Influência de Mudanças Ambientais Sobre As Comunidades de Aves

UNIVERSIDADE ESTADUAL DE SANTA CRUZ
PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA E CONSERVAÇÃO DA

BIODIVERSIDADE
ÍCARO MENEZES PINTO
Influência de mudanças ambientais sobre as comunidades de aves e suas

interações ecológicas em paisagens fragmentadas
ILHÉUS - BAHIA
2020

Tese apresentada à Universidade Estadual de Santa Cruz,

para obtenção do título de doutor em Ecologia e
Conservação da Biodiversidade
Área de concentração: Ecologia e Conservação de

Comunidades
Orientador: Prof. Dr. José Carlos Morante-Filho

Co-orientadora: Profª. Drª. Deborah Faria
Co-orientadora: Profª. Drª. Eliana Cazetta
ILHÉUS - BAHIA
2020

_______________________________________________________________
Prof. Dr. José Carlos Morante Filho
UESC
(Orientador)
_______________________________________________________________
Prof. Dr. Anderson Saldanha Bueno
IFFar
(Avaliador)
_______________________________________________________________
Prof. Dr. Augusto João Piratelli
UFSCAR
(Avaliador)
_______________________________________________________________
Prof. Dr. Erich Arnold Fischer

UFMS
(Avaliador)
_______________________________________________________________
Profa. Dr.ª Erica Hasui
UNIFAL
(Avaliadora)
Ilhéus, 30/06/2020
“Eu sou apenas um rapaz latino-americano
Sem dinheiro no banco
Sem parentes importantes
E vindo do interior
Mas trago de cabeça uma canção do rádio
Em que um antigo compositor baiano me dizia
Tudo é divino, tudo é maravilhoso!”
Antônio Carlos Belchior
“Espécie de ave da família Pipridae. É encontrado na Bolívia, Brasil e Peru, conhecido
popularmente como cabeça-encarnada, uirapuru, irapuru, maria-lenço, patuqueira, dançarino-
de-cabeça-encarnada. Espécie que ocorre na Mata Atlântica de baixada em matas de tabuleiro e
na hiléia bahiana.”
Tomas Sigrist
AGRADECIMENTOS
Agradeço à Universidade Estadual de Santa Cruz (UESC), na qual me graduei bacharel em

Ciências Biológicas, pela estrutura física e excelentes profissionais da educação que auxiliaram
diretamente e indiretamente para a minha formação e realização deste trabalho. À Pró-Reitoria de
Pesquisa e Pós-Graduação da UESC (PROPP nº 00220.1100.1644/10-2018), Rufford Small Grants
for Nature Conservation (nº 22426-1) e REDE SISBIOTA (CNPq nº 563216/2010-7), pelo apoio
financeiro para realização das atividades de campo relacionadas à tese.
Ao Programa de Pós-Graduação em Ecologia e Conservação da Biodiversidade pela
oportunidade de cursar o doutorado e às secretárias Iky Anne Dias e Amábille Kruschewsky pela
amizade e apoio. À Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB) pela concessão
da bolsa de doutorado (nº 0525/2016). Ao Instituto Chico Mendes de Conservação da
Biodiversidade (ICMBio) e à Comissão de Ética no Uso dos Animais – CEUA/UESC pela emissão
das licenças de coleta.
Ao Laboratório de Ecologia Aplicada à Conservação (LEAC), no qual convivi com amigos
ao longo desses 4 anos compartilhando experiências, que com certeza foram essenciais à minha
formação acadêmica.
Agradeço também a Luiz Magnago, Jomar Gomes e Daniel Piotto pela ajuda na
identificação de algumas espécies da flora e também a Jacques Delabie, coordenador do laboratório
de Mirmecologia da Comissão Executiva do Plano de Lavoura Cacaueira - CEPLAC, por permitir
o acesso ao laboratório para identificação de sementes e a bióloga e grande amiga, Mariane Guedes,
por trabalhar com a morfotipagem das sementes. Também agradeço a Gil Reuss e Diogo Caribé
por ajudarem a mapear a área de estudo.
Aos amigos Adrielle Leal, Alesandro Souza, Albérico Queiroz, Fábio Soares, Júlia Perez e
Thamyrys Souza, que foram pessoas importantíssimas para a realização deste estudo.
Ao meu orientador Dr. José Carlos Morante-Filho, por toda orientação, correções,
esclarecimentos, apoio, paciência, por ter acreditado em mim em momentos difíceis que
influenciaram no andamento da tese e por ser parte essencial na minha formação profissional.
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Agradeço também as minhas co-orientadoras, Deborah Faria e Eliana Cazetta, por serem
sempre atenciosas, prestativas, sendo de grande importância na minha formação.
Agradeço também a Drª Carine Emer, por complementar todo arcabouço teórico, ajuda nas
análises e discussões sobre alguns capítulos da tese.
Por fim, agradeço a toda minha família e, em especial, minha amada mãe Ozânia Maria,
meu amado pai José Ferreira “In Memorian”, minha irmã Ingrid Menezes, minha esposa Amanda
Souza e minha filhinha Ágatha, que com muito carinho sempre me apoiaram e não mediram
esforços para que eu concluísse esta etapa da minha vida.
Resumo
A perda de florestas em todo o mundo tem um impacto negativo na biodiversidade global, pois
causa mudanças drásticas na estrutura das comunidades biológicas e suas interações ecológicas. A
perda e fragmentação de habitat mudam a composição e configuração das paisagens naturais e
podem atuar na diversidade das populações de espécies em diferentes escalas espaciais (ex. escala
local ou paisagem). Embora vários estudos tenham avaliado as respostas das comunidades
biológicas à perda e fragmentação de habitat, ainda não está claro como as espécies e suas
interações (ex. dispersão de sementes) podem ser afetadas em diferentes escalas espaciais. Nesse
contexto, esta tese tem como objetivo entender quais são os principais fatores ambientais em escala
local e paisagística que estruturam as comunidades de aves e suas interações. Especificamente,
estudei 20 fragmentos florestais imersos em duas regiões com diferentes tipos e intensidades de
uso do solo, uma com maior cobertura florestal e outra com baixa cobertura florestal, localizadas
na Mata Atlântica do sul do Estado da Bahia, Brasil. No primeiro capítulo, avaliei como
assembleias de aves de sub-bosque dependentes e não dependentes da floresta, bem como
frugívoros e insetívoros, respondem a alterações na quantidade de cobertura florestal, interior de
floresta, densidade de bordas e diferenças em isolamento entre fragmentos florestais em ambas
regiões. Também avaliei em escala local se métricas como número de árvores, diâmetro das árvores
(DAP > 5cm), número de plantas no sub-bosque, abertura de dossel e disponibilidade de frutos
afetam as assembleias de aves. As métricas locais também foram agrupadas em uma análise de
componentes principais, excluindo-se apenas a disponibilidade de frutos, assim utilizamos o
primeiro componente como um índice de complexidade da vegetação. Os resultados demonstram
que riqueza e abundância de aves do sub-bosque de maneira geral, e particularmente aves
dependentes da floresta, frugívoras e insetívoras, diminuem com a redução da cobertura florestal e
do interior da floresta, diminuindo também com o aumento do isolamento entre fragmentos de
floresta na paisagem. Localmente o número de frutos não afetou a riqueza de aves frugívoras, mas
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aves insetívoras foram mais abundantes em florestas com maior complexidade estrutural da
vegetação. No segundo capítulo, avaliei como as variáveis ambientais descritas acima afetam as
redes de interação ave-planta, especificamente o número de interações, links por espécie,
distribuição das interações (uniformidade) e modularidade. Os resultados demonstram um número
reduzido de interações ave-planta na região mais fragmentada e com menor cobertura florestal
como consequência da menor riqueza e abundância de espécies de aves nessa região, sem
alterações na estrutura das redes de interações. No terceiro capítulo, avaliei como diferenças nas
variáveis ambientais mensuradas acima afetam a diversidade beta (β) de espécies de aves, plantas
e interações. Os resultados demonstram que o aumento no isolamento entre remanescentes
florestais, na quantidade de pasto e no número de frutos ampliam a diversidade beta (β) de aves em
paisagens mais florestadas e fragmentos menos isolados em paisagens menos florestadas possuem
maior diversidade beta (β) de aves. Ao contrário de nossas previsões, a diversidade beta (β) de
plantas não foi afetada por nenhum preditor (local ou paisagístico). A diversidade beta (β) de
interações aumentou em paisagens com remanescentes florestais menos isolados e com maior
número de árvores na região menos florestada. Por fim, esses resultados indicam que a diversidade
das assembleias de aves de sub-bosque e seus grupos ecológicos respondem de formas distintas a
mudanças em escala local ou paisagística e que suas interações são reduzidas em paisagens
altamente antropizadas.
Palavras-chave: Avifauna, fragmentação, florestas tropicais, interações ecológicas, perda de

habitat.
Abstract
Forest loss worldwide has a negative impact in global biodiversity as it causes drastic changes in
the structure of biological communities and their ecological interactions. Habitat loss and
fragmentation change the composition and configuration of natural landscapes and can act on the
diversity of species populations at different spatial scales (e.g., landscape or patch-scale). Although
a several studies have evaluated the responses of biological communities to habitat loss and
fragmentation, there is still not clear how species and their interactions (e.g., seed dispersal) can be
affected in different spatial scales. In this context, this thesis aims to understand what the main
environmental factors are in local or landscape-scale that structure bird communities and their
interactions (bird-plant). Specifically, I studied 20 forest sites, i.e., forest patches immersed in
landscapes (buffers) in two regions one a higher forest cover and other with low forest cover. Both
regions show with different types and intensity of land-use and they are located in the Brazilian
Atlantic Forest in southern Bahia State. In the first chapter, I evaluated how assemblages of forest-
dependent and non-forest understory birds, as well as frugivores and insectivores’ guilds respond
to changes in the amount of forest cover, forest interior (core area), edge density and inter-patch
isolation measured by cohesion index. Also, I evaluated in local scale whether metrics such as
number of trees, DBH of trees (> 5cm), number of understory plants, canopy openness and fruit
availability can be affected bird assemblages. Local metrics were also grouped in a principal
component analysis, excluding only the availability of fruits, so I used the first component as an
index of vegetation complexity. The results shown that the richness and abundance of understory
birds, forest-dependent, frugivorous, and insectivorous birds decrease with reduced forest cover
and the interior of the forests, also decreasing with a greater isolation between fragments in the
landscape. Regarding local predictors, the number of fruits did not affect the richness or abundance
of frugivorous birds. However, insectivorous birds were more abundant in forests with greater
structural vegetation complexity. In the second chapter, I assessed how the environmental
predictors described above affect the bird-plant interaction networks, specifically the number of
interactions, links per species, interaction evenness and modularity. The results demonstrated a
lower number of bird-plant interactions in the most deforested region as a consequence of the lower
richness and abundance of understory bird species in this region, without changes in the bird-plant
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network structure. In the third chapter, I evaluated how differences in the environmental predictors
measured above affect the β-diversity of birds, plants species and interactions. The results
demonstrated that increases in inter-patch isolation, increases in the amount of pasture and number
of fruits increases the β-diversity of birds in landscapes whit a higher forest cover and less isolated
patches immersed in landscapes with a low forest cover have greater β-diversity of birds. In contrast
to predictions, plant β-diversity was not affected by any predictor local or landscape-scale. The β-
diversity of interactions increased in landscapes with less isolated forest patches and with a greater
number of trees in more deforested region. Finally, these results indicated that the diversity of
understory bird assemblages and their ecological groups (frugivores and insectivores) respond in
different ways to changes on a local or landscape-scale and that their interactions are reduced by
in a more deforested region.
Keywords: Avifauna, biodiversity, ecological interactions, habitat fragmentation, habitat loss,

tropical forests.
Sumário
Resumo ............................................................................................................................................. I
Abstract ............................................................................................................................................. I
INTRODUÇÃO GERAL ................................................................................................................ 3
Ameaças a biodiversidade em paisagens modificadas pelo homem ............................................... 3
O papel da diversidade de espécies e de seus traços funcionais dentro das comunidades biológicas
......................................................................................................................................................... 4
A importância das aves para a funcionalidade dos ecossistemas .................................................... 6
Perda e fragmentação do habitat: ameaças à Mata Atlântica .......................................................... 8
OBJETIVOS .................................................................................................................................. 11
REFERÊNCIAS BIBLIOGRÁFICAS .......................................................................................... 13
Capítulo I ....................................................................................................................................... 22
Ecological drivers of understory bird assemblages in tropical forest patches: a multi-scale approach
....................................................................................................................................................... 23
Abstract .......................................................................................................................................... 24
1. INTRODUCTION ..................................................................................................................... 25
2. MATERIALS AND METHODS .............................................................................................. 28
3. RESULTS .................................................................................................................................. 34
4. DISCUSSION............................................................................................................................ 37
5. ACKNOWLEDGEMENTS ...................................................................................................... 40
6. REFERENCES .......................................................................................................................... 41
Supporting Information ................................................................................................................. 50
Capítulo II ..................................................................................................................................... 68
Tropical forest loss simplifies bird-plant networks in human-modified landscapes ..................... 69
Abstract .......................................................................................................................................... 70
1. INTRODUCTION ..................................................................................................................... 71
2. MATERIALS AND METHODS .............................................................................................. 74
3. RESULTS .................................................................................................................................. 82
4. DISCUSSION............................................................................................................................ 89
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5. ACKNOWLEDGEMENTS ...................................................................................................... 94
6. REFERENCES .......................................................................................................................... 94
Supporting Information ............................................................................................................... 103
Capítulo III .................................................................................................................................. 119
Environmental predictors of beta diversity of bird-plant networks in the threatened Brazilian
Atlantic forest .............................................................................................................................. 120
Abstract ........................................................................................................................................ 121
1.INTRODUCTION .................................................................................................................... 122
2. MATERIALS AND METHODS ............................................................................................ 125
3. RESULTS ................................................................................................................................ 132
4. DISCUSSION.......................................................................................................................... 136
5. REFERENCES ........................................................................................................................ 139
Supporting information ............................................................................................................... 147
CONSIDERAÇÕES FINAIS ...................................................................................................... 156
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INTRODUÇÃO GERAL
Ameaças a biodiversidade em paisagens modificadas pelo homem
A biodiversidade global refere-se à variedade de vida e seus níveis de organização
no planeta Terra. Inclui, além de espécies, a variabilidade genética intra e inter-específica,
a diversidade de comunidades biológicas, habitats e ecossistemas formados pelos
organismos (CARDINALE et al., 2012). Igualmente, as interações ecológicas realizadas
pelos organismos nos ecossistemas e funções decorrentes dessas interações, como
dispersão de sementes, polinização e predação, também fazem parte da biodiversidade
(COSTANZA et al., 1997; KREMEN, 2005). Portanto, a biodiversidade engloba em sua
totalidade todos os componentes vivos e não vivos que interagem entre si formando os
ecossistemas e em maior escala, a biosfera (MACE et al., 2012).
Atualmente, grande parte dessa biodiversidade é ameaçada pelas atividades
humanas que alteram as condições físicas dos ecossistemas naturais e consequentemente
ocasionam declínios na riqueza e abundância das espécies, podendo levá-las à extinção
(KUEFFER & KAISER-BUNBURY, 2014; MCGILL et al., 2015). A extinção de
espécies é um evento natural. Estima-se que a meia-vida média de uma espécie está entre
10 a 100 milhões de anos e que 99% das espécies que já viveram na Terra atualmente
estão extintas (MILLENNIUM ECOSYSTEM ASSESSMENT, 2005; JOHNSON et al.,
2017). Entretanto, as atuais taxas de extinções de espécies encontram-se muito acima do
esperado, ocorrendo em um período extremamente curto, em níveis de 100 a 1000 vezes
maiores em relação às taxas de extinções naturais (CEBALLOS et al., 2015). Nas regiões
tropicais, que abrigam maior parte da biodiversidade do planeta, é estimado que 0,1% a
0,3% das espécies, e 0,8% das populações se extinguem a cada ano (BALMFORD et al.,
2003). Estudos evidenciaram que impactos antrópicos nos ecossistemas terrestres como
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a perda e fragmentação dos habitats (BARNOSKY et al., 2011; CEBALLOS et al., 2015),
agem em sinergia com outros fatores, como sobre-exploração de recursos naturais,
poluição, caça predatória, invasões biológicas e mudanças climáticas, reduzindo a
biodiversidade em diversas escalas espaciais (SALA et al., 2000; CARDOSO et al., 2004;
BUTCHART et al., 2010).
A interferência humana nos ecossistemas naturais tem sido historicamente
importante, moldando os padrões atuais de biodiversidade global (BENDER et al., 1998;
MURPHY & ROMANUK, 2014; SUPP & ERNEST, 2014). Dessa maneira, a drástica
redução da biodiversidade, especialmente em locais muito diversos é particularmente
preocupante (LAURANCE et al., 2012; PÜTTKER et al., 2020). Existe um consenso de
que a biodiversidade está diretamente relacionada às funções do ecossistema, sendo que
estas são distribuídas no espaço e tempo e determinam o quão um ecossistema é estável
a distúrbios externos (HOOPER et al., 2012; SCHLEUNING et al., 2015). Assim, tanto
a redução na riqueza de espécies, quanto alterações em suas abundâncias como
consequência direta e indireta de fatores antropogênicos, podem ser fortes ameaças ao
funcionamento do ecossistema e ao bem-estar humano (PEREIRA et al., 2010, HAGEN
et al., 2012).
O papel da diversidade de espécies e de seus traços funcionais dentro

das comunidades biológicas
Recentemente, diversos estudos se empenharam em avaliar como a perda e
fragmentação florestal influenciam na composição local de espécies e nas funções
desempenhadas por elas (FLYNN et al. 2009; BOYER & JETZ 2014). Especificamente,
avaliaram como a diversidade de espécies e de suas características fenotípicas (traços
funcionais) diretamente associadas a processos ecológicos desempenhados por elas na

5
comunidade, influenciam no “funcionamento das comunidades” (TILMAN 2001;
PETCHEY & GASTON 2002). Assim, descobriram que muitos grupos ecológicos são
redundantes funcionalmente, isto é, desempenham papéis semelhantes dentro de um
habitat ou ecossistema (ROSENFELD 2002). Por exemplo, aves nectarívoras (ex. beija-
flores) realizam a polinização das flores ao explorar um recurso alimentar, o néctar. Da
mesma maneira, abelhas ao coletarem o pólen das flores acabam às fecundando,
auxiliando no fluxo gênico e reprodução de inúmeras angiospermas (BLÜTHGEN &
KLEIN 2011). Espécies redundantes funcionalmente podem garantir a manutenção de
processos ecológicos como a polinização das flores e/ou dispersão de frutos (ROTHER
et al. 2016; KAISER-BUNBURY et al. 2017).
Entender como as comunidades biológicas se estruturam frente às mudanças
antrópicas em seus ecossistemas é uma tarefa difícil, pois inúmeros fatores influenciam a
sua organização, por exemplo, predação e competição (FOX 1987; SHIBUYA et al.
2011). Em 1975, Diamond propôs a existência de “regras de montagem” que atuam na
organização das comunidades. Assim, ele se propôs compreender como comunidades
distintas são formadas a partir de um mesmo pool de espécies, ou seja, um mesmo
conjunto de espécies. Em 1967, MacArthur e Levins proporam que a organização das
comunidades biológicas se daria pela limitação da similaridade entre espécies dentro da
comunidade. Nessa proposição, as espécies ocupariam nichos diferentes em um
ecossistema como uma forma de evitar competição por recursos (exclusão-competitiva)
como uma estratégia de sobrevivência. Nesse contexto, habitats estruturalmente mais
complexos possibilitariam uma maior diversificação no uso e exploração dos recursos
(especialização), promovendo assim, uma maior diversidade de espécies pela
sobreposição parcial de seus nichos (MACARTHUR & LEVINS 1967). Por outro lado,
habitats estruturalmente menos complexos, com limitações em requerimentos específicos

6
das espécies, atuariam como “filtros ambientais” limitando ou selecionando atributos
funcionais (KEDDY 1992). É sabido que a perda e fragmentação florestal pode atuar
como um filtro ambiental para muitas espécies sensíveis às mudanças em seu habitat
(CLAVEL et al. 2011; LÔBO et al. 2011). Em geral, à medida que os impactos
decorrentes da ocupação e uso do solo se intensificam, ocorre uma diminuição da
diversidade funcional (LALIBERTÉ et al. 2010; ROBERTO et al. 2017). Como
consequência, as interações ecológicas desempenhadas especificamente por tais espécies
também deixam de existir (HAGEN et al. 2012). Embora a riqueza de espécies dentro de
uma comunidade possa ser mantida pela proliferação de outras espécies adaptadas a
ambientes antrópicos (dinâmica compensatória; ver GONZALEZ & LOREAU, 2009), a
diversidade funcional tende a diminuir devido a homogeneização de traços funcionais
(GÁMEZ-VIRUÉS et al. 2015; IBARRA & MARTIN 2015).
A importância das aves para a funcionalidade dos ecossistemas
As aves estão entre os grupos animais mais afetados pela redução e fragmentação
do habitat, sendo um excelente objeto de estudo dada sua grande diversidade taxonômica
e por serem facilmente amostrados, além de apresentarem uma grande variedade de
respostas diante a diferentes alterações ambientais (RAJÃO et al., 2014;
ALEXANDRINO et al., 2016). Estudos têm avaliado os efeitos da redução e
fragmentação do habitat sobre diversas espécies de aves, relatando alterações em riqueza,
abundância e composição de espécies (MORANTE-FILHO et al. 2015). Especificamente,
espécies dependentes de florestas apresentam reduções abruptas em suas populações
quando seu habitat é reduzido e/ou fragmentado, enquanto espécies menos sensíveis
como generalistas de habitat têm se beneficiado das alterações decorrentes das atividades
humanas (MATTHEWS et al., 2014; DOS ANJOS et al., 2015).

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As aves também desempenham diversos papéis ecológicos importantes no
ecossistema mediando funções como o controle de populações de outros vertebrados,
controle de populações de artrópodes, predação e dispersão de sementes, polinização e
transporte de nutrientes (SEKERCIOGLU, 2006; BARROS et al., 2019). Nesse sentido,
é de se esperar que também as funções desempenhadas pelas aves sejam alteradas ou até
mesmo perdidas em ambientes altamente alterados (DOBSON et al., 2006, EMER et al.,
2019). Por exemplo, estudos têm evidenciado que o desaparecimento abutres-de-bico-
preto (Gyps indicus) na Índia, pode causar aumentos no número de carcaças apodrecidas
e de mamíferos detritívoros vetores de doenças (CUNNINGHAM et al., 2003).
Juntamente com outros vertebrados, aves insetívoras são capazes de suprimir populações
de artrópodes herbívoros, podendo reduzir indiretamente danos causados às plantas por
esses artrópodes e consequentemente aumentar a biomassa vegetal (MOONEY et al.,
2010). A ausência dessas aves pode aumentar o número de artrópodes herbívoros e
consequentemente aumentar a taxa de herbivoria foliar nas florestas, causando danos as
plantas (MORANTE-FILHO, et al., 2016). A extinção de aves polinizadoras na ilha Norte
da Nova Zelândia tem reduzido a polinização, a produção de sementes e a densidade de
plantas (ANDERSON et al., 2011). Nos Andes, a perda de grandes aves frugívoras
dispersoras de sementes resultou em um declínio de 40% na dispersão de sementes a
longa distância, e que a longo prazo pode vir afetar as comunidades de plantas que são
dispersas somente por esses animais (DONOSO et al., 2020). Na Mata Atlântica
brasileira, a perda de aves frugívoras de grande porte tem reduzido a complexidade das
redes de interações ave-planta, onde em paisagens altamente fragmentadas as redes de
interações são compostas majoritariamente por aves frugívoras generalistas de corpo
pequeno, que dispersam sementes menores a curtas distâncias (JORDANO et al., 2007;
EMER et al., 2018; 2019). Desse modo, a ausência desses grandes dispersores pode
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causar um acúmulo de sementes abaixo da planta mãe, reduzindo o recrutamento das
plântulas (Janzen-Connell hypothesis; JANZEN, 1970;CONNELL 1971) e a longo prazo
afetar as populações de plantas e até mesmo a capacidade de estoque de carbono das
florestais tropicais (JORDANO et al., 2006; GALETTI et al., 2013; BELLO et al., 2016).
Nesse contexto, não há dúvidas que as aves são essenciais para a funcionalidade dos
ecossistemas. Assim, a ausência de determinados grupos de aves pode afetar
negativamente outras espécies de plantas e animais (SEKERCIOGLU et al., 2004,
BUECHLEY & ŞEKERCIOĞLU, 2016).
Perda e fragmentação do habitat: ameaças à Mata Atlântica
Em ecossistemas terrestres, a conversão dos habitats naturais em decorrência de
mudanças no uso do solo estão entre as principais promotoras da perda de biodiversidade
global (ANDRÉN & ANDREN, 1994, PARDINI et al., 2010, FAHRIG, 2013). Mudanças
na riqueza, abundância e composição das espécies são mais evidentes nas florestas
tropicais, onde grande parte da sua vegetação nativa foi reduzida para a implementação
de atividades agrícolas e/ou pecuárias (FARIA et al., 2006; 2009; BOESING et al., 2018).
Esta perda é especialmente preocupante no Brasil, um dos países mais diversos do mundo
e detentor de 13% da biodiversidade global (LEWINSOHN et al., 2006). A Mata
Atlântica brasileira, por exemplo, é um domínio fitogeográfico altamente fragmentado
com sua área atual ocupando menos de 28% da área original (REZENDE et al., 2018).
Ao longo de décadas, esse domínio fitogeográfico tem sofrido pressões como a
exploração madeireira, incêndios, caça, além dos fatores globais relacionados a mudanças
climáticas que têm diminuído a sua biodiversidade (ROCHA-SANTOS & TALORA,
2012; DE SOUZA & ALVES, 2014; SCARANO & CEOTTO, 2015). Em consequência
dessas pressões, a Mata Atlântica é constituída por vários remanescentes florestais de

9
diversos tamanhos e isolados entre si (RIBEIRO et al., 2009; JOLY et al., 2014). Esses
remanescentes florestais são envoltos por um ou vários tipos de matrizes, como áreas de
pastagens, monoculturas e zonas urbanas (UEZU et al., 2005; PARDINI et al., 2009).
Devido à quebra da conectividade da floresta, a matriz se torna uma barreira física a ser
transpassada, pela qual espécies que possuem baixa mobilidade ou requerimentos mais
específicos relacionados ao hábitat são afetadas por não conseguirem migrar para outros
remanescentes florestais e acabam confinadas dentro dos fragmentos florestais. Outras
espécies que se arriscam a atravessar a matriz antrópica podem não conseguir e acabar
morrendo (e.g., predação e/ou atropelamento) (MAY & NORTON, 1996, ROBINSON et
al., 2010).
Na Mata Atlântica, diversos táxons como mamíferos, aves, plantas e artrópodes
sofrem declínios em suas populações devido, em grande parte, ao desmatamento,
necessitando assim, de medidas urgentes para a sua conservação (UEHARA-PRADO et
al., 2009; ZURITA & BELLOCQ, 2010; JORGE et al., 2013; RIGUEIRA et al., 2013).
Estudos evidenciaram que a quantidade de habitat remanescente e os efeitos de borda
exercem impactos na riqueza de espécies animais e de plantas (PARDINI et al., 2010;
PÜTTKER et al., 2020). Os efeitos de borda também podem afetar negativamente a
abundância dos vertebrados que vivem no interior da floresta (PFEIFER et al., 2017).
Além da redução da riqueza e abundância de espécies animais, os efeitos de borda podem
levar as florestas a estágios iniciais de sucessão ecológica com a simplificação da
estrutura e composição da vegetação (RIITTERS et al., 2000; ROCHA-SANTOS et al.,
2016). Esses efeitos são ainda mais intensos em fragmentos florestais menores,
aumentando com o passar do tempo com a expansão das bordas (HADDAD et al., 2015).
Assim, a fragmentação do habitat tem reduzido 13 a 75% da biodiversidade em

10
ecossistemas tropicais, prejudicando também funções do ecossistema (HADDAD et al.,
2015; MOLINA MELO et al., 2016).
Apesar da Mata Atlântica estar em um estado crítico de conservação, beirando o
colapso devido aos impactos antrópicos, ainda é um domínio fitogeográfico altamente
heterogêneo, pois abrange desde florestas sempre-verdes, decíduas e semi-decíduas até
manguezais, restingas, campos rupestres, florestas mistas de pinheiros de araucária e
outros tipos de habitats (RIBEIRO et al., 2009). Por apresentar essa alta diversidade de
habitats, esse domínio abriga uma rica flora e fauna, as quais, já foram estimadas
aproximadamente cerca de 20.000 espécies de plantas, 263 mamíferos, 936 aves, 306
répteis e 475 anfíbios (MITTERMEIER et al., 2005). Assim, esse domínio fitogeográfico
constitui uma das regiões neotropicais mais diversas do mundo, com altos níveis de
endemismo e altamente ameaçada devido à perda de habitat (ou seja, um hotspot de
biodiversidade) (THOMAS et al., 1998; MYERS et al., 2000; TABARELLI et al., 2010;
CANALE et al., 2012). Devido a essas características, a Mata Atlântica é reconhecida
internacionalmente como Sítio do Patrimônio Mundial Natural e Reserva da Biosfera pela
UNESCO (Organização das Nações Unidas para Educação, Ciência e Cultura). Nesse
domínio, uma série de estudos tem contribuído para se ter uma melhor compreensão sobre
a ecologia das florestas tropicais e a susceptibilidade das espécies às alterações causadas
pelo homem (MARINI & GARCIA 2005; PARDINI ET AL. 2010; JOLY et al. 2014).
Nesse sentido, este projeto buscou aprofundar mais o conhecimento sobre as aves
e o seu papel ecológico. Especificamente, estudamos a avifauna e suas interações (ave-
planta) na Mata Atlântica do Sul da Bahia, uma região que possuí diversos remanescentes
florestais que abrigam ainda exuberante riqueza de espécies (THOMAS et al., 1998; DA
SILVA et al., 2004).

11
OBJETIVOS
O objetivo geral desta tese é avaliar o efeito da alteração na composição e
configuração da paisagem e da estrutura do habitat florestal sobre aves de sub-bosque e
suas interações ecológicas.
- No primeiro capítulo, o objetivo foi determinar como mudanças na cobertura florestal,
quantidade de interior de floresta, densidade de bordas e diferenças em isolamento entre
fragmentos de floresta dentro da paisagem afetam as assembleias de aves do sub-bosque.
Especificamente, avaliar se aves dependentes e não-dependentes de floresta e se guildas
tróficas de aves frugívoras e insetívoras são afetadas por mudanças na composição e
configuração da paisagem. Também foi avaliado em escala local se a densidade de
árvores e plantas no sub-bosque das florestas, bem como a abertura do dossel e
disponibilidade de frutos afetam as assembleias de aves do sub-bosque e seus grupos
ecológicos citados acima.
- No segundo capítulo, o objetivo foi determinar como diferenças em cobertura florestal,
quantidade de interior de floresta, densidade de bordas e isolamento afetam as redes de
interação ave-planta. Também foi avaliado em escala local se a densidade de árvores e
plantas no sub-bosque das florestas, bem como a abertura do dossel e disponibilidade de
frutos afetam as interações ave-planta. Nesse capítulo, o objetivo foi estimar para cada
local da floresta: o número de interações realizadas por espécies de aves e plantas; o
número médio de ligações por espécie; a uniformidade da interação; a modularidade das
redes de plantas de aves e avaliar se essas métricas de rede são afetadas pelos preditores
descritos acima.
12
- No terceiro capítulo, o objetivo foi determinar como os preditores ambientais
mensurados em escala de paisagem como cobertura florestal, quantidade de interior de
floresta, densidade de bordas e diferenças em isolamento entre fragmentos de floresta
dentro da paisagem afetam a diversidade beta (β) de aves, plantas e suas interações.
Também foi avaliado em escala local se a densidade de árvores e plantas no sub-bosque
das florestas, assim como a abertura do dossel e disponibilidade de frutos afetam a
diversidade beta (β) de aves, plantas e interações.

13
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Landscape Ecology 25:147–158. https://doi.org/10.1007/s10980-009-9410-4
22
Capítulo I
23
Ecological drivers of understory bird assemblages in tropical forest patches: a

multi-scale approach
Ícaro Menezes Pinto1*, Eliana Cazetta1, Deborah Faria1 and José Carlos
Morante-Filho1*
1
Applied Conservation Ecology Lab, Programa de Pós-graduação em Ecologia e
Conservação da Biodiversidade, Universidade Estadual de Santa Cruz, Rodovia Ilhéus-
Itabuna, km 16, Salobrinho, 45662-000 Ilhéus, Bahia, Brazil.
* Corresponding authors: icaro.bio.uesc@gmail.com and jcmfilho9@hotmail.com

24
Abstract
Global biodiversity is threatened by the pressures from human-activities through the

exploitation of natural resources, particularly in tropical forests where biodiversity has
decreased abruptly. Usually, in human-modified landscapes, changes in species
composition have occurred as a consequence of landscape composition and configuration.
For instance, forest-dependent birds have a strong negative response to changes in
landscape composition and configuration, while non-forest-dependent birds in general
respond positively to these disturbances. Likewise, trophic guilds such as frugivores and
insectivores can also be affected by landscape changes, especially species inhabiting the
forest understory. Also, birds may respond to qualitative changes within forest sites such
as alteration in vegetation structure or scarcity of resources. Herein we evaluated the
responses of understory birds to local changes in vegetation structure and fruit number in
forest patches and landscape changes in forest cover, core area, edge density and inter-
patch isolation. For this, birds were classified into forest-dependent and non-forest
species and also into trophic guilds (i.e. insectivores, frugivores, carnivores, nectarivores,
granivores and omnivores), subsequently we used the most representative guilds -
frugivorous and insectivorous birds - for statistical analysis. Our study was performed in
20 forest sites distributed in two regions with different land use in the Brazilian Atlantic
forest in the State of Bahia, Brazil. We found that landscape-scale predictors positively
affected the richness and abundance of understory birds. We also observed that forest
sites immersed in landscapes with higher forest coverage, which have a higher proportion
of total core area and are less isolated, exhibited an increase in richness and abundance.
Also, our results showed that in the most deforested region, the richness and abundance
of most ecological groups are negatively affected. Non-forest and insectivorous birds
were less sensitive to habitat change, and mainly affected by vegetation complexity. In
general, our results demonstrated that disturbed landscapes, with low forest cover, core
area and with a higher isolation inter forest sites, exhibited a lower richness and
abundance of understory birds and ecological groups.
Keywords: Atlantic Forest; bird community; habitat loss; habitat fragmentation; human-
modified landscapes; tropical forest; understory birds
25
1. INTRODUCTION
Changes in land-use through by human activities result in a major impact on
biodiversity, mainly in terrestrial ecosystems (Newbold et al. 2015). The overexploitation
of natural resources, expansion of agricultural and livestock activities together with the
advance of urbanization are among the main threats to fauna and flora (Wilson et al.
2016), especially in tropical forests (Keenan et al. 2015) that also suffer strong hunting
pressure (Cullen et al. 2000), selective logging tree (Villela et al. 2006; Rocha-Santos et
al. 2016) and wildfire (dos Santos et al. 2019). Consequently, in human-modified
landscapes the biodiversity tends to be lower when compared to preserved old-growth
forests (Tabarelli et al. 2010; Brancalion et al. 2013).
Declines in biodiversity is a direct result of changes in composition and
configuration of landscapes (e.g., forest loss and fragmentation), that reduces the habitat
amount available for species and limited their dispersal movements among habitat
remnants due presence of an inhospitable matrix (Eycott et al. 2012). In addition, forest
loss and fragmentation also alter the quality of habitat in the level of local patch, because
a myriad of local abiotic changes, which are associated with the edge effects occur with
the fragmentation of forests (Banks-Leite et al. 2010; Cerboncini et al. 2015). In forest
edges occur an increased light incidence (Rigueira et al. 2012; Bomfim et al. 2013),
changes in air and soil temperature (Davies-Colley et al. 2000), wind dynamics,
photosynthesis processes, decomposition of organic matter and in the nutrient cycle
(Laurance et al. 2007; Ordway and Asner 2020). This changes in abiotic conditions in the
forest patches cause a simplify of vegetation structure through decrease in the number of
trees, height and diameter of trees, open the forest canopy, increase in incidence of
understory plants, mainly pioneer plant species that have a lower biomass of fruits for
26
fauna (Rocha-Santos et al. 2016; Benchimol et al. 2017; Pessoa et al. 2017).
Consequently, small forest patches presented a lower habitat complexity and less
vegetation vertical structure in core or edge forest affect richness and abundance of plants
(Benítez and Martínez 2003; Rocha-Santos et al. 2019), arthropods (González et al. 2015;
Benítez-Malvido et al. 2016), mammals (Zimbres et al. 2017; Palmeirim et al. 2020),
birds (Watson et al. 2004; Banks-Leite et al. 2010) and others taxon’s (Pfeifer et al. 2017).
Birds particularly comprise a diverse group of vertebrates that occupy a wide
range of ecological niches (Harvey and Villalobos 2007) playing fundamental roles in
ecosystem functioning, including arthropod control, pollination, and seed dispersal
(Sekercioglu 2006). Because presented positive or negative responses to forest loss and
fragmentation, in addition responses to quality of their habitats (patch-scale), birds are an
excellent group to study effects of changes in land-use promoted by human activities in
your biodiversity (Jeliazkov et al. 2016). Typically, bird assemblages in habitat patches
inserted in more deforested landscapes are poor in forest species number. In contrast, non-
forest-dependent birds can persist or even thrive in human-modified landscapes,
specifically because they are able to disperse among forest patches and use the edges of
forests as habitat for nesting and foraging (Hinsley et al. 2009; Carrara et al. 2015).
Regarding their trophic-guilds, it is known that frugivorous and insectivorous
species are the most sensitive to changes in habitat, while others trophic guilds like
omnivorous, granivorous and pollinators are less affected (Sekercioglu et al. 2004;
Manhães and Dias 2011; Morante-Filho et al. 2015). For example, large frugivorous
species, especially species of Ramphastidae and Cracidae family are the first disappear in
deforested areas (Galetti et al. 2013; Emer et al. 2019; Donoso et al. 2020). The same
response to landscape-scale deforestation is reported for insectivorous birds, although
pattern is often triggered by the simplification of local vegetation structure (Manhães and
27
Dias 2011).
Although several studies have evaluated the responses of birds in human-modified
landscapes, it’s not yet clear whether landscape predictors are more important for
predicting the diversity of understory birds than local predictors (Morante-Filho et al.
2015; Whytock et al. 2020; Zasadil et al. 2020). Mainly because each species has different
requirements related to habitat-use and exploitation (Pigot et al. 2020). In addition, the
spatial scale at which a given landscape attribute is measured may or may not influence
individual responses of species (Jackson and Fahrig 2015; Huais 2018).
Here, we proposed to assess how changes in local and landscape-scale affect
understory birds. We surveyed birds in 20 forest sites located in two regions with
contrasting land-use patterns in the Brazilian Atlantic Forest in southern Bahia State.
First, we evaluated: (1) amount of forest cover, (2) total core area, (3) edge density and
(4) inter-patch isolation. Second, we assessed local predictors in level of patch, such as
the (1) vegetation complexity, (2) number of trees, (3) number of understory plants, (4)
diameter of the trees, (5) canopy openness and (6) fruit availability. For each forest site
we estimated richness and abundance of understory bird community and of the different
ecological groups like forest-dependent and non-forest-dependent birds, besides
frugivorous, and insectivorous birds that were more abundant.
We predicted that forest-dependent, frugivorous, and insectivorous birds will
decrease in abundance and richness in more deforested landscapes, as these bird species
are most sensitive to habitat disturbances (Watson et al. 2004; Harvey and Villalobos
2007; Morante-Filho et al. 2015). Also, we predicted that the increasing edge density in
forest sites along with decreasing total core area will negatively affect forest-dependent
birds, frugivores and insectivores, while benefiting non-forest-dependent species (Carrara
et al. 2015; Morante-Filho et al. 2015). Yet, we predicted that the increasing of isolation
28
among forest sites in landscapes will negatively affect the bird community (Pardini et al.
2009). In addition, we predicted that the simplification of local vegetation structure will
negatively affect forest-dependent birds and insectivorous birds that forage in medium
and low forest strata (Carrara et al. 2015; Stratford and Stouffer 2015). Finally, we predict
that frugivores, besides being affected by the environmental variables described above,
will also respond to the availability of fruits within the forest patches (Morante-Filho et
al. 2018).
2. MATERIALS AND METHODS
2.1. Study area
The study region is located in the southeastern state of Bahia, northeastern Brazil
(Figure 1), in the Brazilian Atlantic Forest. Currently, the region is composed of different
agricultural systems and land-use types such as cocoa plantations (Theobroma cacao),
rubber tree (Hevea brasiliensis), Eucalyptus spp., and cattle pastures (Pardini et al. 2009).
The regional climate, according to the Köppen classification, is of the Af type, hot and
humid, without presenting a well-defined dry season (Gouvêa 1969). The annual averages
of temperature and precipitation are 24° C and 2,000 mm/year, respectively, presenting a
period of low rainfall that runs from December to March.
We used high-resolution satellite images (Quick Bird and World View, 2011 and
Rapid Eye, 2009-2010, with resolutions of 0.6, 0.5 and 5 m, respectively). Then, we
classify and digitize land use using ArcGIS software (ESRI 2012) at a scale of 1:10,000
to identify stains based on visual inspection of color, texture, shape, location, and context.
Therefore, we developed a digital map that covers an area of 3,500 km². Although the
mapped area has similar soil, topography, and floristic characteristics, the northern region
has a high forest cover (HFC region, hereafter), 50% of which corresponds to the native
29
and secondary forest (Morante-Filho et al. 2016). The landscape matrix in the HFC region
is highly heterogeneous, characterized by shaded cocoa plantations (22% of the landscape
matrix) and rubber trees (10%) and other types of land-use (18%) (Figure 1). In contrast,
the southern region has a low forest cover (hereafter, LFC region), due to the intensive
use of the soil, leaving only 30% of the forest with a homogeneous matrix predominantly
composed of pastures (86% of the landscape matrix) and Eucalyptus spp. plantations
(7%) (Morante-Filho et al. 2016).
Based on this mapping, 48 potential sample sites, i.e., buffers of 1 km around
previously selected forest sites. Then, we randomly selected 20 forest sites, inserted in a
gradient of native forest cover (that is, excluding cocoa and rubber plantations) distributed
equally in both regions (Figure 1). Each site was spaced at least 1 km from each other to
prevent the 1 km landscapes around the sample sites from overlapping.
Figure 1. Study area in Southeastern Bahia, Northeastern Brazil. The sampling sites (black circles) and
land cover classes in the high forest cover - HFC region (a) and low forest cover - LFC region (b). In (c)
30
one landscape amplified exhibited a wide range of landscape native forest cover and different land-cover
classes. The black circles represent the landscape scales used in this study that vary 0,1 to 1 km.
2.2. Landscape metrics and their scales of effect
The effects of landscape variables on biodiversity patterns depend on the spatial
scale on which the predictors are measured. Therefore, we applied a multiscale analysis
to assess the effects of landscape composition and configuration in a range of specific
areas surrounding each sampling site (Jackson and Fahrig 2015). Thus, we calculate each
landscape metric in 10 buffers ranging from 100 to 1000 m at 100 m intervals from the
center of each sampling site. We used the FRAGSTATS 4.2 software (McGarigal and
Marks, 1995) to estimated one metric of landscape composition - the forest cover amount
and evaluated three metrics related to landscape configuration - cohesion index that
measures the physical connection between forest patches. Thus, higher values of cohesion
index describe landscapes in which forest patches are closer. Also, we evaluated the total
length of the forest edge (edge density 75m/ha) (Faria et al. 2009) and total core area of
forest sites. These metrics were chosen because they were previously indicated for
influencing the richness and composition of species of birds and plants in human-
modified landscapes (Martensen et al. 2008; Zurita et al. 2012; Morante-Filho et al. 2015).
Thus, we used Generalized Linear Models to identify the most appropriate landscape size
(Appendix S2 in Support Information) to analyze the effect of each landscape metric on
richness and abundance of bird species.
2.3. Local variables - vegetation structure and fruit availability
For evaluating the vegetation structure, we used four plots (25 x 4 m) that were
randomly located at each forest site, with a minimum inter-plots distance of 150 m. We
selected five local variables that are related to the diversity of ecological groups of birds
31
in forest patches (Rocha-Santos et al. 2016; Morante-Filho et al. 2018). From October
2013 to April 2014, we recorded in each plot (1) all the woody plants in the understory
(50-200 cm in height), and (2) all the trees above the understory layer (diameter at breast
height DBH ≥ 5 cm). Then, we estimated (3) the density of all stems and the mean DBH
of all stems (i.e. average DBH per tree). Finally, we also estimated (4) the percentage of
canopy openness within the plots using hemispherical photographs that were taken at 1.5
m from the soil and analyzed with Gap Light Analyzer software (Frazer et al. 1999).
These all four variables were summarized in an index of vegetation complexity using a
Principal Component Analysis (PCA). We used the first component of the PCA that
explained 55.6% of the variation in vegetation structure as a proxy of vegetation
complexity (Appendix S3).
We also used five plots (25 x 4 m) totaling a sampling area of 0.05 ha per site to
estimate the (5) number of fleshy fruits available for bird communities. The abundance
of fruits was estimated from April-September 2017, and October 2017 to April 2018. We
sampled all plants between 0.5 and ~ 7 m height, where all the visible mature fruits
presented on a single branch were counted with the aid of an 8x42 binocular. Then, fruit
number per plant was obtained through the multiplication of the total number of fruits on
the focal branch by the number of branches with fruits per plant (Loiselle and Blake
1990).
2.4. Bird survey
We sampled bird communities in two field seasons: the first was carried out in
April-September 2017 and the second in October 2017 to April 2018, using the mist nets
method. The license for bird capture was granted by Ministério do Meio Ambiente
(MMA); Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis

32
(IBAMA), and Sistema de Autorização e Informação em Biodiversidade (SISBIO);
license number 53792-2. In each forest site, we opened 10 mist nets (12 m long, 2.5 m
high, 31 mm mesh) to capture birds during three consecutive days per field season. The
mist nets were opened from 07:00 to 17:00 and reviewed every 30 minutes in order to
reduce the catch stress. We did not sample on rainy and windy days because such
conditions affect bird movement and therefore may interfere in capture success. Each
captured bird was temporarily marked on one of the right-wing primary feathers with
non-toxic material to avoid recounting the same individual during the 3 consecutive
sampling days by season (total 6 days). Thus, recaptured birds during the same sampling
period were not re-evaluated. We used a sampling effort of 60 hours per forest site, a total
of 12,000 hours/mist nest of bird sampling. All bird was identified according to the
scientific nomenclature of the South American Classification Committee (Remsen et al.
2014).
We classified the birds according to their forest dependency into non-forest
dependent birds (hereafter, non-forest birds) or forest-dependent birds (hereafter, forest
birds), according to Stotz et al. (1996) and Bregman et al. (2014). Non-forest birds are
those that usually occur in secondary forests, forest edges, open vegetations and
anthropogenic areas such as urban areas, cattle pastures, and crops (Bregman et al. 2014).
Forest birds are those that are associated with evergreen or deciduous forest, with closed
canopy or that are more associated with the interior of the forests (Bregman et al. 2014).
We also classified the birds into trophic guilds (i.e. insectivores, frugivores, carnivores,
nectarivores, granivores and omnivores). These trophic guilds reflect the main food
resource of the species, although some species supplement their diet with more than one
type food resource (Wilman et al. 2014). For statistical analysis, we use the information
only of two most representative trophic guilds: insectivorous and frugivorous birds.
33
2.5. Statistical analyses
We used Spearman’s test to assess the correlation between environmental
variables, that is, local and landscape variables. Based on the test result, highly correlated
variables (r ≥ 0.70) were not included within the same model (Appendix S4).
Subsequently, GLM models were created for testing the effects of environmental
variables on species richness and abundance, using the Poisson distribution. Our models
were composed by one landscape predictor (e.g., forest cover, total core area, edge density
or cohesion index) or one local predictor (e.g., fruit number or vegetation complexity)
individually or both together when did not correlated. The study region comprised a fixed
factor in the models, the differences between land-use in both regions that affect
understory bird species (Morante-Filho et al. 2016; Rocha-Santos et al. 2017). All models
were submitted to a model selection approach based on the corrected Akaike information
criterion for small samples (AICc), using the packages lme4 (Bates et al. 2014) and bbmle
(Bolker, 2017), MASS (Venables and Ripley 2002), mgcv (Wood, 2011), nlme (Pinheiro
et al. 2020) and AICcmodavg (Mazerolle, 2020). We consider the models equally
plausible when the difference in AICc (ΔAICc) between the models was less than 2. We
also use the Akaike weight (ωAICc), which varies from 0 to 1 and express the normalized
relative probability of each model, to select the most plausible model (Anderson 2008).
Then, we evaluate the fit of the plausible models using the ratio between residual
deviation and residual degrees of freedom, where values > 1 indicate over-dispersion or
< 1 sub-dispersion (McCullagh and Nelder 1989). We also adjusted the models that
showed over-dispersion using Quasi-Poisson family. In addition, we evaluated the spatial
autocorrelation in the residues of the best models based on Moran I's autocorrelation
coefficient using the ape package (Paradis and Schliep 2019). All analyses and statistical
34
graphs were performed using R software version 3.5.3 (R Core Team, 2019).
3. RESULTS
We recorded a total of 498 birds in 20 forest sites. In only one landscape in the
LFC region, we did not capture birds during the two seasons of sampling. Birds were
distributed in 23 families and 59 bird species (Appendix S1, Table S1). The most
representative families were Thamnophilidae (n = 7), Dendrocolaptidae (n = 6),
Thraupidae (n = 6) and Pipridae (n = 5). The families Pipridae (n = 217) and
Dendrocolaptidae (n = 129) were the most representative in number of individuals. The
species more representative were Ceratopipra rubrocapilla (n = 77), Dixiphia pipra (n =
71), Glyphorynchus spirurus (n = 45), Machaopterus regulus (n = 41), Dendrocincla
turdina (n = 39), Manacus manacus (n = 26), Xiphorhynchus fuscus (n = 25) and Myiobius
barbatus (n = 24). We captured 457 forest-dependent birds, distributed in 20 families and
39 species. From non-forest-dependent birds, 41 individuals were captured, distributed in
9 families and 20 species. The most representative trophic guilds were insectivores (29
species, n = 224) and frugivores (14 species, n = 238). In HFC we captured a total of 360
birds, distributed in 22 families and 44 species, in LFC region we captured 138 birds,
distributed in 19 families and 39 species.
The model selection highlighted several parsimonious models (ΔAICc ≤ 2) to
explain the effect of environmental predictors on bird communities (Table 1; Appendix
S5). We found that understory bird richness and their abundance was positively affected
by forest cover and total core area with a lower abundance of birds in LFC region (S5,
Table S3). But, only richness of understory birds was positively affected by cohesion
index with a greater richness in landscapes with forest patches closer. Richness of forest-
dependent birds was also positively affected by forest cover, total core area, and cohesion
35
index and their abundance was influenced positively in landscapes with patches more
connectedness. Richness and abundance of non-forest birds only was negatively affected
by cohesion index, that is, landscapes with forest patches closer shown a less richness of
non-forest birds. Only the models for non-forest birds showed spatial autocorrelation,
revealing that this data subset is more spatially grouped (Appendix S6, Table S4).
Frugivorous were mainly affected by landscape-scale predictors. The only
predictor that negatively influenced the richness of frugivores was the region, with the
LFC region showing low species richness. We also observed that abundance of frugivores
birds was positively affected by forest cover, total core area and cohesion index. Finally,
we observed that richness of insectivorous bird was positively affected by forest cover,
total core area and cohesion index. Abundance of insectivorous birds was positively
affected by two predictor variables the cohesion index and vegetation complexity.
36
Table 1. Model selection parameters ranked by ΔAICc values used to explain the relationship between the dependent variables and
several environmental predictors observed in 20 forest sites located in the Brazilian Atlantic Forest. Significant variables in models
are highlighted in bold. For more details, see Appendix S5, Table S3.
Bird group Response variable Models ΔAICc df wi
Complete community Richness Total core area + region 0.0 3 0.281
Cohesion + region 0.8 3 0.186
Edge density + region 1.7 3 0.122
Forest cover + region 1.8 3 0.114
Abundance Total core area + region 0.0 3 0.394
Non-forest birds Richness Cohesion 0.0 2 0.383
Abundance Cohesion 0.0 2 0.471
Forest birds Richness Forest cover + region 0.0 3 0.247
Total core area + region 0.5 3 0.193
Abundance Cohesion + region 0.0 3 0.603
Cohesion + vegetation complexity + region 0.1 4 0.348
Frugivorous birds Richness Region 0.0 2 0.363
Abundance Cohesion + fruit availability + region 0.0 4 0.429
Forest cover + vegetation complexity + region 1.2 4 0.241
Total core area + vegetation complexity + region 1.3 4 0.221
Insectivorous birds Richness Cohesion 0.0 2 0.138
Cohesion + vegetation complexity 0.1 3 0.131
Forest cover 0.2 2 0.123
Total core area 0.5 2 0.108
Abundance Cohesion + vegetation complexity 0.0 3 0.739
ΔAICc: difference of the AICc comparting to the best model; df: number of parameters of the model and wi: AICc weight
37
4. DISCUSSION
Our findings highlighted that diversity of understory birds is greatly affected by
landscape-scale predictors than local predictors, although local vegetation complexity
also positively affected the abundance of insectivorous birds. Most ecological groups
assessed showed increases in their richness and abundance in forest sites immersed in
landscapes with greater forest cover, which have a higher proportion of total core area
and closer proximity between forest sites. By contrast, the more deforested region
comprised more impoverished and less abundant bird assemblages of all ecological
groups, except the non-forest and insectivorous birds.
Changes in landscape composition and configuration can affect the bird
communities structure (Dolman and Sutherland 1995; Schmiegelow and Mönkkönen
2002). We observed that total bird community in our forests is composed essentially by
forest-dependent birds; species that normally occur in the forest understory, often
responding negatively to the loss of forest cover in landscapes (Restrepo et al. 1999;
Durães et al. 2013; Morante-Filho et al. 2015; Visco et al. 2015). Forest birds are species
that have specific requirements related to habitat, which include the need for old-growth
forests and less disturbed stands with a high availability of food resources or nesting sites
(García et al. 2011; Ferger et al. 2014). These specific requirements increase their
sensitivity to forest loss and fragmentation, as they typically forest birds require large
habitat patches and forest interiors (Pigot and Tobias 2013; Morante-Filho et al. 2015).
Therefore, it is expected that the loss of forest cover and the amount of total core area
limit the amount of habitat available for understory bird communities, mainly the richness
of forest-dependent birds.
More connected forest patches positively influenced the richness of bird complete
38
community and the abundance of forest birds. It is known that the spatial disruption of
landscape structure – decreasing among-habitat connectivity – is an important
environmental filter, especially for more sensitive species, limiting bird’s dispersal
movements to new locations (Biz et al. 2017; Ramos et al. 2020). This break in the
structural connectivity of the landscape has stronger effects on forest birds, also affecting
their abundance. This result suggests that forest birds are more limited in their dispersion,
thus requiring landscapes with forest sites more connected to each other for their
populations to persist (Visco et al. 2015). In contrast, the greater of connectivity of forest
sites negatively affected the richness and abundance of non-forest birds. Non-forest birds
normally prefer open areas and forest edges than habitats in forest interior (Barros et al.
2019a). Contrary to what we expected, however, the edge density in forest sites did not
influence richness nor abundance of local bird assemblages. Birds can present different
responses according to the amount of edge in forest sites and the distance that the edge
effects penetrate within forest interiors (Pfeifer et al. 2017; Orme et al. 2019), although
edge effects are more variable for birds than for other groups of vertebrates, such as
mammals and reptiles (Pfeifer et al. 2017). Here, the low number of bird captures may
be insufficient to suggest a clearer response for non-forest dependent birds.
Similarly, when evaluating trophic guilds, the richness of insectivorous birds and
abundance of frugivorous birds responded positively to landscape variables such as forest
cover, total core area and cohesion among forest sites. Frugivorous birds exhibited a lower
richness in LFC region and insectivorous birds showed a higher abundance in landscapes
with forest patches less isolated and with a more in vegetation complexity. Recent studies
have reported that frugivorous and insectivorous birds are both affected by increasing
deforestation and fragmentation, becoming more vulnerable in areas where effects of the
surrounding matrix and isolation among forest patches are more intense (Villard and
39
Metzger 2014; Barros et al. 2019b). Also, this result can be explained by the type of
resource that is exploited by the two trophic guilds. Frugivorous birds, for example,
depend on seasonal resources such as fruits (Loiselle and Blake 1990; Carnicer et al.
2008). Therefore, to meet their daily demands frugivorous birds highly depend on the
structural connectivity of the landscape to move between forest patches of forest in their
search for resources in unexplored areas (Castellón and Sieving 2006; Díaz Vélez et al.
2015).
Regarding insectivorous birds, these species are also further affected by forest
cover and inter-patch isolation (Sekercioglu 2002; Stratford and Stouffer 2015). In
addition, vegetation complexity is an important factor for insectivorous birds, particularly
the understory species that require to forage in the middle and lower strata of the forest,
looking for arthropods in branches and trunks (Manhães and Dias 2011; Stratford and
Stouffer 2015). However, in landscapes that suffer strong anthropogenic pressure, the
remaining forest habitats are likely to be degraded, represented by patches at the initial
stages of succession (Walker and Reddell 2007). Insectivorous birds prefer areas with a
higher density of vegetation with favorable microclimate and high availability of
resources (Sekercioglu 2002; Stratford and Stouffer 2015). For instance, preferred food
resources (e.g., Coleoptera) for insectivorous birds can be reduced in more deforested and
fragmentated landscapes (Peter et al. 2015). Therefore, ideal conditions for insectivorous
birds drastically changed in fragments immersed in more deforested landscapes. In
addition, the low dispersal capacity and preferences for old-growth forests or habitats
located in forest interiors becomes another aggravating factor for these birds (Lees and
Peres 2006; Harris et al. 2011). In LFC region the richness and abundance of total bird
community, forest-dependent and frugivorous birds are also less.

40
Conclusions
Our findings demonstrated that understory birds in forest sites immersed in a
deforested landscape are strongly affected by landscape composition and configuration.
Thus, landscape-scale forest loss limits the amount of habitat available for understory bird
species, in addition to increasing the isolation between fragments immersed in the
landscapes. These factors can be critical, considering that bird species belonging to these
groups can require an amount of forest cover approximately ≥ 50% (Morante-Filho et al.
2015) while a large part of the Brazilian Atlantic Forest is highly fragmented (Ribeiro et
al. 2009; Haddad et al. 2015). Our results suggest that the assemblages of forest birds,
frugivores and insectivores are mainly affected by changes in the landscape scale and less
affected by local changes. Although, understory birds are closely linked to vegetation
complexity across in tropical forests (Peter et al. 2015), this study reinforces the idea that
forest loss and fragmentation are the main drives affecting, and ultimately shaping, the
current understory bird assemblages in this tropical and human-modified landscapes.
5. ACKNOWLEDGEMENTS
We thank Albérico Queiroz, Adrielle Leal, Fabio Soares, Thamyrys Souza and
Julia Perez for their help in the fieldwork; and local landowners for allowing us to work
on their property. We also thank Gil Reuss and Diogo Caribé for helping to map the study
area. We also thank Rufford Small Grants for Nature Conservation (No. 22426-1), the
Universidade Estadual de Santa Cruz (No. 00220.1100.1644/10-2018) FAPESB (No.
0525/2016) and CNPq (No. 563216/2010-7) by the financial support. This study was
financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior -
Brasil (CAPES) - Financial Code 001.

41
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Supporting Information
Ecological drivers of understory bird assemblies in tropical forest pacthes:

a multi-scale approach
Ícaro Menezes Pinto1*, and José Carlos Morante-Filho1*
1
* Corresponding authors: icaro.bio.uesc@gmail.com and jcmfilho9@hotmail.com

51
Appendix S1. Bird species
Table S1. Bird list species recorded in 19 forest sites in Brazilian Atlantic Forest. The birds are classified according Stotz et al.,
(1996) the trophic guilds where: FRU - frugivores; INS - insectivores; OMN - omnivores; CAR - carnivores; GRA - granivores
and NEC - nectivores. Also, the birds were classified according their forest dependency (Bregman et al.,2014) in F - forest
dependent and NF - non-forest dependent.
Number of sites occurrence
Trophic Total
Family Specie guild Habitat type HFC LFC abundance
Caryothraustes
Cardinalidae canadensis FRU F 1 1 2
Columbidae Geotrygon montana OMN F 1 1
Leptotila verreauxi GRA NF 2 2
Conopophagidae Conopophaga melanops INS F 4 4
Contigidae Carpornis melanocephala FRU F 1 1
Campylorhamphus
Dendrocolapitidade trochilirostris INS F 2 2
Dendrocincla turdina INS F 8 5 39
Glyphorynchus spirurus INS F 9 5 45
Sittasomus griseicapillus INS F 6 2 13
Xiphorhynchus fuscus INS F 7 3 25
Xiphorhynchus guttatus INS F 2 1 5
Falconidae Micrastur ruficollis CAR F 1 1
Fringillidae Euphonia chlorotica FRU NF 2 2
Euphonia violacea FRU NF 3 1 4
Furnariidae Automolus leucophthalmus INS F 2 3
Furnarius leucopus INS NF 1 2
52
Galbulidae Galbula ruficauda INS NF 1 2

Icteridae Cacicus cela FRU F 2 8
Onychorhynchidae Myiobius barbatus INS F 7 1 24
Picidae Veniliornis affinis INS F 3 1 4
Pipridae Ceratopipra rubrocapilla FRU F 9 2 77
Chiroxiphia pareola OMN F 2 2
Dixiphia pipra FRU F 9 3 71
Machaeropterus regulus FRU F 8 1 41
Manacus manacus FRU F 4 6 26
Ramphastidae Pteroglossus aracari FRU F 1 1
Ramphastos vitellinus FRU F 1 1
Rhynchocyclidae Leptopogon amaurocephalus INS F 2 1 4
Mionectes oleagineus FRU F 1 1
Rhynchocyclus olivaceus INS F 1 3
Tolmomyias flaviventris INS F 2 3
Strigidae Glaucidium minutissimum INS F 1 1 2
Thamnophilidae Drymophila squamata INS F 2 1 7
Formicivora grisea INS NF 1 1
Myrmotherula axillaris INS F 1 1
Myrmotherula urosticta INS F 1 1
Pyriglena leucoptera INS F 1 2 7
Taraba major INS NF 1 1
Thamnophilus ambiguus INS F 1 1
Thraupidae Coereba flaveola NEC NF 1 1 2
Dacnis cayana OMN NF 1 1
Saltator maximus INS NF 1 1 3
Sporophila nigricollis GRA NF 1 1
Tangara cyanoventris FRU F 1 1
53
Tiaris fuliginosus GRA NF 1 1

Tityridae Schiffornis turdina OMN F 6 1 13
Trochilidae Clytolaema rubricauda NEC NF 1 1
Eupetomena macroura NEC NF 2 2
Hylocharis chrysura NEC NF 1 1
Phaethornis ruber NEC F 1 1 2
Turdidae Turdus amaurochalinus FRU NF 2 2
Turdus leucomelas INS NF 4 1 6
Turdus rufiventris OMN NF 1 1 2
Tyrannidae Attila spadiceus OMN F 1
Megarynchus pitangua INS NF 2 2
Myiarchus ferox OMN NF 3 3
Rhytipterna simplex INS F 4 2 7
Xenopidae Xenops minutus INS F 1 2 5
Xenops rutilans INS F 2 2
54
Appendix S2. The selection of best scale of landscape effects on response variables.
Since the effect of landscape variables on biodiversity depends on the spatial scale
at which the predictors are measured (i.e. the so-called “scale of effect”; sensu Fahrig
2013; Jackson and Fahrig 2015), we calculate forest cover, total area core, cohesion index
and edge density in 10 different buffer sizes (landscapes), ranging from 100 to 1000 m in
radius. Therefore, landscapes of 100 m (3.1 ha), 200 m (12.6 ha), 300 m (28.3 ha), 400 m
(50.2 ha), 500 m (78.5 ha), 600 m (113 ha), 700 m (153.9 ha), 800 m (201 ha), 900 m
(254.3 ha) and radius of 1,000 m (314 ha). We tested the effect of the landscape metrics
scale on response variables using the multifit function proposed by Huais (2018) for
analysis at various scales. Therefore, the scale of the effect of each landscape predictor
was defined as the size of the landscape within which the landscape-response relationship
is strongest (i.e. with the highest R, see Fahrig 2013; Jackson and Fahrig 2015). Our
results, shown in Figure S.1, highlight the best effect scale for each landscape predictor.
Figure S1. Results of association between landscape size (scale) and the strength of the
relationship (R2 and P-value) between each landscape variable (forest cover, total core
area, cohesion index, and edge density) and several response variables.
55
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hypothesis. 1649–1663. https://doi.org/10.1111/jbi.12130
Huais, P. Y (2018) multifit: An R function for multi-scale analysis in landscape ecology.
Landscape Ecology, 33(7), 1023–1028. https://doi.org/10.1007/s10980-018-0657-5
Jackson, H. B., and Fahrig, L (2013) Habitat Loss and Fragmentation. Encyclopedia of
Biodiversity (Second Edition), 4, 50–58.
https://doi.org/http://dx.doi.org/10.1016/B978-0-12-384719-5.00399-3
Jackson, H. B., and Fahrig, L (2015) Are ecologists conducting research at the optimal
scale? Global Ecology and Biogeography, 24(1), 52–63.
56
Appendix S3. Vegetation complexity.
We used Principal Component Analysis to describe the structure of local

vegetation based on four variables commonly used in ecological studies: (1) density of
woody plants in the understory (50-200 cm tall), (2) density of trees above the understory
with chest height diameter (DBH) ≥ 5 cm, (3) average DBH per tree and (4) canopy
openness (%). The average density of plants in the understory was 209.65 ± 49.44
(standard deviation) per forest site. The average tree density was 78.15 ± 33.95 trees per
forest site. The average DBH per tree was 11.71 ± 2.00 cm and the average canopy
openness was 9.28% ± 2.12% per forest site. The first two axes explained 80.4% of the
total variation in vegetation complexity (Fig. S1). As more than half of the variance
(52.8%) was explained by the PCA 1, we used this axis as a proxy for the complexity of
the vegetation, which was positively related to the density of trees, average DBH and
plant density in the understory and negatively related to the opening of the canopy.
Figure S2. Biplot representation of the Principal Component Analysis to organize the
forest sites based on vegetation structure. Numbers indicate the percentage of forest cover
surrounding each of the 20 forest sites, and red arrows show the predictors of vegetation
complexity: TD (density of trees with diameter at breast height, DBH ≥ 5 cm), UD
(density of understory plants in the), DBH (mean DBH per tree) and CO (canopy
openness).
57
Appendix S4. Spearman’s correlation test between each environmental variable.
We evaluated the correlation between each metric using the Spearman’s correlation coefficient (r), which the values of the coefficient can
vary between -1 (inverse relations) and +1. Therefore, values indicate the magnitude of correlation between the variables, which can be classified
as "weak" (0.1 <| r | < 0.39), “moderate” (0.39 <| r | < 0.69) or “strong” (0.70 <| r | < 1.00) (Schober and Schwarte 2018). In this study, we
adopted a cut-off point for predictor variables that presented values of r ≥ 0.70, indicating a strong correlation between them. In our study, we
created statistical models containing environmental variables that presented values of Spearman’s correlation less than 0.70.
Table S2. Correlation between predictor variables (forest cover, total core area, edge density, fruit availability and vegetation complexity) used in this
study.
Bird group Richness Forest cover Total core area Edge density Cohesion - Vegetation complexity
Complete Forest cover 0 0.976 -0.731 0.789 - 0.678
community Total core area 0.976 0 -0.685 0.731 - 0.644
Edge density -0.731 -0.685 0 -0.874 - -0.491
Cohesion 0.789 0.731 -0.874 0 - 0.525
Vegetation
complexity 0.678 0.644 -0.491 0.525 - 0
Abundance Forest cover Total core area Edge density Cohesion - Vegetation complexity
Forest cover 0 0.976 -0.698 0.84 - 0.678
Total core area 0.976 0 -0.767 0.766 - 0.644
Edge density -0.698 -0.767 0 -0.399 - -0.586
Cohesion 0.84 0.766 -0.399 0 - 0.478
Vegetation
complexity 0.678 0.644 -0.586 0.478 - 0
58
Richness Forest cover Total core area Edge density Cohesion - Vegetation complexity
Non-forest Forest cover 0 0.881 -0.763 0.769 - 0.302
dependent Total core area 0.881 0 -0.93 0.728 - 0.481
Edge density -0.763 -0.93 0 -0.588 - -0.491
Cohesion 0.769 0.728 -0.588 0 - 0.482
Vegetation
complexity 0.302 0.481 -0.491 0.482 - 0
Forest cover 0 0.881 -0.525 0.769 - 0.302
Total core area 0.881 0 -0.847 0.728 - 0.481
Edge density -0.525 -0.847 0 -0.482 - -0.466
Cohesion 0.769 0.728 -0.482 0 - 0.482
Vegetation
complexity 0.302 0.481 -0.466 0.482 - 0
Forest- Forest cover 0 0.977 -0.751 0.904 - 0.665
dependent Total core area 0.977 0 -0.701 0.816 - 0.64
Edge density -0.751 -0.701 0 -0.71 - -0.491
Cohesion 0.904 0.816 -0.71 0 - 0.539
Vegetation
complexity 0.665 0.64 -0.491 0.539 - 0
Forest cover 0 0.977 -0.698 0.84 - 0.678
Total core area 0.977 0 -0.755 0.786 - 0.64
Edge density -0.698 -0.755 0 -0.399 - -0.586
Cohesion 0.84 0.786 -0.399 0 - 0.478
Vegetation
complexity 0.678 0.64 -0.586 0.478 - 0
59
Richness Forest cover Total core area Edge density Cohesion Fruit availability Vegetation complexity
Frugivorous Forest cover 0 0.977 -0.737 0.759 -0.217 0.678
birds Total core area 0.977 0 -0.762 0.723 -0.25 0.64
Edge density -0.737 -0.762 0 -0.627 0.214 -0.466
Cohesion 0.759 0.723 -0.627 0 0.036 0.348
Fruit availability -0.217 -0.25 0.214 0.036 0 -0.281
Vegetation
complexity 0.678 0.64 -0.466 0.348 -0.281 0
Abundance Forest cover Total core area Edge density Cohesion Fruit availability Vegetation complexity
Forest cover 0 0.976 -0.737 0.84 -0.217 0.678
Total core area 0.976 0 -0.74 0.766 -0.267 0.644
Edge density -0.737 -0.74 0 -0.59 0.214 -0.466
Cohesion 0.84 0.766 -0.59 0 -0.024 0.478
Fruit availability -0.217 -0.267 0.214 -0.024 0 -0.281
Vegetation
complexity 0.678 0.644 -0.466 0.478 -0.281 0
Insectivorous
birds Forest cover 0 0.977 -0.75 0.818 - 0.665
Total core area 0.977 0 -0.762 0.753 - 0.64
Edge density -0.75 -0.762 0 -0.71 - -0.466
Cohesion 0.818 0.753 -0.71 0 - 0.525
Vegetation
complexity 0.665 0.64 -0.466 0.525 - 0
Forest cover 0 0.972 -0.7 0.813 - 0.688
Total core area 0.972 0 -0.761 0.749 - 0.644
Edge density -0.7 -0.761 0 0.644 - -0.586
60
Cohesion 0.813 0.749 0.644 0 - 0.478

Vegetation
complexity 0.688 0.644 -0.586 0.478 - 0
References
Schober, P., and L. A. Schwarte (2018) Correlation coefficients: Appropriate use and interpretation. Anesthesia and Analgesia 126: 1763–1768.
https://doi: 10.1213/ANE.0000000000002864
61
Appendix S5. Models with difference in AICc (ΔAICc) between the models less than 2.
Table S3. Results from General Linear Models testing for the effects of local and landscape predictors on the richness and abundance for a total
community and ecological groups. Significant models (P ≤ 0.05) are highlighted in bold.
Bird group Response Models Estimate Std. Error t-value P-value
variable
Complete Richness Total core area +region
community
Intercept 2.129 0.204 10.415 < 0.001
Total core area 0.004 0.001 2.478 0.024
Region -0.438 0.196 -2.230 0.040
Cohesion + region
Intercept -30.953 15.999 -1.935 0.070
Cohesion 0.336 0.160 2.094 0.052
Region -0.434 0.206 -2.113 0.050
Edge density + region
Intercept 2.621 0.115 22.777 < 0.001
Edge density -0.006 0.003 -2.014 0.060
Region -0.507 0.196 -2.585 0.019
Forest cover + region
Intercept 1.977 0.295 6.692 < 0.001
Forest cover 0.008 0.004 2.107 0.050
Region -0.399 0.215 -1.854 0.081
Complete Abundance Total core area + region
community
Intercept 2.958 0.227 13.018 < 0.001
Total core area 0.005 0.002 3.386 0.004
Region -0.659 0.225 -2.924 0.010
Intercept 2.612 0.327 7.989 < 0.001
62
Forest cover 0.014 0.004 3.286 0.004

Region -0.561 0.238 -2.360 0.031
Non-forest Richness Cohesion
dependent
Intercept 41.923 13.667 3.067 0.007
Cohesion -0.418 0.139 -3.015 0.007
Cohesion + region
Intercept 54.377 17.204 3.161 0.006
Cohesion -0.541 0.173 -3.129 0.006
Region -0.574 0.474 -1.210 0.243
Non-forest- Abundance Cohesion
dependent
Intercept 43.805 14.035 3.121 0.006
Cohesion -0.435 0.142 -3.060 0.007
Cohesion + region
Intercept 52.345 17.902 2.924 0.010
Cohesion -0.520 0.180 -2.890 0.010
Region -0.404 0.498 -0.812 0.428
Forest- Richness Forest cover +region
dependent
Intercept 1.354 0.307 4.410 < 0.001
Forest cover 0.014 0.004 3.751 0.002
Region -0.427 0.211 -2.025 0.059
Total core area + region
Intercept 1.737 0.219 7.944 < 0.001
Total core area 0.007 0.002 3.690 0.002
Region -0.523 0.205 -2.549 0.021
Cohesion + region
Intercept -56.858 18.128 -3.137 0.006
Cohesion 0.594 0.182 3.270 0.005
Region -0.413 0.214 -1.929 0.071
Forest- Abundance Cohesion + region
dependent
63
Intercept -77.876 23.635 -3.295 0.004

Cohesion 0.816 0.237 3.445 0.003
Region -0.597 0.237 -2.516 0.022
Cohesion + vegetation complexity +
region
Intercept -71.362 25.221 -2.830 0.012
Cohesion 0.747 0.255 2.933 0.010
Vegetation complexity 0.580 0.841 0.690 0.500
Region -0.515 0.271 -1.903 0.075
Frugivorous Richness Region
birds
Intercept 1.435 0.135 10.665 < 0.001
Region -0.905 0.251 -3.608 0.002
Frugivorous Abundance Cohesion + fruit availability +
birds region
Intercept -5.567e+01 2.785e+01 -1.999 0.063
Cohesion 5.902e-01 2.792e-01 2.114 0.051
Fruit availability -6.700e-04 3.771e-04 -1.777 0.095
Region -1.125e+00 3.308e-01 -3.400 0.004
Forest cover + vegetation
complexity + region
Intercept 2.708 0.597 4.533 < 0.001
Forest cover 0.020 0.007 2.834 0.012
Vegetation complexity -1.813 1.141 -1.590 0.131
Region -1.356 0.377 -3.598 0.002
Total core area + vegetation
complexity + region
Intercept 3.355 0.587 5.719 < 0.001
Total core area 0.008 0.003 2.853 0.012
Region -1.569 0.381 -4.114 0.001
Insectivorous Richness Cohesion
birds
64
Intercept -60.381 16.601 -3.637 0.002

Cohesion 0.623 0.167 3.742 0.002
Cohesion + vegetation complexity
Intercept -45.681 15.945 -2.865 0.011
Cohesion 0.469 0.161 2.906 0.010
Forest cover
Intercept 0.788 0.235 3.346 0.004
Forest cover 0.015 0.003 4.386 0.003
Cohesion + region
Intercept -51.305 16.577 -3.095 0.007
Cohesion 0.534 0.166 3.212 0.005
Region -0.334 0.190 -1.757 0.097
Total core area
Intercept 1.085 0.172 6.319 < 0.001
Total core area 0.008 0.002 4.466 < 0.001
Intercept 1.335 0.208 6.429 < 0.001
Total core area 0.006 0.002 3.532 0.003
Region -0.345 0.190 -1.815 0.087
Intercept 1.053 0.298 3.533 0.003
Forest cover 0.012 0.004 3.263 0.005
Region -0.278 0.204 -1.361 0.191
Insectivorous Abundance Cohesion + vegetation complexity
birds
Intercept -47.972 17.468 -2.746 0.014
Cohesion 0.498 0.177 2.814 0.012
65
Appendix S6. Spatial autocorrelation test.
We tested spatial autocorrelation on residues of plausible models using the Moran's I test (Legendre 1993). From the derivation of a
geographic distance matrix among forest sites, we tested the effect of the distance on the residuals of the models using the x and y coordinates of
the sample sites where the data were collected for generated an inverse distance matrix with the diagonals set to 0 for the Moran's I test in the GLM
model residuals (for more details see Guisan et al. 2017, p 114). This method considers that the values of P ≤ 0.05 indicate the spatial correlation
between the model variables (Gittleman and Kot 2016).

66
Table S4. Spatial autocorrelation test estimated by best models used to explain the effect of local and landscape predictors on
richness and abundance of bird species.
Bird group Response variable Models Std. P-value
Error
Complete community Richness
Total core area +region 0.089 0.740
Cohesion + region 0.091 0.520
Edge density + region 0.091 0.654
Forest cover + region 0.089 0.634
Complete Community Abundance Total core area + region 0.091 0.481
Non-forest dependent Richness Cohesion 0.093 0.080
Non-forest-dependent Abundance Cohesion 0.093 0.024
Forest-dependent Richness Forest cover +region 0.090 0.632
Total core area + region 0.091 0.990
Forest-dependent Abundance Cohesion + region 0.093 0.960
Cohesion + vegetation 0.093 0.897
complexity + region
Frugivorous birds Richness Region 0.091 0.911
Frugivorous birds Abundance Cohesion + fruit 0.093 0.954
availability + region
Forest cover + vegetation 0.092 0.372
complexity + region
67
Total core area + 0.092 0.259

vegetation complexity +
region
Insectivorous birds Richness Cohesion 0.092 0.064
Cohesion + vegetation 0.091 0.133
complexity
Forest cover 0.090 0.141
Total core area 0.089 0.068
Insectivorous birds Abundance Cohesion + vegetation 0.090 0.356
complexity
References
Gittleman, J. L., and Kot, M (2016) Society of Systematic Biologists Adaptation : Statistics and a Null Model for Estimating Phylogenetic Effects
Author ( s ): John L . Gittleman and Mark Kot Published by : Taylor and Francis , Ltd . for the Society of Systematic Biologists Stable URL :
http: 39(3), 227–241.
Guisan, A., Thuiller, W., and Zimmermann, N. E (2017) Habitat suitability and distribution models: With applications in R. In Habitat Suitability
and Distribution Models: With Applications in R. https://doi.org/10.1017/ 9781139028271
68
Capítulo II
69
Tropical forest loss simplifies bird-plant networks in human-modified landscapes
Ícaro Menezes Pinto1*, Carine Emer2, Eliana Cazetta1, Deborah Faria1 and José
Carlos Morante-Filho1*
1
2
Departmento de Ecologia, Instituto de Biociências, Universidade Estadual Paulista, CP 199,
13506-900 Rio Claro, São Paulo, Brazil.
*Corresponding authors: icaro.bio.uesc@gmail.com and jcmfilho9@hotmail.com

70
Abstract
Global biodiversity is threatened by land-use changes through human activities. This is

mainly due to the conversion of continuous forests into forest patches surrounded by
anthropogenic matrices. In general, sensitive species are lost while species adapted to
disturbances succeed in altered environments; however, little is known if species interactions
also are altered with the resulting landscape changes. Here we evaluated how landscape
predictors (forest cover, total core area, edge density and inter-patch isolation) and local
characteristics (fruit availability and vegetation complexity) affected bird-plant interaction
networks in 19 sites located in two regions with different levels of land use disturbance in
the Brazilian Atlantic forest. We used model selection based on the Akaike information
criterion to test the effect of predictor variables on several network metrics (number of
interactions, links per species, interaction evenness, and modularity). We found number of
interactions was positively affected by the amount of forest cover. However, the number of
fruits and vegetation complexity did not affect the bird-plant networks interactions.
Therefore, bird-plant networks with a fewer number of interactions in the more deforested
region. These results demonstrate the importance of forest cover not only to maintain species
diversity but also their respective mutualistic relationships. We also observed the lack of
significant structure in these networks when comparing to the null models, as a consequence
of a pervasive impoverishment of the bird and plant communities in human-modified
landscapes.
Keywords Anthropocene, Brazilian Atlantic Forest, frugivorous birds, habitat structure,
resource availability, seed dispersal
71
1. INTRODUCTION
Over the course of decades forest ecosystems have been converted into small forest
patches surrounded by several types of anthropogenic matrix such as pastures, agricultural
plantations, and urban areas (Laurance et al. 2014; Haddad et al. 2015). Land-use
intensification in natural landscapes leads to a decrease in the habitat amount and an increase
fragmentation of forests, thereby promoting inter-patch isolation while affecting species
dispersal abilities across anthropic matrices (Newbold et al. 2015). In addition, changes in
local abiotic conditions (e.g., increasing light incidence and temperature and decreasing
humidity) along a gradient from edge to forest interior are commonly observed in forest
patches (Murcia 1995; Laurance et al. 2007). The synergy between processes operating at
both the local and landscape scales may result in a marked change in species composition in
those forest patches, in which the loss of sensitive species might be compensated by the
proliferation of species adapted to disturbances (Supp and Ernest 2014; Morante-Filho et al.
2015).
Recent studies indicate that habitat loss and fragmentation strongly determines the
trajectory of the local forest structure (Arroyo-Rodríguez et al. 2017), leading to a
retrogressive succession process, with the simplification of vegetation and predominance of
pioneer plant species (Lôbo et al. 2011; Thier and Wesenberg 2016). This event also leads to
functional erosion of the arboreal community in the long-term, since these disturbances affect
specific traits related to plant reproduction, such as shortening of the floral anthesis period,
and loss of traits related to zoochoric seed dispersal (Marcilio-Silva et al. 2016; Rocha-Santos
et al. 2019). Functional diversity loss of arboreal community in more deforested landscapes
72
might influence the availability and variability of floral, fruit, and seed resources for the
associated fauna increasing their vulnerability to future disturbances (Magnago et al. 2014;
Pessoa et al. 2017). Therefore, forest patches embedded in more deforested landscapes can
have an imminent loss of individuals per species and disrupt important ecological processes
(e.g., pollination and seed dispersal) (Mitchell et al. 2015; Valiente-Banuet et al. 2015).
Frugivorous birds are particularly sensitive to changes in landscape and local
vegetation structure (Galetti et al. 2013; Morante-Filho et al. 2018). The first to disappear are
the larger frugivorous birds, since small forest patches may not provide the amount of
zoochoric fruits needed to keep their populations viable (Donoso et al. 2016; Pessoa et al.
2017). Also, some frugivorous birds may not be able to move among forest patches,
especially species that prefer to live in forest interior away from the influence of forest edges
and open areas. Thus, small forest patches are typically dominated by medium-sized
frugivores/omnivores and edge-specialists able to fly long distances looking for food in
multiple forest patches in order to meet their daily metabolic requirements (Lees and Peres
2009).
Seed-dispersers are essential for the maintenance of plant populations because they
directly influence species gene flow by removing the seeds away from the parent plant and
dropping them at distances where competition for resources is mostly lower (see Janzen-
Connell hypothesis; Janzen 1970, Connell 1971). Hence, an efficient seed dispersal increases
the probability of recruitment of seedlings and as a consequence might increase plant fitness
(Jordano et al. 2006). Animal-plant interactions play a fundamental role in regulating
ecosystem functioning, especially in tropical forests where up to 90% of plant species are
dispersed by animals, mainly birds (Fleming et al. 1987; Markl et al. 2012). Therefore, the
loss of frugivorous birds may affect the structure and regeneration of the forest in human-
73
modified tropical landscapes, with changes in the phenotypic and genetic characteristics of
plant species (Muñoz et al. 2017).
Yet, there is a lack of information about how disturbances at different spatial scales
affect animal-plant interactions such as the mutualistic relationship between frugivorous
birds and the plants (Mitchell et al. 2015; Valiente-Banuet et al. 2015). In those lines,
ecological networks have proven to be an efficient tool to describe how environmental
changes affect the structure, dynamics, and stability of ecosystems (Schleuning et al. 2014;
Vizentin-bugoni et al. 2019). For instance, in more conserved landscapes, habitat and/or diet
specialist species are able to succeed and interact to each other thus increasing the overall
network specialization (Donatti et al. 2011; Schleuning et al. 2014). In contrast, species
homogenization in more disturbed landscapes can concentrate interactions within some
dominant species in the system, reducing interaction evenness (Rodewald et al. 2014).
Similarly, decreasing species abundance or the loss of species can affect the average number
of links per species by reducing the number of partners available for the interactions to occur
(Muñoz et al. 2017; Marjakangas et al. 2019).
Here, we evaluated how landscape structure, as well as local vegetation
characteristics and fruit availability, affected bird-plant interaction networks. We studied 19
forest sites embedded in two regions with contrasting patterns of land use in the Brazilian
Atlantic Forest. Specifically, we estimated for each forest site: the number of interactions
performed by bird and plant species; the mean number of links per species; the interaction
evenness; and the modularity of the bird plant networks. We predicted a decrease in the
number of interactions and on the mean number of links per species as forest amount
decreases and edge densities increases at the landscape scale (Hagen et al. 2012; Pfeifer et
al. 2017). We also predicted that the decrease on the amount of forest core area, along with
74
increasing forest patches isolation and simplification of the local vegetation, would
negatively affect network structure. Therefore, we expected that the reduction of fruit
availability for frugivorous birds associated to the changes in vegetation complexity will lead
to a decrease in the modularity of bird-plant networks located in deforested landscapes due
to the proliferation of habitat-generalist species. Thus, the interactions might be concentrated
within a few dominant birds in the system, consequently decreasing network evenness in
more deforested landscapes.
2.1. Study area
The study region is located in the southeast of the state of Bahia, northeast of Brazil
(Figure 1), a region dominated by the Atlantic Forest. Currently, this region is composed of
different agricultural systems, and forestry uses such as cocoa (Theobroma cacao), rubber
trees (Hevea brasiliensis) and Eucalyptus plantations, as well as cattle pasture areas (Pardini
et al. 2009). The regional climate, according to the classification of Köppen, is Af type, hot
and humid without a well-defined dry season (Gouvêa 1969). The annual averages of
temperature and precipitation are 24°C and 2,000 mm/year respectively, classified as poorly
seasonal, although there is a period of lower rainfall from December-March.
We used high-resolution satellite images (Quick Bird and World View, 2011 and
Rapid Eye, 2009-2010, with resolutions of 0.6, 0.5 and 5 m, respectively) to acquire cloudless
images for the study region. Then, we classified and digitalized land cover features through
ArcGIS software (ESRI 2012) at 1:10,000 scale, which is adequate for identifying patches
based on the visual inspection of color, texture, shape, location, and context. We developed
75
a digital map that covered an area of 3,500 km2 after intensive ground-truthing. Although the
mapped area presents similar soil, topography, and floristic characteristics, the northern
region harbors a high forest cover (HFC, hereafter), 50% of which corresponds to native old-
growth and secondary forest (Morante-Filho et al. 2016).
The landscape matrix in HFC region is highly heterogeneous but is dominated by
shade cacao plantations (22% of the landscape matrix) and rubber trees (10%) (Figure 1). In
contrast, the southern region has a low forest cover (LFC, hereafter), represented by only
30% of forest, with a homogenous matrix predominantly comprised of cattle pastures (86%
to the landscape matrix) and Eucalyptus sp. plantations (7%) (Morante-Filho et al. 2016).
The HFC and LFC region exhibit medium to advanced stages of secondary succession
according to previous floristic surveys (Rocha-Santos et al. 2017).

76
Figure 1. Study area in Southeastern Bahia, Northeastern Brazil. We show the location of the sampling sites
(black dots) and land cover classes in the HFC region (a), with 50% of remaining forest cover, and in LFC
region (b), with 30% of remaining forest cover. In (c) are exhibited six landscapes embedded within a wide
range of landscape native forest cover and different land-cover classes
Based on this mapping, 48 potential sample sites located within forest sites were
previously selected, and subsequently excluded those with limited access, within indigenous
lands, or in the mountainous forest above 500 m a.s.l. (Thomas 2003). Then, we randomly
selected 20 forest sites, embedded within a gradient of forest cover (i.e. excluding cacao
plantations and rubber trees) distributed equally in both regions (Figure 1).
2.2. Landscape metrics and their scales of effect
We used a patch-landscape approach to evaluate the effects of landscape composition
and configuration within a specific area around each sampling site. We used the software
FRAGSTATS 4.2 (McGarigal and Marks, 1995) to estimate one metric of landscape
composition: the percentage of remaining forest (forest cover, hereafter). We also evaluated
three metrics related to landscape configuration: cohesion index (%) that measures the
physical connectedness among forest patches, the total length of forest edge (edge density,
hereafter) and total core area of forest. We considered a distance of 75 m from the edge to
calculate the total core area because previous studies in the region found significant changes
in forest structure (Faria et al. 2009) and in the species composition at this distance (Pardini
et al. 2009). These metrics were chosen because they were previously indicated to influence
richness and composition of bird and plant species in human-modified landscapes
(Martensen et al. 2008; Zurita et al. 2012; Morante-Filho et al. 2015).

77
The effects of landscape variables on biodiversity depends on the spatial scale at
which predictors are measured (Jackson and Fahrig 2015). Thus, we calculated each
landscape metric within 10 different-sized buffers from the center of each site, ranging from
100 to 1,000 m radius (Appendix S1 in Supporting Information) and spaced by at least 1 km
from one another. We used Generalized Linear Models to identify the most appropriate
landscape size (Table S1) to analyze the effect of each landscape metric on several network
metrics (more details below).
2.3. Vegetation structure and fruit availability
We used local variables that are related to the diversity of frugivorous birds in forest
patches and were previously used in other studies in the same forest sites (Rocha-Santos et
al. 2016; Morante-Filho et al. 2018). For this, four plots (25 x 4 m) were randomly located at
each site, with a minimum inter-plots distance of 150 m. From October 2013 to April 2014,
we recorded in each plot (1) all the woody plants in the understory (50-200 cm in height),
and (2) all the trees above the understory layer (diameter at breast height DBH ≥ 5 cm). Then,
we estimated the (3) density of all stems and the mean DBH of all stems (i.e. average DBH
per tree). We also estimated the (4) percentage of canopy openness within the plots using
hemispherical photographs. The photographs were taken at 1.5 m from the soil and analyzed
with Gap Light Analyzer software (Steindl and Troger 1995). These four variables described
above were summarized in an index of vegetation complexity using a Principal Component
Analysis (PCA). The first component of the PCA explained 55.6% of the variation in
vegetation structure and was therefore used as a proxy for vegetation complexity (Appendix
S2).
78
Further, we used five plots (25 x 4 m) located near the mist nets used for bird
sampling, totaling a sampling area of 0.05 ha per site, to estimate the (5) number of fruits
available for birds. The abundance of fruits was estimated in the period of April-September
2017, and October 2017 to April 2018 in the plants between 0.5 and ~ 7 m height, where all
the mature fruits of a branch were counted with the aid of an 8x42 binocular. Then, fruit
number per individual was obtained through the multiplication of the total fruit number of
focal branch by the number of branches with fruits per plant (Blake et al. 1990). These plants
presenting fruits were also collected using pruning shears and exsiccates were made for
identification in the herbarium of the Executive Commission for the Planning of Cacao
Cropland - CEPLAC, with the help of botanical specialist. The fruits were also collected and
stored in alcohol (96%) for comparison with fruits and seeds present in the samples of feces
and food contents of birds.
2.4. Bird and seed survey
We sampled bird assemblages in two field seasons (April-September 2017 and
October 2017 to April 2018), using mist nets to capture birds and get food content samples
(more details below). The license for capture of birds was granted by Ministério do Meio
Ambiente (MMA); Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais
Renováveis (IBAMA); and Sistema de Autorização e Informação em Biodiversidade
(SISBIO); license number 53792-2, authentication code 67798558 and date of issue
06/11/2017; http://www.icmbio.gov.br/sisbio/verificar-autenticidade.html. In each forest
site, we opened 10 mist nets (12 m long, 2.5 m high, 31 mm mesh) to capture birds during
three consecutive days per season. The mist nets were opened from 07:00 h to 17:00 h and
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reviewed every 30 minutes in order to reduce the catch stress. We avoided sampling on rainy
and windy days because such conditions reduce bird movement and therefore may interfere
in capture success. Each captured bird was temporarily marked on one of the right-wing
primary feathers with non-toxic material to avoid recounting the same individual during
sampling. In this study, we used a sampling effort of 60 hours per forest site, totaling 12,000
hours/mist nest by bird sampling. All bird was identified according to the scientific
nomenclature of the South American Classification Committee (Remsen et al. 2014).
We performed oral administration of tartar emetic (1.5% antimony and potassium
tartrate solution), a technique widely used in ecological studies to induce animal to
regurgitate the food content (Poulin et al. 1994). The solution was administered by drip
through a 3 ml disposable needleless syringe using a dosage of 0.8 ml per 100 g of the
corporal mass. After the solution administration, each bird was placed in a cloth bag for 15
minutes to regurgitate and recover from the process, thus reducing stress (Johnson et al.
2002). Recaptured birds during the same sampling period were not re-evaluated. Fecal
samples were collected only when birds defecated in the mist net or inside the cloth bag.
Fecal samples and regurgitated material were stored in alcohol (96%). Then, seeds and fruits
present in food samples were analyzed in a laboratory through a stereoscopic magnifying
glass to identification at the lower taxonomic level, using a seed bank of the Laboratory of
Applied Ecology from the Universidade Estadual de Santa Cruz. In addition, we used
information present in the literature and specific guides for the identification of plants, fruits,
and seeds (Cestari and Pizo 2013).
2.5. Network description

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For each forest site, we built quantitative interaction network defined by a weighted
adjacent matrix Aij in which rows represent the i plant species present in food content of birds
and columns represent j bird species. The aij elements of the matrix represent the frequency
of interactions between i and j. Because networks were relatively small regarding the number
of species, some widely used network metrics were not possible to run, such as nestedness.
Therefore, we used complementary and non-correlated descriptors (Appendix S3) of the
network structure:
(i) total number of interactions, which is the sum of all unique pairwise combinations of bird
and plant species within the sampled community. Here, we used the number of birds per
species that interacted with each seed morphospecies.
(ii) mean number of links per species, which represents the sum of the links divided by the
number of species (Tylianakis et al. 2007);
(iii) interaction evenness, which indicates how interactions are equally distributed among
species within the network. In this metric, values close to 0 indicate that the distribution of
interactions is heterogeneous, with the presence of super-generalist or dominant species in
the system. In contrast, values close to 1 show higher homogeneity in the distribution of
interactions (Blüthgen et al. 2008);
(iv) modularity, which identifies sub-groups of species that interact more strongly among
themselves than with species from other groups. For this network metric we used the
DIRTLPAwb algorithm described in Beckett (2016) that accounts for quantitative
modularity.
2.6. Statistical analyses

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We used data of 19 out of 20 forest sites because no bird was captured at the landscape
with 15% forest cover in the LFC region. Moreover, we only included birds captured with
identifiable seeds or fruit parts in their food content and/or feces. First, we used Spearman’s
test to assess the correlation between all environmental variables. Based on this result,
variables highly correlated (values ≥ 0.70) were not used in the same model (Appendix S4,
Table S3). Then, given that the structure of the ecological networks can be affected by the
number of interactions observed, we used total bird and seed richness by site as an offset
term in the subsequent analyses to control the possible variation in sample completeness on
network metrics (Henriksen et al. 2019).
We used Generalized Linear Models to evaluate how networks metrics are influenced
by different environmental variables. Models testing the effects of environmental variables
on the number of interactions were constructed using the Poisson distribution, while models’
tests for the effects on the number of links per species, evenness and modularity were created
using the normal distribution. In addition, we included the study region as a fixed factor in
the models, as previous studies have observed that contrasting land-use patterns in HFC and
LFC regions affected bird and plant species (Morante-Filho et al. 2016; Rocha-Santos et al.
2017).
All models were subjected to a model selection approach based on Akaike
information criterion corrected for small samples (AICc), using lme4 (Bates et al. 2014) and
bbmle (Bolker 2017) packages. We considered the models equally plausible when the
difference in AICc (ΔAICc) between models was less than 2. We also used the Akaike weight
(ωAICc), which ranges from 0 to 1, and express the normalized relative likelihood of each
model, to select the most plausible model (Anderson 2008). The models that fitted this
criterion are equally plausible to explain the observed patterns. Then, we evaluated the fit of
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the plausible models using ratio between residual deviation and residual degrees of freedom,
where values > 1 indicate overdispersion (McCullagh and Nelder, 1989). We also fitted the
models that presented overdispersion using the negative binomial distribution. Furthermore,
we evaluated the spatial autocorrelation in the residuals of the best models based on Moran's
I autocorrelation coefficient using the ape package (Paradis and Schliep 2019).
Last, we used null models based on the Patefield algorithm ('method = 1' in the
‘nullmodel’ function) to test the significance of the changes in the network descriptors
independently of network size (Appendix S8, Table S9). We created 100 random networks
for each studied site and used z-scores to test whether the observed networks differ
significantly from the random ones regarding the number of links per species, interaction
evenness and modularity. Z-scores where then fitted as the response variable in the same
statistical model structure described above. Network metrics and null models were estimated
using the bipartite package (Dormann et al. 2009). All statistical analyses and graphs were
carried out in R software version 3.5.3 (R Core Team 2019).
3. RESULTS
We captured 185 individuals belonging to 14 families and 28 bird species in the 19
forest sites. The families Pipridae (five species, n = 144 individuals) and Dendrocolapitidae
(five species, n = 12) were the most representative ones, presenting greater abundance and
richness of bird species reported consuming plants’ propagules. The most abundant species
were Ceratopipra rubrocapilla (n = 51) and Dixiphia pipra (n = 51), followed by
Machaeropterus regulus (n = 26), Manacus manacus (n = 15) and Schiffornis turdina (n =
6). Furthermore, we recorded 22 (mean = 5.2 ± SD = 1.69) species in the HFC region and 12
species (mean = 2.22 ± SD = 0.83) in the LFC region, highlighting a significant difference
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in the number of bird species between regions (t = 5.0, df = 13.4, p < 0.001). We recorded in
HFC region 16 exclusive bird species, of this total 6 bird species occur in both regions.
Regarding LFC region, we found 6 exclusive bird species and 6 bird species in common with
HFC region. Overall, 30.837 seeds/fruits distributed in 68 morphospecies were recorded in
bird’s food content. We were able to identify 10 morphospecies at species level and another
13 into genus level. We observed a significant difference in the number of morphospecies
between regions (t = 3.7, df = 11.2, p = 0.003), with 56 morphospecies in the HFC region
(mean = 9.3 ± SD = 4.9), and only 17 morphospecies in the LFC region (mean = 3.2 ± SD =
1.6). Miconia hypoleuca was the only plant species found in all forest sites. Also, 78.6% of
the bird species (n = 22) consumed fruits of this species (n = 28.734 seeds), which can be
considered a key species for bird diet. We recorded a total number of 268 interactions (mean
= 14.1 per site ± SD = 12.98), and larger networks were observed in more forested landscapes
(Figure 2, Appendix S3).

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Figure 2. Bipartite bird-plant networks in 19 forest sites located in the Brazilian Atlantic forest. At the left networks observed in a high forest cover (HFC) and at
the right networks observed in low forest cover (LFC) region. Values represent the percentage (%) of forest cover measured in 800 m radius landscapes. Orange
bars represent bird species and green bars represent the plant species; the frequency of interactions among bird and plant species are represented by the length of
the bars
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Our results showed that seven models were considered equally plausible to explain
the relationship between different environmental variables and the number of interactions
(Table 1, Appendix S5). However, only two models, which consider the region and forest
cover separately, were significant (Table 2, Figure 3).
Table 1. Model selection parameters based on Akaike’s Information Criterion (AIC), used to
explain the relationship between the dependent variables and several environmental predictors
observed in 19 forest sites located in the Brazilian Atlantic Forest. Models are ranked by ΔAICc
values. Here we show only the more plausible models (i.e. when the difference in AICc between
the models was lower than 2). For more details see Appendix S5.
Network metric Models ΔAICc df wi
Number of interactions Region 0.0 2 0.1728
Total core area + vegetation complexity 1.5 4 0.0836
+ region
Vegetation complexity + region 1.9 3 0.0668
Links per species Intercept - 2 1
Evenness Intercept - 2 1
Modularity Intercept - 2 1
ΔAICc: difference of the AICc comparting to the best model; df: number of parameters of the model and wi: AICc
weight
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Table 2. Results from General Linear Models testing for the effects of local and landscape predictors on the number of interactions in
the bird-plant networks. The total number of interactions was the only network descriptor significantly affected by changes in the
landscape variables studied here. Significant models (P ≤ 0.05) are highlighted in bold.
Models Estimate Std. Error Z-value P-value
Region
Intercept 0.427 0.078 5.487 < 0.001
Region -0.535 0.175 -3.064 0.002
Region + forest cover
Intercept 0.113 0.234 0.481 0.631
Forest cover 0.004 0.003 1.442 0.149
Region -0.374 0.204 -1.835 0.067
Forest cover
Intercept -0.179 0.184 -0.975 0.329
Forest cover 0.008 0.003 2.915 0.004
Total core area + vegetation complexity + region
Intercept 0.777 0.307 2.527 0.012
Total core area 0.003 0.001 1.897 0.058
Region -0.620 0.210 -2.950 0.003
Intercept 0.272 0.166 1.636 0.102
Total core area 0.001 0.001 1.074 0.283
Region -0.444 0.193 -2.295 0.022
Cohesion index + region
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Intercept -12.285 12.900 -0.952 0.341

Cohesion index 0.128 0.129 0.986 0.324
Region -0.404 0.215 -1.881 0.060
Vegetation complexity + region
Intercept 0.683 0.336 2.031 0.042
Region -0.640 0.219 -2.918 0.003
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We observed that the number of interactions was positively related to forest amount
at the landscape scale (Figure 3a), with a higher number of interactions recorded in HFC and
LFC region (Figure 3b).
Figure 3. Relationship between the number of interactions in bird-plant networks and predictors variables. (a)
the relationship between forest cover and the number of interactions; (b) the total number of interactions
observed in high forest cover (HFC) and low forest cover (LFC) region.
All 26 models used to explain the variation in the number of interactions at forest sites
showed a good fit (Appendix S6) and did not show spatial autocorrelation (p > 0.05)
(Appendix S7). In contrast, the number of links per species, evenness, and modularity were
not affected by any landscape or local variables evaluated in this study (Appendix S5, Table
S4-S6). Also, when network size was controlled, we found that the number of links per
species, evenness, and modularity did not differ from the null models, indicating the lack of
significant structural proprieties in these bird-plant networks (Appendix S8).

89
4. DISCUSSION
We showed that deforestation strongly affects the size of bird-plant networks,
especially in the more disturbed region, in which the number of interactions between birds
and plants was extremely low in comparison to the more forested region. The observed
reduction in the number of bird-plant interactions reflects the decline or even the loss of bird
population of certain species, as already detect in previous assessments (Morante-Filho et al.
2015). Despite such numeric decline in interactions, no significant structural changes were
observed in both HFC and LFC regions, possibly because these regions encompass highly
impoverished assemblages of bird species that have already lost part of its functionality due
to defaunation of the larger bodied species (Canale et al. 2012). Most important, our study
provides further evidence about the pervasive effects of landscape-scale forest loss, not only
for species richness, but also for animal-plant interactions.
Forest amount at the landscape scale was the best predictor for explaining the
decreased species interactions in our study. We found no effect of total core area, edge
density and cohesion index on the number of interactions or any other network metric.
Previous studies have also reported significant losses in plant diversity in more deforested
landscapes, especially late-successional, shade-tolerant and zoochoric tree species
(Benchimol et al. 2017; Rocha-Santos et al. 2019). Similarly, forest loss has been cited as the
main factor driving frugivores loss in tropical forests (Coster et al. 2015; Morante-Filho et
al. 2018). Recent studies report significant changes in network structure (e.g., higher
nestedness and lower modularity) after loss of habitat area in Atlantic forest sites (Emer et
al. 2019; Marjakangas et al. 2019) or changes in bird functions in deforested landscapes
90
(Coster et al. 2015). Here, we found depleted bird-plant networks with few pairs of species
interacting with each other.
Our results also showed that the number of interactions depends on the regional
context in which forest patches are inserted, with a higher number of interactions recorded in
HFC region. In our study, this region comprises landscapes highly forested, including native
remnants immersed in a biodiversity-friendly matrix such as cocoa agroforestry systems.
Altogether, these features allow a greater diversity of birds and plants in forest patches (Faria
et al. 2006; Sambuichi et al. 2012) and hence a greater number of interactions. In contrast,
the LFC region is composed of small forest patches surrounded mainly by cattle pasture, a
harsh matrix decreasing the regional species diversity (Morante-Filho et al. 2016), thus
inhibiting interactions between birds and plants. Therefore, the land-use intensity can be an
important factor explaining the results observed here.
Changes in composition and structure of the local vegetation, as well as fruit
availability, are known to shape the diversity of frugivores (García et al. 2011; Plein et al.
2013). Previous studies in the same landscapes studied here have found that deforestation
leads to both a simplification in the forest structure and a decrease in fruit biomass (Rocha-
Santos et al. 2016, 2017; Pessoa et al. 2017). Nevertheless, we found no evidence that local
changes in fruit availability or vegetation complexity affected bird-plant networks, possibly
because the most representative bird family recorded (Pipridae), was abundant in all sites.
Despite the decreasing in abundance or even the loss of species such as C. rubrocapilla, D.
pipra, and M. regulus, the abundance of other species such as M. manacus increased in more
disturbed sites. Some forest specialists can persist in highly deforested landscapes, exploring
different anthropogenic habitat types (Ruiz-Gutiérrez et al. 2008; Hansbauer et al. 2010).
Similarly, previous studies revealed a composition turnover among frugivorous birds in our
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studied sites, leading to a compensatory dynamic in which habitat-generalists replaced forest-
specialists as deforestation increases (Morante-Filho et al. 2018). Although there is a
significant reduction in the number of species in the LFC region regarding to HFC, the
captured species showed little diversification in their diet, foraging mainly on the edges of
the forests.
Interestingly, network structure was not affected by any local or landscape variables
assessed here. Again, the mean number of links per species across landscapes might not be
affected due to the fact that the most recorded birds (~77%) belonged to the Pipridae family.
This family is represented by small sized birds that usually feed on a few plant species which,
in our sites, were characterized by pioneer representatives. This strategy may decrease the
need to move between forest sites to obtain fruits. Similarly, we also did not observe changes
in interaction evenness. Therefore, the values of network evenness were mostly high (Table
S2) indicating the predominance of homogeneity in the distribution of interactions between
birds and plants in this study. This result could reflect the low fruit production by plants in
these landscapes (Pessoa et al. 2017). In this situation, bird assemblages heavily rely on the
most abundant resources available, which are mainly the pioneer species (e.g., Miconia
hypoleuca, Miconia mirabilis and Leandra rufescens) commonly observed in bird’s diet.
Indeed, these plant species corresponded to 97% of the seeds observed in the interaction
networks and were recorded in almost all forest sites, regardless environmental differences
in local or landscape-scale here evaluated.
Network modularity was also unaffected by the environmental changes recorded in
the forest sites, indicating that plants and bird did not form subgroups of interacting partners
that connect more strongly to each other than with other sub-groups in the same network
(Donatti et al. 2011; Emer et al. 2018, 2019). In seed dispersal networks, modularity is
92
strongly associated with the similarity of phenotypic traits that limits resource exploitation
(Donatti et al. 2011). In our study, the interaction network is uniform and shaped by small
species (mean body mass = 13 g) consuming and, most likely, dispersing small-seeded plant
species (Silva et al. 2018). Additionally, our region is severally defaunated, with the absence
of large-bodied species such as cracids (IBAMA 2004), which are particularly threatened by
synergetic effect of habitat loss, and the heavy hunting pressure (Canale et al. 2012). The
absence of large-bodied bird species able to disperse large-seeded plant species (Emer et al.
2018) means that these networks lack modules formed by large-bodied interacting species
that would perform specific ecological functions. Thus, the relative low values of modularity
found in our study are explained by both the lack of large-bodied modules and the presence
of a few remaining species that feed on available fruit.
Limitations
Sampling ecological interactions is still a challenge, as it requires prior knowledge of
species (nodes) and robust estimates of interactions (links) between pairs of potential partner
species. In addition, countless biologic or physical factors can contribute to an increase or
decrease in biodiversity in different locations. For instance, spatio-temporal differences in
fruiting in different forest patches throughout the year can influence the distribution of bird
species (Hasui et al. 2012). The forests of the southern region of Bahia studied here have low
biomass of fruits available for avifauna, as was also observed by the low availability of fruits
estimated in this study. We also observed that only 1/3 of the bird species captured here
contained fruits/seeds during the sampling period of this study. In this context, the space-
time decoupling, and the low probability of interspecific encounters between potentially
93
mutualistic species can decrease the chances of registering interactions (forbidden links;
Jordano 2016). Therefore, a relatively low number of interactions can make it difficult to
observe changes in the structure of networks (e.g., nestedness or modularity) (Jordano 2016).
These factors can be more aggravating in studies on a landscape scale that propose to
evaluate networks of interactions in different forest patches at different spatial scales. In
addition, there is no specific method for recording animal-plant interactions, although the use
of mist nets for sampling birds and evaluating their interactions show an efficiency in
characterizing interactions through the identification of fruits/seeds present food content of
birds (Hernández-Montero et al. 2015; Costa et al. 2016, 2020). Therefore, it is important to
know the qualitative and quantitative shortcomings of data coming from mist nets, mainly
because the birds captured by this method, occur mainly in forest understory of forests
(Vecchi and Alves 2015).
Conclusions
Our results revealed a detrimental decrease in the size of bird-plant networks,
triggered by landscape-scale deforestation. Depleted communities often exhibit gaps in
ecosystem functionality through the loss of functional groups and decrease in the number of
interaction partners (Laliberté et al. 2010; Muñoz et al. 2017). However, contrary to our
expectations, the observed impoverishment of bird-plant interactions following deforestation
was not mirrored by changes in network structure. Most of the interactions exclusively
reported in sites immersed in more forested landscapes are shaped by a few small frugivorous
birds and pioneer plants that are abundant and widely distributed in these sites.
The maintenance of network structure despite the variation in species richness and
94
composition among sites can suggest a high functional redundancy among the remaining bird
assemblages, thus assuring the dispersion of a few widespread pioneer species. Yet, networks
are limited to a few plant and small bird species interacting among themselves and are similar
among sites regardless the landscape or local levels of disturbance. Thus, even in our most
preserved forest sites, characterized by a larger number of interacting species, network
structure is functionally similar to those more disturbed forest sites.
5. ACKNOWLEDGEMENTS
We thank Albérico Queiroz, Adrielle Leal, Fabio Soares, Thamyrys Souza and Julia
Perez for their help in the fieldwork; and local landowners for allowing us to work on their
property. We thank Luiz Magnago, Jomar Gomes, and Daniel Piotto for their help in
identifying some plant species. We also thank Jacques Delabie for allowing access at the
laboratory and Mariane Guedes for working with seed morphotyping. We also thank Gil
Reuss and Diogo Caribé for helping to map the study area. We also thank Rufford Small
Grants for Nature Conservation (No. 22426-1), the Universidade Estadual de Santa Cruz (No.
00220.1100.1644/10-2018) FAPESB (No. 0525/2016) and CNPq (No. 563216/2010-7) by
the financial support. This study was financed in part by the Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Financial Code 001.
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Supporting Information
Tropical forest loss simplifies bird-plant networks in human-modified

landscapes
1
2
Departmento de Ecologia, Instituto de Biociências, Universidade Estadual Paulista, CP
199, 13506-900 Rio Claro, São Paulo, Brazil.
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Appendix S1. Scale of landscape effects.
Because the effect of landscape variables on biodiversity depends on the spatial

scale at which predictors are measured (i.e. the so-called “scale of landscape effects”;
sensu Fahrig 2013; Jackson and Fahrig 2013), we calculated forest cover, total area core,
cohesion index and edge density within ten different-sized buffers (i.e. landscapes),
ranging from 100 to 1000-m radius. Thus, we obtained landscapes of 100 m (3.1 ha), 200
m (12.6 ha), 300 m (28.3 ha), 400 m (50.2 ha), 500 m (78.5 ha), 600 m (113 ha), 700 m
(153.9 ha), 800 m (201 ha), 900 m (254.3 ha) and 1000 m radius (314 ha). We tested the
effect of the landscape metrics scale on the response variables using the multifit function
proposed by Huais (2018) for multi-scale analyzes. Therefore, the scale of the effect of
each landscape predictor was defined as the landscape size within which the landscape-
response relationship is strongest (i.e. with highest R² and lowest p valor, see Fahrig 2013;
Jackson and Fahrig 2015). We found that the strength of the relationship between the
number of interactions and predictor variables differed between scales, with number of
interactions having a stronger relationship on the 800-meter scale for forest cover. The
total core area and the cohesion index within each landscape presented a greater
relationship strength in the scale of 900 meters. The edge density showed a stronger effect
on number of interactions at the 400-meter scale. In relation to the number of links per
species, the forest cover presented a stronger relationship at the 1000-m scale. Also, the
scale of the effect of total area core, cohesion index and edge density on number of links
was, respectively, 1000m, 900m and 400m. The interaction evenness presented a stronger
relationship for the forest cover in the 100-m scale, the scale of the effect of the total core
area, cohesion index and edge density were respectively, 200m, 400m, and 200m. The
modularity presented a stronger relationship for the forest cover in the 1000m scale, and
best scale for total core area, cohesion index, and edge density was, respectively, 1000m,
800m, and 1000m.
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Figure S1. Results of association between landscape size (scale) and the strength of the relationship (R2 and P-value) between each landscape
variable (total core area, forest cover, edge density and cohesion index) and number of interactions, links per species, evenness and modularity.
We also present best-scale for z-score values. The landscape size used in this study is indicated in bold
References
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Huais, P. Y (2018) multifit: An R function for multi-scale analysis in landscape ecology. Landscape Ecology, 33(7), 1023–1028.
https://doi.org/10.1007/s10980-018-0657-5
Jackson, H. B., and Fahrig, L (2013) Habitat Loss and Fragmentation. Encyclopedia of Biodiversity (Second Edition), 4, 50–58.
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Jackson, H. B., and Fahrig, L (2015) Are ecologists conducting research at the optimal scale? Global Ecology and Biogeography, 24(1), 52–63.
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Appendix S2. Vegetation complexity index.
We used a Principal Component Analysis to describe the local vegetation structure

based on four variables commonly used in ecological studies: (1) density of woody plants
in the understory (50-200 cm in height), (2) density of trees above the understory with
diameter at breast height (DBH) ≥ 5 cm, (3) mean DBH per tree and (4) canopy openness
(%). The mean density of understory plants was 211.16 ± 50.32 (standard deviation)
plants per forest site. The mean density of trees was 79.58 ± 34.25 trees per site. The
mean DBH per tree was 11.77 ± 2.04 cm and the mean canopy openness was 9.41% ±
2.09% per site. The first two axes explained 82.4% of the total variance in vegetation
complexity (Fig. S1). As the largest variance (54.6%) was explained by PCA 1, we used
this axis as a proxy for vegetation complexity, which was positively related to the density
of trees, mean DBH and plants density in the understory and negatively related to the
canopy openness.
Figure S2. Biplot representation of the Principal Component Analysis to organize the
forest sites based on vegetation structure. Numbers indicate the percentage of forest cover
surrounding each of the 19 forest sites, and red arrows show the predictors of vegetation
complexity: TD (density of trees with diameter at breast height, DBH ≥ 5 cm), UD
(density of understory plants), DBH (mean DBH per tree) and CO (canopy openness)
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Appendix S3. Network metrics.
Table S1. Network descriptors estimated for the bird-plant interaction networks from the Brazilian Atlantic Forest.
Region* Number of Links Links per Evenness Evenness Modularity Modularity Bird Plant Network
interactions per species (z- (z-score) (z-score) species species size
species score)
HFC 18 1.00 0.18 0.65 0.28 0.24 0.18 6 5 11
HFC 13 0.88 -0.38 0.66 0.53 0.24 0.50 4 4 8
HFC 20 1.00 1.44 0.68 1.18 0.35 0.08 4 12 16
HFC 13 1.11 1.26 0.74 1.19 0.21 0.08 4 5 9
HFC 28 0.92 0.37 0.61 0.66 0.53 0.53 8 16 24
HFC 47 0.96 -0.69 0.53 -0.85 0.27 0.37 7 17 24
HFC 24 0.92 -0.07 0.58 0.93 0.24 0.28 5 8 13
HFC 41 0.90 -0.77 0.51 -1.21 0.28 0.31 7 13 20
HFC 5 0.71 0.68 0.65 0.71 0.44 - 3 4 7
HFC 15 1.00 0.89 0.70 0.97 0.35 0.30 4 9 13
LFC 8 0.78 -0.80 0.72 -1.06 0.47 - 2 7 9
LFC 7 0.80 - 0.71 0.37 0.24 0.72 2 3 5
LFC 4 0.67 0.37 0.63 0.43 0.44 - 3 3 6
LFC 6 0.67 -0.94 0.60 -1.02 0.28 0.96 2 4 6
LFC 3 0.60 - 0.61 - 0.44 - 2 3 5
LFC 6 0.86 - 0.72 - - - 4 3 7
LFC 5 0.80 0.81 0.74 0.78 0.16 0.19 2 3 5
LFC 1 0.50 - - - - - 1 1 2
LFC 4 0.75 0.62 0.75 0.62 0.13 0.27 2 2 4
Mean 14.11 0.83 0.20 0.66 0.28 0.31 0.37 3.79 6.42 10.21
Std.deviation 12.98 0.16 0.77 0.07 0.83 0.12 0.25 2.02 4.81 6.57
* HFC: high forest cover region; LFC: low forest cover region.
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Appendix S4. Spearman’s correlation test between each environmental variable.
We evaluated the correlation between each network metric using the Spearman’s correlation coefficient (r), which the values of the
coefficient can vary between -1 (inverse relations) and +1. Thus, values indicate the magnitude of correlation between the variables, which can be
classified as "weak" (0.1 <| r | < 0.39), “moderate” (0.39 <| r | < 0.69) or “strong” (0.70 <| r | < 1.00) (Schober and Schwarte 2018). In this study,
we adopted a cut-off point for predictor variables that presented values of r ≥ 0.70, indicating a strong correlation between them. In our study, we
created statistical models containing environmental variables that presented values of Spearman’s correlation less than 0.70.
Table S2. Spearman’s correlation test between different predictor variables (forest cover, total core area, cohesion index, edge density, fruit
availability, and vegetation complexity) used in this study.
Fruit Vegetation
Number of interactions Forest cover Total core area Cohesion index Edge density
availability complexity
Forest cover (800 m) 0.97 0.87 -0.73 -0.29 0.70
Total core area (900 m) 0.97 0.78 -0.79 -0.34 0.68
Cohesion index (900 m) 0.87 0.78 -0.43 -0.18 0.55
Edge density (400 m) -0.73 -0.79 -0.43 0.32 -0.69
Fruit availability -0.29 -0.34 -0.18 0.32 -0.44
Vegetation complexity 0.70 0.68 0.55 -0.69 -0.44
Links per species
Forest cover (1000 m) 0.97 0.85 -0.72 -0.37 0.74
Total core area (1000 m) 0.97 0.77 -0.78 -0.37 0.69
Cohesion index (900 m) 0.85 0.77 -0.43 -0.18 0.55
Edge density (400 m) -0.72 -0.78 -0.43 0.32 -0.69
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Evenness
Forest cover (100 m) 0.86 0.83 -0.44 0.02 0.11
Total core area (200 m) 0.86 0.78 -0.82 -0.14 0.37
Cohesion index (400 m) 0.83 0.78 -0.48 0.05 0.33
Edge density (200 m) -0.44 -0.82 -0.4 0.35 -0.54
Fruit availability 0.02 -0.14 0.05 0.35 -0.44
Modularity
Forest cover (1000 m) 0.97 0.86 -0.27 -0.37 0.74
Total core area (1000 m) 0.97 0.78 -0.48 -0.37 0.69
Cohesion index (800 m) 0.86 0.78 -0.03 -0.18 0.56
Edge density (1000 m) -0.27 -0.48 -0.03 0.09 -0.03
References
Schober, P., and L. A. Schwarte (2018) Correlation coefficients: Appropriate use and interpretation. Anesthesia and Analgesia 126: 1763–1768.
https://doi: 10.1213/ANE.0000000000002864
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Appendix S5. Models used to explain the relationship between the metrics of bird-plant
networks and several environmental variables recorded in this study.
Table S3. Models used to explain the relationship between the number of interactions and
several environmental variables observed in 19 forest sites located in the Brazilian Atlantic
forest. The most parsimonious models are highlighted in bold.
Models ΔAICc df wi
Region 0.0 2 0.1728
Total core area + vegetation complexity + region 1.5 4 0.0836
Cohesion index + region 1.6 3 0.0759
Vegetation complexity + region 1.9 3 0.0668
Edge density + region 2.4 3 0.0518
Fruit availability + region 2.8 3 0.0428
Cohesion index 2.9 2 0.0396
Cohesion index + vegetation complexity + region 3.4 4 0.0311
Forest cover + fruit availability + region 3.7 4 0.0273
Forest cover + fruit availability 4.3 3 0.0204
Total core area + fruit availability + region 4.8 4 0.0156
Cohesion index + fruit availability + region 4.9 4 0.0151
Total core area 5.1 2 0.0132
Edge density + fruit availability + region 5.7 4 0.0102
Cohesion index + fruit availability 5.7 3 0.0101
Cohesion index + vegetation complexity 5.7 3 0.0098
Total core area + vegetation complexity 7.7 3 0.0036
Total core area + fruit availability 8.0 3 0.0032
Edge density 8.5 2 0.0025
Vegetation complexity 10.2 2 0.0011
Edge density + fruit availability 11.1 3 <0.001
Fruit availability 11.1 2 <0.001
Null model 169.7 1 <0.001
ΔAICc: difference of the AICc of the best model; df: number of parameters of the model and
wi: AICc weight.
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Table S4. Models used to explain the relationship between the links per species and several
environmental variables observed in 19 forest sites located in the Brazilian Atlantic forest. The
most parsimonious models are highlighted in bold.
Models ΔAICc df wi
Null model 0.0 2 1
Edge density + vegetation complexity + region 36.2 5 <0.001
Region 36.9 3 <0.001
Cohesion index + region 37.3 4 <0.001
Vegetation complexity + region 38.4 4 <0.001
Forest cover + region 39.5 4 <0.001
Edge density + region 39.7 4 <0.001
Fruit availability + region 39.8 4 <0.001
Total core area + region 40.1 4 <0.001
Cohesion index + fruit availability + region 40.2 5 <0.001
Cohesion index + vegetation complexity + region 40.3 5 <0.001
Total core area + vegetation complexity + region 41.5 5 <0.001
Forest cover + fruit availability + region 42.3 5 <0.001
Edge density + fruit availability + region 43.3 5 <0.001
Total core area + fruit availability + region 43.4 5 <0.001
Edge density 48.1 3 <0.001
Total core area 48.5 3 <0.001
Vegetation complexity 48.6 3 <0.001
Forest cover 48.6 3 <0.001
Cohesion index 49.4 3 <0.001
Edge density + vegetation complexity 51.3 4 <0.001
Total core area + vegetation complexity 51.6 4 <0.001
Total core area + fruit availability 51.7 4 <0.001
Forest cover + fruit availability 51.8 4 <0.001
Cohesion index + vegetation complexity 51.8 4 <0.001
Cohesion index + fruit availability 52.4 4 <0.001
ΔAICc: difference of the AICc of the best model; df: number of parameters of the model and wi:
AICc weight.
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Table S5. Models used to explain the relationship between the interaction evenness and
several environmental variables observed in 19 forest sites located in the Brazilian Atlantic
forest. The most parsimonious models are highlighted in bold.
Models ΔAICc df wi
Null model 0.0 2 1
Region 64.2 3 <0.001
Forest cover + vegetation complexity + region 68.9 5 <0.001
Cohesion + fruit availability + region 69.7 5 <0.001
Cohesion index + vegetation complexity + 70.2 5 <0.001
region
Cohesion + fruit availability 80.5 4 <0.001
Forest cover + vegetation complexity 80.6 4 <0.001
ΔAICc: difference of the AICc of the best model; df: number of parameters of the model
and wi: AICc weight.
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Table S6. Models used to explain the relationship between the modularity and several
environmental variables observed in 19 forest sites located in the Brazilian Atlantic forest.
The most parsimonious models are highlighted in bold.
Models ΔAICc df wi
Null model 0.0 2 1
Region 39.3 3 <0.001
Cohesion index + fruit availability + region 42.8 5 <0.001
Cohesion index + vegetation complexity + 46.0 5 <0.001
region
Cohesion index + fruit availability 56.1 4 <0.001
ΔAICc: difference of the AICc of the best model; df: number of parameters of the model and
wi: AICc weight
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Appendix S6. Overdispersion test for statistical models.
We used generalized linear models to evaluate how the response variables are related to
the environmental predictors using the Poisson distribution for the number of interactions and
the Normal distribution for the links per species, modularity, and evenness. We evaluated the
adjustments of best models using the ratio between residual deviation (φ) and residual degrees
of freedom (df), where values > 1 indicate an overdispersion (Crawley 2002). The
overdispersion occurs when the data present greater than expected variance, resulting in an
inflated residual deviation (McCullagh and Nelder 1989; Crawley 2002). Often, this happens
when one or more factors that influence the measured variable were not considered in the
model, when the modeled probability behaves like a random variable, or when specifying an
incorrect error distribution (Carruthers et al. 2008). Thus, we adjusted the models that presented
an overdispersion φ/df > 1 using the negative binomial distribution and re-evaluated if they
presented a good fit.
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Table S7. Adjustment tests for best models using the ratio between residual deviation (φ) and
residual degrees of freedom (df).
Network metric Models φ/df Poisson φ/df Binomial negative
Number of Region 1.04 0.82

interactions Forest cover + region 0.96 0.82
Total core area + vegetation 0.88 0.88

complexity + region
Vegetation complexity + region 1.05 0.90
Network metric Models φ/df Normal φ/df Binomial negative

Links per species Intercept - -
Interaction Intercept - -
evenness
Modularity Intercept - -
φ/df: values > 1 indicate overdispersion.
References
Carruthers, E., Lewis, K., McCue, T., and Westley, P (2008) Generalized linear models: model
selection, diagnostics, and overdispersion. Memorial University of Newfoundland.
https://www.mun.ca/biology/dschneider/b7932/B7932Final4Mar2008.pdf/ (acessed
february 2020)
Crawley, MJ (2002) Statistical computing: An Introduction to Data Analysis using S-Plus.
Wiley, New York.
McCullagh, P. and Nelder, J. A. (1989) Generalized Linear Models, Vol. 37 of Monographs on
Statistics and Applied Probability, 2 edn, Chapman and Hall, London
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Appendix S7. Spatial autocorrelation test.
We tested spatial autocorrelation on residues of plausible models using the Moran's I

test (Legendre 1993). From the derivation of a geographic distance matrix among forest sites,
we tested the effect of the distance on the residuals of the models. Here, we use the x and y
coordinates of the sample sites where the data were collected. From this point, we generated an
inverse distance matrix with the diagonals set to 0 for the Moran's I test in the GLM model
residuals (Guisan et al. 2017). This method considers that the values of P ≤ 0.05 indicate spatial
correlation between the model variables (Gittleman and Kot, 2016).
Table S8. Spatial autocorrelation test estimated by best models used to explain the
effect of several environmental predictors on number of interactions.
Models Moran’s I P-value Std. Moran’s I
Region 0.23 0.09
Total core area + vegetation 0.31 0.09
complexity + region
Vegetation complexity + region 0.38 0.09
References
Gittleman, J. L., and Kot, M. 2016. Society of Systematic Biologists Adaptation : Statistics and
a Null Model for Estimating Phylogenetic Effects Author (s): John L . Gittleman and Mark
Kot Published by : Taylor and Francis , Ltd . for the Society of Systematic Biologists
Stable URL : http: 39(3), 227–241.
Guisan, A., Thuiller, W., and Zimmermann, N. E (2017) Habitat suitability and distribution
models: With applications in R. In Habitat Suitability and Distribution Models: With
Applications in R. https://doi.org/10.1017/ 9781139028271
Legendre, P (1993) Spatial Autocorrelation: Trouble or New Paradigm? Author (s): Pierre
Legendre Published by: Ecological Society of America Spatial Autocorrelation: trouble or
new paradigm? Ecology, 74(6), 1659–1673.
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Appendix S8. Standardized z-scores.
Indexes for the different nulls (as we have already done with the observed networks: links per
species, interactions evenness, and modularity) created by each type of null model (Z-score)
(Dorman et al. 2009).
Table S9. Standardized z-scores for comparing the observed networks with the null networks
and your P-values (p ≤ 0.05).
P-value
Region Number of Links per species Interaction Modularity (z-
interactions (z-score) evenness (z-score) score)
HFC 18 0.857 0.782 0.857
HFC 13 0.702 0.597 0 .617
HFC 20 0.151 0.236 0.936
HFC 13 0.206 0.235 0.936
HFC 28 0.709 0.508 0.596
HFC 47 0.490 0.397 0.711
HFC 24 0.944 0.352 0.780
HFC 41 0.441 0.226 0 .757
HFC 5 0.495 0.475 -
HFC 15 0.375 0.331 0.764
LFC 8 0.426 0.291 -
LFC 7 - 0.713 0.471
LFC 4 0.713 0.664 =
LFC 6 0.349 0.310 0 .337
LFC 3 - - -
LFC 6 - - -
LFC 5 0.417 0.436 0 .849
LFC 1 - - -
LFC 4 0.535 0.535 0 .787
References
Dormann CF, Frund J, Bluthgen N, Gruber B (2009) Indices, Graphs and Null Models:
Analyzing Bipartite Ecological Networks. The Open Ecology Journal 2:7–24.
https://doi.org/10.2174/1874213000902010007
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Capítulo III
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Environmental predictors of beta diversity of bird-plant networks in the

threatened Brazilian Atlantic forest
1
2

Abstract
Global changes in land use induced by human activities have increasingly shaped species
assemblages and their ecological functions, especially in tropical forests. In general, the
species more vulnerable to habitat disturbances undertake a decrease in their populations,
eventually becoming locally extinct, while habitat generalist species may persist or thrive
in human-modified landscapes. These changes in species composition can lead to
disruptions in ecological interactions, increasing dissimilarity levels between interaction
networks inserted in disturbed habitats. Here, we evaluated how local modifications in
vegetation features and fruit availability, as well as changes in landscape structure, affect
β-diversity of understory frugivorous birds and fruiting plant species, and their
interactions, in 18 forest sites located in two regions with contrasting levels of
deforestation and intensity of land use in the Brazilian Atlantic forest. Then, we used β-
diversity matrices to relationship with landscape-scale (e.g., forest cover, total core area,
edge density and inter-patch isolation) and local (e.g., fruit availability and vegetation
complexity) predictors using Mantel tests. We found that forest sites immersed in highly
disturbed landscapes are still able to maintain high β-diversity of birds, plants, and
interactions in contrast to forest sites immersed in more forested landscapes. Also, we
observed that in more forested region the β-birds was positively influenced by
geographical distance between forest sites, amount of pasture cover and fruit number.
Conversely, in more disturbed region, the connectivity among forest sites was the only
predictive variable that positively influence β-diversity of birds. Regarding plant
communities, the β-diversity of plants was not affected by any predictor. The β-diversity
of interactions between frugivorous birds and plants was positively affected by cohesion
and the number of trees in more deforested region.
Key words
Edge effect, frugivorous birds, mutualistic interaction, seed dispersal, tropical forest loss
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1.INTRODUCTION
Natural environments around the world suffer frequent changes in their size and
spatial distribution resulting from human activities, such as urbanization, agriculture and
livestock (Haddad et al. 2015). These disturbances have been causing a sharp decline in
biodiversity, mainly of species highly sensitive to changes in habitat characteristics
(Püttker et al. 2020). For instance, many native species of plants and animals experience
high declines in their populations, with several studies revealing the causal link to habitat
loss and fragmentation (Schmiegelow and Mönkkönen 2002; Vellend 2003). Specifically
in tropical forests, these disturbances create forest sites of different sizes, levels of
disturbance and isolation, in general inserted in agricultural matrix (Ewers and Didham
2006; Boesing et al. 2018). In addition, forest loss and fragmentation have led not only to
significant species losses, but also to changes in the composition of remaining species
and their interactions (Neuschulz et al. 2011; Carlo and Morales 2016). However, the link
between the causes and consequences of changes in species composition in human-
modified landscapes is complex, mainly because species assemblages and their
interactions are shaped by a myriad of factors, such as environmental heterogeneity,
competition and/or dispersal capacity (Plein et al. 2013; Mori et al. 2018), often acting in
synergy (Brook et al. 2008).
Studies have revealed that changes in natural landscapes can lead to two possible
scenarios: biotic homogenization or differentiation (Tscharntke et al. 2012; Socolar et al.
2016). In the former, human disturbance can increase the similarity of species
composition in local communities, decreasing beta-diversity leading to biological
homogenization (Smart et al. 2006). For instance, forest loss can act as an environmental
filter selecting only species that have inherent biological characteristics (e.g., habitat
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generalists, diversified diet and species with high mobility) apt to persist in highly
disturbed habitats (Carlo and Morales 2016; Barros et al. 2019a). In contrast, in the latter,
biotic differentiation, i.e., an increase of beta-diversity, can occur when the community is
composed by unique subsets of species differing from other communities (Socolar et al.
2016). These two possible scenarios may be related to the historical disturbance of the
landscapes, intensity of disturbance, and conservation level of the remaining forest (e.g.,
habitat quality), which can preserve sensitive species in smaller forest sites (Joly et al.
2014; Johnson et al. 2017). Indeed, increases in beta diversity not only affect the species
pool in more disturbed habitats, but can also disrupt ecological functions (Mori et al.
2018).
Recent studies have reported that mutualistic relationships between animals and
plants in highly altered habitats are also affected by non-random species loss, becoming
more simplified and dominated by generalist species (Emer et al. 2018, 2019b).
Therefore, understand how changes in animal and plant networks can impact ecosystem
functionality remains a challenge for the conservation, especially because the
maintenance of multiple functions requires different sets of local species assemblages,
i.e., high β-diversity (García 2016; Emer et al. 2018; Mori et al. 2018). In fact,
conservation practitioners have highlighted the dire need for a better understanding of the
diversity patterns along environmental gradients to better evaluate the different
components of diversity (Baselga 2017). For instance, the total richness of a specific
region (i.e. gamma (γ) diversity) can be separated into two other components: alpha (α)
diversity, which represents the diversity of species in a local habitat, and beta (β)
diversity, which reflects the difference in species composition between sites (Whittaker
1972; Myers et al. 2013). The knowledge of the actual contribution of differences in bird
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assemblages attributed to the within (a) and among forest sites (β) to landscape-scale
diversity (gamma) is key to adequately support conservation actions.
Similarly, β-diversity of interactions can also be measured through the
dissimilarity between interaction networks, allowing to assess how interactions between
species vary over time and space (Poisot et al. 2012). For instance, Emer et al. (2018)
highlighted that although Brazilian Atlantic Forest have undergone strong anthropogenic
pressure, forest patches are still able to maintain high β-diversity of birds which translated
into a high β-diversity of interactions among plant and bird, despite the decrease in the
number of interactions. Therefore, a high β-diversity of interactions can be maintained
due to the unique assemblages of bird persisting in habitats under strong, and often
chronic, anthropogenic disturbance (Tabarelli et al. 2012). Therefore, ecological
networks of animal-plant interactions can be affected by the restrictions imposed by local
characteristics and landscape changes (García 2016; Emer et al. 2018). Indeed, assessing
β-diversity of interactions have been fundamental to understanding the ecological
communities responses in the face of anthropogenic changes (Emer et al. 2018),
contributing thus to conservation of anthropogenic landscapes that still harbor high
biodiversity (Li et al. 2019). However, more information is needed on how the
mechanisms that maintain a high β-diversity of species and interactions in human-
modified landscapes operate at the different spatial (Socolar et al. 2016).
Here, we assess how differences in local features such as vegetation structure and
fruit availability, as well as changes in landscape structure, affect the β-diversity of
frugivorous birds, fruiting plants, and their interactions. Our study was carried out in 18
forest areas located in two regions with contrasting land use patterns in the Brazilian
Atlantic Forest. We predicted that decreases in forest cover and forest patches more
isolated would lead to a differentiation in the biological community, reflecting in a high
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β-diversity of birds (Morante-Filho et al. 2016; Barros et al. 2019b), plants (Farah et al.
2017) and plant-frugivore interactions (Carlo and Morales 2016; Emer et al. 2018). We
also predicted an increase in β-diversity of birds, plants and interactions in sites that show
greater differences between the total core area and edge density (Boesing et al. 2018).
Therefore, the loss of forest cover and decrease in total core area implies in a decrease in
the number of species; affecting the interactions between frugivorous birds and plants
(Emer et al. 2019b). In addition, the associated edge effects may attract habitat generalist
species, increasing the β-diversity of birds, plants, and interactions (Molina Melo et al.
2016; Barros et al. 2019a). We also predicted that a simplification of the vegetation
structure, i.e., forests composed of few trees that have smaller height and diameter, more
open canopies and with a greater number of plants in the understory, would negatively
affect β-diversity of plants, birds and interactions (Watson et al. 2004; Neuschulz et al.
2011; Muñoz et al. 2017; Emer et al. 2018). In addition, we predicted that a variation in
the availability of fruits should attract different dispersers, increasing therefore β-
diversity of birds and interactions (Murcia 1995; Lôbo et al. 2011; Hagen et al. 2012;
Morante-Filho et al. 2018). Finally, we predicted that the total richness of birds and plants
would positively affect the β-diversity of interactions (Emer et al. 2018).
2.1. Study area
This study was conducted in the southeastern region of the state of Bahia,
northeastern Brazil (Fig. 1), formed by the Atlantic Forest biome. The Brazilian Atlantic
Forest is a biome highly fragmented and presents forest mosaics with different stages of
ecological succession (e.g., old-growth and secondary forests) (Thomas et al. 1998;
Ribeiro et al. 2009; Joly et al. 2014). Additionally, this region is composed by various
types of land-use such as agroforestry systems like cocoa (Theobroma cacao), rubber tree
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(Hevea brasiliensis) plantations, Eucalyptus spp., and cattle pastures (Appendix S1, Fig
S3). The northern region has a higher forest cover (HFC region) where 50% of which
corresponds to old-growth and secondary forests concentrated mainly around the Una
Biological Reserve and the Una Wildlife Refuge, two conservation units that have a total
area of 34.804 ha (Morante-Filho et al. 2016). The matrix in the HFC region is highly
heterogeneous and dominated by shade cocoa plantations (22% of the landscape matrix)
and rubber trees (10%). In contrast, the southern region present low forest cover (only
30% of the forest amount; LFC region), with a homogeneous matrix predominantly
composed by cattle pastures (86%) and Eucalyptus spp. (7%) (Morante-Filho et al. 2016).
The HFC and LFC mapped areas have similar soil characteristics, topography and
floristic composition (Benchimol et al. 2017). The regional climate, according to the
Köppen classification, is Af type, hot and humid with annual average temperature of 24
° C and precipitation of 2.000 mm/year. There is no well-defined dry season throughout
the year, although there is a period of lower rainfall from December to March (Gouvêa
1969).
We used high-resolution satellite images with resolutions of 0.6, 0.5 and 5 m,
obtained from Quick Bird and World View, 2011 and Rapid Eye, 2009-2010,
respectively. We classify land use types using ArcGIS software (ESRI 2012). We used 1:
10,000 scale which is considered adequate to identify vegetation patches based on visual
inspection of color, texture, shape, location, and context (Figure 1; for more details see
Appendix S1 in Supporting Information). Therefore, we classify forest types according
to the typologies of the Instituto Brasileiro de Geografia e Estatística (IBGE 2006) and
produce a digital map covering an area of 3.500 km² (central coordinates - 15º28'S and
39º15'W).
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Figure 1. Study area in southern Bahia, Brazil, depicting the types of land cover classes, the high forest
cover region (a), with 50% of the remaining forest cover, and the low forest cover region (b), with 30% of
the remaining forest cover. The forest sites in each landscape are shown with black dots.
Based on this mapping, 48 forest sites were previously selected as potential sites
for data collection. Then, we excluded those sites with limited access, such as forest sites
that are part of indigenous lands or located in mountainous areas (Thomas 2003). We
randomly selected 18 forest sites larger than 3 ha, spaced at least 1.3 km apart, and
distributed across these regions with different land use patterns (Fig. 1). The geographic
distance among sites was not similar in both region (Student t-test; t = -1.97, p-value =
0.054), ranging from 1.53 to 26.89 km in HFC region (14.14 ± 5.92 km, mean ± SE) and
from 1.34 to 31.84 km in LFC region (17.23 ± 7.36 km).
2.2. Landscape metrics and scale of effect
We adopted the patch-landscape approach (sensu McGarigal and Cushman 2002)
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to evaluate the effects of landscape variables on a specific area around each sampling site.
We used FRAGSTATS 4.2 software (McGarigal et al. 2012) to estimate (1) the
percentage of forest cover, (2) pasture cover and (3) the total core area of the fragments
at a fixed distance of 75 m from the edge (Appendix S1, Fig S1). We adopted this distance
because previous studies in the region found significant changes in forest structure (Faria
et al. 2009) and in the composition of ecological groups up to 75 m of the forest edge
(Pardini et al. 2009). In addition, we calculated the landscape cohesion index that
increases simultaneously as the proportion of forest patches in landscape also increased
or as the physical connectedness between forest patches decreases (less connection
between forest patches 0 ≤ cohesion index < 100; more connection between forest
patches), and the total density of forest edge at the landscape. We selected these metrics
because they can influence the richness and composition of bird and plant species in
human-modified landscapes (Laurance 2007; Martensen et al. 2008; Zurita et al. 2012;
Molina Melo et al. 2016).
Since biodiversity responses associated with landscape predictors may vary at
different spatial scales (Fahrig 2013; Jackson and Fahrig 2015), we calculated each
landscape metric on 10 buffers of different size, varied 100 to 1.000 m, from the center
of each forest site (Appendix S2; Figs S4, S5 and S6). We used linear regressions to
identify the landscape size most appropriate to assess the effect of each landscape
predictor on the richness of birds, plants, and interactions (see results in Appendix S2).
Therefore, we used the appropriate size of each predictor’s variable on a landscape-scale
to contrast with the β-diversity of birds, plants, and interactions.
2.3. Vegetation complexity and fruit availability
We selected local variables related to the diversity of frugivorous birds and plants
in forest sites (see Rocha-Santos et al. 2016, Morante-Filho et al. 2018). In each site, we
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evaluated local characteristics using four plots (25 x 4 m), with a minimum distance of
150 m between them (Appendix S1, Fig S2). From October 2013 to April 2014, we
recorded in each plot all (1) understory woody plants (50-200 cm high) and (2) all trees
above the understory stratum (diameter at breast height DBH ≥ 5 cm). Then, we estimated
the (3) mean DBH of all tree (i.e. mean DBH per tree) and (4) percentage of canopy
openness in the plots by hemispheric photographs (Nikon Coolpix 4300 digital camera
equipped with a fisheye lens [Nikon Corp., Tochigi, Japan]). One hemispheric
photograph was taken at the center of the plot 1.5 m from the soil and analyzed with Gap
Light Analyzer software (Steindl and Troger 1995). These four local variables were
summarized in a vegetation complexity index applying a Principal Component Analysis
(PCA). The first component of the PCA explained 55.5% of the variation in local
variables and was therefore used as a proxy for vegetation complexity. The first
component was positively related to number of understory plants and number of trees,
and mean DBH per tree negatively related to canopy openness.
Finally, we also estimated the (5) number of fruits available for frugivorous birds,
using five plots (25 x 4 m) located near mist nests, totaling a sample area of 0.05 ha per
site. Fruit abundance was estimated from April to September 2017 and October 2017 to
April 2018 in plants between 0.5 and 7 m high, where all ripe fruits of a branch were
counted with the aid of binoculars 8x42. The number of fruits per individual was obtained
by multiplying the total number of fruits of the focal branch by the number of fruit
branches per plant (Blake et al. 1990; Blendinger et al. 2016). We also collected
reproductive plants to posterior identification in the Comissão Executiva do Plano de
Lavoura Cacaueira - CEPLAC, with the help of botany experts.
2.5. Bird and seed survey
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Bird communities were sampled in two field campaigns using mist nests: from
April to September 2017 and October 2017 to April 2018. The license for bird capture
was granted by Ministério do Meio Ambiente (MMA); Instituto Brasileiro do Meio
Ambiente e dos Recursos Naturais Renováveis (IBAMA); and Sistema de Autorização e
Informação em Biodiversidade (SISBIO); license number 53792-2. In each forest site we
used 10 mist nets (12 m long, 2.5 m high and 31 mm mesh) to capture birds during three
consecutive days per campaign. The mist nets were opened from 07:00 to 17:00 and
reviewed every 30 minutes to minimize bird capture stress. Therefore, we used a 60-hour
sampling effort per forest site a total of 12,000 hours/mist nest. We avoided sampling on
rainy and windy days as such conditions can reduce bird activity and therefore influence
catch rates. Each captured bird was temporarily marked on one of the right-wing primary
feathers with non-toxic material to avoid recounting the same individual during the
sampling period. We also identified all captured bird according to the scientific
nomenclature of the South American Classification Committee (Remsen et al. 2014).
To collect the food stomach content of the birds, we performed oral administration
of emetic tartar (1.5% antimony solution and potassium tartrate), a usual technique used
in ecological studies to induce animal to regurgitate the food (Morrison et al. 1990; Poulin
et al. 1994). We administered the solution by means of a disposable 3 ml needleless
syringe with a dosage of 0.8 ml per 100 g of the bird's corporal mass. After the solution
administration, each bird was placed separately in a cloth bag for 15 minutes to regurgitate
and recover from the process and then released (Johnson et al. 2002, 2014). We did not
re-evaluate recaptured birds during the same sampling period, thus reducing stress
(Lannes et al. 2010). Fecal samples were collected only when birds defecated during the
release of the mist net or inside the cloth bag. Both material (fecal and regurgitated
samples) were stored in ethanol (96%) (Lijtmaer et al. 2011) and analyzed in the
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laboratory using a stereoscopic magnifying glass. We identified fruits and seeds at the
lowest possible taxonomic level, comparing the samples with the seed bank of the
Applied Ecology Laboratory from the Universidade Estadual de Santa Cruz. We also used
the literature for the identification of plants, fruits, and seeds (Cestari and Pizo 2013).
Only birds with fruits or seeds in their food content samples were considered in further
analysis.
2.5. Data analysis
For each forest site, we calculated frugivorous bird β-diversity using the
abundance of individuals per species on each site. To calculate the β-diversity of plants
per site, the seed abundance was weighted by the total bird abundance present in each site
in order to reduce the influence of bird richness. Finally, we built a bird-plant interaction
matrix based on the bird food content samples. The interaction frequency for each pair of
interacting species was the number of individuals per bird species that interacted with
each morphospecies of seed. Then, we built bipartite quantitative bird-plant networks and
quantify the β-diversity of interactions. Therefore, we estimated β-diversity of bird
species (βbirds), plant species (βplants) and interactions (βinteractions), separately for all 9 forest
sites located in each region.
First, we calculated the β-diversity of bird and plant with the framework proposed
by Baselga, (2017) in the betapart package using the value of overall dissimilarity,
measured as multiple-site dissimilarity from Bray-Curtis index (Baselga 2017). β-
diversity values range from 0 to 1, indicating the degree of dissimilarity between two
communities, i.e., ‘0’ means total similarity and ‘1’ maximum dissimilarity. Then, we
calculated the βinteractions following the method proposed by Poisot et al. (2012) in the
betalink package. We used the bipartite package (Dormann et al. 2008) to estimate the
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beta partitioning with the Bray-Curtis (for more details see ‘bipartite’ package available
in R). The βinteractions, that range from 0 to 1, were calculated including interactions
between species that are exclusive to one site or another (Carstensen et al. 2014).
We used Mantel tests to assess whether the matrices of the β-diversity of birds,
plants and interactions were correlated with geographic distances among sites. Similarly,
we used matrices showing the differences in landscape structure (i.e. forest and pasture
cover, total core area, edge density and cohesion) and local characteristics (i.e. number of
understory plants, number of trees, mean DBH per tree, canopy openness, fruit number,
and vegetation complexity) to evaluate possible differences β-diversity of birds, plants
and interactions among sites. Also, βinteractions was correlated with bird, plant, and total
richness, whereas βbirds and βplants was correlated with plant and bird richness, respectively.
All figures and statistical analyses were performed using the R version 3.5.3 software (R
Development Core Team, 2019).
3. RESULTS
A total of 476 individuals and 58 bird species were captured at 18 forest sites.
However, we obtained fruit and seed samples from 176 individuals, which together
representing 14 families and 27 bird species. The number of bird species per site ranged
from 1 to 8 (3.78 ± 2.07; mean ± SD), and plant species per site ranged from 1 to 18 (6.56
± 5.07). In total, 30.574 seeds/fruits were recorded in the food contents of birds and were
classified into 56 morphospecies. We were able to identify 10 morphospecies at species
level and another 13 into genus level. Miconia hypoleuca was the only plant species found
in food samples in all forest sites, being therefore considered as an important fruiting
species for birds. We recorded a total number of 256 interactions (mean = 14.22 per site
± SD = 13.50), with larger networks observed in HFC region (Appendix S1; Fig S1). We
recorded a total of 21 bird species in the HFC region, while in LFC region only 12 bird
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species were recorded, with only 6 species being shared between both regions. Regarding
plant species, a total of 51 seed morphospecies were recorded in the HFC region
compared to 17 morphospecies recorded in the LFC region. We detected in the HFC
region a βbirds (0.57 ± 0.24) significantly (t = - 2.63, df = 145.2, p-value > 0.009) smaller
than in the LFC region (0.69 ± 0.34). We also observed differences in βplants (t = -3.08, df
= 160, p-value = 0.002) between forest sites located in HFC (0.57 ± 0.30) and LFC (0.72
± 0.31) region. We did not observed differences (t = -0.91, df = 160, p-value = 0.362) in
βinteractions between regions (HFC = 0.82 ± 0.31; LFC = 0.86 ± 0.32).
PREDICTORS OF β-DIVERSITY
βplants and βinteractions were not related to the geographical distance between forest
locations (Table 1). However, an increase in the geographical distance between forest
sites in the HFC region increased βbirds (r = 0.546, p-value = 0.02). In HFC region, our
results also highlighted that forest sites immersed in landscapes with different amount of
pasture cover (r = 0.235, p-value = 0.050) and with a different amount of fruits (r = 0.388,
p-value = 0.047) showed a higher βbirds, while in the LFC region, an increase of cohesion
index between forest sites led to a higher βbirds (r = 0.399, p-value = 0.052). In contrast,
environmental predictors did not affect the βplants in both regions (Table 1). Finally, we
observed that the βinteractions between birds and plants in LFC region are positively related
to increasing cohesion between forest sites (r = 0.393, p-value = 0.014) and between forest
sites with greater differences in number of trees (r = 0.313, p-value = 0.033).
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Table 1. Results of Mantel’s test shown the correlation coefficient (r), and significance values (p-value) among β-diversity of
bird, plant and interactions associated with site location (geographical distance among sampled sites), landscape variables
(forest cover, pasture cover, total core area, edge density and cohesion), local variables (number of understory plants, number
of trees, DBH, canopy openness, fruit number, and vegetation complexity) and bird, plant and total richness in the 18 landscapes
in southern Bahia, Brazil. Significant values highlighted in bold.
Region* Δ Variables βbirds βplants βinteractions
r p-value r p-value r p-value
HFC Site location 0.546 0.002 0.011 0.466 0.179 0.180
HFC Forest cover -0.058 0.609 -0.170 0.865 -0.277 0.974
HFC Pasture cover 0.235 0.050 -0.014 0.471 -0.074 0.621
HFC Total core area -0.027 0.500 -0.048 0.555 -0.185 0.882
HFC Edge density 0.000 0.471 0.206 0.160 -0.039 0.543
HFC Cohesion -0.052 0.545 -0.238 0.806 -0.271 0.924
HFC Vegetation Complexity 0.130 0.286 0.249 0.224 -0.014 0.503
HFC Fruit number 0.388 0.047 - - 0.352 0.066
HFC Number of trees 0.108 0.292 0.481 0.081 -0.115 0.600
HFC Number of understory plants -0.301 0.879 -0.257 0.864 -0.235 0.858
HFC DBH 0.016 0.428 0.319 0.205 -0.227 0.857
HFC Canopy openness -0.129 0.671 0.205 0.903 -0.103 0.664
HFC Bird richness - - 0.152 0.186 0.204 0.112
HFC Plant richness 0.033 0.390 - - 0.143 0.194
HFC Total richness - - - - 0.170 0.162
LFC Site location 0.037 0.395 -0.131 0.745 0.007 0.475
LFC Forest cover 0.020 0.367 -0.041 0.558 0.318 0.065
LFC Pasture cover 0.086 0.308 0.041 0.405 -0.011 0.509
LFC Total core area -0.066 0.593 0.034 0.362 0.287 0.074
LFC Edge density 0.090 0.283 0.207 0.160 0.208 0.109
LFC Cohesion 0.399 0.052 -0.186 0.808 0.393 0.014
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LFC Vegetation Complexity -0.036 0.501 0.807 0.271 0.168 0.183
LFC Fruit number 0.163 0.180 - - 0.238 0.098
LFC Number of trees 0.137 0.198 -0.012 0.524 0.313 0.033
LFC Number of understory plants -0.095 0.648 0.165 0.185 -0.046 0.578
LFC DBH -0.130 0.764 -0.081 0.651 -0.031 0.539
LFC Canopy openness 0.069 0.349 0.084 0.347 0.084 0.330
LFC Bird richness - - -0.187 0.765 -0.042 0.575
LFC Plant richness 0.184 0.263 - - -0.069 0.637
LFC Total richness - - - - 0.079 0.340
* HFC: high forest cover region; LFC: low forest cover region
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4. DISCUSSION
Our findings highlighted that β-diversity of understory birds is associated with
environmental filters that limited their dispersal movements of birds between forest
patches (Veech and Crist 2007; Morante-Filho et al. 2016). We observed that the βbirds
and βplants differ between regions, with the LFC region showing greater β-diversity for
both groups. Our results showed that in LFC region are capable of maintaining high β-
diversity of birds, plants, and interactions.
Regarding plant community, despite the difference in diversity between the HFC
and LFC regions, none of the environmental predictors on the local or landscape scale
affected βplants. This result indicates that other characteristics of the landscape may be
more important for assembling plant community. Plants are more dependent on local
physical conditions within forest patches, such as temperature, humidity, soil pH,
sunlight, water availability, among other factors that can influence recruitment and plant
survival rates(Kessler et al. 2009; Sabatini et al. 2014; Pinto-Ledezma et al. 2018). In
addition, the divergence in plants communities tend to occur divergence continued over
the course of decades (Collins et al. 2017).
Beta diversity of frugivorous bird assemblage showed contrasting results between
regions. We observed that in the HFC region, the differences between patch isolation,
pasture cover, and number of fruits lead to more dissimilar bird communities. It is known
that birds show different responses to environmental disturbances, understory birds have
limitations on their dispersion capacity, showed higher specialization in habitat use, and
consequently their populations tend to decline in anthropogenic habitats (Pardini et al.
2009; Morante-Filho et al. 2015). Therefore, understory birds shown low mobility and
are unable to move long distances through the matrix and migrate to other locations in
136
the forest (Carrara et al. 2015; Carlo and Morales 2016). Therefore, the distance between
the forest sites may favor an increase in the dissimilarity of the understory bird
communities (Martensen et al. 2012). In addition, different amounts of pasture cover can
be attract different generalist bird species who are able to explore the edges forests and
more open habitats (Cerezo et al. 2011). Studies have reported that bird communities that
inhabit landscapes under strong anthropic pressure exhibit lower richness and abundance
(Anjos 2006; Lees and Peres 2006; Pizo and Tonetti 2020). For instance, in cattle
pastures, it is practically impossible for forest birds to inhabit or risk crossing this type of
matrix (Ibarra-Macias et al. 2011; Barros et al. 2019a), like pastures exhibit extreme
conditions for more sensitive birds, such as high temperatures, lack of hiding places,
scarcity of food and sexual partners (Ibarra-Macias et al. 2011). Therefore, the most
sensitive birds can end up confined in forest areas, forming several subsets of species that
inhabit different forest areas. In this way, βbirds can be larger in forest locations more
distant from each other. In the LFC region, we observed that greater differences in the
distances between forest patches positively influences βbirds. Thus, bird communities who
live more isolated in this region are more dissimilar in your composition.
Interestingly, although the understory bird and plant communities show greater
dissimilarity in forest patches immersed in landscapes in the LFC region, βinteractions did
not differ between HFC and LFC. As it is known, the plant community can shape the
frugivorous community (bottom-up control; Muñoz et al. 2017). Therefore, the forest
patches closest to each other in landscapes in the LFC region that exhibited higher values
of βbirds also exhibited greater βinteractions. This result is related to subsets of birds in the
understory that establish local interactions with plants and feed on their fruits (Restrepo
et al. 1999; Neuschulz et al. 2011). Consequently, both birds and plants can be harmed if
one of the interaction partners is extinguished locally (Emer et al. 2019a). Forest sites
137
immersed in more forested landscapes tend to show a higher biomass and nutritional
resources, such as lipids and proteins, which are important for different bird species
(Cramer et al. 2007; Pessoa et al. 2017; Walter et al. 2017). Thus, we suggest that
differences in the number of trees between forest patches can influence βinteractions, that is,
forest sites with more trees have more distinct interactions between birds and plants than
forest sites with fewer trees. A recent study, conducted in the same region, reported that
forest patches in more deforested landscapes such as the LFC region maintain initial
succession attributes, with less dense tree clusters (Rocha-Santos et al. 2016). Although
we did not find a relationship between βbirds, βplants and βinteractions with the vegetation
complexity, usually habitats that exhibit greater structural complexity allow for the
existence of a greater number of niche overlays (Kikkawa 1982; Pellissier et al. 2018).
This greater variety of habitats provided by the structural complexity of the habitat enable
greater diversification in the use and exploitation of available resources (Pellissier et al.
2018). In this way, continuous forests and larger forest patches are capable of harboring
a greater diversity of species regarding small forests with low structural complexity
(García 2016).
Conclusions
Our results highlight that in HFC region, the βbirds in the understory can be
positively influenced by the availability of fruits within the forest sites and also by pasture
cover that small amounts can increases landscape heterogeneity for bird communities.
We also observed that the connectivity between forest patches (i.e. higher cohesion index)
positively influences the βbirds in LFC region. Regarding the plant communities, none of
our measured landscape or local predictors affected βplants, although the beta diversity of
plants is greater in LFC. This result can be related the birds, because the βplants was
138
estimated by their food content samples. Although our results reveal that the forest
patches in the LFC region are still capable of maintaining a high βbirds and βplants, the
βinteractions is similar between HFC and LFC. This result demonstrates in part that there is
a high functional redundancy, although the number of interactions is lower in LFC.
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Supporting information
Environmental predictors of beta diversity of bird-plant networks inthe

threatened Brazilian Atlantic forest
Carlos Morante-Filho1
1
2
147
Appendix S1. Differences between local and landscape characteristics.
We described the structure of local vegetation based on four variables commonly

used in ecological studies: (1) plant density in the understory (50-200 cm in height), (2)
density of trees above the understory with diameter at breast height (DBH) ≥ 5 cm, mean
DBH per tree and canopy openness (%). The average plant density in the HFC region was
237.22 ± 33.75 and in LFC region was 190.56 ± 54.91, showing significant differences (t
= 2.17, df = 13.29, p-value = 0.049) between regions. The average tree density in the HFC
region 92.22 ± 44.28 did not differ from the LFC region 67.33 ± 16.96 (t = 1.56, df =
10.25, p-value = 0.149). Nevertheless, the mean DBH between HFC 12.79 ± 2.50 and
LFC 10.70 ± 0.78 differed significantly (t = 2.40, df = 9.54, p-value = 0.039). The canopy
openness in HFC region 8.56 ± 1.46 did not differ from the LFC region 10.42 ± 2.35 (t =
-2.03, df = 13.39, p-value = 0.063). In addition, we used a Principal Component Analysis
to describe the local vegetation structure. The first two axes explained 83.8% of the total
variance in vegetation structure. As the largest variance (55.5%) was explained by PCA
1, we used this axis as a proxy for vegetation structure complexity, which was positively
related to the density of trees, mean DBH and plant density in the understory and
negatively related to canopy openness. The fruit number in the HFC region was 387.33 ±
395.88 and LFC 395 ± 310.86 did not significant differences (t = -0.05, df = 15.15, p-
value = 0.964) between regions. Finally, the vegetation structure complexity (PCA 1) in
the HFC region was 0.65 ± 0.11 and LFC 0.42 ± 0.21 showing significant differences (t
= 2.94, df = 12.39, p-value = 0.012) between regions.
148
Fig S1. Differences among landscape characteristics of each site between the HFC and
LFC regions of the study. The median (solid line), the 25th and 75th percentiles
(boundaries of box), interquartile range (whiskers above and below box plots), outlier
points (value that lies more than one and a half times the length of the box from either
end of the box), and individual data points are indicated for all 18 landscapes located in
Atlantic forest in southern of Bahia State, Brazil. P-values are shown only for significant
differences.
149
Fig S2. Differences in local characteristics and vegetation complexity (PCA 1) of each
landscape between the HFC and LFC regions of the study. The median (solid line), the
25th and 75th percentiles (boundaries of box), interquartile range (whiskers above and
below box plots), and individual data points are indicated for all 18 forest sites located in
Atlantic forest in southern of Bahia State, Brazil. P-values are shown only for significant
differences.
150
HFC
LFC
Fig S3. Land-cover classes of sampled sites in the HFC and LFC region. Figures represent
the percentage of native forest cover calculated within 800-m radius (201 ha) from the
center of each forest site.
151
Appendix S2. Scale of landscape effects on birds, plants, and interactions richness.
Because the effect of forest loss on biodiversity is known to depend on the spatial
scale at which predictors is measured (i.e. the so-called “scale of landscape effects”; sensu
Jackson and Fahrig 2012; Fahrig 2013), we measured forest and pasture cover, total area
core, edge density, and cohesion index within ten different-sized buffers (i.e. landscapes),
ranging from 100 to 1000-m radius. Thus, we obtained landscapes of 100 m (3.1 ha), 200
m (12.6 ha), 300 m (28.3 ha), 400 m (50.2 ha), 500 m (78.5 ha), 600 m (113 ha), 700 m
(153.9 ha), 800 m (201 ha), 900 m (254.3 ha) and 1,000 m radius (314 ha). We tested the
effect of the landscape metrics scale on the response variables using the multifit function
proposed by Huais (2018) for multi-scale analyzes. Therefore, the scale of the effect of
each landscape predictor was defined as the landscape size within which the landscape-
response relationship is strongest (i.e. with highest R² and lowest p valor, see Fahrig 2013,
Jackson and Fahrig 2015). The strength of the relation between the response variables
and the predictor variables differed between the scales. Bird richness had a stronger
relation on the 800-meter scale for forest and pasture cover. The bird richness presented
a higher relation strength on the 900 and 1000-meter scale for the total core area and edge
density in each landscape, respectively. Already the cohesion showed a stronger effect on
bird richness on the 900-meter scale. In relation to plant richness, the forest cover
presented a stronger relationship in the 800-meter scale and for pasture cover at 800-
meter. In addition, the scale of the total core area effect, edge density, and cohesion index
on plant richness was 800 m, 400 m, and 900 m, respectively. The number of interactions
showed a stronger relationship on the 800-meter scale for forest cover, pasture cover and
cohesion index. The strong effect for total core area in 700 m. Finally, the scale of effect
to the edge density on the number of interactions was 400 m.
152
Fig. S4. Association between landscape size (x-axis) and the strength of the relationship (R², y-axis) between forest and pasture cover, total core
area, edge density and cohesion surrounding each site and the species richness of birds in the Brazilian Atlantic forest. The landscape size used in
this study is indicated with a dashed line.
area, edge density and cohesion surrounding each site and the species richness of plants in the Brazilian Atlantic forest. The landscape size used in
this study is indicated with a dashed line.
153
area, edge density and cohesion surrounding each site and the interactions richness of birds and plants in the Brazilian Atlantic forest. The landscape
size used in this study is indicated with a dashed line.
154
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CONSIDERAÇÕES FINAIS
A perda de biodiversidade global é particularmente preocupante, principalmente

nas florestas tropicais que apresentam elevado nível de endemismo. A expansão de áreas
urbanas, agrícolas e pastagens acabam reduzindo e fragmentando florestas que outrora
eram contínuas. Essas paisagens antropizadas apresentam diferentes características de
composição (ex. tipos de uso do solo, matrizes) e configuração (ex. tamanho, formas ou
isolamento). Consequentemente, essas alterações acarretam mudanças na estrutura das
comunidades da flora e da fauna em diferentes escalas (local ou paisagística). Nossos
resultados ampliam o conhecimento sobre os efeitos da perda e fragmentação do habitat
em duas regiões com diferentes tipos de uso do solo.
Utilizando os resultados do primeiro capítulo, podemos afirmar que as
assembleias de aves do sub-bosque da floresta e seus subgrupos como aves dependentes
de floresta aumentam em riqueza e abundância conforme há uma maior quantidade de
habitat, quantidade de interior de floresta e fragmentos florestais menos isolados na
paisagem. É importante destacar que do total (n = 59) das espécies registradas em nossa
área de estudo, 39 são espécies dependentes de floresta. Assim, nossas predições se
limitam a esse grupo específico do sub-bosque florestal que representam 66% das
espécies capturadas. Em relação as guildas tróficas, frugívoros florestais não foram
afetados pelo número de frutos disponível na paisagem. Entretanto, aves insetívoras
foram mais abundantes em florestas com uma maior complexidade estrutural da
vegetação.
Neste cenário de perda e fragmentação do habitat, a porção mais ao sul da nossa
área de estudo apresentou menor riqueza e abundância de aves. As aves são sensíveis a
mudanças no habitat e tendem a responder negativamente a distúrbios antrópicos.
Consequentemente, observamos que as interações entre aves e plantas são afetadas pela
redução da cobertura florestal na região mais desmatada, apresentando um número
extremamente reduzido de interações. Apesar de observamos uma alta diversidade beta
(β) de aves, plantas e interações em ambas regiões devido a persistência de subconjuntos
de espécies que ainda são capazes de sobreviver em habitats altamente perturbados. Uma
alta diversidade beta (β) de interações pode indicar que tais interações podem ocorrer
apenas localmente e que essas espécies de aves não conseguem dispersar frutos ou
sementes a longas distâncias em uma região com menor quantidade de floresta disponível.
156
A redução do número de interações mutualísticas entre aves e plantas em florestas
antropizadas também pode ser um fator crítico para as populações de plantas que são
dispersas por aves, podendo afetar o recrutamento de plântulas e sua demografia.
Por fim, destacamos a importância de paisagens florestais com interiores
preservados e fragmentos remanescentes menos isolados na manutenção das assembleias
de aves do sub-bosque florestal. Apesar, das aves do sub-bosque conseguirem persistir
por explorar uma gama de recursos, especificamente os frugívoros florestais que
consomem frutos e sementes, essas aves são altamente afetadas em paisagens menos
florestadas, apresentando menor riqueza, abundância e interações com plantas. A
complexidade estrutural da vegetação também é um fator importante para as aves,
especificamente os insetívoros do sub-bosque que forrageam na vegetação mais baixa
próxima ao solo. Consequentemente, paisagens com menor quantidade de habitat
disponível, fragmentos florestais mais isolados e menos complexos estruturalmente,
apresentam menor riqueza de plantas, consequentemente limitando a ocorrência de
potenciais agentes dispersores de sementes e controladores de populações de artrópodes
como as aves.
157

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UNIVERSIDADE ESTADUAL DE SANTA CRUZ

PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA E CONSERVAÇÃO DA

ÍCARO MENEZES PINTO

Influência de mudanças ambientais sobre as comunidades de aves e suas

Influência de mudanças ambientais sobre as comunidades de aves e suas

Tese apresentada à Universidade Estadual de Santa Cruz,

Área de concentração: Ecologia e Conservação de

Orientador: Prof. Dr. José Carlos Morante-Filho

Influência de mudanças ambientais sobre as comunidades de aves e suas

Prof. Dr. Erich Arnold Fischer

Agradeço à Universidade Estadual de Santa Cruz (UESC), na qual me graduei bacharel em

Palavras-chave: Avifauna, fragmentação, florestas tropicais, interações ecológicas, perda de

Keywords: Avifauna, biodiversity, ecological interactions, habitat fragmentation, habitat loss,

A importância das aves para a funcionalidade dos ecossistemas .................................................... 6

Perda e fragmentação do habitat: ameaças à Mata Atlântica .......................................................... 8

Ameaças a biodiversidade em paisagens modificadas pelo homem

A biodiversidade global refere-se à variedade de vida e seus níveis de organização

no planeta Terra. Inclui, além de espécies, a variabilidade genética intra e inter-específica,

a diversidade de comunidades biológicas, habitats e ecossistemas formados pelos

organismos (CARDINALE et al., 2012). Igualmente, as interações ecológicas realizadas

pelos organismos nos ecossistemas e funções decorrentes dessas interações, como

dispersão de sementes, polinização e predação, também fazem parte da biodiversidade

(COSTANZA et al., 1997; KREMEN, 2005). Portanto, a biodiversidade engloba em sua

ecossistemas e em maior escala, a biosfera (MACE et al., 2012).

Atualmente, grande parte dessa biodiversidade é ameaçada pelas atividades

humanas que alteram as condições físicas dos ecossistemas naturais e consequentemente

ocasionam declínios na riqueza e abundância das espécies, podendo levá-las à extinção

(KUEFFER & KAISER-BUNBURY, 2014; MCGILL et al., 2015). A extinção de

estão extintas (MILLENNIUM ECOSYSTEM ASSESSMENT, 2005; JOHNSON et al.,

2017). Entretanto, as atuais taxas de extinções de espécies encontram-se muito acima do

esperado, ocorrendo em um período extremamente curto, em níveis de 100 a 1000 vezes

agem em sinergia com outros fatores, como sobre-exploração de recursos naturais,

poluição, caça predatória, invasões biológicas e mudanças climáticas, reduzindo a

BUTCHART et al., 2010).

A interferência humana nos ecossistemas naturais tem sido historicamente

importante, moldando os padrões atuais de biodiversidade global (BENDER et al., 1998;

redução da biodiversidade, especialmente em locais muito diversos é particularmente

preocupante (LAURANCE et al., 2012; PÜTTKER et al., 2020). Existe um consenso de

que a biodiversidade está diretamente relacionada às funções do ecossistema, sendo que

estas são distribuídas no espaço e tempo e determinam o quão um ecossistema é estável

a redução na riqueza de espécies, quanto alterações em suas abundâncias como

consequência direta e indireta de fatores antropogênicos, podem ser fortes ameaças ao

funcionamento do ecossistema e ao bem-estar humano (PEREIRA et al., 2010, HAGEN

O papel da diversidade de espécies e de seus traços funcionais dentro

Recentemente, diversos estudos se empenharam em avaliar como a perda e

fragmentação florestal influenciam na composição local de espécies e nas funções

avaliaram como a diversidade de espécies e de suas características fenotípicas (traços

funcionais) diretamente associadas a processos ecológicos desempenhados por elas na

comunidade, influenciam no “funcionamento das comunidades” (TILMAN 2001;

redundantes funcionalmente, isto é, desempenham papéis semelhantes dentro de um

flores) realizam a polinização das flores ao explorar um recurso alimentar, o néctar. Da

mesma maneira, abelhas ao coletarem o pólen das flores acabam às fecundando,

auxiliando no fluxo gênico e reprodução de inúmeras angiospermas (BLÜTHGEN &

KLEIN 2011). Espécies redundantes funcionalmente podem garantir a manutenção de

et al. 2016; KAISER-BUNBURY et al. 2017).

Entender como as comunidades biológicas se estruturam frente às mudanças

2011). Em 1975, Diamond propôs a existência de “regras de montagem” que atuam na

organização das comunidades. Assim, ele se propôs compreender como comunidades

distintas são formadas a partir de um mesmo pool de espécies, ou seja, um mesmo

conjunto de espécies. Em 1967, MacArthur e Levins proporam que a organização das

comunidades biológicas se daria pela limitação da similaridade entre espécies dentro da

comunidade. Nessa proposição, as espécies ocupariam nichos diferentes em um

ecossistema como uma forma de evitar competição por recursos (exclusão-competitiva)