high predilection for forest habitats (Filgueiras et al.
2015; Lima et al. 2015). Feeding habits are unknown.
Dichotomius (Selenocopris) carbonarius (Mannerheim,
1829)
Biological and Ecological Data  The species occurs in
Brazilian pastures (Tissiani et  al. 2017) as well as in
Argentina and Paraguay (Schoolmeesters 2022). They have
meat and bananas (Frizzas et  al. 2020). These beetles are
apparently aclimated  to urbanized environments (Frizzas
et al. 2020).
Records  Pernambuco (Bezerros  – Serra Negra, Brejo da
Madre de Deus, Triunfo).
Dichotomius (Selenocopris) geminatus (Arrow, 1913)
Biological and Ecological Data  They are nocturnal, gener-
alist beetles, being attracted to both feces and rotten meat.
They are found most often in open habitats (Silva et  al.
2010).
Records  Rio Grande do Norte (Natal), Paraíba (Areia,
Mamanguape), Pernambuco (Goiana – Tabatinga, Igarassu,
Ipojuca – Maracaípe, Ipojuca – Muro Alto, Tamandaré).
Dichotomius (Selenocopris) gilletti Valois et al., 2017
Biological and Ecological Data  They have generalist feed-
ing habits, being attracted to both feces and rotten meat
(Costa et al. 2009; Silva et al. 2010; Salomão et al. 2021).
The range of the species is limited to northeastern Brazil
(Valois et al. 2017; Araújo et al. 2020).
Records  Paraíba (Areia, João Pessoa), Pernambuco (Abreu
e Lima, Bonito, Brejo da Madre de Deus, Cabo de Santo
Agostinho, Camaragibe, Caruaru – Terra Vermelha, Igarassu,
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna
Paudalho, Recife  – Dois Irmãos, Sirinhaém), Alagoas
(Murici).
Remarks  Dichotomius gilletti was first described in the
revision of the Dichotomius sericeus species group by
Valois et al. (2017). Specimens belonging to the species had
been previously identified as Dichotomius aff. sericeus
(Harold, 1867) in Costa et  al. (2009, 2013), Filgueiras
et al. (2009), Silva et al. (2010), and Salomão and Iannuzzi
(2015).
Dichotomius (Selenocopris) guaribensis Valois et al., 2017
Biological and Ecological Data  They have generalist feed-
ing habits, being attracted to both feces and rotten meat
(Salomão et al. 2020). They seem also to be associated with
forests and coastal plateau savannas (Endres et  al. 2007;
Valois et al. 2017). These beetles are considered very sensi-
tive to anthropogenic impacts (Salomão et al. 2020).
Records  Paraíba (João Pessoa, Mamanguape), Pernambuco
(Ipojuca – Maracaípe).
Remarks  Prior to Valois et al. (2017), specimens collected
in the Guaribas Biological Reserve, Mamanguape, Paraíba,
were identified as Dichotomius sericeus (Harold, 1867)
(Endres et al. 2007).
Dichotomius (Selenocopris) iannuzziae Valois et al., 2017
Biological and Ecological Data  They have generalist feed-
ing habits (Salomão et  al. 2021) and are distributed from
Pernambuco to Minas Gerais (Valois et  al. 2017; Araújo
et al. 2020; Silva et al. 2020).
Records  Pernambuco (Bonito, Brejo da Madre de Deus,
Cabo de Santo Agostinho, Camaragibe, Caruaru, Igarassu,
Sirinhaém), Alagoas (Ibateguara).
Remarks  Prior to Valois et al. (2017), specimens belonging
to this species were identified as Dichotomius aff. sericeus
(Harold, 1867) (Filgueiras et  al. 2011a; Salomão and
Iannuzzi 2015).
61
Dichotomius (Selenocopris) aff. irinus (Harold, 1867)
Biological and Ecological Data  Dichotomius irinus is noc-
turnal (Genes et al. 2019).
Records  Paraíba (Mataraca).
Dichotomius (Selenocopris) machadoi Martínez & Pereira,
1967
Biological and Ecological Data  This species is known
exclusively from the type series collected at a “brejo de alti­
tude” in Bezerros, Pernambuco (Martínez and Pereira 1967).
The feeding habits are unknown.
Records  Pernambuco (Bezerros – Serra Negra).
Dichotomius (Selenocopris) nisus (Olivier, 1789)
Biological and Ecological Data  They are nocturnal
beetles that have coprophagous habits. The species is
widely distributed in South America (Cassenote et  al.
2020). It can be found more frequently in open Caatinga
and pastures, and less frequently in closed areas such as
the Atlantic Forest and the Amazon, with very low abun-
dance in these places (Liberal et al. 2011; Tissiani et al.
2017). They have large biomass and are important in
removing large amounts of excrements from pastures
(Tissiani et al. 2017).
Records  Paraíba (Araruna, Areia, Mamanguape, Mataraca),
Pernambuco (Abreu e Lima, Caruaru, Floresta, Igarassu,
Ipojuca  – Maracaípe, Tamandaré, Triunfo), Alagoas
(Ibateguara).
Dichotomius (Selenocopris) punctulatipennis (Luederwaldt
1930)
Biological and Ecological Data  The species is widely dis-
tributed in the Brazilian Atlantic Forest, from Pernambuco
southward to São Paulo (Nunes and Vaz-de-Mello 2019). It
occupies both lowland and submontane forests as well as
62 L. Iannuzzi et al.

“brejos de altitude” in Pernambuco (Nunes and Vaz-de-­ EURYSTERNINI Vulcano et al., 1961
Mello 2019). Eurysternini is a monophyletic tribe, comprising a single
genus widely distributed in the Neotropical region (Génier
2009; Camero-R and Lobo 2012). Génier (2009) treated
Records  Pernambuco (Caruaru). the taxon as a subtribe of Oniticellini, but this has not
been supported by subsequent phylogenetic analyses
(Tarasov and Génier 2015; Philips 2016; Tarasov and
Remarks  Nunes and Vaz-de-Mello (2019) mentioned in the Dimitrov 2016).
“distribution” section under D. punctulatipennis the pres-
ence of the species in the state of Alagoas, but no specimens Eurysternus Dalman, 1824
from there are listed in their “material examined”. The Eurysternus includes 53 species in 11 species groups and is
Alagoas mention was likely a lapse even though, judging distributed exclusively in the Neotropics (Génier 2009).
from the points correctly recorded by them for the species, it
is indeed  expected that D. punctulatipennis should eventu- Eurysternus calligrammus Dalman, 1824
ally be found to occur in the state.

Biological and Ecological Data  The species is known

Dichotomius (Selenocopris) schiffleri Vaz-de-Mello et  al.,
2001
Biological and Ecological Data  The adults are generalists,
feeding on feces, rotten meat, eggs, fruits, and decomposing
fungi (Vaz-de-Mello and Louzada 2008).
uniquely from the Atlantic Forest of the Brazilian states of
Alagoas, Minas Gerais, and Rio de Janeiro (Génier 2009;
Araújo et al. 2020). It occurs in forests up to 700 m and has
been collected using pitfall traps baited with excrements
(Génier 2009; Araújo et al. 2020).
Records  Alagoas (Murici).

Records  Pernambuco (Ipojuca  – Maracaípe, Ipojuca  –

Muro Alto). Eurysternus caribaeus (Herbst, 1789)

Remarks  Typical from the arboreal restinga of the Atlantic
Forest, this species was included in the IUCN Red List
(2021) as Threatened due to the ongoing destruction of its
habitats. It ranges exclusively through Brazil, from
Pernambuco to Espírito Santo (Valois et al. 2017; Silva et al.
2020).
Biological and Ecological Data  These beetles are consid-
ered to be diurnal (Feer and Pincebourde 2005) and are
highly generalist in terms of feeding habits (Génier 2009).
They can be found in a wide variety of forest habitats
throughout the Neotropics, from Mexico to Argentina
(Génier 2009).

Dichotomius (Selenocopris) semisquamosus (Curtis, 1844) Records  Pernambuco (Abreu e Lima, Caruaru, Igarassu,
Pesqueira – Serra do Ororubá); Paraíba (Areia, João Pessoa).

Biological and Ecological Data  They have coprophagous

habits (Silva et  al. 2007). They can be found in degraded
environments, clearings and pastures, and have been reported
at 1000 m or more (Tissiani et al. 2017).
Records  Paraíba (João Pessoa, Mamanguape, Mataraca),
Pernambuco (Caruaru, Igarassu, Ipojuca  – Maracaípe,
Tamandaré).
Nomenclatural Notes  The authorship of Eurysternus
caribaeus deserves explanation. This species-group name
firstly appeared in the combination Scarabaus caribaeus in
the second volume (of 10) of part A. Käfer of Natursystem
aller bekannten in- und ausländischen Insekten, als eine
Fortsetzung der von Büffonschen Naturgeschichte, a series
published in 21 volumes between 1783 and 1806 by the
German naturalists Carl Gustav Jablonsky and Johann
Friedrich Wilhelm Herbst. According to Evenhuis (1997),
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna
Jablonsky was the sole author of volume 1, whereas all the
other volumes of part A would have Herbst as their sole
author. This would make Herbst alone the author of S. carib­
aeus. Bousquet (2016), however, writes that, besides having
sole-authored the first volume, as said by Evenhuis,
Jablonsky was also the first author of volume 2, the one
where S. caribaeus first appeared, with Herbst as its second
author. The authorship of S. caribaeus, therefore, would be
Jablonsky & Herbst. To date, most workers (if not all) have
treated Herbst as the sole author of E. caribaeus, including
all major catalogues and taxonomic works (e.g., Harold
1869; Gillet 1911; Blackwelder 1944; Jessop 1985; Génier
2009; Schoolmeesters 2022). This seems to be correct, but
not because, as said by Evenhuis (1997), Herbst was the
single author of volume 2.
Volume 2’s preface (“Vorrede”), signed by Herbst and
dated March 1st, 1789, explains that Jablonsky was respon-
sible for the text up to Scarabaus fossor, starting on page
128, whereas the rest of the volume was written by Herbst
alone. This makes sense for two reasons. Firstly, Bousquet
(2016) informed that volume 2 was published into two sepa-
rate hefte, the first, in 1787, containing (among other parts
not relevant here) pages 1–128, the second, in 1789, contain-
ing pages 129–330 and the preface. Secondly, Jablonsky
died in 1787, the year of publication of the first 128 pages of
volume 2. It seems clear, therefore, that Herbst simply took
over the work for volume two from where Jablonsky had left
upon his death. Indeed, that this volume was started by
Jablonsky and finished by Herbst is also expressly stated on
its title page (“[…] zu bearbeiten angefangen von Carl
Gustav Jablonsky, und fortgesetzt von Johann Friedrich
Wilhelm Herbst […]”). On the other volumes’ title pages,
either Jablonsky’s (volume 1) or Herbst’s (3–10) name
appears alone. This double attribution of the authorship on
the title page of volume 2 was likely what misled Bousquet
into thinking that the whole volume had been authored by the
two naturalists. However, the content and any new names
appearing in this volume must be credited to the author of
each part of the text: up to page 133 (i.e., the text of heft 1
plus the end of the text on Scarabaeus fossor on the first five
pages of heft 2), to Jablonsky; the rest (i.e., the greater part
of heft 2), to Herbst. Since Scarabaeus caribaeus appeared
on page 300, heft 2, its authorship indeed belongs to Herbst
alone as currently recognized.
Eurysternus aff. hirtellus Dalman, 1824
Biological and Ecological Data  They are considered
copronecrophagous and diurnal beetles, being found
throughout the year (Génier 2009).
63
Records  Alagoas (Ibateguara).
Eurysternus nigrovirens Génier, 2009
Biological and Ecological Data  They are diurnal beetles,
and have generalist feeding habits, being attracted to both
feces and rotten meat (Génier 2009). They are considered
small beetles, measuring between 5.0 and 7.5 mm in length
(Génier 2009; Cupello and Vaz-de-Mello 2016). The geo-
graphical range of the species stretches mostly through the
South American Dry Diagonal, from Paraíba (Brazil) to Salta
(Argentina) (Génier 2009). They are found most frequently in
the rainy season in the state of Paraíba (Hernández and Endres
2011).
Records  Paraíba (Areia, João Pessoa, Mamanguape,
Mataraca), Pernambuco (Abreu e Lima, Caruaru, Igarassu,
Sirinhaém, Triunfo).
Remarks  This species was identified as Eurysternus aff.
hirtellus in Costa et al. (2009), Costa et al. (2013), Endres
et al. (2007), Filgueiras et al. (2015), Hernández and Endres
(2006), Hernández et al. (2014), Salomão et al. (2014), Silva
et al. (2007) and Silva et al. (2010).
Eurysternus parallelus Castelnau, 1840
Biological and Ecological Data  This species is widely dis-
tributed in the southern half of the Atlantic Forest, being pre-
sented in Brazil, Paraguay, and Argentina, and has also been
recorded at least once in northeastern Brazil (Génier 2009;
Cupello and Vaz-de-Mello 2016; Araújo et  al. 2020). It
seems to be a generalist, having been collected using both
excrements and rotten meat and found in pastures, forests,
and restinga (Génier 2009; Araújo et al. 2020).
Records  Pernambuco (Ipojuca).
Remarks  Cupello and Vaz-de-Mello (2016) found a speci-
men in the old collection of the Museu Nacional, Rio de
Janeiro, Brazil (MNRJ), labeled “Sergipe ?” At the time, the
species was not known to occur in northeastern Brazil and the
authors were skeptical as to the accuracy of the record. Now
that Araújo et al. (2020) have confirmed that E. parallelus is
64 L. Iannuzzi et al.

present in Pernambuco, the Sergipe record seems more likely. Onthophagus (Onthophagus) aff. clypeatus Blanchard, 1846
On the other hand, Cupello and Vaz-de-Mello’s (2016) record
of the species from the state of Mato Grosso is erroneous. It
was based on three MNRJ specimens labeled as collected in Biological and Ecological Data  The feeding habits of this
Mato Grosso, “Rio Caraguatá,” in March 1953, by Fritz species are unknown.
Plaumann. The issue is that, in 1953, the state of Mato Grosso
included the area now belonging to the state of Mato Grosso
do Sul, which was dismembered only in 1977. The “Rio Records  Alagoas (Ibateguara).
Caraguatá” locality collected by Plaumann is apparently not
in the current state of Mato Grosso as Cupello & Vaz-de-
Mello assumed, but in the Atlantic Forest of the municipality Remarks  Although Onthophagus aff. clypeatus was listed
of Bataguassu, near the Paraná River, in Mato Grosso do Sul in Filgueiras et al. (2011a, 2015) and Salomão and Iannuzzi
(see the coordinates provided by Martins [1971: 125]), a state (2015), the precise identity of the species is doubtful, as
where E. parallelus is indeed known to occur (Génier 2009). there are no records of O. clypeatus for Brazil. The species is
There is no evidence that the species occurs in Mato Grosso. known solely from Amazonian areas outside the country
Unfortunately, all these four specimens were destroyed in the (Schoolmeesters 2022).
September 2018 fire that consumed the greater part of the
entomological collection of the MNRJ (Mega 2019).
Onthophagus (Onthophagus) aff. hircus Billberg, 1815

ONTHOPHAGINI Streubel, 1846

The Onthophagini are worldwide in distribution, but their Biological and Ecological Data  They have copropha-
diversity is largely centered in the Old World (Scholtz et al. gous feeding habits (Silva et al. 2007) and are important for
2009). Constituting, by far, the largest of the dung beetle dung removal in Brazilian pastures (Tissiani et al. 2017).
tribes, their systematics is still mostly unresolved. Whereas
morphological data seem to indicate that Onthophagini is
monophyletic (Philips 2016), molecular analyses tell other- Records  Paraíba (Areia, Mataraca), Pernambuco (Caruaru,
wise (Breeschoten et al. 2016). Only a single genus is pres- Igarassu, Itamaracá, Cabo de Santo Agostinho – Paiva).
ent natively in the Americas, Onthophagus, and two others
were introduced from Africa by human agency,
Digitonthophagus and Hamonthophagus (Roggero et  al. Onthophagus (Onthophagus) aff. ptox Erichson, 1847
2016; Génier and Moretto 2017).

Onthophagus Latreille, 1802 Biological and Ecological Data  The feeding habits of this
Cosmopolitan and merophyletic (Philips 2016; Breeschoten species are unknown.
et  al. 2016), Onthophagus is a hyperdiverse genus sensu
Wilson (2003), likely the largest in the animal kingdom,
including 2222 described species (Schoolmeesters 2022). Records  Paraíba (João Pessoa).
Only a small fraction of them, however, is present in the New
World, 223 species (Schoolmeesters, personal communica-
tion to MC, 30 April 2022). Recent taxonomic works on Onthophagus (Onthophagus) aff. ranunculus Arrow, 1913
South American species have been published by Rossini
et al. (2018a, b), but much is still to be discovered. For this
reason, all the identifications listed here are tentative. Biological and Ecological Data  Feeding habits are
unknown.
Onthophagus (Onthophagus) aff. bidentatus Mulsant, 1842

Records  Paraíba (Areia, João Pessoa), Pernambuco (Abreu

Biological and Ecological Data  They have copropha- e Lima, Pesqueira – Serra do Ororubá, Triunfo).
gous feeding habits (Harada et al. 2020).

Digitonthophagus Balthasar, 1959

Records  Pernambuco (Igarassu).
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna
Digitonthophagus includes 16 species and is natively distrib-
uted in the Paleotropical region (Génier and Moretto 2017).
One of its species, D. gazella, has been introduced in pas-
tures in several parts of the globe for the biological control of
the horn fly, Haematobia irritans (Linnaeus, 1758). From
there, they have spread to natural environments and become
naturalized (Nascimento et  al. 1990; Kohlmann 1994;
Matavelli and Louzada 2008; Noriega et  al. 2010; Génier
and Moretto 2017).
Digitonthophagus gazella (Fabricius, 1787)
Biological and Ecological Data  They are nocturnal or
crepuscular beetles (Koller et al. 1999) and have generalist
feeding habits, being attracted to both feces and rotten
meat (Silva et al. 2007). It is an introduced species in the
American continent, originating from the African savannas
(Silva and Vidal 2007; Génier and Moretto 2017). It read-
ily establishes itself in environments with little or no arbo-
real vegetation, high temperatures, and short rainy seasons
(Rivera and Wolf 2007).
Records  Paraíba (Areia), Pernambuco (Caruaru, Floresta,
Igarassu, São Caetano), Alagoas (Ibateguara).
PHANAEINI Kolbe, 1905
Most authors agree that the tribe Phanaeini is monophy-
letic (Philips et  al. 2004; Cupello and Vaz-de-Mello
2013b; Tarasov and Génier 2015; Tarasov and Dimitrov
2016; Cupello et  al. 2021), but there are still some
voices arguing that the inclusion of Gromphas Brullé,
1838 and possibly Oruscatus Bates, 1870 renders the
taxon polyphyletic (Edmonds 1972; Gillett and
Toussaint 2020). With Gromphas and Oruscatus
included, the tribe encompasses 11 genera classified in
two subtribes, Phanaeina and Gromphadina (Cupello
and Vaz-de-Mello 2013b, 2015; Cupello et  al. 2021),
distributed only in the New World, from the eastern
United States to northern Argentina (Edmonds 1972,
1994, 2000; Arnaud 2002; Edmonds and Zídek 2004,
2010, 2012; Gillett et  al. 2009; Cupello and Vaz-de-
Mello 2013b; Chamorro et al. 2014; Génier and Arnaud
2016; Valois et al. 2017; Cupello et al. 2021). The num-
ber of species is still contentious due to the varying
definitions applied by different authors to the microtax-
onomic categories, but there are no less than 180.
Phanaeus MacLeay, 1819
Phanaeus is widely distributed from the United States to
Argentina (Edmonds 1994; Edmonds and Zídek 2012). This
65
genus is the one in the tribe that has witnessed the most
intense taxonomic activity in the last decade. Authors dis-
agree on the number of species, ranging from 54 (Edmonds
and Zídek 2012) to 82 (Moctezuma et  al. 2020, 2021;
Moctezuma and Halffter 2021; Schoolmeesters 2022). They
are organized into two subgenera, Notiophanaeus Edmonds,
1994 and Phanaeus s. str., but the monophyly of these sub-
genera, as well as that of the genus as a whole, have been
called into question in the recent literature (Price 2007, 2009;
Gillett and Toussaint 2020).
Phanaeus (Notiophanaeus) splendidulus (Fabricius, 1781)
Biological and Ecological Data  They are diurnal beetles
(Genes et al. 2019) and have generalist feeding habits (Silva
et al. 2012). The species is widely distributed in the Atlantic
Forest, ranging from Pernambuco (Brazil) south to Misiones
(Argentina) (Edmonds 1994; Edmonds and Zídek 2012;
Gillett et al. 2010; Araújo et al. 2020).
Records  Pernambuco (Bonito, Caruaru), Alagoas (Murici).
Coprophanaeus Olsoufieff, 1924
Coprophanaeus is a New World genus and comprises 44 spe-
cies (Edmonds and Zídek 2010; Cupello and Vaz-de-Mello
2014) classified in three subgenera as defined by Edmonds
(1972) and Edmonds and Zídek (2010): Megaphanaeus
Olsoufieff, 1924, Metallophanaeus Olsoufieff, 1924 and
Coprophanaeus s.str. There is little doubt that the genus is para-
phyletic, with Dendropaemon, Megatharsis and likely
Homalotarsus nested within it, and the subgenera
Metallophanaeus and Coprophanaeus s. str. do not appear to be
clades either (Edmonds 1972; Edmonds and Zídek 2010; Gillett
and Toussaint 2020). Megaphanaeus seems to be the only of
these genus-group taxa to be monophyletic (Maldaner et  al.
2020). The species of Coprophanaeus are found from the
extreme southern United States (Arizona and Texas) to
Argentina (Edmonds and Zídek 2010).
Coprophanaeus (Coprophanaeus) acrisius (MacLeay, 1819)
Biological and Ecological Data  They are nocturnal beetles
that have preferably necrophagous habits, but can also be
attracted to dung in small numbers (Gillett et al. 2010; Costa
et al. 2013). The species ranges mainly through the northern
half of the South American Dry Diagonal, from Paraíba
and Maranhão (Brazil) southwestward to Santa Cruz
(Bolivia) (Edmonds and Zídek 2010; Araújo et  al. 2020).
Some records in areas formally covered by the Atlantic
66
Forest on the coast of northeastern Brazil also exist (Edmonds
and Zídek 2010).
Records  Pernambuco (Abreu e Lima, Goiana, Recife  –
UFPE), Alagoas (Ibateguara).
Remarks  Edmonds and Zídek (2010) recorded the species
from “Tejucupapo,” a district in the Pernambuco municipal-
ity of Goiana.
Coprophanaeus (Coprophanaeus) cyanescens (Olsoufieff,
1924)
Biological and Ecological Data  The species is widely dis-
tributed in the South American Dry Diagonal, from Rio
Grande do Norte and Maranhão (Brazil) southwestward to
Catamarca (Argentina) (Edmonds and Zídek 2010). Some
localities in the Atlantic Forest also had the species recorded
for them, such as Linhares (Espírito Santo, Brazil) and the
Iguazu National Park (Misiones, Argentina) (Gillett et  al.
2010; Edmonds and Zídek 2010). These beetles are noctur-
nal and mostly necrophagous, but occasionally also attracted
to dung (Gillett et al. 2010; Harada et al. 2020).
Records  Paraíba (Areia, Mamanguape, João Pessoa),
Pernambuco (Abreu e Lima, Caruaru, Igarassu, Recife  –
Dois Irmãos, Triunfo), Alagoas (Ibateguara).
Remarks  Specimens from northeastern Brazil were identi-
fied as Coprophanaeus jasius (Olivier, 1789) until 2009
(e.g., Pessôa 1934; Filgueiras et al. 2009; Silva et al. 2007).
After the studies of Gillett et  al. (2010) and Edmonds and
Zídek (2010), these records were corrected to Coprophanaeus
cyanescens.
Coprophanaeus (Coprophanaeus) dardanus (MacLeay,
1819)
Biological and Ecological Data  The species is widely dis-
tributed in the Atlantic Forest, ranging from Santa Catarina
northward to Paraíba; from there, it reaches westward the
Caatinga moist forest enclaves of Ceará and in the eastern
half of the Amazon (Edmonds and Zídek 2010; Cupello and
Vaz-de-Mello 2013a; Araújo et  al. 2020). They are mostly
L. Iannuzzi et al.
necrophagous, but can also be attracted to dung (Gillett et al.
2010; Costa et al. 2013; M. Cupello, personal observation at
Itatiaia National Park, between 2010 and 2016). They have
crepuscular habits (Edmonds and Zídek 2010; M. Cupello,
personal observation; contra Harada et al. 2020).
Records  Paraíba (Areia, João Pessoa), Pernambuco (Abreu
e Lima, Bonito, Cabo de Santo Agostinho – Paiva, Igarassu,
Sirinhaém), Alagoas (Ibateguara).
Coprophanaeus (Megaphanaeus) bellicosus (Olivier, 1789)
Biological and Ecological Data  They are nocturnal and
have necrophagous habits (Falqueto et al. 2005; Silva 2011;
M.  Cupello, personal observation at Itatiaia National Park,
between 2010 and 2016). The species ranges mainly through
the central Atlantic Forest, between the Brazilian states of
Bahia and Rio Grande do Sul (Edmonds and Zídek 2010).
More than 450 km to the north of this core range, we find a
relict population living at a “brejo of altitude” in Caruaru, in
the Pernambuco Endemism Center (Silva 2011).
Records  Pernambuco (Caruaru), Alagoas (Ibateguara).
Coprophanaeus (Megaphanaeus) ensifer (Germar, 1821)
Biological and Ecological Data  They have necrophagous
(Costa et  al. 2013) and crepuscular habits (Iannuzzi et  al.
2016). They are large dung beetles, the largest in the
Americas, measuring between 30 and 56 mm in length, and
can be found through most of the Cerrado and in localities in
the Caatinga, Atlantic Forest, and southern Amazon (Gillett
et al. 2010; Edmonds and Zídek 2010; Maldaner et al. 2019).
This is probably the identifiable dung beetle with the oldest
record from Brazil: one of the four scarab species illustrated,
described, and called “taurus volans” by Marcgrave (1648)
in Historia Naturalis Brasiliae  – the second one on page
247 – is clearly Coprophanaeus ensifer (cf. Maldaner et al.
2017). Since the area explored by Marcgrave, the territory
occupied by the Dutch on the coast of northeastern Brazil
during the mid-seventeenth century, was centered in the
region north of the São Francisco, it is even likely that his
pioneering observations were made precisely in our area of
interest, the Pernambuco Endemism Center. Marcgrave’s
illustration would later be used by Linnaeus (1767) along
with others depicting a different, Amazonian scarabaeine
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna
species to describe Scarabaeus lancifer, creating a nomen-
clatural problem only discovered and fixed 259 years later by
Maldaner et al. (2017).
Records  Paraíba (João Pessoa, Mamanguape), Pernambuco
(Abreu e Lima, Igarassu, Recife – Dois Irmãos, Sirinhaém),
Alagoas (Maceió).
Coprophanaeus (Metallophanaeus) pertyi (Olsoufieff, 1924)
Biological and Ecological Data  They are apparently diur-
nal beetles that have necrophagous habits (Gillett et  al.
2010), and are mainly centered in the Caatinga (Pereira and
d’Andretta 1955; Edmonds and Zídek 2010; Gillett et  al.
2010).
Records  Rio Grande do Norte (Canguaretama), Paraíba
(Mamanguape), Pernambuco (Caruaru, Garanhuns, Igarassu,
Itamaracá).
Coprophanaeus (Metallophanaeus) punctatus (Olsoufieff,
1924)
Biological and Ecological Data  They have necrophagous
habits and are known only from Pernambuco and Espírito
Santo (Edmonds and Zídek 2010; Costa et al. 2013; Salomão
and Iannuzzi 2015).
Records  Pernambuco (Abreu e Lima, Igarassu, Sirinhaém).
Dendropaemon Perty, 1830
Dendropaemon is a rare genus endemic to South America
east of the Andes. It comprises 41 species arranged into 12
subgenera (Génier and Arnaud 2016; Cupello and Génier
2017). The habits of the species are still mostly unknown,
but it is likely that at least some of them are inquilines in the
nests of leafcutter ants and perhaps in those of termites as
well (Vaz-de-Mello and Génier 2009; Génier and Arnaud
2016). This putative inquiline lifestyle was hypothesized as
the reason why the Dendropaemon lost the extravagant horns
and other dorsal outgrowths of their ancestors (Cupello et al.
2021). It seems clear that Dendropaemon is closely related to
Megatharsis and likely to Homalotarsus and that they are
nested within Coprophanaeus (Edmonds 1972; Philips et al.
2004; Génier and Arnaud 2016; Gillett and Toussaint 2020).
67
Dendropaemon (Glaphyropaemon) cf. bahianus Harold,
1868
Biological and Ecological Data  Our record is based on a
specimen collected by the first author, in 2003, in the vicini-
ties of Recife’s international airport. This specimen was later
donated to Fernando Z. Vaz-de-Mello and deposited in the
collection under his care, now part of “Seção de Entomologia
da Coleção Zoológica da Universidade Federal de Mato
Grosso,” Cuiabá, Brazil. Unfortunately, we were not able to
recheck the specimen for this work and confirm its species
identity. Since the only species of Dendropaemon known to
be present in one of the states that we are investigating is D.
bahianus (cf. Génier and Arnaud 2016), we think this is the
most likely identity of our specimen. Dendropaemon bahia­
nus, however, is not known to occur in the Atlantic Forest.
The species is distributed in the northern half of the South
American Dry Diagonal and was at least once collected
using a window trap in a “cerradão” fragment (Génier and
Arnaud 2016). North of São Francisco, it is known from a
single female caught in Cajazeiras, a municipality in the
Caatinga of Paraíba (Génier and Arnaud 2016).
Records  Pernambuco (Recife).
Diabroctis Gistel, 1857
Diabroctis is a monophyletic genus endemic to South
America and comprises five species (Valois et al. 2018).
Diabroctis mimas (Linnaeus, 1758)
Biological and Ecological Data  They have coprophagous
habits (Silva et al. 2014) and are widely distributed in South
America, living in a wide variety of habitats (Gillett et  al.
2010; Valois et al. 2018).
Records  Pernambuco (Caruaru, Igarassu, Pombos, Recife –
Aeroporto, Recife – Dois Irmãos), Alagoas (Ibateguara).
Diabroctis pseudomimas Valois et al., 2018
Biological and Ecological Data  Data on feeding habits are
not available. The species is endemic to northeastern Brazil,
occurring in Ceará, Paraíba, and Pernambuco (Valois et al.
2018).
68
Records  Paraíba (Areia, Bayeux, João Pessoa), Pernambuco
(Itambé).
Oxysternon Castelnau, 1840
Oxysternon comprises 11 species distributed exclusively in
the Neotropical region, from Costa Rica to Paraguay
(Edmonds and Zídek 2004). These species are organized
into two subgenera: Myoxisternon Edmonds, 1972 and
Oxysternon s.str. (Edmonds and Zídek 2004). The phyloge-
netic status of the genus is dubious: while morphological
studies have firmly pointed to its monophyly (Edmonds
1972; Edmonds and Zídek 2004; Price 2007), molecular
analyses usually agree on the polyphyly of the taxon (Price
2009; Gillett and Toussaint 2020). What seems to be clear
is that, regardless of the monophyly of the genus, the spe-
cies of Oxysternon are nested within Phanaeus, rendering
the latter paraphyletic (Price 2007, 2009; Gillett and
Toussaint 2020).
Oxysternon (Oxysternon) silenus Castelnau, 1840
Biological and Ecological Data  They are diurnal or cre-
puscular beetles that have mostly coprophagous habits, but
which can also be collected with rotten meat (Edmonds and
Zídek 2004; Pardo-locarno 2007; Ferreira et al. 2020). They
are considered forest specialists (Edmonds and Zídek 2004)
and their populations are apparently organized into three
geographical isolates: one stretching through the rainforests
west of the Andes, from Costa Rica to Ecuador; another cov-
ering the greater part of the Amazon; and still another known
from a single population in the Atlantic Forest of northeast-
ern Brazil (Edmonds and Zídek 2004; Filgueiras et  al.
2011b).
Records  Alagoas (Ibateguara).
Genera incertae sedis in Scarabaeinae (sensu Tarasov &
Dimitrov, 2016)
Canthidium Erichson, 1847
The phylogenetic status of Canthidium is still uncertain, as no
work has so far investigated it. The genus is distributed from
the United States (Texas) to Argentina (Cupello 2018). It
comprises 178 described species (Cupello 2018; Génier and
L. Iannuzzi et al.
Cupello 2018; Santana et al. 2019; Moctezuma et al. 2019),
most of them organized into two subgenera, Neocanthidium
Martínez et  al., 1964 and Canthidium s.str., and the rest
deemed incertae sedis in the genus (see Cupello 2018). The
microtaxonomy of the group is still largely unexplored, and
the identifications that will follow are mostly tentative.
Canthidium (Canthidium) aff. collare Castelnau, 1840
Biological and Ecological Data  The feeding habits are
unknown.
Records  Paraíba (Areia).
Canthidium (Canthidium) humerale (Germar, 1813)
Biological and Ecological Data  They are predominantly
coprophagous (Silva et al. 2007) and occur in northeastern
Brazil (Cupello 2018).
Records  Paraíba (Mamanguape), Pernambuco (Igarassu;
Caruaru).
Canthidium (Canthidium) korschefskyi Balthasar, 1939
Biological and Ecological Data  They have coprophagous
habits and seem to be unique to forest environments (Almeida
and Louzada 2009). The species appears to be endemic to the
Brazilian Atlantic Forest (Cupello 2018).
Records  Alagoas (Ibateguara).
Canthidium (Neocanthidium) manni Arrow, 1913
Biological and Ecological Data  They are diurnal beetles
(Hernández 2007) that have generalist feeding habits, being
attracted to both feces and rotten meat (Salomão and Iannuzzi
2017). The species seems to occur exclusively in Brazil
(Cupello 2018).
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna
Records  Rio Grande do Norte (Natal), Paraíba
(Mamanguape, Mataraca), Pernambuco (Abreu e Lima,
Caruaru).
Canthonella Chapin, 1930
Canthonella comprises 17 species (Ratcliffe and Smith
1999; Ivie and Philips 2008) distributed in the Greater
Antilles (except Jamaica), South America (except Chile),
and the Virgin Islands (Vaz-de-Mello et al. 2011a).
Canthonella aff. barrerai (Halffter & Martinez, 1968)
Biological and Ecological Data  The feeding habits are
unknown.
Records  Paraíba (João Pessoa), Alagoas (Ibateguara).
Canthonella aff. lenkoi (Pereira & Martinez, 1956)
Biological and Ecological Data  The feeding habits are
unknown.
Records  Alagoas (Ibateguara).
Canthonella silphoides (Harold, 1867)
Biological and Ecological Data  They have generalist feed-
ing habits (Costa et al. 2013; Salomão et al. 2014) and are
apparently widely distributed in South America
(Schoolmeesters 2022).
Records  Pernambuco (Abreu e Lima, Sirinhaém), Alagoas
(Ibateguara).
Canthonella sp.
Records  Pernambuco (Igarassu, Recife – Dois Irmãos).
69
Ontherus Erichson, 1847
Ontherus consists of 60 species in three subgenera:
Caelontherus Génier, 1996, Ontherus s.str. and Planontherus
Génier, 1996 (Génier 1996, 1998; González and
Medina 2015). The genus is Neotropical, distributed from
Mexico to Argentina (Génier 1996; Vaz-de-Mello et  al.
2011a).
Ontherus (Ontherus) aphodioides Burmeister, 1874
Biological and Ecological Data  The feeding habits of this
species are still unknown. It seems to be widely distributed in
South America (Génier 1996).
Records  Pernambuco (Igarassu).
Ontherus (Ontherus) appendiculatus (Mannerheim, 1829)
Biological and Ecological Data  They have coprophagous
habits (Vaz-de-Mello et al. 2011b; Correa et al. 2021). It is a
species considered of great importance for Brazilian pas-
tures, due to its wide distribution and biomass, occurring in
pastures and natural fields across the country. It also occurs
in forested areas in northern Amazonia, and is occasionally
found in forests adjacent to pastures, secondary forests,
small forest fragments, and sand dunes (Tissiani et al. 2017).
The species is widely distributed in South America (Génier
1996).
Records  Rio Grande do Norte (Ceará-Mirim, Natal),
Paraíba (João Pessoa), Pernambuco (Triunfo), Alagoas
(Maceió).
Remarks  Génier (1996) recorded the species from
“Independencia,” supposedly in the state of Paraíba, Brazil.
There is no municipality in Paraíba with such a name, but
there is a square in the capital city, João Pessoa, called Praça
da Independência. We assume this is the “Independencia”
that the label of Génier’s specimen refers to.
Ontherus (Ontherus) azteca Harold, 1869
70
Biological and Ecological Data  The species is widely dis-
tributed from western Mexico south to eastern Brazil (Génier
1996). The feeding habits are unknown.
Records  Paraíba (Mamanguape, Mataraca), Pernambuco
(Igarassu, Ipojuca – Maracaípe), Alagoas (Ibateguara).
Ontherus (Ontherus) digitatus Harold, 1868
Biological and Ecological Data  They have coprophagous
habits (Hernández 2007) and are distributed through much of
South America south of the Amazon (Génier 1996;
Hernández 2007).
Records  Pernambuco (Caruaru).
Ontherus (Ontherus) aff. erosus Harold, 1875
Biological and Ecological Data  The feeding habits of this
species are still unknown.
Records  Alagoas (Ibateguara).
Uroxys Westwood, 1842
Uroxys contains 59 described species (Schoolmeesters 2022)
distributed from Mexico to Argentina (Vaz-de-Mello et  al.
2011a). The microtaxonomy of the genus is arguably the
least known among the New World scarabaeines, and the
identifications that follow are necessarily tentative.
Uroxys bahianus Boucomont, 1927
Biological and Ecological Data  The feeding habits of this
species are still unknown.
Records  Paraíba (João Pessoa), Pernambuco (Triunfo).
Uroxys aff. batesi Harold, 1868
L. Iannuzzi et al.
Biological and Ecological Data  The feeding habits of this
species are still unknown.
Records  Alagoas (Ibateguara).
5.5 Discussion
The result of our work lists 89 dung beetles species, and only
two species were not identified with a binomen, namely a
Canthonella and a Trichillum. These two  genera are rela-
tively small, with 17 and 11 known species, respectively, but
both need taxonomic revision. Another 15 species were des-
ignated as “related” (“aff”) to a described species: one in
Canthidium, Dichotomius, Eurysternus, Ontherus and
Uroxys, respectively; two in Canthonella, three in Canthon
and five in Onthophagus. Except for Canthonella, the other
genera are rich in species, ranging from about 60 species
each (Ontherus and Uroxys), to between 133 and 190
(Ateuchus, Canthidium, and Dichotomius), to amazing
2222  species in the hyperdiverse Onthophagus, the largest
genus in the whole animal kingdom. In addition to their
immense diversity, some of these genera are considered
para- or polyphyletic, and most do not have modern identifi-
cation keys to their Brazilian members. These problems
make accurate identifications difficult.
Six of the 19 tribes currently recognized in the subfamily
(Scholtz et  al. 2009; Tarasov and Dimitrov 2016; Tarasov
2017; Davis et al. 2019; Daniel et al. 2020) were identified in
this study. Deltochilini was the most diverse, with six genera
and 29 species. This monophyletic tribe comprises 22 genera
exclusive to the Neotropical and Nearctic regions (Tarasov
and Dimitrov 2016). In this study, the two richest genera of
the tribe, Canthon and Deltochilum, were also the richest and
the third richest in our study, with 16 and 8 species, respec-
tively. Canthon is a merophyletic genus (Medina et al. 2003),
currently with 180 species recognized (Schoolmeesters
2022). Deltochilum, in turn, comprises 114 species, 52 of
which with recorded presence for Brazil (Silva et al. 2015;
González-Alvarado and Vaz-de-Mello, 2021; Schoolmeesters
2022). So far, the monophyly of the genus has not been
tested.
Another genus that has many species in the Northern
Atlantic Forest in Dichotomius, of the tribe Dichotomiini,
with 16 identified species. Dichotomius is indeed one of the
most diverse genera of Scarabaeinae, comprising more than
190 described species distributed throughout the New World,
from forests to savannas, from mountains to arid regions
(Nunes and Vaz-de-Mello 2013, 2019; Valois et al. 2017).
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna
Of the four states in northeastern Brazil covered by the
Atlantic Forest north of the São Francisco River, three have
had some of their local dung beetle communities formally
surveyed: Paraíba, Pernambuco and Alagoas. Most of the
sampled localities are concentrated in the states of
Pernambuco and Paraíba, where they comprise areas of for-
ests, restinga and brejos de altitude  were surveyed.
Pernambuco is the best sampled state, with 27 localities stud-
ied (some of them composed of different fragments), includ-
ing 12 forest regions, 10 Brejos de Altitude and five restinga
regions. This range of habitats sampled within the Atlantic
Forest domain resulted in high species richness (71 species),
as species with distinct specialized  habitat were not over-
looked. Paraíba has eight sampled localities, five of which
are forests, two Brejo de Altitude, and one restinga. In
Alagoas, the studies have focused on the forest fragments in
Ibateguara, Maceió, Murici, Rio Largo and União dos
Palmares. The Rio Grande do Norte state still has ecosys-
tems of deciduous and semideciduous seasonal forests and
restinga (RBMA 2008), but there are no inventories of dung
beetles, only isolated records. It can be observed that the
dung beetle fauna is better known in the states where there
are active research groups working with these beetles. And
even in these states, there are still many unknown areas.
In Alagoas, the studies are concentrated in the region of
Usina Serra Grande, and despite the small geographic range
of inventories, this single forest fragment resulted in 39 spe-
cies. This large fragment has been described as having large
trees (e.g., Lauraceae, Sapotaceae) and medium-sized fru-
givorous vertebrates (e.g., agoutis, paca) (Pimentel and
Tabarelli 2004), which guarantee resources for dung beetles
(Filgueiras et al. 2011a). We also highlight the presence of
some special dung beetles such as Oxysternon silenus across
the Serra Grande landscape. This copronecrophagous dung
beetle species was also collected in the Coimbra Forest and
the presence of this dung beetle in this region corroborates
the biogeographical connection between the Amazonia and
the Atlantic Forest of northeastern Brazil during the Plio-­
Pleistocene (Prance 1982; Filgueiras et al. 2011b; Ledo and
Colli 2017; Cupello et al. 2020). The state of Alagoas, bor-
dered in the south by the São Francisco River, needs further
sampling to clarify the role of this river in differentiating the
biota from its northern and southern banks. That is, to better
characterize the differences and similarities between the
Pernambuco Endemism Center and the rest of the Atlantic
Forest.
Despite a richness of 89 species, this number is certainly
underestimated due to sampling gaps and the taxonomic
deficiencies of some of the largest genera. Unsampled areas,
especially in the states of Rio Grande do Norte, Paraíba, and
Alagoas, include regions of Atlantic Forest with different
71
characteristics from each other and from areas already sam-
pled, indicating that the panorama of knowledge about the
biodiversity of dung beetles north of the Northern Atlantic
Forest is still quite incomplete. Among the Atlantic Forest
vegetation types of this region, the main gaps in information
about dung beetles lay in semideciduous seasonal forest, the
open ombrophilous forest and ecological tension zones, in
pioneer formation areas, as well as in restingas. Thus, spe-
cies hitherto known only from a few localities or vegetation
types may eventually be found in other studies, expanding
their known distributions.
Many of the species listed from our focus area have a
wide distribution, both in type of habitat and in latitudinal
range, with some species having expanded throughout the
Neotropical region or throughout Brazil. In the Atlantic
Forest north of the São Francisco River, the distribution of
these species was not ubiquitous, with certain restrictions as
to the occupied areas, possibly since it is a patchy, highly
fragmented vegetation amid a restrictive matrix, which only
the true habitat generalist species manage to cross. Eleven
species showed wide distribution occurring in the three states
and types of environments systematically surveyed: Ateuchus
semicribratus, Canthidium manni, Canthon terciae, Canthon
virens chalybaeus, Coprophanaeus dardanus, Copro­
phanaeus pertyi, Deltochilum irroratum, Dichotomius
­geminatus, Dichotomius gilleti, Dichotomius nisus, and
Pseudocanthon xanthurus. In contrast, most species were
recorded from only  one or a few localities. Ten species
occurred only in forests in Pernambuco, 12  in forests in
Alagoas, and 2 in those in Paraíba. For the Brejos de Altitude
areas, 11 species were recorded only in this kind of habitat in
Pernambuco and another exclusively in Paraíba, while, for
the restinga areas, only five species were endemic to them,
three in Pernambuco and another two in Paraíba.
The distribution and the number of microendemic dung
beetles in the Brazilian Atlantic Forest are probably associ-
ated with biogeography elements (e.g., vicariant events) and
anthropogenic activities (which function as an environmen-
tal filter against more sensitive species) that have occurred
from the past to the present, all of which can help explain the
degree of singularity of the region.
The northeastern coast of Brazil has been severely frag-
mented at least since the start of the European colonization
of Brazil in the sixteenth century, with conversion of forests
into human-modified landscapes, mainly related to sugar-
cane plantations (Coimbra-Filho and Câmara 1996), result-
ing in a mosaic of (mostly) small fragments amid a
nonforest matrix (such as monoculture, pastures, and urban
areas) (Santos et  al. 2008). Habitat destruction has been
continuous with a current mean annual forest loss rate of
2.14% and increase in isolation of forest patches (Trindade
72
et  al. 2008). Under these anthropogenic pressures, distur-
bance-adapted dung beetle associated with small forest
fragments, pastures, and sugarcane plantations thrive
(Filgueiras et al. 2015).
Despite the hyperfragmented and alarming scenario of the
Northern Atlantic Forest (Lôbo et  al. 2011; de Lima et  al.
2020), this region comprises a wide range of environmental
conditions and heterogeneous landscapes. Due to the limited
extension of the northern Atlantic Forest and its biogeo-
graphical history, we see a relative influence of elements
from neighboring tropical forests, notably from the Amazon
and the Caatinga dry forest (Melo Santos et al. 2007; Thomé
et  al. 2016). Therefore, dung beetle assemblages are rela-
tively speciose and abundant in these Atlantic Forest rem-
nants (e.g., Silva et al. 2010; Filgueiras et al. 2015; Iannuzzi
et al. 2016).
5.6 Conservation Status
Among the 89 species recorded from the Northern Atlantic
Forest, seven have been listed in the IUCN Red List as “Least
Concern”: Canthidium manni, Canthon lituratus, Canthon
mutabilis, Canthon smaragdulus, Coprophanaeus pertyi,
Deltochilum brasiliense and Ontherus azteca. Two other
have been listed as “Data Deficient” – Canthon simulans and
Sylvicanthon obscurus – and just one, Dichotomius schiffleri,
is deemed “Endangered” (IUCN 2021). This latter species
was included in the IUCN list based on the arguments raised
in its original description (Vaz-de-Mello et al. 2001), namely
the high risk of destruction of its preferential habitat, arbo-
real restingas, by real estate expansion. Another five spe-
cies  – Canthon terciae, Dichotomius fernandosilvai, D.
filgueirasi, D. guaribensis and D. iannuzziae – have recently
been described from specimens from the region, with D. fer­
nandosilvai and D. filgueirasi being endemic.
The composition of the dung beetle communities is not
perfectly homogeneous between states and between sampled
vegetation types, and this variation, which still needs better
sampling for proper measurement, must be considered when
Appendices
L. Iannuzzi et al.
talking about conservation. Northern Atlantic Forest com-
prises heterogeneous vegetal physiognomies, which differ
according to the type of soil, topography, climate, and geo-
graphical distribution (Santiago and Barros 2003; Souza
et  al. 2020; Carvalho et  al. 2021). This variation certainly
affects the dung beetle fauna, and many related ecological
and biogeographic questions remain unanswered, such as the
effect of the São Francisco River as a potential dispersal bar-
rier. To gain knowledge as to the size of the local diversity
and its variations and particularities, we need not only more
inventories, but also that the Atlantic Forest vegetation be
preserved.
5.7 Conclusion
Though one could ask why we have concentrated our
efforts on a single branch of the insect tree of life, one that
is not particularly old, nor particularly species-rich, the
scarabaeine dung beetles (Coleoptera, Scarabaeidae,
Scarabaeinae), their ecological importance for the biolog-
ical communities of which they are part is such that the
attention they attract is fully justified. In addition, these
beetles have immense value as a measure of the conserva-
tion importance of an area, since, being closely linked to
vertebrates (mammals) that provide them with the main
food and reproductive resources, they act as a proxy for
those whose inventory process is very difficult and
expensive.
The information on the diversity of the Northern Atlantic
Forest provided by the dung beetles, even if still reduced in
terms of territorial extension, shows its importance and fra-
gility. Even though many areas remain to be sampled in the
Northern Atlantic Forest, the number of endemic species
already discovered there is significant. One can only wonder
how many still await description. But this will only be pos-
sible if the forest remnants remain standing. The Atlantic
Forest region north of the São Francisco River and its dung
beetle fauna need urgent protection.
Appendix 5.1 Species’ occur-
rence data taken from papers
whose dung beetle distribution is
in the Atlantic Forest north of São
Francisco River, Rio Grande do
Norte state, Northeast region of
Brazil
BF Baía Formosa, CG Canguaretama, CM Ceará-Mirim, JA Jardim de Angicos, MC
Macaíba, NT Natal, PN Parnamirim, RN Rio Grande do Norte (unknown locality)
Appendix 5.2 Species’ occur-
rence data taken from papers
whose dung beetle distribution is
in the Atlantic Forest north of São
Francisco River, Paraíba state,
Northeast region of Brazil
AU Ararauna, AE Areia, BX Bayeux, CP Caaporã, JP João Pessoa, MM Mamanguape, MT
Mataraca, Rio Tinto, PB Paraíba (unknown locality)
Tribo
BF CG CM JA MC NT PN RN
Taxon
Ateuchini
Ateuchus (Ateuchus) semicribratus
Genieridium margareteae
Trichillum externepunctatum
Deltochilini
Deltochilum (Aganhyboma) kolbei
Canthon (Peltecanthon) terciae
Malagoniella (Malagoniella) astyanax
Pseudocanthon xanthurus
Dichotomiini
Dichotomius (Selenocopris) geminatus
Phanaeini
Coprophanaeus (Metallophanaeus) pertyi
Genera incertae sedis
Canthidium (Neocanthidium) manni
Ontherus (Ontherus) appendiculatus
Tribo
AU AE BX CP JP MM MT RT PB
Taxon
Ateuchini
Ateuchus volxemi
“Ateuchus” vigilans
Ateuchus (Ateuchus) semicribratus
Trichillum externepunctatum
Deltochilini
Canthon (Canthon) lituratus
Canthon (Canthon) nigripennis
Canthon (Canthon) virens chalybaeus
Canthon (Peltecanthon) terciae
Deltochilum (Aganhyboma) kolbei
Deltochilum (Deltohyboma) irroratum
Deltochilum (Hybomidium) pseudoicarus
Malagoniella (Malagoniella) astyanax
Dichotomiini
Dichotomius (Cephagonus) filgueirasi
Dichotomius (Dichotomius) bos
Dichotomius (Dichotomius) aff. depressicollis
Dichotomius (Selenocopris) geminatus
Dichotomius (Selenocopris) gilletti
Dichotomius (Selenocopris) guaribensis
Dichotomius (Selenocopris) aff. irinus
Dichotomius (Selenocopris) nisus
Continue...
AU AE BX CP JP MM MT RT PB
Dichotomius (Selenocopris) semisquamosus
Eurysternini
Eurysternus caribaeus
Eurysternus nigrovirens
Onthophagini
Digitonthophagus gazela
Onthophagus (Onthophagus) aff. hircus
Onthophagus (Onthophagus) aff. ptox
Onthophagus (Onthophagus) aff. ranunculus
Phanaeini
Coprophanaeus (Coprophanaeus)
cyanescens
Coprophanaeus (Coprophanaeus) dardanus
Coprophanaeus (Megaphanaeus) ensifer
Coprophanaeus (Metallophanaeus) pertyi
Diabroctis pseudomimas
Genera incertae sedis
Canthidium (Canthidium) aff. collare
Canthidium (Canthidium) humerale
Canthidium (Neocanthidium) manni
Canthonella aff. barrerai
Ontherus (Ontherus) appendiculatus
Ontherus (Ontherus) azteca
Uroxys bahianus
 74 L. Iannuzzi et al.

Appendix 5.3  Species’ occurrence data taken from papers whose dung beetle distribution is in the Atlantic Forest north of São Francisco River, Pernambuco
state, Northeast region of Brazil
Tribo
AL AÇ BZ BO BD BU CB CM CR FL GN GO GR IG IP IT IB PD PL PQ PB RC SC SI TM TR VS
Taxon
Ateuchini
“Ateuchus” vigilans
Ateuchus volxemi
Ateuchus (Ateuchus)
semicribratus
Genieridium margareteae
Trichillum externepunctatum
Trichillum sp.
Deltochilini
Anomiopus nigricans
Anomiopus parallelus
Canthon (Canthon) aff.
juvencus
Canthon (Canthon) lituratus
Canthon (Canthon) mutabilis
Canthon (Canthon) nigripennis
Canthon (Canthon) piluliformis
Canthon (Canthon) virens
chalybaeus
Canthon (Canthon) virens
scrutator
Continue…

AL AÇ BZ BO BD BU CB CM CR FL GN GO GR IG IP IT IB PD PL PQ PB RC SC SI TM TR VS
Canthon (Francmonrosia) aff.
carbonarius
Canthon (Glaphyrocanthon)
oliverioi
Canthon (Glaphyrocanthon)
simulans
Canthon (Peltecanthon)
haroldi
Canthon (Peltecanthon) staigi
Canthon (Peltecanthon)
terciae
Canthon (incertae sedis)
histrio
Canthon (incertae sedis)
machadoi
Canthon (incertae sedis) aff.
maldonadoi
Deltochilum (Aganhyboma)
alpercata
Deltochilum (Calhyboma)
verruciferum
Deltochilum (Deltohyboma)
irroratum
Deltochilum (Deltohyboma)
aff. sextuberculatum
Deltochilum (Euhyboma)
brasiliense
Deltochilum (Hybomidium)
pseudoicarus
Continue...
AL Abreu e Lima, AÇ Araçoiaba, BZ Bezerros, BO Bonito, BD Brejo da Madre de Deus, BU Buíque, CB Cabo de Santo Agostinho, CM Camaragibe, CR
Caruaru, FL Floresta, GN Garanhuns, GO Goiana, GR Gravatá, IG Igarassu, IP Ipojuca, IT Itamaracá, IB Itambé, PD Paudalho, PL Paulista, PQ Pesqueira,
PB Pombos, RC Recife, SC São Caetano, SI Sirinhaém, TM Tamandaré, TR Triunfo, VS Vitória de Santo Antão
 5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna 75

Appendix 5.3 (continued)
AL AÇ BZ BO BD BU CB CM CR FL GN GO GR IG IP IT IB PD PL PQ PB RC SC SI TM TR VS
Malagoniella (Malagoniella)
astyanax
Pseudocanthon xanthurus
Sylvicanthon obscurus
Dichotomiini
Dichotomius (Cephagonus)
fernandosilvai
Dichotomius (Cephagonus)
filgueirasi
Dichotomius (Dichotomius)
bos
Dichotomius (Dichotomius) aff.
depressicollis
Dichotomius (Dichotomius)
mormon
Dichotomius (Selenocopris)
carbonarius
Dichotomius (Selenocopris)
geminatus
Dichotomius (Selenocopris)
gilletti
Dichotomius (Selenocopris)
guaribensis
Dichotomius (Selenocopris)
iannuzziae
Dichotomius (Selenocopris)
machadoi
Dichotomius (Selenocopris)
nisus
Continue...

AL AÇ BZ BO BD BU CB CM CR FL GN GO GR IG IP IT IB PD PL PQ PB RC SC SI TM TR VS
Dichotomius (Selenocopris)
punctulatipennis
Dichotomius (Selenocopris)
schiffleri
Dichotomius (Selenocopris)
semisquamosus
Eurysternini
Eurysternus caribaeus
Eurysternus nigrovirens
Eurysternus parallelus
Onthophagini
Digitonthophagus gazella
Onthophagus (Onthophagus)
aff. bidentatus
Onthophagus (Onthophagus)
aff. hircus
Onthophagus (Onthophagus)
aff. ranunculus
Phanaeini
Coprophanaeus
(Coprophanaeus) acrisius
Coprophanaeus
(Coprophanaeus) cyanescens
Coprophanaeus
(Coprophanaeus) dardanus
Coprophanaeus
(Megaphanaeus) bellicosus
Coprophanaeus
(Megaphanaeus) ensifer
Continue...
 76 L. Iannuzzi et al.

Appendix 5.3 (continued)
AL AÇ BZ BO BD BU CB CM CR FL GN GO GR IG IP IT IB PD PL PQ PB RC SC SI TM TR VS
Coprophanaeus
(Metallophanaeus) pertyi
Coprophanaeus
(Metallophanaeus) punctatus
Dendropaemon
(Glaphyropaemon) cf.
bahianus
Diabroctis mimas
Diabroctis pseudomimas
Phanaeus (Notiophanaeus)
splendidulus
Genera incertae sedis
Canthidium (Neocanthidium)
manni
Canthonella silphoides
Canthonella sp.
Canthidium (Canthidium)
humerale
Ontherus (Ontherus)
appendiculatus
Ontherus (Ontherus)
aphodioides
Ontherus (Ontherus) digitatus
Ontherus (Ontherus) azteca
Uroxys bahianus

Appendix 5.4 Species’ occur- Tribo

rence data taken from papers
whose dung beetle distribution is
in the Atlantic Forest north of São
Francisco River, Alagoas state,
Northeast region of Brazil
IB MC MU RL UP AL
Taxon
Ateuchini
Aphengium ibateguara
“Ateuchus” vigilans
Ateuchus volxemi
Ateuchus (Ateuchus) oblongus
Trichillum externepunctatum
Deltochilini
Canthon (Canthon) mutabilis
Canthon (Canthon) nigripennis
Canthon (Canthon) piluliformis
Canthon (Canthon) virens chalybaeus
Canthon (Glaphyrocanthon) oliverioi
Canthon (Goniocanthon) smaragdulus
Canthon (Peltecanthon) haroldi
Canthon (Peltecanthon) staigi
Deltochilum (Aganhyboma) alpercata
Deltochilum (Deltohyboma) calcaratum
Deltochilum (Deltohyboma) irroratum
Deltochilum (Euhyboma) brasiliense
Deltochilum (Hybomidium) pseudoicarus
Malagoniella (Malagoniella) astyanax
Pseudocanthon xanthurus
Sylvicanthon obscurus
Continue...
5  Dung Beetles from the Atlantic Forest North of the São Francisco River: An Overview of a Fragile Fauna 77

Appendix 5.4 (continued)
IB MC MU RL UP AL
Dichotomiini
Dichotomius (Cephagonus) filgueirasi
Dichotomius (Dichotomius) aff. depressicollis
Dichotomius (Dichotomius) mormon
Dichotomius (Selenocopris) gilletti
Dichotomius (Selenocopris) iannuzziae
Dichotomius (Selenocopris) nisus
Eurysternini
Eurysternus calligrammus
Eurysternus aff. hirtellus
Onthophagini
Digitonthophagus gazella
Onthophagus (Onthophagus) aff. clypeatus
Phanaeini
Coprophanaeus (Coprophanaeus) acrisius
Coprophanaeus (Coprophanaeus)
cyanescens
Coprophanaeus (Coprophanaeus) dardanus
Coprophanaeus (Megaphanaeus) bellicosus
Coprophanaeus (Megaphanaeus) ensifer
Diabroctis mimas
Phanaeus (Notiophanaeus) splendidulus
Oxysternon (Oxysternon) silenus
Genera incertae sedis
Canthidium (Canthidium) korschefskyi
Canthonella aff. barrerai
Canthonella aff. lenkoi
Canthonella silphoides
Ontherus (Ontherus) appendiculatus
Ontherus (Ontherus) aff. erosus
Ontherus (Ontherus) azteca
Uroxys aff. batesi
IB Ibateguara, MC Maceió, UM Murici, RL Rio Largo, UP União dos Palmares, AL Alagoas
(unknown locality)

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 The Most Endemic Taxon of an Area
of Endemism: Harvestmen (Opiliones)
Fauna of NAF and Its Contribution
to Biogeography and Conservation
Adriano Medeiros DeSouza
and Marcio Bernardino DaSilva
Abstract
Harvestmen are mostly composed of very endemic and
narrow-ranged species, especially those living in tropical
forests. Hygrophily, cryptic behavior, and low dispersion
capacity are considered the biological causes of this dis-
tributional trait. Thus, Opiliones have been successfully
used as models for biogeography (historic, phylogeogra-
phy, diversity patterns, etc.) and conservation, as they are
very sensitive to habitat changes, in Atlantic Rain Forest.
The area of endemism of Pernambuco, which comprises
most of NAF, has been highly corroborated for harvest-
men, and 35 of its 48 species (from seven families) are
endemic to the area. Moreover, their unique patterns help
to throw light on the specific aspects of the different geo-
graphic and vegetation unities of the area. Finally, 20
recorded species are unknown to science, revealing a
great diversity still to be discovered.
Keywords
Biodiversity · Areas of endemism · Borborema Plateau ·
Atlantic Rainforest
6.1 Introduction
Among the organisms inhabiting the Atlantic Forest, the har-
vestmen, arachnids of the order Opiliones (Fig.  6.1), are
probably the group with the highest rates of endemism
recorded for this biome. These arachnids are very diverse:
A. M. DeSouza (*) · M. B. DaSilva
Universidade Federal da Paraíba, João Pessoa, Paraíba, Brazil
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
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_6
6
more than 1000 species described for Brazil, and more than
600 are endemic to this biome (Pinto-da-Rocha et al. 2005).
Furthermore, these species present restricted distribution
areas, which have already been demonstrated, even in well-­
known species and well-sampled regions, such as
Southeastern Brazil (DaSilva et  al. 2015; Nogueira et  al.
2019a). This high degree of endemism is related to intrinsic
characteristics, such as low dispersal capacity (Pinto-da-­
Rocha et al. 2007), high philopatry, and a deficiency in the
mechanisms preventing water loss compared to other ani-
mals (Santos 2007).
This characteristic motivated several recent studies focus-
ing on the group’s biogeography, allowing the observation of
unique patterns related to the spatial scale in Brazil, mainly in
the Atlantic Forest, but also in other continents (e.g., Sharma
and Giribet 2012; Boyer and Reuter 2012; Schönhofer et al.
2013; Bragagnolo et al. 2015; DaSilva et al. 2015; Vaschetto
et  al. 2015; Hedin and McCormack 2017; Nogueira et  al.
2019a, b; Cruz-López et al. 2021). Also, these studies have
demonstrated the high historical signal related to biogeo-
graphic patterns, as if harvestmen faithfully kept the past geo-
logical events that shaped the Atlantic Forest biodiversity.
Phylogeographic studies have corroborated these patterns and
added time estimates, showing ancient and, in a way, unex-
pected divergences compared to other organisms in the biome
since it seems that populations remained in the same regions
for dozens of million years (Bragagnolo et  al. 2015; Peres
et al. 2017, 2019; Castro-­Pereira et al. 2021).
In this chapter, knowledge about the biogeographic pat-
terns of the Area of Endemism of Pernambuco (PE) will be
explored from the harvestmen’s unique patterns, but with
general inferences for the entire ecosystem. We hope to bring
information that can elucidate the processes that produced
the unique biota of this region. In addition, the information
presented here can be the basis for establishing the most
appropriate strategies for biodiversity conservation in this
85
86 A. M. DeSouza and M. B. DaSilva

Fig. 6.1  Photographs of

living harvestmen species of
PE. (a) Cosmetus biacutus,
Jaqueira – PE. (b) Cynorta
ceara, Caruaru – PE. (c)
Gonyleptidae Gen sp.,
Jaqueira – PE. (d)
Pseudopucrolia discrepans,
Murici – AL. (e) Pickeliana
sp., Murici – AL. (f)
Mitogoniella modesta,
Murici – AL. (e–f by R
Pinto-da-Rocha)

region, which is one of the least protected areas in the entire
Atlantic Forest.
6.2 The Area of Endemism
of Pernambuco (PE)
Several studies have tried to regionalize the Atlantic Forest
biodiversity, focusing on areas of endemism (Müller 1973;
Prance 1982; Amorim and Pires 1996; Silva et  al. 2004;
DaSilva et al. 2015; Lago-Barcia et al. 2020, among others).
Despite some peculiarities, due to the use of different meth-
odologies and taxonomic groups, such studies present a
remarkable distributional congruence among the different
taxa. In general terms, it is possible to recognize four biogeo-
graphic units (or areas of endemism) for the Atlantic Forest
biodiversity: the first, located further south, is related to the
coastal and Araucaria forests; then we have a second area,
related to Serra do Mar (which may have a series of subdivi-
sions depending on the biological group considered); the
third located in Bahia state; and finally, the fourth area,
located to the north of the São Francisco River, referred to as
Area of Endemism of Pernambuco or Pernambuco Center of
Endemism1 (DaSilva et al. 2015 for more details).
The PE extends from the coast of Paraíba to Sergipe and
comprises the coastal plain, low sedimentary plateaus, and
the Borborema plateau. It presents an annual rainfall of up to
2200 mm and is composed of seasonal semideciduous for-
ests or dense and open ombrophilous forests (Tabarelli et al.
2005). PE constitutes one of the least protected areas of the
Atlantic Forest, with under 5% of its territory under protec-
tion (Ribeiro et al. 2009; Nogueira et al. 2019a). In addition,
it has a long history of native vegetation suppression for sug-
arcane monoculture and consequent forest fragmentation,
which began in the sixteenth century (Galindo-Leal and
Here, we prefer to call Area of Endemism of Pernambuco instead of
1 
Pernambuco Center of Endemism, even considering that the second
name is better known and used in literature. We do it because Center of
Endemism is a name without a well-established concept. It may refer to
an area of endemism or various other related concepts, such as a region
with great richness of endemic species, for example. On the other hand,
“area of endemism” has been conceptualized in many works and brings
the meaning that we want to focus: an area with several endemic species
with high congruence in their distributions.
6  The Most Endemic Taxon of an Area of Endemism: Harvestmen (Opiliones) Fauna of NAF and Its Contribution to Biogeography…
Câmara 2003). Today, it presents forest fragments amid an
inhospitable matrix for most organisms (Ribeiro et al. 2009).
In addition to the coastal and slopes forests, the PE is also
composed of Brejos de Altitude formations. These forma-
tions are located on top of mountain ranges that compose the
Borborema Plateau with elevations between 500 and 1200 m.
They present fertile soils rich in organic matter, which, asso-
ciated with the rainfall regime relief (with orographic rains,
see Andrade-Lima 1982), guarantees the permanence of a
Montane Semideciduous Seasonal Forest (Veloso et al. 1991;
Tabarelli and Santos 2004; Tabarelli et al. 2005; Rodal and
Sales 2008). The Brejos de Altitude are exceptional areas
compared to their surroundings, being “islands” of humid
vegetation in the middle of the Caatinga Biome, a typical
Seasonally Dry Tropical Forest (sensu Pennington et  al.
2000).
The PE fauna is composed of many endemic species.
Several mammal species (Mendes Pontes et al. 2013), birds
(Silva et al. 2002), and amphibians (Cruz et al. 1999) that do
not exist anywhere else on the planet have already been
described. In addition to vertebrates, endemic plants (Prance
1982), orchid bees (Nemésio and Santos 2014), onychopho-
rans (Costa et al. 2018), and arachnids such as harvestmen
(e.g., Saraiva and DaSilva 2016) have also been described
for this region – probably, harvestmen have the higher num-
ber of narrowly endemic species, which is discussed below.
This very restrict distribution makes those species particu-
larly vulnerable to the risk of extinction due to pressures
from human activities, which causes fragmentation and habi-
tat losses (Ribeiro et al. 2011).
Several researchers have already tried to understand the
diversity and endemism patterns in the PE.  This quest to
describe and understand endemism patterns is crucial, as
areas of endemism constitute the basic unit of biogeographic
studies (Nelson and Platnick 1981; Platnick 1991) and repre-
sent regions with a unique biota, which share a common evo-
lutionary history (Cracraft 1985; DaSilva et  al. 2015).
Perhaps one of the first researchers to investigate endemism
patterns in the Neotropics was German Paul Müller, who,
after a series of expeditions to South America and studying
the Neotropics vertebrate fauna, found that this biota was
organized in “Centers of Dispersion” (Müller 1972). One of
these centers corresponds to the Atlantic Forest, which in
turn had a series of subcenters, or “districts,” giving this
region further north in the Atlantic Forest the name
“Pernambuco district” (Müller 1973).
Brown Jr (1977a, b, 1982a) delimited a series of evolu-
tionary and endemism centers for Ithomiinae butterflies
(Nymphalidae), and one of them is spatially related to the
“Pernambuco District” proposed by Müller (1973). A similar
endemism pattern has already been seen by analyzing the
woody plants’ distributions when Prance (1982) identified
26 regions called Centers of Endemism in the Amazon Forest
87
and the Atlantic Forest. In the latter, the Pernambuco Center
of Endemism was recognized with several endemic species,
such as Couepia pernambucensis Prance, 1972
(Chrysobalanaceae). In the same way as Brown Jr (Brown Jr
1977a, b, 1982a, b), the Centers of Endemism proposed by
Prance (1982) were associated with the Pleistocene refuges
due to the Quaternary climatic fluctuations (Haffer 1969).
When analyzing the phylogenetic and biogeographic pat-
terns of flies (Ditomyidae and Rhychosciara) and monkeys
(Platyrrhini), Amorim and Pires (1996) found an endemic
area further north of the Atlantic Forest (called by the authors
as “NEBr”). This area presented a certain incongruity with
the PE already described by other authors (Müller 1973;
Brown Jr 1977a, b, 1982a; Prance 1982), as its limits cover
the Atlantic Forest area and also includes Caatinga Dry
Forest and Cerrado savannah areas in its westernmost
limits.
Another important group of organisms already used to
propose areas of endemism in the Neotropics are birds.
Stattersfield et  al. (1998) indicated five areas of endemism
for birds in the Atlantic Forest, the northernmost area being
called “The Atlantic slope of Alagoas and Pernambuco,”
with limits coinciding with other proposals previously seen.
Silva et al. (2004) defined four areas of endemism, in which
the PE was identified, diagnosed by several endemic species,
as Tangara fastuosa (Lesson, 1831).
Costa et  al. (2000) analyzed primates, marsupials, and
rodents’ distributions in the Atlantic Forest and, through a
Parsimony Analysis of Endemism (PAE), detected three
areas of endemism: Paulista, “SE coast,” and Pernambuco,
which was again corroborated. Silva and Casteleti (2003)
analyzed distribution data of birds, primates and butterflies,
and recognized six areas of endemism, again corroborating
the PE. Similarly to Silva and Casteleti (2003), an approach
with more than one taxa was performed in the Neotropics by
Sigrist and Carvalho (2008), using the PAE with data from
several arthropods, plants, and vertebrates. Three areas of
endemism in the Atlantic Forest were detected: “Southern
Atlantic Forest,” “Coastal Bahia,” and “Pernambuco.”
Most of the studies cited above were mainly based on ver-
tebrate fauna patterns of distributions. For a long time, inver-
tebrates were neglected, being little used or included in
multitaxa studies (e.g., Amorim and Pires 1996; Silva and
Casteleti 2003; Sigrist and Carvalho 2008). Studies with
invertebrates are extremely important since these animals
constitute a large part of forest biomass, being crucial for the
health and maintenance of these ecosystems (Wilson 1987;
Ewers et  al. 2015). In addition, studies with invertebrates
may elucidate questions that are not always addressed with
other groups that have broader distributions. Only more
recently, and especially in the last decade, the Atlantic Forest
invertebrates have been gaining more attention from
researchers.
88
One group that has aroused the greatest interest in recent
years was the arthropods. Ferrari et al. (2010), for example,
used distribution data from more than 200 species of pen-
tatomid stink bugs to delimit 21 areas of endemism, while
Hoffmeister and Ferrari (2016) based their study on 800 spe-
cies of several arthropods taxa with data covering the entire
Neotropics, resulting in 29 areas of endemism, respectively.
Although some areas found by the authors relate to the limits
of the Atlantic Forest, none of them is located in NAF or is
congruent to PE.
As already mentioned here, Opiliones is one of the groups
with the highest endemism rates in the Atlantic Forest (Pinto-­
da-­Rocha et al. 2005). An analysis involving a series of crite-
ria conducted by DaSilva et al. (2015) showed an endemism
pattern that corroborates previous studies with other groups,
but it also diverges in several aspects. In this study, 12 areas
of endemism were proposed, two of which (Bahia and
Fig. 6.2  Area of endemism of Pernambuco (PE) with all known records of harvestmen on a topographic map
A. M. DeSouza and M. B. DaSilva
Pernambuco; Figs.  6.2 and 6.3) are broadly supported by
previous studies (e.g., Kinzey 1982; Prance 1982; Costa
et al. 2000; Silva et al. 2004; Sigrist and Carvalho 2008). The
other areas, located to the south, constitute an endemism pat-
tern much more refined than that described in other studies,
probably due to the already-mentioned intrinsic characteris-
tics of the group that make them very poor dispersers.
Oliveira et al. (2015) investigated the endemism patterns
of spiders throughout Brazil. In this study, the authors recog-
nized four areas of endemism for the Atlantic Forest: “South,”
“Serra do Mar,” “Bahia,” and “Northeast,” the latter further
north. Thus, this proposal supports the hypothesis that this
northern portion of the Atlantic Forest constitutes an endemic
biota of this region. The difference between the area limits
reflects the interaction of several factors, including data qual-
ity (Ferrari et  al. 2010; Hoffmeister and Ferrari 2016), the
method to be used, and the parameters of the analyses defined
6  The Most Endemic Taxon of an Area of Endemism: Harvestmen (Opiliones) Fauna of NAF and Its Contribution to Biogeography… 89

Fig. 6.3  Area of endemism

of Pernambuco (PE) and two
other adjacent areas: Bahia
(BA) and Brejos Cearenses
(BCE), according to DaSilva
et al. (2015) and DaSilva
et al. (2016a), and main
regions and published times
of divergence between their
fauna (red lines) on a type of
vegetation map (Dark
green = humid forests, light
green = seasonal forests, neon
green = savannahs,
beige = Caatinga Dry Forest).
Solid black lines are the
Congruence Core and
hatching black lines are the
Maximum Region of
Endemism of the areas (see
text). Hatching area is the
Sergipe state (see text)

a priori (DaSilva et al. 2015; Oliveira et al. 2015; Hoffmeister
and Ferrari 2016).
Garrafoni et  al. (2017) delimited five areas of ende-
mism for the Atlantic Forest by analyzing the orchid bees’
(Euglossini) distribution, but did not delimit PE, finding a
“Pernambuco and coastal Bahia component,” including
regions that correspond to the Caatinga Dry Forest or tran-
sition areas. Lago-Barcia et  al. (2020) analyzed planari-
ans’ (Platyhelminthes, Tricladida) distribution and found
nine areas of endemism, with some congruency with what
was observed by DaSilva et al. (2015) for harvestmen, but
did not included any data from PE, where the group is
poorly known.
Thus, many different proposals for areas of endemism
have already been hypothesized for the Atlantic Forest, with
limits and areas varying widely between studies, but with a
general congruence between them. As mentioned before, the
proposed areas of endemism require caution in their interpre-
tation. Knowledge gaps (Ferrari et al. 2010; Hoffmeister and
Ferrari 2016), among other factors, can directly interfere
with the results obtained (DaSilva et al. 2015; Oliveira et al.
2015; Hoffmeister and Ferrari 2016), requiring a posteriori
interpretation of these results (DaSilva et  al. 2015).
Furthermore, organisms that respond to more refined scales
can help to elucidate some patterns (DaSilva et  al. 2015;
Lago-Barcia et al. 2020).
90 A. M. DeSouza and M. B. DaSilva

6.3 Harvestmen Allowed Detailing PE onomic knowledge gap (Mendes 2011; Saraiva and DaSilva
Patterns 2016; Araújo-da-Silva and DaSilva in prep.; Saraiva and
DaSilva in prep.; Alves and DaSilva in prep.) and the advance
Due to several intrinsic characteristics of harvestmen already of studies focusing on the diversity patterns at the commu-
mentioned above, combined with the reduction of the taxo- nity level (Nogueira et  al. 2019a). Thus, the knowledge of
nomic gap of the group, thanks to recent systematic reviews this region’s harvestmen fauna has greatly increased, improv-
(Pinto-da-Rocha 2002; Tourinho-Davis 2004; DaSilva and ing our understanding of local endemism patterns.
Gnaspini 2009; Yamaguti and Pinto-da-Rocha 2009; Pinto-­ As mentioned before, the variation in PE limits depends
da-­Rocha and Bragagnolo 2010; DaSilva and Pinto-da-­ on several factors. However, it is possible to notice a spatial
Rocha 2010; Mendes 2011; Kury and García 2016; Carvalho congruence embracing the coastal region from the Sergipe
and Kury 2018; Ázara et al. 2020; Castro-Pereira et al. 2021), state to Paraíba, which is corroborated by the harvestmen
these arachnids started to be used in several studies in the distribution (DaSilva et al. 2015, 2016a; Figure 1). The inter-
Atlantic Forest, proving that such organisms are good mod- pretation of the endemism patterns from different organisms
els for studies in biogeography. One of the first observations requires caution. As demonstrated by DaSilva et al. (2015),
regarding Atlantic Forest harvestmen was its high degree of species can present different distribution patterns, with very
endemism: over 95% of the species occurring in this biome few cases of total congruence between species. Thus, DaSilva
do not exist in any other part of the world (Pinto-da-Rocha et al. (2015) recognized three endemism levels: endemic spe-
et  al. 2005), with some species presenting a distribution cies presenting a restricted and congruent distribution, gen-
restricted to just a few square kilometers. erating a Congruence Core (CC); endemic species with
The great harvestmen diversity in the Atlantic Forest, greater distribution area, called Maximum Region of
which can reach over 60 species in a single locality depend- Endemism (MRE); and widespread species occurring in at
ing on the considered region (Bragagnolo and Pinto-da-­ least two areas of endemism.
Rocha 2003; Pinto-da-Rocha et al. 2005), is associated with PE’s harvestmen fauna embraces 48 species grouped in
several factors. Besides the group’s natural history character- seven families (Table 6.1 and Fig. 6.2). Among these spe-
istics (low dispersion capacity, high level of dependence on cies, 10 can be considered widely distributed since they also
humid environments), the history of the Atlantic Forest itself occur in Caatinga Dry Forest, in the Bahia endemism area,
(Pinto-da-Rocha et  al. 2005) also shaped the harvestmen and in the Brejos de Altitude located in Ceará, Pernambuco,
fauna with the emergence and disappearance of geographic and Paraíba (Brejos Cearenses endemism area, DaSilva
barriers (DaSilva et al. 2016b), isolating populations in some et al. 2016a). All other 38 species are endemic in PE, and
moments and reconnecting them in others, thus promoting most (N = 26) are congruent and restricted to CC (Table 6.1).
the emergence of new species. DaSilva et al. (2015) interpreted MRE as possible under-­
Initial propositions for delimiting areas of endemism with sampled regions, or presenting real biogeographic patterns.
harvestmen from the Atlantic Forest (Pinto-da-Rocha 2002; These would be peripheral regions (where most endemic
Pinto-da-Rocha et al. 2005) showed that the observed ende- species could not live in the past or the present) or transition
mism patterns for these arachnids are different from other regions between areas of endemism. We can hypothesize that
propositions already discussed for other organisms. The har- this division has a well-defined biogeographical meaning for
vestmen showed more restricted distribution than any other PE, which presents a well-delimited area due to the vegeta-
organism analyzed so far. This observed pattern is robust tion. Its CC is composed of slopes and mountainous forests
since it is still recovered even with the inclusion of more and eastern Brejos, i.e., the humid portion, while MRE is
taxa, applying different methodological approaches, and composed of coastal forests on plains and low plateaus, to
using more refined criteria than those used before (DaSilva the north and south, and Brejos further inland, precisely in
et al. 2015, 2016a). regions of semideciduous forests and transition to Caatinga
Initial propositions regarding harvestmen historical rela- Dry Forest and other coastal ecosystems (Figs. 6.2 and 6.3).
tionships were restricted to the South and Southeast regions, MRE would not be adequate for most of the harvestmen
as harvestmen data from the Northern Atlantic Forest was endemic species in current conditions. On the other hand,
very scarce (Pinto-da-Rocha 2002; Pinto-da-Rocha et  al. during the driest periods of the Neogene climate fluctuations,
2005). This region had a significant knowledge gap, with these conditions would be less suitable, reducing the area of
several species recorded only for their type locality, making endemism to the slope and Brejos regions of the east, which
several biogeographical inferences unfeasible. However, this would determine the limits of the CC.
scenario has changed in the last 10 years, due to a collecting By delimiting the harvestmen area of endemism based on
effort carried out by the authors’ research team, as well as objective criteria (DaSilva et al. 2016a), we could determine
from other researchers. This allowed the decrease in the tax- its extension to the interior since Brejos de Altitude occur far
6  The Most Endemic Taxon of an Area of Endemism: Harvestmen (Opiliones) Fauna of NAF and Its Contribution to Biogeography… 91

Table 6.1  List of species and morphospecies of harvestmen in PE area of endemism, classified in endemic (CC or MRE, see text for details) for
the AE or widespread, i.e., occurring in other AEs and ecosystems
Taxa Endemism classification Occurrence of more related taxa or range of widespread species
Laniatores
 Cosmetidae
 Acantholibitia pluriarcuata Widespread Caatinga Dry Forest, BCE, PE
 Cosmetus biacutus Endemic (CC) ?
 Cynorta ceara Endemic (MRE) ?
 Cynorta unciscripta Widespread Caatinga Dry Forest, Amazonia, BCE, PE
 Gryne leprosa Widespread Caatinga Dry Forest, BCE, Cerrado savannah, PE
 Escadabiidae
 Escadabius schubarti Endemic (CC) ?
 Escadabius spinicoxa Endemic (CC)
 Escadabius ventricalcaratus Endemic (CC)
 Escadabius sp. Endemic (CC)
 Recifesius pernambucanus Endemic (CC) ?
 Gonyleptidae
 Bebedoura rugosa Endemic (CC) ?
 Gen. sp. Endemic (CC) (BA, SE, PE)1
 Gen.2 sp. Endemic (CC) ?
 Eusarcus dandara Endemic (CC) (PE (SE, BA, southern AF))2
 Mitogoniella modesta Widespread – BA, PE (PE/BA, southern AF)3
 Pseudopucrolia discrepans Widespread – BA, BCE, PE (BA, PE, BCE)4
 Pseudopucrolia incerta Endemic (CC)
 Pseudopucrolia sp. Endemic (CC)
 Kimulidae
 Tegipiolus pachypus Endemic (RME) (Cerrado savannah cave, PE)5
 Tegipiolus sp. Endemic (CC)
 Stygnidae
 Gaibulus schubarti Widespread – BA, PE Repeated (BA, PE)6
 Gaibulus sp1 Endemic (MRE)
 Gaibulus sp2 Endemic (MRE)
 Gaibulus sp3 Endemic (CC)
 Gaibulus sp4 Endemic (CC)
 Gaibulus sp5 Endemic (CC)
 Gaibulus sp6 Endemic (CC)
 Iguarassua schubarti Endemic (MRE)
 Iguarassua sp1 Endemic (CC)
 Iguarassua sp2 Endemic (MRE)
 Iguarassua sp3 Endemic (CC)
 Iguarassua sp4 Endemic (CC)
 Iguarassua sp5 Endemic (CC)
 Kaapora minutissimus Endemic (CC)
 Gen.3 sp Endemic (MRE) ?
 Obidosius evelinae Widespread Caatinga Dry Forest, BCE, Cerrado savannah, Amazonia, PE
 Obidosius mendopictus Widespread BA, PE
 Pickeliana pickeli Endemic (MRE) (BA, PE)7
 Pickeliana sp1 Endemic (CC)
 Pickeliana sp2 Endemic (CC)
 Stygnus polyacanthus Widespread Caatinga Dry Forest, BCE, PE
 Zalmoxidae
 Garanhunsa pectanalis Endemic (CC) ?
 “Minuides” rudicoxa Endemic (CC) ?
 Pirassunungoleptes analis Endemic (MRE) (PE (Cerrado savannah, BA))8
(continued)
92 A. M. DeSouza and M. B. DaSilva

Table 6.1 (continued)
Taxa Endemism classification Occurrence of more related taxa or range of widespread species
Eupnoi
 Sclerosomatidae
 Abaetetuba sp. ? BA, southern AF9
 Geaya sp. ? ?
 Munequita sp. Widespread BCE, PE
 Pectenobunus sp. ? ?
Other AEs and ecosystems are shown as the occurrence of more related taxa of endemic species or the range of widespread species (phylogenetic
information is shown in parentheses and referenced). Abbreviations: Areas of endemism of PE Pernambuco, BA Bahia, BCE Brejos Cearenses, SE
Sergipe. AF Atlantic Rain Forest, CC Congruence Core, MRE Maximum Region of Endemism. Authors of the species are in Appendix
1
pers. obs., 2Saraiva and DaSilva (2016), 3DaSilva and Gnaspini (2009) and Ázara et al. (2013), 4DeSouza and DaSilva (in prep.), 5Pérez-González
et al. (2017), 6Saraiva and DaSilva (in prep.), 7DeSouza and DaSilva (in prep.), 8Silvino and DaSilva. (in prep.), 9Tourinho-Davis (2004)

to the west, as far as the Ceará state. Therefore, the delimita-
tion of another area of endemism, Brejos Cearenses, allowed
observing that the western Brejos in Pernambuco and Paraíba
states present endemic species with clear separation from the
PE (Fig.  6.3). Such biogeographic pattern was already
observed in other studies (Carnaval 2002; Carnaval and
Bates 2007; Rodal and Sales 2008; Castro-Pereira et al.
2021; Foerster et  al. 2019). The southern limits of PE are
also under discussion, with most of the studies indicating the
São Francisco River as a barrier (Cabanne et  al. 2008;
Carnaval et al. 2009; Batalha-Filho et al. 2013), while others
indicate the role of the Todos os Santos Bay (Pellegrino et al.
2005), an ancient and large sedimentary basin related to the
opening of the Atlantic Ocean (~100 mya). The entire region
between the two geographic landmarks, mainly in the
Sergipe state, can be considered as an ecotone (i.e., a transi-
tional ecosystem), with great influence from the Cerrado and
vegetation of marine influence (IBGE 1985), therefore being
the division between the two forested areas of endemism.
This region can even be delimited as a separate area of ende-
mism for harvestmen as its fauna becomes better known
(e.g., Saraiva and DaSilva 2016; see Table 1 and Figure 3).
6.4 Diversity Patterns of Harvestmen
in PE
The PE harvestmen fauna is also distinct at the community
level. Nogueira et  al. (2019a) found a drastic turnover and
great species dissimilarity between Bahia and Pernambuco
areas of endemism by investigating harvestmen alpha and
beta diversity at the Atlantic Forest. They also found a spe-
cies richness smaller than what is recorded for other areas of
endemism at the south of the biome. Those results reinforce
the hypothesis that the northern region shares a common
evolutionary history. However, in contrast to the lower spe-
cies richness, PE presents a greater phylogenetic diversity
and respective turnover than expected for Atlantic Forest
harvestmen (Nogueira et al. 2019b), suggesting that histori-
cal factors likely influenced this region’s biota together with
current ecological factors such as climate.
Unlike other areas of endemism located in the south of the
Atlantic Forest, the PE comprises harvestmen from families
more diverse in the Amazon Forest, such as Cosmetidae,
Stygnidae, Zalmoxidae, and Kimulidae (Nogueira et  al.
2019b; Table 1). This pattern is not surprising since the rela-
tionship between the NAF with the Amazon Forest is widely
supported by the literature, for several biological groups
(Andrade-Lima 1982; Prance 1982; Tabarelli and Santos
2004; Tabarelli et al. 2005; Santos et al. 2007; Batalha-Filho
et al. 2013; Prates et al. 2016; DalVechio et al. 2018; Silveira
et al. 2019).
The harvestmen diversity patterns in the PE have also been
investigated, comparing localities of eastern slopes, Brejos,
coastal, and low plateau localities (Lorenzo 2015; Peres et al.
in prep.; Figure  4). Nine localities were sampled with stan-
dardized surveys indicating 12–15 species in eastern moun-
tains’ slopes and 2–3 in the northernmost coastal portion of the
area of endemism (Nogueira et  al. 2019a; Table  2).
Furthermore, additional records were summed up totalizing
11 well-sampled localities (Table 6.2). The localities with the
highest harvestmen richness are Mata do Coimbra, Ibateguara –
AL, with 20 species, Murici  – AL and RPPN Frei Caneca,
Jaqueira – PE, 18 species and Serra dos Cavalos, Caruaru –
PE, 17 species, all of them on slopes and tops of mountains,
reducing to 11 species in Usina São José, Igarassu  – PE, a
northern low plateau, and even to 2 species further north.
In Fig.  6.4, four variables compiled from Wordclim
(2022), altitude, annual mean temperature, annual precip-
itation, and precipitation seasonality, were overlapped
with the 11 well-sampled localities and their observed
richness. Figure  6.4 and Table  6.2 illustrate that milder,
rainy, wetter, less seasonal, and higher altitude localities
have higher species richness (an analytical and detailed
approach are presented in Lorenzo 2015 and Peres et al. in
prep.). Also, the eastern slopes and Brejos have greater
similarity compared to coastal and low plateau ones
(Lorenzo 2015).
Table 6.2  Localities where standardized survey of harvestmen was carried out with sampled richness (Lorenzo 2015; Nogueira et al. 2019a) and total richness recorded
Location in the area of Species # in Total species #
State Municipality Locality Coordinates Geographic unity Altitude (m) endemism PE standardized survey recorded
AL Ibateguara Mata do Coimbra, Usina Serra 8.99° S, 35.87° W Mountain slope 500 CC 16 20
Grande
AL Murici Estação Ecológica Murici 9.24° S, 35.84° W Mountain slope 400 CC 17 18
PE Jaqueira Usina Frei Caneca 8.72° S, 35.84° W Mountain slope 650 CC – 18
PE Caruaru Parque Municipal João 8.36° S, 36.03° W Brejos enclaves 870 CC – 17
Vasconcelos Sobrinho, Serra dos
Cavalos
PE Timbaúba Engenho Água Azul 7.609° S, 35.378° Mountain slope 340 CC 9 12
W
PE Igarassu Usina São José 7.83° S, 35.00° W Coastal plateau 80 MRE 9 11
PE Tamandaré Reserva Biológica Saltinho 8.73° S, 35.18° W Coastal plateau 70 MRE 7 8
PB João Pessoa Jardim Botânico Benjamin 7.144° S, 34.860° Coastal plain 30 MRE 5 5
Maranhão W
PB Mamanguape Reserva Biológica Guaribas 6.73° S, 35.13° W Coastal plateau 150 MRE 3 3
PB Cabedelo Floresta Nacional da Restinga 7.06° S, 34.85° W Coastal plain 25 MRE 3 3
de Cabedelo
PB Sapé Reserva Particular Pacatuba 7.04° S, 35.15° W Coastal plateau 120 MRE 2 2
AL Alagoas, PE Pernambuco, and PB Paraíba states. CC Congruence Core and MRE Maximum Region of Endemism of the area of endemism
6  The Most Endemic Taxon of an Area of Endemism: Harvestmen (Opiliones) Fauna of NAF and Its Contribution to Biogeography…
93
94 A. M. DeSouza and M. B. DaSilva

Fig. 6.4  Area of endemism of Pernambuco (PE) with 11 localities (b) annual mean temperature, (c) annual precipitation,. (d) precipitation
where the observed richness of harvestmen species (numbers) were seasonality. Red and green stars are the localities more and less diverse,
showed on geoclimatic variables maps (Wordclim 2022): (a) altitude, respectively (Table 6.2)
6  The Most Endemic Taxon of an Area of Endemism: Harvestmen (Opiliones) Fauna of NAF and Its Contribution to Biogeography…
Those patterns are similar to that found at the PE area of
endemism delimitation, demonstrating that ancient historical
causes and recent ecological causes are directly related and
determined from speciation to current community composi-
tion. The eastern mountains’ slopes and Brejos are more
stable over geologic time and currently have more suitable
conditions for the community, such as higher humidity and
more distributed rainfall throughout the year (e.g., Lorenzo
2015; Peres et al. in prep.).
However, many more collections are still needed to have
a broader scenario of the harvestmen diversity in PE, as this
fauna is known anecdotally for most localities. Twenty col-
lected species still need to be described, and eight have only
one occurrence record, drawing attention to the lack of
knowledge regarding the group’s diversity in PE and the cau-
tion that must be taken to infer biogeographic and diversity
patterns based on these species with a single record and
likely to be rare.
6.5 Phylogenetics and Times
of Divergence – History and Origins
of the Area of the Endemism
DaSilva et al. (2016b) showed the historical biogeographic
relationships of PE with the area of endemism of Bahia, with
a Cladistic Biogeography approach. However, that study
could not investigate other possible relationships with west-
ern Brejos Cearenses or the Amazon. Phylogenetic relation-
ships between PE endemic species and the distribution of
widespread species occurring in PE can be seen in Table 6.1.
It is important to highlight that there is not enough phyloge-
netic information available for most of the species. These
patterns show a possible complex history of reticulate rela-
tionships between PE and other forest areas at different peri-
ods (Batalha-Filho et  al. 2013; DaSilva et  al. 2016a, b;
Carnaval et al. 2009; Silveira et al. 2019).
Phylogenetic and phylogeographic studies with molecu-
lar data from harvestmen also demonstrate the Atlantic
Forest evolutionary history. For example, Peres et al. (2017)
found divergences between populations of Acutisoma lon-
gipes Roewer, 1913 occurring in Southeastern Atlantic
Forest, corroborating the hypothesis that past
­geomorphological events, such as the uplifting of the moun-
tain ranges and origin and the maintenance of the basins of
the great rivers in the Atlantic Forest region had a great influ-
ence on the harvestmen species. Studies with harvestmen in
this regard have shown that events occurring during the
Paleogene-Neogene are probably among the drivers of lin-
eage divergences in these organisms (Bragagnolo et al. 2015;
Peres et  al. 2017, 2019; Castro-Pereira et  al. 2021). The
divergence times of the species indicated by these works are
older than expected compared to most organisms in the same
95
areas, even in the case of highly endemic populations (see
below for NAF). The most recent harvestmen species have
divergences estimated between 5.3 and 20 mya, before
Pleistocene, a period considered important for the diversifi-
cation of the Atlantic Forest biota (e.g., Carnaval et al. 2009;
do Amaral et al. 2016; Mascarenhas et al. 2019; Nascimento
et al. 2021).
Studies in preparation (DeSouza et al., Peres et al.) with
the harvestmen genera Pseudopucrolia, Pickeliana, and
Cynorta corroborate the patterns related to area of endemism
delimitation, with divergences with Bahia estimated in
15–80  mya. Yet, PE internal divergences corroborate a
greater genetic diversity on mountain slopes and eastern
Brejos with ancient divergences with other regions to the
north and inland (20–30 mya). Thus, the CC of the area of
endemism, currently wetter and historically more stable PE
region, is corroborated by different data sources, such as the
distribution of endemic species, the diversity patterns and
molecular data of harvestmen.
In this sense, the evolutionary history of the PE and its
endemism can be revealed by the harvestmen phylogeny
compared to evidence from other taxa. The limits of the area
of endemism seem to have been defined by the surrounding
forest’s contraction during drier past periods, which was
broad and recent in the west and narrower and less drastic in
the south. The connections between PE and other forested
areas, mainly to the west, could have been stronger and even
continuous a few tens of millions of years ago, in the Miocene
(e.g., Silveira et  al. 2019). Such connections are demon-
strated by the biota relationships with Brejos Cearenses and
the Amazon. Many works have addressed those connections
of humid forests between AF and Amazonia, from phyloge-
netic, phylogeographic, ecologic modeling, and palinologic
proxies (e.g., Oliveira et al. 1999; Batalha-Filho et al. 2013;
Sobral-Souza et al. 2015; Prates et al. 2016; Bouimetarhan
et al. 2018; Silveira et al. 2019; Nascimento et al. 2021). For
harvestmen, this connection reaching to the Amazon is little
evidenced, since there is only two widespread species living
from PE until Amazonia (Cynorta unciscripta and Obidosius
evelinae, see Table 6.1), but occurring in Caatinga Dry Forest
as well. It seems there is a faunistic transitional gradient
westward from PE to Brejos Cearenses and so to Amazonia
to forest-dependent harvestmen, which would be an issue for
future works.
To the south, besides the contraction of humid forest from
São Francisco River to Todos os Santos Bay, replaced by dry
forests and Cerrado savannahs (Ab’Saber 1977; IBGE 1985),
the structural complexity of Recôncavo-Tucano sedimentary
basins and its geological faults (of approximately 100 million
years; Blaich et al. 2008) may have influenced the endemism
and the diversification between areas of endemism in different
periods. There is great variation of divergence time between
organisms from PE and Bahia – 0.47 to 22 mya (besides the
96
above-cited unpublished estimations for harvestmen,
Pellegrino et  al. 2005, 3.2–9.1 and 7.9–22.3  mya for
Gymnodactylus lizards; Cabanne et  al. 2008, 0.47  mya for
Xiphorhincus birds; Carnaval et al. 2009, they do not show the
time values, but indicated them in Pleistocene for Hypsiboas
frogs; Thomé et al. 2010, 0.51–1.03 mya for Rhinella toads),
and from PE versus Brejos Cearenses and the Amazon – 0.11
to 2.37  mya (Carnaval and Bates 2007, >0.21  mya for
Proceratophrys and Ischnocnema frogs; Cabanne et al. 2008,
0.11 mya for Xiphorhincus birds; Maldonado-Coelho et  al.
2013, they do not show the time values, but indicated them in
Pleistocene for Pyriglena birds; Prates et al. 2016, 0.156–1.62
mya for Anolis and 0.136–2.37 for Polychrus; DalVechio et al.
2018, 0.19–0.8 mya for Bothrops vipers; Nascimento et  al.
2021, 0.32–0.74 mya for Chiroxiphia birds; Fig.  6.3). This
variation demonstrates that its origin occurred through several
geological and climatic processes in different periods. DaSilva
et al. (2016b) presented a model of “reiterative barriers with
spatial congruence in multiple times,” in which temporal vari-
ation, redundant phylogenetic patterns, and the spatial congru-
ence of the barriers with the area of endemism limits evidence
that events of different geological times are interconnected
(see Table 6.1 and Fig. 6.3). Thus, the tectonic opening of a
sedimentary basin and the uplifting of mountain ranges, as
occurred with the Recôncavo-Tucano basin and the Borborema
Plateau, the emergence of large rivers and marine transgres-
sion in broader valleys, such as in the São Francisco River
region, and the forest contraction in these areas over time (e.g.,
Eocene, Oligocene, Pliocene, and Pleistocene; Auler et  al.
2004; Blaich et  al. 2008; Rossetti and Góes 2009; Werneck
2011; Holbourn et al. 2014) are related events. They unevenly
caused speciations of several organisms, but with great spatial
congruence, which would generate the areas of endemism.
6.6 PE Conservation: How
the Harvestmen Can Help?
In addition to historical factors, distribution patterns of har-
vestmen species are strongly related to its ecology and its
dependence on humidity. The habitat quality and quantity
directly influence species richness and abundance
(Bragagnolo et al. 2007; Porto et al. 2018). Besides, biologi-
cal characteristics such as microhabitat use and dispersal
capacity must contribute to the harvestmen distribution pat-
terns (Proud et al. 2012; Lira and DeSouza 2016). Therefore,
these organisms are good candidates for bioindicators of
forest quality, although more studies are needed on this sub-
ject. PE harvestmen endemic fauna could be bioindicators
since they are often related to humid portions of the forest
and seem to be rare (such as those restricted to CC;
A. M. DeSouza and M. B. DaSilva
Table 6.1). Besides, this is the most degraded portion of the
Atlantic Forest (Ribeiro et al. 2009). In areas with greater
water stress, such as in the Brazilian Northeast, it can be
adequate to consider harvestmen as bioindicators since they
present this strong relationship with humid areas, mainly the
rare species. Thus, Brejos de Altitude as those of the west
portion of the PE are true oases since they present greater
rain and river’s headwater concentrations (Andrade-Lima
1982; IBGE 1985; Cabral et al. 2004). Thus, the harvestmen
fauna can be an indicator of localities with a greater abun-
dance of river sources or greater water availability, even in
the past, since it would allow the maintenance of this sensi-
tive community.
6.7 Concluding Remarks
As demonstrated, there is no doubt that the PE is an impor-
tant sector of the Atlantic Forest. Several species and eco-
logical processes present in this region are unique and cannot
be found anywhere else in the world. In addition to these
characteristics, this is one of the less protected regions of the
Atlantic forest, highlighting the urgency of determining
strategies focused on local biodiversity conservation, includ-
ing the choice of model organisms for monitoring responses
to environmental changes. In this sense, harvestmen could be
a group of interest.
Harvestmen populations’ responses to environmental
changes, associated with its degree of endemism, microhabi-
tat use, and distributional patterns, place these organisms as
a viable option to be considered in the elaboration of PE con-
servation plans. In this sense, we need to improve our knowl-
edge of the Brejos de Altitude harvestmen populations. We
still have a lot to investigate about these organisms, but the
studies carried out so far are promising.
Acknowledgments We would like to thank the Aracnojampa lab
(UFPB), R Pinto-da-Rocha team, and all collaborators for their contri-
butions on the NAF harvestmen knowledge. We also thank the
OmniPaper Project (AB Kury) for the huge database of readily avail-
able taxonomic publications for the order Opiliones. We thank André
Nogueira, Cláudio Carvalho and Ricardo Pinto-da-Rocha for the care-
ful review of the manuscript, which helped greatly improve the final
work. For the financial support, we thank the Fundação de Amparo à
Pesquisa do Estado de São Paulo – FAPESP (Process 2013/50297-0),
the National Science Foundation (NSF/DOB 1343578) and NASA; the
Conselho Nacional de Desenvolvimento Científico e Tecnológico
(Edital MCT/CNPq n° 35/2012 – PPBio/Geoma – Redes de Pesquisa,
Monitoramento e Modelagem em Biodiversidade e Ecossistemas.
Parte–I – PPBio; and the Programa de Pesquisas em Biodiversidade do
Semiárido – CNPq #558317/2009-0 and #457471/2012-3); and AMD
thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
(CAPES) for the master and doctor fellowship and Graduate Program
in Zoology of UFPB.
6  The Most Endemic Taxon of an Area of Endemism: Harvestmen (Opiliones) Fauna of NAF and Its Contribution to Biogeography… 97

 ppendix: Authors of Species (with Reference) Recorded in the Area of Endemism

A
of Pernambuco

Cosmetidae
Acantholibitia pluriarcuata (Mello-Leitão, 1936).
Mello-Leitão CFDe (1936) Notas sobre opiliões. Bolm
Mus nac Rio de J 12(3–4): 1–41
Cosmetus biacutus Roewer, 1947.
Roewer CF (1947) Diagnosen neuer Gattungen und Arten
der Opiliones  - Laniatores. Weitere Weberknechte
XII. Cosmetidae. Senckenbergiana 28(1–3): 1–58
Cynorta ceara Roewer, 1927.
Roewer CF (1927) Weitere Weberknechte II. (2.
Ergänzung der Weberknechte der Erde, 1923). Abh Nat ver
Bremen 26(3): 527–632
Cynorta unciscripta Roewer, 1927.
Roewer CF (1927) Weitere Weberknechte II. (2.
Ergänzung der Weberknechte der Erde, 1923). Abh Nat ver
Bremen 26(3): 527–632
Gryne leprosa Soerensen, 1932.
Henriksen KL (1932) Descriptiones Laniatorum
(Arachnidorum Opilionum Subordinis). Opus posthumum
recognovit et edidit Kai L.  Henriksen. Nye samling af det
Kongelig Danske Videnskabernes Selskabs skrifter 3:
197–422
Gonyleptidae
Bebedoura rugosa Roewer, 1949.
Roewer CF (1949) Über Phalangodiden I. (Subfam.
Phalangodinae, Tricommatinae, Samoinae.) Weitere
Weberknechte XIII. Senckenbergiana 30(1–3): 11–61
Eusarcus dandara Saraiva & DaSilva, Saraiva and DaSilva
2016.
Saraiva NE, DaSilva MB (2016) Event-based biogeogra-
phy of Eusarcus dandara sp. nov. (Opiliones: Gonyleptidae),
an endemic species of the Northern Atlantic Rainforest of
Brazil, and its closely related species. Zootaxa 4205(6):
532–548. 10.11646/zootaxa.4205.6.2
Mitogoniella modesta (Perty, 1833).
Perty M (1833) Delectus animalium articulorum quae in
itinere per Brasilia annni 1817–1820 peracta collegerunt
J.B. Spix et de Martius. pp. 205. Monachii.
Pseudopucrolia discrepans (Roewer, 1943).
Roewer CF (1943) Weitere Weberknechte XI. Über
Gonyleptiden. Senckenbergiana, 26(1–3): 12–68
Pseudopucrolia incerta (Mello-Leitão, 1928).
Mello-Leitão CFDe (1928) Opiliões de Matto-Grosso e
Pernambuco. Bolm Mus nac Rio de J 4(2) 9–13.

Escadabiidae Kimulidae
Escadabius schubarti Roewer, 1949. Tegipiolus pachypus Roewer, 1943.
Roewer CF (1949) Über Phalangodiden I. (Subfam. Roewer CF (1949) Über Phalangodiden I. (Subfam.
Phalangodinae, Tricommatinae, Samoinae.) Weitere Phalangodinae, Tricommatinae, Samoinae.) Weitere
Weberknechte XIII. Senckenbergiana 30(1–3): 11–61 Weberknechte XIII. Senckenbergiana 30(1–3): 11–61
Escadabius spinicoxa Roewer, 1949.
Roewer CF (1949) Über Phalangodiden I. (Subfam.
Stygnidae
Phalangodinae, Tricommatinae, Samoinae.) Weitere
Gaibulus schubarti Roewer, 1943.
Weberknechte XIII. Senckenbergiana 30(1–3): 11–61
Roewer CF (1943) Weitere Weberknechte XI. Über
Escadabius ventricalcaratus Roewer, 1949. Gonyleptiden. Senckenbergiana 26(1–3): 12–68
Roewer CF (1949) Über Phalangodiden I. (Subfam.
Iguarassua schubarti Roewer, 1943.
Phalangodinae, Tricommatinae, Samoinae.) Weitere
Roewer CF (1943) Weitere Weberknechte XI. Über
Weberknechte XIII. Senckenbergiana 30(1–3): 11–61
Gonyleptiden. Senckenbergiana 26(1–3): 12–68
Recifesius pernambucanus H. Soares, 1978.
Kaapora minutissimus (Roewer, 1943).
Soares HEM (1978) Opera Opiliologica Varia. XIV.
Roewer CF (1943) Weitere Weberknechte XI. Über
(Opiliones, Phalangodidae). Papéis Zool S Paulo 32(12):
Gonyleptiden. Senckenbergiana 26(1–3): 12–68
141–144
98
Obidosius evelineae (Soares & Soares, 1978).
Soares HEM, Soares BAM (1978) Opera Opiliologica Varia.
V. (Opiliones, Stygnidae). Bolm Zool Univ S Paulo 3: 81–96
Obidosius mendopictus (H. Soares, 1978).
Soares HEM (1978) Opera Opiliologica Varia.
XI. Misetropius mendopticus, novo gênero e nova espécie e
notas sinonímicas de Stygnidae. Revta Bras Ent 22(2): 71–76
Pickeliana pickeli Mello-Leitão, 1932.
Mello-Leitão CFDe (1932) Opiliões do Brasil. Revta Mus
paul 17(2): 1–505
Stygnus polyacanthus (Mello-Leitão, 1923).
Mello-Leitão CFDe (1923) Opiliões Laniatores do Brasil.
Archos Mus nac Rio de J 24: 107–197
Zalmoxidae
Garanhunsa pectanalis Roewer, 1949.
Roewer CF (1949) Über Phalangodiden I. (Subfam.
Phalangodinae, Tricommatinae, Samoinae.) Weitere
Weberknechte XIII. Senckenbergiana, 30(1–3): 11–61
“Minuides” rudicoxa Roewer, 1949
Roewer CF (1949) Über Phalangodiden I. (Subfam.
Phalangodinae, Tricommatinae, Samoinae.) Weitere
Weberknechte XIII. Senckenbergiana, 30(1–3): 11–61
Pirassunungoleptes analis (Roewer, 1949).
Roewer CF (1949) Über Phalangodiden I. (Subfam.
Phalangodinae, Tricommatinae, Samoinae.) Weitere
Weberknechte XIII. Senckenbergiana, 30(1–3): 11–61.
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 The Spider Fauna of the Northern
Brazilian Atlantic Forest: Effect
of Sampling Bias on Diversity Patterns
and Conservation
Leonardo Sousa Carvalho , Philip Russo,
Antonio Domingos Brescovit, Márcia Oliveira-Tomasi,
Ubirajara de Oliveira, and Adalberto José dos Santos
Abstract
Spiders are a common and supposedly well-known group
of animals that can be found in a large variety of micro-
habitats, including human constructions. These organisms
represent a highly diversified taxon, with significant eco-
logical and human importance. Although spiders are
among the most diversified groups of arthropods, the
knowledge regarding their diversity patterns suffers from
strong biodiversity shortfalls. In Brazil, the distribution of
spider records is strongly aggregated spatially, which can
be explained by a museum effect, and the effect of easy-
to-sample localities. The highest number of records is
found in Atlantic Forest, and therefore, this biome has the
highest number of recorded spider species and endemic
species. However, these records are concentrated in a few
regions. The Northern Atlantic Forest, located north of the
São Francisco River, is one of the least sampled portions
of the biome. This chapter presents a comprehensive
overview of the diversity and distribution patterns of spi-
ders in this part of the Atlantic Forest considering data of
orb-weavers (superfamily Araneoidea) and daddy long-
legs (family Pholcidae) spiders. We produced maps show-
Supplementary Information The online version contains supplemen-
tary material available at https://doi.org/10.1007/978-­3-­031-­
21287-­1_7.
L. S. Carvalho (*)
Campus Amílcar Ferreira Sobral, Universidade Federal do Piauí,
Floriano, Piauí, Brazil
P. Russo · M. Oliveira-Tomasi
Pós-Graduação em Zoologia, Instituto de Ciências Biológicas,
Universidade Federal de Minas Gerais,
Belo Horizonte, Minas Gerais, Brazil
A. D. Brescovit
Laboratório de Coleções Zoológicas, Instituto Butantan,
São Paulo, Brazil
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
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_7
7
ing the spatial variation of the distribution records in order
to evaluate the sampling effort, species richness, beta-
diversity, and areas of endemism. The spider fauna in
Northern Atlantic Forest is known from 212 records of 70
species, and 19 of those are endemic. The present results
evidence and corroborate the hypothesis of strong biodi-
versity shortfalls regarding the spider fauna from this part
of the Atlantic Forest. These results support the striking
need to stimulate the development of more scientific stud-
ies and to allow a proper recognition and conservation of
this fauna.
Keywords
Araneoidea · Biodiversity shortfalls · Biogeography ·
Distribution records · Pholcidae · Spatial analysis
Spiders represent one of the most ubiquitous and familiar
groups of animals. These organisms can be found in a myriad
of microhabitats in natural environments and inside human
constructions. In these environments, spiders are responsible
for the control of insect populations, eating up to 800 million
tons of prey every year (Nyffeler and Birkhofer 2017).
Spiders subdue their prey mostly by the effect of venoms, the
source of an infinitude of substances that can be used in
U. de Oliveira
Centro de Sensoriamento Remoto, Instituto de Geociências,
Universidade Federal de Minas Gerais,
Belo Horizonte, Minas Gerais, Brazil
A. J. dos Santos
Departamento de Zoologia, Instituto de Ciências Biológicas,
Universidade Federal de Minas Gerais,
Belo Horizonte, Minas Gerais, Brazil
103
104
numerous biotechnological applications (Saez and Herzig
2019; Lüddecke et al. 2022). The venom of some spider spe-
cies is also responsible for a considerable number of acci-
dental bites on humans and domestic animals, which raises
their importance for public health (Isbister and White 2004).
On the other hand, spiders also produce silk, which is among
the most fascinating and better-studied natural products with
potential technological applications (Kluge et al. 2008). This
scenario suggests a naive and direct conclusion: Spiders rep-
resent a highly diversified taxon with multiple dimensions of
importance for humans and thus should be a well-known
taxon. However, the reality is somewhat different. The biodi-
versity shortfalls that entangle the web of knowledge regard-
ing the spider fauna are massive. Most importantly, the
knowledge deficits on spider diversity and distribution are
particularly marked in the lesser sampled, but potentially
species-rich portions of the planet. The present chapter aims
to evaluate biodiversity shortfalls regarding the Brazilian
Atlantic Forest spider fauna, focusing on its northern por-
tion, the lesser-known region of this biodiversity hotspot.
7.1 The Brazilian Spider Fauna
and Sampling Bias
Spiders are among the most diverse arthropods in natural
environments worldwide. For tropical regions, up to 700 spe-
cies and two million individuals are expected to be found in
1  ha of a lowland tropical moist forest (Coddington et  al.
2009a). This scenario suggests that most spider species
inventories are biased owing to undersampling (Coddington
et al. 2009a). As a consequence, for example, the outstand-
ingly high local species richness recorded throughout Brazil,
which surpassed 300 species at several sites (e.g., Höfer and
Brescovit 2001; Ricetti and Bonaldo 2008; Bonaldo et  al.
2009; Dias et al. 2009; Castanheira et al. 2016), seems to be
a mere fraction of the real number of species present at each
site.
At a large geographic scale, the state of the art might be
even worse. Although almost 7% of the ca. 50,000 described
spider species in the World are recorded from Brazil (Oliveira
et al. 2015, 2017a; WSC 2022), these species are unevenly
known throughout the country (Oliveira et al. 2016, 2017a).
The distribution records of spiders in Brazil are strongly
aggregated spatially, mostly explained by a museum effect,
i.e., the areas with the largest number of records are those
nearby larger and richer cities or close to old and historically
important research institutions (Oliveira et  al. 2017a).
Besides, the highest peaks of density of spider records in
Brazil are mostly located very close (< 1  km) to access
routes, suggesting a sampling also biased toward easy-to-­
sample localities (Oliveira et al. 2016). The spider communi-
ties at these sites are composed of significantly different
L. S. Carvalho et al.
species from those at more distant (> 1.5  km from access
routes) sites (Oliveira et al. 2016), which emphasizes another
facet of the sampling bias: even well-sampled areas might
present an unseen spider diversity. Such detailed conclusions
are possible owing to the assembling of large databases of
spider records in Brazil, which supported several studies that
evaluated the Brazilian spider diversity patterns (Brescovit
et al. 2011; Oliveira et al. 2015, 2016, 2017a; Santos et al.
2017). Although comprehensive, the results of these publica-
tions revealed strong sampling bias influencing our knowl-
edge on the diversity and distribution of the Brazilian spider
fauna.
The clumped distribution of the spider species records in
Brazil created a massive sampling gap that encompasses
nearly 70% of the Brazilian territory, where there is no record
of spider species (Oliveira et al. 2017a). A sampling bias of
this magnitude is shared by other arachnid groups in the
Brazilian semiarid region (DeSouza et al. 2014, 2017; Porto
et al. 2014; Oliveira et al. 2017a), where similar studies have
been carried out. Poorly sampled areas like these are those
mostly afflicted by Linnean and Wallacean shortfalls (sensu
Hortal et al. 2015), as shown for animals and plants (Oliveira
et  al. 2016). This means that these regions are particularly
likely to hold undescribed species – the Linnean shortfall –
and new species records  – the Wallacean shortfall. In fact,
that is the common result of most expeditions to historically
poorly sampled areas (e.g., Azevedo et  al. 2016; Carvalho
et al. 2017), or of taxonomic papers on species from these
regions (e.g., Huber 2015, 2016; Huber and Carvalho 2019).
7.2 The Atlantic Forest and Its Associated
Arachnid Fauna
The Atlantic Forest presents a complex biogeographic his-
tory, with high habitat heterogeneity and a wide topographi-
cal variation throughout its extension (Brown et  al. 2020).
These characteristics, associated with the largest latitudinal
variation of a tropical forest in the world, provide a suitable
environment for the establishment of a high number of spe-
cies, with high endemism, supporting the proposition of the
Atlantic Forest as one of the world biodiversity hotspots
(Myers et  al. 2000). This biome has been reported to hold
more than 20,000 species of plants, 334 of mammals, 745 of
birds, 528 of amphibians, 219 of snakes, 279 of fruit-feeding
butterflies, 3349 of ants, 87 of termites, 270 of land planari-
ans, more than 500 of harvestmen, and 1672 of spiders
(Ribeiro et al. 2009; Cancello et al. 2014; Moura et al. 2017a;
Oliveira et al. 2017a; Vancine et al. 2018; dos Santos et al.
2018; Nogueira et  al. 2019a, b; Souza et  al. 2019; Lago-­
Barcia et al. 2020; Silva et al. 2021). Many of these species
are struggling to survive on the remaining 8% of the original
Atlantic Forest extent (Silva and Tabarelli 2001; Colombo
7  The Spider Fauna of the Northern Brazilian Atlantic Forest: Effect of Sampling Bias on Diversity Patterns and Conservation
and Joly 2010; Canale et  al. 2012), especially considering
that only 45% of its current animal communities are esti-
mated to be similar to predeforestation times (Brown et al.
2020).
Considering the arachnid orders, our current knowledge
on species richness and distribution is particularly heteroge-
neous throughout the Atlantic Forest. Harvestmen are the
most studied arachnid group in the Atlantic Forest, especially
regarding their biogeography and distribution patterns at
local and regional scales (Almeida-Neto et  al. 2006;
Bragagnolo et al. 2007; DaSilva et al. 2015; Nogueira et al.
2019a, b). Spiders, on the other hand, are the only other
arachnid order comparable to harvestmen in terms of biodi-
versity knowledge throughout the Atlantic Forest. Detailed
data on Atlantic Forest spiders have been shown along with
other taxa or at wider geographic scales (Oliveira et al. 2015,
2016, 2017a, b, 2019b; Santos et al. 2017), while most pub-
lications specifically targeting Atlantic Forest spiders focus
on taxonomic issues (e.g., Huber and Rheims 2011; Huber
2015). Lastly, other Arachnida orders are less diversified
(i.e., less than 15 described species of Amblypygi, Palpigradi,
Schizomida, Scorpiones, and Thelyphonida), completely
absent (e.g., Solifugae and Ricinulei), or lack available data-
bases (e.g., Acariformes and Parasitiformes) to allow the
proper comparison of the known diversity patterns described
for Opiliones and Araneae.
The Atlantic Forest represents a worldwide hotspot for
harvestmen diversity, with hundreds of described species and
up to 97.5% of species endemism (Pinto-da-Rocha et  al.
2005). This biome also harbors about 60% of the Brazilian
harvestmen fauna (Pinto-da-Rocha et al. 2005), besides the
highest harvestmen species richness per site in the world,
with up to 63 species recorded from a single locality in
southeastern Brazil (Bragagnolo and Pinto-da-Rocha 2003).
This high species richness allowed the use of the group as a
model to test predictions of biogeographic hypotheses, such
as the extended Rapoport’s rule (sensu Stevens 1992), which
predicts wider altitudinal ranges for species at higher alti-
tudes. This prediction was not supported for Atlantic Forest
montane harvestmen, as species covering broader elevational
ranges showed optimal elevation below the middle of their
ranges (Almeida-Neto et  al. 2006). This unexpected result
was explained by differential tolerance of temperature and
humidity of species with source populations below mid-­
elevations (Almeida-Neto et  al. 2006). These abiotic vari-
ables are strongly correlated with harvestmen species density
and specimen abundance at fine spatial scales (Almeida-­
Neto et  al. 2006). At broad scales, the harvestmen alpha
diversity increases with the precipitation (Nogueira et  al.
2019b), while its beta diversity patterns are more related to
historical factors (Nogueira et al. 2019a, b).
The wide latitudinal variation in the Atlantic Forest
allowed the recognition of a highly diversified harvestmen
105
fauna in the southeastern Atlantic Forest, while the north-
eastern Atlantic Forest presents a smaller number of species,
belonging to a higher number of families (Nogueira et  al.
2019a, b). However, the historical factors that shaped these
communities resulted in substantial differences in species
composition, with a decrease in the proportion of
Gonyleptidae and an increase in the proportion of
Cosmetidae, Escadabiidae, Stygnidae, and Zalmoxidae spe-
cies in harvestmen communities toward lower latitudes
(Nogueira et al. 2019a). As a consequence, the biome shows
phylogenetically overdispersed harvestmen communities in
its northern portion, and phylogenetic clustering at higher
latitudes (Nogueira et  al. 2019a), a pattern also found for
snakes (Moura et al. 2017b).
Harvestmen data was also used to propose and delimit
areas of endemism (AoE) in the Atlantic Forest (Pinto-da-­
Rocha et al. 2005; DaSilva et al. 2015, 2016), a type of anal-
ysis also carried out for land planarians (Lago-Barcia et al.
2020), orchid bees (Garraffoni et al. 2017), passerine birds
(Silva et al. 2004), spiders (Oliveira et al. 2015), and several
taxa together (Sigrist and de Carvalho 2008; Hoffmeister and
Ferrari 2016). Some of these studies have severe limitations
on the geographic coverage (e.g., Silva et  al. 2004; Lago-­
Barcia et al. 2020) or on the taxonomic completeness of the
database used (e.g., Pinto-da-Rocha et  al. 2005; DaSilva
et al. 2015; DaSilva et al. 2016). Additionally, these studies
used several different algorithms and methodological set-
tings, but they mostly corroborated each other in the areas of
endemism proposed. In northeastern Brazil, two AoEs were
recognized: one in the most northern part of the Atlantic
Forest, and one in the state of Bahia, with different exten-
sions on various studies (Silva et  al. 2004; Oliveira et  al.
2015; DaSilva et al. 2015; Garraffoni et al. 2017). Southward,
the Doce River seems to be a boundary between northern and
southern communities, and it is also the location of an AoE
(Oliveira et al. 2015; DaSilva et al. 2015). In Southeastern
Brazil, the Serra do Mar represents a large AoE (Oliveira
et  al. 2015), that can be further subdivided into several
smaller AoEs (DaSilva et al. 2015; Lago-Barcia et al. 2020).
In Southern Brazil, another large AoE is also commonly rec-
ognized in different studies (Silva et al. 2004; Oliveira et al.
2015; DaSilva et  al. 2015; Garraffoni et  al. 2017; Lago-­
Barcia et al. 2020).
7.3 Spiders from Northern Atlantic
Forest: A Comprehensive Comparison
The Atlantic Forest presents the highest number of records of
spiders and therefore the highest numbers of recorded spider
species (1672 spp.; ca. 52% of the Brazilian spider species)
and endemic species (592 spp.), compared to other Brazilian
biomes (Oliveira et al. 2017a). These records are distributed
106
for almost 90% of the Atlantic Forest range, with about 17%
of this area presenting only a single record of spiders
(Oliveira et al. 2017a). Such sampling coverage is similar to
that observed for the Pampas (80% of coverage, with 33% of
the area with a single record), which is, together with the
Atlantic Forest, significantly better sampled than the other
Brazilian biomes (Oliveira et  al. 2017a). Additionally, the
Atlantic Forest presents about three times more records of its
spider fauna than expected by chance, i.e., the number of
expected records if the entire Brazilian biomes were sampled
proportionally to their area. This suggests that the Atlantic
Forest spiders are also better sampled than in the remaining
Brazilian biomes (Oliveira et al. 2017a). This scenario is not
perfect, however. The distribution of spider species records
in the Atlantic Forest is concentrated in a few regions (e.g.,
southeastern Brazil), as demonstrated by the small number
of spider species inventories ever carried out in this biome
(e.g., Gonçalves-Souza et al. 2005; Dias et al. 2006; Pinto-­
Leite et al. 2008; Peres et al. 2014; Azevedo et al. 2014; de
Pitilin et al. 2019). Only two inventories yielded a sampling
coverage of at least 70% of the spider fauna in Atlantic Forest
sites. A study carried out in Southeastern Brazil observed
293 spider species and estimated about 416 species in the
area, a sampling coverage of 70.4% (Azevedo et al. 2014). In
Northeastern Brazil, another study observed 166 species and
estimated about 211 spider species in the area, a sampling
coverage of 78.67% (Dias et  al. 2006). Although there are
clear methodological differences in the spider sampling at
both studies, this suggests a higher spider species richness in
Southeastern Brazil. Comparisons like this are punctual, not
representing an empirical hypothesis testing based on opti-
mized and/or standardized samplings throughout the Atlantic
Forest. This scenario suggests that the Atlantic Forest should
not be considered sufficiently sampled (Oliveira et al. 2016,
2017a).
The Northern Atlantic Forest – hereafter called “NAF” –
is one of the least sampled portions of the biome, regarding
its spider fauna. In this context, in this chapter, we present a
comprehensive overview of the diversity and distribution
patterns of the NAF spiders, comparing with the available
information for the entire Atlantic Forest spider fauna. To
accomplish this goal, we gathered the data regarding two spi-
der taxa: Araneoidea and Pholcidae (Fig. 7.1). The superfam-
ily Araneoidea comprises 17 families and almost a third of
all known spider species (Wheeler et al. 2017; WSC 2022),
and includes mostly web-weaving spiders. The Araneoidea
database was based on an extensive literature revision and
includes over 25,000 records, of 2677 described species,
from more than 8600 localities in the Neotropical region,
taken from 550 taxonomic and diversity survey papers pub-
lished up to 2017 (P. Russo, unpublished data; partially pub-
lished by Santos et  al. 2017). The spider family Pholcidae
comprises about 1850 described species, being the ninth
most diversified spider family (WSC 2022). Pholcids repre-
L. S. Carvalho et al.
sents a group of (mostly) long-legged spiders that can be
found on the underside of green leaves, among the leaf litter,
or in cave walls around the globe, with a high percentage of
endemism (Huber and Rheims 2011; Huber 2015). The
Pholcidae database comprises information from relevant
taxonomic papers (published up to 2019), besides the infor-
mation of over 8000 examined specimens of 1042 species,
including 611 described and 431 undescribed species, from
the Neotropical region (e.g.,  Huber 2016, 2018a, b; Huber
and Carvalho 2019; Huber and Chao 2019). All duplicated
records (e.g., two records of the same species, with the same
geographic coordinates) were removed from the analyzed
database.
The shapefile used to delimit the NAF is formed by areas
northern to the São Francisco River to its northernmost limit,
encompassing the entire Atlantic Forest biome in the north-
eastern Brazilian states of Alagoas, Pernambuco, Paraíba,
and Rio Grande do Norte (Fig. 7.2). This region is known by
its distinct biota and represents an important area of ende-
mism in South America (Silva and Tabarelli 2000, 2001). To
the sake of clarity, the NAF was delimited including humid
highlands, the so-called “brejos de altitude,” located in the
states of Paraíba (municipalities of Alagoa Grande, Alagoa
Nova, Araruna, Areia, and Bananeiras) and Pernambuco
(municipalities of Agrestina, Bezerros, Bonito, Brejo Madre
de Deus, Camocim de São Félix, Caruaru, Gravatá, São
Vicente Férrer, and Taquaritinga), all in the eastern border of
the Borborema plateau.
We produced maps showing the spatial variation of
parameters related to the sampling effort, endemism, species
composition and the delimitation of areas of endemism based
on the Atlantic Forest spider fauna. The sampling effort sec-
tion also discusses its most direct result, the species richness.
The endemism patterns are discussed by comparing the
known geographic distribution of Atlantic Forest spider spe-
cies, inside and outside this biome. The species composition
is presented as the spatial variation of the beta-diversity
index, calculated with a Jaccard coefficient. This parameter
is discussed based on its turnover and nestedness partitions
and on the beta-diversity owing to environmental predictions
(i.e., generalized dissimilarity model – GDM, described by
Ferrier et  al. 2007). Lastly, the endemism patterns of this
fauna is detailed, including the delimitation of areas of ende-
mism, based on kernel interpolation (i.e., geographical inter-
polation of endemism described by Oliveira et al. 2015), and
the spatial variation of the weighted endemism (as proposed
by Crisp et al. 2001). The sampling effort function (Oliveira
et  al. 2019a) was run with a 150  km search radius for the
entire Atlantic Forest and 50 km for the NAF. The geographi-
cal interpolation of endemism, the species composition inter-
polation and the weighted endemism analyses were run only
for the entire Atlantic Forest, further clipped to the NAF, as
these analyses suffer from analytical biases owing to the geo-
graphic coverage of the database used. The variation in spe-
7  The Spider Fauna of the Northern Brazilian Atlantic Forest: Effect of Sampling Bias on Diversity Patterns and Conservation
Fig. 7.1  Representatives of the Atlantic Forest spider fauna, including
Araneoidea (a–f) and Pholcidae (g–h) species. (a) Dipoena pumicata
(Keyserling, 1886); (b) Eustala taquara (Keyserling, 1892); (c) Pronous
tuberculifer Keyserling, 1881; (d) Manogea porracea (C.  L.  Koch,
cies composition and the GDM were classified with the ISO
cluster unsupervised classification technique, resulting in
maps with 12 and 5 discrete regions for the entire Atlantic
Forest and for the NAF, respectively.
All spatial analyses were carried out using the
BioDinamica tool package, a sublibrary developed for the
software Dinamica-EGO (Oliveira et al. 2019a). The GDM
used the geographic distance and the 19 bioclimatic layers
available at the WorldClim, at a 2.5° resolution (Fick and
Hijmans 2017), with a minimum of ten samples per site,
three I-splines, and an equal weight type. To remove the spa-
tial autocorrelation between the bioclimatic variables, a prin-
cipal component analysis was carried out. Although the fifth
axis in the PCA explained less than expected by chance (i.e.,
in an analysis with 19 layers, each axis is expected to explain
5.26% of the spatial variation by chance), we choose to use
the resulting raster maps for the axes that summed at least
107
1838); (e) Micrathena schreibersi (Perty, 1833); (f) Micrathena fissi-
spina (C. L. Koch, 1836); (g) Saciperere catuaba Huber & Carvalho,
2019; (h) Mesabolivar spinulosus (Mello-Leitão, 1939). (Photos:
P.H.  Martins (a, c, f), Y.F.  Messas (b), L.S.  Carvalho (d, g, h),
P.H. Martins & A. Anker (e))
95% of the variation as predictors (see Table 7.5). All analy-
ses were run using 0.5° side-to-side hexagons. The results
were edited using the GIS software ArcMap 10.3 (ESRI) to
standardize raster maps with continuous data, by using
stretched symbology based on 2.5 standard deviations. Map
correlations were also calculated using ArcMap 10.3 tools.
Correlation coefficients between NMDS-based analyses
(e.g., beta diversity and its partitions; Fig.  7.5) should be
interpreted disregarding its positive or negative signals, as
they represent correlations between ordinated matrices trans-
formed by the multivariate analyses, instead of correlations
between the raw similarity matrices. Therefore, correlation
values shown in NMDS-based maps are shown as its modulo
(i.e., its absolute value). NMDS analyses were run with up to
10,000 tries and used in this study only if a convergence was
achieved and with a stress value lower than 0.2. The final
figures were assembled in CorelDraw, version 2019.
108 L. S. Carvalho et al.

Fig. 7.2  Records of Araneoidea and Pholcidae spider species in the Atlantic Forest. Dotted line in the left map refers to the Northern Atlantic
Forest region, detailed on the right map

Table 7.5  Significant principal components (PC) for the environmental layers used as predictor layers in the generalized dissimilarity modeling
for Atlantic Forest spiders
Parameter PC 1 PC 2 PC 3 PC 4 PC 5
Standard deviation 3.01 2.08 1.44 1.41 0.88
Proportion of variance 47.69% 22.84% 10.92% 10.50% 4.05%
Cumulative proportion 47.69% 70.53% 81.46% 91.96% 96.01%
The selected PCs are those which the total cumulative percentage of total variation sum at least 95%

7.3.1 Sampling Effort and Species Richness
The records of the full databases were clipped to the Atlantic
Forest area and to the NAF, resulting in a database with 5482
nonduplicated records of 842 species among 12 spider fami-
lies (Table 7.1; Supplementary Table S1; Fig. 7.2). Less than
4% of these records are in the NAF, representing 70 species
from 5 spider families (Tables 7.1, 7.2 and 7.3). Although it
seems a very low number of records for spiders at the NAF,
these numbers are higher or about the same number of
records expected by chance, considering the area (in km2)
covered by the Atlantic Forest in the region (Fig.  7.3;
Table 7.2). The low numbers of spider families and species
recorded to the NAF reflects the Linnean shortfall regarding
this fauna. For example, two spider species inventory pub-
lished from NAF localities revealed the presence of unidenti-
fied species of the araneoid families Anapidae, Mimetidae,
Mysmenidae, Tetragnathidae, and Theridiosomatidae, with a
significant portion of all spider families composed by unde-
scribed and/or undetermined species (Dias et al. 2006; Peres
et al. 2007). A good example of the historical Linnean short-
fall regarding this fauna is ascertained by the daddy long-­
7  The Spider Fauna of the Northern Brazilian Atlantic Forest: Effect of Sampling Bias on Diversity Patterns and Conservation 109

Table 7.1  Number of species and records per spider family in the Atlantic Forest
Species Records Total
Family N N&S S N S Records Species
Anapidae 2 2 2 2
Araneidae 3 23 323 51 3274 3325 349
Linyphiidae 1 47 1 132 133 48
Mimetidae 7 104 104 7
Mysmenidae 3 10 10 3
Nesticidae 1 7 1 29 30 8
Pholcidae 14 9 250 133 992 1125 273
Symphytognathidae 3 3 3 3
Synotaxidae 3 10 10 3
Tetragnathidae 12 52 52 12
Theridiidae 3 16 103 26 640 666 122
Theridiosomatidae 12 22 22 12
Total 21 49 772 212 5270 5482 842
Numbers refers to taxa or records from northern (N; i.e., Northern Atlantic Forest) or southern (S) to the São Francisco River, or species distributed
in both (N&S) regions of the Atlantic Forest

Table 7.2  Atlantic Forest area size (in km2) observed and expected number of records, and spider species richness at each Brazilian state
Area (km2) Number of records
State Obs. Exp. % Exp. Species richness
Alagoas 45,246.1 81 71.2 114% 27
Bahia 10,504.2 350 537.5 65% 146
Espírito Santo 241,704.0 300 224.0 134% 136
Goiás 102,986.0 0 52.0 0% 0
Mato Grosso do Sul 194,103.0 22 249.5 9% 20
Minas Gerais 14,385.2 470 1196.7 39% 202
Paraíba 41,460.2 49 28.8 170% 27
Paraná 10,597.0 565 961.0 59% 183
Pernambuco 50,398.0 69 93.6 74% 40
Rio de Janeiro 18,896.6 782 205.3 381% 248
Rio Grande do Norte 93,942.2 13 13.5 96% 8
Rio Grande do Sul 2734.1 1145 509.9 225% 233
Santa Catarina 108,559.0 489 465.1 105% 216
São Paulo 5808.0 1101 821.5 134% 300
Sergipe 165,928.0 46 52.5 88% 29
Expected number of records was calculated proportionally to the area of the Atlantic Forest at each state

legs spiders (Pholcidae) from the NAF, from which 13
species were described since 2015, four are hitherto unde-
scribed and only six are known for more than 10  years
(Table  7.3). It is important to remember that the database
analyzed in the present chapter includes only Araneoidea
taxonomic papers published until 2017, and more recent
publications with records of spiders from the NAF are miss-
ing (e.g., Santanna and Rodrigues 2018; Santanna et  al.
2019; de Castanheira and Baptista 2020; de Castanheira and
Baptista 2021).
The Atlantic Forest shows several spots with high concen-
trations of spider records (Figs.  7.4a, b) and species
(Figs 7.4c, d). Most of the high-density spots southern to the
São Francisco River are located close to larger and richer
cities and historically important research institutions (a.k.a.,
the “museum effect”), following the general pattern observed
for spiders in Brazil (Oliveira et al. 2017a), and partially for
the Brazilian biota as a whole (Oliveira et al. 2016). As also
reported in the literature (Oliveira et  al. 2016, 2017a), the
spider species richness is highly correlated to the number of
records (a crude estimation of sampling effort) throughout
the Atlantic Forest biome (r2 = 0.89; Table 7.4). However, the
patterns observed for the NAF spiders differ significantly,
with a weak negative correlation between the sampling effort
and the species richness of spiders in this region (r2 = −0.46;
Table 7.4). The areas of higher density of records in the NAF
are associated with major cities – as expected – but also with
conservation units and brejos de altitude (Fig.  7.4b). The
concentration of conservation units with high density of
records (see localities 7–10 in Fig. 7.4b) reveals an area with
110 L. S. Carvalho et al.

Table 7.3  List of spider species known from the Northern Atlantic Table 7.3 (continued)
Forest, including their number of records and the Brazilian states where
TAXA AL PB PE RN Total
they occur
 Mesabolivar kathrinae Huber, 2015 2 2 4 8
TAXA AL PB PE RN Total  Mesabolivar murici Huber, 2018 1 2 3
Araneidae 12 11 23 5 51  Mesabolivar spinulosus (Mello-Leitão, 2 2 4 8
 Acacesia hamata (Hentz, 1847) 1 1 2 1939)
 Alpaida natal Levi, 1988 1 1  Mesabolivar togatus (Keyserling, 1 1
 Alpaida veniliae (Keyserling, 1865) 2 2 1891)
 Argiope argentata (Fabricius, 1775) 4 2 4 2 12  Metagonia Br11-107 4 3 7
 Argiope trifasciata (Forsskål, 1775) 1 1  Metagonia Br15-101 1 1
 Cyclosa bifurcata (Walckenaer, 1841) 1 1  Metagonia taruma Huber, 2000 8 3 4 1 16
 Cyclosa caroli (Hentz, 1850) 1 1  Physocyclus globosus (Taczanowski, 2 2
 Eustala taquara (Keyserling, 1892) 2 2 1874)
 Gasteracantha cancriformis 1 1  Psilochorus taperae Mello-Leitão, 1 1
(Linnaeus, 1758) 1929
 Hypognatha belem Levi 1996 2 2  Saciperere catuaba Huber & Carvalho 5 2 3 10
 Hypognatha cryptocephala (Mello-­ 1 1 2019
Leitão, 1947 Theridiidae 9 10 7 26
 Larinia t-notata (Tullgren, 1905) 1 1  Achaearanea hieroglyphica (Mello-­ 1 1
 Mangora missa Levi, 2007 1 1 Leitão, 1940)
 Manogea porracea (Koch, 1838) 1 1  Achaearanea trapezoidalis 1 1
 Metazygia ipago Levi, 1995 1 1 (Taczanowski, 1873)
 Micrathena evansi Chickering, 1960 1 1  Chrosiothes murici Puchulú-­ 1 1
Figueiredo, Santanna & Rodrigues,
 Micrathena fissispina (C. L. Koch, 2 2 4
2017
1836)
 Chrysso albomaculata O. Pickard-­ 1 1
 Micrathena horrida (Taczanowski, 2 2
Cambridge, 1882
1873)
 Chrysso rubrovittata (Keyserling, 1 1
 Micrathena patruelis (C. L. Koch, 2 2
1884)
1839)
 Cryptachaea digitus (Buckup and 1 2 3
 Micrathena picta (C. L. Koch, 1836) 2 2
Marques, 2006)
 Micrathena schreibersi (Perty, 1833) 2 1 1 4
 Cryptachaea hirta (Taczanowski, 1 1 2
 Micrepeira hoeferi Levi, 1995 1 1 1873)
 Pronous tuberculifer Keyserling, 1881 1 1 2  Dipoena atlantica Chickering, 1943 1 1
 Spilasma baptistai Levi, 1995 1 1  Dipoena ira Levi, 1963 1 1
 Verrucosa arenata (Walckenaer, 1841) 1 1  Dipoena pumicata (Keyserling, 1886) 1 1
 Wagneriana transitoria (C. L. Koch, 1 1  Exalbidion fungosum (Keyserling, 1 1
1839) 1886)
Linyphiidae 1 1  Meotipa pulcherrima (Mello-Leitão, 1 1
 Eurymorion murici Rodrigues & Ott, 1 1 1917)
2010  Neopisinus longipes (Keyserling, 1 1
Nesticidae 1 1 1884)
 Nesticella murici Rodrigues & 1 1  Neopisinus recifensis (Levi, 1964) 1 1 1 3
Buckup, 2007  Parasteatoda nigrovittata (Keyserling, 1 2 3
Pholcidae 58 28 39 8 133 1884)
 Carapoia abdita Huber, 2016 1 1  Theridion pernambucum Levi, 1963 1 1
 Carapoia agilis Huber, 2018 4 4  Theridula multiguttata Keyserling, 1 1
 Carapoia alagoas Huber, 2016 8 8 1896
 Carapoia bispina Huber, 2018 1 1  Thymoites murici Rodrigues & 1 1
 Carapoia djavani Huber, 2018 18 1 19 Brescovit, 2015
 Carapoia pulchra Huber, 2018 6 1 7  Wamba crispulus (Simon, 1985) 1 1
 Carapoia saltinho Huber, 2016 2 2 Total 81 49 69 13 212
 Carapoia septentrionalis Huber, 2016 5 2 1 8 Species codes provided for Pholcidae taxa represent standardized codes
 Carapoia suassunai Huber, 2018 3 1 2 6 used in other projects with the taxa and do not represent nomenclatural
 Kambiwa L21-275 1 1 acts according to the International Commission on Zoological
 Kambiwa neotropica (Kraus, 1957) 1 1 Nomenclature – ICZN regulations
 Litoporus Br15-107 1 1 Abbreviations: AL Alagoas, PB Paraíba, PE Pernambuco, RN Rio
Grande do Norte
 Mesabolivar buraquinho Huber, 2018 4 8 5 17
(continued)
7  The Spider Fauna of the Northern Brazilian Atlantic Forest: Effect of Sampling Bias on Diversity Patterns and Conservation 111

Fig. 7.3  Observed and expected number of records at each Brazilian state. Expected number of records is proportional to the area of the Atlantic
Forest at each state

Fig. 7.4  Sampling effort (a, b) and species richness (c, d) of spiders in
the entire Atlantic Forest (a–c) and in its northern region (b–d). Pearson
correlation coefficients are shown in numbers at lines connecting maps.
Main cities: 1: Natal, state of Rio Grande do Norte (RN); 2: João
Pessoa, state of Paraíba (PB); 3: Recife, state of Pernambuco; and 4:
Maceió, state of Alagoas (AL). Other localities with high sampling
effort: 5: Reserva Biológica de Guaribas, Rio Tinto, Paraíba; 6: Parque
Estadual da Mata do Pau Ferro, Areia, Paraíba; 7: Brejo de altitude at
Bonito, Pernambuco; 8: Reserva Biológica de Saltinho, Tamandaré,
Pernambuco; 9: Estação Ecológica de Murici, Murici, Alagoas; 10:
Reserva Biológica de Pedra Talhada, Quebrângulo, Alagoas

high number of spider species in the states of Alagoas and
Pernambuco (Fig.  7.4d). These conservation units play an
important role in maintaining a significant portion of the
NAF remnants, with brejos de altitude (e.g., locality 6  in
Fig. 7.4b) proportionally better preserved than other ecosys-
tems in the biome (Ribeiro et al. 2009). However, it is uncer-
tain whether these localities harbor more spider species than
the remaining NAF, owing to the strong sampling bias and a
low density of records in the surroundings of these localities.
The effect of sampling bias is probably worsened by the
deforestation in the region (see Ribeiro et al. 2009), which is
most likely to have already significantly altered spider com-
munities outside these areas, thus hampering future attempts
to decrease this biodiversity shortfall. However, it is impor-
tant to note that any spider sampling at poorly known regions
should be encouraged, as even human-modified environ-
112 L. S. Carvalho et al.

Table 7.4  Correlation between the parameters analyzed of the Atlantic Forest spiders
Sampling Species Weighted Species composition interpolation
effort richness endemism Total βD βD Turnover
Axis Axis Axis Axis Axis
Parameter 1 2 3 1 2 Axis 3
Sampling effort – −0.46 −0.46 0.1 −0.2 −0 0.1 −0.2 −0
Species richness 0.89 – −1 0.2 −0.4 −0 0.1 −0.4 −0
Weighted endemism −0.01 0.1 – 0.2 −0.4 0.01 0.1 −0.4 −0.1
Species composition Total βD Axis 0.22 0.1 −0.62 – 0.39 0.85 1 0.53 0.83
interpolation 1
Axis 0 0.05 0.12 0 – 0.07 0.5 0.98 0.04
2
Axis 0.25 0.09 −0.17 0.3 0.75 – 0.8 0.27 0.99
3
βD Axis −0.2 −0.09 0.61 1 0.01 0.24 – 0.64 0.73
turnover 1
Axis −0.11 −0.03 0.12 0.1 0.98 0.74 0 – 0.16
2
Axis 0.32 0.15 −0.16 0.3 0.71 0.98 0.3 0.72 –
3
Upper Half represents values for the Northern Atlantic Forest spider fauna; lower half represents values for the entire Atlantic Forest spider fauna.
βD beta-diversity

ments might reveal new spider occurrences (e.g., Correa
et al. 2021).
The effect of sampling bias on the NAF spider diversity
patterns, on the other hand, should be interpreted with cau-
tion. Although it is clear that this effect exists, the evolution-
ary history and the complex geography of the Atlantic Forest
resulted in a highly diverse biota (Brown et al. 2020), with
areas of high species richness highly congruent among sev-
eral taxa, including harvestmen (Nogueira et  al. 2019b),
snakes (Moura et  al. 2017b), birds (Vale et  al. 2018; de
Figueiredo et al. 2021), mammals (de Figueiredo et al. 2021),
and frogs (Vasconcelos et al. 2014). Therefore, the high spe-
cies richness and the latitudinal variation in the species rich-
ness (higher on its southeastern portion), herein shown for
Araneoidea and Pholcidae, seem to be characteristic of this
biome, as previously discussed in the literature (Huber and
Rheims 2011; Huber 2015; Santos et al. 2017).
7.3.2 Endemism and Species Distribution
Patterns
Our databases include records of 70 Araneoidea and
Pholcidae species in the NAF.  Among the 19 species
endemic to the NAF, only seven have been described more
than 10 years ago (Alpaida natal Levi, 1988, Eurymorion
murici Rodrigues & Ott, 2010, Metazygia ipago Levi,
1995, Psilochorus taperae Mello-Leitão, 1929, Spilasma
baptistai Levi, 1995, Theridion pernambucum Levi, 1963,
and Theridula multiguttata Keyserling, 1886). The other
12 endemics were described since 2015 (Rodrigues and
Brescovit 2015; Huber 2016, 2018a), or are hitherto unde-
scribed (e.g., species of Metagonia and Litoporus), 11 of
them are known only from their type-localities. Four
recorded spider species are widely distributed in the World
(Argiope argentata (Fabricius, 1775), Gasteracantha can-
criformis (Linnaeus, 1758), Meotipa pulcherrima (Mello-
Leitão, 1917), and Physocyclus globosus (Taczanowski,
1874)). Among the 47 remaining species, five are known
only from records in the Atlantic Forest northern to the
Doce River (Nesticella murici Rodrigues and Buckup
2007, Litoporus Br15-107, Mesabolivar buraquinho
Huber, 2018, Metagonia Br11-107, and Chrosiothes murici
Puchulú-Figueiredo, Santanna & Rodrigues, 2017), with
records inside and outside the NAF.  Additionally, the
threat status is unknown for all spider species recorded to
the NAF.
Some nonendemic species present interesting distribution
patterns. For example, the orb-weaver Mangora missa Levi,
2007, is known from disjunct records from the state of
Paraíba (in northeastern Brazil) to Southeastern (Rio de
Janeiro and São Paulo) and Southern (Paraná, Santa Catarina
and Rio Grande do Sul) Brazil, with no records in between
(Alagoas, Sergipe, Bahia and Espírito Santo), suggesting a
clear case of Wallacean shortfall. Other species, such as the
spiny orb-weaver Micrathena schreibersi (Perty, 1833)
(Fig. 7.1e) and the daddy long-legs spider Saciperere catu-
aba Huber & Carvalho, 2019 (Fig. 7.1g), have a disjunct dis-
tribution with records in the Atlantic and in the Amazon
forests (Levi 1985; Huber and Carvalho 2019). Both species
are known to be morphologically variable and might be sub-
ject to further splitting after phylogeographic or morphologi-
7  The Spider Fauna of the Northern Brazilian Atlantic Forest: Effect of Sampling Bias on Diversity Patterns and Conservation
cal studies aiming to test species limits between their
populations.
7.3.3 Species Composition
The spider species composition throughout the Atlantic
Forest exhibits a wide spatial variation (Figs. 7.5 and 7.6), as
much as the sampling effort and the species richness
(Fig.  7.4). The species composition variation is strongly
related to the latitude (Figs. 7.5a and 7.6a). When partitioned,
the spatial variation in beta-diversity showed a high correla-
tion with its turnover partition (r2(Axis1) = 0.99; r2(Axis2) = 0.98;
r2(Axis3) = 0.98; Table 7.4; Fig. 7.5b). The nestedness partition
Fig. 7.5  Spatial variation of spider species composition throughout the
Atlantic Forest (a, c, d, f) and its turnover partition (b, e), including a
clipped detail for the northern region (d–f) and classified (see text for
details) map of the total beta-diversity (c, f). Species composition was
obtained by interpolation of NMDS scores, with three axes represented
by an RGB scale. The beta-diversity (βD) is partitioned into turnover
(b, d), while nestedness analyses did not converge and are not shown
113
was impossible to access as its NMDS analysis did not con-
verge and it exhibited a stress of 0.22, yielding a random
result. While decomposing the beta diversity in approaches
like this does not provide evidence of the factors that explain
its variation (e.g., environmental filters, historical factors,
etc.), this analysis allows to measure the importance of the
species substitutions in Atlantic Forest spider communities.
Additionally, we assume that the absence of convergence in
the nestedness partition analysis can be explained by under-
sampling bias. While this bias was described to explain the
relatively high percentage of singletons in inventories of
tropical arthropods (Coddington et al. 2009b), the undersam-
pling bias results in poorly sampled arthropod communities,
especially regarding rare species. Therefore, if the nested-
(see text for details). Lines indicate each axis and Pearson correlation
between them. Different colors on each map should be interpreted as
different spider communities. NMDS for total beta-diversity yielded
nonmetric fit, R2 = 0.971; linear fit, R2 = 0.828. NMDS for the turnover
partition diversity yielded nonmetric fit, R2  =  0.969; linear fit,
R2 = 0.821. The stress value for both analyses was 0.17
114
Fig. 7.6 (a, b) Areas of endemism of spiders in the Atlantic Forest (a)
and its northern region (b). (c, d) Spatial variation of the weighted
endemism of spider species in the Atlantic Forest (c) and its northern
region (d). Gaps or discontinuities in areas of endemism: 1. São
Francisco River mouth; 2. Todos os Santos Bay; 3. Doce River mouth;
ness effect on the beta-diversity is weak or not uniformly
distributed throughout the biome, it might require a more
intense sampling to provide more realistic assumptions.
The results shown herein are consistent with those
reported for harvestmen, an arachnid group that has long
been recognized by the importance of species turnover shap-
ing its communities (Pinto-da-Rocha et al. 2005; Nogueira
et al. 2019a, b). This pattern has also been observed in spi-
ders from other parts of the world. For instance, even when
the beta-diversity was partitioned against a different set of
explanatory factors (turnover vs. species richness), the
­turnover was still the most dominant factor that explained
multiple site dissimilarities in island spider communities
(Wu et  al. 2017). Therefore, although the partition scheme
tested herein (turnover vs. nestedness) presents some short-
comings (see Almeida-Neto et al. 2012; Carvalho et al. 2012)
and analytical issues, our findings do not seem to be purely a
product of analytical bias.
The classification of the species composition map into 12
classes revealed that most breakouts in species composition
in the Atlantic Forest spider fauna are markedly latitudinal
(Fig. 7.5c). This is the same pattern as observed for harvest-
men, based on analyses using the same parameters and soft-
ware (see Nogueira et al. 2019a). It is important to emphasize
that none of these analyses recovered the NAF as delimited
herein, as a unique arachnid community. This result contra-
dicts evidences for plants, which recovered the uniqueness of
this region (e.g., Silva and Tabarelli 2000; Silva and Tabarelli
2001).
L. S. Carvalho et al.
4. Paraíba do Sul River mouth. Brazilian states highlighted: AL Alagoas,
BA Bahia, ES Espírito Santo, MG Minas Gerais, PB Paraíba, PE
Pernambuco, PR Paraná, RJ Rio de Janeiro, RN Rio Grande do Norte,
RS Rio Grande do Sul, SC Santa Catarina, SE Sergipe; and SP São
Paulo.
The spatial variation in species composition is subject to
assessment based on the bioclimatic layers used in the gener-
alized dissimilarity modeling  – GDM.  This modeling was
performed using as predictors the first five principal compo-
nents of the 19 WorldClim bioclimatic variables (Table 7.5).
Most of the temperature variables showed positive high cor-
relation to the first PC axis, while among the precipitation
variables, only the precipitation seasonality was similarly
important (Table 7.6). However, the percentage of deviance
explained by the GDM was 26.66%, a very weak result.
Therefore, the result of this analysis is not discussed herein.
Two factors may explain this result: (1) the quality of the
data used as input is insufficient, owing to the huge sampling
biases; and (2) the predictor variables are not enough to ade-
quately predict the spatial variation of spider communities in
the Atlantic Forest.
7.3.4 Areas of Endemism – AoE
The Atlantic Forest biota has been used several times to the
proposition of areas of endemism, including analyses based
on spiders (Oliveira et  al. 2015), harvestmen (Pinto-da-­
Rocha et al. 2005; DaSilva et al. 2015; DaSilva et al. 2016),
land planarians (Lago-Barcia et  al. 2020), orchid bees
(Garraffoni et al. 2017), passerine birds (Silva et al. 2004),
and for several taxa together (Sigrist and de Carvalho 2008;
Hoffmeister and Ferrari 2016), as previously discussed.
However, the data presented herein represent a significant
7  The Spider Fauna of the Northern Brazilian Atlantic Forest: Effect of Sampling Bias on Diversity Patterns and Conservation 115

Table 7.6  Eigenvectors of covariance factor of the principal components (PC) for the environmental layers used as predictor layers in the general-
ized dissimilarity modeling for Atlantic Forest spiders
Variables PC1 PC2 PC3 PC4 PC5
Mean temperature of coldest quarter 0.97 0.16 0.18 0.04 −0.01
Annual mean temperature 0.93 0.19 0.23 0.20 0.02
Min temperature of coldest month 0.89 0.38 0.19 −0.16 0.05
Mean temperature of driest quarter 0.80 0.37 0.29 0.04 −0.21
Mean temperature of warmest quarter 0.78 0.32 0.32 0.41 0.10
Mean temperature of wettest quarter 0.78 −0.04 0.15 0.33 0.34
Isothermality 0.77 −0.24 −0.16 −0.08 −0.50
Max temperature of warmest month 0.67 0.21 0.26 0.64 −0.04
Precipitation seasonality 0.63 −0.74 −0.08 −0.09 −0.05
Precipitation of wettest quarter 0.02 −0.77 0.59 −0.21 −0.05
Precipitation of wettest month 0.00 −0.77 0.58 −0.19 −0.09
Mean diurnal range −0.25 −0.55 −0.17 0.69 −0.36
Precipitation of warmest quarter −0.39 −0.71 0.42 0.08 0.27
Precipitation of coldest quarter −0.45 0.67 0.40 −0.14 −0.30
Temperature annual range −0.65 −0.33 −0.06 0.67 −0.09
Annual precipitation −0.70 0.02 0.69 −0.06 −0.09
Precipitation of driest quarter −0.75 0.59 0.25 0.07 −0.07
Precipitation of driest month −0.75 0.59 0.25 0.03 −0.05
Temperature seasonality −0.85 0.10 0.06 0.44 0.13
The selected PCs are those which the total cumulative percentage of total variation sum at least 95%. Variables are sorted in order of importance
for the first principal component

increase in the number of species and records in the northern
Atlantic Forest. Thus, to test if the newly gathered informa-
tion corroborates previous studies, a geographic interpola-
tion of endemism was carried out, using nine geographic
distribution classes, a larger set for the entire biome (25, 50,
100, 200, 400, 600, 800, 1000, and > 1000 km) and a smaller
for the NAF (10, 20, 30, 40, 50, 100, 200, 400, and > 400 km).
A total of 102 areas of endemism, supported by at least 2
syndemic species were observed throughout the Atlantic
Forest (Fig.  7.6a), including five observed in the NAF
(Fig. 7.6b). These areas of endemism are largely consistent
with the four major areas of endemism (Sul, Serra do Mar,
Bahia, and Nordeste), previously reported in the literature
(Silva et al. 2004; Pinto-da-Rocha et al. 2005; Sigrist and de
Carvalho 2008; Oliveira et  al. 2015; DaSilva et  al. 2015;
DaSilva et al. 2016; Hoffmeister and Ferrari 2016; Garraffoni
et al. 2017; Lago-Barcia et al. 2020).
The latitudinal distribution of the AoEs in the Atlantic
Forest exhibits at least four gaps or discontinuities, coinci-
dent with the São Francisco river (the southern limit of the
NAF; 1 in Fig. 7.6a), the Todos os Santos bay (2 in Fig. 7.6a),
the Doce River (3 in Fig. 7.6a), and the Paraíba do Sul river
(4 in Fig. 7.6a). These regions might reflect areas with long-­
term climatic instability, which could have acted as dispersal
barriers during past glaciation periods (Oliveira et al. 2015;
DaSilva et  al. 2016). Different spider communities shown
herein between these unstable climatic regions are in agree-
ment with previous predictions based on climatic variability
data (Carnaval et al. 2009; Carnaval et al. 2014; Costa et al.
2018). Although rivers have been considered as potential
barriers for a very long time (e.g., Wallace 1852), there are
divergent results on their effect as a physical barrier to
Atlantic Forest taxa (e.g., Pellegrino et al. 2005; Thomé et al.
2014). For Amazon birds, a more complex scenario has been
proposed, in which rivers act as a barrier for certain species,
but not for all (Oliveira et al. 2017c). The present results are
based on the distribution records of orb-weavers and pholcid
spiders, which should not be considered poor dispersal taxa
(e.g., Bell et  al. 2005). Therefore, we hypothesize that the
areas of endemism and the breaks in spider species composi-
tion shown herein are likely to corroborate a climate-­
physiological constraints scenario, rather than a
river-associated vicariance (Carnaval et al. 2014).
The most important NAF AoEs are coincident with areas
with higher density of records (Fig.  7.4b) and species
(Fig. 7.4d): the brejo de altitude in the municipality of Bonito
and the Estação Ecológica de Murici. These areas are sup-
ported by a small number of syndemics (2–17 at each AoE),
as expected owing to the low spider species richness recorded
for this region of the NAF (70 spp.). Although these AoEs
have been reported in other studies (e.g., Oliveira et al. 2015;
DaSilva et al. 2016), it is not possible to rule out the possibil-
ity that both areas (or their limits) are actually a result of
sampling deficiency outside those specific localities. In fact,
it has been suggested before that AoEs coincide with highly
sampled localities (Nelson et al. 1990; Schulman et al. 2007).
The NAF AoEs delimited for Araneoidea and Pholcidae spi-
ders are located within an area that showed a unique set of
116
species in this region (e.g., Fig. 7.5f). This suggests that the
existence of these AoEs might be due to the evolutionary his-
tory of the lineages that occupy this region, as observed for
harvestmen (Nogueira et al. 2019b) and supported by biome
stability in the region (Costa et al. 2018). However, the sam-
pling bias exists, and it influences the limits of the NAF
AoEs, owing to a huge Wallacean shortfall. This shortfall
directly delimits two AoEs, one based only on two species
endemic to the NAF and known only by their types
(Eurymorion murici and Thymoites murici), and another
based on a species endemic to the NAF and known only by
its types (Spilasma baptistai) and a species nonendemic to
the NAF (Kambiwa neotropica).
We also estimated the weighted endemism (i.e., the spe-
cies richness inversely weighted by species ranges, Daru
et al. 2020) for the whole Atlantic Forest and the NAF. This
exploratory analysis aimed to describe areas with a higher
number of species with restricted distribution, an interesting
parameter for defining conservation priorities (e.g., Oliveira
et al. 2017b). The results for this metric should be interpreted
carefully, owing to the Wallacean shortfall evidenced and
described above. A contrasting pattern for the entire Atlantic
Forest and its northern region was observed. The interpo-
lated weighted endemism revealed several spots with higher
values (Fig.  7.6c) northern from the Doce River (3  in
Fig. 7.6a), in the states of Bahia and Pernambuco. Southern
from the Doce River, in the state of Espírito Santo (ES in
Fig.  7.6c), there is an area with high density of weighted
endemism. In most other regions in southeastern and south-
ern Brazil, the areas with higher number of records (Fig. 7.4a)
and species (Fig. 7.4c), revealed a lower density of weighted
endemism (Fig.  7.6c). If this same analysis is conducted
using only the data for the Northern Atlantic Forest, how-
ever, the weighted endemism pattern (Fig.  7.6d) is almost
identical to the species richness pattern (Fig.  7.4d). We
believe that this particular result is highly influenced by the
sampling bias (e.g., low number of records and species in the
region). In fact, the weighted endemism is weakly negatively
correlated with both the sampling effort and the species rich-
ness (Table 7.4). Nevertheless, the preliminary results shown
here reinforce the revision of conservation priorities in NAF
and select the as-of-yet unprotected patches of Atlantic
Forest that maximizes conservation efforts in the region.
7.4 Directions for the Study of the NAF
Spider Fauna
The observed complex diversity and distribution patterns for
the Atlantic Forest spiders are outcomes of their evolutionary
history in this biome. However, as emphasized in the present
contribution, this knowledge is directly affected by sampling
biases and the correlated biodiversity shortfalls. The Northern
L. S. Carvalho et al.
Atlantic Forest represents a unique region, with contrasting
diversity patterns, when compared to the remaining parts of
the biome. However, a clear understanding of these patterns
is far from being considered robust. As such, five goals
should be prioritized, aiming to provide a better knowledge
of the Northern Atlantic Forest spider fauna:
1. Decrease the concentration of records in a few localities.
As shown (Fig. 7.4b), the highest densities of records are
located closer to larger cities or to historically more sam-
pled conservation units, thus generating a highly concen-
trated distribution of the spider records in the
NAF. Therefore, studies aiming to conduce spider species
inventories at poorly sampled areas should be encour-
aged, which will directly contribute to decreasing this
Wallacean shortfall. The maps provided in the present
chapter (e.g., Fig. 7.4) can be used for the delimitation of
priority areas for spider sampling, in the future.
Considering the high endemism levels showed herein,
surveys performed in poorly sampled areas are likely to
reveal a unique set of species, with several new occur-
rences, and undescribed taxa.
2. Decrease the large number of undescribed taxa. The NAF
spider fauna has historically been neglected in taxonomic
studies, as exemplified by the considerable number of
endemic species that have only recently (< 7 years ago)
been described (11 out of 19 endemics) and the existence
of hitherto undescribed taxa (e.g., Kambiwa, Metagonia
and Litoporus, Table 7.3). Besides, the published species
inventories from localities at the NAF suggest that a huge
portion of this biota is hitherto to be described or belong
to taxa that have not been the subject of taxonomic revi-
sion for such a long time (e.g., Psilochorus), thus impos-
sible to be recognized. These factors evidence the
significant Linnean shortfall regarding this spider fauna.
3. Evaluate the species limits of highly variable or widely
distributed taxa. The existence of morphological varia-
tion associated with a large geographic distribution is a
promising starting point for phylogeography studies
based on molecular data, or morphological studies using
geometric morphometrics, both aiming to test the species
limits. These studies might confirm or refute the species
delimitation for some taxa, providing robust evidence on
the validity of the species that occur in the region.
4. Provide conservation profiles of NAF spider fauna and
propose conservation plans, when necessary. None of the
spider species recorded from the Northern Atlantic Forest
has ever had its threat status accessed. While some poorly
known taxa are likely to be recognized as data deficient
(e.g., Psilochorus taperae), most nonendemic taxa might
be categorized as of least concern (e.g., Micrathena sch-
reibersi and Saciperere catuaba). However, species with
restricted distribution (e.g., Carapoia abdita Huber,
2016, Carapoia agilis, Huber 2018 and Carapoia bispina,
7  The Spider Fauna of the Northern Brazilian Atlantic Forest: Effect of Sampling Bias on Diversity Patterns and Conservation
Huber 2018), which have not been recorded from any
conservation unit, are likely to be threatened to extinction
and require a detailed threat assessment.
7.5 Conclusion
In the present chapter, we provide a comprehensive revision
of the diversity and distribution patterns of the Araneoidea
and Pholcidae spiders of the Northern Atlantic Forest. This
fauna is known only from 212 records of 70 species. Many
species of other spider taxa were not treated in this chapter,
and a significant portion of this fauna is yet to be described.
Herein, we presented evidence of wide biodiversity short-
falls regarding the spider fauna from the most northern por-
tion of the Atlantic Forest biome, in northeastern Brazil.
These effects include a small number of records, clumped in
a few localities. However, the comparison with the informa-
tion for the entire Atlantic Forest allowed us to notice that the
NAF spider fauna presents a higher than previously reported
endemism level. While this fauna has been historically
neglected, this emphasizes the urgent need for scientific
research, to allow a proper recognition and conservation of
this unique fauna.
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 Termites from the Northern Atlantic
Forest, Brazil: Ecology and Conservation 8
Alexandre Vasconcellos, Eliana Marques Cancello,
Flávia Maria da Silva Moura, Joice Paulo Constantini,
Matilde Vasconcelos Ernesto, Alane Ayana Vieira de
Oliveira Couto, and Antônio Carvalho da Silva Neto

Abstract both in monocultures and in forest fragments inserted into

The Northern Atlantic Forest (NAF) is located north of the
São Francisco River, encompassing the Brazilian states of
Rio Grande do Norte, Paraíba, Pernambuco and Alagoas.
The NAF is an endemism hotspot and is extremely threat-
ened, with only 5.4% of its original coverage remaining,
considering the 90  m edge influence, and almost half of
the forest fragments comprising less than 1 ha. Seventy-
four termite species have been registered in the
NAF. Historical factors, such as a more recent past con-
nection with the Amazon Forest, and ecological factors,
such as a lower thermal amplitude compared to other areas
in this biome, can act as modulating agents for termite
communities in the NAF. Only three species can be con-
sidered as pests in the urban environment and one in sug-
arcane monocultures. Twelve termite species build
conspicuous nests, with an estimated average density of 56
nests/ha for the set of NAF areas, ranging from 5 to 157
nests/ha. The density of individuals varied from 1798 to
5662/m2, corresponding to a live biomass of 3.8–13.2 g/
m2. Of the areas where the termites were sampled, some
demonstrated an increased potential for the conservation
of NAF biodiversity. The adequate management of agri-
cultural landscapes, such as sugarcane monoculture plan-
tations, can mitigate negative effects on termite populations,
A. Vasconcellos (*) · M. V. Ernesto · A. C. da Silva Neto
Laboratório de Termitologia, Departamento de Sistemática e
Ecologia, CCEN, Universidade Federal da Paraíba, Paraíba, Brazil
e-mail: avasconcellos@dse.ufpb.br
E. M. Cancello · J. P. Constantini
Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil
F. M. da Silva Moura
Laboratório de Pesquisa em Ensino, Zoologia e Conservação,
CSTR, Universidade Federal de Campina Grande, Paraíba, Brazil
A. A. V. de Oliveira Couto
Estação Experimental de Cana-de-açúcar do Carpina, Universidade
Federal Rural de Pernambuco, Pernambuco, Brazil
the matrix. The increased biomass suggests that termites in
the NAF play an active role in key-­ecological processes,
such as plant necromass decomposition and soil bioturba-
tion, in addition to influencing populations of other organ-
isms, whether as a food resource or as influencing agents
on the spatial heterogeneity of the ecosystem.
Keywords
Biogeography · Density · Diversity · Isoptera ·
Neotropical Region · Pests
8.1 Introduction
Termites are dominant arthropods in tropical ecosystems
around the world, especially in terms of biomass (Bignell
and Eggleton 2000). The global dry biomass of termites has
been estimated as 50 Mt., which is slightly lower than human
biomass (60 Mt) (Tuma et al. 2020). Depending on the eco-
system, they can account for 40% to 65% of the overall bio-
mass of soil macrofauna and approximately 80% of the
invertebrate biomass in decomposing trunks (Wood and
Sands 1978; Bandeira and Torres 1985). Termites compose a
monophyletic group, comprising 3171 described species,
and are currently placed in the order Blattaria and infraorder
Isoptera (Constantino 2022). It is estimated that the actual
number of species and genera can reach up to 5000 and 700,
respectively (Constantino 2018). The families Kalotermitidae,
Rhinotermitidae, Serritermitidae, Stolotermitidae and
Termitidae occur in the Neotropical region, accounting for
108 genera and 615 species. In Brazil, only the first three
families and Termitidae have been registered, comprising
349 species (Constantino 2022).
At a regional and global scale, termite distribution can be
influenced by a set of spatial, environmental and historical
factors, which can act in an isolated manner or synergisti-

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 121
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_8
122
cally, including latitude, longitude, altitude, distance, paleo-
climatic stability, rainfall and temperature (Eggleton et  al.
1994; Gathorne-Hardy et al. 2001; Palin et al. 2011; Cancello
et  al. 2014; Dambros et  al. 2017; Cunha et  al. 2018). At a
local scale, communities may respond to soil depth and
physical and chemical composition, interspecific interac-
tions (competition and predation), canopy height and habitat
disturbance, both anthropogenic and natural (Lee and Wood
1971; Abe and Darlington 1985; Bandeira and Vasconcellos
2002; Davies et al. 2003; Roisin et al. 2006; Dambros et al.
2016).
Termite colonies are composed of individuals distributed
into castes (e.g. reproductive, soldiers and workers) which
have distinct morphologies and functions (Roisin 2000).
Small dry branches in the forest canopy, at heights of over
20 m, and miniscule tunnels in the ground, reaching depths
of up to 70 m, can house individuals of a colony (Lee and
Wood 1971; Roisin et al. 2006). A striking consequence of
termite colonial life is the construction of nests in order to
house reproductive castes and their offspring, which can vary
from tens to millions of individuals (Emerson 1938). In gen-
eral, nests are classified based on their structural characteris-
tics, including the type of material used and the location of
construction, and how individuals of a colony relate to them.
We can observe four nest models (Noirot 1970; Abe 1987;
Shellman-Reeve 1997): (i) “one-piece-type” (nest in wood)
where termites live confined within their nutritional source,
with the size and longevity of the colony being severely
affected by the size of the piece of wood; (ii) “intermediate
type”, constructed inside wood, which is also used as food,
however individuals of the colony can forage outside the nest
and construct accessory structures, such as galleries and tun-
nels, connecting the nest to sources of supplementary
resources; (iii) “separate type”, constructed in microhabitats
other than inside wood, such as the surface or profile of soils
or on live or dead trees. In these cases, nests can be known as
epigeal, subterranean or arboreal; and (iv) “inquiline-type”,
constructed within the nests of other termite species, gener-
ally in epigeal or arboreal nests. In the Neotropical region,
the nests of Cornitermes spp. and Constrictotermes spp. can
house several other termite species, including inquiline spe-
cies that are highly specialised for this lifestyle, such as
Serritermes serrifer and Inquilinitermes spp.
The construction of nests and the complex network of gal-
leries and tunnels promote marked alterations in the chemi-
cal, physical and hydraulic properties of the soil, as well as
considerably increasing the spatial heterogeneity of the eco-
system with direct and indirect positive effects on the main-
tenance of populations of organisms belonging to different
trophic groups (Lee and Wood 1971; Wood and Sands 1978;
Jones et al. 1994; Jouquet et al. 2016). Invertebrates that can
be affected by termite constructions include, among others,
ants, bees, mites, springtails, wasps, spiders, centipedes,
beetles and scorpions (Kistner 1969; Domingos 1985). It is
A. Vasconcellos et al.
even possible to observe some vertebrates, such as birds, liz-
ards, snakes, bats and rats, using nests as refuges and repro-
duction or predation sites. Termite activities aid in water
retention and the maintenance of nutrient flow in the soil
throughout the year, affecting the survival of plants and
microbial activity and, consequently, mitigating the negative
effects of prolonged droughts in humid tropical forests on
primary productivity and indirectly on secondary productiv-
ity (Ashton et al. 2019).
Termites feed on a diverse range of resources, including
live and dead wood, leaf litter, roots, humus, herbivore dung,
microepiphytes, fungi, dry grass and animal corpses (Wood
1978; Noirot 1992). Wood consumption is characterised by a
food preference gradient ranging from live wood to wood in
advanced stages of decomposition mixed with soil. The
humidification gradient of consumed substrates is one of the
factors responsible for the segregation of feeding niches
among species in a community (Donovan et  al. 2001;
Bourguignon et al. 2009). Termites are among a select group
of insects capable of digesting and assimilating products that
breakdown cellulose, due to morphological specialisations
present in their mouthparts and digestive tubes, and physio-
logical specialisations such as the production of their own
enzymes, presence of a pH gradient along the digestive tube
and an association with a diverse community of symbiotic
microorganisms (flagellated eukaryotes, bacteria and
archaea) (Brune 2014; Bourguignon et  al. 2018). These
insects can consume 14% to 50% of the annual plant necro-
mass production, reaching values of over 80% in some arid
and semi-arid ecosystems (Wood and Sands 1978; Ohiagu
and Wood 1979).
The functional relevance of termites is directly related to
their biomass, nutritional ecology, foraging behaviour and
construction of biogenic structures (e.g. nests and subterra-
nean tunnels) in ecosystems. Furthermore, apterous and
alates are prey for many taxa, exerting influence on higher
trophic levels (Deligne et  al. 1981; Silva et  al. 2021). As
such, a broad and multidimensional view of these aspects
naturally places termites among the greatest decomposers of
plant necromass and ecosystem engineers at a global scale,
having a direct and indirect influence on biodiversity and key
ecosystem processes, such as energy and nutrient flow and
primary and secondary productivity.
8.2 The Northern Atlantic Forest
and the “Brejos de Altitude”
The Atlantic Forest is the second largest humid forest com-
plex in South America and is currently isolated from the
Amazon and Andean Forests by a corridor of open or semi-­
open formations, including the Caatinga, Cerrado and Chaco
(Ab’Saber 1977; Santos et al. 2007). Originally, the Atlantic
Forest covered an estimated area of 1.6 million km2 (18% of
8  Termites from the Northern Atlantic Forest, Brazil: Ecology and Conservation
Brazilian territory), extending as a coastal strip for over
3000  km between the Brazilian states of Rio Grande do
Norte (5°S) and Rio Grande do Sul (30°S) and reaching
other more western Brazilian states, such as Goiás and Mato
Grosso do Sul and other South American countries, such as
Argentina and Paraguay (Morellato and Haddad 2000;
Marques et al. 2021). Throughout its extension, the Atlantic
Forest presents great altitudinal variation (0–3000  m) and
soil and climate diversity, as well as a complex of associated
ecosystems such as mangroves, “restingas” (sand forests),
dunes and mountain grasslands (Marques et al. 2021).
From the beginning of European colonisation, over
500 years ago, the Atlantic Forest has been severely defor-
ested throughout its extension for timber extraction, charcoal
production, agriculture, pastures and city construction
(Morellato and Haddad 2000). It is estimated that between
11% and 16% of the original coverage remains, with the size
of most fragments covering less than 50 ha and presenting
elevated levels of human interference (Ribeiro et  al. 2009;
Lima et al. 2020). The situation is even more alarming in the
northern region of the biome, located north of the São
Francisco River. In this sector, known as the Northern
Atlantic Forest (NAF), a large part of the Atlantic Forest was
converted into sugarcane monocultures and areas for urban
expansion, with only 5.4% of its original coverage remain-
ing, considering the 90  m edge influence (Almeida and
Souza this volume). The NAF is the most threatened sector
of the Atlantic Forest; however, it still houses several endemic
and threatened taxa (Araujo et al. this volume; DeSouza and
DaSilva this volume; Vieira et al. this volume).
Within the limits of the NAF or associated with the east-
ern side of the Borborema Plateau, there are “islands” of
humid forest, known locally as “Brejos de Altitude” or
“Brejos Nordestinos”. These areas are associated with the
plateaus at altitudes of over 500 m and experience the effects
of orographic rainfall (Andrade-Lima 1982; Rodal et  al.
2008). The majority of “Brejos de Altitude” are found within
the Borborema Plateau domain, which occurs between the
Brazilian states of Rio Grande do Norte and Alagoas. Some
authors consider the “Brejos de Altitude” as old members of
the vegetational complex that connected the Amazon and the
Atlantic Forest (Vivo 1997; Costa 2003; Santos et al. 2007).
In this chapter, the “Brejos de Altitude” located on the east-
ern side of the Borborema Plateau is considered as part of the
NAF (Fig. 8.1).
A set of historical and ecological processes are involved
in the patterns of diversity and endemism observed in the
Atlantic Forest. Climate change during the Late Quaternary
appears to have altered the distribution of the Biome, creat-
ing a large central forest corridor in the state of Bahia and
another smaller one north of the São Francisco River, where
the NAF is currently located. Additionally, micro-refuges
were created on mountain tops in the south-eastern and
southern regions, coinciding with the diversity patterns of
123
several taxa (Carnaval and Moritz 2008; Carnaval et  al.
2014). The Rio Doce Valley region (19°S) also represents an
important sector of species turnover, which can be connected
to the topographic barrier of the region and ecophysiological
restrictions related to variations in temperature and precipita-
tion (Costa et al. 2000; Saiter et al. 2016). Other factors such
as marine transgressions and regressions and the connection
routes with the Amazon Forest, may also influence the biota
throughout the Atlantic Forest (Bigarella 1975).
The connection between the two largest blocks of humid
forests in South America has been suggested by several
authors (Andrade-Lima 1982; Costa 2003; Wang et al. 2004).
There are at least three possible past connection routes
between the Amazon Forest and the Atlantic Forest (Batalha-­
Filho et al. 2013). The first is through the southern region of
the Cerrado and the Brazilian state of Mato Grosso and the
transition towards the Chaco and palm savannas of Bolivia
and Paraguay (old connections  – middle to late Miocene).
The second is through the central region of the north-eastern
Cerrado and Caatinga, through the galley forests (young
connections – Pliocene and Pleistocene). Finally, the third is
along the coastal zone of the north-eastern states of Rio
Grande do Norte, Ceará, Piauí and Maranhão. There is strong
evidence that at the beginning of European colonisation, the
coast of the Atlantic Forest extended to the mouth of the
Amazon River, forming a vast Atlantic biome, which also
included the gallery forests which penetrated the interior of
the Caatinga and Cerrado. Thus, it is possible that a rela-
tively short time ago there was a certain continuity in the
distribution of some taxa between these biomes, especially
in the region where the NAF is found (Coimbra-Filho and
Câmara 1996).
8.3 Local and Regional Termite Diversity
in the NAF
The first list of termite species in the NAF was published by
Bandeira et al. (1998). Forty-three morphospecies were reg-
istered in 0.4 ha of fragments inserted into the urban matrix
along the cost of the Brazilian state of Paraíba. Previous
taxonomic studies have individually registered some species
in the NAF (e.g. Krishna and Araujo 1968; Constantino
1995). Currently, there are approximately 4000 termite sam-
ples deposited in the Isoptera Collection at the Federal
University of Paraíba (CIUFPB), originated from a diversity
of ecosystems comprising the Atlantic Forest Complex of the
NAF, including the “Brejos de Altitude” on the eastern side
of the Borborema Plateau, semi-deciduous forests, “restin-
gas”, and mangroves. Additionally, there is a relevant num-
ber of NAF samples deposited in the Museum of Zoology at
the University of São Paulo (MZUSP).
We registered 74 termite species in the NAF (Table 8.1),
originating from the databank of the CIUFPB, collected
124
Fig. 8.1 (a) Locations with termite samples in the Northern Atlantic
Forest; (b) Species richness and (c) sampling effort based on kernel
interpolation. (1) Natal, (2) Parnamirim, (3) Nísia Floresta, (4) Timbau
do Sul, (5) Mataraca, (6) Mamanguape, (7) Cabedelo, (8) João Pessoa,
(9) Santa Rita, (10) Sapé, (11) Areia, (12) Igarassu, (13) Recife, (14)
Ipojuca, (15) Tamandaré, (16) Natuba, (17) São Vicente Ferrer, 18)
Taquaritinga do Norte, 19) Brejo da Madre de Deus, 20) Bezerros, 21)
Bonito, 22) Caruaru, 23) Ibateguara, 24) Murici, 25) Quebrangulo. The
shapefile used to delimit the NAF is formed by areas north of the São
from 25 locations (Fig. 8.1), and composed from the taxo-
nomic and ecological studies published (Krishna and Araujo
1968; Constantino 1995; Bandeira et  al. 1998, 2003; Silva
and Bandeira 1999; Rocha and Cancello 2009, 2020;
Vasconcellos 2010; Souza et al. 2012; Cancello et al. 2014;
Ernesto et  al. 2014; Acioli and Constantino 2015; Oliveira
and Constantino 2016; Couto et al. 2019; Silva et al. 2019;
Feitosa et  al. 2021). In the complex of ecosystems that
­comprise the Brazilian Atlantic Forest, 151 species were reg-
istered belonging to Kalotermitidae, Rhinotermitidae and
Termitidae (Feitosa et al. 2021). Based on the species regis-
tered in this study for the NAF, 16 are newly registered for
the Brazilian Atlantic Forest. The elevated number of unde-
termined samples of the subfamily Apicotermitinae and the
low effectiveness of the sampling methods for accessing
Kalotermitidae colonies in tree canopies, suggest that the
actual species richness in the NAF may be greater. Using
external and internal morphology for the analysis of 247
samples of Apicotermitinae from the “Refúgio de Vida
Silvestre Mata do Buraquinho” (S07o08′41″ and W34o51′40″),
only eight species were determined, about 50% of the mor-
phospecies recorded for the subfamily (unpublished data)
A. Vasconcellos et al.
Francisco River’s northernmost limit, encompassing the entire Atlantic
Forest biome in the north-eastern Brazilian states of Alagoas,
Pernambuco, Paraíba and Rio Grande do Norte. For this shapefile, we
added the areas of some municipalities that present “Brejos de Altitude”,
located in the states of Paraíba (municipalities of Alagoa Grande,
Alagoa Nova, Araruna, Areia and Bananeiras) and Pernambuco (munic-
ipalities of Agrestina, Bezerros, Bonito, Brejo  da Madre de Deus,
Camocim de São Felix, Caruaru, Gravatá, São Vicente Férrer and
Taquaritinga)
(some species in Fig. 8.2). In addition, observing the records
of Kalotermitidae alates, captured using light traps, also in
the Refúgio de Vida Silvestre Mata do Buraquinho, was pos-
sible to observe that conventional sampling methods were
only able to access a portion of the actual species richness in
tropical humid forests (Medeiros et al. 1999).
In NAF locations where more than 50 samples were col-
lected, species richness varied from 11 to 56/location, where
the greatest values were registered for the “Refúgio de Vida
Silvestre Mata do Buraquinho” (56 spp.) in the state of
Paraíba, forest fragments of the “Usina São José” (54 spp.)
(S07o49′07″ and W35o00′45″) in the state of Pernambuco,
and the “Estação Ecológica de Murici-ESEC” (53 spp.)
(S09o14′10″ and W35o47′17″) in the state of Alagoas. Over
2000 samples were collected in the first two areas, whereas
in the third area, only 250 were collected. Thus, the ESEC
Murici may represent an important area for the conservation
of termite biodiversity within the NAF, as previously indi-
cated for other taxa such as amphibians and birds (Araujo
et al. this volume; Vieira et al. this volume). In addition to the
areas mentioned above, other areas also have an elevated
conservation potential, whether due to the composition of
8  Termites from the Northern Atlantic Forest, Brazil: Ecology and Conservation 125

Table 8.1  List of termite species occurring in the Brazilian Northern Atlantic Forest, including the Brazilian states of Alagoas (AL), Paraíba (PB),
Pernambuco (PE) and Rio Grande do Norte (RN)
Species Distribution Source
KALOTERMITIDAE
Calcaritermes rioensis Krishna 1962 AL, PB, PE RPL; CIUFPB
Cryptotermes brevis (Walker 1853) (*) PB, PE RPL; CIUFPB
Cryptotermes dudleyi Banks 1918 (*) PB, PE, RN RPL; CIUFPB
Glyptotermes sicki Krishna & Emerson 1962 AL, PB, PE CIUFPB
Glyptotermes sp. PE CIUFPB
Eucryptotermes hagenii (Müller 1873) PE CIUFPB
Neotermes paraensis (Costa-Lima 1942) PE RPL; CIUFPB
Neotermes zanclus Oliveira 1979 PB, PE CIUFPB
Rugitermes sp. PE CIUFPB
Tauritermes bandeirai Scheffrahn & Vasconcellos 2020 PB, PE RPL; CIUFPB
RHINOTERMITIDAE
Acorhinotermes subfusciceps (Emerson 1925) PE CIUFPB
Coptotermes gestroi (Wasmann 1896) (*) PE RPL; CIUFPB
Coptotermes testaceus (Linnaeus 1758) AL, PB, PE RPL; CIUFPB
Heterotermes longiceps (Snyder 1924) AL, PB, PE, RN RPL; CIUFPB
Heterotermes sulcatus Mathews 1977 PB, PE RPL; CIUFPB
Heterotermes tenuis (Hagen 1858) PE RPL; CIUFPB
Rhinotermes hispidus Emerson 1925 AL, PE RPL; CIUFPB
Rhinotermes marginalis (Linnaeus 1758) AL, PB, PE RPL; CIUFPB
TERMITIDAE
APICOTERMITINAE
Anoplotermes banksi Emerson 1925 AL, PB, PE RPL; CIUFPB
Anoplotermes meridianus Emerson 1925 AL, PB, PE RPL; CIUFPB
Anoplotermes sp. AL, PB, PE CIUFPB
Aparatermes sp. AL, PB, PE CIUFPB
Grigiotermes hageni (Snyder & Emerson 1949) AL, PB, PE RPL; CIUFPB
Humutermes krishnai (Bourguignon & Roisin 2016) AL, PB RPL; CIUFPB
Hydrecotermes sp. AL, PB, PE RPL; CIUFPB
Longustitermes manni (Snyder 1922) AL, PB RPL; CIUFPB
Ruptitermes bandeirai Acioli & Constantino 2015 AL RPL; CIUFPB
Ruptitermes reconditus (Silvestri 1901) AL, PB, PE RPL; CIUFPB
Rustitermes boteroi Constantini, Castro & Scheffrahn 2020 AL, PB, PE RPL; CIUFPB
NASUTITERMITINAE
Araujotermes sp. AL, PE CIUFPB
Atlantitermes stercophilus Constantino & DeSouza 1997 AL, PB, PE RPL; CIUFPB
Convexitermes manni (Emerson 1925) PB RPL; CIUFPB
Diversitermes diversimiles (Silvestri 1901) AL, PB, PE, RN RPL; CIUFPB
Nasutitermes callimorphus Mathews 1977 AL, PB, PE, RN RPL; CIUFPB
Nasutitermes corniger (Motschulsky 1855) AL, PB, PE, RN RPL; CIUFPB
Nasutitermes coxipoensis (Holmgren 1910) PB, PE CIUFPB
Nasutitermes ehrhardti (Holmgren 1910) PE RPL
Nasutitermes ephratae (Holmgren 1910) AL, PB, PE RPL; CIUFPB
Nasutitermes gaigei Emerson 1925 AL, PB, PE RPL; CIUFPB
Nasutitermes jaraguae (Holmgren 1910) AL, PB, PE, RN RPL; CIUFPB
Nasutitermes kemneri Snyder & Emerson 1949 PB RPL; CIUFPB
Nasutitermes macrocephalus (Silvestri 1903) PB, PE, RN RPL; CIUFPB
Nasutitermes obscurus (Holmgren 1910) PB, PE RPL; CIUFPB
Nasutitermes rotundatus (Holmgren 1906) AL, PE RPL; CIUFPB
Nasutitermes unduliceps Mathews 1977 PB, PE CIUFPB
Subulitermes baileyi (Emerson 1925) AL, PB, PE RPL; CIUFPB
Velocitermes aporeticus (Mathews 1977) AL, PB, PE, RN RPL; CIUFPB
(continued)
126 A. Vasconcellos et al.

Table 8.1 (continued)
Species Distribution Source
SYNTERMITINAE
Embiratermes neotenicus (Holmgren 1906) AL, PB, PE RPL; CIUFPB
Ibitermes curupira Fontes 1985 AL RPL; CIUFPB
Ibitermes inflatus Vasconcellos 2002 PB, PE RPL; CIUFPB
Labiotermes labralis (Holmgren 1906) AL, PB, PE, RN RPL; CIUFPB
Silvestritermes heyeri Wasmann 1915 AL, PB, PE, RN RPL; CIUFPB
Syntermes grandis (Rambur 1842) PB, PE RPL; CIUFPB
Syntermes molestus (Burmeister 1839) PE RPL; CIUFPB
Syntermes nanus Constantino 1995 AL, PB, PE, RN RPL; CIUFPB
Vaninitermes ignotus (Constantino 1991) AL, PB, PE RPL; CIUFPB
TERMITINAE
Amitermes amifer Silvestri 1901 AL, PE RPL; CIUFPB
Amitermes aporema Constantino 1993 PB, PE RPL; CIUFPB
Amitermes bandeirai Rocha & Cancello 2020 AL, PB, PE, RN RPL; CIUFPB
Cavitermes tuberosus (Emerson 1925) AL, PB, PE RPL; CIUFPB
Cylindrotermes sapiranga Rocha & Cancello 2007 AL, PB, PE, RN RPL; CIUFPB
Dentispicotermes sp. AL, PB, PE CIUFPB
Dihoplotermes inusitatus Araujo 1961 AL, PE RPL; CIUFPB
Microcerotermes indistinctus Mathews 1977 AL, PB, PE, RN RPL; CIUFPB
Microcerotermes strunckii (Sörensen 1884) AL, PB, PE RPL; CIUFPB
Neocapritermes guyana Krishna & Araujo 1968 PE RPL; CIUFPB
Neocapritermes opacus (Hagen 1858) AL, PB, PE, RN RPL; CIUFPB
Neocapritermes talpa (Holmgren 1906) AL, PE CIUFPB
Neocapritermes talpoides Krishna & Araujo 1968 PB, PE RPL; CIUFPB
Orthognathotermes longilamina Rocha & Cancello 2009 AL, PB, PE RPL; CIUFPB
Orthognathotermes tubesauassu Rocha & Cancello 2009 PB, PE RPL; CIUFPB
Termes hispaniolae (Banks 1918) PB RPL; CIUFPB
Termes medioculatus Emerson 1949 AL, PB, PE, RN RPL; CIUFPB
Termes fatalis Linnaeus 1758 PB RPL; CIUFPB
Source: RPL records published in the literature, CIUFPB records from the Isoptera Collection of the Federal University of Paraíba. Species in bold
are new records for the Atlantic Forest based on Feitosa et al. (2021). (*) Exotic species

their communities (species richness, biomass, abundance
and feeding groups) or because they have species that are
only shared with the Amazon forest, such as the “Reserva
Biológica de Pedra Talhada” (S09o13′41″ and W36o25′43″)
and forest fragments in the “Usina Serra Grande” (S08o30′00″
and W35o52′00″) in the state of Alagoas; “Parque Ecológico
Municipal João Vasconcelos Sobrinho” (S08o21′43″ and
W36o01′45″), “Reserva Ecológica Mata do Mucuri”
(S08o30′00″ and W35o43′00″) and the “Reserva Municipal
Mata do Estado” (S07o37′00″ and W35o30′00″) in
Pernambuco; the “Reserva Ecológica Estadual Mata do Pau-­
Ferro” (S06o58′00″ and W35o44′00″) and “Reserva Biológica
Guaribas” (S06o43′00″ and W35o10′50″) in the state of
Paraíba.
8.4 Historical, Ecological
and Anthropogenic Determinants
of Termite Diversity in the NAF
Although the NAF represents the most threatened sector in
the Atlantic Forest, with the lowest remaining vegetation cov-
erage, it still houses approximately 50% of the termite species
registered in this biome (Cancello et al. 2014; Feitosa et al.
2021; Lins-e-Silva et al. 2021; Almeida and Souza this vol-
ume). With the current level of taxonomic knowledge, there is
no record of species endemic to the NAF. On the other hand,
this sector only shares species with the Amazon Forest,
including Acorhiotermes subfuscipes, Neocapritermes tal-
poides, Rhinotermes hispidus, R. marginalis and Nasutitermes
gaigei. A more recent past connection with the Amazon
Forest (Pliocene and Pleistocene), through more mesic
regions and gallery forests in the Caatinga and Cerrado and
through a coastal arc north of the Amazon River mouth, may
explain this sharing of species (Coimbra-Filho and Câmara
1996; Batalha-Filho et  al. 2013). Acorhinotermes, a genus
with two described species only found in the Amazon Forest,
was registered in two small fragments located in areas of the
“Brejos de Altitude” in the NAF, reinforcing the hypothesis of
a more recent historical northern connection between the two
largest blocks of humid forests in South America.
From an ecological perspective, the variation in climatic
elements throughout the Atlantic Forest is also a predictive
factor of termite species richness and abundance. At 15 sam-
pling points, distributed across 20 latitudinal degrees (from
the city of João Pessoa/Paraíba  – 07° to Blumenau/Santa
8  Termites from the Northern Atlantic Forest, Brazil: Ecology and Conservation 127

Fig. 8.2  Some termite species of the subfamily Apicotermitinae found (t), Rustitermes boteroi. Figs. (d), (e), (i), (j), (n), (o), (s) and (t) repre-
in the Brazilian Northern Atlantic Forest. (a)–(e) Anoplotermes banksi; sent the enteric valves. Scale: 1 mm
(f)–(j), Grigiotermes hageni; (k)–(o), Humutermes krishnai; and (p)–
128
Catarina  – 27°), termite species richness and abundance
were negatively related to latitude, where thermal amplitude
and evapotranspiration potential were the main predictors of
this variation within communities (Cancello et  al. 2014).
The direct effects of temperature on termite distribution at a
regional scale are unknown, but ecophysiological limita-
tions connected to foraging and nesting behaviours or sym-
biotic microbial activity may underlie variations in species
composition and feeding groups along latitudinal or altitudi-
nal gradients. On the other hand, in the NAF region, below
7° latitudinal, species richness and abundance decrease,
which may at first, appear contradictory to the results found
by Cancello et  al. (2014). However, in this NAF region,
there is a strong influence of marine transgressions and
regressions that occurred in the Quaternary (Bigarella
1975), which were responsible for the formation of sandy
soil with a low water and nutrient retention capacity and had
a direct effect on the establishment of lowland semi-­
deciduous forests. In general, sandy soil provides less sta-
bility for the construction of subterranean termite tunnels
and nests (Lee and Wood 1971).
Thus, as with other tropical forests around the world,
soil type and regeneration time following anthropogenic
disturbances affect the NAF termite communities, with the
strongest effects occurring on soil and wood/soil-feeders
(Bandeira and Vasconcellos 2002; Bandeira et  al. 2003).
On the other hand, agricultural practices can be maintained
in a landscape context, where the deleterious effects of nat-
ural habitat loss are mitigated by the functional connectiv-
ity of forest fragments (Couto et al. 2020). In a landscape
context, the proximity between forest fragments inserted
into an agricultural matrix, can act synergistically with the
dispersion ability of termite species, and can favour gene
flow. However, isolated forest fragments can have the oppo-
site effect and can favour the local extinction of termite
populations.
8.5 Nests and Constructor Species
Twelve termite species construct nests with defined and vis-
ible structures in the NAF, with the number of constructor
species and nest density varying substantially depending on
the area. Species that construct arboreal nests or those that
are associated with fallen wood on the ground are:
Anoplotermes banksi, Labiotermes labralis, Microcerotermes
indistinctus, M. strunckii, Nasutitermes corniger, N.
­ephratae, N. gaigei, N. macrocephalus, N. obscurus,
Silvestritermes heyeri and Termes medioculatus (some nests
in Fig. 8.3). Although N. gaigei nests have a defined struc-
ture, which shelters the royal couple and their brood, they are
not easily found in these areas, as they are generally located
inside trunks in advanced stages of decomposition on the
ground. A similar situation occurs with T. medioculatus
A. Vasconcellos et al.
nests, which are generally located at the base of live or dead
trees and are not always easily visualised. Only two species
construct epigeal-­type nests in the NAF, Embiratermes neo-
tenicus and Termes medioculatus. Their nests are very com-
mon in areas within Pernambuco and Alagoas but are
relatively rare in Paraíba and absent in Rio Grande do Norte.
There are records of arboreal polycalic nests for N. corniger
in forest fragments and in the urban environments of many
cities located within the NAF (Vasconcellos and Bandeira
2006).
The average nest density for the set of areas in the NAF is
estimated as 57 nests/ha, varying from 2.6 to 157 nests/ha for
the “Mata Vertente” (S8°11′12″ and W35°47′29″ – 978 ele-
vation) in Pernambuco and “Refúgio de Vida Silvestre Mata
do Buraquinho” in Paraíba (50  m), respectively (Bandeira
et al. 1998; Bandeira et al. 2003; Vasconcellos et al. 2008;
Vasconcellos 2010; Silva et al. 2019). There is an apparent
decrease in nest density in accordance with altitude. The
greatest densities registered were for Microcerotermes
indistictus (54 nests/ha) and Nasutitermes corniger (23
nests/ha) in the “Reserva Biológica Guaribas” in the state of
Paraíba (Vasconcellos et al. 2008). During the study period,
there was a greater density of soil-feeders’ nests in areas with
greater regeneration times (30 years) after selective cutting,
while nests of wood-feeders were more common in more
recent areas (17 years).
8.6 Abundance, Biomass and Nutrient
Cycles
The estimates of biomass and abundance in the NAF are
within the range of values previously registered for other
tropical humid forests around the world (Bignell and
Eggleton 2000). The estimated density of individuals in all
the microhabitats, including soil, nests, leaf litter and trunks
of four NAF areas varied between 1798 and 5662  ind./m2,
corresponding to a live biomass of 3.8–13.2 g/m2 (Bandeira
and Vasconcellos 2002; Vasconcellos 2010). The upper-­
density limit estimate (5662  ind./m2), registered in the
“Reserva Biológica de Pedra Talhada”, represents the great-
est values for a humid forest in the Neotropical region. On
the other hand, the largest estimated values of biomass were
reported for a forest in the Central Amazon, with 14–17  g
(fresh weight)/m2, mainly due to the occurrence of large leaf-­
feeder termites such as Syntermes molestus (Burmeister) and
Syntermes spinosus (Latreille), considered to be among the
largest neotropical termites (Martius 1998).
In three NAF forests, soil represented the microhabitat
with the greatest termite abundance and biomass, with an
elevated quantity of species and individuals at depths of up to
20 cm (Vasconcellos 2010). Specifically, in this microhabi-
tat, we can find 1030–4331  ind./m2 and a biomass of 1.5–
10.2  g (fresh mass)/m2 (Bandeira et  al. 1998; Silva and
8  Termites from the Northern Atlantic Forest, Brazil: Ecology and Conservation 129

Fig. 8.3  Some conspicuous

termite nests in the Northern
Atlantic Forest, Brazil.
(a)–(b), Nasutitermes
ephratae (intact and open);
(c)–(d), Embiratermes
neotenicus (intact and open);
(e)–(f), Silvestritermes heyeri
(intact and open); (g),
Nasutitermes gaigei; and (h)
Termes medioculatus. Ruler
size = 30 cm; pincer: 12 cm
and tool: 43 cm

Bandeira 1999; Bandeira and Vasconcellos 2002). There was
no apparent significant difference in the density of individu-
als between the dry and rainy seasons (Silva and Bandeira
1999).
The estimated biomass and abundance of termites in the
remnant areas of the NAF suggest that these insects play an
important role in the dynamic ecological processes related to
energy flow and nutrient cycling of plant necromass. Wood
consumption by Nasutitermes corniger, N. ephratae and N.
macrocephalus, was estimated to account for 66.9 kg of dry
wood/ha/year, corresponding to approximately 2.9% of the
annual production of wood-litter in a fragment of Atlantic
Coastal Forest in the NAF. This consumption, together with
that of the other 18 exclusively wood-feeding termite species
known to occur in this fragment, highlights the important
role termites have in the decomposition process in the NAF
(Vasconcellos and Moura 2010).
8.7 Pest Species in Urban
and Agricultural Environments
Over 10 termite species have been registered to cause some
type of damage to buildings in the urban environment within
the NAF limits (Vasconcellos et al. 2002; Albuquerque et al.
2012). Three of these species are exotic: Coptotermes
gestroi, Cryptotermes brevis and C. dudley. Although C.
gestroi represents the main pest species in the south-eastern
130
region of Brazil, it has only been registered with a low fre-
quency in buildings in the city of Recife, state of Pernambuco
(Albuquerque et al. 2012). On the other hand, C. brevis rep-
resents an important pest, with an increased potential of
damaging wood objects, especially those related to historical
heritage (Vasconcellos et  al. 2002). Among the native spe-
cies, only Nasutitermes corniger can be treated as a pest in
the urban environment. This species is present in practically
all the cities within the NAF and has been registered in 68%
and 82% of buildings in João Pessoa and Recife, respectively
(Vasconcellos et  al. 2002; Albuquerque et  al. 2012). The
presence of polycalic nests in the urban environment
increases the complexity of N. corniger control. The popula-
tion of a single polycalic nest distributed throughout five
houses, covering an area of 7820 m2, was estimated to com-
prise 637,679 individuals, well above the population of a
single nest (Vasconcellos and Bandeira 2006; Vasconcellos
2010). The colonisation success of this species in the urban
environment is due to its great biological versatility, mainly
with regards to reproductive mechanisms, feeding habits and
nidification (Vasconcellos et al. 2002). The high frequency
of C. brevis and N. corniger in buildings, together with the
economic damages caused by these species, suggests that
only these two species can be considered as effective pests in
cities inserted within the limits of the NAF. The other species
within urban environments occur only eventually, causing
very little damage, thereby suggesting that they are not effec-
tive pests at all.
Sugarcane is prominently the main crop developed in the
NAF and together with disordered urban growth, it can be con-
sidered as one of the main factors responsible for the loss in
vegetation cover in the NAF. Fourteen species of termites have
been found in cane fields in the states of Pernambuco and
Paraíba, including various soil-feeding species of Apico­
termitinae. However, it appears that only Cylindro­termes sapi-
ranga cause damage to sugarcane cultures, while the remaining
species do not show any potential of becoming pests (Miranda
et al. 2004; Couto et al. 2019). The importance of termites for
the maintenance of tropical soil fertility, aeration and porosity
makes it clear that basic studies on the reproductive biology
and population dynamics of C. sapiranga should be encour-
aged, from the perspective of developing control agents and
species-specific management techniques.
8.8 Conclusion and Conservation
Perspectives
Habitat loss and fragmentation of the NAF due to continual
anthropogenic pressure over the past 500 years is the main
risk to the maintenance of populations, independent of taxa.
Among the areas where termites were sampled, some dem-
onstrated an elevated potential for the conservation of biodi-
versity. Most of these areas are already classified as
A. Vasconcellos et al.
Conservation Units; however, they still experience frequent
and intense anthropogenic pressure on their natural capital.
The fragments inserted into the sugarcane culture matrix
still have relatively complex termite communities, in terms
of species richness, feeding groups and biomass, including
various soil-feeders, without potential as pests, present in
monoculture soil. Thus, some sugarcane management meth-
ods can alleviate pressure on termites such as, (i) refraining
from using fire as a collection method; (ii) in a landscape
context, promote reconnection or keep fragments close to
each other, regardless of their size (see Couto et al. 2020) and
(iii) using species-specific control methods for termites con-
sidered as pests, with the aim of maintaining ecosystem ser-
vices provided by populations of other species that do not
have the potential of becoming pests.
Although the NAF has the lowest remaining vegetation
cover in the Atlantic Forest, it houses almost half of the ter-
mite species found in this biome, as well as having relatively
distinct communities from other sectors of the Atlantic
Forest, especially those located below the Rio Doce Valley.
Furthermore, some species are exclusively shared with the
Amazon Forest, reinforcing a more recent connection
between these two large blocks of South American rainfor-
ests. From a functional perspective, an increased termite bio-
mass, especially within soils, was registered in NAF areas,
suggesting the active participation of these insects in soil
decomposition and formation processes, influencing popula-
tions of organisms from different trophic levels, whether as a
food resource or as ecosystem engineers.
Acknowledgments  We thank Dr. Adelmar Gomes Bandeira (in memo-
rium) for the seed of termitology planted in the northeast of Brazil and
for his untiring desire to share knowledge. Our thanks are also extended
to M.Sc. Tarsila A. Cavalcanti for the critical reading and suggestions
on the manuscript. AV and EMC thank CNPq for the productivity in
research fellowship (proc.309820/2020-0 and 308408/2019-5). We also
thank CAPES for MVE’s doctoral scholarship,  the Research Support
Foundation of the State of Paraíba (FAPESQ - Edital 09/2021 Demanda
Universal and our colleagues that helped during field expeditions.
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 Fishes from the Northern Atlantic Forest
and Their Conservation
Manoela M. F. Marinho, Sergio M. Q. Lima, Roney E. C. de
Paiva, and Telton P. A. Ramos
Abstract
The Northern Atlantic Forest (NAF) is drained by small to
medium-sized coastal drainages located north of São
Francisco River that are inhabited by 48 native freshwater
fish species, of which one is endangered and one is
endemic. Most are small-sized species long adapted to a
variety of aquatic microhabitats. The ichthyofaunal com-
position of the Northern Atlantic Forest may be drasti-
cally altered due to intense anthropogenic actions over 5
centuries. The main threats affecting the ichthyofauna,
that is, removal of riparian vegetation, urbanization, and
introduction of non-native species, are discussed. To pro-
tect these fishes, proper management of Conservation
Units is indispensable, but also ichthyofaunal surveys and
taxonomic studies. This chapter is unique in offering a
taxonomic list of the freshwater fishes from the NAF, with
discussion on the effectiveness of the protected areas in
the region. It serves as a starting point for development
planning and support for conservation acts of fish species
in NAF. We highlight data survey was only possible due
to fish collections of federal universities in Northeastern
Brazil.
Keywords
Pernambuco Endemism Center · Freshwater fishes ·
Northeastern Brazil · Conservation Units
M. M. F. Marinho (*) · T. P. A. Ramos
Laboratório de Sistemática e Morfologia de Peixes, Departamento
de Sistemática e Ecologia/CCEN, Universidade Federal da
Paraíba/UFPB, João Pessoa, PB, Brazil
S. M. Q. Lima · R. E. C. de Paiva
Laboratório de Ictiologia Sistemática e Evolutiva, Departamento
de Botânica e Zoologia, Centro de Biociências, Universidade
Federal do Rio Grande do Norte,
Natal, RN, Brazil
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
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_9
9
9.1 Introduction
The tropical Atlantic Forest is among the world’s five
hotspots of diversity (Myers et  al. 2000). These areas of
remarkable concentrations of endemic species are undergo-
ing great loss of habitat. Currently, the projected future is
bleak: only 11.6% of the original extent of the Atlantic Forest
is estimated to remain—most as small, isolated, and dis-
turbed fragments (Ribeiro et al. 2009). Approximately 70%
of the Brazilian population lives in large cities within this
forest domain (Martinelli et al. 2013), with increased pollu-
tion and deforestation rates. It is so threatened that, in the
absence of great conservation efforts, it is likely to lose
much, if not most, of its remaining vegetation within the
foreseeable future (Myers et al. 2000).
Unfortunately, biodiversity assessments and conservation
policies often neglect freshwater biota because, in most
cases, data on freshwater species remain poorly known in
order to be included (Heilpern 2015), despite continental
waters being considered the most highly threatened ecosys-
tems in the world (Abell et al. 2008; Saunders et al. 2002).
Aquatic environments of the Atlantic Forest had undergone a
long history of land use effect, which caused profound modi-
fication in fish diversity along the years (Menezes et al. 2007;
Dala-Corte et al. 2020). One catastrophic consequence is that
67 fish species occurring in such rich drainage systems are
threatened (PAN 2021), which corresponds to about 20% of
the ichthyofauna.
The Atlantic Forest located north of the São Francisco
River, also known as the Northern Atlantic Forest (NAF) or
Pernambuco Endemism Center, is drained by a series of
small coastal drainages running directly to the Atlantic
Ocean (Fig.  9.1). These rivers and streams are partially or
fully included in the Atlantic Forest. Thus, the distribution of
most species extends beyond the Atlantic Forest into the dry
neighboring Caatinga domain. This complex of small- to
medium-sized drainages is included in the freshwater ecore-
gion of Northeastern Caatinga and Coastal Drainages sensu
133
134
Fig. 9.1  Coastal hydrographic basins draining the Northern Atlantic
Forest: Cururipe (1), Poxizinho (2), Ipoca (3), São Miguel (4), Mundaú
(5), Pratagi (6), Paraíba do Meio (7), Manguaba (8), Una (9), Saltinho
(10), Sirinhaém (11), Ipojuca (12), Jaboatão (13), Capibaribe (14),
Abell et  al. (2008). Fishes inhabiting this area belong to
orders and families typically found in other neotropical
hydrographic basins, but are comparatively poor in terms of
the number of species (Rosa et al. 2003). According to the
authors, even the reminiscent ichthyofauna is poorly docu-
mented, although major efforts have been done recently in
the area. Ichthyological surveys in several drainages were
performed during the last decades and provided a large
amount of data about the fish fauna of the area (see Berbel-­
Filho et  al. 2018). However, concerning the continental
waters of the Northern Atlantic Forest, information are
mostly restricted to specific river basins, as a result of ich-
thyofauna studies for specific purposes (e.g., Oliveira-Silva
M. M. F. Marinho et al.
Itapessoca (15), Goiana (16), Abiaí (17), Gramame (18), Paraíba do
Norte (19), Miriri (20), Mamanguape (21), Camaratuba (22), Curimataú
(23), Catu (24), Jacú (25), Trairi (26), Pirangi (27), Potengi (28), Ceará-­
Mirim (29), Maxaranguape (30), Punaú (31), Boqueirão (32)
et  al. 2018; Ramos et  al. 2019), and no compilation is
available.
In this context, this chapter represents the first compila-
tion data for the ichthyofauna from the NAF. Our contribu-
tion is based on the literature, recently collected material in
the area, and examination of specimens deposited in fish col-
lections. The purpose of this chapter is to offer a taxonomic
list of freshwater fish species for the area, data on endemism,
and conservation status and to characterize the water envi-
ronments of NAF. Thus, we aim to answer questions such as
which species can be found in which microhabitats? What
are the main threats of the ichthyofauna and the main chal-
lenges to conserving them? Are the protected areas effective
9  Fishes from the Northern Atlantic Forest and Their Conservation
in conserving the fishes? We hope this contribution helps to
fill the gap of information on freshwater fishes from NAF,
observed by Menezes et al. (2007), serving as a starting point
for development planning and support for conservation acts
of fish species of this region.
9.2 Hidrography of the Northern Atlantic
Forest
The Atlantic Forest is diverse in aquatic systems and micro-
habits, presenting different types of water bodies, from
streamlets to large rivers, ponds, and lakes. There are shaded
waters covered by dense forest; open sunlit waters; tributar-
ies having muddy, rocky, or sandy substrates; plain areas
with slow-moving waters; or steeper areas with rapids and
waterfalls (Menezes et al. 2007). The formation of most of
these watersheds is related to old processes that took place
during and after the breakup of Gondwana, which influenced
water direction, tributary positions, and waterflow of the
aquatic environments draining the oldest terrenes of the con-
tinent: the ancient Brazilian crystalline shield (Ribeiro 2006).
Specifically in the NAF, there are also plenty of distinct
watersheds, formed by a series of old and modern processes
that started at the ancient orogenetic belt of the Borborema
province, with strong control of tectonic activities along the
eastern rifted continental margin of the Brazilian Platform,
promoting dynamism between adjacent drainages which
resulted in headwater captures and deviation of river courses
(Ribeiro 2006). These historical factors are responsible for
the design of the hydrographical basins found in the area
nowadays. As freshwater fishes are confined into hydro-
graphic drainages, such geological processes directly influ-
ence fish distributional patterns, causing faunal interchange
and cladogenetic events (Lundberg et al. 1998; Ribeiro 2006;
Camelier and Zanata 2014). Sea level fluctuations at the Late
Pleistocene also caused dispersion and vicariance of
freshwater fish fauna on the coastal drainages of South
­ stretch, and many microbasins are restricted to the domain,
America (Weitzman et  al. 1988). However, recent recon-
struction of paleodrainages indicated low connections among
coastal basins in the area due to a narrow continental shelf
along NAF (Thomaz and Knowles 2018). Thus, the geo-
graphical distribution of freshwater fishes of the east coastal
hydrographic basins is a result of historical factors mingled
with ecological conditions imposed by the environment
along geological time.
The small to medium-sized coastal drainages of NAF
drain the east portion of Eastern Brazilian Shield, repre-
sented by the Borborema plateau, and flow directly into the
Atlantic Ocean (Fig. 9.1). The headwaters of most of these
rivers and streams are included in the Caatinga domain,
which is characterized by a semi-arid climate with low pre-
cipitation and high temperatures and evaporation. The
135
Atlantic Forest emerges in their lower course, partially or
fully covering the waterbodies. Such humid domain is sub-
ject to high precipitation—raining seasons are predominant
during the autumn and winter, extending from February to
July (Bernardes 1960). North of the São Francisco River, the
Atlantic Forest is characterized by higher temperatures with
lower amplitudes, compared to southern portions (Cancello
et al. 2014).
The headwaters NAF drainages may show intermittent
and seasonal regimes, depending on their extensions into the
Caatinga (Rosa et  al. 2003). In the Rio Grande do Norte
State, rivers such as the Potengi and the Curimataú are under
higher influence of the Caatinga domain. On the other hand,
the headwaters of watersheds draining the Paraíba,
Pernambuco, and Alagoas State are in mountain forests
(“Brejos de Altitude”), with their high and middle course in
the Caatinga and lower course in the Atlantic Forest (Rosa
et al. 2003). Drainages with more intimate contact with the
Atlantic Forest have a torrential regime in the raining season
(Rosa et  al. 2003), such as the Paraíba do Norte and
Capibaribe rivers.
Larger drainages of NAF are the Potengi, Mamanguape,
Paraíba do Norte, Capibaribe, Ipojuca, Una, and Camaçari
rivers. Additionally, there are a series of small basins close to
the Atlantic shore (Fig. 9.1). Many natural microhabits are
found within these basins: wide rivers with deep and muddy
bottom, shallow margins with sandy banks, shallow streams
with rapid waters and rocky bottoms, shaded stretches cov-
ered with dense riparian vegetation, quiet waters with differ-
ent kinds of aquatic plants, and areas with clear or black
waters fringed by dunes (Fig. 9.2). Particular fish species are
adapted to only one of the aforementioned microhabits, but
generalist species may occur in many, as they are adaptable
to a wide variety of ecological conditions (Menezes et  al.
2007). The lower courses near the shore of these hydro-
graphic basins are strongly influenced by the tide. Because
the Atlantic Forest in this area is represented by a slender
many of these small coastal environments are under intense
tidal influence, preventing the occurrence of typical freshwa-
ter fish fauna.
9.3 The Ichthyofauna
The freshwater ichthyofauna of the Atlantic Forest north of
the São Francisco River is poor in terms of fish richness. This
ichthyofauna is certainly reduced due to historical processes,
climate alterations, and anthropic activities that caused local
or regional extinctions (Rosa et al. 2003). A total of 58 fresh-
water fish species were recorded from drainages of the NAF,
belonging to 6 orders and 19 families (compiled from Ramos
et al. 2005, 2017, 2018a, b, 2019, 2020; Paiva et al. 2014;
136 M. M. F. Marinho et al.

Fig. 9.2  Examples of water bodies and microhabitats found in the Northern Atlantic Forest: (a) Meio stream at Parque Estadual Mata do Xem-­
Xem, Paraíba do Norte river basin (Paraíba State), (b) Abiaí river (Paraíba State), (c), (d), and (f) Pratagi river estuary (Rio Grande do Norte State)

Lira et  al. 2015; Costa et  al. 2017; Gouveia et  al. 2017;
Furtado et al. 2018; Berbel-Filho et al. 2018; Oliveira-Silva
et  al. 2018; Medeiros et  al. 2019, and additional data of
museum collections). Species belonging to typical marine
groups that enter in freshwater, such as those of the families
Engraulidae, Eleotridae, Gobiidae, and Syngnathidae, were
not included. Out of 58 species, 48 are native and 10 are non-­
native species (Table 9.1; Fig. 9.3). Thirty species are added
to the most-inclusive compilation of the whole Atlantic
Forest by Menezes et al. (2007), which now accounts for 355
native species. Native fish species of the NAF account for
about 13.5% of the species known to occur in the Atlantic
Forest. As expected to Neotropical freshwater native fish
fauna, Characidae (Characiformes) is the most representa-
tive family, contributing with 12 species (corresponding to
25% of the total number of species), followed by Loricariidae
(Siluriformes) with 6 species (12.5%) and Serrasalmidae
(Characiformes) and Cichlidae (Perciformes), with 4 species
each (8.3%). Interestingly, almost half of the families are
represented by just one species (Fig. 9.3).
9  Fishes from the Northern Atlantic Forest and Their Conservation
Table 9.1  Taxonomic list of freshwater fish species of the Northern
Atlantic Forest with indication of endemic species to the area (ENAF)
or endangered species (EN)
ORDER/Family/Species
CHARACIFORMES
Crenuchidae
Characidium bimaculatum Fowler, 1941
Erythrinidae
Erythrinus erythrinus (Bloch & Schneider, 1801)
Hoplerythrinus unitaeniatus (Spix & Agassiz, 1829)
Hoplias cf. malabaricus
Lebiasinidae
Nannostomus beckfordi Günther, 1872*
Parodontidae
Apareiodon davisi Fowler, 1941
Anostomidae
Leporinus piau Fowler, 1941
Curimatidae
Steindachnerina notonota (Miranda-Ribeiro, 1937)
Prochilodontidae
Prochilodus brevis Steindachner, 1875
Serrasalmidae
Metynnis lippincottianus (Cope, 1870)
Myleus micans (Lütken, 1875)*
Psectrogaster saguiru (Fowler, 1941)
Serrasalmus brandti Lütken, 1875
Serrasalmus rhombeus (Linnaeus, 1766)
Serrasalmus spilopleura Kner, 1858
Characidae
Astyanax cf. bimaculatus (Linnaeus, 1758)
Cheirodon jaguaribensis Fowler, 1941
Compsura heterura Eigenmann, 1915
Hemigrammus marginatus Ellis, 1911
Hemigrammus rodwayi Durbin, 1909
Hemigrammus unilineatus (Gill, 1858)
Hyphessobrycon cf. piabinhas Fowler, 1941
Psalidodon cf. fasciatus (Cuvier, 1819)
Psellogrammus kennedyi (Eigenmann, 1903)
Serrapinnus heterodon (Eigenmann, 1915)
Serrapinnus piaba (Lütken, 1875)
Serrapinnus potiguar Jerep & Malabarba, 2014
Triportheidae
Triportheus signatus (Garman, 1890)
SILURIFORMES
Auchenipteridae
Trachelyopterus galeatus (Linnaeus, 1766)
Heptapteridae
137
Table 9.1 (continued)
Pimelodella papariae (Fowler, 1941)
Rhamdia quelen (Quoy & Gaimard, 1824)
Callichthyidae
Aspidoras depinnai Britto, 2000
Callichthys callichthys (Linnaeus, 1758)
Megalechis thoracata (Valenciennes, 1840)
Loricariidae
Hypostomus papariae (Fowler, 1941)
Hypostomus pusarum (Starks, 1913)
Parotocinclus cesarpintoi Miranda Ribeiro, 1939
Parotocinclus jumbo Britski & Garavello, 2002
Parotocinclus spilosoma (Fowler, 1941)
Pseudancistrus papariae Fowler, 1941
EN GYMNOTIFORMES
Gymnotidae
Gymnotus cf. carapo Linnaeus, 1758
Gymnotus darwini Campos-da-Paz & Santana, 2019 ENAF
CYPRINODONTIFORMES
Poeciliidae
Poecilia hollandi (Henn, 1916)
Poecilia reticulata Peters, 1859*
Poecilia vivipara Bloch & Schneider, 1801
Xiphophorus maculatus (Günther, 1866)*
Rivulidae
Kryptolebias ocellatus (Hensel 1868)
SYNBRANCHIFORMES
Synbranchidae
Synbranchus aff. marmoratus Bloch, 1795
PERCIFORMES
Cichlidae
Astronotus ocellatus (Agassiz, 1831)*
Cichla monoculus Spix & Agassiz, 1831*
Cichlasoma orientale Kullander, 1983
Cichlasoma sanctifranciscense Kullander, 1983
Coptodon rendalli (Boulenger 1897)*
Crenicichla brasiliensis (Bloch, 1792)
Geophagus brasiliensis (Quoy & Gaimard, 1824)
Laetacara curviceps (Ahl, 1923)*
Oreochromis niloticus (Linnaeus, 1758) *
Parachromis managuensis (Günther, 1867)*
2022)
*Non-native species are marked with an asterisk. Classification follows Fricke et al. (
(continued)
138 M. M. F. Marinho et al.

Fig. 9.3  Species richness per family from the Northern Atlantic Forest

Fig. 9.4  Representatives of the ichthyofauna from the Northern Atlantic Forest: (a) Apareiodon davisi, (b) Hoplias cf. malabaricus, (c) Astyanax
cf. bimaculatus, (d) Hemigrammus unilineatus, (e) Parotocinclus jumbo, (f) Parotocinclus spilosoma, (g) Gymnotus cf. carapo, (h) Cichlasoma
orientale, (i) Crenicichla brasiliensis
9  Fishes from the Northern Atlantic Forest and Their Conservation
The only species endemic to the NAF is Gymnotus dar-
wini, popularly known as “sarapó” or “tuvira” (Fig. 9.4g).
It is known only from coastal river systems of the
Pernambuco State from small drainages totally inserted
into the Atlantic Forest (Campos-da-Paz and de Santana
2019).
Most species of the NAF are small-sized, measuring
about 20 cm of standard length (SL), reflecting the small to
medium-sized coastal drainages in the area. The smallest
species are those belonging to the family Characide, such as
the cheirodontins Compsura heterura, Serrapinnus potiguar,
and S. piaba; the Poeciliidae of the genera Poecilia hollandi
and Poecilia vivipara; and the Loricariidae Parotocinclus
cesarpintoi, attaining about 3  cm of SL (Reis et  al. 2003;
Jerep and Malabarba 2014). Despite their small size, they
represent taxa inhabiting distinct aquatic microhabitats, evi-
dencing the ecological diversity in the area. The cheirodon-
tins (known as “piabas,” “tetras”) are found in small, slow to
moderate-moving clear-water streams, with a large amount
of floating and submerged vegetation and sandy bottom
(Dias and Fialho 2009; Jerep and Malabarba 2014). These
fishes feed on vegetal itens, algae, insects, and microcrusta-
ceans (Dias and Fialho 2009). They usually form large,
mixed, mid-water shoals and are associated to macrophytes.
The poeciliids (“barrigudinhos,” “guarús,” “lebistes,” gup-
pies) are top-dwelling species, living in small shoals at the
margins of small streams, lagoons, and large rivers. Poecilia
hollandi is apparently rare at NAF, being recorded only in
one locality in the Manguaba river (UFGRS 16995), a small
basin fully located in the Atlantic Forest domain at the
Alagoas State. On the other hand, Poecilia vivipara is one of
the most abundant species in some water bodies (Ramos
et al. 2005, 2019). It is a resilient species, widespread in both
freshwater and euryhaline coastal environments (Menezes
et  al. 2007). Small loricariids (“cascudinhos”) such as
Parotocinclus spp. are bottom-dwelling species found in
small watercourses characterized by moderate to fast r­ unning
water currents, commonly associated with rocks and peb-
bles. Parotocinclus jumbo (Fig.  9.4e) was collected in flat
areas in the middle reach of the Paraíba do Norte River dur-
ing the dry season, where clear waters of slow-moving cur-
rents with sandy and rocky substrate are predominant. In the
collection site of Taboca Municipality, at the west portions of
the Atlantic Forest near the transition to the Caatinga domain,
the river was almost dry, and the fish was confined to isolated
pools (Britski and Garavello 2002).
Besides Poecilia vivipara, other abundant species are
Astyanax cf. bimaculatus (Fig. 9.4c), Hemigrammus margin-
atus, H. rodwayi, and Psalidodon cf. fasciatus (Ramos et al.
2005, 2018a, b, 2019; Oliveira-Silva et al. 2018). They are all
small-sized characid species growing no longer than 12 cm
of SL (Reis et  al. 2003). Many species of Astyanax (or
Psalidodon, depending on the classification) are most likely
139
to survive radical habitat changes, because they are adapted
to feed on a variety of food items such as insects, small
fishes, and plant material (Menezes et al. 2007). According
to the authors, these species may become more abundant
after deforestation. Thus, a high number of individuals of
Astyanax cf. bimaculatus and Psalidodon cf. fasciatus may
indicate drastic habitat change caused by urbanization,
deforestation, and pollution, common processes in the mod-
ern history of the Atlantic Forest.
Larger species, such as the characiforms of the families
Anostomidae (“piaus”), Serrasalmidae (“pacus,” “pira-
nhas”), Prochilodontidae (“curimatãs”), Curimatidae (“bran-
quinhas”), and also Erythrinidae (“traíras”) are of importance
for artisanal fisheries. Adult individuals of species of these
families are mostly abundant in larger water bodies, but juve-
niles may be found in small tributaries. In the Mamanguape
river, Prochilodus brevis is especially abundant in the lower
reaches of the river. Due to its detritivore habitus, it is
expected to occur on river bottoms where a larger amount of
accumulated material is found (Oliveira-Silva et  al. 2018).
The erythrinid Hoplias cf. malabaricus is found on the bot-
tom of ponds and lakes, seeking protection in the substrate.
Its cryptic coloration (Fig. 9.4b) allows catching other fishes
by ambush. Remaining native species are of limited or no
commercial value. Some are occasionally found in the inter-
national aquarium trade such as Aspidoras depinnai,
Geophagus brasiliensis, Gymnotus cf. carapo, Hemigrammus
unilineatus (Fig.  9.4d), Metynnis lippincottianus, and
Parotocinclus jumbo, but are not often commercialized.
The lower course of rivers and streams close to the shore
is under constant influence of tides, where salinity varies
daily. Marine fishes may enter continental watercourses on
these areas for food and protection. Freshwater fishes occur-
ring in lower areas are those more tolerant to salinity. For
example, Cichlasoma orientale (Fig.  9.4h), Crenicichla
brasiliensis (Fig. 9.4i), Hemigrammus marginatus, Hoplias
malabaricus, and Poecilia vivipara were collected in areas
under tidal influence (about 0.5 km from the sea) (Paiva et al.
2014).
9.4 Main Threats and Conservation
Due to 5 centuries of intense anthropogenic actions in the
Atlantic Forest, ichthyologists have stated that only a portion
of the original taxonomic entities and ecological associations
can be observed today and that many species may have
undergone local or global extinction before being discovered
(Menezes et al. 2007). Unfortunately, our knowledge on the
effects of continuous degradation of the Atlantic Forest and
its habits is fragmentary, representing a problem to under-
stand historical aspects of fish evolution and distribution in
the area (Menezes et al. 2007; Abilhoa et al. 2011). In the
140
Northern Atlantic Forest, it is possible that severe habitat
alteration in coastal drainages may have caused drastic
changes in the faunal composition along the years. The main
obvious threats affecting the fish fauna of the region are
those related to habitat loss, such as removal of riparian veg-
etation and urbanization, and also introduction of non-native
species.
Riparian deforestation causes profound negative impacts
in the physical and chemical parameters of the aquatic envi-
ronment. When the forest is removed, the input of allochtho-
nous material is altered. Aquatic animals that depend on the
forest for food, shelter and breeding sites are primarily
affected (Schneider and Winemiller 2008; Teresa et al. 2015).
Insolation becomes intense and may alter daily fluctuation of
water temperature (Menezes et al. 2007) and growth of pho-
tosynthesizing aquatic organisms (Lorion and Kennedy
2009). Deforestation in the nearby aquatic environment also
causes soil erosion because it lacks the sponge-like capacity
of the forest root system, so the water runs rapidly, “wash-
ing” the landscape and deeply modifying silt loads, espe-
cially during the rainy season (Menezes et al. 2007; Casatti
et al. 2012). By altering abiotic conditions, such as tempera-
ture and dissolved oxygen, deforestation has long been pre-
dicted to influence recruitment and survival of Neotropical
aquatic organisms (Lowe-McConnell 1987; Teresa et  al.
2015). Furthermore, the composition and representation of
functional ichthyofaunal groups change when riparian zones
are deforested. Modifications associated with habitat avail-
ability, food resources, and physicochemical conditions
appear to restrict the occurrence of specialized species and
instead benefit tolerant generalists (Teresa et al. 2015).
As for the whole Atlantic Forest, we can now describe
only a fraction of the original biodiversity and the ecologi-
cal associations of the fishes as they existed before European
colonization because we have no access to how water bod-
ies of the original Atlantic Forest were (Menezes et  al.
2007). Dala-Corte et  al. (2020) found that streams in
Atlantic Forest landscapes under a long history of land use
effects (e.g., agriculture and cattle ranching) may lack sev-
eral indicator species because fish diversity is already
largely reduced in this biome due to a long history of defor-
estation. In the NAF, sugarcane monoculture in the six-
teenth to eighteenth centuries was responsible for
deforestation of a large part of riparian vegetation (Lins-e-
Silva et al. 2021). This area is one of the most anthropized
of the Atlantic Forest, with low vegetation cover and high
vegetation debit in riparian areas per municipality (Rezende
et al. 2018). Furthermore, the lack of studies on freshwater
fishes from Northeast Brazil is well documented (Rosa
et al. 2003; Menezes et al. 2007). According to Lima et al.
(2021), five of six less-studied Brazilian basins are located
in the Northeast. Also, despite the Atlantic Forest holding
the largest number of papers on stream-dwelling fishes, it is
M. M. F. Marinho et al.
clear that its northern stretch is the most understudied
(Lima et al. 2021: Fig. 9.3).
Another important threat for the ichthyofauna in NAF is
urbanization. European colonization in Brazil initiated
about 500 years ago on the Atlantic coast, where the largest
cities and capitals are concentrated. This is the same for the
NAF—most populated places are capitals that are fully sit-
uated in the Atlantic Forest (or what remains of it): Natal
(Rio Grande do Norte State), João Pessoa (Paraíba State),
Recife (Pernambuco State), and Maceió (Alagoas State).
Urban expansion is responsible for poor water quality in
the area due to domestic sewage dump, landfill, solid waste
disposal, and also removal of riparian vegetation (ANA
2015). These threats initiate a cascade of physical and
chemical changes in the aquatic environment that affect the
biota directly (McKinney 2006). Besides obvious changes
in water temperature, pH, soil characteristics, and deterio-
ration due to input of toxic substances by pollutants, from
microorganisms to fish, all biological communities are
affected, damaging the dynamics of food webs. Urbanization
also influences the foraging behavior of fish due to changes
in the availability of prey (Ganassin et al. 2018). All these
processes can cause deep ecological changes, for instance,
a significant decrease on energy exchange between the for-
est and aquatic environments (Abilhoa et al. 2011). Species
that are susceptible to any of these variations tend to be the
first to disappear.
The introduction of non-native species is also intense in
the area and is considered the second largest cause of biodi-
versity loss worldwide (Bellard et al. 2016). Of 58 freshwa-
ter fishes listed, 10 (17.2%) are exotic species. Non-native
species belong to four families: Cichlidae (with six species),
Poeciliidae (two), Serrasalmidae (one), and Lebiasinidae
(one), the latter represented exclusively by exotic species.
Most non-native species are common in the aquarium trade
and may have been released accidentally: Nannostomus
beckfordi, Xiphophorus maculatus, Astronotus ocellatus,
Laetacara curviceps, and Parachromis managuensis.
Oreochromis niloticus and Coptodon rendalli are important
food sources and are commonly used in fish farming. They
are reared in inland ponds or floating cages, in which escape
is almost inevitable (Vicente and Fonseca-Alves 2013).
Species of Cichla have been largely introduced in northeast-
ern Brazil dams through government fish breeding programs
for food sources (Leão et  al. 2011). They have also been
introduced intensively for sport fishing. Poecilia reticulata is
intentionally released for mosquito control, and often, its
population exhibits explosive growth (El-Sabaawi et  al.
2016). Most of the aforementioned species represent a threat
for native species due to key characteristics such as resis-
tance to environmental changes, aggressive behavior, pisciv-
orous diet, and fast maturity, causing negative impact on the
aquatic biota. For example, Oreochromis niloticus is known
9  Fishes from the Northern Atlantic Forest and Their Conservation
to be highly tolerant to environmental change, to have high
reproductive rate, and to compete with native species for
food and other resources (Vicente and Fonseca-Alves 2013).
Species of Cichla are carnivorous with very aggressive pre-
dation behavior and are possibly responsible for local extinc-
tions of native species (Leão et al. 2011). Poecilia reticulata
is favored and highly adapted to urbanized environments, as
it is considered a synanthropic species (McKinney 2006),
and may compete with native fauna. Proper management
(e.g., forestry code enforcement, reducing exotic species
introduction) is decisive for conservation of Atlantic Forest
ichthyofauna (Abilhoa et  al. 2011), besides strengthening
oversight and dissemination of basic information on the
release of non-native species and their potential harm.
When discussing ichthyofaunal threats and introduction
of allochthonous species in Northeast Brazil, the water trans-
position project from the São Francisco River (Integration
Project of São Francisco River with hydrographic basins
from the North Northeast—known as PISF) must be cited.
This project aimed to eradicate hydrological shortage in the
Northeast semi-arid region (Brasil 2004; Pittock et al. 2009).
As a first step, the PISF is transposing waters from the São
Francisco River to the four largest basins from Northeastern
Caatinga and Coastal Drainages ecorregion: Paraíba do
Norte, Piranhas-Açu, Apodi, and Jaguaribe rivers (Silva
et al. 2020). Paraíba do Norte is unique in having a stretch in
the Atlantic Forest. The headwaters of the Paraíba do Norte
are located in the Serra de Jabitacá (Monteiro municipality at
Paraíba State). The upper and medium portions are intermit-
tent, draining the dry Caatinga domain. The lower portion is
perennial, located in the Atlantic Forest, flowing into the
Atlantic Ocean (Ramos et al. 2018a, b).
The water transposition from the São Francisco River to
the Paraíba do Norte River began in March 2017, through
artificial canals along the east axis. Ramos et al. (2018a, b)
warned for the potential negative impacts to the native fish
fauna of Paraíba do Norte River caused by biological inva-
sions of typical fishes from the São Francisco River through
artificial canals. The first record of an allochthonous species
in the Paraíba do Norte River through PISF was made in
2018 through samples of a few specimens of the “tetra-­
fortuna” Moenkhausia costae (Steindachner 1907) in a
pound located at the upper river stretch (Poções), at Monteiro
municipality (Paraíba State), the first place to receive waters
from São Francisco (Ramos et al. 2021). The Poções pond,
as well as other ponds nearby, have been monitored before
water transposition, and the species has never been recorded
in the area until 2018. Further samples made in 2020 revealed
that M. costae is now among the most abundant species of
the pond established in the area (Ramos et al. 2021). Although
the Poções pond is located within the Caatinga domain, the
introduction of species upstream is dangerous as it can rap-
idly occupy downstream portions of the river at the Atlantic
141
Forest. Non-native species may unbalance the stability in the
ecosystems leading to extinction of native species through
long-term predation and competition, eventually causing the
replacement of native species by exotic ones (Vicente and
Fonseca-Alves 2013). In the Paraíba do Norte River, there
are two native species that deserve special attention on this
matter: the “cascudinho” Parotocinclus spilosoma, which is
endemic from that basin, and the “canivetinho” Apareiodon
davisi, an already threatened species. It seems quite evident
that multiple pressures in the aquatic environment including
anthropogenic actions may lead both to extinction.
The only threatened species from NAF is Apareiodon
davisi, classified as Endangered (EN). Its occurrence is men-
tioned to be restricted to the Caatinga domain (ICMBIO
2018), but recent samples caught in the NAF further recorded
the species in the area. However, the localities where A. davisi
used to be collected are deforested by sugarcane monoculture
and farming, causing silting and erosion of the water bodies.
Furthermore, populations are fragmented due to intense
impoundment (ICMBIO 2018). Two other species may be
classified as threatened in future evaluation: Parotocinclus
cesarpintoi and P. spilosoma, both rare species endemic to the
Northeastern Caatinga and Coastal Drainages ecoregion,
where NAF is included, since their areas of occurrence are
also deeply modified due to urbanization.
As indicated before, the main threats affecting the fish
fauna in the Northern Atlantic Forest are those related to
habitat loss through removal of riparian vegetation and
urbanization. Thus, development planning intending the cre-
ation of Conservation Units is indispensable to protect the
ichthyofauna as they play an essential role to reduce degra-
dation of natural environments. Within the NAF, there are 33
Federal Conservation Units (Fig.  9.5). Eight are located in
the Alagoas, 16 in Pernambuco, 6 in Paraíba, and 4 in the Rio
Grande do Norte states. There are further 98 state or
Municipal Conservation Units (20 located in the Alagoas,
57 in Pernambuco, 18 in Paraíba, and 3 in the Rio Grande do
Norte states) but data on location, maps, and information on
faunal survey are diffuse, preventing proper evaluation of
their areas and ichthyofauna.
Of the 33 Federal Conservation Units, data on ichthyofaunal
surveys are only available in three: APA (Environmental
Protected Area) de Tambaba, REBIO (Biological Reserves)
Guaribas, and REBIO Pedra Talhada. This is rather unfortunate
because information on integrity of these areas and whether
endemic or threatened species are in fact being protected is
poor, preventing proper evaluation of ichthyofaunal conserva-
tion. According to ICMBIO (2018), there is no record of
Apareiodon davisi within any conservation unit, reinforcing
how ichthyological surveys in these areas are necessary.
Surveys at APA (Environmental Protection Area) of Tambaba
revealed the presence of two exotic species, Cichla monoculus
and Poecilia reticulata in small coastal microbasins (Graú,
142
Fig. 9.5  Map of Northern Atlantic Forest showing hydrographic basins
and Federal Conservation Units. 1 APA (Environmental Protection
Area) de Piaçabuçu, 2 APA Marituba do Peixe, 3 RESEX (Extractivist
Reserves) Lagoa do Jequiá, 4 APA de Santa Rita, 5 APA do Catolé e
Fernão Velho, 6 APA Costa dos Corais, 7 REBIO (Biological Reserves)
de Pedra Talhada, 8 APA de Murici; 9 REBIO de Saltinho, 10 APA de
Sirinhaém, 11 RVS (Wildlife Refuge) Mata do Urucu, 12 RVS Mata
Serra do Cotovelo, 13 RVS Serra do Cumaru, 14 RVS Mata de Bom
Jardim, 15 RVS Mata do Contra Açude, 16 RVS Sistema Gurjaú, 17
Mucatú, Bucatú, and Gurugi basins) (Ramos et al. 2019). As
discussed, these species represent threats for the native ich-
thyofauna, and their populations should be monitored.
Unfortunately, Poecilia reticulata was also recorded in REBIO
Guaribas in the Camaratuba River (Gouveia et al. 2017) and
RPPN (Natural Heritage Private Reserves) Fazenda Pacatuba
(Furtado et al. 2018) and State Park Mata do Xem-Xem (Ramos
et al. 2018a, b), both in Paraíba do Norte River. Another exotic
M. M. F. Marinho et al.
RVS Mata de Caraúna, 18 RVS Engenho Moreninho, 19 RSV Mata de
Tapacurá, 20 ESEC (Ecological Station) de Caetés, 21 RSV Mata de
Miritiba, 22 RSV Mata da Usina São José, 23 RESEX Acaú-Goiana, 24
APA de Tambaba, 25 FLONA (National Forests) da Restinga de
Cabedelo, 26 APA Barra do Rio Mamanguape, 27 ARIE (Area of
Relevant Ecological Interest) Manguezais da Foz do Rio Mamanguape,
28 REBIO Guaribas, 29 ARIE da Barra do Rio Camaratuba, 30 APA
Piriqui-Una, 31 APA Bonfim/Guaraíra, 32 FLONA de Nísia Floresta,
and 33 APA de Jenipabu
species registered within Conservation Units is the “tilápia”
Oreochromis niloticus found at the REBIO Guaribas (Gouveia
et  al. 2017) and State Park Mata do Xem-Xem, also in the
Paraíba do Norte River basin (Ramos et al. 2018a, b). Therefore,
ichthyological surveys and proper management plans in pro-
tected areas are essential for preserving fish species.
The only endemic fish species of the NAF, Gymnotus dar-
wini, is only known from two localities within Conservation
9  Fishes from the Northern Atlantic Forest and Their Conservation 143

Units: Refúgio Ecológico Charles Darwin (RECD), in the quelen (Koerber & Reis 2019), and Gymnotus cf. carapo
Botafogo river drainage and Reserva Biológica (REBIO) do (Campos-da-Paz & Santana 2019). Cheirodon jaguaribensis
Saltinho, Formoso river drainage (Campos-da-Paz and de is probably a species close to Hemigrammus (H. A. Britski,
Santana 2019). According to the authors, future investiga- pers. comm.) that needs proper redescription to understand
tions are necessary to determine whether such restricted its real identity and distribution. Specimens identified herein
occurrences are the result of actual anthropic impact in adja- as Hyphessobrycon cf. piabinhas are very similar to H.
cent disturbed areas or from poor collection efforts focused parvellus Ellis 1911, a species also occurring in drainages
on electric-knifefish sampling and suggest new ichthyologi- south to the São Francisco River. The specific limits of these
cal studies in the region. The species is not classified as populations remain open to question.
threatened due to its occurrence within Conservation Units, Three species recorded in the area, Pimelodella papariae,
highlighting the importance of these protected areas. Pseudancistrus papariae, and Psectrogaster saguiru, were
described by Fowler in 1941 and are only known from their
type localities, the Papary lake at Rio Grande do Norte State.
9.5 Challenges and Recommendations The Papary lake is located in the Nísia Floresta municipality,
in the NAF. Recent collection efforts in the area, as well as
Native species occurring in the Atlantic Forest north of the one of its tributaries, the Trairi river, did not yield records of
São Francisco were mostly described during the eighteenth any of the three species, indicating the locality may be errone-
to twentieth centuries, but new species are still being discov- ous (Medeiros et al. 2019). On the other hand, Pseudancistrus
ered: Aspidoras depinnai described in 2000, Parotocinclus papariae and Psectrogaster saguiru occur in both Piranhas
jumbo in 2002, Serrapinnus potiguar in 2014, and Gymnotus and Jaguaribe rivers, at the Caatinga domain (Lima et  al.
darwini in 2019, all endemic to the Northeastern Caatinga 2017; Vari 1989). Other authors have also questioned the type
and Coastal Drainages ecoregion, where NAF is included. localities of species described by Fowler (1941), such as Vari
Gymnotus darwini, the only endemic fish species from the (1989), Lima et  al. (2017), and Berbel-­Filho et  al. (2018).
NAF, was the last to be described and represents the first spe- Therefore, further investigations are necessary to address this
cies of the genus described from coastal localities north of issue. These examples illustrate the importance of taxonomic
the mouth of the São Francisco River (Campos-da-Paz and specialists, as well as the education of future generations in
de Santana 2019). Authors claim that such recent discoveries systematics, for understanding freshwater fish identifications
are probably the result of limited collecting efforts in the area for conservation purposes. Moreover, to understand the eco-
(Britto 2000; Campos-da-Paz and de Santana 2019) and that system dynamics and improve conservation in the Atlantic
new ichthyological studies are necessary to protect the fishes Forest, basic ecological studies are fundamental (Abilhoa
(Campos-da-Paz and de Santana 2019). et al. 2011).
Information gaps on biodiversity impair fish conserva- It is important to highlight that data survey of the present
tion as there is little understanding about species distribu- study was only possible due to fish collections of federal uni-
tion, abundance, dispersal processes, metapopulation versities in Northeastern Brazil, which have stored material
structures, population viability, and many other basic bio- sampled by many ichthyologists for decades (Carvalho-­Rocha
logical data (Abilhoa et al. 2011). During the last decades, et al. 2019; Costa et al. 2019; Zanata et al. 2019). Biological
ichthyological surveys have been conducted in the Pratagi, collections are indispensable not only for taxonomy but also
Ceará-Mirim, Trairi, Curimataú, Jaguaribe, and Paraíba do for studies on morphology, evolution, ecology, biogeography,
Norte, mainly in Rio Grande do Norte and Paraíba States conservation, epidemiology, and others. They contain valuable
(Berbel-Filho et al. 2018; Ramos et al. 2018a, b; Medeiros information on biological diversity of the past, present, and for
et  al. 2019). For this reason, collection efforts in under-­ the future and are essential for planning conservation acts and
sampled regions, such as Maxaranguape, Potengi, Pirangi, restoring degraded areas. However, biological collections in
Jacú, Miriri, Goiana, Capibaribe, Sirinhaém, Manguaba, Brazil are historically neglected, with serious difficulties even
and São Miguel River basins, are recommended, but taxo- for basic maintenance (Mega 2020; Santos and Carbayo
nomic studies are also necessary to understand the real 2021). Adding new specimens to already poorly funded insti-
diversity and distribution in the area. tutions is a huge challenge but not doing so will, ultimately,
One of the major impediments to the knowledge of the limit their utility (Hilton et  al. 2021). With the advent of
fish fauna in the area is to achieve accurate identification of molecular systematics, biological collections now hold a new
its populations. There are several species that are known to role, which is to maintain specimens or part of specimens for
be probably species complexes that need taxonomic revi- a large variety of genetic approaches. Unfortunately, these
sions, such as Hoplias cf. malabaricus (Rosso et al. 2018), institutions in Brazil still lack the ideal infrastructure to hold
Astyanax cf. bimaculatus (Garutti & Langeani 2009), long-term genetic resources (e.g., ultrafreezers, liquid nitro-
Psalidodon cf. fasciatus (Melo & Buckup 2006), Rhamdia gen storage, cryo-­facilities) (Santana et al. 2021), and it is not
144
different in the Northeastern region of the country. Furthermore,
data of most collections in northeastern Brazil are not even
available online on digital platforms (Lima et  al. 2017). In
view of that, allocation of funds to basic maintenance of scien-
tific collections, digitizing old and new data to make them
public, and storing material for molecular studies are essential
to keep scientific research alive for fish conservation in the
Northern Atlantic Forest.
9.6 Conclusion
Because of 5 centuries of intense anthropogenic actions,
severe habitat alteration may have caused drastic changes in
the ichthyofaunal composition of the Northern Atlantic
Forest, which is considered depauperated. Nevertheless, the
area is inhabited by 48 native freshwater fishes, of which one
is endangered and one is endemic, and all need protection.
The main threats affecting the fish fauna of NAF are those
related to habitat loss, such as removal of riparian vegetation
and urbanization, along with introduction of non-native spe-
cies. Thus, creation and proper management of Conservation
Units are indispensable to protect the ichthyofauna, also,
strengthening oversight and dissemination of information on
the release of non-native species and their potential harm.
Moreover, basic taxonomic and ecological studies are imper-
ative to generate data to subsidize conservation efforts. This
chapter was only possible due to fish collections of federal
universities in Northeastern Brazil, which have stored mate-
rial sampled by many ichthyologists for decades and are a
valuable tool to understand the ichthyofauna over time.
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 Species Richness, Distribution Pattern,
and Conservation of Amphibians 10
in the Northern Portion of the Brazilian
Atlantic Forest

Washington Luiz Silva Vieira, Geraldo Jorge Barbosa de
Moura, Francisco Vicente Macedo Júnior,
Gindomar Gomes Santana, Tamí Mott,
Marcos Jorge Matias Dubeux,
Filipe Augusto Cavalcanti do Nascimento,
and Kleber Silva Vieira

Abstract
The northern biogeographic region of the Atlantic Forest,
designated as the Pernambuco Endemism Center (PEC),
has high species richness and a high degree of endemism,
which confers a unique identity to the region. Despite its
biological importance, this region is also one of the most
threatened and least known portions of the biome. In this
chapter, we integrate the information available in the lit-
erature with that available in the main herpetological col-
lections in the region to characterize the current knowledge
on species composition, richness, distribution pattern, and
conservation of amphibians in the PEC. In total, 97 spe-
cies belonging to two orders, 15 families and 36 genera
were recorded. Of these, 50 are endemic to the Atlantic
Forest and 14 have restricted distribution to the PEC. The
total surface richness indicated areas of greater species
richness predominantly in the central portion of the PEC,
constituting regions that still present Dense Ombrophilous
Forest fragments. Furthermore, a very representative
number regarding the conservation of species is threat-
ened or lacking available population data. Despite the
growing number of studies published in the last 2 decades,
knowledge about the amphibian fauna of the PEC is still
incipient. This fact reinforces the need for greater invest-

W. L. S. Vieira (*) T. Mott · F. A. C. do Nascimento

Laboratório de Ecofisiologia Animal, Departamento de Sistemática
e Ecologia da Universidade Federal da Paraíba,
João Pessoa, Paraíba, Brazil
G. J. B. de Moura
Laboratório de Estudos Herpetológicos e Paleoherpetológicos,
Universidade Federal Rural de Pernambuco,
Recife, Pernambuco, Brazil
F. V. M. Júnior
Programa de Pós-Graduação em Biodiversidade, Centro de
Ciências Agrárias, Universidade Federal da Paraíba,
Areia, Paraíba, Brazil
G. G. Santana
Laboratório de Ecofisiologia Animal, Departamento de Sistemática
e Ecologia da Universidade Federal da Paraíba,
João Pessoa, Paraíba, Brazil
Laboratório de Herpetologia (Integrado ao Laboratório de
Etnoecologia), Departamento de Biologia, Centro de Ciências
Biológicas e da Saúde, Universidade Estadual da Paraíba,
Campina Grande, Paraíba, Brazil
Laboratório de Biologia Integrativa, Instituto de Ciências
Biológicas e da Saúde, Universidade Federal de Alagoas,
Maceió, Alagoas, Brazil
Setor de Herpetologia, Museu de História Natural, Universidade
Federal de Alagoas, Maceió, Alagoas, Brazil
M. J. M. Dubeux
Laboratório de Biologia Integrativa, Instituto de Ciências
Biológicas e da Saúde, Universidade Federal de Alagoas,
Maceió, Alagoas, Brazil
Setor de Herpetologia, Museu de História Natural, Universidade
Federal de Alagoas, Maceió, Alagoas, Brazil
Programa de Pós-Graduação em Biologia Animal, Departamento
de Zoologia, Instituto de Biociências, Universidade Federal de
Pernambuco, Recife, Pernambuco, Brazil
K. S. Vieira
Laboratório de Ecofisiologia Animal, Departamento de Sistemática
e Ecologia da Universidade Federal da Paraíba,
João Pessoa, Paraíba, Brazil
Bolsista CNPq pelo Programa de Desenvolvimento Científico e
Tecnológico Regional, Universidade Estadual da Paraíba,
Campina Grande, Paraíba, Brazil

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 147
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_10
148 W. L. S. Vieira et al.

ment in faunal inventories in non-sampled areas and long-­ diversity (more than 720 species) is represented by amphib-
term ecological studies, which can help define priority ians (about 9.5% of the global diversity of this taxonomic
areas and support adequate conservation policies and group) (Vancine et  al. 2018; Figueiredo et  al. 2021), with
actions for amphibians in one of the most important and 70% (504 species) being endemic to this biome (Figueiredo
threatened areas of the Brazilian Atlantic Forest. et al. 2021).
Amphibians are a very diverse group in the Atlantic Forest
Keywords (Vasconcelos et al. 2014), being predominantly represented
by frogs (toads, frogs, and tree frogs), with more than 700
Amphibian · Diversity · Ecology · Conservation · known species (495 endemic), followed by Gymnophiona
Pernambuco Endemism Center · Northeastern Brazil (caecilians), with 12 known species (9 endemic) (Figueiredo
et  al. 2021). The biological attributes of Atlantic Forest
amphibians, such as their morphological structures, habitat
10.1 Introduction use, behavioral repertoires, reproductive modes, and devel-
opment patterns are also the most diversified worldwide
The Atlantic Forest is the second largest tropical rainforest (Vasconcelos et  al. 2014; Dubeux et  al. 2020a; Nunes-de-­
on the American continent and originally covered a total area Almeida et al. 2021).
of 1.5 million ha (Tabarelli et al. 2005; Muylaert et al. 2018; The distribution of amphibian species richness along the
Marques et  al. 2021). This forest block extended continu- Atlantic Forest is not homogeneous due to the broad latitudi-
ously as an arc along the Brazilian coast reaching eastern nal (contemplating tropical and subtropical areas) and longi-
Paraguay and northwestern Argentina (Muylaert et al. 2018; tudinal range (generating a temperature and precipitation
Marques et  al. 2021). According to phylogeographic and gradient from the coast to the interior) and the variation in
palynological evidence, the Atlantic Forest and the Amazon vegetation composition and elevation. This diversity follows
Forest were connected during the Quaternary (33,000– a geographic pattern with greater richness in the mountain-
25,000 years ago), and these two forests were then separated ous Serra do Mar region, decreasing toward the north and the
by the great South American diagonal of seasonally dry plant south of the biome (Peres et al. 2020; Figueiredo et al. 2021).
formations in the last glaciation (110,000–10,000 years ago) This distribution pattern presents regionalizations congruent
(Bigarella et al. 1975; Prado and Gibbs 1993; Costa 2003; with the endemic areas of the Atlantic Forest, which can be
Muylaert et al. 2018; Marques et al. 2021). divided into four biogeographic regions, as proposed by
The evolutionary history of the Atlantic Forest is quite Vasconcelos et al. (2014).
complex, and many hypotheses have been proposed to The North biogeographic region proposed by Vasconcelos
explain the diversification mechanisms of its fauna and flora et al. (2014) encompasses a region known as the Pernambuco
(Carnaval et al. 2009; Marques et al. 2021), such as the ref- Endemism Center (PEC), encompassing the coastal Atlantic
uge theory from the Pleistocene that resulted in the isolation Forest portion and the inland humid forest enclaves north of
and subsequent diversification of species (Ab’Saber 1977) the São Francisco River between the states of Alagoas and
originating the currently recognized endemism centers Rio Grande do Norte. This Atlantic Forest portion is mainly
(Carnaval and Moritz 2008); the uplift of Serra do Mar and distributed over the lowlands of the Barreiras Formation and
changes in ocean level that influenced landscape diversifica- the foothills of the Planalto da Borborema, up to 1000 m in
tion and climate change (Leite et al. 2016; Figueiredo et al. altitude, in northeastern Brazil (Tabarelli et  al. 2006a;
2021); the speciations resulting from species isolation by the Pereira-Filho et  al. 2020). The PEC has a high degree of
São Francisco, Jequitinhonha, Doce, and Paranapanema endemic species, which gives a unique identity to the area,
river basins (Dantas et al. 2011); and the divergence in spe- and is one of the lesser-known portions of the biome despite
cies composition between regions influenced by seasonally its high biological importance (Dubeux et al. 2020a; Pereira-­
dry vegetation formations such as the Cerrado and Caatinga Filho et  al. 2020). The amphibian fauna of this region is
(Cabanne et  al. 2011; Marques et  al. 2021). The complex composed of species with restricted range that presumably
evolutionary history and heterogeneity of Atlantic Forest evolved/survived extinction within Pleistocene forest ref-
environments are factors that may explain the great diversity uges (sensu Vasconcelos et al. 2014).
and high sectoral levels of endemism in this biome (Sobral-­ Given the incipient knowledge in relation to biodiversity
Souza and Lima-Ribeiro 2017; Figueiredo et al. 2021). at the northern portion of the Brazilian Atlantic Forest
Considered one of the biomes with the greatest biodiver- (Pernambuco Endemism Center), the objectives of this chap-
sity on the planet (Myers et  al. 2000; Vences and Kohler ter are: (a) to provide an updated list of amphibian species
2008; Mittermeier et al. 2011), the Atlantic Forest is home to for the region; (b) understand how species richness varies
more than 2600 species of terrestrial vertebrates, of which geographically and identify areas with high richness; (c) pro-
954 are endemic (Figueiredo et al. 2021). About 28% of this vide biological information and the conservation status of
10  Species Richness, Distribution Pattern, and Conservation of Amphibians in the Northern Portion of the Brazilian Atlantic Forest
the species; and (d) discuss the main threats to the PEC
amphibian populations. We hope that the information pre-
sented herein can support further studies and conservation
policies for the amphibian fauna of the most threatened por-
tion of the Atlantic Forest, as it is one of the regions with the
highest habitat loss rates and the lowest coverage of pro-
tected areas in the entire biome.
10.2 Amphibians from the Northern
Portion of the Brazilian Atlantic
Forest
The occurrence data for the amphibian species in the north-
ern portion of the Brazilian Atlantic Forest were obtained
from specimen data deposited in the following zoological
collections in the region: Herpetological Collection of the
Natural History Museum of the Federal University of
Alagoas (MHN-UFAL), Herpetology Collection of the
Federal University da Paraíba (CHUFPB), and Collection of
Herpetology and Paleoherpetology of the Federal Rural
University of Pernambuco (CHP-UFRPE/LEHP). The
records were complemented with information available in
the literature obtained from the Scopus, SciELO, Web of
Science, and Google Scholar databases using the key terms:
“Amphibia,” “amphibians,” “Atlantic Forest,” and “Northeast
of Brazil,” and combined terms using the names of the fed-
eration states inserted in the Pernambuco Endemism Center
(PEC), for example, “amphibians from Alagoas,” “amphibi-
ans from Paraíba,” or “amphibians from the Atlantic Forest
of Pernambuco,” from the use of the key search terms in
Portuguese and English. In parallel, the Lattes Curriculum of
all senior researchers located in institutions in the PEC states
(AL, PE, PB, RN) were visited and sorted in searching for
articles, books, and book chapters on the subject.
The taxonomic nomenclature followed Frost (2021), and
the phylogeny of amphibian families followed the hypothe-
sis of Jetz and Pyron (2018). Species with uncertainties
regarding taxonomic identification were excluded from the
list. The conservation status of each species followed the Red
Book of the International Union for the Conservation of
Nature and Natural Resources (IUCN 2021) and the Red
Book of the Endangered Brazilian Fauna of the Chico
Mendes Institute for Biodiversity Conservation (ICMBio
2018). The geographic distribution of species in the biomes
was obtained from the following works or databases: Silva
et  al. (2006), Oliveira et  al. (2010), Buarque-Júnior and
Moura (2011), Moura et  al. (2011), Santos (2011), Santos
and Santos (2011), Silva and Moura (2011), Haddad et  al.
(2013), Maciel et al. (2013a, b), Daher et al. (2014), de Sá
et  al. (2014), Chaves et  al. (2015), Langone et  al. (2015),
Moura et al. 2015, Santana et al. (2015, 2016), Santos et al.
(2016), Almeida et al. (2016a), Amorim et al. (2016), Mott
149
et  al. (2016), Barbosa et  al. (2017), Garda et  al. (2017);
Freitas et al. (2019), Andrade et al. (2016), Melo et al. (2018),
Abrahão et  al. (2019), Moura et  al. (2019), Lisboa et  al.
(2019), Dubeux et  al. (2020b), Andrade et  al. (2020),
Magalhães et al. (2020), Frost (2021), Oliveira et al. (2021),
Santos et al. (2021), and SiBBr (2021). The species occur-
rence frequency was categorized as frequent, infrequent, and
rare according to Haddad et al. (2013), considering the infor-
mation available for the locations inventoried in the PEC.
Biological information on species was obtained from refer-
ence works, for example, habitat use, habit, and calling sites
(Haddad et  al. 2013); reproductive modes (Haddad and
Prado 2005; Vieira et  al. 2009a; Nunes-de-Almeida et  al.
2021), and trophic guilds of larvaes (Altig and Johnston
1989; McDiarmid and Altig 1999; Dubeux et  al. 2019,
2020c).
The species richness distribution in the PEC was calcu-
lated using geographic data from species occurrence records,
computed using multiple GIS layers, with spatial reference
GCS_WGS_1984 in the QGIS 3.20.2 software program. The
spatial representation of richness was obtained through lin-
ear interpolation, with approximation calculated for every
three known record points (Law and Collins 2018). Thus, we
produced a total surface richness for the PEC amphibians
with regions ranging from low to high number of species.
10.2.1 Historical Synthesis of Northern
Portion of the Brazilian Atlantic Forest
Amphibian Studies
The first scientific studies on amphibians in the northern por-
tion of the Brazilian Atlantic Forest (Pernambuco Endemism
Center) date from the end of the nineteenth century in visits
by Boulenger (1888), who described Nototrema fissipes
(synonym of Gastrotheca fissipes), Hylodes plicifera (syn-
onym of Haddadus plicifer), and Hylodes ramagii (synonym
of Pristimantis ramagii) among his contributions to the
knowledge of the region in his work on reptiles and amphib-
ians from Iguarasse (now Igarassu), Pernambuco, Brazil. In
this same study, the author superficially described the exter-
nal morphology of the tadpole of Rana palmipes (synonym
of Lithobates palmipes) and recorded species identified as
Hyla rubra (species belonging to the clade Scinax ruber) and
Paludicola biligonigera (species of the clade Physalaemus
cuvieri).
During the first half of the twentieth century, Lutz (1926,
1930) presented detailed information on the species of the
Leptodactylus genus, including the description of new spe-
cies from Pernambuco Endemism Center (PEC). The study
presented an identification key and illustrations of 12
Leptodactylus species and the description of L. troglodytes
for the state of Pernambuco, without further specification; L.
150
natalensis for the municipality of Natal, Rio Grande do
Norte; L. vastus (previously identified as L. gigas) for
Independência, currently Guarabira municipality, Paraíba
state; and L. ochraceus for the state of Pernambuco (Engenho
Tapera), type-locality later designated as the municipality
São Lourenço da Mata (Caramaschi 2008).
Over the following years, 16 new species were described
for the PEC, 8 for the state of Alagoas, 7 for the state of
Pernambuco, and 1 for the state of Paraíba (Frost 2021).
Among the species described, we can highlight Phyllodytes
acuminatus Bokermann 1966, the first species described for
the state of Alagoas, as well as Crossodactylus dantei
Carcerelli and Caramaschi 1993, Phyllodytes gyrinaethes
Peixoto et al. 2003, and Scinax muriciensis Cruz et al. 2011,
all described for the municipality of Murici, in Alagoas.
Moreover, three new cryptic species have been described in
the last 2  years: Pithecopus gonzagai Andrade et  al. 2020,
whose type-locality is the municipality of Limoeiro, in
Pernambuco; Dendropsophus tapacurensis Oliveira et  al.
2021 from the Tapacurá Ecological Station, São Lourenço da
Mata, also in Pernambuco; and Adelophryne nordestina
Lourenço-de-Moraes et al. 2021, simultaneously registered
in the states of Pernambuco and Alagoas.
Although the study of PEC amphibians has progressively
increased in recent years, gaps still remain, such as knowl-
edge on the larval stage of these species (Dubeux et  al.
2020c). Currently, nine species of PEC amphibians do not
have their known tadpole (Vitreorana baliomma, Ceratophrys
joazeirensis, Crossodactylus dantei, Leptodactylus ochra-
ceus, Boana exastis, Dendropsophus tapacurensis, Scinax
muriciensis, S. cretatus, and Sphaenorhynchus cammaeus).
The work by Cruz and Peixoto (1982) on the biology of
Atelopus pernambucensis (synonym of Frostius pernambu-
censis), including the unprecedented description of its tad-
pole for the municipality of Recife, Pernambuco, can be
considered a pioneer. Although work with tadpoles in the
region grew significantly in the following years, they were
restricted to punctual descriptions (e.g., Pombal and
Madureira 1997; Pugliese et  al. 2000; Peixoto et  al. 2003;
Carvalho-e-Silva et  al. 2003; Carnaval and Peixoto 2004;
Alves et al. 2004; Nascimento and Skuk 2006, 2007; Vieira
et  al. 2007a, 2009b; Nascimento et  al. 2009, 2010; Lisboa
et  al. 2011a; Rodrigues et  al. 2017; Dubeux et  al. 2020d).
Works of a broader nature focused on tadpoles in the region
have begun to be made available only more recently, includ-
ing guides and identification keys (i.e., Andrade and Moura
2011a; Dubeux et al. 2019, 2020c).
Studies on PEC amphibian communities are also incipient,
with most of them being restricted to faunal inventories with
little or no information about the natural history of the species
(e.g., Santos et al. 1998; Santos and Carnaval 2002; Santana
et al. 2008; Santos 2011; Santos and Santos 2011; Silva and
Moura 2011; Buarque-Júnior and Moura 2011; Santos and
W. L. S. Vieira et al.
Moura 2012, Magalhães et al. 2013; Carvalho-e-­Silva et al.
2015; Santos et al. 2016; Almeida et al. 2016a; Roberto et al.
2017; Barbosa et al. 2017; Melo et al. 2018; Mesquita et al.
2018; Barbosa et  al. 2019, 2020; Dubeux et  al. 2020a, b;
Oliveira et al. 2021). Long-term ecological studies for PEC
amphibian communities do not exist. The first studies on pop-
ulation and community ecology descriptively presented the
composition of the diet of a few species (Santos et al. 2004),
their reproductive activity (Amorim et al. 2009; Santos and
Vasconcelos 2012), parasitology (Martins-Sobrinho et  al.
2017; Sena et al. 2018), habitat use and temporal distribution
(Albertim et al. 2010; Santos 2011; Silva and Moura 2011;
Lima et  al. 2011; Pereira et  al. 2016), autoecology (Lisboa
et al. al. 2011b; Caldas et al. 2016; Morais-Júnior et al. 2019;
Araújo et  al. 2020), and bioacoustics (Oitaven et  al. 2017;
Santos et al. 2020a). Only two studies tested the influence of
phylogenetic and ecological factors on niche partitioning pat-
terns in the use of microhabitats and diet in anuran communi-
ties (Leite-Filho et al. 2017; Caldas et al. 2019). Ecological
information regarding tadpole assemblages is very scarce,
and the only available works discuss the vertical distribution
(Souza et  al. 2011) and habitat segregation by tadpoles in
temporary ponds (Andrade et al. 2014).
Unfortunately, data on the natural history of species of the
order Gymnophiona are lacking for the PEC, and the informa-
tion available is restricted to occurrence records (e.g., Santana
et al. 2008; Moura et al. 2011; Maciel et al. 2013b; Almeida
et al. 2016a; Amorim et al. 2016; Mott et al. 2016). The lack of
information about caecilians is due to their fossorial habits and
the consequent difficulty in finding and collecting these ani-
mals. General knowledge about PEC amphibians has increased
significantly in the last 2 decades, mainly due to the strength-
ening of research groups established in public universities in
the region. It is expected that studies with amphibians in the
PEC will continue to grow exponentially through the partner-
ships and multidisciplinarity of these groups. As a result, it is
expected that some species will be described for the region in
the coming years, in addition to expanding knowledge about
their richness and distribution with the addition of inventoried
areas and ecological studies.
10.2.2 Species Richness, Endemism,
and Distribution Pattern
A total of 2019 species occurrence records were obtained for
the northern portion of the Brazilian Atlantic Forest, distrib-
uted in 128 locations in 109 municipalities in the states of
Alagoas, Pernambuco, Paraíba, and Rio Grande do Norte. In
total, 97 species belonging to two orders (95 from Anura and
2 from Gymnophiona), 15 families and 36 genera were
recorded (Fig. 10.1). Hylidae was the richest family with 43
species recorded, followed by Leptodactylidae with 23 spe-
10  Species Richness, Distribution Pattern, and Conservation of Amphibians in the Northern Portion of the Brazilian Atlantic Forest
cies, and together these two families account for about 68%
of the richness in the region (Figs. 10.1 and 10.2; Appendix).
There were records of an invasive species, Lithobates cates-
beianus, for the municipality of Maceió (Alagoas state),
Paulista, Igarassu and Recife (Pernambuco state), and
Parnamirim (Rio Grande do Norte state) (Giovanelli et  al.
2008; Moura et al. 2019; Instituto Hórus 2021).
The regional richness of Pernambuco Endemism Center
(PEC) amphibians ranged from low to high number of spe-
cies (<8–52 spp.; Fig.  10.3). The areas of greatest species
richness are located in the central portion of the PEC in the
states of Alagoas and Pernambuco (Fig.  10.3), places with
richness ranging between 15 and 52 species (e.g., Moura
et al. 2011; Almeida et al. 2016a; Santos et al. 2016; Freitas
et al. 2019; Dubeux et al. 2020c; Oitaven et al. 2021; Oliveira
et al. 2021). In addition to being historically better studied,
this portion of the PEC also presents the largest remnant
fragments and continuous vegetation, presenting Dense
Ombrophilous Forest phytophysiognomy, with higher
humidity when compared to forest fragments in the north of
the PEC, which are more influenced by Caatinga phytophys-
iognomies in the west of the states (Tabarelli et  al. 2006a;
Nemésio and Santos-Junior 2014). The northernmost portion
presents lower richness, with a maximum of 34 species
recorded in seasonal semi-deciduous forest areas (i.e.,
Mesquita et al. 2018) and in ecotonal areas of Atlantic Forest
with Caatinga (i.e., Magalhães et al. 2013).
Fig. 10.1  Species richness by amphibian family from the northern portion of the Brazilian Atlantic Forest (Pernambuco Endemism Center). The
phylogeny of the families followed Jetz and Pyron (2018) and the amphibian silhouettes are from phylopic. (http://www.phylopic.org/)
151
Regarding endemism, a total of 50 species are endemic to
the Atlantic Forest, of which 14 (28% of the total endemic
spp) are restricted to the PEC; 8 belonging to the Hyidade
family (Boana freicanecae, Phyllodytes acuminatus, P. bre-
virostris, P. edelmoi, P. gyrinaethes, Scinax muriciensis, S.
skuki, and Sphaenorhynchus cammaeus); 2 are from the
Leptodactylidade family (Leptodactylus ochraceus e
Physalaemus caete); and only 1 for the Craugastoridae
(Haddadus plicifer), Eleutherodactylidae (Adelophryne nor-
destina), Hylodidae (Crossodactylus dantei), and
Microhylidae (Chiasmocleis alagoana) (Appendix). The
areas of greatest endemism coincide with those with the
greatest species richness in the PEC (Fig.  10.3). The area
with the highest number of species restricted to the PEC was
the Murici Ecological Station (ESEC), Alagoas state, with
nine species (Almeida et  al. 2016a). This followed by the
Frei Caneca Private Natural Heritage Reserve (Reserva
Particular do Patrimônio Natural—RPPN) and Pedra Dantas
RPPN, both located in the state of Pernambuco, with four
endemic species each (Moura et  al. 2011; Roberto et  al.
2017); Caetés ESEC and Marechal Newton Cavalcanti
Instruction Center, both in the state of Pernambuco;
Environmental Protection Area of Catolé and Fernão Velho,
state of Alagoas; and the Pedra Talhada Biological Reserve
(REBIO), Alagoas and Pernambuco states, with three PEC
endemic species each (Barbosa et  al. 2017; Dubeux et  al.
2020a, b; Oitaven et al. 2021).
152
Fig. 10.2  Example of some amphibian species from the northern portion of
the Brazilian Atlantic Forest (Pernambuco Endemism Center).
Aromobatidae: (a) Allobates olfersioides; Bufonidae: (b) Frostius pernam-
bucensis, (c) Rhinella hoogmoedi, Centrolenidae: (d) Vitreorana baliomma;
Ceratophryidae: (e) Ceratophrys joazeirensis; Craugastoridae: (f)
Pristimantis ramagii; Eleutherodactylidae: (g) Adelophryne nordestina;
Hemiphractidae: (h) Gastrotheca fissipes; Hylidae: (i) Aplastodiscus sibila-
tus, (j) Boana freicanecae, (k) Dendropsophus tapacurensis, (l) Phyllodytes
W. L. S. Vieira et al.
gyrinaethes, (m) Scinax muriciensis; Hylodidae: (n) Crossodactylus dantei;
Leptodactylidae: (o) Leptodactylus latrans, (p) Physalaemus cuvieri;
Odontophrynidae: (q) Macrogenioglottus alipioi, (r) Proceratophrys rena-
lis; Microhylidae: (s) Chiasmocleis alagoana, (t) Stereocyclops incrassatus,
Phyllomedusidae: (u) Hylomantis granulosa; Pipidae: (v) Pipa carvalhoi;
Ranidae: (w) Lithobates palmipes; Siphonopidae: (x) Siphonops paulensis.
(Photograph by Washington L S Vieira (e), Cláudio Sampaio (x) and other
photographs by Marcos J M Dubeux)
10  Species Richness, Distribution Pattern, and Conservation of Amphibians in the Northern Portion of the Brazilian Atlantic Forest
Fig. 10.3  Amphibian species richness distribution map of the northern portion of the Brazilian Atlantic Forest. (Pernambuco Endemism Center)
Of the 97 species recorded, 50 have a restricted distribu-
tion to the Atlantic Forest, 15 were recorded, which are reg-
istered both in the Atlantic Forest and the Caatinga, 1 has
disjoint distribution occurring in the Atlantic Forest and
Cerrado, and 31 have wide continental distribution with
records in at least three biomes (Appendix). Some typical
species of the Atlantic Forest (e.g., Boana albomarginata, B.
faber, Dendropsophus decipiens, D. oliveirai, Leptodactylus
payaya, Pristimantis ramagii, Proceratophrys renalis,
Rhinella crucifer, and Scinax cretatus) can be found in the
morphoclimatic domain of the Caatinga, but restricted to
submontane humid forest enclaves called “brejos de alti-
tude” (i.e., Freitas et al. 2019; Barbosa et al. 2020). In addi-
tion, endemic species of the Caatinga (sensu Garda et  al.
2017), such as Ceratophrys joazeirensis, Leptodactylus caat-
ingae, Proceratophrys cristiceps, Physalaemus cicada, P.
kroyeri, Pseudopaludicola pocoto, and Scinax pachycrus,
were also recorded in the “brejos de altitude” and in ecotonal
areas with the Atlantic Forest biome (e.g., Moura et al. 2011;
Magalhães et  al. 2013; Freitas et  al. 2019; Dubeux et  al.
2020a, b, c, d).
153
The composition of the PEC amphibian fauna is propor-
tionally constituted by species with restricted distribution to
the Atlantic Forest and species with wide distribution in the
South American diagonal of seasonally dry plant formations
(Appendix; e.g., Vieira et  al. 2007b; Moura et  al. 2011;
Almeida et  al. 2016a; Garda et  al. 2017). This faunal
­composition characterizes the PEC area as a transition region
between the phytogeographic domains of the Atlantic Forest
and Caatinga which, added to the endemic species of this
region, gives the PEC a unique and significantly different
faunal identity from that found in other Atlantic Forest
regions (Vasconcelos et  al. 2014). A similar pattern was
observed in seasonal semi-deciduous forest fragments of the
Atlantic Forest in relation to the flora, whose composition is
formed by wide distribution species in the Caatinga and
Cerrado (Cestaro and Soares 2004).
The Pernambuco Endemism Center amphibian fauna may
be the result of a complex biogeographic history that occurred
in the northern portion of the Atlantic Forest during the late
Paleogene to the Quaternary periods (Bigarella et al. 1975;
Costa 2003; de Sá et al. 2019; Marques et al. 2021). Multiple
154
connections between the Amazon and the Atlantic Forest
were suggested based on phylogeographic evidence using
amphibians, “reptiles,” mammals, birds, and plants as mod-
els (Santos et al. 2007; Carnaval et al. 2009; Ledo and Colli
2017; de Sá et  al. 2019). In addition, anuran phylogenetic
hypotheses suggested that several endemic lineages of the
Atlantic Forest share a more recent common ancestor with
amazonian species (Blackburn and Duellmand 2013;
Caminer et al. 2017; de Sá et al. 2019).
Eocene–Oligocene climate fluctuations (35-33 mya)
likely caused the contraction and separation of previously
continuous tropical forest areas that generated rainforest
refugia (Zachos et al. 2001; Jaramillo et al. 2010; de Sá et al.
2019). These areas may have isolated lineages that diverged,
giving rise to endemic species with a restricted distribution
to the north of the Atlantic Forest (Blackburn and Duellmand
2013; Vasconcelos et  al. 2014; Caminer et  al. 2017; de Sá
et  al. 2019). In addition, more recent climate change with
alternating wet and dry conditions during the Quaternary
also resulted in forest expansions and shrinkages, which
shaped the landscape, again giving rise to humid forest ref-
uges during dry periods at the Last Glacial Maximum (LGM)
during the Pleistocene (Oliveira et  al. 1999; Wang et  al.
2004; Vieira et  al. 2018; Baker et  al. 2020). At this time,
many species probably survived and differentiated from
being isolated on islands of humid forests in the northern
portion of the Atlantic Forest (“Pernambuco refugium”)
(Carnaval et  al. 2009; Vasconcelos et  al. 2014). With the
resumed warmer and wetter periods with recurrent extreme
rains during the Holocene, there was again an expansion of
forest areas (Oliveira et al. 1999; Wang et al. 2004).
Changes in the environment during the Quaternary sig-
nificantly influenced the diversification of the South
American biota. However, the nature of the diversification
was probably more complex than initially hypothesized by
the Pleistocene refuge theory (Baker et al. 2020). Successive
intermittent expansions and contractions of forest areas,
influenced by alternating wet and dry conditions during the
Quaternary, probably led to dispersal and subsequent isola-
tion of species, promoting diversified lineages. In addition,
an exchange of biota changed the composition and regional
species richness, triggering new evolutionary radiations in
the northern portion of the Atlantic Forest (Prates et al. 2016;
Baker et al. 2020).
W. L. S. Vieira et al.
10.2.3 Conservation
According to the most recent assessments by the IUCN
(2021), the amphibian fauna of the Pernambuco Endemism
Center (PEC) has four species threatened with extinction at a
global level, two of which are categorized as Vulnerable
(VU; Allobates olfersioides and Adelophryne baturitensis),
one Endangered (EN; Scinax skuki), and one Critically
Endangered (CR; S. muriciensis). In addition, 71 species are
considered Least Concern (LC), 14 species have Deficient
Data for evaluation (DD), and 10 Not Evaluated (NE)
(Appendix). Regarding an assessment at the national level
according to ICMBio (2018), seven species are currently
threatened with extinction, namely, two Vulnerable (VU; A.
olfersioides and Hylomantis granulosa), three Endangered
(EN; Crossodactylus dantei, Physalaemus caete and
Chiasmocleis alagoana), and two Critically Endangered
(Phyllodytes gyrinaethes and S. muriciensis). In addition, 1
is considered Near Threatened (NT; P. edelmoi), 70 are con-
sidered Least Concern (LC), 13 are classified as Deficient
Data (DD), and 7 as Not Evaluated (NE) (Appendix).
Among the states covered by the PEC, only the state of
Pernambuco has an official list of threatened species (SEMAS
Resolution n° 01/2015), upon which 12 species registered
for the PEC are considered threatened in the state, three of
which are classified as Vulnerable (VU; Frostius pernambu-
cencis, Gastrotheca fissipes, and H. granulosa), seven as
Endangered (EN; A. olfersioides, Boana exastis, B. freican-
ecae, P. acuminatus, P. brevirostris, P. edelmoi, and P. gyri-
naethes), and two as Critically Endangered (CR; G. pulchra
and P. caete) (Moura et al. 2019). Considering the endemic
species of the PEC, two are considered threatened on the
global list (IUCN 2021), six on the national list (ICMBio
2018), and seven on the list of the state of Pernambuco
(Moura et al. 2019) (Appendix). Although Adelophryne nor-
destina and Dendropsophus tapacurensis have recently been
described and have not yet had the opportunity to be evalu-
ated in any of the available threatened species lists, they will
possibly be classified at some threat level as they meet some
of the criteria used, such as restricted geographic distribution
and constant loss of habitat.
The species in the different threat categories of the IUCN
(2021), ICMBio (2018), and the state of Pernambuco list
(Moura et  al. 2019) are endemic to the Atlantic Forest,
10  Species Richness, Distribution Pattern, and Conservation of Amphibians in the Northern Portion of the Brazilian Atlantic Forest
dependent on forested areas and with infrequent or rare
occurrence frequencies (sensu Haddad et  al. 2013)
(Appendix). Furthermore, population trend information pro-
vided by the IUCN (2021) indicates that 49 species are sta-
ble, 26 unknown, 21 decreasing, and 1 increasing (Appendix).
Although most amphibians in the PEC are considered the
least concern and with a stable population, a representative
number is threatened (most endemic to the Atlantic Forest
and restricted to the PEC), in decline, or with no population
data (Appendix). These results indicate a worrying situation
in relation to species conservation in the PEC, since most
states do not have official lists of threatened species.
Furthermore, data from the national action plan for the con-
servation of threatened herpetofauna in the Atlantic Forest of
northeastern Brazil suggest more effective measures in spe-
cies conservation (Abrahão et al. 2019).
Threats to the PEC amphibian fauna are similar to those
affecting the morphoclimatic domain of the Atlantic Forest
as a whole: high deforestation and habitat degradation rates,
use of pesticides in agricultural fields, air and water pollu-
tion, extensive livestock raising, introduction of invasive
alien species, pathogens, illegal removal of bromeliads, and
climate change (Abrahão et  al. 2019). All of these factors,
along with others, synergistically act together in complex
interactions and have increased the threat to PEC amphibians
in recent decades (Sobral-Souza et al. 2018).
Historical deforestation mainly caused by expanding the
agricultural frontier, extensive cattle raising, and unplanned
urban sprawl have reduced the original area of the Atlantic
Forest to only 15% of its original extent (Tabarelli et  al.
2006b). The northern portion of the Brazilian Atlantic Forest
was historically one of the areas most affected by deforesta-
tion, currently being represented by less than 6% of its original
coverage (Tabarelli et al. 2006b). This remaining cover mostly
consists of small fragments (mostly smaller than 50  ha)
immersed in a matrix of monocultures and pastures (Uchoa-
Neto and Tabarelli 2002; Tabarelli et al. 2006b; Fundação SOS
Mata Atlântica 2021; Solórzano et al. 2021). The intense habi-
tat fragmentation generates a loss of connectivity of forest
remnants, which can lead to a reduction in gene flow and con-
sequently to an inbreeding depression in populations; in turn,
associated with the number of species described in recent
years, this disappearance of populations can lead to extinction
155
of species, which have not yet been discovered by science
(Tabarelli et al. 2006b; Haddad et al. 2013).
Associated with the negative effects of habitat fragmenta-
tion, the impact of roads on the terrestrial vertebrate fauna is
another threat that deserves attention (Grilo et  al. 2018).
Vehicle traffic causes high mortality for frogs, especially
during the reproductive period, when many individuals are
run over when crossing roads in search of breeding sites,
during the dispersion of young individuals or when adult
individuals migrate between forest fragments (Silva et  al.
2007; Andrade and Moura 2011b; Almeida et al. 2016b). In
addition, the increase in agricultural activities and extensive
cultivation of monocultures, usually using pesticides and
herbicides (including glyphosate), cause malformations and
mortality in amphibians at different development stages,
which can lead to local extinction of species (Gonçalves
et  al. 2017; Ferrante et  al. 2017; Ferrante and Fearnside
2020); furthermore, it constitutes a threat aggravated by the
fact that the period of increased application of pesticides and
herbicides in crops coincides with the amphibians’ breeding
season during the rainy season, which, in addition to carry-
ing a higher concentration of substances to water bodies,
increases the chances of interfering with the reproductive
success of populations (Gonçalves et al. 2017).
The presence of alien-invasive species is another factor of
great concern, since the occurrence of Lithobates catesbeia-
nus and some alien species of Testudines (Trachemys elegans
and T. dorbigni) were registered in the PEC (Giovanelli et al.
2008; Moura et al. 2019; Santos et al. 2020b; Instituto Hórus
2021). These species are very competitive, and they can neg-
atively impact native amphibian populations as they do not
have natural predators that regulate their population growth,
preying on tadpoles and adults, in addition to disturbing the
structure of aquatic communities (Leão et al. 2011; Moura
et  al. 2019). In addition, L. catesbeianus individuals are
potential reservoirs of the aquatic keratinophilic fungus
Batrachochytrium dendrobatidis (BD) (Leão et  al. 2011;
Silva et al. 2013), which causes the so-called chytridiomyco-
sis. This pathogen has been indicated as one of those respon-
sible for the decline and extinction of amphibian populations
in various parts of the world (Carnaval et al. 2006; Scheele
et  al. 2019). The presence of this fungus in the PEC has
already been confirmed for amphibian populations in all
156
states (Carnaval et  al. 2006; Lisboa et  al. 2013; Valencia-­
Aguilar et al. 2015; Lambertini et al. 2021).
Amphibians are especially vulnerable to climate change
because they are ectodermal animals, which regulate their
body temperature through an external source of heat. They
also have thin and permeable skin, so they are very suscepti-
ble to dehydration; in addition, their reproductive cycles are
related to temperature and precipitation variations and depend
on aquatic environments for reproduction (Blaustein et  al.
2001; Loyola et al. 2014; Vilela et al. 2018). A study devel-
oped with PEC frogs indicates that endemic species and
restricted geographic distribution will possibly be negatively
affected by climate change due to unfavorable conditions in
temperature and precipitation regimes (Vilela et al. 2018).
Despite the PEC having high species richness and high
endemism rate, only 3.7% of its total area remains protected
(Uchoa-Neto and Tabarelli 2002). Almost all of the PEC’s
Atlantic Forest remnants are located within private proper-
ties, mainly belonging to large sugar and alcohol production
plants (Uchoa-Neto and Tabarelli 2002) and secondarily in
areas of use by the armed forces. Legally protected areas
during the first years of the last decade totaled 113 conserva-
tion units, of which 69 are federal full protection conserva-
tion units (CUs) and only one of sustainable use (Uchoa-Neto
and Tabarelli 2002). Despite this, most PEC conservation
units have irregular shapes, are smaller than 5000 ha, are sur-
rounded by monoculture and pasture matrices, do not present
connectivity between forest fragments, and have been under-
going continuous changes in structure and floristic composi-
tion due to the edge effect (Uchoa-Neto and Tabarelli 2002).
If not resolved, all of these problematic aspects, added to the
constant pressure still exerted on these areas, reduce the
effectiveness of the objectives of the PEC CUs, making these
areas ecologically unfeasible in the long term (Forman 1997;
Uchoa-Neto and Tabarelli 2002; Sobral-Souza et al. 2018).
The conservation actions for amphibians in the PEC
(Abrahão et al. 2019; Machado et al. 2021) recommend ade-
quate inspection and management of conservation unit areas
W. L. S. Vieira et al.
(CUs), implementation of new integral protected areas,
greater stimulus for creating new Private Natural Heritage
Reserves (RPPNs), establishment of connectivity between
isolated forest fragments, support and encouragement of
more sustainable agricultural practices in monoculture fields
around forest fragments, mapping priority areas for conser-
vation, and developing research aimed at the recovery of
degraded areas.
Finally, support for scientific research, especially new
field inventories, monitoring and control of invasive alien
species and the BD fungus, developing environmental edu-
cation programs with greater dissemination and populariza-
tion of species, developing long-term ecological studies on
the structure of communities (larval and adult stages), and
research with computer models, which indicate the possible
negative effects of climate change on species, are all neces-
sary. Such actions are fundamental and of an emergency
nature for better conservation of amphibians in one of the
most important and threatened areas of the Atlantic Forest
and, in turn, will enable creating more efficient management
plans for the conservation of these species and the ecosys-
tems they inhabit (Moura et al. 2019, Machado et al. 2021).
Acknowledgments We would like to thank Professor Paulo
G.  Montenegro for his support in the Laboratory of Animal
Ecophysiology of the Department of Systematics and Ecology (DSE);
biologist Dr. Fagner R.  Delfim for providing information from the
records of amphibian specimens in the Herpetology Collection of the
DSE-UFPB (CHUFPB); the Conselho Nacional de Desenvolvimento
Científico e Tecnológico (CNPq), process 477121/2011-0 and
476058/2013-9, for financial support; FAPESQ—Fundação de Apoio à
Pesquisa do Estado da Paraíba (Edital 002/13-FAPESQ/MCT/CNPq.
Proc.: 313232/2015-6 and 300324/2018-9) for the research grant to
Kleber S Vieira and Edital 09/2021, No 3127/2021 for financial support;
the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
(CAPES) for the Master’s scholarship to Francisco VM Júnior; and to
the Graduate Program in Biodiversity at UFPB.  MJMD thanks the
Fundação de Amparo à Ciência e Tecnologia do Estado de
Pernambuco—FACEPE (IBPG-1117-2.04/19); and TM thanks the
Conselho Nacional de Desenvolvimento Científico e Tecnológico—
CNPq (309904/2015-3 e 312291/2018-3) for financial support.
 ppendix: Amphibian Species Recorded at the Northern Portion of the Brazilian Atlantic Forest (Pernambuco Endemism
A
Center), Northeastern Brazil
Frequency of Continental Habitat Habit Calling sites Reprodu- Trophic guilds of Endemic of Population Conservation
occurrence distribution ctive mode larvaes the PEC trend status
Species IUCN ICMBio
ANURA
Aromobatidae
Allobates olfersioides (Lutz 1925) Infrequent AF Fa Te/ Ri, St 28 Bentonic No Decreasing VU VU
Rh
Bufonidae
Frostius pernambucensis Rare AF Fa Ar/ Br 4 Endotrophic No Decreasing LC DD
(Bokermann 1962) Cr
Rhinella crucifer (Wied-Neuwied Frequent AF Fa, Oa Te Sw, Po, Ri, 2 Bentonic No Decreasing LC LC
1821) St
Rhinella granulosa (Spix 1824) Frequent AF, Ca, Ce Fa, Oa Te Sw, Po 2 Bentonic No Stable LC LC
Rhinella diptycha (Cope 1862) Frequent AF, Ca, Ce, Am Fa, Oa Te Sw, Po, Ri, 2 Bentonic No Stable LC LC
St
Rhinella hoogmoedi (Caramaschi Frequent AF Fa Te Sw, Po 2 Bentonic No Unknown LC LC
and Pombal 2006)
Centrolenidae
Vitreorana baliomma (Pontes Rare AF Fa Ar Ri, St Bentonic No Decreasing LC DD
et al. 2014)
Ceratophryidae
Ceratophrys joazeirensis Infrequent AF, Ca Oa Te Sw, Po 1 Unknown No Unknown DD DD
(Mercadal de Barrio 1986)
Craugastoridae
Haddadus plicifer (Boulenger Rare AF Fa Te/Cr Ff 27 Direct Yes Unknown DD DD
1888) development
Pristimantis ramagii (Boulenger Frequent AF, Ca Fa Te/Cr Ff, Lv 27 Direct No Decreasing LC DD
1888) development
Pristimantis vinhai (Bokermann Infrequent AF Fa Te/Cr Ff 27 Direct No Decreasing LC LC
1975) development
Eleutherodactylidae
Adelophryne baturitensis Infrequent AF Fa Te/Cr Ff 27 Direct No Decreasing VU LC
(Hoogmoed et al. 1994) development
Adelophryne nordestina Infrequent AF Fa Te/Cr Ff 27 Direct Yes Unknown NE NE
(Lourenço-de-Moraes et al. 2021) development
Hemiphractidae
Gastrotheca fissipes (Boulenger Rare AF Fa Ar Tc/Ve 69 Paraviviparous No Stable LC DD
1888)
Gastrotheca pulchra (Caramaschi Rare AF Fa Ar Tc/Ve 69 Paraviviparous No Unknown DD DD
and Rodrigues 2007)
10  Species Richness, Distribution Pattern, and Conservation of Amphibians in the Northern Portion of the Brazilian Atlantic Forest

Hylidae
Aplastodiscus sibilatus (Cruz Infrequent AF Fa Ar Sw, Po, Ri, 10 Bentonic No Unknown DD DD
157

et al. 2003) St
 Frequency of Continental Habitat Habit Calling sites Reprodu- Trophic guilds of Endemic of Population Conservation
158

occurrence distribution ctive mode larvaes the PEC trend status

Species IUCN ICMBio
Boana albomarginata (Spix Frequent AF Fa, Oa Ar Sw, Po, Ve 1 Bentonic No Stable LC LC
1824)
Boana atlantica (Caramaschi and Frequent AF Fa, Oa Ar Sw, Po, Ri, 16 Bentonic No Stable LC LC
Velosa 1996) St, Ve
Boana crepitans (Wied-Neuwied Frequent AF, Ca, Ce Fa, Oa Ar Sw, Po, Ve 1 and 12 Bentonic No Stable LC LC
1824)
Boana exastis (Caramaschi and Rare AF Fa Ar Sw, Po, Ri, 16 Unknown No Unknown DD LC
Rodriguez 2003) St, Ve
Boana faber (Wied-Neuwied Frequent AF Fa, Oa Ar Sw, Po, Ve 1 and 12 Bentonic No Stable LC LC
1821)
Boana freicanecae (Carnaval and Infrequent AF Fa Ar Ri, St, Ve 16 Bentonic Yes Unknown DD DD
Peixoto 2004)
Boana raniceps (Cope 1862) Frequent AF, Ca, Ce, Am, Fa, Oa Ar Sw, Po, Ve 1 Bentonic No Stable LC LC
Ch, Pa
Boana semilineata (Spix 1824) Frequent AF Fa Ar Sw, Po, Ri, 16 Bentonic No Stable LC LC
St, Ve
Corythomantis greeningi Frequent AF, Ca, Ce Oa Ar Sw, Po, Ri, 1 Bentonic No Stable LC LC
(Boulenger 1896) St, Ve
Dendropsophus branneri Frequent AF, Ca, Ce Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
(Cochran 1948) Ve
Dendropsophus decipiens (Lutz Infrequent AF Fa, Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
1925) Ve
Dendropsophus dutrai (Gomes Infrequent AF Oa Ar Sw, Po, Lv, 1 Unknown No Unknown DD DD
and Peixoto 1996) Ve
Dendropsophus elegans Frequent AF Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
(Wied-Neuwied 1824) Ve
Dendropsophus minutus (Peters Frequent AF, Ca, Ce, Am, Oa Ar Sw, Po, Lv, 3 Nektonic No Stable LC LC
1872) Ch, Pa, Pp Ve
Dendropsophus nanus (Boulenger Frequent AF, Ca, Ce, Am, Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
1889) Ch, Pa, Pp Ve
Dendropsophus oliveirai Frequent AF Oa Ar Sw, Po, Lv, 1 Nektonic No Decreasing LC LC
(Bokermann 1963) Ve
Dendropsophus soaresi Frequent AF, Ca Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
(Caramaschi and Jim 1983) Ve
Dendropsophus studerae Infrequent AF Fa Ar Sw, Po, Lv, 1 Nektonic No Unknown DD DD
(Carvalho-e-Silva et al. 2003) Ve
Dendropsophus tapacurensis Frequent AF Fa, Oa Ar Sw, Po, Lv, 22 Nektonic No Unknown NE NE
(Oliveira et al. 2021) Ve
Phyllodytes acuminatus Frequent AF Fa Ar/ Br 4 Arboreal Yes Decreasing LC NT
(Bokermann 1966) Ph
Phyllodytes brevirostris (Peixoto Infrequent AF Fa Ar/ Br 4 Arboreal Yes Decreasing DD DD
and Cruz 1988) Ph
Phyllodytes edelmoi (Peixoto Infrequent AF Fa Ar/ Br 4 Arboreal Yes Decreasing DD NT
W. L. S. Vieira et al.

et al. 2003) Ph
 Frequency of Continental Habitat Habit Calling sites Reprodu- Trophic guilds of Endemic of Population Conservation
occurrence distribution ctive mode larvaes the PEC trend status
Species IUCN ICMBio
Phyllodytes gyrinaethes (Peixoto Infrequent AF Fa Ar/ Br 4 Arboreal Yes Decreasing DD CR
et al. 2003) Ph
Phyllodytes luteolus (Wied-­ Frequent AF Fa Ar/ Br 4 Arboreal No Decreasing LC LC
Neuwied 1824) Ph
Scinax auratus (Wied-Neuwied Frequent AF Fa Ar/ Sw, Po, Lv, 1 Nektonic No Stable LC LC
1821) Ph Ve
Scinax cretatus (Nunes and Frequent AF Fa, Oa Ar Sw, Po, Lv, 1 Unknown No Unknown LC LC
Pombal 2011) Ve
Scinax eurydice (Bokermann Frequent AF Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
1968) Ve
Scinax fuscomarginatus (Lutz Frequent AF, Ca, Ce, Am, Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
1925) Ch, Pa Ve
Scinax fuscovarius (Lutz 1925) Frequent AF, Ca, Ce, Am, Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
Ch, Pa Ve
Scinax melanodactylus Infrequent AF Fa, Oa Ar Sw, Po, Lv, Unknown Nektonic No Unknown NE NE
(Lourenço, Luna and Pombal Ve
2014
Scinax muriciensis (Cruz et al. Rare AF Fa Ar Sw, Po, lv, Unknown Nektonic Yes Decreasing CR CR
2011) Ve
Scinax nebulosus (Spix 1824) Frequent AF, Ca, Ce, Am, Fa, Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
Pa Ve
Scinax pachycrus (Miranda-­ Frequent AF, Ca Fa, Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
Ribeiro 1937) Ve
Scinax ruber (Laurenti 1768) Infrequent AF, Ce, Am, Pa Fa, Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
Ve
Scinax skuki (Lima et al. 2011) Rare AF Fa Ar Sw, Po, Lv, Unknown Bentonic Yes Decreasing EN DD
Ve
Scinax x-signatus (Spix 1824) Frequent AF, Ca, Ce, Am, Fa, Oa Ar Sw, Po, Lv, 1 Nektonic No Stable LC LC
Pa Ve
Scinax tropicalia (Novaes-e-­ Infrequent AF Fa, Oa Ar Sw, Po, Lv, 1 Unknown No Unknown NE NE
Fagundes et al. 2021) Ve
Sphaenorhynchus cammaeus Rare AF Fa Ar Sw, Po, Lv, 3 Unknown Yes Unknown NE NE
(Roberto et al. 2017) Ve
Sphaenorhynchus prasinus Infrequent AF Fa, Oa Ar Sw, Po, Lv, 3 Bentonic No Decreasing LC LC
(Bokermann 1973) Ve
Trachycephalus atlas (Bokermann Infrequent AF, Ca Oa Ar Sw, Po 2 Nektonic No Unknown LC LC
1966)
Trachycephalus mesophaeus Infrequent AF Fa Ar Sw, Po 2 Nektonic No Decreasing LC LC
(Hensel 1867)
Trachycephalus nigromaculatus Infrequent AF, Ce Fa, Oa Ar Sw, Po, Lv, 2 and 16 Nektonic No Stable LC LC
(Tschudi 1838) Ve
Trachycephalus typhonius Frequent AF, Am, Ce Fa, Oa Ar Sw, Po 16 Nektonic No Stable LC LC
(Linnaeus 1758)
10  Species Richness, Distribution Pattern, and Conservation of Amphibians in the Northern Portion of the Brazilian Atlantic Forest
159
 Frequency of Continental Habitat Habit Calling sites Reprodu- Trophic guilds of Endemic of Population Conservation
160

occurrence distribution ctive mode larvaes the PEC trend status

Species IUCN ICMBio
Hylodidae
Crossodactylus dantei (Carcerelli Rare AF Fa Te/ Ri, St Unknown Unknown Yes Decreasing DD EN
and Caramaschi 1993) Rh
Leptodactylidae
Adenomera aff. hylaedactyla Frequent AF, Ca, Ce, Am Fa, Oa Te/Cr Ff, Lv 62 Endotrophic No Stable LC LC
(Cope 1868) nidicolous
Leptodactylus caatingae (Heyer Infrequent AF, Ca Oa Te Sw, Po 64 Bentonic No Unknown LC LC
and Juncá 2003)
Leptodactylus fuscus (Schneider Frequent AF, Ca, Ce, Am, Oa Te Sw, Po 64 Bentonic No Stable LC LC
1799) Ch, Pa, Pp
Leptodactylus latrans (Steffen Infrequent AF Oa Te Sw, Po 45 Bentonic No Stable LC LC
1815)
Leptodactylus macrosternum Frequent AF, Ca, Ce, Am, Oa Te Sw, Po 45 Bentonic No Stable LC LC
(Miranda-Ribeiro 1926) Ch, Pa
Leptodactylus mystacinus Frequent AF, Ca, Ce, Am, Oa Te Sw, Po 64 Bentonic No Stable LC LC
(Burmeister 1861) Ch, Pa
Leptodactylus natalensis (Lutz Frequent AF Fa Te/Cr Sw, Po 50 Bentonic No Stable LC LC
1930
Leptodactylus ochraceus (Lutz Rare AF Fa Te/Cr Unknown Unknown Unknown Yes Unknown NE DD
1930
Leptodactylus payaya (Magalhães Infrequent AF, Ca Fa, Oa Te Sw, Po 45 Bentonic No Unknown NE NE
et al. 2020)
Leptodactylus spixi (Heyer 1983) Infrequent AF Fa Te/Cr Sw, Po 64 Bentonic No Stable LC LC
Leptodactylus syphax Infrequent AF, Ca, Ce Oa Te/ Ri, St 63 Bentonic No Stable LC LC
(Bokermann 1969) Rh
Leptodactylus troglodytes A. Lutz Frequent AF, Ca, Ce Oa Te Sw, Po, Ri, 64 Bentonic No Stable LC LC
1926 St
Leptodactylus vastus A. Lutz Frequent AF, Ca, Ce Oa Te Sw, Po, Ri, 44 and 50 Bentonic No Stable LC LC
1930 St
Physalaemus albifrons (Spix Frequent AF, Ca, Ce Oa Te Sw, Po 45 Bentonic No Stable LC LC
1824)
Physalaemus caete (Pombal and Rare AF Fa Te Sw, Po 45 Bentonic Yes Decreasing DD EN
Madureira 1997)
Physalaemus cicada (Bokermann Frequent AF, Ca Oa Te Sw, Po 45 Bentonic No Stable LC LC
1966)
Physalaemus cuvieri (Fitzinger Frequent AF, Ca, Ce, Am, Oa Te Sw, Po 45 Bentonic No Stable LC LC
1826) Ch, Pa, Pp
Physalaemus kroyeri (Reinhardt Infrequent AF, Ca Oa Te Sw, Po 45 Bentonic No Stable LC LC
and Lütken 1862)
Pleurodema diplolister (Peters Frequent AF, Ca, Ce Oa Te Sw, Po 45 Bentonic No Stable LC LC
1870)
Pseudopaludicola jaredi Infrequent AF, Ca Oa Te Sw, Po 3 Bentonic No Unknown NE NE
(Andrade et al. 2016)
W. L. S. Vieira et al.
 Frequency of Continental Habitat Habit Calling sites Reprodu- Trophic guilds of Endemic of Population Conservation
occurrence distribution ctive mode larvaes the PEC trend status
Species IUCN ICMBio
Pseudopaludicola mystacalis Frequent AF, Ca, Ce, Am, Oa Te Sw, Po 3 Bentonic No Stable LC LC
(Cope 1887) Ch, Pa, Pp
Pseudopaludicola pocoto Frequent AF, Ca Oa Te Sw, Po 3 Bentonic No Unknown NE LC
(Magalhães et al. 2014)
Odontophrynidae
Macrogenioglottus alipioi Infrequent AF Fa Te/Cr Sw, Po 2 Bentonic No Stable LC LC
(Carvalho 1946)
Odontophrynus carvalhoi (Savage Infrequent AF, Ca Fa, Oa Te Ri, St 16 Bentonic No Unknown LC LC
and Cei 1965)
Proceratophrys cristiceps (Müller Infrequent AF, Ca Fa, Oa Te/Cr Sw, Po, Ri, 16 Bentonic No Stable LC LC
1883) St
Proceratophrys renalis (Miranda-­ Frequent AF Fa Te/Cr Ri, St 16 Bentonic No Unknown NE LC
Ribeiro 1920)
Microhylidae
Chiasmocleis alagoana (Cruz Rare AF Fa Te/Cr Sw, Po 1 Neustonic Yes Decreasing DD EN
et al. 1999)
Dermatonotus muelleri (Boettger Frequent AF, Ca, Ce, Am, Fa, Oa Te/Cr Sw, Po 1 Neustonic No Stable LC LC
1885) Ch, Pa, Pp
Elachistocleis cesarii (Miranda Frequent AF, Ca, Ce Oa Te/Cr Sw, Po 1 Neustonic No Unknown NE LC
Ribeiro 1920)
Stereocyclops incrassatus (Cope Infrequent AF Fa Te/Cr Sw, Po 1 Neustonic No Stable LC LC
1870)
Phyllomedusidae Neustonic
Hylomantis granulosa (Cruz Infrequent AF Fa Ar Ri, St 21 and 25 Neustonic No Decreasing LC VU
1989)
Pithecopus gonzagai (Andrade Frequent AF, Ca Oa Ar Sw, Po 36 Neustonic No Stable NE NE
et al. 2020)
Pipidae
Pipa carvalhoi (Miranda-Ribeiro Frequent AF, Ca Oa Aq Sw, Po 70 Neustonic No Stable LC LC
1937)
Ranidae
Lithobates catesbeianus (Shaw Infrequent AF, Ca, Ce, Am Fa, Oa Sa Sw, Po 2 Bentonic No Increasing LC NE
1802)
Lithobates palmipes (Spix 1824) Frequent AF, Am, Ca, Ce Fa, Oa Sa Sw, Po 2 Bentonic No Stable LC LC
Gymnophiona
Siphonopidae
Siphonops annulatus (Mikan Infrequent AF, Am, Ce Fa, Oa Cr/ Dnc 38 Derm Larv No Unknown LC LC
1820) Fo
Siphonops paulensis Boettger Infrequent AF, Am, Ca, Ce Fa, Oa Cr/ Dnc 38 Direct No Unknown LC LC
1892 Fo development
Continental distribution in biomes: Ce Cerrado, Ca Caatinga, Fa Atlantic Forest, Am Amazon Forest, Ch Chaco, Pa Pantanal, Pp Pampas; Habitat: Fa Forested area, Oa Open area; Habit: Aq
Aquatic, Ar Arboreal, Cr Cryptic, Fo Fossorial, Ph Phytotelmata, Rh Rheophilic, Sa Semi-aquatic, Te Terrestrial; Calling sites: Br Bromeliad, Ff Forest floor, Lv Low vegetation, Po Ponds, Ri River
10  Species Richness, Distribution Pattern, and Conservation of Amphibians in the Northern Portion of the Brazilian Atlantic Forest

or stream backwaters, St stream or rivulet, Sw Swamp, Tc Tree crown, Ve Vegetation, Dnc Do not call; Trophic guilds of larvae: Derm larv Dermatophagous larvae; Conservation status: DD Data
Deficient, EN Endangered, LC Least Concern, NE Not evaluated, NT Near Threatened, VU Vulnerable. Population trend followed IUCN (2021)
161
162 W. L. S. Vieira et al.

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 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.
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 Bird Diversity and Conservation
of the Northern Atlantic Forest
Helder F. P. Araujo, Hermínio A. L. S. Vilela,
Benjamin Phalan, and Pedro F. Develey
Abstract
The Northern Atlantic Forest (NAF) houses the most frag-
mented forest cover and the largest number of endangered
birds of the entire Atlantic Forest. The regional biota has
been assembled over time because of speciation in situ and
biotic exchanges with other rainforest regions and the adja-
cent ecoregions. Currently, there are 485 bird species in
NAF, and, from that, 171 are forest dependent and 50 taxa
are threatened. Due to the number of forest fragments and
vegetation heterogeneity, the distribution of bird species
richness is not homogenous in NAF. There is a greater con-
centration of forest-dependent, endemic, and threatened
birds in forest fragments located between Pernambuco and
Alagoas. Recently, three bird endemic species from the NAF
were added to the list of globally extinct species (Glaucidium
mooreorum, Philydor novaesi, and Cichlocolaptes mazar-
barnettii), and one is considered extinct in the wild due to
still survives in captivity (Pauxi mitu). Besides, the critically
endangered Myrmotherula snowi has a population with less
than 20 individuals recorded in a single site. To reverse this
scenario, actions to protect and restore forest remnants and
direct management of threatened species (in situ and ex situ)
are urgently needed.
Keywords
Biogeography · Critically endangered species ·
Extinction · Habitat loss
H. F. P. Araujo (*)
Department of Bioscience, Federal University of Paraíba, Areia,
Paraíba, Brazil
e-mail: helder@cca.ufpb.br
Hermínio A. L. S. Vilela · P. F. Develey
Sociedade para a Conservação das Aves do Brasil – SAVE Brasil,
São Paulo, Brazil
B. Phalan
Parque das Aves, Paraná, Brazil
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
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_12
12
12.1 Introduction
The Northern Atlantic Forest (NAF) is an intricate and fasci-
nating region to understand the role of evolutionary and eco-
logical drivers of bird diversity and how human activities
change the patterns of biodiversity. NAF supports a rich bird
diversity while houses the most endangered birds of the
entire Atlantic Forest (MMA/ICMBio 2018). Biogeography
dynamics allowed the accumulation of evolutionary lineages
associated with South Atlantic Forest, Amazonia rainforest,
Caatinga semiarid region, and savannas from central Brazil
(Cerrado). The vegetation heterogeneity and topographic
variation keep conditions to maintain high bird diversity
(Pereira et al. 2016). However, NAF retains just only 12% of
its original vegetation cover and is currently one of the most
degraded areas of the whole Atlantic Forest (Ribeiro et  al.
2011; SOSMA 2015). Because of that, species accumulate in
NAF through both speciation and biotic interchange, but spe-
cies are lost due to regional extinction characterizing the
region as a hotspot within another hotspot (Tabarelli et  al.
2006).
The world has knowledge about the bird diversity of NAF
since the seventeenth century because of records done by
naturalists and artists during the Dutch occupation in the
Brazilian northeast (1630–1654) (Teixeira 1992, 2009;
Vanzolini 1996). Some of these works were used to include
species in the Systema Naturae by Carl Von Line in the sev-
enteenth century. We highlight the Dutch works as the
detailed and illustrated Historia Naturalis Brasiliae
(Marcgrave 1648) and the paintings in the “Theatrum Rerum
Naturaliun Brasiliae” and “Libri Principis.” Some ornithol-
ogists analyzed these materials (eg., Schneider 1938; Pinto
1942; Teixeira 1992, 2009) and, because of that, we can evi-
dence of local or global extinction of iconic species in the
NAF (Fig. 12.1). Besides, many other bird species are threat-
ened or extinct mainly because of habitat reduction caused
by deforestation promoted by sugarcane and forestry pres-
sure (Coimbra Filho and Câmara 1996; Rêgo and Hoeflich
185
186 H. F. P. Araujo et al.

2001). Currently, the forest bird species occur in reduced and

fragmented forest patches in the NAF, and protecting and
restoring the habitat remnants and understanding the natural
history of some species to guide intensive population man-
agement are essential to actions for urgent bird conservation
practices (Develey and Phalan 2021).
Here, we present a synthesis of the general process that
drove accumulation and loss of bird diversity in NAF and a
soon discussion about bird conservation strategies. For that,
we organized the chapter in three main topics: (1) Regional
Species Composition and Local Richness, (2)
Biogeographical Dynamics, and (3) Conservation status and
strategies.
12.2 Regional and Species Composition
and Local Richness
A review of the birds recorded in NAF considering the bib-
liography, museums, collections, and fieldwork listed 434
bird species in NAF (Roda 2003). Updating the checklist
with new records and taxonomy revision of some species,
we listed 486 bird species from 70 families (Table  12.1),
which represent approximately 25% of the total number of
species recorded in Brazil (Pacheco et  al. 2021). From
these species, 35% occur in natural or anthropic open habi-
tats as waterbody, savanna patches, urban areas, and agri-

Fig. 12.1  Bird species

extinct in Northern Atlantic
Forest recorded by naturalists
(Marcgrave 1648; left) and
artists (Teixeira 2009; right)
during the Dutch occupation
in the Brazilian northeast
(1630–1654). Up to bottom:
Alagoas Curassow (Pauxi
mitu), Blue-and-yellow
Macaw (Ara ararauna), and
Ornate Hawk-­Eagle
(Spizaetus ornatus). Alagoas
Curassow is considered
extinct in the wild but still
survives in captivity. The
other two species occur in
other regions of South
America (more details about
the local extinct possibility of
these species in NAF can see
in: (Teixeira 1992; Carlos and
Girão 2006)
12  Bird Diversity and Conservation of the Northern Atlantic Forest 187

cultural fields (eg., Great Kiskadee—Pitangus sulphuratus); Table 12.1  List of birds from Northern Atlantic Forest following
nomenclature by Brazilian Ornithological Records Committee (Pacheco
other species (25%) occur in mosaic of forest and open
et al. 2021)
habitats, as they can visit gardens and crop fields, but also
Habitat IUCN MMA
are recorded in forest habitats (eg., Burnished-buff
Taxon use Source 2021 2018
Tanager—Stilpnia cayana); and about 40% of all species Tinamidae
are forest dependent (eg., Ceara Woodcreeper—  Tinamus solitarius F RW NT NT
Xiphorhychus atlanticus) (Table  12.1). Photos or sound  Crypturellus soui F RW
records of 463 species (95%) species are available in the albigularis
WikiAves website (www.wikiaves.com.br), which show  Crypturellus strigulosus F RW NT
the advance of community-based science and how this  Crypturellus zabele F RW VU
practice can contribute to new information about some tax-  Crypturellus variegatus F RW
 Crypturellus O RW
onomic groups and distribution data (Chandler et al. 2017; parvirostris
Develey 2021).  Crypturellus tataupa S RW
The distribution of forest-dependent species is not homog- lepidotus
enous at NAF. Currently, most of the remaining forest frag-  Rhynchotus rufescens O RW
ments are concentrated between the states of Alagoas and rufescens
Pernambuco. Consequently, it is in this region that the great-  Nothura boraquira O RW
 Nothura maculosa O RW
est diversity of forest birds is concentrated (Pereira Júnior
cearensis
et al. 2016). In degraded and fragmented forest landscapes, Anatidae
the habitat amount hypothesis predicts that species richness  Dendrocygna bicolor O RW
should increase with the total amount of habitat (forest in  Dendrocygna viduata O RW
this case) in the ‘local landscape’(Fahrig 2013). Although  Dendrocygna O RW
this hypothesis cannot be sufficient to predict forest species autumnalis autumnalis
richness in some regions (Torrenta and Villard 2017), habitat  Cairina moschata O RW
 Sarkidiornis sylvicola O RW
amount seems to have a significant effect on forest-bird spe-
 Amazonetta brasiliensis O RW
cies richness in NAF (Fig. 12.2). This pattern confirms the
 Anas bahamensis O RW
role of forest habitat loss on local and regional extinction of bahamensis
bird species in NAF.  Netta erythrophthalma O W
Although there is information about bird species from  Nomonyx dominicus O RW
NAF for 4 centuries and declines of population or forest Cracidae
species richness have been recognized, the region is still  Penelope superciliaris F RW CR
one of the most interesting for studies focusing on the alagoensis
 Ortalis araucuan F RW
effects of human-modified landscapes on bird diversity.
 Pauxi mitu F RW EW EW
Precisely, it is a strategic region for studies about questions
Odontophoridae
such as “How habitat amount, quality, and configuration of  Odontophorus capueira F RW CR
forest habitats affect forest bird species richness and abun- plumbeicollis
dance?” Although amount, heterogeneity, and quality of Podocipedidae
habitat and landscape structure have effects on forest-bird  Tachybaptus dominicus O RW
diversity (Heikkinen et  al. 2004; Ghadiri Khanaposhtani  Podilymbus podiceps O RW
antarcticus
et al. 2012; Stein et al. 2014; Huang et al. 2015), what are
Columbidae
the roles of these variables in landscapes with reduced for-
 Columba livia O RW
est patches? This is an issue that helps questions like “How  Patagioenas speciosa F RW
to revert the trajectory of bird extinction in a rich diversity  Patagioenas picazuro S RW
area?” which is still unresolved in NAF. Therefore, evaluat- marginalis
ing the influence of human disturbances on the environ-  Patagioenas F RW
mental filters is very important for conservation and cayennensis sylvestris
restoration practices focusing on the recovery of threatened  Geotrygon montana F RW
montana
bird species in the NAF. For example, in urbanizing regions,  Geotrygon violacea F RW
larger forest areas seem to protect a greater proportion of violacea
the regional species richness of birds and differences in  Leptotila verreauxi S RW
approximans
(continued)
188 H. F. P. Araujo et al.

Table 12.1 (continued) Table 12.1 (continued)

Habitat IUCN MMA Habitat IUCN MMA
Taxon use Source 2021 2018 Taxon use Source 2021 2018
 Leptotila rufaxilla F RW  Glaucis hirsutus F RW
rufaxilla hirsutus
 Zenaida auriculata O W  Phaethornis ruber ruber F RW
 Claravis pretiosa S RW  Phaethornis pretrei S RW
 Columbina passerina O RW  Phaethornis F RW CR
griseola margarettae camargoi
 Columbina minuta O RW  Heliactin bilophus O RW
minuta  Heliothryx auritus F RW
 Columbina talpacoti O RW auriculatus
talpacoti  Polytmus guainumbi F RW
 Columbina squammata O RW thaumantias
squammata  Chrysolampis mosquitus S RW
 Columbina picui O RW  Anthracothorax S RW
strepitans nigricollis
Cuculidae  Discosura longicaudus F RW
 Guira guira O RW  Lophornis magnificus F RW
 Crotophaga ani O RW  Heliomaster squamosus F RW
 Tapera naevia naevia O RW  Calliphlox amethystina S W
 Micrococcyx cinereus O W  Chlorostilbon lucidus S RW
 Piaya cayana pallescens S RW pucherani
 Coccyzus melacoryphus S RW  Thalurania watertonii F RW EN EN
 Coccyzus americanus S A10  Eupetomena macroura O RW
 Coccyzus euleri S RW simoni
Nyctibiidae  Aphantochroa S RW
 Nyctibius griseus S RW cirrochloris
griseus  Chrysuronia versicolor S RW
Caprimulgidae versicolor
 Nyctiphrynus ocellatus F RW  Chrysuronia leucogaster F RW
ocellatus bahiae
 Antrostomus rufus rufus S RW  Chionomesa fimbriata S RW
 Lurocalis semitorquatus F RW nigricauda
nattereri  Hylocharis sapphirina F RW
 Nyctidromus albicollis S RW  Chlorestes cyanus F RW
albicollis cyanus
 Hydropsalis parvula O RW  Chlorestes notata notata F RW
 Hydropsalis longirostris O W Aramidae
 Hydropsalis torquata S RW  Aramus guarauna O RW
torquata guarauna
 Nannochordeiles O RW Rallidae
pusillus pusillus  Rallus longirostris S RW
 Podager nacunda O W crassirostris
 Chordeiles acutipennis O RW  Porphyrio martinica O RW
acutipennis  Rufirallus viridis viridis S RW
Apodidae  Laterallus flaviventer O W
 Cypseloides senex F W  Laterallus O RW
 Chaetura cinereiventris F W melanophaius
 Chaetura spinicaudus S R  Laterallus exilis O RW
aethalea  Mustelirallus albicollis O RW
 Chaetura meridionalis S RW albicollis
 Chaetura brachyura S R  Neocrex erythrops S RW
brachyura olivascens
 Tachornis squamata O RW  Pardirallus maculatus O RW
 Panyptila cayennensis S RW maculatus
Trochilidae  Pardirallus nigricans O RW
nigricans
 Florisuga fusca F RW
(continued)
(continued)
12  Bird Diversity and Conservation of the Northern Atlantic Forest 189

Table 12.1 (continued) Table 12.1 (continued)

Habitat IUCN MMA Habitat IUCN MMA
Taxon use Source 2021 2018 Taxon use Source 2021 2018
 Amaurolimnas concolor S RW  Nannopterum O RW
castaneus brasilianum brasilianum
 Aramides mangle S RW Ardeidae
 Aramides cajaneus S RW  Tigrisoma lineatum O RW
cajaneus marmoratum
 Porphyriops melanops O RW  Cochlearius cochlearius O RW
melanops cochlearius
 Gallinula galeata O RW  Botaurus pinnatus O RW
Charadriidae pinnatus
 Pluvialis dominica O W  Ixobrychus exilis O RW
 Pluvialis squatarola O W erythromelas
 Vanellus chilensis O RW  Nycticorax nycticorax O RW
lampronotus hoactli
 Charadrius O RW  Nyctanassa violacea O W
semipalmatus  Butorides striata striata O RW
 Charadrius wilsonia O RW  Ardeola ralloides O W
wilsonia  Bubulcus ibis ibis O RW
 Charadrius collaris O RW  Ardea cocoi O RW
Haematopodidae  Ardea alba egretta O RW
 Haematopus palliatus O W  Egretta thula thula O RW
Recurvirostridae  Egretta caerulea O W
 Himantopus mexicanus O RW Cathartidae
 Himantopus melanurus O W  Coragyps atratus O RW
Scolopacidae foetens
 Numenius hudsonicus O RW  Cathartes aura ruficollis O RW
 Limosa lapponica O W  Cathartes burrovianus O RW
 Arenaria interpres O RW urubutinga
morinella Pandionidae
 Calidris canutus rufa O RW  Pandion haliaetus O RW
 Calidris himantopus O W carolinensis
 Calidris alba O RW Accipitridae
 Calidris minutilla O W  Gampsonyx swainsonii S RW
 Calidris fuscicollis O RW swainsonii
 Calidris melanotos O RW  Elanus leucurus O RW
leucurus
 Calidris pusilla O RW
 Chondrohierax F RW
 Limnodromus griseus O RW
uncinatus uncinatus
griseus
 Leptodon forbesi F RW EN EN
 Gallinago undulata O R
gigantea  Elanoides forficatus S RW
yetapa
 Gallinago paraguaiae O RW
 Spizaetus tyrannus F RW
 Actitis macularius O RW
tyrannus
 Tringa solitaria O RW
 Rostrhamus sociabilis O RW
solitaria
 Harpagus bidentatus F RW
 Tringa melanoleuca O RW
bidentatus
 Tringa semipalmata O RW
 Ictinia plumbea S RW
 Tringa flavipes O RW
 Accipiter bicolor F RW
Jacanidae pileatus
 Jacana jacana jacana O RW  Geranospiza S RW
Ciconiidae caerulescens gracilis
 Ciconia maguari O W  Buteogallus O W NT NT
Anhingidae aequinoctialis
 Anhinga anhinga O RW  Heterospizias O W
anhinga meridionalis
Phalacrocoracidae  Urubitinga urubitinga O W
(continued) (continued)
190 H. F. P. Araujo et al.

Table 12.1 (continued) Table 12.1 (continued)

Habitat IUCN MMA Habitat IUCN MMA
Taxon use Source 2021 2018 Taxon use Source 2021 2018
 Rupornis magnirostris O RW Ramphastidae
nattereri  Ramphastos vitellinus F RW
 Parabuteo unicinctus O W ariel
 Geranoaetus O RW  Pteroglossus inscriptus F RW
albicaudatus inscriptus
albicaudatus  Pteroglossus aracari F RW
 Geranoaetus O RW aracari
melanoleucus Picidae
melanoleucus  Picumnus F RW
 Pseudastur polionotus F RW NT NT pernambucensis
 Buteo nitidus nitidus O RW  Picumnus limae S RW
 Buteo brachyurus S RW  Melanerpes candidus O W
brachyurus  Veniliornis affinis F RW
 Buteo albonotatus F RW ruficeps
Tytonidae  Veniliornis passerinus S RW
 Tyto furcata tuidara O RW taenionotus
Strigidae  Campephilus S W
 Megascops choliba S RW melanoleucos
decussatus  Dryocopus lineatus S RW
 Megascops alagoensis F RW ? ? improcerus
 Pulsatrix perspicillata F RW VU  Celeus flavus subflavus F R CR
pulsatrix  Celeus ochraceus F RW
 Bubo virginianus deserti S R  Piculus flavigula F RW
 Strix virgata borelliana F RW erythropis
 Glaucidium F R CR EX  Piculus chrysochloros F R
mooreorum  Colaptes melanochloros S RW
 Glaucidium brasilianum S RW EX nattereri
brasilianum  Colaptes campestris S W
 Athene cunicularia O W Cariamidae
 Asio clamator O RW  Cariama cristata O RW
Trogonidae Falconidae
 Trogon viridis viridis F RW  Herpetotheres S RW
 Trogon curucui curucui F RW cachinnans cachinnans
 Trogon muriciensis F RW ? ?  Micrastur ruficollis F RW
 Trogon collaris eytoni F R EN ruficollis
Momotidae  Micrastur semitorquatus F RW
 Baryphthengus F R semitorquatus
ruficapillus  Caracara plancus O RW
 Momotus momota F RW EN  Milvago chimachima O RW
marcgravianus chimachima
Alcedinidae  Falco sparverius cearae O RW
 Megaceryle torquata O RW  Falco rufigularis S R
torquata ophryophanes
 Chloroceryle amazona S RW  Falco femoralis O RW
 Chloroceryle aenea F A6W femoralis
 Chloroceryle americana S RW  Falco peregrinus O RW
americana anatum
Galbulidae Psittacidae
 Galbula ruficauda F RW  Touit surdus F RW VU VU
rufoviridis  Brotogeris tirica F RW
Bucconidae  Brotogeris chiriri F W
 Chelidoptera tenebrosa S R  Pionus maximiliani F W
tenebrosa  Pionus reichenowi F RW VU VU
 Monasa nigrifrons F RW  Amazona rhodocorytha F R
nigrifrons  Amazona aestiva S W
 Nystalus maculatus O RW  Amazona amazonica F RW
(continued) (continued)
12  Bird Diversity and Conservation of the Northern Atlantic Forest 191

Table 12.1 (continued) Table 12.1 (continued)

Habitat IUCN MMA Habitat IUCN MMA
Taxon use Source 2021 2018 Taxon use Source 2021 2018
 Forpus xanthopterygius O RW  Conopophaga cearae F RW EN
 Pyrrhura griseipectus F R EN EN Formicariidae
 Eupsittula aurea S RW  Formicarius colma F RW
 Eupsittula cactorum S RW ruficeps
caixana  Chamaeza campanisona F RW
 Aratinga jandaya S RW campanisona
 Primolius maracana F W Scleruridae
 Thectocercus S R  Sclerurus macconnelli F R VU
acuticaudatus bahiae
haemorrhous  Sclerurus caudacutus F RW CR
 Diopsittaca nobilis S RW caligineus
cumanensis Dendrocolaptidade
Thamnophilidae  Sittasomus F RW
 Myrmorchilus strigilatus S RW griseicapillus reiseri
strigilatus  Dendrocincla taunayi F RW EN
 Terenura sicki F RW CR CR  Dendrocolaptes medius F RW
 Myrmotherula axillaris F RW  Dendrocolaptes F RW
luctuosa platyrostris intermedius
 Myrmotherula snowi F RW CR CR  Xiphorhynchus F RW VU
 Formicivora grisea F RW atlanticus
grisea  Xiphorhynchus guttatus F RW
 Formicivora rufa rufa S RW guttatus
 Thamnomanes caesius F RW VU  Dendroplex picus F RW
caesius bahiae
 Dysithamnus mentalis F RW  Campylorhamphus F RW EN
emiliae trochilirostris
 Herpsilochmus S RW trochilirostris
pectoralis  Lepidocolaptes S RW
 Herpsilochmus frater F RW angustirostris
 Herpsilochmus F RW Xenopidae
atricapillus  Xenops minutus F RW VU
 Thamnophilus S RW alagoanus
capistratus  Xenops rutilans rutilans F RW
 Thamnophilus torquatus S RW Furnariidae
 Thamnophilus palliatus S RW  Furnarius figulus figulus S RW
palliatus  Furnarius leucopus S RW
 Thamnophilus pelzelni F RW assimilis
 Thamnophilus F RW VU  Furnarius rufus O RW
caerulescens  Cichlocolaptes F B EX EX
pernambucensis mazarbarnetti
 Thamnophilus aethiops F RW EN  Philydor novaesi F RW EX EX
distans  Automolus lammi F RW EN VU
 Taraba major stagurus S RW  Phacellodomus rufifrons O RW
 Hypoedaleus guttatus F RW specularis
leucogaster  Cranioleuca F RW
 Radinopsyche sellowi S RW semicinerea semicinerea
 Myrmoderus ruficauda F RW EN EN  Certhiaxis cinnamomeus O RW
soror cearensis
 Pyriglena F RW VU  Synallaxis scutata F RW
pernambucensis scutata
 Cercomacroides laeta F RW  Synallaxis infuscata F RW EN EN
sabinoi  Synallaxis hypospodia O RW
 Drymophila squamata F RW  Synallaxis albescens O RW
Conopophagidae albescens
 Conopophaga F RW VU  Synallaxis frontalis S RW
melanops nigrifrons Pipridae
(continued) (continued)
size, and isolation influences species similarity (Enedino
192 H. F. P. Araujo et al.

Table 12.1 (continued) Table 12.1 (continued)

Habitat IUCN MMA Habitat IUCN MMA
Taxon use Source 2021 2018 Taxon use Source 2021 2018
  Neopelma pallescens F RW  Tolmomyias F RW
  Chiroxiphia pareola F RW sulphurescens
  Manacus manacus F RW pallescens
gutturosus  Tolmomyias F RW
  Ceratopipra F RW poliocephalus
rubrocapilla  Tolmomyias flaviventris F RW
Cotingidae sclateri
  Carpornis F RW VU VU  Todirostrum cinereum S RW
melanocephala cearae
  Lipaugus vociferans F RW  Poecilotriccus F RW
  Procnias averano F RW VU plumbeiceps
averano plumbeiceps
  Procnias nudicollis F R NT NT  Poecilotriccus fumifrons S RW
fumifrons
  Cotinga maculata F W CR EN
 Myiornis auricularis F W
  Xipholena atropurpurea F RW VU VU
 Hemitriccus F RW VU
Tityridae
griseipectus
  Schiffornis turdina F RW VU naumburgae
intermedia
 Hemitriccus striaticollis O RW
  Iodopleura pipra F RW EN EN striaticollis
leucopygia
 Hemitriccus S RW
  Tityra inquisitor F R margaritaceiventer
inquisitor wuchereri
  Tityra cayana F RW  Hemitriccus mirandae F RW VU VU
braziliensis
Tyrannidae
  Pachyramphus viridis F RW
 Hirundinea ferruginea S RW
viridis
bellicosa
  Pachyramphus S RW
 Zimmerius acer F RW
polychopterus
 Euscarthmus O RW
  Pachyramphus F RW
meloryphus
marginatus marginatus
 Ornithion inerme F RW
  Pachyramphus validus F RW
 Camptostoma obsoletum O RW
Oxyruncidae
obsoletum
  Oxyruncus cristatus F RW
 Elaenia flavogaster S RW
cristatus
flavogaster
Onychorhynchidae
 Elaenia spectabilis S RW
  Myiobius barbatus F RW
 Elaenia chilensis S RW
mastacalis
 Elaenia mesoleuca F RW
  Myiobius atricaudus F R
snethlagei  Elaenia cristata O RW
Pipritidae  Elaenia chiriquensis O RW
albivertex
  Piprites chloris chloris F W
 Myiopagis gaimardii F RW
Platyrinchidae
subcinerea
  Platyrinchus mystaceus F RW VU
 Myiopagis caniceps F RW
niveigularis
caniceps
  Platyrinchus F MHNAL356 VU NT
 Myiopagis viridicata F RW
leucoryphus
viridicata
Rhynchocyclidae
 Capsiempis flaveola F RW
  Mionectes oleagineus F RW flaveola
oleagineus
 Phaeomyias murina O RW
  Leptopogon F RW murina
amaurocephalus
 Phyllomyias fasciatus F RW
amaurocephalus
fasciatus
  Corythopis delalandi F W
 Serpophaga subcristata S RW
  Phylloscartes ceciliae F RW CR CR subcristata
  Rhynchocyclus F RW  Pseudocolopteryx O W
olivaceus olivaceus sclateri
(continued) (continued)
12  Bird Diversity and Conservation of the Northern Atlantic Forest 193

Table 12.1 (continued) Table 12.1 (continued)

Habitat IUCN MMA Habitat IUCN MMA
Taxon use Source 2021 2018 Taxon use Source 2021 2018
 Attila spadiceus F RW VU  Pygochelidon O RW
uropygiatus cyanoleuca cyanoleuca
 Legatus leucophaius F RW  Stelgidopteryx ruficollis S RW
leucophaius ruficollis
 Myiarchus tuberculifer F RW  Progne tapera tapera O RW
tuberculifer  Progne chalybea O RW
 Myiarchus swainsoni S RW domestica
pelzelni  Tachycineta albiventer O RW
 Myiarchus ferox ferox S RW  Tachycineta leucorrhoa O RW
 Myiarchus tyrannulus S RW  Hirundo rustica O RW
bahiae erythrogaster
 Rhytipterna simplex F RW Troglodytidae
simplex  Troglodytes musculus O RW
 Casiornis fuscus F RW musculus
 Pitangus sulphuratus O RW  Pheugopedius F RW
maximiliani genibarbis genibarbis
 Philohydor lictor lictor O RW  Cantorchilus S RW
 Machetornis rixosa O RW longirostris bahiae
rixosa Polioptilidae
 Myiodynastes maculatus F RW  Ramphocaenus F RW
maculatus melanurus melanurus
 Megarynchus pitangua F RW  Polioptila atricapilla S RW
pitangua Donacobiidae
 Myiozetetes similis S RW  Donacobius atricapilla O RW
pallidiventris atricapilla
 Tyrannus melancholicus O RW Turdidae
despotes  Catharus fuscescens F PeW
 Tyrannus savana O RW  Turdus flavipes flavipes F RW
 Empidonomus varius S RW  Turdus leucomelas S RW
rufinus albiventer
 Sublegatus modestus S RW  Turdus fumigatus F R
modestus fumigatus
 Arundinicola O RW  Turdus rufiventris S RW
leucocephala juensis
 Fluvicola albiventer O RW  Turdus amaurochalinus S RW
 Fluvicola nengeta O RW  Turdus albicollis F RW
nengeta crotopezus
 Myiophobus fasciatus O RW Mimidae
flammiceps
 Mimus gilvus antelius O RW
 Cnemotriccus fuscatus F RW
 Mimus saturninus O RW
bimaculatus
arenaceus
 Lathrotriccus euleri F RW
Estrildidae
euleri
 Estrilda astrild O RW
 Contopus cinereus F RW
pallescens Passeridae
 Satrapa icterophrys S W  Passer domesticus O RW
Vireonidae Motacillidae
 Cyclarhis gujanensis S RW  Anthus chii O RW
cearensis Fringillidae
 Hylophilus S RW  Spinus yarrellii S RW VU VU
amaurocephalus  Cyanophonia S PeW
 Vireo chivi S RW cyanocephala
Corvidae  Euphonia chlorotica S RW
 Cyanocorax S RW chlorotica
cyanopogon  Euphonia violacea F RW
Hirundinidae aurantiicollis
 Euphonia pectoralis F RW
(continued)
(continued)
194 H. F. P. Araujo et al.

Table 12.1 (continued) Table 12.1 (continued)

Habitat IUCN MMA Habitat IUCN MMA
Taxon use Source 2021 2018 Taxon use Source 2021 2018
Passerellidae  Tersina viridis viridis F RW
  Ammodramus humeralis O RW  Cyanerpes cyaneus F RW
humeralis cyaneus
  Arremon taciturnus F RW  Dacnis cayana S RW
  Zonotrichia capensis O RW paraguayensis
matutina  Saltator maximus F RW
Icteridae maximus
  Leistes superciliaris O RW  Saltator similis similis F RW
  Cacicus solitarius S RW  Saltator fuliginosus F RW
  Cacicus cela cela S RW  Coereba flaveola S RW
  Cacicus haemorrhous S RW chloropyga
affinis  Asemospiza fuliginosa F RW
  Icterus jamacaii S RW fuliginosa
  Icterus pyrrhopterus S RW  Volatinia jacarina O RW
tibialis jacarina
  Molothrus rufoaxillaris O W  Loriotus cristatus F RW
  Molothrus bonariensis O RW brunneus
bonariensis  Coryphospingus S RW
  Anumara forbesi S RW VU VU pileatus pileatus
  Gnorimopsar chopi O RW  Tachyphonus rufus S RW
sulcirostris  Ramphocelus bresilia F RW
  Agelaioides fringillarius O RW bresilia
  Chrysomus ruficapillus O RW  Sporophila lineola O RW
frontalis  Sporophila nigricollis O RW
Parulidae nigricollis
  Geothlypis S PeW  Sporophila ardesiaca O W
aequinoctialis  Sporophila caerulescens O RW
  Setophaga pitiayumi F RW caerulescens
pitiayumi  Sporophila albogularis O RW
  Myiothlypis flaveola F RW  Sporophila leucoptera O RW
flaveola cinereola
  Basileuterus culicivorus F RW  Sporophila bouvreuil O RW
auricapilla  Sporophila angolensis O RW
Cardinalidae angolensis
  Piranga flava saira S RW  Thlypopsis sordida S RW
  Habia rubica bahiae F RW sordida
  Caryothraustes F RW  Cypsnagra hirundinacea O PiW
brasiliensis  Conirostrum speciosum F RW
  Cyanoloxia brissonii S RW speciosum
brissonii  Conirostrum bicolor F RW
Thraupidae bicolor
  Charitospiza eucosma S PiW  Sicalis flaveola O RW
brasiliensis
  Nemosia pileata pileata S RW
 Sicalis luteola O RW
  Compsothraupis S RW
luteiventris
loricata
 Pipraeidea melanonota F W
  Coryphaspiza melanotis O PiW VU EN
 Cissopis leverianus F R
  Emberizoides herbicola O RW
leverianus
herbicola
 Schistochlamys S RW
  Porphyrospiza O PiW
melanopis olivina
caerulescens
 Schistochlamys S RW
  Chlorophanes spiza F RW
ruficapillus
axillaris
 Paroaria dominicana O RW
  Hemithraupis flavicollis F RW
melanoxantha  Thraupis sayaca sayaca S RW
  Hemithraupis guira F RW  Thraupis palmarum S RW
guira palmarum
(continued) (continued)
et al. 2018).
12  Bird Diversity and Conservation of the Northern Atlantic Forest 195

Table 12.1 (continued) Based on genomic evolutionary relationships (Harvey

Habitat et al. 2020), an endemic and very restricted species in NAF,
IUCN MMA
Taxon use Source 2021 2018
Alagoas Antwren (Myrmotherula snowi), diverged more
 Stilpnia cayana flava S RW than 2 million years ago from its sister species Unicolored
 Tangara fastuosa F RW VU VU
Antwren (M. unicolor), which occurs in Southeastern
 Tangara cyanocephala F RW
corallina
Atlantic Forest (Fig.  12.3). A similar pattern occurs with
 Tangara cyanomelas F RW Buff-breasted Tody-Tyrant (Hemitriccus mirandae), but this
Habitat use: O—birds that occur in natural or anthropic open habitats, species occurs in some interior forest patches in the NAF and
S—birds that occur in mosaic of forest and open habitats, F—forest-­ rainforest enclaves into the Caatinga dry forest region
dependent birds. Source of bird record information: R (Roda 2003), W (Fig.  12.3). However, another congeneric forest species,
(www.wikiaves.com.br), A6 (Araujo et  al. 2006), A10 (Araujo et  al. White-bellied Tody-Tyrant (H. griseipectus), occurs also in
2010), Pe (Pereira et  al. 2012), Pi (Pichorim et  al. 2014), MHNAL
(Museum of Natural History of Federal University of Alagoas). Global NAF but has disjunct distribution with Amazonian popula-
(IUCN 2021) and national (ICMBIO/MMA 2018) threatened status. tions. This pattern also promoted speciation in NAF as exem-
The names in bold represent the endemic birds of the Northern Atlantic plified by Pernambuco Fire-eye (Pyriglena pernambucensis),
Forest or Pernambuco Endemism Center which is disjunct of its sister species East Amazonian Fire-­
eye (P. leuconota), which occurs in east Amazon and some
12.3 Biogeographical Dynamics patch forest in the northern Cerrado (Fig.12.3). This same
pattern can be seen in White-winged Cotinga Xipholena
Regional biota is the result of a hierarchy of processes such atropurpurea and X. lamellipennis, but, beyond NAF, the
as speciation, immigration, and extinction, where dispersion first species occurs further south in Atlantic Forest, precisely
barriers and environmental filters drive local communities, up to Espírito Santo. The estimated split of P. pernambucen-
which are influenced by mechanisms such as interactions, sis and X. atropurpurea with their Amazonian sister species
niche occupancy, niche disturbances, and local extinctions was between one and 2 million years ago (Fig. 12.3). Another
(Leibold et  al. 2004; Myers and Harms 2009; Chase and different example shows the influence of the adjacent
Myers 2011; Cornell and Harrison 2014). The megadiversity Caatinga dry forest region in the forest bird diversity of
in Amazonia, for example, is mainly explained by coloniza- NAF.  Planalto Slaty-Antshrike (Thamnophilus pelzelni)
tion time in each region and long-term sympatry of various occurs in some semi-deciduous forest in NAF but also occurs
evolutionary lineages, suggesting intriguing interactions in dry forest, riverine forest, and other arboreal habitats from
between species diversification and local richness accumula- Caatinga and Cerrado regions (Fig. 12.3). Still, some Cerrado
tion (Wiens et al. 2011). In NAF, some biogeography history typical species can be found in patches of like-savanna habi-
patterns of bird endemic species and other forest species pro- tats in NAF (Araujo 2013; Pichorim et  al. 2014; Sagot-­
vide insights into the role of speciation, immigration, and Martin et al. 2020). These history and habitat variations are
extinction structuring bird regional biota.

Fig. 12.2  Effect of forest 160

habitat amount on the
richness of forest-­bird species
140
in Northern Atlantic Forest.
The figure shows a
richness of forest-bird species

generalized additive model 120

(R2 = 0.56, p < 0.0001)
(Bruce and Bruce 2017) based 100
on data of species richness
and locations available in
Pereira et al. (2016) 80

60

40

20

0
0 1000 2000 3000 4000 5000
forest habitat amount (ha)
196
Fig. 12.3  Examples of phylogenetic affinities of forest-bird species/
populations that occur in Northern Atlantic Forest: Myrmotherula
snowi, Hemitriccus mirandae, Pyriglena pernambucensis, Xipholena
just examples of the biogeographical dynamism that drove
bird regional biota in NAF.
Regardless of biogeographical history, the result was the
isolation of species or populations of birds in the current
fragmented and reduced forest patches in NAF. Because of
that, this region is also known as Pernambuco Endemism
Center (PEC) or Pernambuco Endemism Area (Silva et  al.
2004). Many bird taxa support the PEC (27 species and sub-
species, see Table  12.1), and some of them are listed as
threatened species and others are considered extinct cur-
H. F. P. Araujo et al.
atropurpurea, and Thamnophilus pelzelni. The phylogenies were
adapted from the suboscine passerines phylogeny, estimated using data
from 2389 genomic regions. (Harvey et al. 2020)
rently. Very recent taxonomic revisions resulted in the
description of two new and endemic species of NAF, Alagoas
Screech-Owl, Megascops alagoensis (Dantas et  al. 2021),
and Alagoas Black-throated Trogon, Trogon muriciensis
(Dickens et al. 2021); the first is only known from some for-
est patches in Pernambuco and Alagoas, and the second only
from Alagoas. These and other examples point out biogeog-
raphy mechanisms associated with previous connections and
retractions of forest regions in South America, which should
be occurred during past climate changes (Batalha-Filho et al.
12  Bird Diversity and Conservation of the Northern Atlantic Forest 197

2013; Carvalho et  al. 2017; Nascimento et  al. 2021).
Therefore, urgent actions for conservation focusing on these
species not just keep the current diversity but also maintain a
living museum of fascinating histories.
12.4 Conservation Status and Strategies
Northern Atlantic Forest houses 50 threatened bird taxa (spe-
cies and subspecies), 25 considered globally threatened by
the International Union for Conservation of Nature (IUCN)
and 50 by the Brazilian Environment Ministry (ICMBio/
MMA) (ICMBIO/MMA 2018; IUCN 2021) (Table 12.1 and
Fig.  12.4). This difference is because the national red list
evaluates subspecies and species while the global red list
classifies just species. Regardless of that, NAF is the site of
several recent extinctions. The last wild Alagoas Curassow
likely died out in the 1970s, but fortunately, a small captive
population persists. The Alagoas Foliage-gleaner (Philydor
novaesi) and Cryptic Treehunter (Cichlocolaptes mazarbar-
netti) disappeared in the early twenty-first century. The
Pernambuco Pygmy-owl (Glaucidium mooreorum) has not
been recorded for 20  years and is listed as Critically
Endangered (Possibly Extinct). Three further birds are glob-
ally Critically Endangered, of which the Alagoas Antwren is
likely on the brink of extinction: it has disappeared from
three of its four recorded sites. The remaining population, at
Murici in Alagoas, is now very small, with just eight birds
recorded during intensive fieldwork over 6 months in 2020
and 2021 (H. Vilela, pers. obs.). The situation of the other
two Critically Endangered species, Orange-bellied Antwren
(Terenura sicki) and Alagoas Tyrannulet (Phylloscartes ceci-
liae), is somewhat better, and while their populations are
very small, both are still found at multiple sites. Another pos-
sible extinct species in NAF is Gray-breasted Parakeet
(Pyrrhura griseipectus), which was recorded in the 1980

Fig. 12.4  Two new species

descripted from Northern
Atlantic Forest (NAF): (a)
Alagoas Screech-Owl
(Megascops alagoensis—
photo: Arthur Andrade) and
(b) Alagoas Black-throated
Trogon (Trogon muriciensis—
photo: Hermínio Vilela) can
be considered Critically
Endangered (Dantas et al.
2021; Dickens et al. 2021).
Examples of globally
Critically Endangered bird
species in NAF: (c) Orange-
bellied Antwren (Terenura
sicki—photo: Silvia
Linhares), (d) Alagoas
Antwren (Myrmotherula
snowi—photo: Arthur
Andrade), and (e) Alagoas
Tyrannulet (Phylloscartes
ceciliae—photo: Thiago
Zanetti). Example of bird
species that disappeared in the
early twenty-first century: (f)
Alagoas Foliage-gleaner
(Philydor novaesi—photo:
Ciro Albano)
198
decade (Teixeira et  al. 1988). Currently, Gray-breasted
Parakeet is considered an Endangered species with occur-
rence in some sites of the states of Ceará and Bahia (IUCN
2021)(www.wikiaves.com.br), but not more in NAF.
Although it is not evaluated by IUCN or MMA, the two new
species (Alagoas Screech-Owl and Alagoas Black-­ throated
Trogon) can be considered Critically Endangered (Dantas et al.
2021; Dickens et al. 2021). Other taxa are currently recognized
as Critically Endangered subspecies, of which some may be
recognized as species in the future—including the northeastern
subspecies of Rusty-margined Guan (Penelope superciliaris
alagoensis), Spot-winged Wood-quail (Odontophorus capu-
eira plumbeicollis), Margaretta’s Hermit (Phaethornis marga-
rettae camargoi), and Black-tailed Leaftosser (Sclerurus
caudacutus caligineus). To reverse all these scenarios of bird
diversity erosion in NAF, actions to protect and restore forest
remnants and direct management of threatened species (in situ
and ex situ) are urgently needed.
Fig. 12.5  Distribution of the number of threatened bird species [modified from MMA/ICMBio (2018)] and Important Bird and Biodiversity Areas
(IBAs) in Northern Atlantic Forest [modified from SAVE Brasil (2009)]
H. F. P. Araujo et al.
As a global strategy to identify, monitor, and protect a
network of critical areas for birds and biodiversity, BirdLife
International implemented the Important Bird and
Biodiversity Areas (IBAs) Program that identified 12,000
worldwide IBAs in 200 countries (BirdLife International
2014). The distribution of threatened bird species in NAF is
not homogeneous (Fig. 12.5), but there are 19 IBAs in NAF
spatially located where a major concentration of threatened
bird species occurs (Fig. 12.5). Another conservation strat-
egy in Brazil is the National Action Plans for the Conservation
of Endangered Species (PANs), which are public policies,
agreed with society, that identify and guide priority actions
to combat threats that put species populations and environ-
ments at risk and thus protect them (MMA/ICMBio 2018).
The PAN of Atlantic Forest birds establishes priority conser-
vation strategies for 104 bird taxa, about 45% of all threat-
ened bird species in Brazil, and most of them occur in NAF
(MMA/ICMBio 2018) (Fig. 12.5).
12  Bird Diversity and Conservation of the Northern Atlantic Forest
The most urgent conservation need for birds of NAF is to
halt any further degradation of habitats and to understand the
effects of historical habitat loss on the threatened species. In
that respect, protected areas, both public and private, play a
key role. Federal, state, and municipal-protected areas incor-
porate some of the best-remaining forests in the region but are
underfunded and lack the support they need to be fully effec-
tive. Especially in light of the limitations of conservation
efforts on public land, forests on private land are also of
immense importance. These include private nature reserves
(Brazilian acronym: RPPNs) and areas protected by the Forest
Code (known as Legal Reserves and Areas of Permanent
Preservation). These areas on private land support popula­
tions of species such as Orange-bellied Antwren, Alagoas
Tyrannulet, and Seven-colored Tanager (Tangara fastuosa).
With so little forest remaining, populations of many spe-
cies have been drastically reduced from their historical lev-
els. Habitat limitation is further limited by the exposure of
remaining fragments to edge and isolation effects. To secure
populations of endemic species in the long term, large-scale
forest restoration is needed. Progress is already being made,
with restoration projects underway by CEPAN (Centro de
Pesquisas Ambientais do Nordeste), IPMA (Preservation of
the Atlantic Forest), SAVE Brasil, and others.
Forest restoration will take many decades to recreate
mature forest habitat, and in the meantime, some of the most
threatened species will only survive with intensive popula-
tion management. The most advanced example of this is the
Alagoas Curassow, with the global population entirely in
human care, except for a first attempt with the first individu-
als being released back into the wild in 2019. Work is
­underway by SAVE Brasil, Parque das Aves and others to
find and protect nests of the Alagoas Antwren and to develop
ex situ methods to establish an insurance population of the
species. In the future, other Critically Endangered birds may
require similar interventions.
The Northern Atlantic Forest as it was originally has
already been lost. Even so, the diversity of birds that still
exists in the region allows the determination of unique eco-
logical and biogeographic patterns, leading even to the
description of new taxa. Fortunately, many conservation
efforts focusing on species, local communities, or landscape
restoration are being implemented throughout the region and
bring us hope that at least part of the region’s unique diver-
sity will be perpetuated.
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 Mammals of the Pernambuco
Endemism Center: Diversity, 13
Biogeography, Research Gaps,
and Conservation Concerns

Anderson Feijó, Mayara Beltrão, Anna Ludmilla da Costa-­

Pinto, Patrício Adriano da Rocha, Marco Antônio de
Freitas, Bruno Augusto Torres Parahyba Campos,
Diego Astúa, and Pedro Cordeiro-Estrela

Abstract
We present an overview of the mammal fauna in the
Pernambuco Endemism Center (PEC), addressing diversity
and biogeographic patterns, collection effort trends, main
threats, and conservation concerns. We listed 137 mammal
species as part of the original fauna of the PEC, including
five locally extinct and six endemic taxa. We are neverthe-
less aware that this diversity is still underestimated as new
A. Feijó (*)
Key Laboratory of Zoological Systematics and Evolution, Institute
of Zoology, Chinese Academy of Sciences, Beijing, China
M. Beltrão
Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil
A. L. da Costa-Pinto
Museu de História Natural, Universidade Federal de Alagoas,
Maceió, Brazil
Instituto de Ciências Biológicas e Saúde, Universidade Federal de
Alagoas, Maceió, Brazil
P. A. da Rocha
Programa de Pós-Graduação em Ciências Biológicas, Universidade
Federal da Paraíba, João Pessoa, Brazil
M. A. de Freitas
Instituto Chico Mendes de Conservação da Biodiversidade
(ICMBio), ESEC Murici, Murici, Brazil
Bruno Augusto Torres Parahyba Campos
Programa de Pós-Graduação em Biodiversidade Meio Ambiente e
Saúde, Universidade Estadual do Maranhão, Caxias, Brazil
D. Astúa
Laboratório de Mastozoologia, Departamento de Zoologia, CB,
Universidade Federal de Pernambuco, Recife, Brazil
P. Cordeiro-Estrela
Programa de Pós-Graduação em Ciências Biológicas, Universidade
Federal da Paraíba, João Pessoa, Brazil
Laboratório de Mamíferos, Departamento de Sistemática e
Ecologia, CCEN, Universidade Federal da Paraíba,
João Pessoa, Brazil
species continue to be added and described to the region.
We further found that 56% of the PEC has not yet been
surveyed. The PEC mammal assemblage represents a het-
erogeneous fauna with a strong influence of adjacent open
biomes and the eastern Amazon. We also explored the
deforestation scenario in the PEC and how it impacts mam-
mals. Only 2.8% of the remaining fragments have an area
larger than 3 km2 and are on average 3.6 km distant from
each other; a more alarming panorama than often depicted.
Finally, we discuss the effects of sugarcane crops and hunt-
ing on mammal communities. Throughout this chapter, we
highlight key areas and themes that have been neglected in
the PEC and can help direct efficient conservation actions.
Keywords
Northern Atlantic Forest · Northeastern Brazil ·
Deforestation
13.1 Introduction
The Atlantic Forest encompasses approximately 4000 km of
coastline, spanning from 3.6°  S to 33.4°  S, with altitudes
ranging from sea level to 2892 m, and includes very diverse
vegetation formations, which resulted in unique ecoregions
(Marques and Grelle 2021). The large span of the Atlantic
Forest results in its contact with almost all other Brazilian
biomes (Cerrado, Caatinga, Pantanal, Pampa), except with
Amazon, which contact occurred in forest expansions during
the glacial and interglacial climatic cycles through
­northeastern Brazil, in the Pernambuco Endemism Center
(PEC). The PEC is defined as an ecoregion of the Atlantic
forest delimited by a riverine barrier at its south, the São
Francisco river, by the Caatinga biome at its western and

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 201
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_13
202 A. Feijó et al.

northern borders and by the Atlantic Ocean at its east coast
(Fig. 13.1).
Mammals in the PEC constitute a peculiar assemblage
with diverse evolutionary origins and a long history of resil-
ience to habitat alteration. Atlantic Forest mammals share
this small region of the northern coast of Brazil with
Amazonian clades and elements typical of the Caatinga sea-
sonally dry forest. As a result of this heterogeneity among
Atlantic Forest ecoregions and its interface, continuously
with the Caatinga and cyclically with the Amazon, the PEC
fauna represents a distinct assemblage from the rest of the
Atlantic Forest that is highly threatened by human activities,
leading previous authors to recognize it as a center of ende-
mism and a hotspot within a hotspot (Costa et al. 2000; Silva
and Casteleti 2003; Batista et  al. 2021; Dalapicolla et  al.
2021).
In this chapter, we present an overview of the mammalian
fauna in the Pernambuco Endemism Center, detailing the
current diversity and recent discoveries and exploring bio-
geographic patterns with special attention to the past connec-
tion between the PEC and eastern Amazon. Additionally,
using a large database based on museum records and field
surveys, we analyze the collection effort along the PEC and
reveal sampling biases in the region. We further review the
past and ongoing projects on mammals carried out in each of
the four states included in the PEC. Our goal here is to high-
light which subjects have been over- and understudied.
Finally, we present a new perspective on the deforestation
scenario in the PEC, with updated numbers of sizable forest
remnants per state and their degree of isolation, and explore
the effects of sugarcane and hunting on the conservation of
PEC mammals.
13.2 Diversity
We recognized 137 terrestrial mammal species in the PEC,
including five locally extinct and six endemic taxa (Table 13.1
and Fig. 13.1). We listed as part of the PEC fauna the West
Indian Manatee Trichechus manatus given its distribution
extends to the freshwater continental systems, estuaries, and
rivers (Bonvicino et al. 2020). This total represents ca. 36%

Table 13.1  List of mammals of the Pernambuco Endemism Center (PEC)

Species AL PE PB RN
DIDELPHIMORPHIA
Didelphidae
Caluromys philander (Linnaeus, 1758) MHNUFAL 961 UFPB 2382 UFPB 2380 PH Marinho, D.Obs
Didelphis albiventris Lund, 1840 MHNUFAL 300 UFPE 774 UFPB 2393 Photo1
Didelphis aurita Wied-Neuwied, 1826 MHNUFAL 009 UFPB 1978
Marmosa murina (Linnaeus, 1758) MHNUFAL 037 UFPB 3911 UFPB 2539
Marmosa demerarae (Thomas, 1905) MHNUFAL 052 UFPB 3910 UFPB 5034
Monodelphis americana (Müller, 1776) MHNUFAL 011 UFPB 1908 UFPB 3965
Monodelphis domestica (Wagner, 1842) MHNUFAL 098 UFPB 4714 UFPB 1962
Metachirus myosuros (Temminck, 1824) UFPE 784 UFPB 10627
Cryptonanus agricolai (Moojen, 1943) MHNUFAL 022 UFPE 2403 UFPE 3014
Gracilinanus agilis (Burmeister, 1854) MHNUFAL 368 MN 17162 UFPB 4686
Thylamys karimii (Petter, 1968) UFPB 11717
CINGULATA
Dasypodidae
Dasypus novemcinctus Linnaeus, 1758 MZUSP 7527 UFPE 1706 UFPB 746 Santos et al. (2019)
Chlamyphoridae
Euphractus sexcinctus (Linnaeus, 1758) MA Freitas, D.Obs Silva Jr and Mendes-­ UFPB 742 Santos et al. (2019)
Pontes (2008)
Cabassous tatouay (Desmarest, 1804) MHNUFAL 51 UFPB 7613
PILOSA
Bradypodidae Souto et al. (2019)
Bradypus variegatus Schinz, 1825 MHNUFAL 491 UFPE 1843 UFPB 762
Cyclopedidae
Cyclopes didactylus (Linnaeus, 1758) MN 17294 Miranda and Superina UFPB 6882 Miranda and Superina
(2010) (2010)
Mymercophagidae
Myrmecophaga tridactyla Linnaeus, 1758†
Tamandua tetradactyla (Linnaeus, 1758) MN 23950 UFPB 6874 UFPB 781 Santos et al. (2019)
SIRENIA
Trichechus manatus (Linnaeus, 1758) Alves et al. (2015) Alves et al. (2015); Barros et al. Barros et al. (2017b)
Attademo et al. (2020) (2017b)
(continued)
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns 203

Table 13.1 (continued)
Species AL PE PB RN
PRIMATES
Atelidae
Alouatta belzebul (Linnaeus, 1766) MN 25671 Fialho et al. (2014) UFPB 416 Fialho et al. (2014)
Cebidae
Callithrix jacchus (Linnaeus, 1758) MHNUFAL 7 UFPE 1591 UFPB 5253 Santee and Arruda (1994)
Sapajus flavius (Schreber, 1799)* Fialho et al. (2014) UFPB 5091 UFPB 5104 Fialho et al. (2014)
LAGOMORPHA
Leporidae
Sylvilagus brasiliensis (Linnaeus, 1758)* MN 24034 UFPE 1740 UFPB 927 PH Marinho, D.Obs
RODENTIA
Caviidae
Cavia aperea Erxleben, 1777 MHNUFAL 0378 UFPB 2084
Galea spixii (Wagler, 1831) MHNUFAL 0478 UFPB 2008 UFPB 9541 PH Marinho, D.Obs
Hydrochoerus hydrochaeris (Linnaeus, 1766) MHNUFAL 0202 Yang et al. (2021) UFPB 6236 PH Marinho, D.Obs
Kerodon rupestris (Wied-Neuwied, 1820) Vieira (1953) MA Freitas, D.Obs
Cuniculidae
Cuniculus paca (Linnaeus, 1766) UFPB 4097 UFPB 6451
Dasyproctidae
Dasyprocta iacki Feijó & Langguth, 2013* MN 8232 UFPB 6919 Photo2
Dasyprocta prymnolopha Wagler, 1831 MZUSP 7371 MN 7636
Echimyidae
Phyllomys sp. Iack-Ximenes UFPE (PHA 358) UFPB 5690
et al. (2005)
Thrichomys laurentius Thomas, 1904 UFPE (PHA183) UFPB 11753
Erethizontidae
Coendou prehensilis (Linnaeus, 1758)* MZUSP 7531 UFPE 1770 UFPB 931
Coendou speratus Mendes Pontes et al., 2013* MHNUFAL 048 UFPE 1708
Cricetidae
Akodon cursor (Winge, 1887) MHNUFAL 025 UFPB 3526 UFPB 163
Necromys lasiurus (Lund, 1840) MHNUFAL 012 UFPE 1914 UFPB 10634
Oxymycterus dasytrichus (Schinz, 1821) MHNUFAL 0310 UFPB 2678
Cerradomys langguthi Percequillo, Hingst-­ MHNUFAL 0312 UFPE 1854 UFPB 10314
Zaher & Bonvicino, 2008
Holochilus oxe Prado, Knowles & Percequillo, MHNUFAL 023 MN 66572 MZUSP 8419
2021
Hylaeamys oniscus (Thomas, 1904)* UFPB 3775 UFPB 1999 UFPB 1931
Nectomys rattus (Pelzeln, 1883) UFPB 3559 UFPB 2794
Nectomys squamipes (Brants, 1827) MHNUFAL 0444 UFPE 1082
Oecomys catherinae Thomas, 1909 MHNUFAL 066 UFPB 4447 UFPE 1890
Oligoryzomys nigripes (Olfers, 1818) MHNUFAL 010 UFPE 815 UFPB 1818
Oligoryzomys stramineus Bonvicino & Weksler, UFPB 3790 UFPB 1817 UFPB 1866
1998
Oligoryzomys mattogrossae (J. A. Allen, 1916) UFPB 977 UFPB 1893 UFPB-MPS78
Pseudoryzomys simplex (Winge, 1887) UFPB 4460 UFPB 826
Calomys mattevii Gurgel-Filho, Feijó & UFPE (DAM) 177 UFPB 4471
Langguth, 2015
Rhipidomys mastacalis (Lund, 1840) MHNUFAL 041 UFPE 1565 UFPB (JLF
27)
Sciuridae
Guerlinguetus brasiliensis (Gmelin, 1788) MZUSP 7532 UFPE 2814 UFPB 2980
CHIROPTERA
Emballonuridae
Centronycteris maximiliani (Fischer, 1829) UFPE 768
Diclidurus albus Wied-Neuwied, 1820 UFPE 371 Ferreira et al.
(2013)
Peropteryx kappleri Peters, 1867 MHNUFAL 0548 UFPE 223 UFPB 1300
Peropteryx leucoptera Peters, 1867 UFPE 1338 UFPB 10717 Barros et al. (2017a)
(continued)
204 A. Feijó et al.

Table 13.1 (continued)
Species AL PE PB RN
Peropteryx macrotis (Wagner, 1843) UFPB 3600 UFPE 221 UFPB 10692 Vargas-Mena et al.
(2018a)
Rhynchonycteris naso (Wied-Neuwied, 1820) MHNUFAL 0447 MHNUFAL 0173 UFPB 1312
Saccopteryx bilineata (Temminck, 1838) UFPB 5560
Saccopteryx leptura (Schreber, 1774) MHNUFAL 0451 UFPB 1294 UFPB 8170
Molossidae
Cynomops planirostris (Peters, 1866) UFPB 8313 UFPB 6609
Eumops glaucinus (Wagner, 1843) MHNUFAL 0101 UFPE 1878 UFPB 4929
Molossops temminckii (Burmeister, 1854) MHNUFAL 0233 UFPB 7361
Molossus molossus Pallas, 1766 MHNUFAL 038 UFPB 3172 UFPB 10566 Vargas-Mena et al.
(2018a)
Molossus rufus Geoffroy, 1805 MHNUFAL 0242 UFPE 219 UFPB 10693
Promops nasutus (Spix, 1823) UFPB 3169 P.Rocha, Barros et al. (2017a)
D.Obs.
Mormoopidae
Pteronotus gymnonotus (Wagner, 1843) UFPB 8931
Natalidae
Natalus macrourus (Gervais, 1856) UFPB 1 Vargas-Mena et al.
(2018a)
Noctilionidae
Noctilio leporinus (Linnaeus, 1758) UFPE 1368 UFPE 1732 UFPB 10575 UFPB 6036
Phyllostomidae
Carollia perspicillata (Linnaeus, 1758) MHNUFAL 0206 MHNUFAL 0163 UFPB 10712 Barros et al. (2017a)
Rhinophylla pumilio Peters, 1865 MHNUFAL 0209 UFPB 7030 UFPB 10799
Desmodus rotundus (Geoffroy, 1810) MHNUFAL 0220 MHNUFAL 0171 UFPB 11280 Barros et al. (2017a)
Diaemus youngii (Jentink, 1893) UFPB 11234 UFPB 7456
Diphylla ecaudata Spix, 1823 UFPE 1355 UFPB 6017 UFPB 10332
Anoura caudifer (Geoffroy, 1818) UFPE 1342
Anoura geoffroyi Gray, 1838 UFBA-mor-404
Dryadonycteris capixaba Nogueira et al., 2012 UFPB 4203
Lichonycteris degener Miller, 1931 UFPB 4202
Glossophaga soricina (Pallas, 1766) MHNUFAL 0139 MHNUFAL 0170 UFPB 10522 Barros et al. (2017a)
Lonchophylla mordax Thomas, 1903 UFPE 1383
Trinycteris nicefori (Sanborn, 1949) UFPB 4351 UFPE 3654
Micronycteris megalotis (Gray, 1842) UFPE 1341 UFPB 11238 UFPB 3781
Micronycteris minuta (Gervais, 1856) MHNUFAL 0205 UFPE 1083 UFPB 10791
Micronycteris schmidtorum Sanborn, 1935 MHNUFAL 0245 USNM 555703 UFPB 9240
Lonchorhina aurita Tomes, 1863 UFPE 1370 UFPB 10718
Macrophyllum macrophyllum (Schinz, 1821) UFPE 311 UFPB 3892
Trachops cirrhosus (Spix, 1823) MHNUFAL 0140 MHNUFAL 0161 UFPB 7553 Barros et al. (2017a)
Lophostoma brasiliense Peters, 1867 MHNUFAL 0453 MHNUFAL 0162 UFPB 8930 Barros et al. (2017a)
Lophostoma silvicola d’Orbigny, 1836 UFPB 3582 UFPE 1332 UFPB 11281
Phylloderma stenops (Peters, 1865) UFPE 7025
Phyllostomus discolor (Wagner, 1843) MHNUFAL 0321 MHNUFAL 0169 UFPB 10716 Barros et al. (2017a)
Phyllostomus elongatus (Geoffroy, 1810) MHNUFAL 0204 UFPE 3856
Phyllostomus hastatus (Pallas, 1767) UFPE 1357 UFPB 7036 UFPB 11279 Barros et al. (2017a)
Tonatia bidens (Spix, 1823) UFPB 4215 UFPB 1574 UFPB 16
Tonatia maresi Williams, Willig & Reid, 1995 UFPB 4214 UFPB 7041 UFPB 4354
Chrotopterus auritus (Peters, 1856) UFPB 1573
Ametrida centurio Gray, 1847 UFPB 9154
Artibeus fimbriatus Gray, 1838 MHNUFAL 0462 UFPB 4100 UFPB 11590
Artibeus lituratus (Olfers, 1818) MHNUFAL 0100 MHNUFAL 0168 UFPB 10506 Barros et al. (2017a)
Artibeus obscurus (Schinz, 1821) MHNUFAL 0356 MHNUFAL 0166 UFPB 10807
Artibeus planirostris (Spix, 1823) MHNUFAL 044 MHNUFAL 0167 UFPB 10804 UFPB 6035
Artibeus cinereus (Gervais, 1856) MHNUFAL 0211 MHNUFAL 0164 UFPB 8755 Barros et al. (2017a)
Chiroderma doriae Thomas, 1891 UFPB 4348 UFPB 7465 UFPB 7327
Chiroderma villosum (Peters, 1860) UFPB 4349 UFPB 7470 UFPB 4
Platyrrhinus incarum (Thomas, 1912) UFPB 4199
(continued)
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns 205

Table 13.1 (continued)
Species AL PE PB RN
Platyrrhinus lineatus (Geoffroy Saint-Hilaire, MHNUFAL 0344 UFPB 7463 UFPB 10788 UFPB 6037
1810)
Platyrrhinus recifinus (Thomas, 1901) UFPB 4347 UFPE 1446 UFPB 10714
Pygoderma bilabiatum (Wagner, 1843) UFPB 4338 UFPB 10790
Vampyressa aff. pusilla UFPB 4208
Sturnira lilium (Geoffroy Saint-Hilaire, 1810) MHNUFAL 0297 MHNUFAL 0172 UFPB 6038
Sturnira tildae De La Torre, 1959 Martins et al. (2020)
Thyropteridae
Thyroptera tricolor Spix, 1823 UFPB 4345
Vespertilionidae
Myotis lavali Moratelli et al., 2011 MHNUFAL 0136 MHNUFAL 0165 UFPB 11214 Barros et al. (2017a)
Myotis nigricans (Schinz, 1821) MHNUFAL 001 UFPE 1709 UFPB 1604 UFPB 1631
Myotis riparius Handley 1960 MVZ 185996 UFPB 11225
Myotis ruber (Geoffroy, 1806) UFPE 1345 UFPB 1603
Rhogeessa hussoni Genoways & Baker, 1996 UFPE 207 UFPE 1634
Eptesicus brasiliensis (Desmarest, 1819) UFPB 5400 UFPB 10532
Eptesicus furinalis (d’Orbigny & Gervais, 1847) UFPE 1378 UFPE 1400 UFPB 1641 Vargas-Mena et al.
(2018a)
Lasiurus egregius (Peters, 1870) UFPE 1281
Lasiurus blossevillii (Lesson, 1826) UFPB 3613 UFPB 8193 Barros et al. (2017a)
Lasiurus ega (P. Gervais, 1856) UFPE 344 UFPB 3893
CARNIVORA
Canidae
Cerdocyon thous (Linnaeus, 1766) MN 25585 MN 25580 UFPB 8848 UFPB 844
Mustelidae
Eira barbara (Linnaeus, 1758) UFPB 3564 Feijó and Langguth Feijó and
(2013) Langguth
(2013)
Galictis cuja (Molina, 1782) Nagy-Reis et al. UFPB 6476 UFPB 1375 Nagy-Reis et al. (2020)
(2020)
Lontra longicaudis (Olfers, 1818) MHNUFAL 0490 UFPB 7303 UFPB 5970 Laurentino et al. (2020)
Procyonidae
Nasua nasua (Linnaeus, 1766) UFPB 3566 UFPE 2746 Beltrão et al.
(2019)
Potos flavus (Schreber, 1774) UFPB 3565
Procyon cancrivorus (Cuvier, 1798) UFPB 4098 UFPE 2747 UFPB 6861 Nagy-Reis et al. (2020)
Felidae
Herpailurus yagouaroundi (É. Geoffroy Nagy-Reis et al. UFPE 1768 PH Marinho, D.Obs
Saint-Hilaire, 1803) (2020)
Leopardus emiliae (Thomas, 1914) MN 24895 UFPE 1593 UFPB 7954 UFPB 9604
Leopardus pardalis (Linnaeus, 1758) Nagy-Reis et al. Ramos et al. (2021) Beltrão et al. Marinho et al. (2017)
(2020) (2019)
Leopardus wiedii (Schinz, 1821) UFPE 978 UFPB 6456
Puma concolor (Linnaeus, 1771)†
Panthera onca (Linnaeus, 1758)†
PERISSODACTYLA
Tapirus terrestris (Linnaeus, 1758)†
ARTIODACTYLA
Cervidae
Mazama gouazoubira (Fischer, 1814) MA Freitas, D.Obs PH Marinho,
Unpublished
Tayassuidae
Dicotyles tajacu (Linnaeus, 1758) MHNUFAL 0482
Tayassu pecari (Link, 1795)†
The presence of species per state is indicated based on voucher specimens, literature, direct observation, or photographs. MHNUFAL Museu de
História Natural da Universidade Federal de Alagoas, Maceió, Alagoas, UFPB Universidade Federal da Paraíba, João Pessoa, Paraíba, UFPE
Universidade Federal de Pernambuco, Recife, Pernambuco, MN Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, MZUSP
Museu de Zoologia da Universidade de São Paulo, São Paulo, MVZ Museum of Vertebrate Zoology, Berkeley, USA, USNM Smithsonian National
Museum of Natural History, Washington, USA
†Extinct in the PEC; *Endemic to the PEC; D.Obs. = Direct observation; Photo1  = https://www.inaturalist.org/observations/1605398 ; Photo2  =
https://www.inaturalist.org/observations/84135631
206
Fig. 13.1  Mammal species in the PEC per taxonomic order showing
the number of extinct and endemic taxa. Inset maps show the Brazilian
biomes and the location of the PEC in purple. Black dots represent the
location of state capitals. The delimitation of the PEC was based on the
of the mammals recorded in the Atlantic Forest biome (AF)
and ca. 18% of the Brazilian terrestrial fauna (Quintela et al.
2020; Abreu et al. 2021; Figueiredo et al. 2021). The giant
anteater Myrmecophaga tridactyla, the puma Puma con-
color, the jaguar Panthera onca, the white-lipped peccary
Tayassu pecari, and the tapir Tapirus terrestris are now con-
sidered extinct in the PEC. Garbino et al. (2018) listed seven
species locally extinct in the PEC, but recent evidence (see
Table  13.1) revealed some relict natural (non-introduced)
populations of gray brocket deer Mazama gouazoubira and
collared peccary Dicotyles tajacu.
Among the non-extinct fauna, small mammals comprise
77% of the entire assemblage (Table 13.1). Bats are by far
the most diverse group in the PEC, with 70 species (53% of
the PEC mammalian fauna), which is more than half of the
bat  species present in the AF (Figueiredo et  al. 2021).
Marsupials (11 species, 8.4%) represent about 35% of the
marsupial diversity in the biome. Small rodents, on the other
hand, with 21 species, represent only 14% of the rodent diver-
sity in the AF, reflecting higher ecoregional endemism and
restricted distributions among rodents. Accordingly,
Dalapicolla et al. (2021) recognized the PEC as one of the
seven areas of endemism for small rodents in the AF. Overall,
14 rodents are exclusive to this part of the biome, of which
A. Feijó et al.
Instituto Nacional de Pesquisas Espaciais (INPE), available at http://
terrabrasilis.dpi.inpe.br/downloads/. Abbreviations: AF Atlantic Forest,
RN Rio Grande do Norte, PB Paraíba, PE Pernambuco, AL Alagoas
four are endemic to the PEC (the medium-sized Dasyprocta
iacki, Coendou prehensilis and Coendou speratus, and the
small-sized Hylaeamys oniscus) (Fig.  13.2). Notably, this
high endemism has been just recently documented. The red-­
rump agouti D. iacki and the dwarf porcupine C. speratus
were described in 2013 (Feijó and Langguth 2013; Mendes-­
Pontes et al. 2013), and the actual species limits of C. pre-
hensilis were just redefined by Menezes et al. (2021).
The medium and large mammal fauna in the PEC com-
prises a very diverse group and originally included all orders
of mammals occurring in Brazil (Quintela et al. 2020). We
followed Feijó and Langguth (2013) and considered medium
and large mammals all species of the orders Artiodactyla,
Carnivora, Cingulata, Lagomorpha, Pilosa, Perissodactyla,
Primates, and part of Rodentia (Cuniculidae, Dasyproctidae,
Erethizontidae, and Hydrochoerinae). Carnivora is particu-
larly diverse, with 11 species, but includes only taxa widely
distributed in the country (Table  13.1). In contrast, among
the three species of Primates, the blonde capuchin monkey
Sapajus flavius is endemic to the PEC, and the red-handed
howler Alouatta belzebul has a disjunct distribution in the
PEC and eastern Amazon. The only member of the order
Lagomorpha is the endemic tapeti Sylvilagus brasiliensis, a
species long-standing viewed as widely distributed in South
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns
Fig. 13.2  The six PEC endemic mammal species. (a) Brazilian porcu-
pine Coendou prehensilis. (b) Dwarf porcupine Coendou speratus. (c)
Tapeti Sylvilagus brasiliensis. (d) Red-rumped agouti Dasyprocta iacki.
(e) Rice rat Hylaeamys oniscus. f. Blonde capuchin monkey Sapajus
America, but recently restricted to the PEC (Ruedas et  al.
2017) as was Coendou prehensilis (Menezes et al. 2021).
When species diversity is compared among the Brazilian
states, Pernambuco is the richest state with 110 confirmed
species, followed by Alagoas (106 species) and Paraíba (103
species). Rio Grande do Norte has only 45 species with con-
firmed presence in the PEC (Table  13.1), which is
likely  related to a lack of studies in this state (see Sect.
13.4). Even though these richnesses are fairly similar, some
intriguing cases are worth mentioning. Paraíba is the most
sampled state, having received three times more collection
effort than Alagoas and Rio Grande do Norte (see next sec-
tion), but Alagoas still holds a higher verified diversity.
Some species have been commonly recorded in some states,
but never in others. For example, Didelphis aurita seems to
have its northern distribution limited to the Pernambuco
Atlantic Forest as it was never collected in Paraíba or Rio
Grande do Norte. Metachirus myosurus also extends its
northward range to the Pernambuco and Paraíba limits.
Similarly, the available records of Coendou speratus,
Nectomys squamipes, Trinycteris nicefori, and Phyllostomus
elongatus are limited to Pernambuco and Alagoas. In con-
trast, Thylamys karimii was only recorded in the PEC in
Paraíba (even though it occurs in other inland localities out-
side the PEC in the other states). Coatis Nasua nasua are
often observed in Pernambuco, even closer to urban centers
or within crops, while its first record to Paraíba was just
207
flavius. Photos by Marco Antônio Freitas (a–b), Helio Lourencini (c,
retrieved from inaturalists.org), Hugo Fernandes-Ferreira (d), Mayara
Beltrão (e), Bruna M. Bezerra (f)
recently published (Beltrão et  al. 2019). Potos flavus,
Vampyressa aff. pusilla, and Thyroptera tricolor were only
recorded in the PEC in Alagoas. Whether these examples
can be attributed only to opportunistic captures or suggest a
particular biogeographic filter (see next section), limiting
those species to extend their distribution across the PEC,
remains an open question. An alternative explanation is that
most of those taxa rely strongly on humid forest cover to
survive, and the remnant fragments in Paraíba are composed
of semi-deciduous forests and are no longer suitable to
maintain their populations. As we discuss below, Alagoas
still holds a considerable number of fragments compared to
Paraíba. In this scenario, local extinction in Paraíba would
be higher than that documented for the PEC.
In addition to the fauna documented here, there is com-
pelling evidence suggesting a still undescribed diversity.
Campos (2009) recognizes the population of Rhipidomys
from Bezerros, Pernambuco, as a distinct lineage that still
lacks a binomial name. Loss and Leite (2011) and Machado
et al. (2018) advocate that the population of Phyllomys in the
PEC represents a distinct unnamed species.
A quite peculiar pattern is that five of the six endemic spe-
cies are of medium size (Table 13.1 and Fig. 13.2). In Brazil,
as a comparison, about 62% of the endemic species are small
mammals (bats, marsupials, and small rodents; Quintela
et  al. 2020). In the whole Atlantic Forest, small mammals
account for 82% of endemics (Figueiredo et al. 2021). In the
208
adjacent biome, small rodents and bats represent 9 of the 11
Caatinga endemic species (Carmignotto and Astúa 2017).
This scenario leads us to anticipate that endemic small mam-
mals are being overlooked in the PEC and likely reflect the
lack of taxonomic and phylogenetic studies involving popu-
lations from the region. The recent findings of Campos
(2009), Loss and Leite (2011), and Machado et  al. (2018)
support our expectations.
Furthermore, several new bat species have been added to
the PEC fauna in the last few years (Nunes et al. 2013, 2018;
Vilar et al. 2015). Some of these new occurrences represent
the first record for the Atlantic Forest, such as Molossops
temminckii previously recorded only in Caatinga and Cerrado
(Nunes et  al. 2013) and Ametrida centurio, viewed as an
Amazon endemic (Vilar et al. 2015). In common, these two
bats were trapped in canopy mist nets. The use of this new
sampling method allows the capture of species poorly sam-
pled in the understory, where the great majority of the studies
have focused. So far, within the PEC, canopy mist nets have
been applied only in two municipalities in Paraíba
(Mamanguape and João Pessoa). Similarly, the use of acous-
tic techniques to survey bats has revealed that several species
(in particular molossids and vespertilionids) are more com-
mon than previously thought based on mist-net surveys
(P.A.  Rocha, unpublished data). In a parallel scenario, the
recent systematic use of camera traps and road monitoring to
survey medium and large mammals has brought the presence
of rare species into the light. The ocelot Leopardus pardalis
was not recorded by Feijó and Langguth (2013) in the PEC,
but Marinho et al. (2017) and Beltrão et al. (2019) reported it
for the Atlantic Forest of Rio Grande do Norte and Paraíba,
respectively. We can thus expect more species will be added
to the PEC mammal fauna when complementary methods
are widely applied. In addition, the sampling effort in the
PEC has been extremely biased toward a few protected areas
and the state capitals (see Sect. 13.4). The state of Alagoas,
which harbors a relatively high number of protected areas,
the larger forest remnants in the PEC, and has a poor history
of mammal surveys (see below), is particularly promising for
new findings.
13.3 Biogeography
The Pernambuco Endemism Center was originally defined as
one of the six endemism centers of the Atlantic Forest biome
(Silva and Casteleti 2003), which encompassed two terres-
trial ecoregions (Olson et al. 2001), the Pernambuco Coastal
Forest and the Pernambuco Interior Forests (a transition
zone between Caatinga and Atlantic Forest). This large bio-
geographical unit was also termed and defined as the portion
of the Atlantic Forest to the north of the São Francisco River
(Tabarelli et  al. 2005). Ribeiro et  al. (2009) used the
term biogeographical subregion for the PEC, terming it
A. Feijó et al.
Pernambuco and dismembering the PEC into coastal low-
lands (Pernambuco) from the interior or coastal highlands
(Brejos Nordestinos also known as Brejos de Altitude). The
latter also included forest formations more consensually
included in the Caatinga biome as the Araripe region in the
core of this seasonally dry forest biome. It is clear that these
high-altitude mesic forest enclaves have dynamic and diverse
histories, which deserve individual detailed accounts and,
therefore, cannot be treated as a single unit (Pôrto et al. 2004;
Guedes et  al. 2014). As Marques and Grelle (2021) have
shown, except for the interior altitudinal mesic forest
enclaves, the biogeographical regionalizations of the PEC
are congruent. For analytical purposes, the PEC as here
defined encompasses lowland coastal Atlantic Forests of the
states of Alagoas, Pernambuco, Paraíba, and Rio Grande do
Norte (Fig. 13.1).
Neighboring biogeographical units (ecoregions or bio-
geographical subregions) are also consensual. Within the
Atlantic Forest biogeographical subdivisions to the south,
we have the Bahia Coastal Forest ecoregion or Bahia bio-
geographic subregion or Bahia Corridor (Marques and Grelle
2021). The PEC distinguishes itself from its neighboring
Atlantic Forest ecoregion, the Bahia Corridor, in many defin-
ing characteristics. It harbors a distinct climatic regime with
lower precipitation (1000–1300  mm/yr), distributed much
more seasonally, mostly concentrated in the fall-winter
months of March–August, with substantial annual variation
originating from El Niño-Southern Oscillation (Cirino et al.
2015). Its geology is dominated by tabuleiros formations,
tablelands of small altitude ~100  m plateaus, cut by west-­
east coastal drainage systems of perennial rivers that origi-
nate at the limit of the western Borborema plateau (~500 m).
The Borborema plateau corresponds to the Caatinga biome
ecoregion of the same name. This ecoregion has the largest
contact zone with the PEC, followed by the two seasonally
dry forest lowlands Depressão Sertaneja Setentrional to the
North and Depressão Sertaneja Meridional to the South
(Silva et al. 2018). Climatic and geological differences from
its neighboring ecoregions, together with the São Francisco
river, an old drainage system that has been erected as respon-
sible for ancient (Pliocene) vicariant events on faunal com-
ponents (Nascimento et  al. 2013), have contributed to the
evolution of a distinct faunal assemblage within the PEC.
Most likely, this is the less dynamic pattern that can be
attributed to the PEC, which is likely a much more complex
and dynamic system interacting with three other biogeo-
graphical units: the Atlantic Forest enclaves within the
Caatinga biome, the Borborema ecoregion high-altitude pla-
teau of the Caatinga biome, and cyclical contacts with the
Amazon biome in glaciation-driven climatic cycles
(Fig. 13.3).
Atlantic Forest enclaves within the Caatinga biome are
mid-altitude mesic enclaves of moist forest surrounded by
the seasonally dry forests of the Caatinga biome. They allow
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns
Fig. 13.3  Mammal species in the PEC shared with other biomes. Left panel shows the overall proportion per biome, and the right panel shows
the number of species (and percentage) shared between biomes and the PEC fauna
the presence of forest specialist taxa such as the arboreal
Sigmodontine rodent Rhipidomys. Depending on the defini-
tion (e.g., Atlantic Forest Brazilian law), forest enclaves of
the Atlantic Forest can encompass the northernmost altitudi-
nal enclaves in Ceará state, which harbor Amazonian faunal
components, such as Coendou baturitensis. Irrespective of
their definition, they can be viewed either as refuges, islands,
or stepping stones for forest specialist taxa dispersal through
the seasonally dry forest matrix of the Caatinga.
Despite its small extension, the PEC has high vegetation
heterogeneity. Its northern part in the states of Paraíba and
Rio Grande do Norte harbors semi-deciduous or deciduous
forests, whereas its southern components in the states of
Pernambuco and Alagoas are characterized by ombrophilous
forests. Caatinga small mammal endemics such as Thylamys
karimii and Thrichomys laurentius are only or mainly found
in the northern portion (Table 13.1). Conversely, this north-
ern part does not account for species that thrive in more
mesic environments, such as Didelphis aurita and Metachirus
myosurus (Table  13.1), or accounts for these species pres-
ence in very low densities, as for coatis. The distributional
limit between the water rats Nectomys squamipes, in the
south, and N. rattus, in the north, likely located within the
state of Pernambuco, reinforce the existence of a transition
zone between drier environments under the influence of the
Caatinga biome to the north and moister environments
under the southern Atlantic Forest and oceanic influences in
the southern region of the PEC.
The biogeographic position of the PEC is also noticeable
since it is bordered on the western flanks by three ecoregions
of the seasonally dry forests of the Caatinga biome, the
Boborema plateau at westward, the Depressão Serteneja
Setentrional at its northwestern border, and the Depressão
Sertaneja Meriodional at its southwestern border (Velloso
et al. 2002) and Atlantic Forest ecoregion the Bahia Coastal
209
Forest at its south (Marques and Grelle 2021). Although the
vegetation composition of the PEC is a characteristic of the
Atlantic Forest, the analysis of small mammals communities
among ecoregions of the Atlantic Forest (Bovendorp et  al.
2017; Figueiredo et al. 2017; Dalapicolla et al. 2021) and the
neighboring Caatinga ecoregions (Martins 2018) shows the
transitional nature of the PEC small mammal fauna. Small
mammal communities from the PEC show less dissimilarity
with neighboring Caatinga ecoregions than with other
Atlantic Forest ecoregions (Fig.  13.4). In addition, it has
stronger affinities with dry Atlantic Forest showing its cli-
matic distinctiveness from more mesic Atlantic Forest ecore-
gions especially the forests from Bahia state (Fig. 13.4).
Finally, the PEC is also a dynamic region considering the
faunal shared component between the Amazon biome and
the Atlantic Forest. Costa (2003) showed connection routes
between the two largest moist forest biomes of the Neotropics,
including the route connecting the eastern Amazon and the
northern Atlantic Forest. More recently, it has been shown
that this connection is recurrent (Thomé et al. 2016), inter-
rupted when seasonally dry forests from the Caatinga biome
expanded into rain forest domains along the Pleistocene and
the late Holocene Last Glacial Maximum. Figure 13.5 shows
the distinct cyclic climatic conditions throughout the
Quaternary in northern Brazil. These maps illustrate that,
during different periods, temperature and precipitation in the
northern part of the PEC tend to be more similar to the north-
ern part of the Caatinga and eastern Amazon than to the
southern portion of the PEC, which is overall warmer and
more humid. Such uneven past climate scenarios may help
explain the present-day distinct vegetation formation within
the PEC and possible connections with eastern Amazon and
Caatinga.
In conclusion, the PEC is often viewed as the northern-
most part of the Atlantic forest. However, patterns of ende-
210
Fig. 13.4  Dissimilarity (Sorensen index) among small mammal com-
munities from Atlantic Forest ecoregions (green) and neighboring
ecoregions of the Caatinga biome (purple). The PEC is represented by
Pernambuco coastal and interior forest ecoregions. The Complexo
mism of small and medium-sized mammals, phylogeographic
patterns, and community structure of small mammals also
highlight this ecoregion as a dynamic transition zone at the
crossroads among three forested biomes, the Atlantic Forest,
the Amazon, and the Caatinga.
13.4 Research Trends and Sampling Gaps
Although the PEC has a relatively small area, there is a clear
historical difference in mammal studies across its four states.
To explore research trends on mammals in the PEC, we com-
piled the records available in the mammal collections of the
A. Feijó et al.
Chapada Diamantina ecoregion (blue) can be classified in both biomes
depending on biological or environmental law criteria. Ecoregions
based on Olson et al. (2001)
Universidade Federal da Paraíba (UFPB), Universidade
Federal de Pernambuco (UFPE), and the Museu de História
Natural of the Universidade Federal de Alagoas (MHN/
UFAL). We complemented this dataset with the data avail-
able in the Global Biodiversity Information Facility (https://
doi.org/10.15468/dl.drejhs accessed on 16 July 2021) and
the Atlantic/Neotropical series data papers. These data
papers represent a recent effort to assemblage records derived
from published and unpublished studies based on diverse
methods (e.g., field survey, interview, road kills, camera
traps, direct observation) and include bats (Muylaert et  al.
2017), camera traps (Lima et  al. 2017), small non-volant
mammals (Bovendorp et  al. 2017), primates (Culot et  al.
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns 211

Fig. 13.5  Climate changes throughout the Quaternary in northern Alagoas, BA Bahia, CE Ceará, MA Maranhão, PA Pará, PB Paraíba, PE
Brazil. (a) Annual Mean  Temperature. (b) Precipitation seasonality. Pernambuco, PI Piauí, RN Rio Grande do Norte, SE Sergipe, TO
Climatic scenarios based on Brown et al. (2018). Abbreviations: LGM Tocantins
Last Glacial Maximum, LIG Last Interglacial, Brazilian states: AL
212
2019), middle-and-large mammals (Souza et al. 2019), xen-
arthrans (Santos et  al. 2019), and carnivores (Nagy-Reis
et al. 2020) datasets.
After excluding erroneous records, those derived from
invasive species and with a high level of uncertainty (above
20 km) in the geographic coordinates, our final dataset com-
prises 7590 individual records of mammals in the PEC.
Chiroptera (n  =  3940; 51.9%) is by far the most sampled
order of mammals, comprising half of all records (Fig. 13.6).
Rodentia (1380; 18.2%) is the second most recorded group,
followed by Didelphimorphia (909; 12%), Carnivora (611;
8.1%), Primates (370; 4.9%), Pilosa (253; 3.3%), Cingulata
(84; 1.1%), Lagomorpha (22; 0.3%), and Artiodactyla (21;
0.3%). Most of the records came from Paraíba (n  =  3349;
44.1%) and Pernambuco (3125; 41.2%) states, while Alagoas
(808; 10.6%) and Rio Grande do Norte (308, 4.1%) were the
least sampled states. It is noteworthy that the original Atlantic
Forest extension covers only 7.7% of the state of Rio Grande
do Norte  (the remaining is  covered by Caatinga), while it
covers about 37% of Alagoas; therefore, Alagoas can be con-
sidered the least studied state in the PEC for mammals.
The spatial distribution of the records reveals a clear geo-
graphic bias (Figs. 13.6 and 13.7). About 67% of the PEC
contain less than five individual records, and grid cells with
none or only one record represent 56% of the whole area.
Overall, the sampling effort is concentrated in the eastern
portion of the PEC, surrounding the state capitals and in
Fig. 13.6  Records of
mammals in the PEC
classified by taxonomic order
and Brazilian state. (a) Map
shows the distribution of the
7590 records (see text for
details) colored by taxonomic
order. Barplots show the
records per taxonomic order
(b) and per state (c).
Abbreviations: AL Alagoas,
PB Paraíba, PE Pernambuco,
RN Rio Grande do Norte
A. Feijó et al.
some of the protected areas. A large part of the north and
west of Alagoas and the west of Pernambuco have very few
records (Fig. 13.7). Although Rio Grande do Norte has the
least number of records, they are more evenly distributed
than Alagoas. Paraíba exhibits a more even distribution of
records across the state.
The ten most sampled areas, which account for about
60% of records, are (Fig. 13.7): Reserva Biológica (Rebio)
Guaribas (n  =  1228 records; 16.2% of all records), João
Pessoa (757; 10%), Reserva Particular do Patrimônio Natural
(RPPN) Pacatuba (524; 6.9%), Estação Ecológica (ESEC)
Caetés–Aldeia region (385; 5.1%), Rebio Saltinho (382;
5%), Brejo dos Cavalos (221; 2.9%), Usina Salgado-Ipojuca
(208; 2.7%), ESEC Tapacurá (204; 2.7%), ESEC Murici
(197; 2.6%), and Ibateguara (182; 2.4%).
When exploring the spatial pattern per group, the bias
toward the eastern portion of the PEC becomes more evident
(Fig. 13.7). Medium and large mammals are poorly recorded
far from the state capitals, revealing a more opportunistic
collection of these groups likely associated with road-killed
animals. Small non-volant mammals are slightly better sam-
pled in the western portion, and bats tend to have a higher
density of records per grid cell.
Overall, these findings show that the sampling effort for
mammals in the PEC has mostly been limited to a few pro-
tected areas. Except for Paraíba, the other states have very
limited and geographically restricted sampled sites for most
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns
Fig. 13.7  Density of records at 15 km grid resolution in the PEC for all
mammals (left map) and for distinct taxonomic groups separately. Red
dots represent the state capitals and the top 10 most sampled areas are
of the groups. Even for bats, the most sampled mammalian
group, 82% of the PEC remain unstudied (with less than five
records per grid cell). To help researchers define new target
areas for future projects, we associated the map of sampling
effort density with that of forest remnants and protected
areas (Fig. 13.8). To calculate the density of protected areas
(PA) across the PEC, we first split them into 10  ×  10  km
grids and retrieve the centroid point of each grid cell to
account for differences in area. This dataset was then com-
bined with the centroid coordinates of private protected
areas, known as Private Reserves of Natural Heritage (from
the original Portuguese “Reserva Particular do Patrimônio
Natural”—RPPN), provided by Carvalho et  al. (2021)
(Fig. 13.8e).
Correlation tests reveal a weak association between den-
sity of forest remnants (and PA) and density of mammal
records at 15  km grid resolution (remnants: r  =  0.16,
t = 2.6351, df = 257, p = 0.0089; PA: r = 0.16, t = 2.6011,
df = 257, p = 0.0098). This suggests that grid cells with avail-
able forest remnants and PAs have an overall lower density
of mammal collection. The most promising areas for future
studies, that is, areas with low sampling effort but with a
213
listed on the left map. Note the difference in record density scales
across maps
relatively high density of forest remnants or PAs, are located
in Alagoas and western Pernambuco (Figs. 13.8d, g).
In summary, we recommend future projects aiming to sur-
vey the diversity of mammals in the PEC to target the west-
ern region, especially in Alagoas and Pernambuco. Carvalho
et al. (2021) found that the western portion of the PEC pres-
ents the highest sampling relevance for vertebrate studies
given its environmental heterogeneity relative to the eastern
portion. Despite the low number of government-protected
areas in the PEC, Alagoas, and Pernambuco have 64 RPPNs,
many of which are located in poorly sampled zones
(Fig. 13.8g). These are good candidate areas for future field
studies.
13.5 History of Mammal Research Across
States
In addition to the sampling collection bias detailed above,
research projects carried out across the states of the PEC have
distinct goals. In this section, we present a brief overview of
the main historic and current studies developed in each state.
214
Fig. 13.8  Maps of sampling effort density (a), forest remnants (b–d),
and protected areas (e–g) in the PEC. Panels b and e show the distribu-
tion of forest remnants and protected areas (RPPNs are shown as cen-
troid points) in the PEC. Panels c and f are density maps of the forest
13.5.1 Alagoas
In the 1950s, Vieira (1953) published the first scientific sur-
vey focusing on mammals of Alagoas, presenting 27 species
distributed in nine orders. At that time, four of the species
(three bats Rhynchonycteris naso, Lonchophylla mordax,
and Molossus rufus, and the silky anteater Cyclopes didacty-
lus) were unknown to northeastern Brazil. This checklist was
based on specimens collected in expeditions that took place
between 1951 and 1952, and the specimens are currently
deposited at the Museu de Zoologia of Universidade de São
Paulo (MZUSP). Also, between 1940 and 1956, expeditions
were conducted by the National Plague Service (“Serviço
Nacional da Peste”‘—SNP), a government project aiming to
identify natural reservoirs of the bacterium causing bubonic
plague, Yersinia pestis, and control the disease (Oliveira and
Franco 2005). During this period, small non-volant mam-
mals were collected, mostly rodents, but also some marsupi-
als, in the Agreste of northeastern Brazil, the transitional
region between coastal humid forests and semiarid inland,
contributing to more than 50,000 specimens now housed at
the Museu Nacional of the Universidade Federal do Rio de
Janeiro (MNRJ). Of these, about 7500 specimens were col-
lected in the PEC of Alagoas (Oliveira and Franco 2005) and
A. Feijó et al.
remnants and protected areas at 15 km grid resolution. In panels d and
g, warmer-colored grid cells represent areas with a higher density of
forest remnants (d) and protected areas (g) but a lower density of mam-
mal records
have been continuously used in several studies on small
mammals to address questions in diverse topics, such as
reproductive biology (Cerqueira and Lara 1991; Cerqueira
2005; Guilhon et  al. 2019) and taxonomy (Iack-Ximenes
et al. 2005; Tribe 2005; Mendes-Pontes et al. 2013; Caccavo
and Oliveira 2016).
Other studies on public health, specifically on the spread
of Schistosoma mansoni infections, have also contributed
with information about the small mammals of Alagoas. For
example, Amorim (1962) listed 15 species for the municipal-
ity of Viçosa, including eight not listed by Vieira (1953):
Nectomys squamipes, Akodon sp., Necromys lasiurus,
“Oryzomys subflavus”, “Oryzomys eliurus” (probably
Cerradomys langguthi and Oligoryzomys nigripes),
Thomazomys pyrrhorhinos (currently Wiedomys pyrrhorhi-
nos), Cercomys c. laurentius (currently Thrichomys lauren-
tius), and Monodelphis domestica. Chieffi et  al. (1994)
reported five rodents (Rattus rattus, Holochilus brasiliensis
[currently H. oxe], Nectomys squamipes, “Oryzomys” sp.,
and Galea spixii) for the municipality of Branquinha.
Unfortunately, none of these studies listed voucher speci-
mens, making it difficult to update the species identity, such
as those classified as “Oryzomys,” or to confirm it, such as
the presence of W. pyrrhorhinos, which is considered
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns
endemic to the Caatinga biome (Carmignotto and Astúa
2017).
In the 1990s, surveys were conducted by researchers from
Pernambuco and Paraíba universities in some of the main
remnants of Alagoas: Rebio de Pedra Talhada (Guerra 2015;
Guerra and Langguth 2015) and Usina Serra Grande
(Fernandes 2003; Sá-Neto 2003; Sá-Neto et al. 2013). These
studies aimed to survey the mammal assemblage in these
important fragments within the PEC and were the first to
present a more comprehensive list of bat species to the state.
In the forest remnants of Usina Serra Grande, in addition to
assessing the effect of fragmentation on the composition of
mammals and other ecological aspects, 15 mammals were
considered locally extinct: the gray brocket Mazama
gouazoubira, the tapir Tapirus terrestris, the jaguar Panthera
onca, the puma Puma concolor, the margay Leopardus wie-
dii, and the bush dog Speothos venaticus. These are the first
comprehensive surveys for the state, after nearly 50  years,
covering distinct groups of mammals, such as artiodactyls,
lagomorphs, primates, bats, carnivores, xenarthrans, marsu-
pials, and rodents. Additionally, Feijó and Langguth (2013)
published a systematic review of the medium and large
mammals from northeastern Brazil, including Alagoas.
Among the examined materials are those collected by Vieira
(1953) and by the SNP expeditions, and they recorded 20
species for the PEC in Alagoas.
Since 2012, with the creation of a specific sector for mam-
mals and a mammal collection at the MHN/UFAL in Alagoas,
along with the hiring of the permanently employed mam-
malogist, Anna Ludmilla da Costa-Pinto, surveys have been
carried out in the state, confirming the occurrence of several
species and expanding the known distribution for others,
namely, Coendou speratus (Nascimento and dos Santos
2014), Cabassous tatouay (Nascimento 2013), and
Phyllostomus discolor (Costa-Pinto 2020). The museum cur-
rently harbors approximately 600 specimens of 84 mammal
species, mostly collected in the PEC of Alagoas. A recent
effort was also made to generate a list of bat species for the
state, using only records with voucher specimens housed in
museums and including acoustic analyses for some species
(Leal et  al. 2022). Researchers at MHN/UFAL are now
resuming projects in important fragments of the PEC of
Alagoas, such as the Murici Ecological Station (ESEC
Murici), where a 1-year inventory and ecological surveys of
small non-volant mammals have already been carried out,
and efforts are now being focused on bats and medium and
large-sized mammals. Another research front on mammals is
starting on Serra da Saudinha, an important remnant in the
metropolitan area of Maceió where there is a proposal to cre-
ate an RPPN. There are also plans for mammal surveys in
fragments south of the PEC, where there is a historical sam-
pling effort gap.
215
Finally, a new species of South American marsh rat was
just described from the PEC, Holochilus oxe (Prado et  al.
2021). The specimen used for the species description was
collected by A.L. Costa-Pinto in 2013 at ESEC Murici, being
the first mammal holotype for the state of Alagoas. This dis-
covery reinforces the need for studies aiming to explore the
mammal taxonomy in the region and highlights how much
remains to be discovered in the PEC of Alagoas.
13.5.2 Pernambuco
The history of mammals collected in Pernambuco (but not, at
first, necessarily of proper scientific research) is mixed with
the history of Brazilian and Neotropical Mammalogy itself
(Hershkovitz 1987). While it is now known that Vicente
Pinzón did land in Pernambuco at the beginning of 1500s,
before the so-called official discovery of Brazil, and that he
is credited for collecting and bringing to Europe the first
known marsupial (Ávila-Pires and Oliveira 2014), it cannot
be for sure determined where those specimens came from in
Brazil.
Nevertheless, our knowledge on Pernambuco mammals,
whether through depicted or collected specimens dates as
back as the 1600s, due to the short but impressive presence
of the Dutch West India Company (DWIC) in northeastern
Brazil and settled in Pernambuco, between 1624 and 1654,
especially during the presence of Johan Maurits, Count of
Nassau-Siezen as Governor-General (Whitehead 1976). In
1638, Count Maurits led an expedition that included Georg
Marcgrave, a naturalist trained in botany and astronomy. His
notes and illustrations were published (Marcgrave 1648) a
few years after his death (Hershkovitz 1987). The accurate
depictions of specimens (many of which undoubtedly came
from the coastal Atlantic forest) ultimately were used by
Linnaeus (1758) in the Systema Naturae (Hershkovitz 1987).
While it may be argued that most of those specimens were
not collected, and descriptions were based on illustrations
and that not all specimens reported by Marcgrave were nec-
essarily from Pernambuco (as their explorations included
also Alagoas, Ceará, Paraíba, and Rio Grande do Norte),
they represent nonetheless the first records of mammals of
Pernambuco studied (Ávila-Pires and Oliveira 2014), and
many were very likely collected in Pernambuco, due to the
proximity of Recife, the headquarters of the DWIC. In fact,
there are records of captive mammals in a zoo-botanical gar-
den built by Nassau in Recife, including rodents, carnivores,
and primates (Almeida et  al. 2011). While this zoo appar-
ently lasted for a few years only, captive specimens were
likely studied by Marcgrave (Almeida et  al. 2011).
Additionally, there seems to be little doubt that some might
have been collected and brought alive to Europe way before
216
the Nassau period, as a clear and detailed depiction of a
Sapajus flavius appears in the frescos of the Medici Villa of
Poggio a Caiano, painted by Andrea del Sarto around 1519–
1521, and was likely based on the Pope Leo X’s menagerie
(Masseti and Veracini 2010). A long gap separates the time
of Marcgrave’s work and subsequent collections at the PEC,
such as those by Alphonse Robert in the early twentieth cen-
tury, which resulted in new rodent species from the PEC in
Pernambuco (Oliveira and Langguth 2004), but the modern
development of mammal studies in the PEC dates only from
the second half of the twentieth century. With the hiring of
Deoclécio Guerra at the Universidade Federal de Pernambuco
and the simultaneous creation of the Mammal Collection at
the same institution in 1968 (Astúa 2011), research on PEC
mammals was initially focused on bats. Deoclécio Guerra
remained the curator of the Mammal collection until his
retirement in 1998. Thirteen years later, he would return to
the UFPE as an MSc student, where he graduated in 2007
with a thesis on the bats of Pernambuco, based on the revi-
sion of nearly 1300 specimens held at the Mammal
collection.
Along with the studies of Deoclécio Guerra on bats,
research on mammals of the PEC in Pernambuco has also
had a strong influence of Maria Adelia Monteiro da Cruz,
who started working at the Universidade Federal Rural de
Pernambuco (UFRPE) in 1984. Her research, which focused
mostly on primate behavior, also extended later to other
mammal groups and resulted ultimately in the first list of
Pernambuco mammals (Cruz et al. 2002). Her ongoing work
resulted so far in over 30 articles, 12 book chapters, and 15
supervised theses and dissertations focused mostly on the
behavior and ecology of PEC primates. Since then,
Pernambuco has developed a strong tradition in ethology,
with many studies on PEC primates with the hiring of
Antonio S. Souto at UFPE in 1992, Nicola Schiel at UFRPE
in 2008, and Bruna M. Bezerra at UFPE in 2014. Their stud-
ies on PEC mammals (ethology, bioacoustics, and conserva-
tion) sum up about 50 articles, 5 book chapters, and 22 theses
and dissertations supervised, including important informa-
tion on the ecology and behavior of the PEC endemic Sapajus
flavius. Also at the UFPE from 1995 to 2013, Antonio
R. Mendes Pontes worked initially on primate behavior but
later conducted several surveys in forest fragments in the
PEC, focused both on small and large mammals and occa-
sionally on bats, resulting in 16 articles, 5 book chapters, and
supervised 12 theses and dissertations on PEC mammals,
including the description of the PEC endemic Coendou spe-
ratus. Other permanently employed mammalogists that
occasionally work or have worked on PEC mammals (col-
lecting, publishing, and directing graduate students) include
Diego Astúa (at the UFPE since 2006 and current curator of
the Mammal Collection), Luiz A.M. Silva (at the UFPE since
2008), Martin A. Montes (at the UFRPE since 2008), Enrico
A. Feijó et al.
Bernard (at the UFPE since 2009), and Filipe M. Aléssio (at
the UPE since 2014). Maria José Souza (from 1971 at the
UFPE until retiring in 1992) and Neide Santos (at the UFPE
since 2003) have also worked on cytogenetics of rodents and
bats from the PEC, and additional work on parasitology of
PEC mammals has been conducted by Jaqueline B. Oliveira,
working since 1991 at the UFRPE. In addition to terrestrial
mammals, Pernambuco has historically concentrated
research on manatees, starting in the early 1980s with the
creation of the “Projeto Peixe-Boi” and the resulting con-
struction of a rehabilitation center for stranded manatees in
Itamaracá Island, and the creation of the “Centro Nacional
de Conservação e Manejo de Sirênios–Centro Peixe-Boi,”
(later expanded to “Centro Nacional de Pesquisa,
Conservação e Manejo de Mamíferos Aquáticos”–CMA)
during the 1990s. The CMA has been under the direction of
Fabia Luna since 2008, and her work, since she entered the
CMA in 1999, has so far resulted in over 20 articles, in addi-
tion to several chapters, books, and educational guides on
manatees (both from the PEC and other localities).
During the last decade, the main collecting effort focused
on PEC mammals in Pernambuco was the doctoral work of
Asfora (2011), which resulted in over 500 specimens from
several localities within the PEC and are currently housed in
the Mammal Collection of the UFPE. Additional knowledge
on Pernambuco PEC mammals has also come from recent
revisionary and taxonomic studies that have clarified the sta-
tus of several species occurring in the PEC, including defin-
ing name-bearing types or identifying (or rediscovering)
taxa, especially endemic ones. Because several species were
named in the Systema Naturae (Linnaeus 1758) based on
Marcgrave’s illustrations, they remained lacking any physi-
cal type or type locality. Subsequently and consequently,
Thomas (1911) restricted these type localities to
“Pernambuco,” even though there was no information on
whether specimens from the Nassau period came from
Pernambuco, Paraíba or Rio Grande do Norte (Thomas 1911,
p.  124). The absence of physical types from Linnaeus’
descriptions was recently fixed for some particularly impor-
tant taxa, such as the endemics Coendou prehensilis (Leite
et al. 2011) and Sylvilagus brasiliensis (Ruedas et al. 2017).
Along with the rediscovered Sapajus flavius (Oliveira and
Langguth 2006) and recently described Coendou speratus
(Mendes Pontes et al. 2013), these four PEC endemic mam-
mals have now proper name-bearing types and precise type
localities in Pernambuco based on solid taxonomic and
voucher-based work, thus, highlighting both their impor-
tance and the still incipient knowledge existing on several of
these mammals.
Despite its taxonomic importance, and possibly related to
the focus (on ecology, visual surveys, and behavioral studies)
of many of the research projects, Pernambuco remains pro-
portionally under-sampled.
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns
13.5.3 Paraíba
To provide a summarized overview of the main historical and
current studies on mammals in the Atlantic Forest of Paraíba,
we applied a more quantitative approach. We carried out sys-
tematic surveys using two databases (Web of Science and
Scopus) and curricula of key researchers who work or have
worked with mammals at the federal and state universities of
Paraíba (UFPB/UEPB), extracted from the Plataforma
Lattes, a curricula database maintained by the Brazilian
Science and Technology Ministry. Using the keywords
“Paraíba” and “mammals,” the Web of Science search
returned 43 results, of which only six are studies carried out
within the PEC, and the Scopus search returned 54 results, of
which only one occurred in the PEC. A total of nine research-
ers (Alexandre Ramlo Torre Palma, Alfredo Langguth,
Anderson Feijó, Carla Soraia Soares de Castro, Fabiana
Lopes Rocha, Luiz Carlos Serramo Lopes, Patrício Adriano
da Rocha, Pedro Cordeiro-Estrela, and Rômulo Romeu
Nóbrega Alves) had their curriculum analyzed individually.
A total of 93 results were retrieved and distributed among
scientific projects (23; 24.7%), including those related to
undergraduate (9; 9.6%; TCC), master’s (32; 34.4%; MSc
thesis), and doctorate (8; 8.6%; PhD dissertation) projects, as
well as articles (19; 20.4%) and books/book chapters (2;
2%). When projects and articles overlapped, only one prod-
uct was counted to avoid overestimation. The same rationale
was applied when there was an overlap of publications
among the evaluated researchers, as well as between the arti-
cles collected by the databases and those retrieved through
the curriculum. This estimate provides an overall panorama
of the mammal research in the PEC of Paraíba.
The final 96 products (projects, articles, books) were clas-
sified according to research lines, taxonomic scope, and spe-
cies body size and lifestyle. In total, seven research lines were
delimited: ecology (30; 31.3%), inventory (17; 17.7%), sys-
tematics and taxonomy (16; 16.7%), behavioral ecology (9;
9.4%), ecology and conservation (8; 8.3%), ethnobiology (6;
6.3%), ecoepidemiology (5; 5.2%), and data paper (5; 5.2%).
Regarding the taxonomic scope, the community scale was the
most contemplated, totaling 53 studies (55.2%), followed by
species level (38; 39.6%), population level (4; 4.2%) studies,
and, finally, only one (1%) study evaluated mammals in two
scales, population and communities. As for body size and life-
style, there were five studies in which it was not possible to
safely recover the studied group. Thus, of the studies evalu-
ated, medium and large-sized mammals correspond for 38.8%
(33), followed by bats with 31.8% (27), small non-volant
mammals with 22.4% (19), and, finally, aquatic mammals
were the least group studied in the state, only 7.1% (6). The
remaining 7.1% (6) of the studies addressed more than one
group. Therefore, in the PEC of Paraíba, most of the studies
carried out have addressed ­ecological aspects of communities
217
of medium and large-sized mammals and bats. On the other
hand, studies with ethnobiological, eco-epidemiological, and
genetics approaches are scarce, as are those studies focusing
on population and aquatic mammals.
According to the data surveyed, the first records of studies
on mammals in the PEC of Paraíba were carried out in 1982
by Alfredo Langguth through a project aimed at surveying
the mammal fauna in forest remnants. However, one of the
recovered studies (Feijó et al. 2016) still referred to an earlier
project in 1951 aiming to survey the mammal fauna of the
Mamanguape region, before the creation of the Rebio
Guaribas. From then until the 2000s, 11 studies were carried
out addressing ‘ecology.’ ‘behavioral ecology,’ ‘ecology and
conservation,’ and ‘taxonomy and systematics,’ including
four focusing on communities and seven at the species level.
From the early 2000s to 2010, 13 studies were developed on
‘ecology,’ ‘behavioral ecology,’ ‘inventory,’ and ‘taxonomy
and systematics’ and distributed into eight, three, and one
study, on the community, species, and population levels,
respectively. Finally, from 2010 to 2021, 72 studies were car-
ried out covering all research lines here delimited.
It is noteworthy that only seven studies had clear conser-
vation goals; this low number compared to projects on
‘inventory,’ ‘taxonomy and systematics,’ and ‘ecology’ sug-
gests a logical route of studies to explore a given geographic
region, where first it is necessary to inventory the fauna,
define the taxonomic status and phylogenetic relationships
of this fauna, understand the ecology of the species, and then
from these bases, it is possible to drawn relationships
between the fauna and the ecosystem in which they are
inserted. This is corroborated by studies involving ‘ecology
and conservation,’ which were all but one recently devel-
oped, starting in 2012. Therefore, the trajectory of studies
with mammals in the PEC of Paraíba reflects important
advances and contributions to the PEC. It is possible to
observe the need to advance in developing research lines and
start new ones, such as ‘ecology and conservation’ and ‘con-
servation genetics.’ This is because, after about 70  years
since the first studies linked to the deforestation scenario, it
is poignant to develop studies applied to conservation, which
can help and support territorial planning decisions, the cre-
ation of new protected areas, and the choice of priority areas
for forest restoration in the state.
13.5.4 Rio Grande Do Norte
Rio Grande do Norte is one of the least studied states for
mammals in Northeastern Brazil. Recently, a growing effort
has begun to document the mammal fauna of the Caatinga
portion of Rio Grande do Norte, including information on
bats (Vargas-Mena et al. 2018a, b) and medium-large-sized
mammals (Marinho et al. 2018). The Atlantic Forest portion,
218
on the other hand, remains mostly neglected. The few studies
related to terrestrial mammals are incidental species records,
such as Feijó and Nunes (2010) for Myotis nigricans,
Miranda and Superina (2010) for Cyclopes, Marinho et  al.
(2017) for Leopardus pardalis, and Laurentino et al. (2020)
for Lontra longicaudis, and ethnozoological studies (Oliveira
et al. 2020; Sousa et al. 2020). One recent study provides a
list of bats collected at the Nísia Floresta National Forest
(Barros et al. 2017a). The authors recorded 16 species and
the vouchers are housed at UFPE. Later, Vargas-Mena et al.
(2018a) added five bat species to the PEC of Rio Grande do
Norte. Clearly, our knowledge of the PEC mammals of the
Rio Grande do Norte is so scarce that we do not know which
species are still present in the very few forest remnants.
Considering the small size of the remaining forest patches
(see next topic), we can expect higher extinction rates in the
Rio Grande do Norte compared to the other states of the
PEC.
13.6 Conservation Concerns
The main threats faced by mammals in the PEC are similar
to other parts of the Atlantic Forest: habitat loss due to defor-
estation and fragmentation, and hunting. These threats, how-
ever, are more accentuated in the PEC than in other parts of
the biome.
13.6.1 Deforestation Scenario in the PEC
The process of deforestation of the Atlantic Forest began as
early as 10,000 years BP by the pre-Columbian indigenous
populations (Barreto 2013; Solórzano et al. 2021). As sum-
marized by Solórzano et al. (2021), by the time the European
colonizers set foot in Brazil, about 60%–80% of the coastal
Atlantic Forest had already shown some level of alteration
caused by the indigenous occupation, agriculture practices,
hunting pressures, and landscape domestication. After the
Europeans arrived, this process aggravated.
The first and still predominant monoculture in the north-
eastern coast of Brazil is sugarcane. Since the 1540s, when
the first sugarcane mills were installed in Pernambuco
(Schwartz 2005), the demand for land to supply the sugar
and, more recently, ethanol production has led to a massive
replacement of the original forest (Bernard et al. 2011, Zheng
et al. 2021; Figs.13.9 and 13.10a). The Atlantic Forest rem-
nants in the PEC cover only 12.2% of the original area
(Fundação SOS Mata Atlântica and INPE 2021). It is less
than in other regions of Brazil; the Southeast region holds
16% of AF remnants and the South region 20.6%. Within the
PEC, Alagoas is the state facing the highest forest loss (only
11.5% of the original Atlantic Forest remaining), followed
A. Feijó et al.
by Pernambuco (12.2%), Paraíba (12.5%), and Rio Grande
do Norte (15.5%). These alarming numbers, however, do not
properly reflect the severe scenario faced by mammals in the
PEC. They are overestimated, given they include mangroves,
restingas, urban patches, and very small fragments, unsuit-
able to keep a long-term mammal population. The actual sce-
nario, considering only forest fragments with an area size of
at least 3 km2 (300 ha), is that only ~3% is left from the origi-
nal Atlantic Forest in the PEC (Fig. 13.9). This number goes
up to 7.7% in the southeastern and 9.1% in the southern
Brazilian regions. Indeed, the southern and central portions
of the Atlantic Forest have, in general, a higher proportion of
forest remnants and larger fragments in relation to the PEC
(Fig. 13.9).
For conservation purposes, the total area of forest rem-
nants is not the only metric to consider when assessing the
animal population viability. The size of each fragment and
how they are connected are two other key metrics. Based on
the 2019’s Atlas of Atlantic Forest Remnants from Fundação
SOS Mata Atlântica (http://mapas.sosma.org.br/dados/),
there are 8232 fragments of forest (excluding restingas, man-
groves, and urban patches) within the limits of the PEC. Of
these, 97.2% have less than 3  km2 and only 1.9% have an
area larger than 6  km2 (Fig.  13.10). This pattern is similar
across all states. Focusing on forest fragments with an area
of at least 3 km2 (300 ha), we found a relatively higher con-
centration in the east and north of Alagoas (57 fragments;
41%), west and north of Pernambuco (57; 41%), center-north
of Paraíba (19; 13.7%), and the very few remaining in Rio
Grande do Norte (6; 4.3%) are located at the south
(Fig.  13.10b). The third metric, the distance between frag-
ments, provides information on the degree of isolation. We
found that the average distance between the nearest frag-
ments is 3.6 km. However, about a quarter (21.6%) of forest
fragments are isolated at least in a 6 km radius (Fig. 13.10d).
These findings provide important insights into the frag-
mentation scenario in the PEC. First, the great majority of
the forest remnants are too small to support long-term viable
populations of medium-large or forest-dependent mammals.
Even for small mammals, as most populations comprise spe-
cies of this size, they require a minimum of 13 km2 (1300 ha)
for marsupials and 25 km2 (2500 ha) for rodents to ensure
demographic and genetic viability (Brito and Figueiredo
2003; Brito and Fonseca 2006). Second, the distance between
forest remnants is beyond most species’ home range, espe-
cially for small non-volant mammals that account for 24% of
the mammal fauna (Table  13.1). As a result, for forest-­
dependent species or those incapable to cross the altered sur-
rounding matrix, each fragment represents an island. In this
scenario, we may expect that, to survive, species need to ven-
ture out into the sugarcane or other matrices surrounding the
fragments.
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns
Fig. 13.9  Atlantic Forest remnants, excluding restingas and man-
groves, based on the 2019’s Atlas of Atlantic Forest Remnants from
Fundação SOS Mata Atlântica. In panel a, map shows the distribution
of the forest remnants with area size above 3 km2 throughout the biome.
Color coding according to the area size. Barplot shows the overall pro-
portion of forest remnants per 1-degree grid. Note that the southern
13.6.2 The Sugarcane Factor
One of the negative effects of changing land use from natural
forests to agricultural areas is vegetation simplification,
resulting in a homogenization of the landscape (Caudill et al.
2015). Because habitat diversity and structural complexity
are key factors in determining species richness and abun-
dance (MacArthur and MacArthur 1961), crops harbor a
poorer and more depleted fauna compared to adjacent forest
patches (Prevedello and Vieira 2010; Gheler-Costa et  al.
2012; Ferreira et  al. 2018). Studies in crops within the
Atlantic Forest reveal the importance of tree cover and
understory to sustain the local fauna (Umetsu and Pardini
2007), two features that are absent in most annual crops, as
in the monoculture of sugarcane (Gheler-Costa et al. 2012,
Ferreira et al. 2018). Another layer of complexity is related
to the temporal heterogeneity related to the sugarcane annual
cycle, wherein in earlier stages of crop growth the species
diversity is even more reduced (Mamba et al. 2019).
The surrounding matrix also plays an important role in
affecting the community composition within natural habi-
tats. An overwhelming pattern found in studies surveying
219
portion of the biome has a relatively larger proportion of forest rem-
nants and larger fragments. Panel b shows the forest remnants in the
PEC filtered according to the area size. Maps show only forest frag-
ments with areas above 1 km2, 3 km2, 6 km2, and 10 km2, respectively.
Color-coded according to the area size. Percentage values refer to the
number of remnants covering the area of the PEC in each scenario
mammals in the PEC forest remnants is the overall low abun-
dance, predominance of generalists and open-areas special-
ists, and the rarity of forest-dependent species (Asfora and
Pontes 2009; Beltrão 2019). Small mammals are usually
more affected by agricultural systems than medium and
large-sized species due to their smaller home ranges and
restricted dispersal abilities (Burel et al. 1998). However, the
higher exposure in crops makes larger species easier targets
for hunting, while the high densities, short generation time,
and narrow niche of small mammals might allow them to
survive longer within small fragments (Crooks 2002; Gibson
et al. 2013).
Compared to other crops, sugarcane is very hostile to
native small mammal populations because of its low struc-
tural complexity, annual harvesting cycles, fire practices
(still largely applied in the PEC), extensive land use, and
large soil exposure (Gheler-Costa et  al. 2012; Beca et  al.
2017; Beltrão 2019; Rodrigues et al. 2019). These character-
istics result in a very low permeability for mammals across
the sugarcane matrix and greatly restrict their movement
between fragments in the landscape (Rodrigues et al. 2019;
Beltrão 2019). Nevertheless, the impact of crops is uneven
220
Fig. 13.10  Atlantic Forest remnants and sugarcane extension in the
PEC. (a) Distribution of remnants, including forests, restingas, man-
groves, and sugarcane crops. Small grids highlight areas with large
fragments or around state capitals. (b) Maps show only forest fragments
with an area above 3 km2 (300 ha), excluding restingas and mangroves.
Color-coded according to the area size. (c) Proportion of forest rem-
nants per area (in km2) for each state. Values above 3 are not shown
(only 2.8% of the fragments have an area larger than 3 km2). Note that
A. Feijó et al.
the great majority of the fragments have an area smaller than 0.5 km2
(d) Proportion of nearest distances between fragments (in km). Values
above horizontal bars represent the percentage of fragments isolated
within at least 2 km, 4 km, 6 km, and 10 km radius. Calculation based
on fragments above 3 km2. The extension of sugarcane in the PEC was
based on Zheng et al. (2021) for the year 2019 and the forest remnants
on the 2019’s Atlas of Atlantic Forest Remnants from Fundação SOS
Mata Atlântica
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns
across ecological groups, depending on the degree of habitat
specialization. The sugarcane matrix is expected to be a
stronger barrier for forest-dependent mammals than for gen-
eralists or open-area specialists (Buchi and Vuilleumier
2016). However, within the PEC, the few available studies
show an overall limited use of the altered matrix for small
mammals (Rodrigues et al. 2019, Beltrão 2019). Using 2800
pitfall-days for a year to survey the forest-crop border of
three areas of Paraíba, Beltrão (2019) captured only nine
individuals of three generalist species (Didelphis albiventris,
Akodon cursor, and Marmosa demerarae). Additionally,
comparing the native small mammal assemblage within the
sugarcane crop to the adjacent forest fragments, only three,
all open-area specialists (Calomys mattevii, Necromys lasi-
urus, and Monodelphis domestica), out of 16 recorded spe-
cies were considered to be permeable to the sugarcane matrix
(Beltrão 2019). These findings suggest that, even for species
with higher resiliency to habitat alteration, movements
between sugarcane and forest fragments are very limited. In
particular, the maximum distances recorded for the small
mammals between a fragment and the surrounding sugar-
cane matrix ranged between 70 and 450 m (Beltrão 2019).
Another study estimated that forest-specialist species can
travel up to 150 m in a crop inserted in the Atlantic Forest
(Hatfield et  al. 2018). This scenario is alarming when we
cross these data with the observed distance between frag-
ments in the PEC (Fig. 13.10d). It thus seems reasonable to
conclude that most small mammal species cannot completely
cross the sugarcane matrix and move between fragments.
This insular condition generated by agricultural systems is
one of the main factors related to local extinctions (Castro
and Fernandez 2004).
For medium and large-sized species, the situation is not
much less worrisome. For example, previous studies have
failed to register primate species using the sugarcane matrix
across the Atlantic Forest (Dotta and Verdade 2011; Beca
et al. 2017). An intriguing exception refers to observations of
blonde capuchin monkey Sapajus flavius invading the matrix
to feed on sugarcane (Carla Soraia Castro, personal commu-
nication). Beltrão (2019) recognized only three medium-­
sized taxa (Cerdocyon thous, Eira barbara, and Cabassous
tatouay) as permeable to the sugarcane matrix. Although
more field studies are needed, dispersion across large exten-
sions of crops is clearly a limiting factor for most
mammals.
As a consequence of low permeability, the communities
recorded in the sugarcane matrix are poor in mammals with
one or few taxa dominating the landscape (Beltrão 2019,
Rodrigues et  al. 2019), often representing an unbalanced
subset of the adjacent natural community, or in some cases, a
new unrelated assemblage (Caudill et  al. 2015; Beca et  al.
2017). In addition, within crops, the presence of exotic spe-
221
cies Rattus rattus, Rattus norvegicus, and Mus musculus is
not rare. Curiously, highly fragmented landscapes and the
use of the sugarcane matrix can bring some additional advan-
tages for those generalist and opportunistic taxa able to use
the crop. Because of an excess of shelter and food, coupled
with reduced competition within the agricultural landscape,
some rodent species have higher abundances within crops
than in natural habitats (Gheler-Costa et al. 2012). The suc-
cess of some rodents in this matrix type, however, can lead to
a peak in population size and, in turn, to a public health prob-
lem as many of the species are potential reservoir hosts for
pathogens (Figueiredo et al. 2010; Santan Lima et al. 2021).
Atypically high abundance of generalist species might also
exert extra pressure on fragment-limited taxa by increasing
competition. Furthermore, the transformation from forest to
open landscape in the PEC seems to favor open-biome typi-
cal species to spread within the Atlantic Forest, such as
Thylamys karimii and Thrichomys laurentius (Beltrão 2019,
Rodrigues et al. 2019).
In summary, the available evidence reveals the mammal
diversity patterns (low abundance, low diversity per frag-
ment, rare forest-adapted taxa) observed across the PEC
reflect the long and extensive fragmentation history driven
by sugarcane crops and human settlements. Our challenge is
to understand which key factors contribute to the mainte-
nance of the populations, which we believe are multifacto-
rial, including the high resilience capacity of species, the
temporal heterogeneity of the sugarcane crops that might
facilitate movements between remnants, or other unappreci-
ated factors.
13.6.3 Hunting
Although illegal, hunting is still a common practice in the
PEC, even within protected areas (Souza and Alves 2014;
Barbosa et al. 2020). Mammals are among the most targeted
groups, especially those species of medium size, whose pop-
ulations are already depleted due to habitat loss. In the PEC,
at least 27 species are listed as game mammals: the three
armadillos (Euphractus sexcinctus, Dasypus novemcinctus,
Cabassous tatouay), large rodents (Hydrochoerus hydro-
chaeris, Dasyprocta prymnolopha, Dasyprocta iacki,
Cuniculus paca, Coendou prehensilis, Coendou speratus,
Galea spixii, Guerlinguetus brasiliensis), carnivores
(Cerdocyon thous, Eira barbara, Galictis cuja, Herpailurus
yagouaroundi, Leopardus emiliae, Leopardus wiedii, Nasua
nasua, Lontra longicaudis, Procyon cancrivorus), the deer
Mazama gouazoubira, the collared peccary Dicotyles tajacu,
the endemic tapeti Sylvilagus brasiliensis, the anteater
Tamandua tetradactyla, the sloth Bradypus variegatus, the
common marmoset Callithrix jacchus, and the opossum
222 A. Feijó et al.

Didelphis albiventris. These species include most of the Table 13.2  Mammals hunted in Murici protected areas (ESEC and
APA), Alagoas state, between January 2017 and September 2021.
medium-large fauna present in the PEC. They are hunted
Numbers based on apprehended animals/items by the Instituto Chico
mainly for their meat, but also for folk medicinal purposes Mendes de Conservação da Biodiversidade (ICMBio) agents
(mostly armadillos), pets (marmosets and sloths), and as a
Species Items apprehended Quantity
control hunting (mainly carnivores and anteaters) (Souza and Dasypus novemcinctus Carcass; tail 63
Alves 2014). Coendou speratus Carcass; quills 18
As a clear example of the negative hunting impacts and Cuniculus paca Carcass; hairs 11
associated practices in the PEC, we explored unpublished Dasyprocta spp. Carcass; hairs 10
data on hunting practices compiled between 2017 and 2021 Nasua nasua Carcass; penis 9
from the ESEC Murici and its surroundings. ESEC Murici Coendou prehensilis Carcass; quills 8
was created in 2001 and has an area of 6131 ha. Adjacent to Dycoteles tajacu Skull; meat 6
the ESEC, there is the Área de Proteção Ambiental (APA) Tamandua tetradactyla Carcass 5
Euphractus sexcinctus Carcass 3
Murici, a government-protected area with 133,000 ha cover-
Hydrochoerus hydrochaeris Carcass 1
ing 10 municipalities in northern Alagoas. The Murici’s pro-
Galea spixii Carcass 1
tected areas harbor together a rich fauna, including Sylvilagus brasiliensis Carcass 1
endangered and relict populations; among the recorded Leopardus emiliae Skin 1
mammals are A. belzebul, C. didactylus, C. paca, C. spera- Bradypus variegatus Claws 1
tus, C. prehensilis, L. wiedii, L. emiliae, L. pardalis, H. Eira barbara Carcass 1
yaguarondi, L. longicaudis, M. gouazoubira, and D. tajacu. Total 139
Some of the species are locally extinct throughout most of
the PEC, such as the gray brocket deer M. gouazoubira and
the collared peccary D. tajacu.
Data gathered by one of us (MAF) shows that at least 139 13.6.4 Extinction Scenario
specimens from 15 mammal species were hunted in Murici
during the last 4 years alone (Table 13.2). Nearly half of the Despite the high levels of deforestation and hunting prac-
hunted animals were nine-banded armadillos, but, alarm- tices, the confirmed extinction rate in the PEC is surprisingly
ingly, the PEC endemics C. speratus, C. prehensilis, and D. low. This led us to postulate two possible complementary
iacki are also heavily hunted in Murici. These impressive scenarios. One, there are unrated extinctions. Because mam-
numbers refer only to those individuals apprehended by mal surveys in the PEC systematically began in the last
ICMBio agents and are thus underestimated. 70 years, we do not have a temporal glimpse of the mammal
Contrary to the still widespread belief, hunting in the PEC assemblage in a more pristine condition. The animals
is not related to subsistence needs and serves more as a rec- reported by Marcgrave (1648) are mostly confined to
reational activity. According to ICMBio agents, in Murici, medium-large mammals and, apart from the five missing
hunting increases on weekends and holidays, and hunters large species, the remaining fauna is still present in the PEC,
often use firearms and vehicles, expending high-cost although much less abundant. After Marcgrave, the docu-
resources. Depending on the target species and season, hunt- mentation of the original PEC fauna is scant as most
ers use distinct strategies. For armadillos, specific home- nineteenth-­century naturalists did not explore this region
made traps called tatuzeiras (Fig. 13.11c), cylindrical wire (Hershkovitz 1987; Feijó and Langguth 2013). In the 1950s,
cages with an inner trigger, are set at the entrance of the bur- Vieira (1953) reported a rich and still existing fauna from
rows. Trained domestic dogs are also often used, which can Alagoas. If a strictly forest-dependent rodent, marsupial, or
bring an additional problem to the native fauna by spreading even a bat ever occurred in the PEC but did not cope with
pathogens. These techniques are commonly used in other habitat loss and disappeared before 1950, we do not know.
states of the PEC (Barbosa et al. 2020) and across the coun- The second scenario that might explain the low-­
try (Alves et al. 2016). In the last 4 years, only within Murici, documented extinction is a higher resiliency to habitat altera-
186 firearms and 173 tatuzeiras were retrieved by ICMBio tion than previously thought. As we addressed before, for
agents (Fig. 13.11). several species of small mammals, the large extension of
The hunting scenario described in Murici is just an iso- sugarcane crops seems to act as an impermeable barrier
lated example of common practices in the PEC. The removal between distant isolated forest fragments. Under that notion,
of medium-large mammals from the remnant forest frag- each fragment represents an island, and the local diversity
ments due to hunting is a big challenge for conservation. The will be balanced between extinction and colonization rates.
presence of environmental agents is fundamental to control- Taking advantage of well-established island biogeography
ling and preventing hunting and should be enhanced across predictions, if dispersion is limited, local extinctions are
protected areas. likely a common outcome in small fragments. Studies show
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns
Fig. 13.11  Hunting practices in the PEC. (a) Carcasses of paca, arma-
dillo, coati, and aguti apprehended by ICMBio agents. (b) Firearms
retrieved from hunters in Murici, Alagoas. (c) Examples of armadillo-­
that most of the forest fragments in the PEC have lost a large
part of the original fauna, keeping only generalists or open-­
habitat taxa. Magalhães (2015), sampling nine urban forest
patches in João Pessoa, found two to eight species of small
mammals in fragments with 22 to 515 ha. The ten sampled
species across all fragments are generalist, and some are
more typical of open than forested biomes. This observed
richness represents five species less than those reported by
Percequillo et al. (2008) for the same region. A very similar
pattern was reported by Asfora and Pontes (2009). They
sampled 12 fragments (area size ranging from 10 to 3400 ha)
in Pernambuco and Alagoas and the local diversity varied
from zero (in fragments with 10 and 200 ha) to nine species
of small non-volant mammals. Notably, Hylaeamys oniscus,
a strict forest species, was recorded only in the largest frag-
ment (Asfora and Pontes 2009). In addition to the much-­
reduced assemblage, the abundance recorded in both studies
was very low, with capture rates lower than 3%.
223
traps tatuzeiras. (d) Hunting tools, traps, and bushmeat of coati, pec-
cary, and armadillo. (Photos by Marco Antônio Freitas)
These findings point to widespread local extinctions and
reduced recolonizations in the PEC and reveal a limited
carrying capacity across fragments. Surprisingly, some-
how, arboreal and forest-dependent species (e.g.,
Rhipidomys and Oecomys) have found ways to avoid
extinction (so far) and can still be found in fragments as
small as 50 ha (Asfora and Pontes 2009). Such resiliency
might suggest an unappreciated ability to disperse between
fragments. However, if this trend of local extinction offset-
ting colonization continues, the next generation of mam-
malogists may find only non-­forested taxa within Atlantic
Forest remnants, and more species will be added to the PEC
extinction list. Losing a nonrandom assemblage of the
fauna will result not only in diversity loss but also in func-
tional loss, disrupting the ecosystem balance, and ulti-
mately, increasing the risk of extinction cascades (Sanders
et al. 2018). To revert this trend and allow populations to
better move across fragments, it is critical to identify which
224
areas are acting as primary sources of biodiversity and
understand how animals are moving across the altered
matrix. In this sense, the study of Beltrão (2019) is a pio-
neer and sets a model for future studies. Surveys should
target not just the fragments but also the surrounding areas.
Knowing what, when, and how the animals are using the
deforested landscape will provide crucial information to
guide reforestation and connectivity programs.
13.6.5 Some Words of Hope
Having detailed the perils associated with fragmentation,
habitat loss, hunting, and prominent extinctions in the PEC,
we want to end this Conservation section by showing that
there are still ways to coexist with nature. As stated by
Swaisgood and Sheppard (2010), “If conservation is to pre-
vail and endure, we will need to marshal our forces with
equal doses of realism and hope.” Therefore, some positive
perspectives are worth mentioning.
Back in the 1950s, Vieira (1953) noted that four species
found in Alagoas were unknown to the northeastern coast of
Brazil. Seventy years later, we continue to add (and describe)
species of mammals to the PEC. The discoveries of Coendou
speratus and Ametrida centurio bring an important message
that the 12.2% of Atlantic Forest remnants still shelter great
surprises for mammalogists.
According to SoS Mata Atlântica, the deforestation rate
has been mainly steady or decreasing in the states of the PEC
in the last 5 years (Fundação SOS Mata Atlântica and INPE
2021). Between 2019 and 2020, Pernambuco reduced the
deforestation area by 52% compared to 2018–2019. Alagoas
and Rio Grande do Norte lost only 10  ha in this period.
Recently, Dias et al. (2022) showed that greening (increase
in vegetation biomass) has predominated over browning
(decrease in vegetation biomass) in the PEC in the last
35  years, suggesting that improved forest condition of the
PEC fragments is likely associated with reduced logging
activities. Moreover, the number of protected areas (PAs)
under private ownership (RPPN) is much higher than the
ones under government management (although governmen-
tal PAs are usually larger), suggesting an increasing aware-
ness of the private sector on the importance of protecting
biodiversity. Together, government and private PAs play a
complementary role in conserving and reducing the gap
between fragments. In particular, RPPNs help increase land-
scape connectivity to facilitate dispersion among forest frag-
ments (Mesquita and Vieira 2004; Oliveira et  al. 2010).
Currently, there are 69 RPPNs in the PEC; Alagoas has by
far the highest number of RPPNs (47, 68%) followed by
Pernambuco (17; 25%); in contrast, there are only two and
three RPPNs in the Atlantic Forest portion of the Paraíba and
Rio Grande do Norte, respectively (Carvalho et al. 2021).
A. Feijó et al.
To stimulate the creation of more private protected areas,
we need to educate landowners that conserving native forest
patches (and reforesting) is beneficial to their crop produc-
tion. In addition to helping preserve biodiversity, numerous
studies have shown the importance of forest fragments to
increase productivity in crops, acting as pollinator reservoirs
and increasing soil capacity for storing water (e.g., Sousa
et al. 2019; Halinski et al. 2020). For example, Halinski et al.
(2020) show that canola seed production in southern Brazil
is higher closer to native forest fragments. They estimate that
without forest remnants, the total income loss would be ca.
US$ 528 (R$ 2818) per hectare. Examining the primary pro-
ductivity of sugarcane crops in Paraíba, Sousa et al. (2019)
found an increase in crop productivity in forest-dominated
areas. These two studies exemplify the positive relationship
between native vegetation and crop productivity and ulti-
mately farmers’ profits.
Many ecosystem benefits offered by fauna and flora,
especially in intensely fragmented regions, remain unex-
plored in Brazil. We encourage future projects to explore this
topic and quantify and monetize ecosystem services in a way
to emphasize their importance for the private sector and gov-
ernments. In addition, actions for forest conservation and
restoration associated with better crop management (e.g.,
agricultural intensification instead of the advance of mono-
culture on new natural habitat areas) are ways to improve the
conservation value of sugarcane in the PEC.
13.7 Conclusion
The PEC comprises only 3.5% of the original extension of
the Atlantic Forest biome but encompasses about 36% of its
mammalian fauna. Despite its reduced area, six species are
endemic to this region, although this number is likely under-
estimated. In recent years, due to the use of complementary
survey methods, numerous taxa have been added to the PEC
mammal list, including species previously restricted to the
Amazon or open biomes. These records reinforce the hetero-
geneous composition of this fauna, with a strong influence of
adjacent biomes and an important historical link between
past tropical forests, connecting the Amazon and coastal
Atlantic forests. This unique biogeographical aspect led to
the recognition of the PEC as an important endemism center
for several groups, including bats and small rodents.
Surprisingly, new species of forest-dependent mammals are
still being described even in face of reduced forest remnants
and elevated hunting pressure. We further predict a still over-
looked mammalian diversity. Our analyses of sampling
efforts revealed that 56% of the PEC has not yet been sur-
veyed, and about 60% of the effort was limited to only ten
sites. Large parts of Alagoas, Pernambuco, and Rio Grande
do Norte remain poorly surveyed. In this chapter, we pointed
13  Mammals of the Pernambuco Endemism Center: Diversity, Biogeography, Research Gaps, and Conservation Concerns
out promising study areas for mammals considering the
availability of forest remnants and protected areas.
Our review of the historical and ongoing projects shows
that studies with clear conservation goals, population genet-
ics, and ecological studies assessing the effects of crops on
mammal populations are rare. Understanding how species
use forest remnants and move across the surrounding matrix
is key to assessing extinction vulnerability. The actual frag-
mentation scenario, in which most remnants are too small to
support long-term viable populations and those with an area
larger than 3 km2 are isolated, likely forces animals to ven-
ture out into the altered surroundings. The low level of
extinction is surprising and may indicate high resilience
among forest dependents or that local extinction is
underrated.
We hope this chapter motivates mammalogists to fill the
sampling and thematic gaps identified here.
Acknowledgments  We are deeply grateful to Alexandra M. R. Bezerra
and Ana Paula Carmignotto for their comments on an earlier version of
the manuscript. Special thanks to Paulo Henrique Marinho for kindly
providing information on mammals from Rio Grande do Norte and Ana
Carolina Loss for information on Phyllomys. Hugo Fernandes-Ferreira
and Bruna Bezerra kindly provided photographs of the Dasyprocta
iacki and the Sapajus flavius group, respectively. Paulo Asfora and
Thais Lira greatly helped in compiling a list of mammals from
Pernambuco that served as a basis for the one used here. We thank the
Japungu Agroindustrial and Reserva Biológica Guaribas for all the sup-
port offered during the fieldwork of MGB.
AF is supported by the Second Tibetan Plateau Scientific Expedition
and Research Program (2019QZKK0402 and 2019QZKK0501), the
Chinese Academy of Sciences President’s International Fellowship
Initiative (2021PB0021). MGB is supported by São Paulo Research
Foundation (FAPESP; 2020/02570-2); Rufford Foundation—Small
grant (20950-1), Coordenação de Aperfeiçoamento de Pessoal de Nível
Superior—Brasil (CAPES) —Finance Code 001, and Idea Wild. PAR is
supported by the postdoctoral fellowships (88882.317933/2019-01).
DA is funded by grants from FACEPE, CNPq, CAPES, and UFPE.
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 Fisheries and Uses of Coastal Aquatic
Fauna in the Northernmost Brazilian
Atlantic Forest
Rômulo Romeu Nóbrega Alves, Márcia Freire Pinto,
Anna Karolina Martins Borges,
and Tacyana Pereira Ribeiro Oliveira
Abstract
Coastal ecosystems provide habitats and resources to a
rich aquatic fauna explored by local people for subsis-
tence and economic purposes. In this chapter, we high-
light the primary fishing resources captured in areas of the
northernmost Atlantic Forest coastal remnants in Brazil.
We evidence the close relationship between local inhabit-
ants and aquatic animals and reveal that the use of fishing
resources is widely practiced among human populations
living in the vicinity of estuaries and mangroves. Fish
comprise the major group exploited, primarily as food
resources; however, mollusks and crustaceans are also
commonly captured. The species recorded can provide
several raw materials, which can be harnessed and used
for one or several purposes (i.e., as curios, medicinal and
magical-religious purposes, and tourism attractions).
R. R. N. Alves (*)
Departamento de Biologia, Universidade Estadual da Paraíba,
Campina Grande, PB, Brazil
Programa de Pós-Graduação em Etnobiologia e Conservação da
Natureza, Universidade Federal Rural de Pernambuco, Recife, PE,
Brazil
M. F. Pinto
Departamento de Biologia, Universidade Estadual do Ceará,
Limoeiro do Norte, CE, Brazil
e-mail: marcia.freire@uece.br
A. K. M. Borges
Programa de Pós-Graduação em Etnobiologia e Conservação da
Natureza, Universidade Federal Rural de Pernambuco, Recife, PE,
Brazil
e-mail: anna.kmborges@ufrpe.br
T. P. R. Oliveira
Programa de Pós-Graduação em Etnobiologia e Conservação da
Natureza, Universidade Federal Rural de Pernambuco, Recife, PE,
Brazil
Centro de Ciências Biológicas e Sociais Aplicadas, Universidade
Estadual da Paraíba, João Pessoa, PB, Brazil
e-mail: tacyana@servidor.uepb.edu.br
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
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_14
14
Several aquatic species exploited in the region figure in
the official list of Brazilian threatened species, evidencing
the importance of understanding the interface between
resource exploitation and biodiversity conservation.
Keywords
Animal conservation · Crustaceans · Ethnobiology ·
Ethnozoology · Fishes
14.1 Introduction
The Atlantic Forest stands out among Brazilian ecosystems
for the highest levels of diversity ever found in tropical for-
ests and for a high level of endemism (Giulietti and Forero
1990; McNeely et al. 1990). However, the exploitation pro-
cess of natural resources, together with the industrial and
urban growth of the country, which intensified in the twenti-
eth century, caused significant impacts on this biome, trans-
forming it into a series of forest fragments, many of which
are currently sparse and unconnected. According to the 2020
SOS Mata Atlântica Foundation annual report, there is only
12.4% of the biome’s original coverage left in the Brazilian
territory, with an increasing deforestation rate of 27.2% in
the years 2018 to 2019, representing the highest rate since
2016, as shown in the Atlas of Atlantic Forest Remnants of
2018–2019 (Fundação SOS Mata Atlântica 2020).
The Atlantic Forest is associated with a series of coastal
and marine ecosystems. The mangrove ecosystem stands out
among these as a highly productive environment (Bouillon
et al. 2008), which directly and indirectly benefits adjacent
ecosystems, as well as the different human groups that use
them. Mangrove forests are important environments for
maintaining different types of organisms that inhabit these
places or that use them during some period of their life cycle,
whether for food, reproduction, or to avoid predators (Alves
and Nishida 2002; Nordi et al. 2009). Many animal species
229
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in mangrove areas are permanent residents, developing their
life cycle exclusively in estuarine areas and frequently enter-
ing the mangroves (Vannucci 2001). However, others seek
these areas for developing the first stages of their life cycle,
which is why mangroves are considered natural breeding
grounds for a large number of marine or freshwater species
(Sandilyan and Kathiresan 2012; Walters et al. 2008).
Mangroves are an essential source of various resources
such as wood, medicines, dyes, fish, crustaceans, and mol-
lusks (Walters et al. 2008). Therefore, it is not surprising that
many human communities living around these areas have a
historical and traditional dependence on these ecosystems
for their livelihoods. Much of the Brazilian artisanal fisheries
are based on estuarine species that spend a significant part of
their life cycle in the mangroves, including fish and inverte-
brates, which comprise the main fishing resources exploited
by people residing in the vicinity of these areas. The exploi-
tation of mangrove resources in the Brazilian Northeast is of
great social importance in coastal areas close to mangroves
and the Atlantic Forest, generating several direct and indirect
jobs. Many social groups in these areas, such as traditional
communities of artisanal fishermen, farmers, extractivists,
and quilombolas1, establish direct relationships with the
environment, not only utilitarian relationships of natural
resources but also symbolic, spiritual, and magical, which
are extremely important for the cultural and social constitu-
tion of these groups.
The Brazilian Northeast has a population of 57,071,654
inhabitants, of which 32% live in the coastal zone (MCTIC
2021). These populations exploit coastal environments and
exert pressure on resources, shaping the social and cultural
relations, whose economic implications directly affect
nature. Therefore, the need to understand how social groups
relate to coastal environments is evident in order to under-
stand and historically value cultural aspects and to enable
reflections and proposals for actions regarding the mitigation
or compensation of the negative impacts arising from these
relationships. A better understanding of the processes and
actors involved in the use of resources in the estuary-­
mangrove complex can generate conservation benefits for
both exploited species and the populations that exploit them.
In this perspective, several studies have focused on the rela-
tionships between human beings and these environments,
which harbor high population density in coastal areas. These
relationships imply holistic issues, which involve several
research areas. In the case of human interactions with ani-
mals, we highlight the utilitarian perspective Ethnozoology
can apply, seeking to understand how humans exploit animal
resources to provide food and for various other purposes
such as ornamental, medicinal, and magical-religious (Alves
et al. 2018).
R. R. N. Alves et al.
Ethnozoological research has been carried out in several
coastal areas under the influence of the Atlantic Forest, north
of the São Francisco River, mainly in the states of Paraíba,
Pernambuco, and Alagoas (Fig.  14.1, Chap. 2), providing
information on the exploitation of fauna and its uses by local
populations. In this chapter, we highlight the main fishing
resources captured in the region and the multiplicity of uses
applied to them and their consequent social and conserva-
tionist implications.
14.2 Aquatic Fauna Used in Coastal
Regions
Information from ethnozoological studies developed on the
coast of the States of Paraíba, Pernambuco, and Alagoas
show that the use of fishing resources is widely practiced
among human populations living in the vicinity of estuaries
and mangroves (Alves et al. 2005; Alves and Nishida 2002,
2003; Mourão and Nordi 2006; Nishida et  al. 2006a, b, c;
Nordi et  al. 2009; Pinto et  al. 2015; Rangely et  al. 2018;
Rocha et al. 2008). Several taxonomic groups are used, pri-
marily fish, but mollusks and crustaceans are usually cap-
tured to obtain meat for food (Pinto et al. 2018). Moreover,
we can also highlight the past use of mammals and aquatic
reptiles, whose exploitation has been reduced over time due
to bans on capture and trade in the country, although these
activities can still occur sporadically and illegally in some
locations.
Several other products, besides meat, are obtained from
the exploited animals and implemented for various uses,
including for medicinal and magical-religious purposes and
as curiosities or aquarium organisms (Alves and Rosa 2006;
Mota et al. 2020; Pinto et al. 2015; Rocha et al. 2008; Rosa
et al. 2005, 2011). Although the whole animal can be used, it
is more common to use body parts or by-products from dead
and more rarely live specimens (Alves and Rosa 2007b).
Thus, the same species can provide several raw materials
which can be harnessed and used for one or several purposes.
This situation represents a way of optimizing the use of ani-
mals, although the primary motivation for capture is usually
directed to a specific use. As an example, various by-­products
of fish, invertebrates, and mammals have magical-religious
uses, being used in offerings (which may or may not involve
sacrifices) and as magical amulets (Alves et  al. 2012; Leo
Neto and Alves 2010; Leo Neto et al. 2009, 2011; Rosa et al.
2011). The multiplicity of uses can be an additional pressure
factor on the species, and therefore, their impacts must be
correctly evaluated and contextualized. In the next sessions,
the taxonomic groups captured and their respective uses in
the region are discussed.
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest 231

Fig. 14.1  Fish caught by

fishers from Tamandaré
beach, Pernambuco, Northeast
coast of Brazil. (Photograph:
Marcia Freire Pinto)

14.3 Fish and Other Vertebrates the bottom of reef or rocky environments and are considered
as “slow moving  species”, such as groupers (Epinephelus
Fish constitute the most diverse group of the aquatic fauna spp.), sea basses (Mycteroperca spp.), and snappers
exploited in the region. Research indicates that at least 263 (Lutijanus spp.). However, in some locations, “fast-­
fish species are captured and used (Table 14.1), belonging to swimming fish” that live close to the surface (water vein),
78 families, of which Carangidae (9%; n = 23), Sciaenidae such as the cero (Scomberomorus regalis (Bloch, 1793)) and
(7%; n  =  19), and Scombridae (6%; n  =  16) are the most the mackerel (Scomberomorus cavalla (Cuvier, 1829)), are
representative. Most species are fished for commercial also considered high-priced. Low-price fish are those whose
­purposes (86%; n = 227) and/or for local consumption (80%; meat is not very tasty and are usually found in muddy bot-
n = 212), characterizing fishing as an economic activity that toms and have a more varied diet, such as catfish (e.g.,
generates income and livelihood for fishermen’s families. Genidens genidens (Cuvier, 1829)). Thus, the highest quality
Although fish are mainly used for food, we also found fish have the greatest commercial value and, therefore, are
records of other uses, such as for medicinal purposes (4%; under greater fishing pressure, as fishermen know where to
n  =  10), to produce handicrafts (2%; n  =  3), for magical-­ find and how to catch them.
religious purposes (1%; n  =  2), for ornamental purposes Stingrays and sharks are among the cartilaginous fish
(1%; n = 2), and as baits (Pinto et al. 2015). At least 196 spe- caught in estuarine regions and are mainly used for food con-
cies are sources of products that serve more than one use. In sumption, being marketed locally. As some species of these
addition, fish are closely linked to the fishing culture, to the fish use estuaries to reproduce and as nurseries, they end up
perception and knowledge of fishers about these animals and being vulnerable to overfishing. Stingrays are widely fished,
the different factors that affect their behavior and distribu- traded, and consumed for food, and are also used for medici-
tion. Fish are present in the paintings, music, strings, draw- nal purposes. Sharks caught in estuarine areas are mostly
ings, and imagery of fishing communities. young and are popularly called “cação,” also being mainly
Bony fish represent the largest amount of fish captured traded for food purposes. Adult sharks are mostly captured at
(Fig. 14.1). Among the most commercialized for food pur- sea; however, the meat is not usually commercialized but
poses are the white swordfish (Triakidae), snooks shared among fishers’ family members and friends in the
(Centropomidae), grunts (Haemulidae), tarpons community. Sharks of the Carcharhinus genus stand out
(Megalopidae), mullets (Mugilidae), sardines (Engraulidae among the most fished species. One of the major important
and Clupeidae), mojarras (Gerreidae), and weakfish conservation issues regarding shark fishing refers to the
(Sciaenidae). The meat flavor and value are usually related to commercialization of fins mostly for a traditional Chinese
the habitat and behavior of the animals by fishermen (Pinto dish (shark fins soup) consumed in Asian countries, espe-
et al. 2017). For example, the highest quality fish (which are cially in China (Rose 1996; Barreto et al. 2017). Sharks are
considered the tastiest and most expensive) mostly live on fished, but only the fins of these animals are removed, which
Table 14.1  Fish species and their uses in areas of the northernmost Atlantic Forest coastal remnants in Brazil
232

Common name Local name (Portuguese) IUCN MMA State Use

Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Acanthuridae
Acanthurus bahianus Barber Caraúna LC X X X X
Castelnau, 1855 surgeonfish
Acanthurus chirurgus Doctorfish Caraúna-preta LC X X X X
(Bloch, 1787)
Acanthurus coeruleus Blue tang Caraúna-azul LC X X X
Bloch & Schneider, 1801 surgeonfish
Achiridae
Achirus lineatus Lined sole Sóia-redonda LC X
(Linnaeus, 1758)
Albulidae
Albula nemoptera Threadfin Ubarana-boca-de-rato DD X X X
(Fowler, 1911) bonefish
Albula vulpes (Linnaeus, Bonefish Ubarana NT X X X X
1758)
Antennariidae
Antennarius Longlure frogfish Aniquim-mole LC X
multiocellatus
(Valenciennes, 1837)
Ariidae
Genidens genidens Guri sea catfish Bagre-ariaçu; Bagre-giriaçu; giruaçu; LC X X X X
(Cuvier, 1829) juruaçu; Bagre-branco;
Bagre-miguel-raio
Bagre bagre (Linnaeus, Coco sea catfish Bagre-bardecha; Bagre-bandeira; LC X X X
1766) Bagre-fita
Aspistor quadriscutis Bressou sea Bagre-amarelo; Bagre-mestre-mané LC X X
(Valenciennes, 1840) catfish
Sciades proops Crucifix sea Bagre-corre-costa NE X X X
(Valenciennes, 1840) catfish
Cathorops spixii (Agassiz, Madamango sea Bagre-bandim; Bagre-manguim NE X X X X
1829) catfish
Sciades herzbergii (Bloch, Pemecou sea Bagre-barba-roxa LC X X X
1794) catfish
Balistidae
Balistes vetula Linnaeus, Queen triggerfish Cangulo-amarelo; Cangulo-­ NT X X X X
1758 verdadeiro; cangulo-do-papo-amarelo;
Cangulo-papo-louro; Cangulo-azul
Balistes capriscus Grey triggerfish Cangulo-fernando; Cangulo-fernandi; VU X X X
Gmelin, 1788 cangulo-branco; Cangulo-papo-­
branco; Cangulo-patriota
R. R. N. Alves et al.
 Common name Local name (Portuguese) IUCN MMA State Use
Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Canthidermis sufflamen Ocean triggerfish Cangulo-mané-do-arroio; Cangulo-­ LC X X X
(Mitchill, 1815) mané-­de-arroz; Cangulo-preto;
Cangulo-guiné
Melichthys niger (Bloch, Black triggerfish Cangulo-mané-do-arroio; Cangulo-­ LC X X X
1786) mané-­de-arroz; Cangulo-preto;
Cangulo-guiné
Batrachoididae
Amphichthys Bocon toadfish Pacamon; Pocomão LC X X X
cryptocentrus
(Valenciennes, 1837)
Batrachoides Pacuma toadfish Pacamon; Pocomão LC X X X
surinamensis (Bloch &
Schneider, 1801)
Thalassophryne nattereri Trinidad Tob Pacamon; Pocomão LC X X X
Steindachner, 1876
Belonidae
Tylosurus acus (Lacepède, Agujon needlefish Agulhão-branco LC X X X
1803)
Strongylura timucu Timucu Agulhão-espinha-verde LC X X X
(Walbaum, 1792)
Bothidae
Bothus spp. Plate fish Sóia X
Carangidae
Alectis ciliaris (Bloch, African pompano Galo-de-penacho; Galo-do-alto; LC X X X X
1787) Galo-de-fita
Caranx sp. Capitão-garajuba X X X
Caranx bartholomaei Yellow jack Xaréu-amarelo LC x x X X X
Cuvier, 1833
Caranx crysos (Mitchill, Blue runner Guarassuma; garassuma; Chincharro; LC X X X X
1815) Xerelete
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest

Caranx hippos (Linnaeus, Crevalle jack Xaréu-branco LC X X X X

1766)
Caranx latus Agassiz, Horse-eye jack Garacimbora; Aracimbora; LC X X X X X
1831 Garachimbora; Guachimbora; Xáreu
Caranx ruber (Bloch, Bar jack Xaréu preto; Garajuba-branca LC X X X
1793)
Chloroscombrus Atlantic bumper Pelombeta; Pilombeta; Palombeta LC X X X X
chrysurus (Linnaeus,
1766)
Decapterus macarellus Mackerel scad Garapau LC X X X
(Cuvier, 1833)
(continued)
233
Table 14.1 (continued)
234

Common name Local name (Portuguese) IUCN MMA State Use

Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Elagatis bipinnulata Rainbow runner Arabaiana; Gurubatã; Guiubatá; LC X X X
(Quoy & Gaimard, 1825) Peixe-rei
Oligoplites palometa Maracaibo Tibiro; Timbiro LC X X X
(Cuvier, 1832) leatherjacket
Oligoplites saliens Castin Tibiro; Timbiro LC X X X
(Bloch, 1793) leatherjacket
Oligoplites saurus (Bloch Leatherjacket Tibiro; Timbiro LC X X X
& Schneider, 1801)
Selar crumenophthalmus Bigeye scad Garapau LC X X
(Bloch, 1793)
Selene setapinnis Atlantic moonfish Galo LC X X
(Mitchill, 1815)
Selene vomer (Linnaeus, Lookdown Galo-de-penacho; Galo-do-alto; LC X X X X
1758) Galo-de-fita
Seriola dumerili (Risso, Greater amberjack Olhete; Arabaiana-cachorro LC X X X X
1810)
Seriola fasciata (Bloch, Lesser amberjack Arabaiana-roliça; Arabaiana-branca LC X X X
1793)
Seriola lalandi Yellowtail Arabaiana-amarela; Arabaiana-preta LC X X X
Valenciennes, 1833 amberjack
Seriola rivoliana Longfin yellowtail Arabaiana-chata LC X X X
Valenciennes, 1833
Trachinotus spp. Floripa pompano Pampo; Piraroba X X X
Trachinotus carolinus Florida pompano Pampo-cabeça-mole LC X X
(Linnaeus, 1766)
Trachinotus goodei Great pompano Pampo-garabebel LC X X
Jordan & Evermann, 1896

Carcharhinidae
Carcharhinus spp. Cação-lombo-preto X
Carcharhinus spp. Cação-toalha X
Carcharhinus acronotus Blacknose shark Cação flamengo EM X X X
(Poey, 1861)
Carcharhinus falciformis Silky shark Cação-aba-preta; Cação-sicurí; VU X X X
(Müller & Henle, 1839) Galha-preta; Tubarão-galha-preta;
Tubarão-aba-preta; Cação-flamengo
Carcharhinus limbatus Blacktip shark Cação-aba-preta; Cação-sicurí; VU X X X X
(Müller & Henle, 1839) Galha-preta; Tubarão-galha-preta;
Tubarão-aba-preta; Cação-flamengo
Carcharhinus leucas Bull shark Cação-cabeça-chata; VU X X X X
(Müller & Henle, 1839) Tubarão-cabeça-chata
R. R. N. Alves et al.
 Common name Local name (Portuguese) IUCN MMA State Use
Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Galeocerdo cuvier (Péron Tiger shark Cação-pintadinho; Cação-pintado; NT X X X X
& Lesueur, 1822) Jaguara; Cação-tigre; Tubarão-tigre
Prionace glauca Blue shark Cação-azul; Cação-barriga-mole NT X X X
(Linnaeus, 1758)
Rhizoprionodon lalandii Brazilian Cação-verga-de-ouro VU X X X X X
(Valenciennes, 1839) sharpnose shark
Rhizoprionodon porosus Caribeean Cação-verga-de-ouro VU X X X X
(Poey, 1861) sharpnose Shark
Centropomidae
Centropomus pectinatus Tarpon snook Camurim-branco; Camurim-impim; LC X X X
Poey, 1860 Camurim-tábua
Centropomus undecimalis Common snook Camurim-açu; Camurim-corcundo; LC X X X X
(Bloch, 1792) Camurim-preto
Centropomus parallelus Fat snook Camurim NE X X
Poey, 1860
Centropomus spp. Camurim X X
Chaetodontidae
Chaetodon spp. Spotfin Parum-jandáia; Peixe-prato; pintado X X X
butterflyfish
Clupeidae
Opisthonema oglinum Atlantic thread Sardinha; Sardinha-azul; LC X X X X X
(Lesueur, 1818) herring Sardinha-de-gaia
Harengula jaguana Poey, Scaled herring Sardinha-cascuda; LC X X X
1865 Sardinha-casca-grossa
Sardinella aurita Round sardinella Sardinha-maromba LC X X X
Valenciennes, 1847
Sardinella brasiliensis Brazilian Sardinha-roliça DD X X X X
(Steindachner, 1879) sardinella
Coryphaenidae
Coryphaena equiselis Pompano Dourado; Dourado-azedinho LC X X X
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest

Linnaeus, 1758 dolphinfish

Coryphaena hippurus Common Dourado; Dourado-cabeça-de-bolina LC X X X
Linnaeus, 1758 dolphinfish
Cyclopsettidae
Syacium micrurum Channel flounder Soia LC
Ranzani, 1840
Cynoglossidae
Symphurus spp. Spottedfin Sóia-linguado; Linguado NE X X X
tonguefish
Dasyatidae
Dasyatis guttata (Bloch & Longnose stingray Arraia-branca; Arraia-couro-de-lixa NT X X X X X X
Schneider, 1801)
Hypanus americanus Southern stingray Arraia-mijona DD X X X X
(Hildebrand & Schroeder,
1928)
235

(continued)
Table 14.1 (continued)
236

Common name Local name (Portuguese) IUCN MMA State Use

Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Dasyatis marianae Brazilian Raia olhão EN X X
(Gomes, Rosa & Gadig, large-eyed
2000) stingray
Dasyatis sp. Arraia-de-pedra; Arraia-de-croa X X
Diodontidae
Chilomycterus antillarum Web burrfish Baiacu-espinho LC X X
Jordan & Rutter, 1897
Chilomycterus spinosus Baiacu-espinho LC X X
(Linnaeus, 1758)
Echeneidae
Echeneis naucrates Live sharksucker Piolho LC X X
Linnaeus, 1758
Remora remora Shark sucker Piolho LC X X X
(Linnaeus, 1758)
Echinorhinidae
Echinorhinus brucus Bramble shark Peixe-prego EN X X X
(Bonnaterre, 1788)
Elopidae
Elops saurus Linnaeus, Ladyfish Ubarana-boca-larga LC X X X X
1766
Engraulidae
Anchoa januaria Rio anchovy Manjuba LC X X X
(Steindachner, 1879)
Anchoa tricolor (Spix & Piquitinga Manjuba LC X X X X
Agassiz, 1829) anchovy
Cetengraulis edentulus Atlantic anchoveta Sardinha-rabo-de-fogo LC X X
(Cuvier, 1829)
Lycengraulis grossidens Atlantic Arenque-amarelo LC X X X
(Spix & Agassiz, 1829) sabretooth
anchovy
Lycengraulis batesii Bates’ sabretooth Arenque-boca-larga; LC X X X
(Günther, 1868) anchovy Arenque-boca-de-velho
Ephippidae
Chaetodipterus faber Atlantic spadefish Enxada; Parum-branco LC X X X X X
(Broussonet, 1782)
Exocoetidae
Hemiramphus brasiliensis Ballyhoo halfbeak Agulha-preta LC X X
(Linnaeus, 1758)
R. R. N. Alves et al.
 Common name Local name (Portuguese) IUCN MMA State Use
Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Cheilopogon cyanopterus Margined Avuador-holandês LC X X X
(Valenciennes, 1847) flyingfish
Hirundichthys affinis Fourwing Avuador-da-pesca; LC X X X
(Günther, 1866) flyingfish Peixe-avuador-pequeno
Exocoetus volitans Tropical two-wing Avuador-do-alto; LC X X
Linnaeus, 1758 flyingfish Peixe-avuador-grande
Fistulariidae
Fistularia petimba Red cornetfish Agulhão-trombeta LC X X X
Lacepède, 1803
Fistularia tabacaria Cornetfish Agulhão LC X X
Linnaeus, 1958
Gempylidae
Gempylus serpens Cuvier, Snake mackerel Espada-preta LC X X X
1829
Gerreidae
Diapterus auratus Irish mojarra Carapitinga; Carapeba LC X X X X X
Ranzani, 1842
Diapterus rhombeus Caitipa mojarra Carapeba LC X X X
(Cuvier, 1829)
Eucinostomus sp. Slender mojarra Carapicu X X X
Eucinostomus argenteus Silver mojarra Carapicu LC X X
Baird & Girard, 1855
Eugerres brasilianus Brazilian mojarra Carapeba LC X X X X
(Cuvier, 1830)
Eucinostomus havana Bigeye mojarra Carapicu-roliço LC X X X
(Nichols, 1912)
Eucinostomus gula (Quoy Jenny mojarra Carapicu-açu LC X X X
& Gaimard, 1824)
Gerres cinereus Yellon fin mojarra Carapicu LC X X X
(Walbaum, 1792)
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest

Ginglymostomatidae
Ginglymostoma cirratum Nurse shark Cação-lixa VU VU X X X X
(Bonnaterre, 1788)
Gobiidae
Bathygobius soporator Frillfin goby Amoré LC X X
(Valenciennes, 1837)
Gobionellus sp. Taicica X
Gymnuridae
Gymnura micrura (Bloch Smooth butterfly Arraia-manteiga NT X X X X X
& Schneider, 1801) ray
Haemulidae
Anisotremus surinamensis Black margate Salema-açu; Salema-preta; Salema-­ DD X X X
(Bloch, 1791) pintada; Avô-de-pirambu; Pirambu
(continued)
237
Table 14.1 (continued)
238

Common name Local name (Portuguese) IUCN MMA State Use

Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Anisotremus virginicus Porkfish Frade; Salema-feiticeira; Salema-­ LC X X X X
(Linnaeus, 1758) freada; Salema-amarela
Conodon nobilis Barred grunt Coró-amarelo; Coró-rajado; LC X X X X
(Linnaeus, 1758) Coróqui-amarelo
Haemulon aurolineatum Tomtate grunt Xira-roliça LC X X X
Cuvier, 1830
Haemulon album Cuvier, White margate Xira-branca DD X X X
1830
Haemulon chrysargyreum Smallmouth grunt Sapuruna LC X X
Günther, 1859
Haemulon parra Sailor’s grunt Cancanhé. Marcasso LC X X X X
(Desmarest, 1823)
Haemulon plumierii White grunt Biquara LC X X X X
(Lacepède, 1801)
Haemulon macrostomum Spanish grunt Cavalo-pedrez; Xirão LC X X X X
Günther, 1859
Haemulon squamipinna Xira listradim; xira-amarela NE X X X X
(Rocha & Rosa, 1999
Haemulon steindachneri Chere-chere grunt Macasso; Omacasso LC X X X
(Jordan & Gilbert, 1882)
Orthopristis ruber Corocoro grunt Cabeça-de-coco; cabeça-dura; LC X X X X
(Cuvier, 1830) Canguito
Pomadasys Roughneck grunt Coró-branco; Coróqui-branco LC X X X X
corvinaeformis
(Steindachner, 1868)
Hemiramphidae
Hemiramphus balao Balao halfbeak Agulha-preta LC X X X
Lesueur, 1821
Hemiramphus brasiliensis Ballyhoo halfbeak Agulha-rabo-de-fogo LC X X X X
(Linnaeus, 1758)
Hyporhamphus roberti Slender halfbeak Agulha-branca LC X X X
(Valenciennes, 1847)
Holocentridae
Holocentrus adscensionis Squilrrelfish Mariquita; jaguriçá; LC X X X X
(Osbeck, 1765) Mariquita-verdadeira
Myripristis jacobus Blackbar Vovozinha LC X X X X
Cuvier, 1829 soldierfish
Istiophoridae
Kajikia albida (Poey, Atlantic White Agulhão-roliço; Atum; Agulhão-negro VU VU X X X
1860) marlin
Makaira nigricans Blue marlin Agulhão-roliço; Atum; Agulhão-negro VU EN X X X
Lacepède, 1802
R. R. N. Alves et al.
 Common name Local name (Portuguese) IUCN MMA State Use
Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Tetrapturus pfluegeri Longbill spearfish Agulhão-marli LC X X X
Robins & de Sylva, 1963

Istiophorus albicans Atlantic sailfish Agulhão-chato; Agulhão-de-vela NE X X X X

(Latreille, 1804)
Labridae
Bodianus rufus (Linnaeus, Spanish hogfish Budião-perua-choca; Budião-­ LC X
1758) papagaio; Papagaio; Bobó-papagaio
Halichoeres radiatus Puddingwife Bodião LC X X
(Linnaeus, 1758) wrasse
Labrisomidae
Labrisomus nuchipinnis Hairy blenny Macaco LC X X X
(Quoy & Gaimard, 1824)
Lamnidae
Carcharodon carcharias White shark Cação-espelho; Cação-branco; VU VU X X X
(Linnaeus, 1758) Tubarão-branco
Isurus oxyrinchus Shortfin mako Cação-cavala; Tubarão-cavala EN X X X
Rafinesque, 1810
Lobotidae
Lobotes surinamensis Tripletail Peixe-sono; Dorminhoco LC X X X
(Bloch, 1790)
Lutjanidae
Etelis oculatus Queen snaper Mariquitão; Pargo-Mariquitão DD X X X
(Valenciennes, 1828)
Lutjanus spp. Dog snapper Baúna; Vermelha; Dentão; X X X
Carapitanga
Lutjanus spp. Parguina X X X
Lutjanus analis (Cuvier, Mutton snapper Cioba; Ciquira NT X X X X X
1828)
Lutjanus apodus Schoolmaster Baúna de fogo LC X X X
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest

(Walbaum, 1792) snapper

Lutjanus cyanopterus Cubera snapper Caranha VU VU X X
(Cuvier, 1828)
Lutjanus jocu (Boch & Dog snapper Dentão DD X X
Schneider, 1801)
Lutjanus synagris Lane snapper Ariacó NT X X X X
(Linnaeus, 1758)
Lutjanus vivanus (Cuvier, Silk snapper Pargo-olho-de-vidro LC X X X X
1828)
Lutjanus buccanella Blackfin snapper Pargo-boca-negra DD X X X X X
(Cuvier, 1828)
Lutjanus griseus Grey snapper Cambuba; Caranha LC X X X
(Linnaeus, 1758)
(continued)
239
Table 14.1 (continued)
240

Common name Local name (Portuguese) IUCN MMA State Use

Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Ocyurus chrysurus Yellowtail snapper Guaiúba-amarela; Guaiúba-paiguina DD X X X X
(Bloch, 1791)
Rhomboplites aurorubens Vermillion Pargo-piranga; Pargo-pinanga; VU X X X
(Cuvier, 1829) snapper Pargo-pininga
Malacanthidae
Malacanthus plumieri Sand tilefish Pirá LC X X X X X
(Bloch, 1786)
Megalopidae
Megalops atlanticus Tarpon Camurupim VU VU X X X X X
Valenciennes, 1847
Mobulidae
Mobula hypostoma Lesser devil ray Raia manta EN X X
(Bancroft, 1831)
Monacanthidae
Aluterus spp. Dotterel filefish Cangulo-fóia; Cangulo-folha; X X X X
Cangulo-seda
Monacanthus ciliatus Fringed filefish Cangulo-de-areia; Cangulo-peruá LC X X X
(Mitchill, 1818)
Stephanolepis hispidus Planehead filefish Cangulo-de-areia LC X X
(Linnaeus, 1766)
Mugilidae
Mugil spp. Zereda; Olho-preto; X X X X
Saúna;Tamatarana; Tainha; Curimã;
Saúna-seleste; Tainha-olho-branco;
Saúna-olho-branco; Tainha-olho-de-­
fogo; Tainha-olho-negro;
Tainha-parati
Mugil curema White mullet Tainha; Saúna LC X X
Valenciennes, 1836
Mullidae
Pseudupeneus maculatus Spotted goadtifsh Saramonete LC X X X X
(Bloch, 1793)
Mulloidichthys martinicus Yellow goatfish Saramonete-rei LC X X X X
(Cuvier, 1829)
Muraenidae
Gymnothorax funebris Green moray Moréia-verde LC X X X
Ranzani, 1839
Gymnothorax moringa Spotted moray Moréia-pintada LC X X X X
(Cuvier, 1829)
Gymnothorax ocellatus Caribbean Moréia-pintada; Mututuca LC X X X X
Agassiz, 1831 ocellated moray
R. R. N. Alves et al.
 Common name Local name (Portuguese) IUCN MMA State Use
Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Gymnothorax spp. Goldentail moray Moréia-preta; Amoréia X X X X
Myliobatidae
Aetobatus narinari Spotted eagle ray Arraia-pintada; Arraia-malhada; EN X X X X X
(Euphrasen, 1790) Arraia-pinta-de-manga; Arraia-chita
Manta birostris Giant manta Arraia-dois-chifres; Arraia-jamanta; EN VU X X X
(Walbaum, 1792) Arraia-morcego
Rhinoptera bonasus Cownose ray Arraia-boca-de-gaveta; arraia-gaveta VU X X X X
(Mitchill, 1815)
Narcinidae
Narcine spp. Lesser electric ray Treme-treme X
Narcine brasiliensis Brazilian electric Raia treme-treme NT VU X X
(Olfers, 1831) ray
Ogcocephalidae
Ogcocephalus vespertilio Seadevil Cachimbo; Cachimbau LC X
(Linnaeus, 1758)
Ostraciidae
Acanthostracion Scrawled cowfish Baiacu-caixão LC X X
quadricornis (Linnaeus,
1758)
Lactophrys trigonus Buffalo trunkfish Baiacu-caixão LC X X X
(Linnaeus, 1758)
Paralichthyidae
Paralichthys tropicus Tropical flounder Soia DD
Ginsburg, 1933
Polynemidae
Polydactylus oligodon Littlescale Barbudo LC X X X
(Günther, 1860) threadfin
Polydactylus virginicus Barbu Barbudo LC X X X X X
(Linnaeus, 1758)
Pomacanthidae
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest

Holacanthus tricolor Rock beauty Parú LC X X

(Bloch, 1795)
Pomacanthus arcuatus Gray angelfish Parum-preto; Peixe-vidro; LC X X X X X
(Linnaeus, 1758) Quebra-pedra
Pomacentridae
Abudefduf saxatilis Sergeant-major Saberé; Saberé-rajado; Sargentinho LC X X X
(Linnaeus, 1758)
Stegastes pictus Yellowtip Castanheta NE X X X
(Castelnau, 1855) damselfish
Pomatomidae

(continued)
241
Table 14.1 (continued)
242

Common name Local name (Portuguese) IUCN MMA State Use

Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Pomatomus saltatrix Bluefish Enchova; Anchova VU X X X
(Linnaeus, 1766)
Priacanthidae
Priacanthus arenatus Atlantic bigeye Cantante LC X X X X
Cuvier, 1829
Pristigasteridae
Pellona harroweri American coastal Sardinha-berimberim LC X X X
(Fowler, 1917) pellona
Rachycentridae
Rachycentron canadum Cobia Beijupirá; cação-de-escama LC X X X
(Linnaeus, 1766)
Rhicodontidae
Rhincodon typus Smith, Whale shark Tubarão-baleia; Tubarão-cachalote EN VU X X
1828
Rhinobatidae
Pseudobatos percellens Chola guitarfish Cação-viola; Viola EN VU X X X X
(Walbaum, 1792)
Scaridae
Scarus trispinosus Greenback Bobó-espinha-verde; Budião-azul; EN EN X X X
Valenciennes, 1840 parrotfish Budião-bico-verde; Budião-verde;
Bobó-bico-verde
Scarus taeniopterus Princess parrotfish Budião LC X X X
Lesson, 1829
Scarus zelindaeMoura, Zelinda’s Budião DD VU X X X
Figueiredo & Sazima, parrotfish
2001
Sparisoma axillare Gray parrotfish Batata; Batatoa; Boboa; Bobó-batatão; DD VU X X X
(Steindachner, 1878) Bobó-cabeça-seca; Budião-batata;
Budião; Budião-rabo-de-forquilha
Sparisoma frondosum Agassiz’s Budião DD VU X X X
(Agassiz, 1831) parrotfish
Sparisoma radians Bucktooth Batata; Batatoa; Boboa; Bobó-batatão; LC X X X
(Valenciennes, 1840) parrotfish Bobó-cabeça-seca; Budião-batata;
Budião
Sparisoma amplum Reef parrotfish Budião-rabo-de-forquilha LC X X X
(Ranzani, 1841)
Sparisoma rubripinne Redfin parrotfish Batata LC X X
(Vallenciennes, 1840)
Sciaenidae
Cynoscion acoupa Acoupa weakfish Pescada-amarela VU X X X
(Lacepède, 1801)
R. R. N. Alves et al.
 Common name Local name (Portuguese) IUCN MMA State Use
Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Ctenosciaena Barbel drum Pescada LC X X
gracilicirrhus (Metzelaar,
1919)
Cynoscion jamaicensis Jamaica weakfish Goete LC X
(Vaillant & Bocourt,
1883)
Cynoscion microlepidotus Smallscale Pescada-de-dente LC X X X X
(Cuvier, 1830) weakfish
Cynoscion leiarchus Smooth weakfish Pescada-branca LC X X X
(Cuvier, 1830)
Cynoscion virescens Green weakfish Pescada-bacalhau; Pescada-camuçu; LC X X X
(Cuvier, 1830) comeocu; Pescada-cangussu;
Pescada-muçu; Pescada-curuvina;
Pescada-cabeça-de-cobra;
Pescada-cururuca
Cynoscion sp. Pescada X X
Isopisthus parvipinnis Bigtooth corvina Pescada-chata LC X X X
(Cuvier, 1830)
Larimus breviceps Cuvier, Shorthead drum Boca-mole LC X X X X
1830
Macrodon ancylodon King weakfish Rabo de fogo LC X X
(Bloch & Schneider,
1801)
Menticirrhus americanus Southern Curuca LC X X
(Linnaeus, 1758) kingcroaker
Menticirrhus littoralis Gulf kingcroaker Perna de moça LC X X
(Holbrook, 1847)
Micropogonias furnieri Whitemouth Curuca; Cururuca; Corvina LC X X X X
(Desmarest, 1823) croaker
Micropogonias undulatus Atlantic croaker Pescada-perna-de-moça LC X X X
(Linnaeus, 1766)
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest

Ophioscion Spotted croaker Cabeça-de-côco LC X X

punctatissimus Meek &
Hildebrand, 1925
Paralonchurus Banded croaker Coróqui-de-barbela; LC X X X
brasiliensis (Steindachner, Pescada-perna-de-moça
1875)
Stellifer sp. Cabeçudo X X
Stellifer microps Smalleye stardrum Pescada-curuvina; Pescada-cabeça-­ LC X
(Steindachner, 1864) de-cobra; Pescada-cururuca
Umbrina coroides Cuvier, Sand drum Pescada branca LC X X
1830
Scombridae
Acanthocybium solandri Wahoo Cavala-impim; cavala-impinge; LC X X X X
(Cuvier, 1832) cavala-preta
(continued)
243
Table 14.1 (continued)
244

Common name Local name (Portuguese) IUCN MMA State Use

Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Auxis rochei (Risso, 1810) Bullet tuna Atum; Bonito LC X X X
Auxis thazard (Lacepède, Frigate tuna Atum; Bonito LC X X X X
1800)
Euthynnus alletteratus Little tunny Atum; Bonito LC X X X X X
(Rafinesque, 1810)
Katsuwonus pelamis Skipjack tuna Atum; Bonito LC X X X
(Linnaeus, 1758)
Sarda sarda (Bloch, Atlantic bonito Atum; Bonito LC X X X
1793)
Scomber colias Gmelin, Atlantic chub Cavalinha; Cavalinha-do-sul LC X X X
1789 mackerel
Scomberomorus Serra Spanish Serra-pininga; Serra-pinta-amarela LC X X X X X
brasiliensis Collette, mackerel
Russo & Zavala-Camin,
1978
Scomberomorus cavalla King mackerel Cavala-branca; cavala-perna-de-moça LC X X X X X
(Cuvier, 1829)
Scomberomorus regalis Cero Serra LC X X X X
(Bloch, 1793)
Thunnus sp. Albacora X X
Thunnus albacares Yellowfin tuna Albacora-de-aba-amarela; Albacora-­ LC X X X X
(Bonnaterre, 1788) gaia-­amarela; Albacora-amarela;
Albacora-de-lajo
Thunnus alalunga Blackfin tuna Albacora-branca; Albacora-legítima LC X X X
(Bonnaterre, 1788)
Thunnus atlanticus Blackfin tuna Albacora-cachorro; Albacora-preta LC X X X X
(Lesson, 1831)
Thunnus obesus (Lowe, Bigeye tuna Albacora-de-aba-amarela; Albacora-­ VU X X X
1839) gaia-­amarela; Albacora-amarela
Thunnus thynnus Atlantic bluefin Albacora-maguru LC EN X X
(Linnaeus, 1758) tuna
Scorpaenidae
Scorpaena brasiliensis Barbfish Aniquim LC X X
Cuvier, 1829
Scorpaena plumieri Spotted Aniquim; Beatriz LC X X X X
Bloch, 1789 scorpionfish
Scorpaenodes spp. Reef scorpionfish Aniquim X X X
Serranidae
Alphestes afer (Bloch, Muttom hamlet Sapê LC X X X
1793)
Cephalopholis fulva Coney Piraúna-amarela; Piraúna-flor-de-­ LC X X X X
(Linnaeus, 1758) algodão; Piraúna-perua-choca;
Piraúna-vermelha; Piraúna-preta;
R. R. N. Alves et al.

Garoupinha
 Common name Local name (Portuguese) IUCN MMA State Use
Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Epinephelus adscensionis Rock hind Peixe-gato; Mané-velho; LC X X X X
(Osbeck, 1771) Garoupa-pintada
Epinephelus guttatus Red hind Garoupa-preta LC X X X
(Linnaeus, 1758)
Epinephelus itajara Atlantic goliath Mero VU CR X X X X X
(Lichtenstein, 1822) grouper
Epinephelus morio Red grouper Garoupa-branca VU VU X X X
(Valenciennes, 1828)
Mycteroperca acutirostris Comb grouper Sirigado-papuã LC X X
(Valenciennes, 1828)
Mycteroperca bonaci Black grouper Sirigado NT VU X X
(Poey, 1860)
Mycteroperca interstitialis Yellowmouth Sirigado-boca-de-sino VU VU X X X
(Poey, 1860) grouper
Mycteroperca microlepis Gag grouper Sirigado-bico-fino; VU X X X
(Goode & Bean, 1879) Sirigado-masca-fumo
Mycteroperca tigris Tiger grouper Sirigado; Badejo DD X X X
(Valenciennes, 1833)
Mycteroperca venenosa Yellowfin grouper Sirigado; Badejo NT X X X
(Linnaeus, 1758)
Rypticus saponaceus Greater soapfish Sabão LC X X X
(Bloch & Schneider,
1801)
Sparidae
Archosargus Sheepshead Sargo LC X X X
probatocephalus
(Walbaum, 1792)
Archosargus rhomboidalis Western Atlantic Salema-açu; Sargo LC X X X
(Linnaeus, 1758) seabream
Calamus penna Sheepshead porgy Pena-branca LC X X X
(Valenciennes, 1830)
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest

Calamus pennatula Pluma porgy Pena-açu LC X X X X

Guichenot, 1868
Sphyraenidae
Sphyraena barracuda Great barracuda Goiva; Gorana; Bicuda; Barracuda LC X X X X
(Edwards, 1771)
Sphyraena guachancho Guachanche Goiva; Gorana; Bicuda; Barracuda LC X X X X
Cuvier, 1829 barracuda
Sphyraena sphyraena European Goiva; Gorana; Bicuda; Barracuda LC X X X
(Linnaeus, 1758) barracuda
Sphyrnidae
Sphyrna lewini (Griffith Scalloped Cação-panã; martelo; Tubarão CR CR X X X X
& Smith, 1834) hammerhead martelo; tubarão-panã
(continued)
245
Table 14.1 (continued)
246

Common name Local name (Portuguese) IUCN MMA State Use

Family/scientific name (English)a (2021) (2022) AL PB PE F Co Med H S-R Aq
Sphyrna mokarran Great Cação-panã; martelo; Tubarão CR CR X X X
(Rüppell, 1837) hammerhead martelo; tubarão-panã
Sphyrna zygaena Smooth Cação-panã; martelo; Tubarão VU CR X X X
(Linnaeus, 1758) hammerhead martelo; tubarão-panã
Sphyrna tiburo (Linnaeus, Bonnethead Cação-panã-chapéu-redondo; EN CR X X X
1758) Cação-sombreiro; Tubarão-sombreiro
Squalidae
Squalus cubensisHowell Cuban dogfish Cação-de-espeto LC X X X X X
Rivero, 1936
Syngnathidae
Hippocampus reidi Longsnout Cavalo-marinho NT VU X X X X
Ginsburg 1933 seahorse
Synodontidae
Trachinocephalus myops Snakefish Traíra LC X X X
(Forster, 1801)
Tetraodontidae
Colomesus psittacus Banded puffer Baiacu-camisa-de-meia LC X X
(Bloch & Schneider,
1801)
Lagocephalus spp. Smooth puffer Baiacu-guarajuba; Baiacu-garajuba; X X X
Baiacu-arara
Lagocephalus laevigatus Smooth puffer Baiacu-xaréu LC X X
(Linnaeus 1766)
Sphoeroides testudineus Checkered puffer Baiacu-pintado LC X X
(Linnaeus, 1758)
Sphoeroides spp. Bandtail puffer Baiacu-franguinho; Baiacu-­ X X X
pintadinho; Baiacu-pintado
Triakidae
Mustelus sp. Cação-namorado; Cação-banguelo X X
Mustelus sp. Cação-manteiga X X X
Trichiurus lepturus Largehead hairtail Espada-branca LC X X X X
Linnaeus, 1758
Triglidae
Prionotus punctatus Bluewing searobin Voador LC X X
(Bloch, 1793)
Xiphiidae
Xiphias gladiusLinnaeus, Swordfish Agulhão-espadarte; Agulhão-Meca; LC X
1758 Meca
a
Source: fishbase.org
Conservation status of aquatic species: NE Not Evaluated, DD Data Deficient, LC Least Concern, NT Near Threatened, VU Vulnerable, EN Endangered, CR Critically Endangered
States: AL Alagoas, PB Paraíba, PE Pernambuco
Species uses: F Food, Co Commercial, Med Medicinal, H Handicrafts, S-R Spiritual-religious, Aq Aquarium
R. R. N. Alves et al.
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest
are later returned to the sea still alive, being popularly called
“charutos” (Rodrigues-Filho et  al. 2009). This practice is
called finning and is prohibited in Brazil (MPA/MMA 2012).
Reef fish are also fished for both food and aquarium pur-
poses. Live reef fish may also be used as tourist attractions for
underwater recreation where people dive, feed the fish, and
take pictures. This has been a common practice on the reefs of
Maragogi (Alagoas), Porto de Galinhas (Pernambuco), and
Picãozinho (Paraíba), although prohibited in some locations.
We can also mention offshore recreational fishing (Filizola-
Freire et al. 2018), which has grown in some regions.
Some fish stand out for not being consumed for food pur-
poses, but they still have multiple uses. The seahorse
(Hippocampus reidi Ginsburg, 1933) is a good example of
this, as its capture and trade are primarily intended for
medicinal use, aquarium hobby (as ornamental fish), handi-
crafts (as souvenirs), and magical-religious purposes (Alves
and Rosa 2006, 2007a). The use of seahorses goes beyond
trade, as these fish are also subjected to tourist exploitation in
some mangrove areas in NE Brazil. As an example, the “sea-
horse tours” tourist activity is carried out in the Maracaípe
River estuary (Pernambuco), which involves the temporary
removal of the seahorse from the habitat for a display to tour-
ists in glass containers (Ternes et al. 2016), although so far
there is no evidence on the sustainability of this activity and
Fig. 14.2  West Indian manatees (Trichechus manatus) in Peixe-boi Project, Paraíba State, Northeast coast of Brazil. (Photograph: Lena Bezerra
via Wikimedia Commons)
247
no impact assessment on the stress caused to the animals by
this interaction.
Considering other groups of vertebrates, mammals are
also important in terms of exploitation and use. One of the
largest marine animals found in estuaries, the West Indian
manatee (Trichechus manatus, Linnaeus, 1758) (Fig. 14.2),
uses these ecosystems to feed, rest, and reproduce. It was an
easy target for capture by humans for a long time because it
is docile, slow  moving behavior, and as a food resource.
According to some fishermen, the taste of manatee meat was
compared to that of beef, and the fat of these animals was
used for medicinal purposes and the oil as a fuel source
(Lima et al. 1992).
Hunting for food purposes is considered to be primarily
responsible for the current conservation status of the West
Indian manatee (Silva et al. 2018), which is considered one
of the most endangered aquatic mammals in Brazil (Luna
et al. 2018). The hunting of this animal has been prohibited
in the country since 1967 (Brasil 1967), and its capture and
use have drastically decreased as a result, especially since
the 1980s when the federal government created the “Peixe-­
Boi” Project (Andrade et  al. 2011). The species currently
continues to be threatened by habitat loss caused by the silt-
ing of rivers and deforestation of mangroves, by strandings
and accidents caused by vessels, and by capture, whether
248
incidental (in shrimp trawls) or intentional (Andrade et  al.
2011; Silva et al. 2018).
Dolphins and whales, together with manatees, correspond
to the most common marine mammals on the northeastern
Brazilian coast. Sotalia guianensis (Van Bénéden, 1864) dol-
phins can be accidentally caught in gill nets, and in these
cases, their products can be used for human consumption of
meat, as bait, handicrafts, medicinal and mystical purposes
(Alves and Rosa 2006; Alves et al. 2010). In some places,
these animals approach the beach, which occasionally causes
strandings or accidents with motorized boats. The bait is
mainly used for longline fishing for pelagic fish such as tuna,
yellowfin, and sharks. To obtain it, longitudinal cuts are
made along the dolphin’s body, removing the meat, along
with the skin and fat. Then these “strips” are cut into smaller
pieces (bait) so that they fit on the hooks. The process for
obtaining meat for human consumption is similar to that of
bait, but the meat is separated from the skin and fat, leaving
only the “fillet”. When using dolphins for handicrafts, the
carcasses are buried on the beach or in the backyards of local
residents’ houses in order to obtain a clean skeleton of the
animals. Handicraft items (e.g., earrings, bracelets, and
necklaces) are made from bones and teeth, or the entire or
partial skeleton is used as a souvenir (Pinto et al. 2018; Alves
et al. 2010). Raw materials obtained from other large verte-
brates, such as whales and sea turtles, are eventually used for
medicinal purposes, although they are rare events mainly due
to bans  imposed by environmental agencies; however, the
Fig. 14.3  A hawksbill turtle (Eretmochelys imbricata) spawning on a beach of Paraíba State, Northeast coast of Brazil. (Photograph: Acervo do
Instituto Parahyba de Sustentabilidade—IPAS)
R. R. N. Alves et al.
capture of turtles can occur illegally, both for food and for
medicinal purposes (Alves and Rosa 2006).
Sea turtles spawn on some beaches in northeastern Brazil
in areas close to “restingas” (Fig.  14.3), which have also
been configured as remnants of the Atlantic Forest. For many
years, sea turtles were used for various purposes such as
food, commercial, magical-religious purposes, as handi-
crafts and household items, and for medicinal and cosmetic
purposes. However, these uses have declined dramatically
since the institution of IBAMA Ordinance no. 1522 of
December 19, 1989, which legally protects sea turtles
nationally.
14.4 Estuarine–Marine Invertebrates
Several groups of marine invertebrates are also of great
importance in the region, constituting a source of income for
a significant portion of the coastal population. The crab fauna
is one of the most conspicuous in mangrove areas and repre-
sents an important part of the livelihoods of fishermen in
estuarine areas (Nascimento et  al. 2012a, b, 2016, 2017;
Nordi et al. 2009). Among the most important species are the
mangrove land crab Ucides cordatus (Linnaeus, 1763), the
crab Cardisoma guanhumi Latreille, 1825, and the
Callinectes spp. crabs. The mangrove land crab has attracted
the most attention as a fishing resource, being captured in
large quantities in mangrove areas, constituting one of the
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest
main food items of the regional cuisine, and is much appreci-
ated by local residents and tourists (Alves and Nishida 2002,
2003; Nascimento et al. 2017). The mangrove land crab is
the main traded faunal resource in some areas north of the
São Francisco, as in the estuaries of the Mamanguape
(Fig.  14.4) and Paraíba rivers (Paraíba state), as well as at
Rio Formoso and São José da Coroa Grande (Pernambuco
state), contributing to income generation for many families.
Shrimp and lobsters are also among the exploited marine
crustaceans. Among shrimp, the species Xiphopenaeus
kroyeri (Heller, 1862), Macrobrachium carcinus (Linnaeus,
1758), and Penaeus spp. (Fig. 14.5) are the most exploited
(Alves et  al. 2005; Alves and Nishida 2002; Montenegro
et  al. 2007; Nishida et  al. 2006a, b). Shrimp are common
fishing targets and are widely consumed by fishermen and
their families; however, commercializing these animals for
food is more advantageous from an economic point of view
due to their commercial value compared to fish and other
meats (Pinto et  al. 2017). Shrimp are caught with nets or
trawls and are mainly used for the food trade (Pinto et  al.
2021). Small shrimps are used as bait for catching fish, and
some are used as food. It is worth noting that shrimp farming
in ponds has been implemented in several areas in recent
years, such as the estuary of the Mamanguape River (Nishida
and Alves 2001). Shrimp farming is one of the main threats
to the conservation of species that inhabit mangroves and
estuaries, as it causes the deforestation of large mangrove
vegetation areas (ICMBIO 2018a). Nishida and Alves (2001)
highlighted that this activity grew along the estuary of the
Mamanguape river (Paraíba), with many nurseries in their
vast majority implanted in the absence of inspection by envi-
Fig. 14.4  Gatherer of the
mangrove land crab
‘caranguejo uçá’ (Ucides
cordatus) in the mangrove
forest of Mamanguape
estuary, Paraíba State,
Northeast coast of Brazil.
(Photograph: Marcia Freire
Pinto)
249
ronmental agencies, as in other areas of the NE Brazil
(ICMBIO 2018a).
Lobsters are caught in some fishing communities on the
northeast coast of the country, but the largest fisheries occur in
the state of Ceará (Alencar et al. 2020), although on a smaller
scale in other states, as Paraíba and Pernambuco. Lobsters can
be part of the menu of fishermen and their families; however,
it is primarily sold whole or processed (meat) for international
trade. The main species caught are the red lobster Panulirus
argus (Latreille, 1804) (Fig.  14.6) and the green lobster
Panulirus laevicauda (Latreille, 1817), although the spotted
lobster Panulirus echinatus Smith, 1869 is frequently found,
as well as the slipper lobsters Scyllarides brasiliensis Rathbun,
1906 and Scyllarides delfosi Holthuis, 1960.
Octopus, squid, and whelk stand out among the mollusks
exploited in the region. These animals are fished for food,
but some are also used for medicinal purposes. In addition,
the collection of mollusk shells for handicraft production is
performed a lot on the coast (Dias et al. 2011; Jennings 1987;
Lunn et al. 2008; Pinto et al. 2013; Rosa et al. 2011; Wood
and Wells 1988). These shells are also collected and used in
construction in some communities. Some people also use
shells in religious rituals and as symbolic items (Dias et al.
2011; Leo Neto et al. 2009, 2012) or as household items.
Some mollusks are common in reef environments, such as
octopuses (Octopus spp.), which humans mainly use for
food. However, as with other fishing resources, some capture
practices are predatory, such as using bleach sprayed into the
burrows to expel these animals. Mollusk collection in estua-
rine regions mainly involves women (Nishida et al. 2006a,
c). The clam Anomalocardia flexuosa (Linnaeus, 1767)
250 R. R. N. Alves et al.

Fig. 14.5  Shrimp (Penaeus

sp.) captured by fishers from
Tamandaré beach,
Pernambuco, Northeast coast
of Brazil. (Photograph:
Marcia Freire Pinto)

Fig. 14.6  Fisherman with

red lobster (Panulirus argus)
caught on Tamandaré beach,
Pernambuco, Northeast coast
of Brazil. (Photograph:
Marcia Freire Pinto)

stands out due to its high abundance in estuaries, high vol-
ume captured, and high local consumption (Fig. 14.7). Other
bivalves are also collected and used for food purposes, such
as Austromacoma constricta (Bruguière, 1792), the “sururu”
(Mytella spp.), the “lambreta” Phacoides pectinatus (Gmelin,
1791), the “taioba” Iphigenia brasiliensis (Lamarck, 1818),
the “unha de velho” Tagelus plebeius (Lightfoot, 1786), and
the oyster (Crassostrea spp.). Some of these animals are also
used for medicinal, magical-religious purposes and for pro-
ducing handicrafts (Alves and Rosa 2006; Dias et al. 2011;
Leo Neto and Alves 2010; Leo Neto et  al. 2011, 2012)
(Fig. 14.8).
Other marine invertebrates such as echinoderms are also
used by people, including starfish (Asteroidea and
Ophidiasteridae), whose skeleton is perhaps one of the most
used as decoration objects. These animals are also used in
folk medicine (Alves and Rosa 2006, 2007a, 2010). However,
some people believe that having the skeleton of this animal
in the house is synonymous with bad luck. The starfish is
also a magical-religious symbol in the case of religion of
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest 251

Fig. 14.7  Community of shellfish fishers in Cabedelo, Paraíba, Brazil, Northeast coast of Brazil. (Photograph: Marcia Freire Pinto)

Fig. 14.8  Handicrafts with

mollusks shells in a shop in
Alagoas, Northeast coast of
Brazil. (Photograph: Marcia
Freire Pinto)
252
African origin. The Echinometra lucunter sea urchins
(Linnaeus, 1758) also have their skeletons used as decorative
objects. In Suape Bay, on the southern coast of the State of
Pernambuco, the consumption of this species occurs in a cul-
tural event called “Festa da Ouriçada” (Sea Urchin Festival),
with origins in the local belief derived from popular
Catholicism. According to Oliveira and Andrade (2013), the
peculiarity of “Ouriçada” is to celebrate and commensurate
the sea urchin, which is an extraordinary practice concerning
local eating habits and an exception in the daily life of this
fishing village. The customary fishing of that community is
replaced for 1  day by the unusual ritual of collecting sea
urchins, which takes place along the natural sandstone reefs
of Suape Bay. This sea urchin collection requires specific
knowledge about tidal dynamics and navigation techniques.
It is primarily an activity carried out by men, who are also
responsible for preparing the coconut straw bonfire that will
roast the sea urchins. After roasting, the urchins are usually
broken, and women finish the “ouriçada” dish (Fig. 14.9).
Fig. 14.9  Preparation of
Echinometra lucunter to be
consumed by people during
the “Festa da Ouriçada”. (Sea
Urchin Festival), municipality
of Cabo de Santo Agostinho,
Pernambuco, Northeast coast
of Brazil. (Photograph:
Angelo G. C. Alves)
R. R. N. Alves et al.
14.5 Implications for Conservation
and Final Considerations
Several aquatic animal species exploited in the coastal areas
along the Atlantic Forest remnants are threatened with
extinction and figure in the Brazilian red list of threatened
species (MMA 2022). The starfish Oreaster reticulatus
(Linnaeus, 1758) and Luidia senegalensis (Lamarck, 1816)
and the crab Cardisoma guanhumi comprise the threatened
invertebrates. Moreover, 24 fish species are threatened
(Table  14.1): the Atlantic goliath grouper Epinephelus ita-
jara (Lichtenstein, 1822); the Black grouper Mycteroperca
bonaci (Poey, 1860); the Yellowmouth grouper Mycteroperca
interstitialis (Poey, 1860); the longsnout seahorse
Hippocampus reidi; the blue marlin Makaira nigricans
Lacepède, 1802; the Atlantic white marlin Kajikia albida
(Poey, 1860); the Atlantic bluefin tuna Thunnus thynnus
(Linnaeus, 1758); the cubera snapper Lutjanus cyanopterus
(Cuvier, 1828); the tarpon Megalops atlanticus Valenciennes,
14  Fisheries and Uses of Coastal Aquatic Fauna in the Northernmost Brazilian Atlantic Forest
1847; the parrotfish Scarus zelindae Moura, Figueiredo &
Sazima, 2001; Scarus trispinosus Valenciennes, 1840;
Sparisoma frondosum (Agassiz, 1831) and Sparisoma axil-
lare (Steindachner, 1878); the red grouper Epinephelus
morio (Valenciennes, 1828); the Chola guitarfish Pseudobatos
percellens (Walbaum, 1792); the rays Narcine brasiliensis
(Olfers, 1831) and Manta birostris (Walbaum, 1792); and the
sharks Sphyrna lewini (Griffith & Smith, 1834), Sphyrna
mokarran (Rüppell, 1837), Sphyrna tiburo (Linnaeus, 1758),
Sphyrna zygaena (Linnaeus, 1758), Rhincodon typus Smith,
1828, Carcharodon carcharias (Linnaeus, 1758), and
Ginglymostoma cirratum (Bonnaterre, 1788). Finally, the
sea turtles Eretmochelys imbricata (Linnaeus, 1766), Caretta
caretta (Linnaeus, 1758), and Dermochelys coriacea
(Vandelli, 1761); the dolphin Sotalia guianensis; and the
West Indian manatee Trichechus manatus also figure in the
Brazilian Red List.
Most species under conservation concerns are threatened
due to overfishing and habitat degradation in Brazil
(ICMBIO 2018b), the multiplicity of uses causing intense
extractive pressure on natural populations, and in some
cases, this pressure has contributed to the decline of wild
populations of already threatened species (Alves and Souto
2015). Furthermore, tourism has brought about substantial
changes in many fishing communities, including in their
diets. For example, in Tamandaré, Pernambuco, tourism has
changed the eating habits of fishermen’s families and made
them prefer to sell fish instead of consuming it, as fish,
shrimp, and lobster are more expensive compared to other
meats (beef, lamb, pork, processed) (Pinto et  al. 2017). A
similar situation is pointed out by Santos et al. (2022), who
investigated the diet of Potiguara Indians living on the
northern coast of Paraíba and found high consumption of
protein sources derived from domestic animals and industri-
alized products, suggesting that these populations are con-
suming less protein derived from wild animals. One of the
factors associated with this change in diet is the environ-
mental degradation of the Atlantic Forest in the region and
the marked defaunation observed in this biome, which made
terrestrial vertebrates previously consumed through hunting
inaccessible. In addition, with the overfishing of most spe-
cies of economic importance, many coastal communities
have been incorporating or even replacing fishing activities
with tourist activities, which can thus add new pressures to
fishing resources and coastal ecosystems. Santos et  al.
(2022) also point out that the higher consumption of domes-
tic protein is largely associated with the dense road network
and easier access to food markets from neighboring urban
centers. Indeed, connection to markets via roads has
been considered in several places as an important determi-
nant of household food consumption (Kramer et al. 2009).
Furthermore, Araújo and Bramwell (2002) state that tour-
ism expansion interferes with the livelihoods of fishing
253
communities, with state and municipal financial resources
being directed to tourist activity, which consequently deval-
ues traditional cultures.
Acknowledgments We thank the Universidade Estadual da Paraíba
(UEPB), the Research Support Foundation of the State of Paraíba
(FAPESQ - Edital 09/2021 Demanda Universal), and the Brazilian
National Council for Scientific and Technological Development (CNPq -
Edital Universal 422041/2018-1) for the financial support. Thanks are also
due to CNPq for the productivity grant awarded to RRNA.
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 Hunting and Uses of Terrestrial
Vertebrates in the Northernmost
Region in the Atlantic Forest in Brazil
Rômulo Romeu Nóbrega Alves, José Aécio Alves Barbosa,
and Anna Karolina Martins Borges
Abstract
Many wild vertebrates of the Atlantic Forest have been
exploited by human populations, including several endan-
gered species. The practice of hunting is quite common in
this area, and people use animal resources in various
ways. In this scenario, beyond ecological research of the
exploited animals, ethnozoological information is impor-
tant to support plans for sustainable management and
conservation strategies for the fauna of this region. In this
chapter, we discuss the use of wildlife resources in the
northernmost region in the Atlantic Forest in Brazil and
its implications for conservation. There are records that at
least 163 vertebrate species have been hunted in the
region, belonging to the following taxa: Aves (n  =  94;
58%), Mammalia (n = 36; 23%), Reptilia (n = 28; 17%),
and Amphibia (n  =  5; 4%). The species or resources
derived from them are used locally for the following pur-
poses: food (68 species), traditional medicine (39 spe-
cies), and pets (66 species). At least 75 species are
associated with commercialization, mainly birds intended
for use as pets. A total of 44 species are hunted for being
involved in conflict situations with the human population,
mainly snakes. Of the 163 species recorded, 127 are
included on lists of threatened species, with 7 species in
categories of greatest conservation concern (vulnerable,
endangered, or critically endangered), and hunting,
R. R. N. Alves (*)
Departamento de Biologia, Universidade Estadual da Paraíba,
Campina Grande, PB, Brazil
J. A. A. Barbosa
Programa de Pós-graduação em Recursos Naturais, Centro de
Tecnologia e Recursos Naturais, Universidade Federal de Campina
Grande, Campina Grande, PB, Brazil
A. K. M. Borges
Programa de Pós-Graduação em Etnobiologia e Conservação da
Natureza, Universidade Federal Rural de Pernambuco,
Recife, PE, Brazil
e-mail: anna.kmborges@ufrpe.br
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
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_15
15
regardless of motivation, is one of the factors that has
impacted all their populations. The list of hunted species
highlights the urgency of further ethnozoological studies,
as well as the biology and ecology of the most used spe-
cies, in order to determine the pressure and influence that
commercialization exert on their natural populations. This
information is crucial for elaborating animal management
and conservation plans.
Keywords
Animal uses · Bushmeat · Ethnozoology · Game animals
· Wildlife
15.1 Introduction
The Brazilian Atlantic Forest, one of the most important
tropical forests on the planet and a global biodiversity hotspot
(Zachos and Habel 2011), is the most degraded Brazilian
biome. It is estimated that more than 70% of the Atlantic
Forest has been devastated since the colonization of Brazil,
and what remains is fragmented and threatened with destruc-
tion in several regions (Rezende et  al. 2018; Silva et  al.
2016). The impacts resulting from different forestry exploi-
tation and land use cycles since the colonial period (Silva
et  al. 2016), added to the high population density in the
biome (Scarano and Ceotto 2015) and the overexploitation
of forest resources by human populations (e.g., wood, fruits,
hunting of wild animals), have drastically reduced the
Atlantic Forest vegetation, consequently affecting all its fau-
nal biodiversity (Paglia et al. 2008).
Despite still harboring a great diversity of vertebrates, the
loss caused by the devastation of the biome was drastic
(Canale et al. 2012), and many of the species are currently
threatened. In addition to the loss of habitat, one of the main
reasons for this situation is hunting, which, despite legal
restrictions, continues to be practiced for subsistence, sports,
recreational, and even professional purposes (Chiarello et al.
257
258
2008; Dirzo et al. 2014; Fernandes-Ferreira and Alves 2017;
Fernandes-Ferreira et al. 2012; Hanazaki et al. 2009; Souza
and Alves 2014). As in tropical forest areas around the world,
hunting activities have affected animal populations (Alves
et al. 2018; Ripple et al. 2016), to a greater or lesser extent,
especially the most exploited species. Thus, conservation
measures must necessarily include an understanding of the
social, cultural, and ecological aspects that involve these
activities.
Considering that it is currently widely recognized that
factors such as overexploitation, hunting, and illegal trade in
wild animals are threats to several vertebrate species through-
out Brazil (Alves 2012; Alves et al. 2009b; Bonaudo et al.
2005; Fernandes-Ferreira et al. 2012; Machado et al. 2008;
Peres and Nascimento 2006; Silvius et al. 2004), it becomes
difficult to devise efficient strategies for animal conservation
without considering the human element and its interactions
with other animals. Thus, understanding the multidimen-
sional context of hunting is essential to design effective con-
servation solutions (Alves 2012; Alves et al. 2009b). In this
context, measures that seek the conservation and sustainable
use of fauna must not only bring together zoological and
ecological information but also the economic and cultural
interactions that link ecological and social systems in a com-
mon system, which influence each other (Alves and
Albuquerque 2012; Bogart et al. 2009; Chapin and Whiteman
1998; Geist and Lambin 2002).
Studies that address hunting are generally still incipient in
Brazil (Alves and Souto 2011; Fernandes-Ferreira and Alves
2017; Teixeira 1992). Such research has mostly focused on
the Amazon region and more recently on the northeastern
semiarid region (Alves et  al. 2009b, 2010a; Barbosa et  al.
2010, 2011; Fernandes-Ferreira et  al. 2012). A few recent
studies in the Atlantic Forest reveal that hunting persists
clandestinely in many places, despite the great fragmentation
of the Atlantic Forest, with population decline of many spe-
cies targeted by hunting (Castilho et  al. 2018, 2019). It is
also important to emphasize that a good part of the officially
endangered species in the country inhabits this biome
(Tabarelli et al. 2003), evidencing the need for ­ethnozoological
studies on hunting and regional uses of animals, which are
fundamental to provide subsidies for implementing environ-
mental management and conservation of local species.
In this chapter, we document the use of faunal resources
in Atlantic Forest areas located north of the São Francisco
River. Hunting studies for this region are scarce and concen-
trated in locations in the State of Paraíba but also allow an
analysis of hunting practices associated with such uses and
their implications for conservation in the region. It is
expected that the results can support elaboration of conserva-
tion and management strategies for the most exploited spe-
cies, in addition to providing an understanding of the ways in
which the fauna is used by local populations and their
R. R. N. Alves et al.
impacts on biodiversity, making it possible to later adopt
public policies aimed at the conservation and preservation of
the faunal heritage, which constitutes a valuable source of
food and other products for local populations.
15.2 Hunting Fauna and Its Uses
Despite few studies on hunting having been conducted in
areas of the Atlantic Forest north of São Francisco, an expres-
sive number (n = 162) of game vertebrates has already been
recorded in Atlantic Forest areas of the State of Paraíba,
including birds, mammals, reptiles, and amphibians
(Table 15.1; Fig. 15.1). These animals are hunted for differ-
ent reasons, including the use of meat for food, zootherapeu-
tic use (using the animal’s body parts for medicinal purposes),
and to capture pets. There is also hunting motivated by con-
flict, meaning directed to kill animals with the aim of pro-
tecting crops, preventing predation of domestic animals, and
protecting oneself and hunting dogs, in addition to killing
venomous animals motivated by fear.
Birds are the group whose largest number of species is
hunted in the region, totaling 94 species (58% of the total),
distributed in 27 families, of which Thraupidae is the most
representative (23 species). Most bird species (n = 59 spe-
cies) are captured for use as pets, especially species in the
Thraupidae family. The characteristics of birds considered
relevant for selecting for use as pets mainly include song/
sound and feather color. This same situation occurs in other
locations in Brazil, where birds represent the main group of
wild animals that are targeted for use as pets (Alves et  al.
2010b, 2013b; Licarião et al. 2013; Nascimento et al. 2015).
This popularity of pet birds fuels a clandestine trade that
involves at least 65 of the species recorded in this chapter
(including all 23 recorded species of the Thraupidae family).
Other studies reinforce this finding, such as research on the
bird trade in state capital cities such as João Pessoa, where
20 species traded in local markets were recorded (Gama and
Sassi 2008), and in the metropolitan region of Recife, where
there are records of 106 species (Pereira and Brito 2005).
Part of the origin of commercialized birds is certainly associ-
ated with the Atlantic Forest fragments located near urban
areas, in addition to the animals that come from commercial
routes that involve different locations in all regions of Brazil
(Alves et al. 2013b).
A less representative portion of bird species (n = 25; 26%)
is used for food purposes, mainly from the Columbidae fam-
ily (11 species). Birds of this family are widely used as a
food resource by human populations in Northeast Brazil
(Alves et  al. 2013a; Bezerra et  al. 2011, 2012; Fernandes-­
Ferreira et al. 2012). In addition to columbids, tinamids and
cracids are also birds commonly used as a food resource in
areas where they coexist with humans. Similarly, Fernandes-­
15  Hunting and Uses of Terrestrial Vertebrates in the Northernmost Region in the Atlantic Forest in Brazil 259

Table 15.1  Game species and the respective motivations in the northernmost in the Atlantic Forest, Brazil
English name Local name IUCN CITES MMA Motivation Fonte
Family/scientific name (2022) (2021) F T M P C
Amphibia
Leptodactylidae
Leptodactylus Jia LC X Barbosa (2019)
macrosternum Miranda-­
Ribeiro, 1926
Leptodactylus Jia LC X Barbosa (2019)
troglodytes Lutz, 1926
Leptodactylus vastus Jia-pimenta LC X Barbosa (2019)
Lutz, 1930
Ranidae
Lithobates palmipes Amazon River Frog Jia-verde LC X X Barbosa (2019)
(Spix, 1824)
Bufonidae
Rhinella jimi (Stevaux, Sapo-cururu LC X Barbosa (2019)
2002)
Aves
Accipitridae
Accipiter bicolor Bicolored Hawk Gavião LC X Barbosa (2019)
(Vieillot, 1817)
Buteo albonotatus Kaup, Zone-tailed Hawk Gavião-preto LC X Barbosa (2019)
1847
Buteogallus lacernulatus White-necked Hawk Gavião-­ VU VU X Barbosa (2019)
(Temminck, 1827) preguiça
Elanus leucurus White-tailed Kite Gavião-­ LC X X X Barbosa (2019)
(Vieillot, 1818) peneira
Rupornis magnirostris Roadside Hawk Gavião-carijó LC X Barbosa (2019)
(Gmelin, 1788)
Cardinalidae
Cyanoloxia brissonii Ultramarine Azulão LC X X Souza and Alves
(Lichtenstein, 1823) Grosbeak (2014) and Barbosa
(2019)
Charadriidae
Vanellus chilensis Southern Lapwing Quero-quero LC X Souza and Alves
(Molina, 1782) (2014) and Barbosa
(2019)
Columbidae
Claravis pretiosa Blue Ground-dove Rolinha-azul LC X Barbosa (2019)
(Ferrari-Perez, 1886)
Columbina minuta Plain-breasted Rolinha-­ LC X X Souza and Alves
(Linnaeus, 1766) Ground-dove cambuta (2014) and Barbosa
(2019)
Columbina passerina Common Rolinha-­ LC X Barbosa (2019)
(Linnaeus, 1758) Ground-dove cinzenta
Columbina picui Picui Dove Rolinha-­ LC X X Alves et al. (2017),
(Temminck, 1813) branca Souza and Alves
(2014), and Barbosa
(2019)
Columbina squammata Scaled Dove Rolinha-­ LC X Alves et al. (2017)
(R.Lesson, 1831) cascavel
Columbina talpacoti Ruddy Rolinha-­ LC X X Alves et al. (2017),
(Temminck, 1810) Ground-dove caldo-­de-­ Souza and Alves
feijão (2014), and Barbosa
(2019)
Geotrygon montana Ruddy Quail-dove Juriti-­ LC X X Barbosa (2019)
(Linnaeus, 1758) vermelha
(continued)
260 R. R. N. Alves et al.

Table 15.1 (continued)
English name Local name IUCN CITES MMA Motivation Fonte
Family/scientific name (2022) (2021) F T M P C
Leptotila rufaxilla Gray-fronted Dove Juriti LC X X Barbosa (2019)
(Richard & Bernard,
1792)
Leptotila verreauxi White-tipped Dove Juriti-pupu LC X X Souza and Alves
Bonaparte, 1855 (2014) and Barbosa
(2019)
Patagioenas cayennensis Pale-vented Pigeon Pomba-galega LC X Souza and Alves
Bonnaterre, 1792 (2014) and Barbosa
(2019)
Patagioenas speciosa Scaled Pigeon Pedrês LC X X Souza and Alves
(J.F.Gmelin, 1789) (2014) and Barbosa
(2019)
Cracidae
Ortalis guttata (Spix, Speckled Acauã LC X X Souza and Alves
1825) Chachalaca (2014) and Barbosa
(2019)
Penelope superciliaris Rusty-margined Jacu NT CR X X Souza and Alves
Temminck, 1815 Guan (2014) and Barbosa
(2019)
Falconidae
Caracara plancus Southern Caracara Carcará LC X Barbosa (2019)
(Miller, 1777)
Falco femoralis Aplomado Falcon Gavião-coleira LC II X Barbosa (2019)
Temminck, 1822
Herpetotheres Laughing Falcon Acauã LC II X X X Barbosa (2019)
cachinnans (Linnaeus,
1758)
Micrastur ruficollis Barred Caburé LC II X Barbosa (2019)
(Vieillot, 1817) Forest-falcon
Fringillidae
Euphonia chlorotica Purple-throated Vim-vim LC X X Souza and Alves
(Linnaeus, 1766) Euphonia (2014) and Barbosa
(2019)
Euphonia violacea Violaceous Gaturão-de-­ LC X X Barbosa (2019)
(Linnaeus, 1758) Euphonia bananeira
Furnariidae
Xenops minutus White-throated Bico-virado LC X X Barbosa (2019)
(Sparrman, 1788) Xenops
Icteridae
Agelaioides badius Grayish Baywing Asa-de-telha LC X X Barbosa (2019)
(Vieillot, 1819)
Icterus jamacaii Campo Troupial Concriz LC X X Souza and Alves
(Gmelin, 1788) (2014) and Barbosa
(2019)
Icterus pyrrhopterus Variable Oriole Xexeu LC X X Souza and Alves
(Vieillot, 1819) (2014) and Barbosa
(2019)
Leistes militaris Red-breasted Xexeu-escuro LC X X Barbosa (2019)
(Linnaeus, 1758) Blackbird
Odontophoridae
Odontophorus capueira Spot-winged Capoeira LC X X X Barbosa (2019)
(Spix, 1825) Wood-quail
Parulidae
Basileuterus culicivorus Stripe-crowned Sebinho LC X X Barbosa (2019)
(Deppe, 1830) Warbler
Myiothlypis flaveola Flavescent Warbler Canário-do-­ LC X X Barbosa (2019)
(Baird, 1865) mato
(continued)
15  Hunting and Uses of Terrestrial Vertebrates in the Northernmost Region in the Atlantic Forest in Brazil 261

Table 15.1 (continued)
English name Local name IUCN CITES MMA Motivation Fonte
Family/scientific name (2022) (2021) F T M P C
Passerellidae
Ammodramus humeralis Grassland Sparrow Tico-rato LC X X Barbosa (2019)
(Bosc, 1792)
Arremon taciturnus Pectoral Sparrow Salta-caminho LC X X Barbosa (2019)
(Hermann, 1783)
Zonotrichia capensis Rufous-collared Tico-tico LC X X Souza and Alves
(Muller, 1776) Sparrow (2014) and Barbosa
(2019)
Pipridae
Ceratopipra rubrocapilla Cabeça-­ LC X X Barbosa (2019)
Temminck, 1821 vermelha
Chiroxiphia pareola Blue-backed Padre LC X X Barbosa (2019)
(Linnaeus, 1766) Manakin
Polioptilidae
Polioptila plumbea Tropical Bate-rabo LC X X Barbosa (2019)
(Gmelin, 1788) Gnatcatcher
Psittacidae
Amazona amazonica Orange-winged Papagaio LC II X X X Barbosa (2019)
(Linnaeus, 1766) Amazon
Forpus xanthopterygius Blue-winged Tapacu LC II X X Barbosa (2019)
(Taczanowski, 1883) Parrotlet
Touit surdus (Kuhl, Golden-tailed Perequito-do-­ VU II VU X X Barbosa (2019)
1820) Parrotlet mato
Rallidae
Aramides cajaneus Gray-cowled Saracura LC X Souza and Alves
(Statius Muller, 1776) Wood-rail (2014) and Barbosa
(2019)
Gallinula chloropus Common Moorhen Galinha-­ LC X Souza and Alves
(Linnaeus, 1758) d’água (2014) and Barbosa
(2019)
Thamnophilidae
Formicivora rufa (Wied, Rusty-backed Papa-formiga LC X X Barbosa (2019)
1831) Antwren
Herpsilochmus pileatus Bahia Antwren Chorozinho VU VU X X Barbosa (2019)
(Lichtenstein, 1823)
Taraba major (Vieillot, Great Antshrike Chorró-boi LC X X Barbosa (2019)
1816)
Thamnophilus punctatus Northern Slaty Chorró LC X X Barbosa (2019)
(Shaw, 1809) Antshrike
Thamnophilus torquatus Rufous-winged Choquinha LC X X Barbosa (2019)
Swainson, 1825 Antshrike
Thraupidae
Coereba flaveola Bananaquit Chupa-lima LC X X Barbosa (2019)
(Linnaeus, 1758)
Cyanerpes cyaneus Red-legged Azulinho LC X X Barbosa (2019)
(Linnaeus, 1766) Honeycreeper
Dacnis cayana Blue Dacnis Verdinho LC X X Barbosa (2019)
(Linnaeus, 1766)
Emberizoides herbicola Wedge-tailed Canário-do-­ LC X X Barbosa (2019)
(Vieillot, 1817) Grass-finch campo
Loriotus cristatus Flame-crested Tié-galo LC X X Barbosa (2019)
(Linnaeus, 1766) Tanager
Nemosia pileata Hooded Tanager Azedinho LC X X Barbosa (2019)
(Boddaert, 1783)
(continued)
262 R. R. N. Alves et al.

Table 15.1 (continued)
English name Local name IUCN CITES MMA Motivation Fonte
Family/scientific name (2022) (2021) F T M P C
Paroaria dominicana Red-cowled Galo-de-­ LC X X Souza and Alves
(Linnaeus,1758) Cardinal campina (2014) and Barbosa
(2019)
Ramphocelus bresilius Brazilian Tanager Sangue-de-boi LC X X Barbosa (2019)
(Linnaeus, 1766)
Saltator maximus Buff-throated Trinca-ferro LC X X Barbosa (2019)
(Muller, 1776) Saltator
Schistochlamys Black-faced Sanhaçu-­ LC X X Barbosa (2019)
melanopis (Latham, Tanager coleira
1790)
Sicalis flaveola Saffron Finch Canário-da-­ LC X X Souza and Alves
(Linnaeus, 1766) terra (2014) and Barbosa
(2019)
Sporophila albogularis White-throated Golado LC X X Barbosa (2019)
(Spix, 1825) Seedeater
Sporophila angolensis Chestnut-bellied Curió LC X X Souza and Alves
(Linnaeus, 1766) Seed-Finch (2014) and Barbosa
(2019)
Sporophila bouvreuil Copper Seedeater Caboclinho LC X X Souza and Alves
(Muller, 1776) (2014) and Barbosa
(2019)
Sporophila leucoptera White-bellied Chorão LC X X Souza and Alves
(Vieillot, 1817) Seedeater (2014) and Barbosa
(2019)
Sporophila lineola Lined Seedeater Bigode LC X X Barbosa (2019)
(Linnaeus, 1758)
Sporophila nigricollis Yellow-bellied LC X X Souza and Alves
(Vieillot, 1823) Seedeater (2014) and Barbosa
(2019)
Tachyphonus rufus White-lined Tanager Tié-preto LC X X Barbosa (2019)
(Boddaert, 1783)
Tangara cayana Burnished-buff Sanhaçu-­ LC X X Barbosa (2019)
(Linnaeus, 1766) Tanager caboclo
Tangara palmarum Palm Tanager Sanhaçu-verde LC X X Barbosa (2019)
(Wied, 1821)
Tangara sayaca Sayaca Tanager Sanhaçu-­ LC X X Souza and Alves
(Linnaeus, 1766) cinzento (2014) and Barbosa
(2019)
Thlypopsis sordida Orange-headed Canário-sapé LC X X Barbosa (2019)
(D’Orbigny & Tanager
Lafresnaye, 1837)
Volatinia jacarina Blue-black Tiziu LC X X Barbosa (2019)
(Linnaeus, 1766) Grassquit
Tinamidae
Crypturellus noctivagus Yellow-legged Zabelê NT VU X X X Barbosa (2019)
(Wied, 1820) Tinamou
Crypturellus parvirostris Small-billed LC X X Souza and Alves
(Wagler, 1827) Tinamou (2014) and Barbosa
(2019)
Crypturellus soui Little Tinamou Nambu-sabiá LC X Barbosa (2019)
(Hermann, 1783)
Crypturellus tataupa Tataupa Tinamou Nambu-pé-­ LC X X Souza and Alves
(Temminck, 1815) roxo (2014) and Barbosa
(2019)
Nothura maculosa Spotted Nothura Codorniz LC X X Souza and Alves
(Temminck, 1815) (2014) and Barbosa
(2019)
(continued)
15  Hunting and Uses of Terrestrial Vertebrates in the Northernmost Region in the Atlantic Forest in Brazil 263

Table 15.1 (continued)
English name Local name IUCN CITES MMA Motivation Fonte
Family/scientific name (2022) (2021) F T M P C
Rhynchotus rufescens Red-winged Nambu-apê LC X Barbosa (2019)
(Temminck, 1815) Tinamou
Tityridae
Pachyramphus White-winged Caneleiro LC X X Barbosa (2019)
polychopterus (Vieillot, Becard
1818)
Trochilidae
Eupetomena macroura Swallow-tailed Beija-flor-­ LC II X Barbosa (2019)
(Gmelin, 1788) Hummingbird tesoura
Florisuga fusca (Vieillot, Black Jacobin Beija-flor-­ LC II X Barbosa (2019)
1817) preto
Troglodytidae
Cantorchilus longirostris Long-billed Wren Rouxinol LC X X Barbosa (2019)
(Vieillot, 1819)
Pheugopedius Moustached Wren Pai-avô LC X X Barbosa (2019)
genibarbis (Swainson,
1838)
Trogonidae
Trogon curucui Blue-crowned Perua-choca LC X X Barbosa (2019)
Linnaeus, 1766 Trogon
Turdidae
Turdus leucomelas Pale-breasted Sabiá-cinzenta LC X X Barbosa (2019)
Vieillot, 1818 Thrush
Turdus rufiventris Rufous-bellied Sabiá-­ LC X X Barbosa (2019)
Vieillot, 1818 Thrush laranjeira
Tyrannidae
Capsiempis flaveola Yellow Tyrannulet Sebinho LC X X Barbosa (2019)
(Lichtenstein, 1823)
Fluvicola nengeta Masked Lavandeira LC X Barbosa (2019)
(Linnaeus, 1766) Water-tyrant
Myiophobus fasciatus Bran-colored Caga-sebo LC X X Barbosa (2019)
(Muller, 1776) Flycatcher
Todirostrum cinereum Common Sibito LC X X Barbosa (2019)
(Linnaeus, 1766) Tody-flycatcher
Tytonidae
Tyto furcata (Temminck, American Barn Owl Rasga-­ LC II X X Barbosa (2019)
1827) mortalha
Vireonidae
Cyclarhis gujanensis Rufous-browed Pitiguari LC X X Barbosa (2019)
(Gmelin, 1789) Peppershrike
Hylophilus Gray-eyed Greenlet Vite-vite LC X X Barbosa (2019)
amaurocephalus
(Nordmann, 1835)
Mammalia
Atelidae
Alouatta belzebul Red-handed Howler Guariba VU II VU X Barbosa (2019)
(Linnaeus, 1766) Monkey
Bradypodidae
Bradypus variegatus Brown-throated Preguiça LC II X X X Alves et al. (2017),
Schinz, 1825 Sloth Souza and Alves
(2014), and Barbosa
(2019)
Callitrichidae
Callithrix jacchus Common Marmoset Sagui LC II X X X Souza and Alves
(Linnaeus, 1758) (2014) and Barbosa
(2019)
(continued)
264 R. R. N. Alves et al.

Table 15.1 (continued)
English name Local name IUCN CITES MMA Motivation Fonte
Family/scientific name (2022) (2021) F T M P C
Canidae
Cerdocyon thous Crab-eating Fox Raposa LC II X X Souza and Alves
(Linnaeus, 1766) (2014) and Barbosa
(2019)
Caviidae
Cavia aperea Erxleben, Brazilian Guinea Preá LC X Alves et al. (2017)
1777 Pig
Galea spixii (Wagler, Spix’s Yellow-­ Preá LC X Souza and Alves
1831) toothed Cavy (2014) and Barbosa
(2019)
Hydrochoerus Capybara Capivara LC X X X Souza and Alves
hydrochaeris (Linnaeus, (2014) and Barbosa
1766) (2019)
Chlamyphoridae
Cabassous unicinctus Southern Naked-­ Tatu-rabo-­ LC X X Souza and Alves
(Linnaeus, 1758) tailed Armadillo mole (2014) and Barbosa
(2019)
Euphractus sexcinctus Yellow Armadillo Tatu-peba LC X X X X Alves et al. (2017),
(Linnaeus, 1758) Souza and Alves
(2014), and Barbosa
(2019)
Cricetidae
Oecomys catherinae Rato-do-mato LC X X Barbosa (2019)
Thomas, 1909
Cuniculidae
Cuniculus paca Agouti Paca LC X X Souza and Alves
(Linnaeus, 1766) (2014) and Barbosa
(2019)
Cyclopedidae
Cyclopes didactylus Silky Anteater Tamanduí LC X X Barbosa (2019)
(Linnaeus, 1758)
Dasypodidae
Dasypus novemcinctus Nine-banded Tatu-­ LC X X X Alves et al. (2017),
Linnaeus, 1758 Armadillo verdadeiro Souza and Alves
(2014), and Barbosa
(2019)
Dasypus septemcinctus Brazilian Lesser Tatu-mirim LC X X Souza and Alves
Linnaeus, 1758 Long-nosed (2014) and Barbosa
Armadillo (2019)
Dasyproctidae
Dasyprocta azarae Agouti Cutia DD X Alves et al. (2017)
Lichtenstein, 1823
Dasyprocta iacki Feijó & Cutia DD X X Barbosa (2019)
Langguth, 2013
Dasyprocta Black-rumped Cutia LC X Souza and Alves
prymnolopha Wagler, agouti (2014)
1831
Didelphidae
Caluromys philander Bare-tailed Woolly Cuíca-lanosa LC X Barbosa (2019)
Linnaeus, 1758 Opossum
Didelphis albiventris White-eared Timbu LC X X Alves et al. (2017),
Lund, 1840 Opossum Souza and Alves
(2014), and Barbosa
(2019)
Didelphis marsupialis Common Opossum Timbu LC X X Barbosa (2019)
Linnaeus, 1758
(continued)
15  Hunting and Uses of Terrestrial Vertebrates in the Northernmost Region in the Atlantic Forest in Brazil 265

Table 15.1 (continued)
English name Local name IUCN CITES MMA Motivation Fonte
Family/scientific name (2022) (2021) F T M P C
Marmosa demerarae Woolly Mouse Cuíca LC X Barbosa (2019)
(Thomas, 1905) Opossum
Marmosa murina Linnaeus’s Mouse Cuíca LC X Barbosa (2019)
Linnaeus, 1758 Opossum
Erethizontidae
Coendou prehensilis Brazilian Porcupine Porco-espinho LC X X Alves et al. (2017),
(Linnaeus, 1758) Souza and Alves
(2014), and Barbosa
(2019)
Felidae
Leopardus tigrinus Northern Tiger Cat Gato-do-mato VU I EN X X Souza and Alves
(Schreber, 1775) (2014) and Barbosa
(2019)
Leopardus wiedii Margay Gato-maracajá NT I VU X Alves et al. (2017)
(Schinz, 1821)
Puma yagouaroundi Jaguarundi Oncinha LC II VU X X Souza and Alves
(É.Geoffroy Saint-­ (2014) and Barbosa
Hilaire, 1803) (2019)
Leporidae
Sylvilagus brasiliensis Tapeti Coelho EN X X X Souza and Alves
(Linnaeus, 1758) (2014) and Barbosa
(2019)
Mustelidae
Eira barbara (Linnaeus, Tayra Irara LC X Souza and Alves
1758) (2014) and Barbosa
(2019)
Galictis vittata Greater Grison Furão LC X X Barbosa, 2019
(Schreber, 1776)
Lontra longicaudis Neotropical Otter Lontra NT I X Souza and Alves
(Olfers, 1818) (2014) and Barbosa
(2019)
Myrmecophagidae
Tamandua tetradactyla Southern Tamandua Tamanduá LC X X Alves et al. (2017),
(Linnaeus, 1758) Souza and Alves
(2014), and Barbosa
(2019)
Phyllostomidae
Carollia perspicillata Seba’s Short-tailed Morcego LC X X Barbosa (2019)
(Linnaeus, 1758) Ba
Procyonidae
Nasua nasua (Linnaeus, South American Quati LC X X Souza and Alves
1766) Coati (2014) and Barbosa
(2019)
Procyon cancrivorus Crab-eating Guaxinim LC X X X Souza and Alves
(G. Cuvier, 1798) Raccoon (2014) and Barbosa
(2019)
Sciuridae
Guerlinguetus alphonsei Alphonse’s Squirrel Caxinguelê NE X X Souza and Alves
(Thomas, 1906) (2014) and Barbosa
(2019)
Reptilia
Alligatoridae
Caiman latirostris Broad-snouted Jacaré LC I X X X Alves et al. (2017),
(Daudin, 1801) Caiman Souza and Alves
(2014), and Barbosa
(2019)
(continued)
266 R. R. N. Alves et al.

Table 15.1 (continued)
English name Local name IUCN CITES MMA Motivation Fonte
Family/scientific name (2022) (2021) F T M P C
Paleosuchus palpebrosus Dwarf Caiman Jacaré LC X X Alves et al. (2017)
(Cuvier, 1807) and Barbosa (2019)
Boidae
Boa constrictor Red-tailed Boa Jiboia LC II X X X Alves et al. (2017)
Linnaeus, 1758 and Barbosa (2019)
Epicrates assisi Jiboia LC X X Souza and Alves
Machado, 1945 (2014) and Barbosa
(2019)
Chelidae
Mesoclemmys Cágado NE II X X Barbosa (2019)
tuberculata
(Luederwaldt, 1926)
Phrynops geoffroanus Cágado-de-­ NE II X X Barbosa (2019)
(Schweigger, 1812) barbicha
Colubridae
Chironius exoletus Cobra-verde NE X Barbosa (2019)
(Linnaeus, 1758)
Drymarchon corais Indigo Snake Papa-pinto LC X Souza and Alves
(Boie, 1827) (2014) and Barbosa
(2019)
Drymoluber dichrous Cobra-rasteira NE X Barbosa (2019)
(Peters, 1863)
Oxybelis aeneus Brown Vinesnake Cobra-cipó LC X Souza and Alves
(Wagler, 1824) (2014) and Barbosa
(2019)
Spilotes pullatus Chicken Snake Caninana LC X Souza and Alves
Linnaeus, 1758 (2014) and Barbosa
(2019)
Tantilla melanocephala Black-headed Snake Cobra-de-­ LC X Souza and Alves
(Linnaeus, 1758) areia (2014) and Barbosa
(2019)
Xenodon merremii Boipeva LC X Barbosa (2019)
(Wagler, 1824)
Dipsadidae
Apostolepis cearensis Gomes’ Burrowing Cabeça-de-­ LC X Barbosa, 2019
Gomes, 1915 Snake coral
Erythrolamprus viridis Crown Ground Cobra-verde LC X Souza and Alves
(Günther, 1862) Snake (2014) and Barbosa
(2019)
Oxyrhopus trigeminus Brazilian False Falsa-coral LC X Souza and Alves
Bibron & Duméril, 1854 Coral Snake (2014) and Barbosa
(2019)
Philodryas nattereri Corre-campo LC X Souza and Alves
Steindachner, 1870 (2014) and Barbosa
(2019)
Sibon nebulatus Cloudy Snail-eating Dormideira LC X Barbosa (2019)
(Linnaeus, 1758) Snake
Elapidae
Micrurus ibiboboca Caatinga Coral Coral DD X Souza and Alves
(Merrem, 1820) Snake (2014) and Barbosa
(2019)
Iguanidae
Iguana iguana Common Green Camaleão LC II X X X Alves et al. (2017),
(Linnaeus, 1758) Iguana Souza and Alves
(2014), and Barbosa
(2019)
Scincidae
(continued)
15  Hunting and Uses of Terrestrial Vertebrates in the Northernmost Region in the Atlantic Forest in Brazil 267

Table 15.1 (continued)
English name Local name IUCN CITES MMA Motivation Fonte
Family/scientific name (2022) (2021) F T M P C
Psychosaura Hoge’s Mabuya Calango-cobra LC X Barbosa (2019)
macrorhyncha (Hoge,
1946)
Teiidae
Ameiva ameiva Giant Ameiva Bico-doce LC X Barbosa (2019)
(Linnaeus, 1758)
Salvator merianae Black-and-white Teju LC X X X Alves et al. (2017),
(Duméril & Bibron, Tegu Souza and Alves
1839) (2014), and Barbosa
(2019)
Testudinidae
Chelonoidis carbonarius Jabuti NE II X X X X Barbosa (2019)
(Spix, 1824)
Typhlopidae
Amerotyphlops Pernambuco Worm Cobra-de-­ LC VU X Barbosa (2019)
paucisquamus (Dixon, Snake duas-cabeças
1979)
Viperidae
Bothrops erythromelas Caatinga Lancehead Jararaca LC X Souza and Alves
Amaral, 1923 (2014)
Bothrops leucurus Whitetail Jararaca LC X Barbosa (2019)
Wagler, 1824 Lancehead
Crotalus durissus Cascabel Cascavel LC X X Alves et al. (2017),
Linnaeus, 1758 Rattlesnake Souza and Alves
(2014), and Barbosa
(2019)
Conservation status (IUCN and MMA): NE not evaluated, DD data deficient, LC least concern, NT near threatened, VU vulnerable, EN endan-
gered, CR critically endangered. CITES: Use: F food, T trade, M traditional medicine, P pet, C conflict. CITES: (I) Appendix I – species in serious
threat of extinction; (II) Appendix II – species vulnerable to exploitation whose trade must be controlled; (III) Appendix III – protected species in
at least one country

Ferreira et al. (2012), Teixeira et al. (2014) and Loss et al.
(2014) also evidenced a high preference for birds of these
families as a trophic resource in the Brazilian semiarid
region, where they still occur in more preserved places.
Cracids also suffer high hunting pressure in other regions of
Brazil, such as the Amazon region (Amaral 2009; Barros
et al. 2011), in other areas of the Atlantic Forest (Chiarello
2000) and in the Pantanal (Oliveira Júnior and Sato 2006),
and in other Latin American countries (Redford and Robinson
1987; Begazo and Bodmer 1998; Yahuarcani et  al. 2009;
Santos-Fita et al. 2012). This is one of the main reasons why
many species of the group appear on endangered species lists
(IUCN 2022; MMA 2021), corresponding to one of the most
hunted families throughout the Neotropics (Brooks and
Fuller 2006). The medicinal use of birds has also been
recorded in the region and involves at least 15 species. In this
case, the whole animal, its parts, and/or products may be
used to prepare home remedies, which are used to treat vari-
ous diseases, constituting a similar situation that occurs in
several locations in Brazil and in the world, wherein prod-
ucts obtained from birds are used in their traditional medical
systems (Alves and Rosa 2013; Alves et al. 2007a; Bezerra
et al. 2013; Williams et al. 2013).
There are records of ethnozoological interactions between
local residents with at least 35 species of mammals; this situ-
ation is not surprising considering that mammals are used for
different purposes by human populations or are the target of
conflicting relationships, which motivates their capture or
slaughter (Hanazaki et  al. 2009; Lopes and Ferrari 2000;
Ojasti 1984; Torres et  al. 2009). The data compiled in our
research show that at least 31 species of mammals are used
as a protein source. Following a trend similar to that recorded
in different Neotropical biomes, mammals represent the pre-
ferred taxonomic group with regard to game species hunted
for food (Mena et  al. 2000; Monroy-Vilchis et  al. 2008;
Ojasti 2000; Robinson and Redford 1991; Robinson et  al.
1999; Silvius et  al. 2004). This preference is clearly influ-
enced by the larger size of mammals (in relation to other
terrestrial vertebrates), which implies a greater return in bio-
mass for hunters (Alvard et  al. 1997; Alves et  al. 2009b;
Mena et al. 2000; Peres and Nascimento 2006).
It should be noted that there has been a recognized popu-
lation decline of several species of medium and large mam-
mals in the Atlantic Forest areas of Brazil, which historically
were important targets for local hunters, but are currently no
longer available in abundance in most of what remains of the
268
Fig. 15.1  Summary of the number of hunted species registered for
northernmost in the Atlantic Forest, Brazil, the motivations for their
hunting, and their conservation status. Use: F food, T trade, M tradi-
tional medicine, P pet, C conflict. Conservation status (IUCN and
MMA): NE not evaluated; DD data deficient, LC least concern, NT near
biome (Galetti et al. 2021). As a result, local hunters tend to
seek replacement species, causing pressure to shift to other
previously unpreferred species of mammals or taxa. Several
studies have shown that larger mammals are under more
intense hunting pressure, show high area requirements, and
have low abundance and population growth rates, which
make them extremely sensitive to habitat fragmentation and
alteration (Henle et al. 2004; Noss et al. 1996; Terborgh and
Winter 1980), which has been one of the main factors that
have impacted the Brazilian Atlantic Forest. Therefore, it is
expected that with the rarity of larger mammals, hunting will
be directed to medium and small-sized species.
Although the main motivation for hunting mammals is the
use of their meat, they provide a range of by-products that
can be used for several other purposes, including medicinal
use (at least 10 species) and pets (at least five species); these
numbers are certainly underestimated given the few studies
on the topic. The use of resources obtained from mammals,
in addition to meat, optimizes their use, so it is not surprising
that most mammal species compiled in this work have mul-
tiple uses. It should also be noted that there is a clandestine
trade in products derived from animals for various purposes,
which is certainly a stimulator for hunting in the region.
Some works carried out in markets and fairs in cities located
R. R. N. Alves et al.
threatened, VU vulnerable, EN endangered, CR critically endangered.
CITES: (I) Appendix I  – species in serious threat of extinction; (II)
Appendix II – species vulnerable to exploitation whose trade must be
controlled; (III) Appendix III – protected species in at least one country.
(This figure has been designed using resources from Flaticon.com)
in state capital cities such as João Pessoa, Recife, and Natal
attest that several products derived from mammals are mar-
keted for medicinal (Alves et al. 2008, 2009c, 2010c; Alves
and Rosa 2010; Ferreira et al. 2009) and/or religious/magic
purposes (Alves et al. 2012a), and certainly, this commerce
extends to other ends. Animals can be traded alive (for use
with pets), or they can provide products such as meat, skin,
bones, fat, and other parts, which are traded for food, medici-
nal, ornamental, or religious-magical purposes. Another
motivating factor for hunting is the conflicts between local
residents and some wild species, which are mainly motivated
by the predation of domestic animals by wild mammals
(especially carnivores) and the destruction of crops (herbi-
vores), especially rodents and some carnivores, like the crab-­
eating fox, Cerdocyon thous (Linnaeus, 1766), and the
crab-eating raccoon, Procyon cancrivorus (G. Cuvier, 1798).
There are various forms of interactions with local popula-
tions involving at least 28 species of reptiles. Such interac-
tions are associated with the utilitarian value of the species,
but they are related to conflicts (22 species), mainly in the
case of snakes. Few species of reptiles are used as food
(n  =  8), mainly being from the Chelidae and Alligatoridae
families (2 species each). However, a greater number of spe-
cies (n = 11) are used for medicinal purposes, which is in line
15  Hunting and Uses of Terrestrial Vertebrates in the Northernmost Region in the Atlantic Forest in Brazil
with ethnozoological research that has revealed that reptiles
are among the most used animals in traditional Brazilian
medicine (Alves 2009; Alves and Alves 2011; Alves et  al.
2007a, 2010d; Oliveira et al. 2010; Souto et al. 2011). Among
the species of medicinal reptiles used in the region consid-
ered herein, we highlight the black-and-white tegu, Salvator
merianae Duméril & Bibron, 1839; the cascabel rattlesnake,
Crotalus durissus Linnaeus, 1758; the common green iguana,
Iguana iguana (Linnaeus, 1758); and the red-tailed boa, Boa
constrictor Linnaeus, 1758, which are used in several other
locations in Brazil by traditional communities and sold in
public markets in several cities (Alves et  al. 2007b, 2008;
Alves and Pereira-Filho 2007; Alves and Rosa 2007, 2010;
Ferreira et al. 2009, 2012).
Although many species of reptiles in Brazil have utility
value, a greater number of species are the target of conflicts,
being slaughtered because they are considered harmful and
pose a risk to people and domestic animals (Alves et  al.
2009a, 2012b, 2019). Therefore, it is not surprising that of
the 28 species recorded in our study, 22 are involved in con-
flicting relationships with the local population, especially
snakes, mainly from the Colubridae family (7 species). It is
noteworthy that practically all snakes, regardless of whether
or not they are venomous, are generally killed in eventual
encounters with people, so the number of species associated
with conflicts is certainly even greater considering that all
snakes that occur in the region tend to be the target of conflict
with the local human population. The consumption of
amphibians involves a few species (n  =  5), being used for
food purposes or in traditional medicine, mainly species of
the Leptodactylidae family. The consumption of wild
amphibians for food in Brazil is very occasional and gener-
ally involves few species.
15.3 Conservation Implications and Final
Considerations
Of the 162 game species recorded for the Atlantic Forest
areas north of São Francisco, 156 are included in the lists of
threatened species, with 94 bird species, 34 mammal species,
23 reptile species, and 5 amphibian species, distributed in the
categories of least concern, near threatened, vulnerable,
endangered, and data deficient (IUCN 2022; MMA 2021).
Of these, 7 species are in categories of greatest conservation
concern (vulnerable, endangered, or critically endangered;
Fig. 15.2), and hunting, regardless of motivation, is one of
the factors that have impacted all of their populations.
Hunting in the Atlantic Forest area north of São Francisco,
as in other locations in Brazil, is influenced by a series of
biological, socioeconomic, political, and institutional factors
(Alves et al. 2018; Castilho et al. 2018). Understanding these
factors behind the motivations for hunting is crucial to pro-
269
mote behavioral changes, with conservation being the major
objective (St John et al. 2012; Nuno et al. 2013). However,
research on hunting, especially illegal hunting, is extremely
difficult (Ashayeri and Newing 2012), presenting several
challenges, and the data is subjected to bias (Keane et  al.
2008). The reasons that stimulate hunting of some species
are multiple, even motivating clandestine commercializa-
tion, particularly species of birds used as pets, constituting
an additional factor of pressure since the demand on them
increases. The trade in animals is common in urban areas,
occurring clandestinely in markets and fairs or through
orders between hunters and consumers negotiated over the
internet. Recent ethnozoological research has shown that the
trade in wild animals that historically took place in markets
and fairs has changed in pattern, with many commercializa-
tion activities taking place on the internet (Alves et al. 2019;
Borges et al. 2021a, b; Magalhães and São Pedro 2012). This
situation has intensified and is worrying, especially consider-
ing that it is a way of circumventing possible inspection
operations by environmental agencies. It is noteworthy that
markets in medium and large urban centers are still points of
an active trade in live wild animals and products from dead
animals in the Northeast of Brazil; however, the internet has
potentiated this trade, and therefore, this new route must be
carefully considered in the strategies for monitoring and
inhibiting illegal wildlife trade.
Hunting in the region generally shows similar patterns to
those recorded in other regions of Brazil. Mammalian fauna
is the most representative group in use for food; birds stand
out when game is intended for use as pets, and reptiles, espe-
cially snakes, are the animals most affected by hunting moti-
vated by conflicts with humans. The overlapping motivations
for hunting represent another aspect to be considered from a
conservationist perspective. In view of this scenario, mea-
sures that seek the conservation of game fauna are urgent,
especially considering the ineffectiveness of Brazilian legis-
lation that regulates hunting, capturing, and commercializa-
tion of wild fauna. The conservation of faunal resources is a
challenge that must be faced from social, economic, ecologi-
cal, and cultural perspectives. From a biological point of
view, the list of hunted species is extensive and indicates the
urgency of ethnozoological studies and studies on the biol-
ogy and ecology of the most used species in order to deter-
mine the pressures and influences that usage and
commercialization exert on their natural populations. From
an ecological and conservationist perspective, these activi-
ties become a worrying aspect regarding the conservation of
biodiversity when carried out without any kind of manage-
ment and may generate changes in the composition of the
animal community, mainly triggered by its selective charac-
ter (Redford 1997). Lastly, the exploitation of fauna must be
considered within the larger context of degradation and habi-
tat loss, in addition to the other forms of exploitation, which
270 R. R. N. Alves et al.

Fig. 15.2  Species in categories of concern for conservation and their uses that motivate hunting in the northernmost region in the Atlantic Forest,
Brazil. Conservation status: VU vulnerable, EN endangered, CR critically endangered
15  Hunting and Uses of Terrestrial Vertebrates in the Northernmost Region in the Atlantic Forest in Brazil 271

have contributed to the decline of these species that inhabit Alves RRN, Nogueira E, Araujo H et al (2010b) Bird-keeping in the
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 Index

A Endemism, 1, 8, 23, 34, 123, 134, 148, 170, 196, 229

Amphibian, 8, 87, 104, 124, 148–161, 170, 258, 269 Ethnobiology, 217
Animal conservation, 258 Ethnozoology, 2, 230
Animal uses, 230, 258, 268, 269 Extinction, 2, 5, 87, 117, 128, 135, 139, 141, 148, 154, 155, 185, 187,
Anthropogenic pressures, 72, 130 195, 197, 207, 218, 221–225, 252, 267, 268
Araneoidea, 106–109, 112, 115, 117
Areas of endemism, 86–90, 92, 95, 96, 105, 106, 114–116, 206
Atlantic Forest, 1, 7, 23, 33, 122, 133, 148, 170, 185, 229, 257 F
Atlantic rainforest, 148 Fishes, v, vi, 2, 133–144, 230–249, 252, 253
Freshwater fishes, 2, 134, 135, 137, 139, 140, 143, 144

B
Biodiversity, 1, 2, 8, 13, 14, 23, 24, 30, 34, 43, 48, 71, 85, 86, 96, 104, H
105, 122, 124, 130, 133, 140, 143, 148, 149, 179, 181, 185, Habitat fragmentation, 23, 155, 268
198, 210, 224, 257, 258, 269 Habitat loss, 15, 28, 30, 40, 56, 87, 128, 130, 140, 141, 144, 149, 187,
Biodiversity shortfalls, 2, 104, 111, 116, 117 199, 218, 221, 222, 224, 247, 269
Biogeography, v, 30, 34, 37–40, 71, 85, 90, 95, 105, 143, 170, 185, Herpetofauna, 155, 170
195, 196, 208–210, 222
Borborema plateau, 12, 48, 86, 87, 96, 106, 123, 135, 208
Brejos, 8, 9, 12, 20, 27, 30, 34, 35, 39, 42, 170 I
Brejos de Altitude, 2, 3, 8, 9, 11–12, 24, 26, 27, 34, 48–50, 58, 61, 62, Isoptera, 2, 23, 121, 123, 126
71, 87, 90, 96, 106, 109, 111, 115, 122–124, 126, 135, 153,
170, 172, 175, 176, 208
Bushmeat, 223 L
Landscape analysis, 13–14

C
Center, v, 8, 9, 14, 23, 28, 34, 37, 38, 43, 148, 151, 170, 171, 181, 195,
253, 269
Conservation, 2, 8, 24, 34, 124, 133, 148, 170, 186, 230, 258
Conservation status, 2, 7–20, 30, 40, 48, 49, 72, 134, 148, 149, 157,
161, 186, 197–199, 246, 247, 267, 268, 270
Conservation units, 14, 24, 28, 48, 109, 111, 116, 117, 130, 141–144,
156, 172, 179
Critically endangered species, 197
Crustaceans, 230, 249
D 259–268, 270
Density, 11, 12, 24, 25, 28, 40, 104, 105, 109, 111, 115, 116, 128, 129,
209, 212, 213, 219, 230, 257
Distribution records, 104, 115
Diversity, 2, 7, 27, 41, 123, 133, 148, 170, 185, 229, 257
E 201–225
Ecology, v, 2, 19, 40, 48, 96, 121–130, 143, 150, 170, 216, 217, 269
Endemic species, 1, 2, 8, 30, 37, 42, 48, 49, 72, 86, 87, 90, 92, 95,
105, 116, 133, 137, 148, 151, 153, 154, 156, 171, 176, 178,
179, 195, 196, 199, 207, 208
N
Neotropical region, 30, 34, 55, 59, 62, 68, 71, 106, 121, 122, 128, 178,
179
Nordestinos, 8–13, 20, 27, 48, 123, 208
Northeastern, v, vi, 2, 8, 9, 11, 29, 49, 52, 71, 105, 106, 133, 141, 143,
144, 170, 198, 218, 224, 248, 258
Northeastern Brazil, v, 8, 9, 11, 12, 15, 35, 49, 51, 53, 54, 56, 57, 60,
63, 66–68, 71, 105, 106, 112, 117, 140, 143, 144, 148, 155,
157–161, 201, 214, 215, 217, 248
Northern Atlantic Forest (NAF), 1–3, 9, 15–20, 34–39, 42,
43, 121–130, 133, 134, 176, 178, 181, 185–199,
P
Pernambuco Endemism, 195, 196
Pernambuco Endemism Center (PEC), 1, 2, 9, 23–30, 43, 48,
50, 53, 58, 66, 133, 148–161, 170–172, 175–180, 195, 196,
Pests, 34, 129–130
Pholcidae, 106–110, 112, 115, 117
Protected areas, v, 2, 3, 5, 14, 18–20, 24, 86, 134, 141–143, 149, 156,
179, 199, 208, 212, 213, 217, 221, 222, 224, 225

© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 275
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
276 Index

R S
Rain forest, 11, 23, 209 Scarabaeidae, 49, 50, 72
Restinga, 11, 13, 49, 50, 62, 63, 71, 72, 123, 142, 170, 172, 175, 218, Spatial analysis, 107
248
Richness, 2, 8, 11, 24, 25, 28–30, 34–38, 41, 42, 49, 50, 71, 86, 92, 96,
104–106, 108–116, 124, 126, 128, 130, 135, 138, 148–151, W
153, 154, 156, 170–181, 186–195, 207, 219, 223 Wildlife, 142, 170, 269