TITULO - Inpa · 2017-04-18 · Simonetti 2001) reduzindo assim a diversidade nas florestas...
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INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA ALUNO: Alexander Roldán Arévalo Sandi TITULO: MAMÍFEROS DE MÉDIO E GRANDE PORTE DISPERSORES DE SEMENTES EM FLORESTAS DE TERRA FIRME AO LONGO DE UM GRADIENTE DE DEGRADAÇÃO NA AMAZÔNIA ORIENTAL MANAUS, AM 2017
Transcript of TITULO - Inpa · 2017-04-18 · Simonetti 2001) reduzindo assim a diversidade nas florestas...
INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA
PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA
ALUNO:
Alexander Roldán Arévalo Sandi
TITULO:
MAMÍFEROS DE MÉDIO E GRANDE PORTE DISPERSORES DE SEMENTES EM FLORESTAS
DE TERRA FIRME AO LONGO DE UM GRADIENTE DE DEGRADAÇÃO NA AMAZÔNIA
ORIENTAL
MANAUS, AM
2017
ALUNO:
Alexander Roldán Arévalo Sandi
TITULO:
MAMÍFEROS DE MÉDIO E GRANDE PORTE DISPERSORES DE SEMENTES EM FLORESTAS
DE TERRA FIRME AO LONGO DE UM GRADIENTE DE DEGRADAÇÃO NA AMAZÔNIA
ORIENTAL
Dissertação apresentada à
Coordenação do Programa de Pós-
Graduação em Ecologia, como
parte dos requisitos para
obtenção do título de Mestre em
Biologia com ênfase em Ecologia.
Orientador:
Darren Norris
Co-Orientador:
Paulo Estefano D. Bobrowiec
MANAUS, AM
2017
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BANCA EXAMINADORA DA DEFESA ORAL PÚBLICA
Prof. Dr. Wilson Roberto Spironello (INPA):
APROVADO
André Pinassi Antunes (Wildlife Conservation Society):
APROVADO
Sérgio Henrique Borges (Universidade Federal do Amazonas):
APROVADO
2
FICHA CATALOGRÁFICA
S213 Sandi, Alexander Roldán Arévalo
Mamíferos de médio e grande porte dispersores de sementes em florestas de
Terra firme ao longo de um gradiente de degradação na Amazônia oriental
/Alexander Roldán Arévalo Sandi . --- Manaus: [s.n.], 2017.
41 f.: il.
Dissertação (Mestrado) --- INPA, Manaus, 2017.
Orientador: Darren Norris
Coorientador: Paulo Bobrowiec
Área de concentração: Ecologia
1. Mamíferos . 2.Ecologia de comunidades . 3. Florestas de Terra firme . I. Título.
CDD 599
Sinopse
Estudou-se a perda da diversidade taxonômica e funcional dos mamíferos terrestres de
meio e grande porte importantes para a regeneração natural ao longo de um gradiente de
degradação em uma floresta de Terra firme, no entorno do Parque Nacional do Amapá,
AP, Amazônia oriental.
Palavras-chave: Floresta amazônica, armadilhagem-fotográfica, floresta intacta, floresta
secundaria, neotropical, perda de espécies.
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AGRADECIMENTOS
Primeiro quero agradecer a minha família pelo apoio e confiança de sempre e por ter
dado as condições de chegar onde estou hoje. Obrigado para meu pai Roldán, minha
mãe Delicia e meus irmãos Marco e Ericka. Obrigado por acreditar nos meus sonhos (e
“locuras”). Amo muito vocês.
Sou extremamente grato ao Fernando Fernandez, professor responsável do Laboratório
de Ecologia e Conservação de Populações da UFRJ, por me abrir as portas no mundo da
pesquisa brasileira e pelos conselhos (orais e escritos) e pelo apoio nos meus primeiros
meses na Terra Brasilis. Também agradeço a todo o pessoal que conheci no LECP e as
grandes lembranças que tenho com eles tanto no laboratório mesmo quanto no campo
da Floresta Nacional da Tijuca no projeto de reintrodução da cutia vermelha. Espero
possam continuar com a refaunação por essas latitudes da Mata Atlântica e preenchendo
as florestas vazias.
Agradeço ao ICMBio por conceder a oportunidade de trabalhar no Parque Nacional do
Amapá, especialmente ao Érico Emed Kauano e Sueli Gomes Pontes dos Santos que
forneceram todo o apoio logístico possível.
Sou especialmente grato a todos assistentes de campo que trabalharam comigo, em
especial ao Cremilson Alves Marques e família. Obrigado por todo o empenho em
conduzir o trabalho de campo junto comigo e pelas longas conversas mesmo até nos
momentos mais difíceis. Também fico muito grato com todas as famílias do rio Falsino
e Araguari que me permitiram trabalhar nas propriedades deles e me receberam e
ajudaram no que era possível.
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Agradeço também aos membros do Laboratório de Ecologia e Conservação de
Vertebrados da UNIFAP pelo tempo que a gente compartilhou juntos assim como nas
nossas saídas de campo que desde já são inesquecíveis.
Agradeço ao PPG-Ecologia do INPA pela oportunidade que me foi dada. Aprendi muito
nesses dois anos e que aumentaram ainda mais meu fascínio pela pesquisa. Agradeço
sinceramente a todos os professores pelos ensinamentos assim como aos funcionários e
especialmente a minha turma de mestrado em Ecologia de 2015.
Fico muito grato com o meu orientador e co-orientador. Ao Darren Norris, pelo aceite
em me orientar e pela disposição e por me instigar a pensar mais no estudo, desde a
construção do projeto até a conclusão da dissertação. Ao Paulo Bobrowiec muito
obrigado pela disponibilidade, disposição e contribuição nesse estudo.
Também agradeço a todas as amizades que fui conhecendo durante a minha vida de
mestrando, tanto em Manaus quanto em Macapá, assim como aos velhos amigos do Rio
de Janeiro. Obrigado por todo. A minha vida ficou muito mais divertida com a
companhia e as amizades de vocês.
Por fim agradeço a CAPES pela bolsa concedida durante os dois anos de curso de
mestrado e ao CNPq (projeto #446926/2014-0) pelo auxílio financeiro que permitiu o
desenvolvimento do projeto.
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RESUMO
Há um interesse crescente na restauração/regeneração de hábitats neotropicais
degradados, mas o papel potencial dos regeneradores naturais permanece incerto. As
respostas de mamíferos terrestres à fragmentação e perda de hábitat já são conhecidas,
mas ainda não se sabe como este grupo responde aos efeitos da degradação florestal.
Nesse estudo testamos a hipótese que áreas que sofreram degradação nos anos mais
recentes apresentam maior perda da diversidade comparadas com as áreas de
degradação mais antiga. Quantificamos a diversidade funcional e taxonômica de oito
espécies de mamíferos terrestres dispersores de sementes ao longo de um gradiente de
degradação na Amazônia brasileira oriental. Instalamos armadilhas-fotográficas em 15
áreas com diferentes graus de degradação (cinco áreas cada de floresta secundária velha,
floresta secundária nova e pasto abandonado) e comparamos com as suas áreas
pareadas-controle (floresta intacta sem registro de extração mecanizada de madeira).
Encontramos uma redução significativa na diversidade funcional e taxonômica em áreas
degradadas. Nossos resultados sugerem que quando rodeados por grandes áreas
florestais contínuas, a diversidade taxonômica e funcional pode retornar a valores de
pré-degradação.
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ABSTRACT
There is increasing interest in the restoration/regeneration of degraded neotropical
habitats yet the potential role of natural regenerators remains unclear. The response of
terrestrial mammals to habitat loss and fragmentation are well documented, but little is
known regarding how they respond to forest degradation. We test the hypothesis that
the assemblage of terrestrial mammals in sites with more intense degradation show
greater loss of taxonomic and functional diversity. We quantified the taxonomic and
functional diversity of eight terrestrial mammal seed-disperser species across a
degradation gradient in the eastern Brazilian Amazon. We installed camera-traps in 15
lowland sites within small-holder properties with different degrees of degradation (five
sites each of late second-regrowth forest, early second-regrowth forest and abandoned
pasture). Species richness and functional dispersion were compared with 15 paired
forest control sites. We found a significant reduction in taxonomic and functional
diversity in degraded areas. Yet, we also found that diversity in degraded sites could be
similar to control sites even in some early-second regrowth areas. Our findings suggest
that when surrounded by large intact forest areas the taxonomic and functional diversity
close to human small-holdings can return to pre-degradation values.
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RESUMEN
Hay un interés creciente en la restauración/regeneración de hábitats neotropicales
degradados, pero el papel potencial de los regeneradores naturales permanece incierto.
Las respuestas de mamíferos terrestres a la fragmentación y perdida de hábitat ya son
conocidas, pero aún no se sabe cómo este grupo responde a los efectos de la
degradación forestal. En este estudio cuantificamos la diversidad funcional e
taxonómica de ocho especies de mamíferos terrestres dispersores de semillas a lo largo
de un gradiente de degradación en la Amazonia brasileira oriental. Testamos la hipótesis
que áreas que sufrieron degradación en los años más recientes presentan mayor pérdida
de diversidad comparadas con las áreas de degradación más antigua. Instalamos
cámaras-trampa en 15 áreas con diferentes grados de degradación (cinco áreas cada de
floresta secundaria tardía, floresta secundaria temprana y pasto abandonado) y
comparamos con sus áreas pareadas-controle (floresta intacta sin registro de extracción
mecanizada de madera). Encontramos una reducción significativa en el número y
diversidad de especies en áreas degradadas. Nuestros resultados sugieren que cuando
rodeados por grandes áreas forestales continuas, la diversidad taxonómica e funcional
pode retornar a valores de pre-degradación.
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INDICE GERAL
AGRADECIMENTOS.................................................................................................................. 3
RESUMO ...................................................................................................................................... 5
ABSTRACT .................................................................................................................................. 6
RESUMEN ................................................................................................................................... 7
INTRODUÇÃO GERAL .............................................................................................................. 9
OBJETIVO GERAL ................................................................................................................... 13
OBJETIVOS ESPECÍFICOS ...................................................................................................... 13
Capítulo I. ................................................................................................................................... 14
ABSTRACT ................................................................................................................................ 16
PORTUGUESE ABSTRACT ..................................................................................................... 16
INTRODUCTION ...................................................................................................................... 18
METHODS ................................................................................................................................. 20
SAMPLING DESIGN ...................................................................................................................... 21
MAMMAL SURVEY ....................................................................................................................... 22
FUNCTIONAL DIVERSITY ASSESSMENT ........................................................................................ 22
DATA ANALYSIS ......................................................................................................................... 23
RESULTS ................................................................................................................................... 25
SAMPLING EFFORT AND MAMMAL DIVERSITY ........................................................................... 25
TAXONOMIC AND FUNCTIONAL DIVERSITY ................................................................................. 25
DISCUSSION ............................................................................................................................. 27
SAMPLING EFFORT AND MAMMAL COMMUNITY ........................................................................ 28
TAXONOMIC AND FUNCTIONAL DIVERSITY ................................................................................. 29
CONCLUSIONS ......................................................................................................................... 30
ACKNOWLEDGMENTS .......................................................................................................... 30
DATA AVAILABILITY STATEMENT ................................................................................... 31
LITERATURE CITED ............................................................................................................... 32
SUPPLEMENTAL MATERIAL ........................................................................................................ 37
CONCLUSÃO ............................................................................................................................ 41
REFERENCIAS .......................................................................................................................... 42
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INTRODUÇÃO GERAL
Nos anos recentes há um aumento de áreas degradadas nas florestas tropicais
principalmente pelos avances das fronteiras agrícolas e do desmatamento (Benayas et al.
2007, Lewis et al. 2015). As áreas de florestas degradadas são severamente danificadas
pela exploração excessiva de produtos madeireiros e/ou não madeireiros, mal manejo,
incêndios frequentes, sobrepastoreio entre outras atividades antrópicas (Aronson et al.
2011, Kirby et al. 2006, Lees & Peres 2008). Esses fatores danificam o solo e a
biodiversidade ao ponto de inibir ou comprometer severamente o restabelecimento da
floresta depois que cessam os distúrbios (Aronson et al. 2011, Barlow et al. 2016). Em
quase todos os casos de degradação ou fragmentação nas florestas tropicais existe uma
perda da diversidade de espécies e interações bióticas na escala local (Lindenmayer et al.
2002), regional (Sax & Gains 2003) e global (Barnosky et al. 2012).
Uma resposta para equilibrar essa perda da diversidade é a restauração de
florestas e paisagens em grandes escalas especialmente pela regeneração natural
(Chazdon & Uriarte 2016). Atualmente existem grandes áreas que apresentam
regeneração natural nas florestas tropicais da América do Sul (Ramankutty & Foley
1999, Chazdon & Guariguata 2016). Segundo Omeja et al. 2016 para que terras
desmatadas tenham valor de conservação, é necessário compreender capacidade de
regeneração da vegetação, a capacidade com que os animais colonizam e crescem em
áreas de regeneração e a natureza das interações entre plantas e animais. Portanto, é
preciso fornecer resultados de recuperação da fauna nas florestas em regeneração e do
papel central que a fauna desempenha sobre a regeneração vegetal com processos como
a dispersão de sementes que é fundamental para a regeneração natural (Bowen et al.
2007, Bascompte & Jordano 2007).
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Assim, a dispersão de sementes é um dos processos que aceleram plantações de
árvores em áreas degradadas e é fundamental para a restauração da biodiversidade (van
der Pijl 1982). Dentre os agentes dispersores, os vertebrados se destacam por sua
marcada influência na composição florística, estruturais e funcionais das comunidades
vegetais, inclusive em áreas restauradas dispersando sementes a grandes distâncias e em
grande quantidade (Wunderle 1997, Bascompte & Jordano 2007, Wescott et al. 2005).
É estimado que cerca de 75% das árvores nas florestas tropicais possuam frutos
adaptados para atrair vertebrados, sendo estes relevantes para o processo de regeneração
(Howe & Smallwood 1982), especialmente os mamíferos que dispersam grande
quantidade de sementes e a longas distâncias (Fragoso 1997, Wunderle 1997, Stoner et
al. 2007, Matías et al. 2010, Omeja et al. 2016).
Os mamíferos têm um papel importante no funcionamento dos ecossistemas, tais
como dispersão e predação de sementes assim como na distribuição, abundancia e
recrutamento de numerosas espécies de plantas (Fleming & Heithaus 1981, Clark &
Clark 1989, Beck 2006). Os mamíferos herbívoros de médio e grande porte (peso >
1Kg) são seletivos no consumo de sementes e plântulas e a ausência deles pode liberar
algumas plantas da herbivoría com a dominância delas sobre as outras (Roldán &
Simonetti 2001) reduzindo assim a diversidade nas florestas (Terborgh et al. 2008).
Donatti et al. (2009) concluíram que mamíferos pequenos não cumprem adequadamente
o papel ecológico dos mamíferos de médio e grande porte. Portanto, os mamíferos
herbívoros de médio e grande porte representam um componente chave para projetos de
restauração em grande parte da região neotropical (Aide et al. 2000), especialmente na
recuperação de áreas degradadas ou a serem restauradas (Aronson et al. 2011)
As respostas dos mamíferos terrestres de médio e grande porte à perda de hábitat
e fragmentação já são conhecidas para diversidade taxonômica, como número de
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espécie, abundância e composição de espécies (Turner 1996, Michalski & Peres 2007,
Norris et al. 2008), mas ainda não se conhece como a diversidade funcional de
mamíferos de médio e grande porte respondem aos efeitos da degradação florestal e
quais traços funcionais são sensíveis a mudanças da qualidade dos hábitats modificados.
Classicamente, as mudanças da diversidade biológica têm sido avaliadas usando
riqueza de espécies ou índices de diversidade taxonômica (i.e., índices de diversidade de
Simpson e Shannon), mas tais dados provem um panorama incompleto da diversidade
biológica porque esses índices não consideram a variabilidade funcional entre espécies
(Moretti et al. 2009, Villéger et al. 2010). Porém nesses últimos anos tem um
incremento do estudo da diversidade biológica como diversidade funcional que é a
distribuição das espécies e suas abundancias no espaço funcional numa comunidade ou
a diversidade de traços funcionais presentes numa comunidade pesado pelas suas
abundancias (Mouillot, et al. 2013, Petchey & Gaston 2006, Tilman 2001).
Portanto, estudos ecológicos são necessários para informar sobre o manejo e a
recuperação da diversidade nas florestas que foram degradadas. Especificamente,
fornecendo informação sobre a influência dos mamíferos terrestres de médio e grande
porte na regeneração natural que ajudaria a melhorar as atividades de restauração
praticadas atualmente, incluindo redução de custos e aceleração de processos da
restauração ecológica. Assim é interessante manipular os processos naturais já
disponíveis em sistemas de regeneração, ao invés de investir em intervenções artificiais
muito mais trabalhosas e custosas, como coletas de sementes silvestres, cultivo de
plântulas em grandes viveiros de mudas, e plantios de mudas em áreas a serem
recuperadas.
Nesse estudo analisamos as mudanças na diversidade funcional e taxonômica de
mamíferos terrestres de médio e grande porte importantes para a regeneração natural,
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especialmente dispersão de sementes ao longo de um gradiente de degradação (floresta
intacta ou controle, capoeira velha, capoeira nova, pasto abandonado) em uma floresta
de Terra firme na Amazônia oriental brasileira. Nossa hipótese é que áreas que sofreram
degradação nos anos mais recentes (floresta secundária nova) ou com maior intensidade
(pasto abandonado) apresentam maior perda de diversidade taxonômica e diversidade
funcional comparadas com as áreas de vegetação secundária antiga e floresta intacta.
Nós prevemos que a diversidade funcional e taxonômica assim como os traços
funcionais importantes para a dispersão de sementes pelos mamíferos como estrutura
social, tamanho corporal, tamanho de área de vida e guilda trófica serão reduzidos ou
perdidos nas áreas que sofreram degradação nos anos mais recentes ou com maior
intensidade.
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OBJETIVO GERAL
Analisar a diversidade funcional e taxonômica de mamíferos terrestres de médio e
grande porte dispersores de sementes em florestas de Terra firme ao longo de um
gradiente de degradação na Amazônia oriental.
OBJETIVOS ESPECÍFICOS
a) Comparar a mudança da diversidade funcional e taxonômica de mamíferos
terrestres de médio e grande em florestas de Terra firme ao longo de um
gradiente de degradação na Amazônia oriental.
b) Analisar a porcentagem de diferença na diversidade funcional e taxonômica de
mamíferos terrestres de médio e grande em florestas de Terra firme ao longo de
um gradiente de degradação na Amazônia oriental.
14
Capítulo I.
Arévalo-Sandi, A.R.; Bobrowiec, P.E.D. and Norris, D.
Diversity of mammalian seed dispersers along a
degradation gradient in a lowland Amazon rainforest.
Manuscrito submetido ao periódico Biotropica.
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Arévalo-Sandi et al.
Mammal Diversity in Degraded Amazon Forests
Diversity of mammalian seed dispersers along a degradation gradient in a lowland
Amazon rainforest
Alexander Arévalo-Sandi1,2, Paulo Estefano D. Bobrowiec1, Darren Norris1, 2
1Programa de Pós-graduação em Ecologia, Instituto Nacional de Pesquisas da Amazônia
Av. André Araújo 2936, Petrópolis 69067-375 Manaus, AM, Brazil.
2Laboratório de Ecologia e Conservação de Vertebrados / Universidade Federal do
Amapá, Universidade Federal do Amapá (UNIFAP), Rod. Juscelino Kubitscheck, Km
02, 68902-280, Macapá, AP, Brazil.
Received ; revision accepted .
3Corresponding author; e-mail: [email protected]
16
ABSTRACT
There is increasing interest in the restoration/regeneration of degraded neotropical
habitats yet the potential role of natural regenerators remains unclear. The response of
terrestrial mammals to habitat loss and fragmentation are well documented, but little is
known regarding how they respond to forest degradation. We test the hypothesis that
the assemblage of terrestrial mammals in sites with more intense degradation show
greater loss of taxonomic and functional diversity. We quantified the taxonomic and
functional diversity of eight terrestrial mammal seed-disperser species across a
degradation gradient in the eastern Brazilian Amazon. We installed camera-traps in 15
lowland sites within small-holder properties with different degrees of degradation (five
sites each of late second-regrowth forest, early second-regrowth forest and abandoned
pasture). Species richness and functional dispersion were compared with 15 paired
forest control sites. We found a significant reduction in taxonomic and functional
diversity in degraded areas. Yet, we also found that diversity in degraded sites could be
similar to control sites even in some early-second regrowth areas. Our findings suggest
that when surrounded by large intact forest areas the taxonomic and functional diversity
close to human small-holdings can return to pre-degradation values.
PORTUGUESE ABSTRACT
Há um interesse crescente na restauração/regeneração de hábitats neotropicais
degradados, mas o papel potencial dos regeneradores naturais permanece incerto. As
respostas de mamíferos terrestres à fragmentação e perda de hábitat já são conhecidas,
mas ainda não se sabe como este grupo responde aos efeitos da degradação florestal.
Nesse estudo quantificamos a diversidade funcional e taxonômica de oito espécies de
mamíferos terrestres dispersores de sementes ao longo de um gradiente de degradação
17
na Amazônia brasileira oriental. Testamos a hipótese que áreas que sofreram
degradação nos anos mais recentes apresentam maior perda da diversidade comparadas
com as áreas de degradação mais antiga. Instalamos armadilhas-fotográficas em 15
áreas com diferentes graus de degradação (cinco áreas cada de floresta secundária velha,
floresta secundária nova e pasto abandonado) e comparamos com as suas áreas
pareadas-controle (floresta intacta sem registro de extração mecanizada de madeira).
Encontramos uma redução significativa no número e diversidade de espécies em áreas
degradadas. Nossos resultados sugerem que quando rodeados por grandes áreas
florestais contínuas, a diversidade taxonômica e funcional pode retornar a valores de
pré-degradação.
Keywords: Amazon rainforest; Brazil; camera-trapping; intact forest; second-regrowth
forest; species loss.
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1
INTRODUCTION 2
AGRICULTURE CONTINUES TO DRIVE FOREST LOSS AND FRAGMENTATION ACROSS THE BRAZILIAN 3
AMAZON (Lewis et al. 2015, INPE 2016). The loss and fragmentation of tropical forests causes 4
drastic losses of species diversity and biotic interactions at local, regional and global scales 5
(Haddad et al. 2017). One option to revert this loss of diversity is the restoration of degraded 6
forests and deforested landscapes (Chazdon & Uriarte 2016). However restoration actions are 7
often considered to be economically expensive, especially in developing nations (Aronson et al. 8
2006). Faced with limited resources there is increasing interest in integrating natural regeneration 9
within restoration actions (Chazdon & Uriarte 2016). Plant-animal interactions are fundamental 10
for tropical forest biodiversity (Bascompte & Jordano 2007) and the recovery of faunal diversity 11
and associated ecosystem services (e.g. seed dispersal) are fundamental for natural regeneration 12
processes in degraded forests (Bowen et al. 2007, Chazdon & Uriarte 2016). 13
Mammals play an important role in the recovery processes of altered areas, because of their 14
capacity for dispersal and predation of seeds and seedlings of many plant species (Stoner et al. 15
2007). Medium and large-bodied mammals (weight> 1 kg) can disperse a large numbers of seeds 16
over long distances (Wunderle 1997, Stoner et al. 2007). For example, lowland tapirs can travel 17
over 4 kilometers per day (Fragoso 1997) and disperse seeds of more than 70 species with 18
different types and sizes of seeds in a single location (Hibert et al. 2013). The absence of large 19
mammals may release some plant species from the herbivory and increase their dominance, which 20
consequently decreases biodiversity in forests (Wright et al. 2007, Terborgh et al. 2008). 21
Traditional analyzes of biological diversity such as number of species, abundance and 22
composition consider that the species of an assembly are phenotypically similar and do not 23
19
necessarily reflect the intrinsic ecological and evolutionary attributes of the species (Moretti et al. 24
2009, Villéger et al. 2010, Weiher 2011). Functional traits are measures of diversity that 25
incorporate phenotypic information from species that directly affect the individual's performance 26
in the environment (Weiher 2011, Mason & de Bello 2013). Functional traits allow evaluation of 27
how morphological, physiological and/or behavioral characteristics respond to changes along an 28
environmental gradient (Mason et al. 2013). Degraded areas at different stages of regeneration 29
filter which species with specific functional traits persist in secondary vegetation (Keddy 1992, 30
Lohbeck et al. 2014). These traits allow species to meet their ecological requirements in degraded 31
forest landscapes. 32
The responses of medium and large-bodied terrestrial mammals to habitat loss and 33
fragmentation have been extensively evaluated for taxonomic diversity, such as species number, 34
abundance and composition (Peres 2001, Asquith & Mejía-Chang 2005, Michalski & Peres 2007). 35
However, it is not yet known how the functional diversity of medium and large-bodied mammals 36
respond to the effects of forest degradation and which functional traits are sensitive to changes in 37
the quality of degraded habitats. In this study we analyzed the changes in functional and 38
taxonomic diversity of medium and large-bodied terrestrial mammals important for natural 39
regeneration, especially seed dispersal along a degradation gradient (intact forest, late second-40
regrowth forest, early second-regrowth forest, abandoned pasture) in terra-firme forest in the 41
eastern Brazilian Amazon. Our hypothesis is that areas that have suffered degradation in recent 42
years (early second-regrowth forest) or with greater intensity (abandoned pasture) present greater 43
loss of taxonomic and functional diversity compared to areas of late second-regrowth and intact 44
forest. We predict that functional diversity and number of species will be reduced or lost in areas 45
that have been recently or more intensely degraded. 46
20
47
METHODS 48
STUDY AREA.—This study was conducted in private properties surrounding the Amapá National 49
Forest (Floresta Nacional Amapá —hereafter ANF). ANF is a sustainable-use protected area of 50
approximately 460,000 ha (ICMBio 2014), located on the pre-Cambrian Guianan shield craton at 51
the base of the Tumucumaque Uplandsin the northeast Brazilian Amazon (0°55’29”N, 52
51°35’45”W, Fig. S1). The regional phytophysiognomies consist of evergreen tropical rainforest 53
vegetation, predominantly never flooded “terra-firme” forest, with some areas of flooded forest, 54
bamboo and rocky outcrops (ICMBio 2014). The regional climate is classified by Köppen-Geiger 55
as Am (Equatorial monsoon, (Kottek et al. 2006)) with annual rainfall ranging from 2,200 mm to 56
2,500 mm during the last five years (2012 – 2016, (ANA 2017)). During the months with highest 57
precipitation levels (February, March and April), rainfall may reach 500 mm/month. The dry 58
season (September to November) is characterized by total precipitation below 150 mm/month 59
((ANA 2017), Fig. S2). 60
The ANF is part of a large (> 4 million hectares) connected group of protected areas (Fig. 61
S1, (ICMBio 2014)) that maintain both continuous undisturbed forests and the complete regional 62
community of medium-sized and large-bodied vertebrates (ICMBio 2014, Togura et al. 2014, 63
Michalski et al. 2015). The maintenance of medium-sized and large-bodied vertebrates that are 64
often preferred hunter targets (Peres & Palacios 2007) can be largely explained by the relatively 65
low human population densities in the study area. The most recent census provides an estimate of 66
3.8 habitants/km2 in the area (Porto Grande municipality, (IBGE 2010)). Although population 67
density across Brazilian Amazonia ranges widely (from <1 to >1000 inhabitants per km2), the 68
population density in our study area appears to be fairly representative considering the densities 69
21
from all nine states of the legal Brazilian Amazon (IBGE 2010, Norris et al. 2011). We therefore 70
believe that our study region is representative of the most frequently encountered human 71
population density across Brazilian Amazonia (IBGE 2010, Norris et al. 2011). 72
73
SAMPLING DESIGN.—Data were sampled during the wet-dry season transition (May to September 74
2016), with total monthly rainfall ranging from 80 – 171 mm (Fig. S2). This period corresponds to 75
the peak/end of fruiting of lowland Amazon forests in the study region (Steege & Persaud 1991, 76
van Schaik et al. 1993, Mendoza et al. 2017), and as such was chosen to obtain the best possible 77
sample of terrestrial frugivores expected to be active during periods of fruit and seed availability 78
(Bodmer 1991, Bodmer & Ward 2006, Hanya & Aiba 2010). Data collection was conducted in 15 79
terra-firme sites located in private small-holder properties that were selected on the basis of 80
differences in land-use histories and forest succession/regeneration stage (Fig. S1). All sites were 81
close (110 – 500m) to rivers that are navigable by motorized boats (100 – 200m wide) but due to 82
riverbank formation the sites are never flooded. Based on the land-use history these 15 sites were 83
grouped into three degradation classes: late second-regrowth forest (N = 5, most recent human 84
disturbance between 20 and 25 years), early second-regrowth (N = 5, most recent human 85
disturbance between 1 and 5 years), and pasture (N = 5, recently cleared and abandoned pasture 86
areas dominated by grasses/herbs but that had never been used to raise livestock, with the most 87
recent disturbance between 1 and 17 years). Each of the 15 degraded sites was paired with a 88
nearby (30 to 150 m) control site i.e. 20 – 30 m tall terra-firme forest site without a history of 89
mechanized timber extraction. 90
91
22
MAMMAL SURVEY.—To sample mammal seed dispersers, we installed camera traps 92
equipped with infrared triggers (Bushnell Trophy Cam, 8MP, Overland Park, KS, USA) in each of 93
the 30 sites. Cameras were placed at 14 sites for 30 consecutive days (June-July 2016) then 94
immediately transferred to the remaining 16 sites (July-August 2016). All cameras were installed 95
30–40 cm above the ground and were programmed to film for 40 seconds post-activation, with 10 96
second intervals between videos. Cameras functioned continuously (24 hours a day) during the 97
30-day sample period. In some of the pasture sites, we had to exclude a number of collection days 98
due to memory cards becoming full and batteries finishing. The species recorded by the camera 99
traps were identified with the aid of field guides (Emmons & Feer 1997, Reis et al. 2006, Paglia et 100
al. 2012). Scientific names follow (Paglia et al. 2012). 101
102
FUNCTIONAL DIVERSITY ASSESSMENT.—We considered as ‘functional’ a morphological or 103
behavioral trait that can be relevant to ecosystem functioning or filtered by environmental 104
gradients (natural or human-induced) (Dıaz & Cabido 2001). We selected four traits (trophic 105
guild, group living, body mass, and home range, Table 1) that influence/characterize species 106
interactions with the tropical flora including seed dispersal, herbivory, seed predation, and 107
trampling (Stoner et al. 2007, Wright et al. 2007). Trophic guild (categorical, with 3 classes: 108
scatter-hoarder, folivore-frugivore and omnivore-frugivore), group living (binomial, yes or no), 109
and body mass (log transformed for analyses) reflect the type, distance and amount of fruits and 110
seeds that species consume. Home range (categorical, four classes: 1=0–10ha; 2=11–50ha; 3=51–111
100ha; 4=>100ha) strongly influences the spatial distribution and extent to which a species travels 112
in search of food and disperses seeds (Stoner et al. 2007, Wright et al. 2007). 113
114
23
DATA ANALYSIS.— All analysis were conducted using the R language and environment for 115
statistical computing (R Core Team 2016), with base functions and functions available in the 116
following packages: vegan (Oksanen et al. 2016), FD (Laliberté et al. 2014), and ggplot2 117
(Wickham 2009). 118
To estimate the relative abundance of mammals, we considered only independent videos, 119
with over 30 min intervals when the same species was recorded during the same day on the same 120
camera (Norris et al. 2010, Michalski et al. 2015). The relative abundance of each species was 121
expressed as the number of independent videos per 10 trap-days (Michalski & Peres 2007, Norris 122
et al. 2010, Michalski et al. 2015). To assess whether the sampling effort was sufficient to record 123
the majority of species in the degraded and control sites and the three degradation classes, we 124
compared cumulative species curves with the specaccum function (Oksanen et al. 2016). 125
We calculated a taxonomic diversity (TD) and functional diversity (FD) value for each of 126
the 30 sites. Taxonomic diversity was calculated as the observed species richness (hereafter 127
“species richness”) at each site. Although there are myriad taxonomic diversity metrics, we chose 128
species richness as it is both widely used and clearly interpretable (Hortal et al. 2006, Magurran & 129
McGill 2011) and with eight species and 30 sites there were elevated correlations between 130
richness values and alternatives such as Shannon and Simpson diversity (Spearman rho > 0.89). 131
Functional diversity was calculated using Functional Dispersion (FDis) (Laliberté & Legendre 132
2010). We used FDis because it is not strongly influenced by outliers, accounts for relative 133
abundances, is unaffected by species richness and can be calculated from any 134
distance/dissimilarity measure (Laliberté & Legendre 2010, Laliberté et al. 2014), and having 135
been used in a similar study (Ahumada et al. 2011). Functional Dispersion was estimated with the 136
dbFD function (Laliberté et al. 2014). To examine patterns in taxonomic and functional diversity 137
24
between the degradation intensity classes we calculated pair-wise differences between degraded 138
and control site values. 139
TABLE 1. Functional traits and number of independent videos (detection) and relative abundance 140 (RA) of eight mammal species along a degradation gradient in the eastern Amazon. 141
Functional traits Detectione RAf
Order/Species GLa BMb HRc TGd Control Degraded Control Degraded
Rodentia
Cuniculus paca No 9.3 11 FF1,2 12 14 1.2 1.4
Dasyprocta leporina No 5.5 (3-8) 11 SH1,2 91 29 9.1 2.9
Myoprocta acouchy No 1 11 SH1,2 17 5 1.7 0.5
Artiodactyla
Mazama americana No 36 (24-48) 31,2 FF1,3 9 11 0.9 1.1
Mazama nemorivaga No 20 (15-25) 21 FF1,3 5 2 0.5 0.2
Pecari tajacu Yes 26 (17-35) 41 OF1,3 27 5 2.7 0.5
Tayassu pecari Yes 35 (25-45) 41 OF1,3 1 2 0.1 0.2
Perissodactyla
Tapirus terrestris No 260 41 FF1,3 3 3 0.3 0.3
a Group living, from Jones et al. (2009). 142
b Body mass, in kg (log transformed for analyses). From Paglia et al. (2012). 143
c Home range class. 1=0–10ha; 2=11–50ha; 3=51–100ha; 4=>100ha. From 1Jones et al. (2009), 144 2Maffei and Taber (2003). 145
d Trophic guild. FF = Folivore-frugivore, SH = Scatter-hoarder, OF = Omnivore-frugivore, from 146 1Paglia et al. (2012), 2Arita et al. (1990), 3Bodmer (1991). 147
e Total detections with independent videos. 148
f Relative abundance (RA) expressed as the number of independent videos per 10 camera-trap 149 days. 150
25
151
RESULTS 152
SAMPLING EFFORT AND MAMMAL DIVERSITY.— From a sampling effort of 827 camera-trap days 153
(450 and 377 camera-trap days, control and degraded sites respectively), we obtained an overall 154
capture rate of 0.29 videos per trap-day (236 independent videos/ 827 trap-days). Overall there 155
were less detections in degraded compared with control areas (165 and 71 independent videos, 156
control and degraded areas respectively). The number of detections also declined with increasing 157
degradation intensity (45, 26, 0 independent videos, late second-regrowth, early second-regrowth, 158
pasture respectively). 159
We recorded between zero and six mammal species at each site (Fig. 1). The species 160
accumulation curves tended to stabilize (i.e. approached an asymptote), suggesting that sampling 161
effort was sufficient to detect the eight mammal species when all (N=30), control (N=15) and 162
degraded (N=15) sites were considered (Fig. S2). All eight species were recorded in late second-163
regrowth sites, where the accumulation curve also approached an asymptote (Fig. S3). In contrast 164
a total of five (63%) species (Dasyprocta leporina, Myoprocta acouchy, Mazama americana, M. 165
nemorivaga and Pecari tajacu) were recorded in the early second-regrowth sites (Fig. S3). None 166
of the eight species were recorded on the abandoned pasture. 167
168
TAXONOMIC AND FUNCTIONAL DIVERSITY.— There was a clear loss in species richness and 169
functional dispersion in pasture areas, however several early and late second-regrowth sites 170
showed high number of species and functional dispersion (Fig. 1). 171
26
172 Figure 1. Comparison of species richness and functional dispersion along a degradation gradient 173 in the eastern Amazon. Boxplots show means and 95% confidence limits estimated via 174
nonparametric bootstrap. 175 176
Taxonomic diversity declined with increasing degradation intensity, with a reduction in mean 177
species richness in both early second-regrowth and pasture sites (Fig.1). In contrast, both late and 178
early second-regrowth classes retained similar mean functional diversity values to those found in 179
control sites (Fig. 1). 180
Species richness differed markedly between degraded areas and the paired controls (Fig. 2, 181
one-way ANOVA with White-corrected covariance matrix, F2, 12 = 15.8, P < 0.001). There was a 182
significant reduction (95% CI did not overlap 0) in the number of species found in pasture and 183
early secondary-regrowth areas (Fig. 2). In contrast only pasture areas showed a significant 184
reduction in functional dispersion (Fig. 2) and there was no significant difference between 185
degradation class (Fig. 2, one-way ANOVA with White-corrected covariance matrix, F2, 12 = 0.99, 186
P = 0.40). In other words, the late secondary-regrowth sites lost on average 15.3% in functional 187
diversity but gained 5% in species richness compared with control areas (Fig. 2). Whereas the 188
more intensely degraded early second-regrowth sites suffered reductions in both mean functional 189
27
and taxonomic diversity (31.7% and 12%, species richness and functional dispersion respectively, 190
Fig.2). With zero detections, pasture sites lost on average 100% of taxonomic and 60% of 191
functional diversity (one area where one and zero species were recorded at the paired control and 192
degraded sites) (Fig. 2). 193
194
195
Figure 2. Percentage differences in species richness and functional dispersion along a degradation 196
gradient in the eastern Amazon. Pair-wise differences calculated using control sites as reference. 197 Lower and higher species number and functional dispersion are represented by negative (−) and 198 positive (+) values respectively. Boxplots show means and 95% confidence limits estimated via 199
nonparametric bootstrap. 200
201
DISCUSSION 202
Our results indicate that more intensely disturbed sites, such as abandoned pastures, and early (1-5 203
year) second-regrowth forests experience reduced taxonomic and functional diversity of medium 204
and large bodied terrestrial mammal species that are potentially important for the maintenance and 205
regeneration of Amazon forests. Here we discuss our findings firstly in light of the sampling 206
design adopted and then in relation to the potential for the regeneration of degraded Amazon 207
forests. 208
209
28
SAMPLING EFFORT AND MAMMAL COMMUNITY. — The difference between the observed and 210
extrapolated species richness values obtained indicates that our sampling effort was sufficient to 211
record all eight species in both control and degraded sites. This finding was to be expected, as all 212
eight species are widespread and ubiquitous across lowland Amazon forests (Arita et al. 1990, 213
Emmons & Feer 1997, Peres & Palacios 2007, Paglia et al. 2012). However, fewer species were 214
detected in the more intensely disturbed sites (early secondary-regrowth and pasture). We believe 215
that the absence of some species is not related to the sampling effort, but factors associated with 216
anthropogenic disturbances such as hunting around the small holder properties (Michalski & Peres 217
2007, Peres & Palacios 2007, Wright et al. 2007). 218
Differences in sample effort are known to determine the number of species detected 219
(Magurran & McGill 2011). None of the target species were recorded in pasture sites, which also 220
had a lower sampling effort (77 camera-trap days). This reduced sampling effort could contribute 221
to the reduced number of species detected in pasture sites. Previous studies have shown that 222
several of our study species do use pasture areas (Estrada et al. 1994, Daily et al. 2003) and we 223
cannot exclude the possibility that increased effort would result in the detection of at least some 224
species that may intermittently traverse pasture sites. With the same effort (77 camera-trap days) 225
we detected 3 and 6 species in early and late second-regrowth sites, which is still well above the 226
zero detections in pasture sites. We therefore conclude that the reduced sample effort does not 227
generate a systematic bias in our analysis. Given the stark reduction in pasture sites and our 228
overall survey effort, we believe that the observed patterns in taxonomic and functional diversity 229
generally reflect the true patterns (e.g. species rarity) in the different degradation intensity classes. 230
231
29
TAXONOMIC AND FUNCTIONAL DIVERSITY. — We expected taxonomic and functional diversity to 232
decrease with increasing land use intensity (Flynn et al. 2009). As expected we found drastic 233
reduction in taxonomic and functional diversity in pasture areas, but considerably more variation 234
in early and late second-regrowth areas. In a global review Bowen et al. (2007) showed that 235
richness/abundances are variable in abandoned pasture, regrowth forest and control areas for 236
diverse species groups (invertebrates, reptiles, birds and mammals). Our eight study species 237
include a broad spectrum of traits (e.g. body size ranges over three orders of magnitude) and are 238
found across tropical and sub-tropical regions of South America (Emmons & Feer 1997, 239
Eisenberg & Redford 1999). As the species are found across a variety of habitats, a direct effect of 240
differences in habitat quality is unlikely. Rather, we expect the variation in the results to reflect 241
differences in both species traits and human impacts (Arita et al. 1990, Peres & Palacios 2007, 242
Wright et al. 2007). 243
We found that taxonomic and functional diversity was divergent among the degraded areas. 244
For example, the number of species was greater in late second-regrowth compared with early 245
second-regrowth sites but the functional diversity values were more similar. Although species 246
were lost, the functional diversity of the mammal assemblage was retained at intermediate 247
degradation intensity (early second-regrowth sites, excluding pasture). The persistence of 248
functional diversity in this group of mammals is good news for forest landscape restoration 249
initiatives (Wright et al. 2007, Chazdon & Uriarte 2016). 250
There are a number of options for forest restoration in regions where human populations are 251
below 10/km2 (IUCN WRI 2014). The proximity to large areas of remnant forests and potential 252
for agroforestry generate opportunities for both the restoration of ecosystem services and socio-253
economic development (Chazdon & Uriarte 2016). Different ecological, biophysical and 254
30
socioeconomic factors correlate with the success of natural regeneration of tropical forests 255
(Latawiec et al. 2016). Within our study area there is a potential to generate US$ 2,958,800 a year 256
from açai (Euterpe oleracea) agroforestry production close (<2km) to rivers (Norris et al. 2016). 257
Although passive/natural regeneration is not without costs for local small-holders (Zahawi et al. 258
2014), the potential to integrate lucrative açai agroforestry and natural regeneration facilitated by 259
functionally diverse terrestrial mammal assemblages in degraded areas must not be overlooked. 260
261
CONCLUSIONS 262
Our findings generate new insight not only for understanding species ecology but also the 263
potential role for this group in the regeneration of degraded forest areas across the Amazon basin. 264
Although we found a loss in taxonomic and functional diversity with increasing disturbance 265
intensity we also found that diversity in degraded sites could be similar to control sites even in 266
some early second-regrowth areas. These findings suggest that the functional diversity of these 267
species (including the potential to act as regenerators of degraded areas) can be retained in 268
degraded forest areas close to human small-holdings if there is both a low human population 269
density and large areas of contiguous protected areas. 270
271
ACKNOWLEDGMENTS 272
The Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) and the Amapá 273
National Forest staff (Érico Emed Kauano and Sueli Gomes Pontes dos Santos) and the Federal 274
University of Amapá (UNIFAP) provided logistical support. We thank the Brazilian Ministério do 275
Meio Ambiente (“MMA”) for authorizing data collection (SISBIO permits 40355–1 and 47859-276
2). We also thank the local landowners who gave permission for data collection at their properties. 277
31
We are deeply indebted to Cremilson and Cledinaldo Alves Marques and family for their 278
dedication, commitment and assistance during the fieldwork. We thank the following Brazilian 279
agency for financially supporting data collection: Conselho Nacional de Desenvolvimento 280
Cientifico e Tecnológico (“CNPq” project #446926/2014-0). Authors also thank FAPEAM 281
(scholarship to PB, #062.01173/2015) and CAPES (scholarship to AAS). 282
283
DATA AVAILABILITY STATEMENT 284
The data used in this study will be archived via the PPBio node of the DataOne respository: 285
https://www.dataone.org/ . 286
287
288
32
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36
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22:284-287,doi:10.1111/rec.12098. 425
37
SUPPLEMENTAL MATERIAL 426
Supplemental material S1: Study sites. 427
428
Fig. S1. Map of the study area in the eastern Amazon. Showing the location of 15 study sites, grouped into 429
three degradation intensity classes: late second-regrowth forest (LSF, triangles), early second-regrowth forest 430
(ESF, squares) and pasture (PA, circles). 431
432
38
Supplemental S2: Study area rainfall 433
Camera traps were installed and operational across the wet-dry transition (May – September 2016). During the 434
survey period the total monthly rainfall was 168, 152, 171, 100 and 80 mm (monthly totals for May, June, July, 435
August and September respectively, Fig. S2). 436
437
438
Figure S2. Monthly rainfall recorded close (36 km) to the Amapá National Forest study site. Weather station 439
data available from the Brazilian National Water Agency (station ID: 8052000). Monthly totals are presented 440
from five years (2012, 2013, 2014, 2015 and 2016). Boxplots show means and 95% confidence limits estimated 441
via nonparametric bootstrap. The blue line and shaded areas are the mean value and 95% confidence intervals 442
from a GAM model illustrating the trend in rainfall. 443
444
ANA. Sistema de Monitoramento Hidrológico (Hydrological Monitoring System). Agência Nacional de 445
Águas[[nl]]National Water Agency, Available at http://hidroweb.ana.gov.br 2016 [08.01.2017]. 446
447
448
39
Supplemental S3: Species accumulation curves from all, control and degraded sites. 449
450
Figure S3: Species accumulation curve. Detection of species recorded with camera-traps randomized 1000 451
times and results used to derive mean (solid blue line) and 95% confidence intervals (light blue polygon). 452
Bootstrap estimates of extrapolated species richness and 95% confidence intervals are shown with black line 453
and light gray shaded area, respectively. Comparison between all (n = 30), control (n = 15) and degraded (n = 454
15) sites. 455
456
40
Supplemental S4: Species accumulation curves from degraded sites.
Figure S4: Species accumulation curve. Detection of species recorded with camera-traps
randomized 1000 times and results used to derive mean (solid blue line) and 95%
confidence intervals (light blue polygon). Bootstrap estimates of extrapolated species
richness and 95% confidence intervals are shown with black line and light gray shaded
area, respectively. Comparison between early (n = 5) and late (n = 5) secondary-
regrowth sites.
41
CONCLUSÃO
Os mamíferos formam uma parte importante na regeneração das florestas. A degradação
ambiental tem uma resposta usualmente negativa na ocorrência das espécies e também
nos tipos funcionais de espécies. Consequentemente, a ausência de uma espécie
frugívora tem um efeito negativo na regeneração de ambientes degradados via dispersão
de sementes. Nesse estudo mostramos para mamíferos terrestres de meio e grande porte
dispersores de sementes que a diversidade funcional aumenta e a diversidade
taxonômica diminui em áreas que já iniciaram a regeneração. Em áreas com impactos
mais severos como pastos abandonados a diversidade é praticamente perdida e a
recuperação do banco de sementes é feita somente por aves e morcegos.
Nossos resultados geram uma nova percepção não apenas para a compreensão da
ecologia das espécies, mas também o papel potencial desse grupo na regeneração de
áreas florestais degradadas na bacia amazônica. Apesar de termos encontrado uma perda
na diversidade taxonômica e funcional com o aumento da intensidade de perturbação,
verificou-se também que a diversidade em sítios degradados poderia ser semelhante aos
locais de controle, mesmo em algumas áreas de segundo rebrote precoce. Esses
resultados sugerem que a diversidade funcional dessas espécies (incluindo o potencial
de atuar como regeneradores de áreas degradadas) pode ser mantida em áreas florestais
degradadas próximas às pequenas propriedades humanas se houver uma baixa
densidade populacional humana e grandes áreas contíguas de áreas protegidas.
42
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