Moura, N. 2014 - Sustainable Amazon

Transcription

UNIVERSIDADE FEDERAL DO PARÁ/MUSEU PARAENSE
EMILIO GOELDI
PROGRAMA DE PÓS-GRADUAÇÃO EM ZOOLOGIA
DOUTORADO EM ZOOLOGIA
Biodiversidade de aves em múltiplas paisagens na
Amazônia brasileira
Tese apresentada ao Programa de Pósgraduação
em
Zoologia,
Nível
Doutorado, do Museu Paraense Emílio
Goeldi e Universidade Federal do Pará
como requisito parcial para obtenção do
grau de Doutor em Zoologia.
Orientador: Dr. Alexandre Aleixo
Co-orientador: Dr. Toby A. Gardner
Belém- PA
2014
Nárgila Gomes de Moura
BIODIVERSIDADE DE AVES EM MÚLTIPLAS PAISAGENS NA
AMAZÔNIA BRASILEIRA
Tese aprovada como requisito para obtenção do grau de Doutor em Zoologia
no curso de Pós-Graduação em Zoologia do Museu Paraense Emílio Goeldi e
Universidade Federal do Pará.
Dr. Alexandre Aleixo
Orientador
Museu Paraense Emílio Goeldi
Dr. Toby A. Gardner
Co-orientador
Stockholm Environment Institute
Dra. Ima Vieira
Titular
Dr. Mario Cohn-Haft
Titular
Instituto Nacional de Pesquisa da Amazônia
Dr. Marco Aurélio Pizo
Titular
Universidade Estadual Paulista Júlio de Mesquita Filho
Dr. Marcos Pérsio Dantas Santos
Titular
Universidade Federal do Pará
Dr. Luciano Montag
Suplente
Universidade Federal do Pará
Dr. Ulisses Galatti
Suplente
2
"There
is,
however,
one
natural
feature of this country, the interest
and grandeur of which may be fully
appreciated in a single walk: it is the
"virgin forest."
(carta de Wallace em 1849 (sobre
Amazônia) aos membros da Instituição
dos Mecânicos em Neath, no País de
Gales publicado no livro My Life de
Wallace em 1905).
3
Agradecimentos
Tenho imensa gratidão por diversas pessoas e instituições que tornaram essa tese
possível. Arrisco dizer que esses quatro anos foram os melhores que já vivi, sempre
cheio de desafios, conquistas e muito aprendizado.
Agradeço ao CNPq pela concessão da bolsa de doutorado e ao programa Ciências
sem fronteiras pela grande oportunidade de ficar 6 meses na Universidade de
Cambridge, onde a convicência com outros pesquisadores e contato direto com o
inglês foi absolutamente fundamental para a elaboração dessa tese .
Agradeço ao Instituto Nacional de Ciência e Tecnologia - Biodiversidade e Uso da
Terra na Amazônia (CNPq 574008/2008-0), National Environment Research Council
(NE/G000816/1), Darwin Initiative (17–023), CAPES, Lancaster University, Embrapa
Amazonia Oriental (SEG: 02.08.06.005.00), e The Nature Conservancy pelo
financiamento do projeto Rede Amazônia Sustentável.
Agradeço aos proprietários e sindicatos dos produtores rurais de Paragominas e
Santarém pelo apoio e autorização da pesquisa nas propriedades.
Agradeço imensamente ao meu orientador Dr. Alexandre Aleixo, pela valiosa
oportunidade que agarrei com muita vontade, pelo voto de confiança, apoio e também
pelas gratificantes conversas e discussões, pela amizade!
Agradeço, mas sem ter realmente como agradecer ao meu Co-Orientador Dr. Toby
Gardner, por ter aceitado me orientar em um projeto tão especial como Rede
Amazônia Sustentável. Agradeço também por ter me recebido de braços abertos
durante o meu período sanduíche na Universidade de Cambridge, que sem dúvida um
uma experiência inesquecível. Pelas prazerosas conversas, reuniões, discussões,
dedicação, otimismo, pela confiança e pela valiosa amizade. TOBY MUITO
OBRIGADA!
Também agradeço profundamente ao Dr. Alex Lees pelos grandes e intensos
ensinamentos durante os oito meses de trabalho de campo, com quem aprendi não
apenas a identificar, mas apreciar toda a beleza dentro de cada canto, de cara
raridade, de cada nova descoberta. Agora a ornitologia pra mim deixou de ser apenas
trabalho, passou a ser também way of life! Agradeço pela imensa paciência em corrigir
minhas bobagens, o que era ainda pior por serem em inglês, pelas conversas,
discussões, pelas ótimas passarinhadas (sempre tão inspiradoras).
4
Também agradeço a Dra Joice Ferreira, fundamental na execução dessa pesquisa,
pela grande contribuição nos manuscritos. Também agradeço pelos inesquecíveis
momentos em que também esteve presente durante minha estadia em Cambridge,
pelos deliciosos jantares sempre regados a bons vinhos e boas músicas, pela grande
amizade! Valeu Dra!
Agradeço ao Dr. Jos Barlow pelas imensas contribuições e discussões na preparação
dos manuscritos.
Agradeço também ao tão carinhoso Dr. William Overall (Bill), a primeira pessoa a me
mostrar a imensidão da floresta amazônica. Sempre cheio de histórias fascinantes.
Agradeço a duas grandes amigas Ivaneide e Taty que sempre foram meu braço direito
durante todo o doutorado, conversas sempre tão divertidas e inspiradoras. Ivaneide
sempre pronta no Skype para qualquer grito! A Taty sempre tão positiva e carinhosa!!
Obrigada queridas, vocês foram muito importantes nessa caminhada!
Agradeço aos colegas do MPEG: Antonita, Boto, Bruno, Denise, Dudu, Fátima, Gabi,
Lincoln, Marcos, Mateus, Mel, Pablo, Romina, Sidney, Tibério, todos sempre muito
queridos!
Também agradeço às minhas queridas amigas Grazi e Tharsi que, pelas valiosas
conversas, discussões e inspirações e claro e pela ajuda em algumas análises.
Aos guerreiros do RAS: Abel, Amanda, Bibito, Bob, Brad, Ciça Christian, Dadá,
Edevandro (in memoriam), Erika, Karol, Luke, Martines, Nego (in memoriam), Pita,
Selma, Valderi, Williams.
Agradeço ao Ian e Nathália Thompson pela valiosa amizade, sempre presentes nas
melhores passarinhadas.
Aos meus queridos amigos goianos que me viram sair em busca de um sonho e
sempre estiveram muito presentes, mesmo distante: Antônio Estevão, Gleiciane,
Henrique, Negão, Rodolfo, Sejana, Taty, Yedda.
Agradeço também à Fernanda Carneiro, super companheira de graduação e que me
ajudou muito no processo de construção do meu projeto de doutorado, e mais tarde na
proposta para o doutorado sanduíche, hoje professora da UEG, uma pesquisadora
admirável! Valeu Fê!
5
Agradeço à minha família tão especial que sempre estiveram torcendo e estimulando
toda essa minha longa caminhada. Meus pais Max e Valdite fontes e inspiração sobre
o que é ser perseverante e capaz! Minhas queridas irmãs Lísia e Eveline, sempre ali
de prontidão e na torcida e vibrando a cada conquista! Minha querida vovó Georgeta,
um exemplo de disciplina e força de vontade. Amo vocês!
Por fim, agradeço a pessoa que esteve 24h por dia do meu lado durante os 4 anos,
sempre me enchendo de alegria e tornando qualquer desafio quase impossível em
uma imensa conquista. Alex, muito obrigada, sem você teria sido muito mais difícil ♥!
6
Sumário
Capítulo 1: Introdução geral
23
1.
Amazônia
23
2.
Mudanças de uso da terra
25
3.
As aves, a paisagem amazônica e as mudanças de uso da terra
28
4.
Projeto Rede Amazônia Sustentável (RAS)
29
5.
Objetivos e estrutura da tese
30
Capítulo 2: Avian biodiversity in multiple-use landscapes of the Brazilian
Amazon
32
Abstract
32
1.
Introduction
33
2.
Methods
34
2.1
Study regions and experimental design
34
2.2
Data analyses
37
3.
Results
38
3.1
Species richness responses
40
3.2
Differences in species composition
44
3.3
Differences in species richness with changes in landscape-scale total
forest cover
49
3.4
Additive partitioning of diversity
50
4.
Discussion
51
4.1
Production areas
51
4.2
Secondary forests
52
4.3
Disturbed primary forests
54
4.4
Effects of landscape scale forest loss on avian diversity
55
5.
Conclusions
55
Capítulo 3: Idiosyncratic responses of forest-associated Amazonian birds
to disturbance and land-use changes
57
Abstract
57
1.
Introduction
58
2.
Materials and methods
60
2.1
Study regions and experimental design
60
2.2
Bird surveys
62
2.3
Environmental variables
66
7
2.3.1 Local variables
66
2.3.2 Landscape variables
67
2.4
Data analysis
68
3.
Results
68
3.1
Species occupancy patterns
68
3.2
Importance of predictor variables
71
4.
Discussion
78
4.1
Patterns of avian species occupancy
78
5.
Conclusions
80
Capítulo 4: Two hundred years of local extinction in Eastern Amazonian 82
Abstract
82
1.
Introduction
83
2.
Methods
85
2.1
Study site
85
2.2
Data collection
86
2.3
Data analyses
87
3.
Results
88
3.1 Possible extinctions in the MRB
88
3.2 Forest dependency of threatened species
93
3.3 Reassessment of species threat status
94
4.
98
Discussion
4.1 Patterns of local extinction in the MRB avifauna
100
4.2 Colonization of MRB by non-forest bird species
102
4.3 The future of the MRB avifauna
102
Capítulo 5: Conclusão geral
105
1.
A importância das florestas primárias
106
2.
Valor da conservação das florestas secundárias
107
3.
Áreas agrícolas
109
4.
Conservação na Amazônia dentro e fora das áreas de proteção
110
5.
O futuro da Amazônia
112
6.
Pesquisas futuras
112
Referências Bibliográficas
113
Anexo 1
137
8
ANEXO 2
156
9
Lista de Figuras
Figura 1.1 Área com exploração madeireira em Paragominas (A) e
floresta primária intacta na Floresta Nacional de Tapajós , Belterra
24
(B) ( N. Moura).
Figura 1.2 Taxa anual de desmatamento na Amazônia legal entre
1988 e 2013 (INPE 2013).
25
Figura 1.3 Áreas de pastagem em Paragominas ( N. Moura).
26
Figura 1.4 Madeira explorada na Floresta Nacional do Tapajós
(Santarém) (A) e transporte madeira em Paragominas (B). N.
27
Moura.
Figura 1.5 Área de floresta primária sendo queimada (A) (J.
Barlow); resíduos de madeira para produção de carvão em
27
Paragominas (B) ( N. Moura).
Figura
1.6
Parceria
desenvolvida
sob
a
Rede
Amazônia
Sustentável.
30
Figure 2.1 Map of Paragominas (a) and Santarém/Belterra (b)
showing the location of the 18 catchments surveyed in each
municipality. Two example catchments are presented for each
municipality in (c) showing the location of transects and transects
design and positioning of point count stations (d).
35
Figure 2.2 Individual based species rarefaction curves per transect
between land-use systems considering the entire avian assemblage
(A and B) and forest-associated species (C and D) in PGM. Legend:
dark green- primary forest; light green - secondary forest; blue -
39
pasture; yellow - mechanised agriculture; red - plantation.
Figure 2.3 Individual-based species rarefaction curves per transect
between land-use systems considering the entire avian assemblage
(A and B) and forest birds (C and D) in STM. Legend: dark green primary forest; light green - secondary forest; blue - pasture; yellow -
10
mechanised agriculture; red - small-holder agriculture.
40
Figure 2.4 Species rarefaction curves per catchment in PGM and
STM, considering the entire avian assemblage (filled circles) and
forest birds (empty circles).
40
Figure 2.5 Box plots comparing avian species richness between
land-use types and degradation forest classes in PGM and STM,
using the entire avian assemblage (a and c) and just forest birds (b
and d). Non-significant pairwise differences between land-use types
are indicated by the presence of the same letter (according to Mann42
Whitney U).
Figure 2.6 Box plots comparing avian species richness between
land-use types, forest degradation classes and
secondary forest
age classes in PGM and STM, using the entire avian assemblage (A
and C) and just forest birds (B and D). Non-significant pairwise
differences between land-use types are indicated by the presence of
the same letter (according to Mann-Whitney U).
43
Figure 2.7 NMDS plots of community structure of forest birds in all
land-use types (a and c) and between different primary forest
disturbance classes (b and d) in PGM and STM. Considering all
land-use types (a and c) black circles = primary forest; empty circles
= secondary forest; grey squares = pasture; empty squares =
mechanised agriculture and black triangles = small-holder. For
different primary forest disturbance classes (b and d) black triangles
= undisturbed; grey hexagons = secondary forest; crossed squares
= burnt forest; empty hexagons = logged&burnt forest; grey
hexagons = logged forest; empty circles = secondary forest.
45
Figure 2.8 NMDS plots of forest species in each forest type in PGM
and STM. Legend: empty circles - primary forest; black triangle intermediate secondary forest; black square-old secondary forest;
black cross - young secondary forest; empty square - mechanised
agriculture; grey square - pasture; black circle - plantation and black
triangle - small-holder.
47
11
Figure 2.9 NMDS plots of community structure of entire avian
assemblage in all land-use types (a and c) and between different
primary forest degradation classes (b and d) in PGM and STM.
Considering all land-use types (a and c) black circles = primary
forest; empty circles = secondary forest; grey squares = pasture;
empty squares = mechanised agriculture and black triangles =
small-holder. For different primary forest disturbance classes (b and
d) black triangles = undisturbed; grey hexagons = secondary forest;
crossed squares = burnt forest; empty hexagons = logged&burnt
forest; grey hexagons = logged forest; empty circles = secondary
forest.
47
Figure 2.10 Linear regressions between percentage of primary
forest cover (aggregating all disturbance classes within a 10 km
radius of each catchment) and richness of forest birds in PGM adj.R²
= 0.46 and STM adj.R² = 0.79 (p-values significant at 0.001).
50
Figure 2.11 Linear regressions between percentage of total forest
cover (in a radius of 10 km) of each catchment, of forest birds
richness in PGM (adj.r² = 0.4) and STM (adj.r² = 0.75); (p-values
significant at 0.001).
50
Figure 2.12 Additive diversity partitioning (in %) in different land-use
systems in PGM and STM, using forest birds. Black = Alpha (point
counts); light grey = Beta (among point counts) and dark grey = Beta
(among transects).
51
Figure 3.1. Map of Paragominas (a) and Santarém/Belterra (b)
showing the location of the 18 catchments surveyed in each
municipality. Two example catchments are presented for each
municipality in (c) showing the location of transects and transects
design and positioning of point count stations and vegetation plots
(d).
61
Figure 3.2. Focal species (in taxonomic order) occupancy of
different land use types in the municipalities of Paragominas (filled
circles) and Santarém (empty circles).Illustrations reproduced with
the permission of Lynx Edicions.
70
12
Figure 3.3. Distribution of the weighted importance values of
environmental variables in primary forest for the 30 focal species in
PGM and STM. NTL: number of time the transect was logged; NTB:
number of time the transect was burned; EdgePS: Average
distances to forest edges (primary forest +secondary forest >10
years); PFD: percentage of forest pixels degraded; TPL: total
number of tree, palm and liana species; UD: understory density;
BLL: biomass of
leaf
litter; BT10: biomass of
trees with
circumference >10 cm; BDT: biomass of dead trees; DPC:
71
deforestation curvature profile.
Figure 3.4 Partial dependence plot for the three most important
variables from random forest analysis in Paragominas (top panel)
and Santarém (bottom panel). BT10: biomass of trees with
circumference >10 cm. EdgePS: Average distances to forest edges
(primary forest +secondary forest >10 years); PFD: percentage of
forest pixels degraded.
72
Figure 3.5 Ranked goodness-of-fit (pseudo-R²) models for each
focal species in Paragominas and Santarém.
73
Figure 3.6 R² weighted importance by species in PGM for each
environmental variable NTL: number of time the transect was
logged; NTB: number of time the transect was burned; EdgePS:
Average distances to forest edges (primary forest +secondary forest
>10 years); PFD: percentage of forest pixels degraded; TPL: total
BLL: biomass of
leaf
trees with
circumference >10cm; BDT: biomass of dead trees; DPC:
deforestation curvature profile, ELEV: Elevation.
74
Figure 3.7 R² weighted importance by species in STM for each
environmental variable. NTL: number of time the transect was
13
BLL: biomass of
leaf
trees with
deforestation curvature profile; ELEV: Elevation.
76
Figure 3.8. Cluster heat-map of species with goodness-of-fit ≥ 0.4
after RF modelling for both Paragominas and Santarém. Each cell is
coloured based on the R² weighted values generated by RF. The
cluster on the left side of each heat-map groups species with similar
response patterns according to their relationship with different
predictor variables. Table legend: F- frugivores, O- omnivore, Iinsectivore; Flock: SO- solitary, MF- monospecific flock, FD- flock –
dropout;
Strata:
M-
midstory,
C-
canopy,
U-
understory.
Environmental variables: NTL: number of time the transect was
BLL: biomass of
leaf
trees with
deforestation curvature profile; ELEV: Elevation.
77
Figure 4.1 Map indicating the position of the study regions MRB and
Paragominas in Brazil (a) and the state of Pará (b); extent of
remaining forest cover in the MRB (forest as dark pixels, urban and
agricultural areas in white) (c) and one of two specimens of Rufousrumped Foliage-gleaner (Philydor erythrocercum) collected by Sir
Alfred Russel Wallace at ‘Pará’ (old name for Belém) in May 1849
and deposited at the Natural History Museum, Tring, England (A. C.
Lees © Natural History Museum, Tring) (d). This latter species was
last reported in the MRB in 1965, but according to the Solow
calculations is potentially still extant. It is most likely to persist in the
6,367 km2 Refúgio de Vida Silvestre Metrópole da Amazônia, the
largest area of contiguous primary forest left in the MRB.
85
Figure 4.2 Last record, extinction date (year), and confidence
intervals for 47 species unrecorded in the Metropolitan region of
Belém, Brazil, after 1980 (gray squares, last record of species
presumed extinct but for which there are insufficient records to use
14
the Solow equation (n<4); white triangles, last record for species
considered extant based on Solow equation; black circles, date of
last record for species considered extinct based on Solow equation;
white circles, extinction date inferred based on Solow equation;
semi-filled diamond, species extant based on Solow equation and
extinct based on sighting rate; semi-filled circle, species extinct
based on Solow equation and extant based on sighting rate;
crosses, 95% confidence interval for extinct species based on Solow
92
equation).
Figure 4.3 Relationship between inferred extinction date in the
Metropolitan region of Belém and occupancy of catchments in
93
Paragominas, Brazil (r² = 0.16, p < 0.05).
Figure 4.4 Schematic of framework illustrating how time since last
record interacts with confidence of extinction (bold, globally
threatened species [IUCN 2013]; asterisk, included on the regional
red list). The framework can be used to determine how species can
be classified locally as possibly extinct, probably extinct or extinct
98
(adapted from Butchart et al. [2006]).
Figura
5.1
Gradiente
de
perturbação
em
Paragominas
e
Santarém/Belterra . (A) floresta primária intacta, (B) floresta primária
que sofreu corte seletivo, (C) floresta primária que sofreu corte
seletivo e queimada, (D) floresta secundária, (E) plantação de
eucalipto, (F) agricultura familiar, (G) pastagem e (H) agricultura
mecanizada. Fotos C, D e F. A.C. Lees e fotos A, B,E, G e H N.
105
Moura.
Figura 5.2 Guaruba guarouba (ararajuba). Espécie extinta na região
metropolitana de Belém. O último registro foi de A. Wallace em 1848
(A. C. Lees © Natural History Museum, Tring).
106
Figura 5.3 Espécies registradas em áreas de floresta primária e
secundária. (A) Philydor erythrocercum (limpa-folha-de-sobre-ruivo),
(B) Willisornis virdua (rendadinho), (C) Ibycter americana (gralhão) e
(D) Taeniotriccus andrei (maria-bonita) (N. Moura).
108
Figura 5.4 Espécies registradas nas paisagens agrícolas de
15
Paragominas
e
Santarém/Belterra.
(A)
Columbina
passerina
(rolinha-cinzenta), (B) Anthus lutescens (caminheiro-zumbidor),
Melanerpes candidus (pica-pau-branco) e (D) Crotophaga ani (anupreto) (N. Moura).
110
Figura 5.5 Áreas protegidas na Amazônia até 2010 (Veríssimo et al.
111
2011).
16
Lista de Tabelas
Table 2.1 Total number of transects allocated to each land-use type
in both study regions.
37
Table 2.2 PERMANOVA Pseudo-F statistic values of global test (pvalues in parenthesis) and t values of pair-wise comparison (pvalues in parenthesis) for forest birds composition in different landuse types and forest disturbance classes in two regions, PGM and
STM, of the Brazilian Amazon. NA indicates that the comparison is
not valid as the land use in question is unsampled in the respective
municipality.
46
Table 2.3 PERMANOVA Pseudo-F values of global test (p-values in
parenthesis) and t-values of pair-wise comparison (p-values in
parenthesis) for the forest bird assemblage in different land-use
types and primary forest degradation classes in PGM and STM. NA
indicates that the comparison is not valid as the land use is
unsampled in the municipality in question.
48
Tabela 2.4 PERMANOVA Pseudo-F values of global test (p-values
in parenthesis) and t-values of pair-wise comparison (p-values in
parenthesis) for the entire bird assemblage in different land-use
types, primary forest degradation classes and secondary forest age
in PGM and STM. NA indicates that the comparison is not valid as
the land use is unsampled in the municipality in question.
49
Table 2.5 Percentage of total species and forest birds (in
parentheses) shared between land-use system in PGM and STM.
53
Table 2.6 Percentage of all species and forest birds (in parentheses)
shared between different forest degradation classes in PGM and
STM.
53
Table 3.1 Total number of transects allocated to each land-use type
in both study regions
62
17
Table 3.2 Focal species and their respective life strategies such as
diet, feeding strategy, flocking behaviour and forest strata occupied.
PGM and STM represent Paragominas and Santarém-Belterra study
64
regions respectively.
Table 4.1 Species unrecorded in the last 33 years in the
Metropolitan region of Belém.
90
Table 4.2 Principle threats and Red List evaluations of threatened
taxa at the State (Pará), national (Brazil) and global (IUCN) level and
status of of the species in the MRB and Paragominas.
95
Table 4.3 Long term species loss from Neotropical forest regions.
99
18
Resumo
Cobrindo aproximadamente 5.500 km², a Amazônia é o maior remanescente de
floresta tropical do planeta. A região representa uma prioridade global para
conservação por estar estar sujeita às maiores taxas absolutas de perda e degradação
das florestas no mundo, colocando em risco a sua rica biodiversidade e importantes
serviços ecossistêmicos. Apesar da quantidade de trabalhos buscando entender quais
os impactos das mudanças de uso da terra sobre a biodiversidade ser crescente,
muitos estudos ainda são limitados pela escala, quantidade de amostragem e a
quantidade de habitats amostrados. Destarte, os objetivos dessa tese foram: 1) Avaliar
a perda de espécies de aves ao longo de um gradiente de impacto antrópico (que
variou desde floresta primária, floresta secundária, silvicultura, pastegem, agricultura
familiar e agricultura mecanizada) em duas diferentes regiões da Amazônia brasileira
(Paragominas e Santarém) na tentativa de esclarecer os efeitos da heterogeneidade
da paisagem, dos diferentes usos da terra na região e histórico de ocupação e deste
modo estimar o valor da conservação; 2) investigar os padrões de ocupação de
diferentes espécies e se esses padrões são influenciados por fatores locais, regionais
e históricos nos municípios de Paragominas e Santarém; 3) buscar evidência para
extinção histórica da avifauna de florestas de terra firme em uma
fronteira de
desmatamento antiga (a Região Metropolitana de Belém), e comparar com os padrões
de ocupação de uma área que possui impactos mais recentes (Paragominas). Em
Paragominas e Santarém foram selecionadas 18 microbacias aleatoriamente com 8 a
12 transectos onde foram feito pontos de escuta, amostragem da vegetação e solo. Os
resultados mais importantes mostraram que 1) as florestas primárias apresentaram
maior riqueza de espécies florestais, ao contrário das áreas agrícolas, que além da
baixa riqueza, também apresentaram uma comunidade diferente; 2) a riqueza nas
florestas primárias intactas foi estatisticamente semelhante àquela das florestas que
sofreram apenas corte seletivo; 3) a estrutura da comunidade foi, diferente entre todas
as classes de floresta primária; 4) as florestas secundárias apresentaram riqueza e
estrutura de comunidade intermediária, porém ainda estatisticamente diferentes as
florestas primárias; 5) a partição aditiva revelou que a composição de espécies variou
mais entre os transectos de floresta intacta, diminuindo de maneira constante em
transectos com o aumento da degradação florestal e intensidade do uso da terra; 6) as
espécies (florestais), focais ( declinaram ao longo do gradiente e foram raras nas
áreas de florestas secundárias e em geral ausentes nas áreas agrícola, respondendo
idiosincraticamente às diferentes variáveis ambientais; e 7) na região metropolitana de
19
Belém, 47 espécies (14% das espécies da região) estão provavelmente extintas sendo
a perda de habitat, degradação florestal, caça e tráfico de animais silvestres os
principais fatores resposáveis. Muitas dessas espécies que desapareceram nos
arredores de Belém, também são raras ou já estão extintas em Paragominas. Todavia,
a conservação de grandes extensões de floresta continua sendo o fator mais
importante para a conservação das espécies importantes do ponto de vista
conservacionista. Não menos importante, para diminuir a pressão de ocupação sobre
áreas florestais, a intensificação do uso nas áreas já defaunadas pode proteger os
remanescentes da degradação, além de ser o melhor caminho para equilibrar o
desenvolvimento e as metas de conservação.
20
Abstract
Covering about 5,500 km ² Amazon is the largest remaining expanse of tropical
rainforest. Thus, Amazonia is a global conservation priority subject to the highest
absolute rates of forest loss and degradation worldwide, jeopardizing its rich
biodiversity and important ecosystem services. Despite an increasing volume of work
trying to understand the impacts of land-use change on regional biodiversity, many
studies are limited by their spatial extent, sample size and the breadth of habitat types
studied. The aims of this thesis were to: 1) evaluate the loss of bird species along a
gradient of anthropogenic impact (ranging from primary forest to mechanized
agriculture) in two different regions of the Brazilian Amazon (Paragominas and
Santarém) in an attempt to elucidate the effects of landscape heterogeneity, differing
land-uses and history of occupation and thereby estimate their relative values for
conservation; 2) investigate the occupancy patterns of different species and whether
these patterns are influenced by local, regional and historical factors in the
municipalities of Santarém and Paragominas; 3) search for evidence of historical
extinctions of the avifauna of terra firme forests on an old deforestation frontier (the
metropolitan region of Belém) and compare the occupation patterns with an area which
has been impacted more recently (Paragominas). In Paragominas and Santarém 18
watersheds were selected randomly with 8-12 transects per watershed in which point
counts and vegetation sampling was carried out. The most important results indicate
that 1) primary forests showed exhibit the highest richness of forest species and
agricultural areas the lowest, with a near-complete turnover in community; 2) although
richest in species, undisturbed primary forests were not statistically separable in
richness from logged forests although they were from more depaurperate logged and
burned forest;. 3) community structure was however different between all classes of
primary forest; 4) secondary forests had intermediate richness and community
structure, but were still statistically different in both from primary forests; 5) diversity
partitioning revealed that species composition varied the most among undisturbed
forest transects, and steadily decreased with increasing forest degradation and landuse intensity; 6) focal species declined along the gradient and were rare in areas of
secondary forests and generally absent from agricultural areas and responded
idiosyncratically to different environmental variables; 7) the metropolitan region of
Belém may have lost 47 species (14% of the regional species pool) probably due to
habitat loss, degradation and hunting/traffic. Many of these species that have
disappeared from around Belém are also rare or extinct in neighboring Paragominas.
21
The conservation of large areas of forest remains the most important conservation
goal, and these should be protected from fires and frequent logging events. Given the
low bird diversity in agricultural areas, intensifying land-use (whilst maintaining or
expanding landscape connectivity) in such areas may better balance development and
conservation goals.
22
Capítulo 1
Introdução Geral
1.
Amazônia
As
florestas
tropicais
ocorrem
em
mais
de
80
países,
ocupando
aproximadamente 1.150 milhões de ha, em sua maioria na bacia amazônica, bacia do
Congo e sudoeste de Ásia (Mayaux et al. 2005), sendo consideradas um dos os
biomas mais complexos em termos de estrutura, riqueza e diversidade de espécies.
As florestas tropicais possuem um papel importante na prestação de serviços
ecossistêmicos (Myers 1996, Grimes et al. 2004) como, por exemplo, regulação do
clima (e.g. Malhi et al. 2008), fotossíntese e regulação dos níveis do gás carbônico
(e.g. Malhi et al. 2009), fornecimento de bens como alimento, madeira e água (e.g.
Shone e Caviglia-Harris 2006), além de ser um grande reservatório de biodiversidade
(Laurance 2007).
Entretanto, com estimativas de aumento da população mundial para 10,9
bilhões até 2100 (United Nations 2013), tem aumentado também a demanda para
produção de alimentos, biocombustíveis e madeira (Tilman et al. 2011, Laurence et al.
2014) e, deste modo, aumentando também a pressão para expansão agrícola nas
áreas tropicais, com estimativas de que 109 milhões de ha de floresta serão
desmatados para agricultura até 2050 (Tilman et al. 2001), principalmente na América
do Sul e África subsaariana, que possuem grandes áreas de terras com potencial
agrícola ainda inexplorado (Tilman et al. 2011).
Com aproximadamente 40% dos remanescentes de florestas tropicais do
planeta (Hubbell et al. 2008), a bacia amazônica estende-se do oceano Atlântico até
as encostas orientais da Cordilheira dos Andes, fazendo parte de nove dos 12 países
da América do Sul (Ab’Saber 1977). Quase 70% do bioma pertencem ao Brasil,
ocupando 49,2% do território brasileiro e abrigando 13,38% da população (IBGE
2013).
A floresta amazônica também é conhecida pela sua biodiversidade tanto
terrestre quanto aquática. Apesar da exata quantidade de espécies ser ainda
desconhecida, há aproximadamente 50.000 espécies de plantas vasculares (Hubbell
et al. 2008) e pelo menos 1300 espécies de aves (Whitney e Conh-Haft 2013).
23
É considerada uma floresta heterogênea tanto em termos de estrutura quanto
em composição de espécies (Tuomisto et al. 1995), podendo o bioma ser
biogeograficamente dividido em oito centros de endemismo; três deles de ocorrência
exclusiva no Brasil, Tapajós, Xingu e Belém, estando os dois últimos com a maior
porcentagem de sua área desmatada (Silva et al. 2005).
A Amazônia tem sido ameaçada pelas constantes pressões de desmatamento
(Fearnside 2008, Vieira et al. 2008), dando lugar às pastagens, agricultura (Colson et
al. 2010), silvicultura (Barlow et al. 2007b), biodiesel (Butler e Laurance 2009),
extração madeireira (Asner et al. 2006), construção de barragens (Fearnside 2001) e
também pelas mudanças climáticas potencias, como as intensas secas ocorridas no
sudoeste da Amazônia em 2005 (Saleska et al 2007, Nobre et al. 2007) e em 2010
(Lewis et al. 2011).
A
B
Figura 1.1 Área com exploração madeireira em Paragominas (A) e floresta primária intacta na
Floresta Nacional de Tapajós , Belterra (B) ( N. Moura).
No Brasil, a taxa anual de desmatamento diminuiu por quatro anos
consecutivos (2009 a 2012, sendo 2012 a menor taxa já registrada), Fig. 1.2. Porém,
entre agosto de 2012 e julho de 2013, foram desmatados 5.843 km² de floresta, 28% a
mais do que havia sido registrado no período anterior, sendo os estados do Mato
Grosso e Rondônia os que mais contribuíram para esse aumento (INPE 2013). Esses
estados compõem o Arco do Desmatamento, que se estende do Maranhão até
Rondônia, área de forte expansão agrícola.
24
.
Figura 1.2 Taxa anual de desmatamento na Amazônia legal entre 1988 e 2013 (INPE 2013).
2.
Mudanças de uso da terra
Mudança de uso da terra é a conversão de paisagens naturais para uso
humano ou a modificação das práticas de manejo em terras dominadas pelo homem
(Foley et al. 2005) que podem incluir agricultura de corte e queima, corte seletivo,
conversão de floresta em pastagens e áreas de produção agrícola, plantio comercial
de árvores (eucalipto, paricá etc) e urbanização (Gardner et al. 2009, Peres et al.
2010), havendo uma expansão dessa paisagem modificada nas últimas décadas
(Foley et al. 2005, Laurance et al. 2014).
Por muitos anos, a criação de pastagens foi o principal agente de
desmatamento. Até 2010 66% das áreas desflorestadas na Amazônia Legal foram
para criação de pastos (TerraClass 2010). Fatores como baixa fertilidade, alta
pluviosidade e degradação dos solos em algumas regiões amazônicas (Arima et al.
2005) levaram ao abandono das pastagens, promovendo o crescimento de floresta
secundária em diversos estágios de desenvolvimento (Vieira et al. 2008) que
atualmente têm sido apontadas como um importante potencial para a preservação da
biodiversidade, especialmente as florestas secundárias antigas (Chazdon et al. 2009).
25
Figura 1.3 Áreas de pastagem em Paragominas ( N. Moura).
De acordo com Putz e Redford (2010), a degradação florestal consiste em
florestas primárias que já sofreram perda de estrutura e composição pelo corte
seletivo, queimada, invasão de espécies exóticas, excesso de caça, em geral ações
provocadas pelo homem.
Na Amazônia,
degradação
a retirada de madeira (Fig. 1.4) é um dos causadores de
mais importantes. Apesar da exploração
madeireira ainda
ser
subestimada, pelo menos 27 milhões de metros cúbico de madeira são removidos
anualmente, degradando áreas entre 12.075 e 19.283 Km², muitas vezes
ultrapassando o total anual de área desmatada (Asner et al. 2005).
Os efeitos gerados pelo corte seletivo são diversos, dentre eles a alteração na
estrutura da floresta pelos danos causados no dossel, subosque e árvores
remanescentes (Uhl e Vieira 1989, Nepstad et al. 1999, Asner et al. 2004), aumento da
susceptibilidade da floresta ao fogo (Uhl e Kauffman 1990, Nepstad et al. 1999),
liberação de carbono na atmosfera (Asner et al. 2005) e danos à biodiversidade (Dunn
2004a, Barlow et al. 2006).
26
A
B
Figura 1.4 Madeira explorada na Floresta Nacional do Tapajós (Santarém) (A) e transporte
madeira em Paragominas (B). N. Moura.
De maneira geral, a floresta amazônica é resistente à ação do fogo (Holdsworth
e Uhl 1997). Todavia, a exploração madeireira aumenta a quantidade de resíduos
lenhosos que podem funcionar como combustíveis e altera a abertura do dossel,
ressecando o solo e sub-bosque, tornando a floresta mais susceptível ao fogo
(Holdsworth e Uhl 1997). E ainda, as florestas exploradas comumente estão próximas
às áreas de pastagens e agricultura nos quais o fogo é utilizado para a limpeza e
manutenção.
As queimadas, além de aumentarem a liberação de gás carbônico para a
atmosfera (Haugaasen et al. 2003), têm consequências graves para a biodiversidade.
Barlow et al. (2002) relataram que o fogo, além de afetar estrutura da floresta, também
afetou negativamente as aves de sub-bosque, contribuindo com significativa perda de
espécies quando comparado às áreas não queimadas.
A
B
Figura 1.5 Área de floresta primária sendo queimada (A) (J. Barlow); resíduos de madeira para
produção de carvão em Paragominas (B) ( N. Moura).
27
3.
As aves, a paisagem amazônica e as mudanças de uso da terra
As aves têm sido amplamente utilizadas como bioindicadores devido aos
seguintes fatores: 1) ecologia relativamente bem conhecida; 2) grande número de
espécies apresentam sensibilidade à perda de habitat e fragmentação; 3) são
relativamente fáceis de detectar; e 4) apresentam alta relação custo/benefício como
indicadores ecológicos (Gardner et al. 2008).
Vários fatores ameaçam a permanência e sobrevivência da avifauna nas
florestas tropicais, dentre eles a fragmentação, perda de habitat e degradação
florestal, os quais afetam a distribuição (Van Houtan et al. 2007) e riqueza (Lees e
Peres 2006) das comunidades, desencadeando a extinção local de algumas espécies
(Stratford e Stouffer 1999, Lees e Peres 2008b). De forma indireta, as aves também
podem ser afetadas por meio das mudanças na abundância e/ou composição de
espécies de outros grupos biológicos (Feeley e Terborgh 2008), como o efeito cascata
gerado pela remoção de grandes predadores dos fragmentos que resulta em aumento
de mesopredadores, elevando a pressão de predação sobre as espécies de aves
(Crooks e Soulé 1999).
Com o aumento das áreas modificadas pelas ações humanas na Amazônia,
sejam elas para criação de pastagens ou exploração madeireira, diversos estudos têm
sido feitos com o intuito de compreender as respostas da avifauna a essas mudanças
de uso da terra. Para definir com precisão a importância das áreas modificadas para a
conservação da biodiversidade regional, é necessário saber qual a proporção de
espécies que habitam as áreas modificadas em relação àquelas que coexistem na
floresta original (Gardner et al. 2009).
O Projeto Dinâmica Biológica de Fragmentos Florestais – PDBFF foi um dos
pioneiros a buscar este tipo de informação. Iniciado em 1979 e ainda em andamento, o
PDBFF investiga as consequências ecológicas do desmatamento e da fragmentação
florestal, monitorando fragmentos que variam de 1 a 100 ha na Amazônia Central
antes e após a fragmentação, estudando diversos tipos de perturbação em grupos
biológicos como a avifauna, principalmente sobre as espécies de sub-bosque, como
efeito de borda (e.g. Laurance 2004), tamanho do fragmento (e.g. Stouffer et al. 2008),
efeito pela matriz circundante (e.g. Antongiovanni e Metzger 2005), extinção (Stratford
e Stouffer 1999), entre outros.
Diversos estudos sobre como a fragmentação afeta a avifauna também foram
realizados no norte do Mato Grosso (região de Alta Floresta), que possui uma
28
paisagem muito fragmentada, mostrando efeitos negativos sobre as comunidades de
aves e mamíferos, extinção local em pequenos fragmentos (Lees e Peres 2006, 2008),
como a incapacidade de algumas espécies se movimentarem em uma paisagem
fragmentada (Lees e Peres 2009) e a baixa riqueza de espécies na matriz não-florestal
(Mahood et al. 2012).
No nordeste da Amazônia, na fronteira entre os estados do Pará e Amapá
(Projeto Jari), foi estudado o impacto da plantação eucaliptos e das florestas
secundárias (e.g. Barlow et al. 2007b), bem como o efeito de queimadas recorrentes
(e.g. Barlow et al. 2006) que também afetaram negativamente a avifauna de subbosque.
Porém, apesar dos efeitos das modificações de uso da terra na Amazônia
serem relativamente bem conhecidos, grandes partes das pesquisas são ainda
limitadas pela escala espacial ou concentrada em regiões bem estudadas e de acesso
relativamente fácil. Além disso, há tendência em se priorizar os efeitos da
fragmentação, exploração de madeira ou impactos do fogo em pequenas áreas
(Gardner et al. 2009, Peres et al. 2010).
4.
Projeto Rede Amazônia Sustentável (RAS)
O RAS é uma iniciativa multidisciplinar de pesquisa que envolve mais de 30
organizações nacionais e internacionais (Fig. 1.6) que trabalham para avaliar as
dimensões ecológicas e sociais da sustentabilidade dos usos da terra na Amazônia
oriental (Gardner et al. 2013).
O RAS possui um inovador desenho experimental, utilizando múltiplas escalas
espaciais para a coleta de dados relacionados à biodiversidade e socioeconômica,
envolvendo três objetivos principais: 1) quantificar e compreender as consequências
ecológicas do desmatamento, degradação, exploração florestal e conversão para
agricultura em múltiplas escalas espaciais; 2) avaliar os fatores que determinam os
padrões dos tipos de uso da terra, escolha de gestão, produtividade agrícola, lucros e
padrões de bem-estar nos agricultores; 3) utilizar os resultados multidisciplinares para
avaliar a relação entre conservação e desenvolvimento e, assim, identificar os
potenciais "trade-offs" e sinergias.
29
.
Figura 1.6 Parceria desenvolvida sob a Rede Amazonia Sustentável.
Os estudos foram realizados em dois municípios paraenses: Paragominas e
Santarém/Belterra, regiões que possuem distintas características biofísicas e
históricas de uso da terra e ocupação humana.
Os dois municípios estão em diferentes regiões biogeográficas; Paragominas
no centro de endemismo Belém e Santarém/Belterra no centro de endemismo Tapajós
(Silva et al. 2005). Santarém/Belterra foram fundadas em 1661, enquanto
Paragominas apenas em 1959, com a criação da rodovia Belém-Brasília. Ambos
municípios também possuem iniciativas de sustentabilidade. Em Paragominas foi
implantada a iniciativa Município Verde para a retirada do município do topo da lista
dos que mais desmatam a Amazônia e, em Santarém, foi implantada a moratória para
a expansão da soja. Em ambos, as iniciativas foram fortemente apoiadas pelo governo
local, instituições não governamentais e pelos sindicatos dos produtores rurais,
tornando possível a execução do RAS.
5.
Objetivos e estrutura da tese
Os três principais objetivos desta tese foram:
1. Avaliar a perda de espécies de aves ao longo de um gradiente de impacto
antrópico nos municípios de Paragominas e Santarém/Belterra, regiões que
apresentam similar cobertura florestal, porém com diferentes históricos de uso;
30
2. Investigar os padrões de ocupação de diferentes espécies nas paisagens de
estudo e se esses padrões são influenciados por fatores locais, paisagísticos e
históricos nos municípios de Paragominas e Santarém/Belterra;
3. Buscar evidência para extinção histórica da avifauna de terra firme na Região
Metropolitana de Belém, fronteira de desmatamento mais antiga na Amazônia,
e compará-las com os dados coletados em Paragominas, sujeita ao
desmatamento mais recente.
Essa tese foi escrita em 5 capítulos. No capítulo 1 foi feita uma introdução geral
da tese. Os capítulos 2, 3 e 4 foram escritos na forma de artigos científicos em inglês,
de forma que alguns elementos, como, os materiais e métodos podem, naturalmente,
conter informações já citadas, o que facilitará a compreensão de cada capítulo
individualmente, sem a necessidade de retornar a uma seção específica para
materiais e métodos para avaliação de alguma informação relevante.
Em cada manuscrito, os resultados foram interpretados e discutidos de maneira
que maximizasse os interesses científicos gerais. A ênfase teórica pode, pois, ser
diferenciada entre os capítulos. No capítulo 5, é feita uma conclusão geral com os
resultados obtidos.
Os capítulos 2 e 4 já foram publicados (Moura et al. 2013, Moura et al. 2014). O
capítulo 3 está em preparação para ser submetido à Biotropica.
Os capítulos foram apresentados de acordo com o conteúdo e não pela ordem
cronológica publicada. No capítulo 2, foi explorado a resposta da comunidade de aves
às mudanças de uso da terra em um gradiente de perturbação (de floresta primária
não perturbada, florestas degradadas por corte seletivo e/ou queima, florestas
secundárias, pastagens, silvicultura, agricultura familiar e áreas de agricultura
mecanizada). Já no capítulo 3, foi investigada a resposta de um grupo de espécies
representativo de toda comunidade ao gradiente de perturbação. No capítulo 4, foram
utilizados os dados coletados desde 1812 relativos à avifauna na região metropolitana
de Belém, após a vinda dos primeiros naturalistas, como Alfred Russel Wallace,
embasando evidências para extinção local com a utilização de dados coletados em
Paragominas como baseline.
No anexo 1, foram listadas as espécies registradas durante o levantamento nos
municípios de Paragominas e Santarém/Belterra e, no anexo 2, estão listados outros
resultados publicados com base nos dados coletados em Paragominas e
Santarém/Belterra.
31
Capítulo 2
Avian biodiversity in multiple-use landscapes of the Brazilian
Amazon
Publicado como: Moura, N. G., A. C. Lees, C. B. Andretti, B. J. W. Davis, R. R. C.
Solar, A. Aleixo, J. Barlow, J. Ferreira, and T. A. Gardner. 2013. Avian biodiversity in
multiple-use landscapes of the Brazilian Amazon. Biological Conservation, 167, 339–
348.
Abstract
Habitat loss and degradation is the most pervasive threat to tropical biodiversity
worldwide. Amazonia sits at the frontline of efforts to both improve the productivity of
tropical agriculture and prevent the loss of biodiversity. To date our understanding of
the biodiversity impacts of agricultural expansion in Amazonia is restricted to findings
from small scale studies that typically assess the importance of a limited number of
land-use types. Here we investigate local and landscape-scale responses of
Amazonian avian assemblages to land-cover changes across a gradient of land-use
intensity ranging from undisturbed primary forest to mechanised agriculture in 36
drainage catchments distributed across two large regions of the eastern Brazilian
Amazon. We found that species richness of forest-associated birds declined
progressively along this gradient, accompanied by marked shifts in assemblage
composition. We found significant changes in species composition, but not richness,
between primary forests that had been subject to different levels of disturbance from
logging and fire. Secondary forests retained levels of species richness intermediate
between primary forests and production areas, but lacked many forest-dependent
species. Production areas (arable crops, cattle pastures and plantation forests) all
retained far fewer species than any forest habitat, and were largely dominated by taxa
commonly associated with open areas. Diversity partitioning revealed that species
composition varied the most among undisturbed forest transects, and steadily
decreased with increasing forest degradation and land-use intensity. Our results
emphasise the importance of protecting both remaining areas of primary forest in
private lands, as well as protecting the same forests from further disturbance events.
Keywords: tropical agriculture; forest disturbance; landscape-scale; biodiversity;
Brazilian Forest Code; private lands
32
1.
Introduction
In the tropics, land-use change has been the principal driver of biodiversity loss
(Sala et al. 2000, Hooper et al. 2012) and ecosystem function impairment (Cardinale et
al. 2012). Understanding the impacts of land-use change on patterns of species
occurrence and abundance is of fundamental importance for developing effective
conservation strategies (Gardner et al. 2009, Waltert et al. 2011, Balmford et al. 2012).
In the Brazilian Amazon, despite significant reductions in deforestation, 4,656
km² of forest were still lost in 2012 (INPE 2013). The loss and degradation (e.g. from
timber extraction, fire and over-exploitation of non-timber forest products) of primary
forest remains the most important threat facing the biodiversity of the region (Peres et
al. 2010), and is being driven by agricultural expansion (Davidson et al. 2012) and
catalysed by major infrastructure improvements including road building and paving
projects (Fearnside 2007, Fearnside et al. 2012).
Although the impacts of forest loss, fragmentation and degradation on
Amazonian biota are now increasingly understood, the majority of existing studies are
limited in their spatial scale, concentrated in well-studied areas of the region, and have
tended to focus on either fragmentation, forestry or fire impacts over a narrow range of
land-uses (see reviews in Gardner et al. 2009, Peres et al. 2010, Laurance et al. 2011).
In addition the vast majority of studies assessing the impacts of land-use change on
biodiversity across the tropics have been limited to site-based assessments, despite
increasing evidence indicating that landscape scale characteristics (such as the loss of
total forest cover) can have a major influence on local species distribution patterns (e.g.
Bennett et al. 2006, Pardini et al. 2010). As a consequence, insights into the impacts of
multiple land-uses on Amazonian biota have up until now remained largely within the
domain of meta-analyses (e.g. Barlow et al. 2006), which do not account for important
differences in landscape context.
Here we evaluate avian responses to changes in forest disturbance and landuse across nearly 400 study sites distributed across 36 catchments in two different
regions of the Brazilian Amazon, encompassing the full gradient of dominant
Amazonian land-use types. Birds are excellent indicators of the ecological
consequences of disturbance because their ecology is relatively well known, they are
relatively easy to identify and cheap to survey (provided expert field observers can be
sourced), and they exhibit a broad range of interspecific responses to human impacts
at spatial and temporal scales that can be readily interpreted by snap-shot field
assessments (Howard et al. 1998, Lees and Peres 2006, Gardner et al. 2008).
33
We have three main aims. First we assess the loss of bird species (total number
of species and number of primary forest-associated species separately) along a
gradient of human impact from undisturbed primary forest through primary forest that
has been varyingly disturbed by logging and fire, secondary re-growth, plantation
forests, pastures and mechanised agriculture. This assessment contributes important
information towards debates regarding the relative biodiversity value (compared to a
primary forest baseline) of production areas (Peres et al. 2010, Mahood et al. 2012),
secondary forests (Dent and Wright 2009), and forests degraded by fire and logging
compared to relatively undisturbed primary forest (Barlow et al. 2006). Second, we
compare patterns of avian species richness across catchments (separate landscapes)
distributed along a gradient of deforestation in each study region, providing the first
assessment of how changes in total forest cover can influence landscape-scale
patterns of diversity in multiple-use tropical forest regions. Third, we investigate how
patterns of avian diversity are partitioned across multiple spatial scales and within each
major land-use type, from point counts to transects to landscapes, and ask whether
differences in total forest cover explain these patterns through relative contributions of
the α, and β diversity components (Tylianakis et al. 2006).
2.
Methods
2.1 Study regions and experimental design
This study was conducted in two regions of eastern and central Pará state (Fig.
2.1), Brazilian Amazonia, in the municipalities of Paragominas (PGM) between 28 July
and 20 November 2010 and 18 to 29 May 2011 (NGM and ACL) and in
Santarém/Belterra (STM) between 16 October 2010 and 8 February 2011 (NGM, ACL,
CBA and BJWD). Both regions have been heavily impacted by deforestation but have
significant differences in their historical trajectory of colonization and both past and
present land-uses (Gardner et al. 2013). The municipality of Paragominas (1.9 Mha) is
located in north-east Pará state, 300 km south-east of Belém. The average annual
temperature is 27ºC, with an average humidity of 81% and annual rainfall averaging
1766 mm (Watrin and Rocha 1992). The municipalities of Santarém/Belterra (ca 1
Mha) lie south-east of the confluence of the Amazonas and Tapajós rivers, and have
an average annual temperature of 25ºC, with an average humidity of 86%, with annual
rainfall averaging 1920 mm (Parrotta et al. 1995, Nepstad et al. 2002).
34
Figure 2.1 Map of Paragominas (a) and Santarém/Belterra (b) showing the location of the 18
catchments surveyed in each municipality. Two example catchments are presented for each
municipality in (c) showing the location of transects and transects design and positioning of
point count stations (d).
Both regions were divided into approximately evenly-sized catchments, which
were delineated using a digital elevation model and SWAT (Soil and Water
Assessment Tool) for ARCGIS 9.3. Eighteen catchments (of c.5000 ha) were selected
for each region capturing the full gradient of deforestation in 2009 (10-100% forest
cover in Santarém; 6-100% forest cover in Paragominas), whilst also ensuring
adequate representation of current land-use practices, the spatial distribution of the
rural population, and major soil types. Between eight and twelve 300 m transects were
allocated to each catchment, distributed using a stratified-random sampling design
across each catchment to increase the likelihood that they would capture important
internal heterogeneities in forest and/or production systems (depending on catchment
size with an even density of 1 transect per 400 ha). To reduce the dependency
between transects within each catchment transects were separated by a minimum
distance of 1.5 km. In total we sampled 196 transects in PGM and 165 in STM. All
landowners in each catchment were visited prior to any fieldwork to introduce the
project and secure permissions for surveys in private properties. Land-use
classification was made using 2010 Landsat images and a decision tree classification
algorithm (Gardner et al. 2013).
35
In each transect three point count (PC) stations were located at 0, 150 and 300
m. A total of 1083 PCs were conducted across both regions. For further details on siteselection see Lees et al. (2012, 2013a) and Gardner et al. (2013). We carried out two
repetitions of three 15 minute, 75 m fixed width PCs per transect, recording all species
seen or heard. Repetitions ensured that temporal variation in avian vocal activity was
minimized, and PCs were recorded using solid state recorders – for more details on
survey methodology, full species lists and links to digital vouchers see Lees et al.
(2012, 2013a) and Anexo 1.
We classified land-use types into six broad groups (see Table 2.1), namely:
‘primary forest’: the region’s original climax physiognomy that has never been clearfelled for agriculture (although may have been extensively degraded by disturbance
and human exploitation); secondary forests: forests that developed after complete
clearance (Putz and Redford 2010); tree plantations - in this case commercial
plantations, typically of Eucalyptus sp., teak (Tectona grandis) or paricá (Schizolobium
parahyba var. amazonicum); cattle pasture; mechanised agriculture: typically soybean
fields or rice; and small-holder agriculture: farms typically smaller than 100 ha and
consisting of small-scale manioc plantations and/or fruit trees. Primary forest transects
were further sub-classified by disturbance type. These classifications were based on
ground-truthed observations of past disturbance events (Gardner et al. 2013), resulting
in four types of primary forest: ‘undisturbed’ for which no evidence of recent humaninduced degradation was apparent, ‘selectively logged’ for forest which have
undergone detectable logging, ‘burnt’ for forests in which fire scars were found on trees
and charcoal deposits detected on the ground and logged&burnt for those forests
exposed to both of these stressors. We also subdivided secondary forests into three
age classes: old (> 20 years old), intermediate (5-20 years old) and young (< 5 years
old). Ageing of secondary forests was done through visual inspection of a 20 year timeseries of Landsat images for each transect, calibrated by interviews with local farmers.
36
Table 2.1 Total number of transects allocated to each land-use type in both study regions.
Land-use type
Primary forest
Paragominas
Santarém
Undisturbed
9
17
Logged only
44
25
Burnt only
0
9
Logged&burnt
44
23
Old
5
21
Intermediate
12
18
Young
8
4
Reforestation
9
0
Pasture
53
25
Mechanised agriculture
12
16
Small-holder agriculture
0
7
196
165
Secondary forest
Total
2.2 Data analyses
We analysed the responses of total species richness as well as richness and
turnover for the subset of ‘primary forest-associated birds’ (hereafter termed ‘forest
birds’). These forest birds represent the core avifauna of undisturbed terra firme forests
but not necessarily birds restricted to those habitats, as some core primary forest
species also occur (or indeed proliferate) in human-modified forest and non-forest
habitats (e.g. Palm Tanager Tangara palmarum and Bananaquit Coereba flaveola).
These categorizations were based on previously published classification of birds from
the region (e.g. Parker et al. 1996, Henriques et al. 2003, Lees et al. 2013b).
To compare avian responses between different land-use systems and
catchments we used sample-based rarefaction curves, with 95% confidence intervals
(Colwell et al. 2004). The rarefaction curves between bird richness and total forest
cover were constructed in EstimateS 7.5 (Colwell 2004). Comparisons between
species richness in each land-use type were also made using a non-parametric
Kruskall-Wallis test with 95% confidence intervals followed by the Mann-Whitney U test
to check for significant pairwise differences. These were performed in Statistica V.7.1
(Statsoft 2005).
To explore relationships between forest cover and forest bird species richness
we performed linear regressions using percentage of total forest cover (primary and old
37
secondary forests combined) and the percentage of primary forest cover only in a 10
km buffer around the centroid of each catchment (to standardise comparisons of
landscape context) as predictor variables for avian species richness.
To assess the variation in species composition between land-use systems and
different primary forest disturbance classes we produced non-metric multi-dimensional
scaling ordinations (NMDS; Clarke and Green, 1988) using the Bray-Curtis similarity
matrix for species presence-absence data. To assess the statistical significance of
observed differences in assemblage composition between different land-use types and
forest degradation classes we conducted a one-way PERMANOVA which uses
pseudo-F values to compare among-group to within-group similarity and assesses
significance by permutation. All multivariate assemblage analyses were carried out in
Primer v.6 (PRIMER-E Ltd, Plymouth, UK, Clarke and Gorley 2006).
To describe the relative contribution of diversity components α (alpha – total
species per point count), βamong points (beta diversity among points within a transect) and
βamong transects (beta diversity among transects in a catchment) in the total diversity per
catchment (γ; gamma diversity), we used additive partitioning of diversity (Lande 1996),
where γ = α + β. This approach allows the additive partitioning of the total diversity in a
region to be broken down into scale-specific diversity components, which can be
directly compared (Veech et al. 2002, Gering et al. 2003). In addition, this approach
can be important to help understand what factors are controlling the spatial distribution
of biodiversity (Veech et al. 2002). In the context of our study, the overall forest bird
diversity can be described by the following formula: γcatchments = αpoints
count
+ βPoints +
βTransects. We omitted plantations and small-holder agriculture from these analyses as
our sample size was too small to make reliable inferences. The additive partitioning
was performed using the adipart function of the vegan package (Oksanen et al. 2011)
in R software v.2.13.1 (R Development Core Team 2011).
3.
Results
We recorded 24,449 detections of 467 bird species, of which 336 were forest
birds, with 359 species (252 forest birds) in PGM and 377 (286 forest birds) in STM (full
species lists can be found in Lees et al., 2012, 2013a). The species accumulation
curves indicated that surveys in most land-use types were near asymptotic (Fig. 2.2
and 2.3). The cumulative richness across catchments (Fig. 2.4) illustrates a steady
accumulation of species as new catchments were inventoried. Ten catchments,
distributed throughout each region, were necessary to capture 90% of total species and
38
91% of forest bird species in PGM and 89% of total species and 90% of forest birds in
STM (Fig.2.4).
Figure 2.2 Individual based species rarefaction curves per transect between land-use systems
considering the entire avian assemblage (A and B) and forest-associated species (C and D) in
PGM. Legend: dark green- primary forest; light green - secondary forest; blue - pasture; yellow mechanised agriculture; red - plantation.
39
Figure 2.3 Individual-based species rarefaction curves per transect between land-use systems
considering the entire avian assemblage (A and B) and forest birds (C and D) in STM. Legend:
dark green - primary forest; light green - secondary forest; blue - pasture; yellow - mechanised
agriculture; red - small-holder agriculture.
Figure 2.4 Species rarefaction curves per catchment in PGM and STM, considering the entire
avian assemblage (filled circles) and forest birds (empty circles).
3.1 Species richness responses
In PGM, avian richness (all species) in primary (mean = 50, sd = 12) and
secondary (mean = 40, sd = 10) forests was found to be significantly higher than all
other land-uses (Fig. 2.5a, H = 116, df = 6, N = 196; p<0.001) and secondary forest
was statistically less species rich than all primary forest disturbance classes.
40
Agricultural (mean = 16, sd = 8) and plantation forest (mean = 19, sd = 8) areas had
similar avian species richness. When the secondary forests were split by age category
all three were significantly lower in richness than all primary forest disturbance classes
(H = 116, df = 8, N = 196; p<0.001, Fig. 2.6). Considering only richness of forest birds,
there was no significant difference between undisturbed (mean = 51, sd = 10) and
logged (mean = 50, sd = 13) forest Fig. 2.5b (H = 155, df = 6, N = 195; p<0.001),
whereas both were distinct from logged&burnt (mean = 41, sd = 13) and secondary
forests (mean = 12, sd = 24); (Fig 2.5b). After being subdivided by age category (H =
156, df = 8, N = 195; p<0.01) the different secondary forest ages classes remained
distinct from all primary forest classes.
41
Figure 2.5 Box plots comparing avian species richness between land-use types and
degradation forest classes in PGM and STM, using the entire avian assemblage (a and c) and
just forest birds (b and d). Non-significant pairwise differences between land-use types are
indicated by the presence of the same letter (according to Mann-Whitney U).
42
Figure 2.6 Box plots comparing avian species richness between land-use types, forest
degradation classes and secondary forest age classes in PGM and STM, using the entire avian
assemblage (A and C) and just forest birds (B and D). Non-significant pairwise differences
between land-use types are indicated by the presence of the same letter (according to MannWhitney U).
In STM considering all birds, the undisturbed forest (mean = 51, sd = 8) was
statistically indistinguishable from all the primary forest disturbance classes (burnt
[mean = 51, sd = 11], logged [mean = 47, sd = 10] and logged&burnt [mean = 46, sd =
8]); Fig. 2.5c (H = 93, df = 7, N = 165; p<0.001). Secondary forests (mean = 38, sd =
12) were distinct from all other land-use types, and mechanised agriculture (mean =
10, sd = 7) was indistinguishable from pasture (mean = 25, sd = 10) and small-holder
agriculture (mean = 31, sd = 10). We were unable to demonstrate significant
differences between individual secondary forest age classes and most forest and nonforest land-uses, likely due to the small sample sizes (Fig. 2.6; H = 96, df = 9, N = 165;
p<0.001).
Considering only forest birds in STM, Fig. 2.5d (H = 154, df = 6, N = 195;
p<0.001), undisturbed forest (mean = 51, sd = 8) was indistinguishable from burnt
forest (mean = 49, sd = 13), but distinct from both logged (mean = 46, sd = 10) and
logged&burnt forest (mean = 45, sd = 10). Secondary forests (mean =30, sd = 14) and
43
small-holder agriculture (mean = 9, sd = 4) had intermediate species richness and were
distinct from all other land-uses, but pastures (mean = 8, sd = 4) and mechanised
agriculture (mean = 3, sd = 3) had similarly low species richness. Splitting the
secondary forest into different ages categories (H = 156, df = 8 N = 195; p<0.001, Fig.
2.6) the species richness of old secondary forest (mean = 36, sd = 13) was statistically
distinct from all other land-uses (including all primary forest classes), whereas young
(mean = 126, sd = 12) and intermediate (mean = 25, sd = 11) secondary forests hosted
similar numbers of forest species to pasture and areas of small-holder agriculture.
3.2 Differences in species composition
Species composition of forest birds changed consistently along a gradient of
human impacts between primary forests, secondary forests, plantations, pastures and
mechanised agriculture (Fig. 2.7, Table 2.2, PERMANOVA, Pseudo-F = 26.152, p<
0.001 and Pseudo-F 16.372, p<0.001 for PGM and STM respectively). All species
assemblages were significantly different from each other with the exception of pastures
and plantations in PGM (p = 0.573; Table 2.2) and small-holder agriculture and
pastures in STM (p = 0.271; Table 2.2). Considering each secondary forest age class
(Fig. 2.8), the forest bird assemblage composition was different from all primary forests
disturbance classes in both regions (PERMANOVA, Pseudo-F = 26.152, p<0.001 and
Pseudo-F = 16.372, p<0.001 for PGM and STM respectively, Table 2.4). The species
composition was not significantly different between old and intermediate secondary
forest (p =0.42) in PGM although it was different in STM (p<0.05).
44
Figure 2.7 NMDS plots of community structure of forest birds in all land-use types (a and c) and
between different primary forest disturbance classes (b and d) in PGM and STM. Considering all
land-use types (a and c) black circles = primary forest; empty circles = secondary forest; grey
squares = pasture; empty squares = mechanised agriculture and black triangles = small-holder.
For different primary forest disturbance classes (b and d) black triangles = undisturbed; grey
hexagons = secondary forest; crossed squares = burnt forest; empty hexagons = logged&burnt
forest; grey hexagons = logged forest; empty circles = secondary forest.
45
Table 2.2 PERMANOVA Pseudo-F statistic values of global test (p-values in parenthesis) and t
values of pair-wise comparison (p-values in parenthesis) for forest birds composition in different
land-use types and forest disturbance classes in two regions, PGM and STM, of the Brazilian
Amazon. NA indicates that the comparison is not valid as the land use in question is unsampled
in the respective municipality.
Land uses
PGM
STM
Global test land use
28.122 (<0.001)
17.361 (<0.001)
Mechanised agriculture, Pasture
Mechanised agriculture, Primary forest
Mechanised agriculture, Secondary Forest
Pasture, Primary forest
Pasture, Secondary forest
Primary forest, Secondary forest
Plantation, Pasture
Plantation, Primary forest
Plantation, Mechanised agriculture
Plantation, Secondary forest
Small-holders, Secondary forest
Small-holders, Mechanised agriculture
Small-holders, Pasture
Small-holders, Primary forest
1.960 (<0.05)
5.448 (<0.001)
3.783 (<0.001)
8.984 (<0.001)
4.458 (<0.001)
3.792 (<0.001)
0.891 (0.57)
4.698 (<0.001)
1.693 (<0.001)
3.04 (<0.001)
NA
NA
NA
NA
1.539 (<0.001)
4.671 (<0.001))
3.336 (<0.001)
6.448 (<0.001)
3.962 (< 0.001)
4.339 (<0.001)
NA
NA
NA
NA
2.604(<0.001)
1.689 (<0.05)
1.142 (0.238)
4.171 (<0.001)
9.029 (<0.001)
2..322 (<0.001)
2.929 (<0.001)
2.952 (<0.001)
3.904 (<0.001)
2.159 (<0.001)
3.518 (<0.001)
NA
NA
NA
NA
6.1774 (<0.001)
1.617 (<0.001)
2.747 (<0.001)
1.741 (0.001)
3.672 (<0.001)
1.169 (<0.001)
3.48 (<0.001)
0.947 (0.586)
1.416(<0.05)
1.365 (<0.001)
1.855 (<0.001)
Forest disturbance classes
Global test
Logged&burnt, Logged
Logged&burnt, Secondary forest
Logged&burnt, Undisturbed
Logged, Secondary forest
Logged, Undisturbed
Secondary forest, Undisturbed
Burnt, Logged&burnt
Burnt, Logged
Burnt, Undisturbed
Burnt, Secondary forest
Forest
disturbance classes were also distinct
in their species composition
(PERMANOVA, Pseudo-F = 9.062, p<0.001 and Pseudo-F = 6.18, p<0.001 for PGM and STM
respectively; Table 2.2, Fig 4b and d). In PGM the avian assemblages of all forest disturbance
classes were significantly different from each other (Table 2.2), whilst in STM burnt and
logged&burnt forests appear to be similar (p = 0.623; Table 2.2). Considering all species (rather
than just forest species) the NMDS plots (Fig. 2.9) exhibited the same broad gradient pattern,
but assemblages were less tightly aggregated (Table 2.3).
46
Figure 2.8 NMDS plots of forest species in each forest type in PGM and STM. Legend: empty
circles - primary forest; black triangle - intermediate secondary forest; black square-old
secondary forest; black cross - young secondary forest;
empty square - mechanised
agriculture; grey square - pasture; black circle - plantation and black triangle - small-holder.
Figure 2.9 NMDS plots of community structure of entire avian assemblage in all land-use types
(a and c) and between different primary forest degradation classes (b and d) in PGM and STM.
Considering all land-use types (a and c) black circles = primary forest; empty circles =
secondary forest; grey squares = pasture; empty squares = mechanised agriculture and black
47
triangles = small-holder. For different primary forest disturbance classes (b and d) black
triangles = undisturbed; grey hexagons = secondary forest; crossed squares = burnt forest;
empty hexagons = logged&burnt forest; grey hexagons = logged forest; empty circles =
secondary forest.
Table 2.3 PERMANOVA Pseudo-F values of global test (p-values in parenthesis) and t-values
of pair-wise comparison (p-values in parenthesis) for the forest bird assemblage in different
land-use types and primary forest degradation classes in PGM and STM. NA indicates that the
comparison is not valid as the land use is unsampled in the municipality in question.
Land uses
PGM
STM
Mechanised agriculture, Pasture
30.432 (<0.001)
2.717 (<0.001)
21.529 (<0.001)
2.442 (<0.001)
Mechanised agriculture, Primary forest
Mechanised agriculture, Secondary forest
Pasture, Primary forest
Pasture, Secondary forest
5.144 (<0.001)
3.568 (<0.001)
9.647 (<0.001)
4.926 (<0.001)
5.702 (<0.001)
3.989 (<0.001)
7.073 (<0.001)
4.232 (<0.001)
Primary forest, Secondary forest
Plantation, Pasture
3.969 (<0.001)
1.726 (<0.05)
4.337 (<0.001)
NA
Plantation, Primary forest
Plantation, Mechanised agriculture
Plantation, Secondary forest
Small-holders, Secondary forest
Small-holders, Mechanised agriculture
Small-holders, Pasture
4.333 (<0.001)
1.579 (<0.05)
2.757(<0.001)
NA
NA
NA
NA
NA
NA
2.676 (<0.001)
2.295 (<0.001)
1.31 (0.0649)
Small-holders, Primary forest
NA
4.495 (<0.001)
Forest degradation classes
Global test
9.7309 (<0.001)
6.193 (<0.001)
Logged & burnt, Logged
Logged & burnt, Secondary forest
2.394 (<0.001)
2.979 (<0.001)
1.599 (<0.001)
3.663 (<0.001)
Logged & burnt, Undisturbed
Logged, Secondary forest
Logged, Undisturbed
Secondary forest, Undisturbed
Burnt, Logged & burnt
Burnt, Logged
2.971 (<0.001)
4.188 (<0.001)
2.149 (<0.001)
3.749 (<0.001)
NA
NA
1.732 (<0.001)
3.6635 (<0.001)
1.169 (0.084)
3.468 (<0.001)
0.948 (0.591)
1.408 (<0.05)
Burnt, Undisturbed
Burnt, Secondary forest
NA
NA
1.359 (<0.05)
1.858 (<0.001)
48
Tabela 2.4 PERMANOVA Pseudo-F values of global test (p-values in parenthesis) and t-values
of pair-wise comparison (p-values in parenthesis) for the entire bird assemblage in different
land-use types, primary forest degradation classes and secondary forest age in PGM and STM.
NA indicates that the comparison is not valid as the land use is unsampled in the municipality in
question.
Land uses
PGM
STM
6.327 (<0.001)
4.978 (<0.001)
Logged, Logged a& burnt
Logged, Undisturbed
Logged, young
Logged, Intermediate
Logged, Old
Logged&burnt, Undisturbed
Logged&burnt, Young
Logged& burnt, Intermediate
Logged&burnt, Old
Undisturbed, young
Undisturbed, Intermediate
Undisturbed, Old
Young, Intermediate
Young, Old
Intermediate, Old
Burnt, Logged
Burnt, Logged&burnt
Burnt, Undisturbed
Burnt, Intermediate
Burnt, Old
Burnt, Young
2.321(<0.001)
2.159 (<0.001)
3.517 (<0.001)
2.878 (<0.001)
1.958 (<0.05)
2.952 (<0.001)
2.913 (<0.001)
2.113 (<0.001)
1.507 (<0.05)
3.588 (<0.001)
3.191 (<0.001)
2.604 (<0.001)
1.404 (<0.001)
1.59 (<0.001)
1.001 (0.425)
NA
NA
NA
NA
NA
NA
1.616 (<0.001)
1.168 (0.082)
2.711 (<0.001)
3.344 (<0.001)
3.047 (<0.001)
1.741 (<0.001)
2.294 (<0.001)
2.641 (<0.001)
2.152 (<0.001)
2.69 (<0.001)
3.224 (<0.001)
3.028 (<0.05)
1.082 (<0.001)
1.741 (<0.001)
1.4 (<0.05)
1.415 (<0.05)
0.946 (0.583)
1.364 (<0.05)
1.926 (<0.001)
1.587 (<0.001)
2.019 (<0.05)
3.3 Differences in species richness with changes in landscape-scale total
forest cover
We found a significant positive and broadly linear relationship (Fig. 2.10 and
Fig. 2.11) between richness of forest birds and primary forest cover (aggregating all
forest disturbance classes) and total forest cover within each catchment in both
regions. These relationships were weaker in PGM than in STM for both primary forest
cover and total forest cover (primary forest cover: adj.r² = 0.46, p<0.001 and adj.r² =
0.79, p<0.001 for PGM and STM respectively; total forest cover: adj.r² 0.4, p<0.001 and
adj.r² = 0.75, p<0.001 for PGM and STM respectively).
49
Figure 2.10 Linear regressions between percentage of primary forest cover (aggregating all
disturbance classes within a 10 km radius of each catchment) and richness of forest birds in
PGM adj.R² = 0.46 and STM adj.R² = 0.79 (p-values significant at 0.001).
Figure 2.11 Linear regressions between percentage of total forest cover (in a radius of 10 km)
of each catchment, of forest birds richness in PGM (adj.r² = 0.4) and STM (adj.r² = 0.75); (pvalues significant at 0.001).
3.4 Additive partitioning of diversity
Additive partitioning indicated an increasingly higher percentage contribution for
alpha (point count) diversity in more intensively used areas, with this trend being
especially marked in STM. The βAmong points component (species turnover among points
in a transect) did not vary markedly across land uses. In contrast, β Among transects (species
turnover among transects in a catchment) had a greater influence on gamma diversity
in both regions, with turnover in species composition among transects being higher in
primary forest than either secondary forest or production areas (Fig. 2.12).
50
Figure 2.12 Additive diversity partitioning (in %) in different land-use systems in PGM and STM,
using forest birds. Black = Alpha (point counts); light grey = Beta (among point counts) and dark
grey = Beta (among transects).
4.
Discussion
We found that Amazonian bird assemblages in multiple-use agricultural landscapes
change markedly along a gradient of human impacts and land-use intensity in a predictable
fashion. We observed a decrease in total species richness and an increasing shift in species
composition when comparing undisturbed primary forest to increasingly degraded primary
forest, secondary forest, plantations, pastures and arable fields. This general conclusion is
supported by results from similar studies of land-use intensity gradients elsewhere in the humid
tropics, including Indonesia (Waltert et al. 2004), Mexico (Pineda and Halffter 2004) and
Ecuador (Tylianakis et al. 2006). In the following sections we draw on our results to assess in
more detail the relative biodiversity conservation value of production systems, secondary forests
and varyingly (un)degraded primary forests.
4.1 Production areas
The conservation value of production areas in the Neotropics has been the
subject of considerable debate, with some studies from Central America indicating that
non-forest production areas – the tropical ‘countryside’ – may host a significant
proportion of the baseline avifauna community (e.g. 70% of native forest birds sampled
in pastures and coffee plantations in Costa Rica; Lindell et al. 2004). However,
comparable studies from South American production landscapes have found much
lower levels of diversity (e.g. 32% of native forest birds sampled in cattle pastures and
scrub in the Brazilian Amazon (Mahood et al. 2012). In part, the difference between the
Amazon and Central America may reflect the more heterogeneous and structurally
diverse old agricultural landscapes that characterize parts of Central America (Lindell
et al. 2004).
51
The results from our study indicate that production areas typical of much of
eastern Amazonia (i.e. degraded cattle pastures, and mechanised agriculture) may
harbour only slightly more than one third of the regional avifauna (43 and 38% in PGM
and STM respectively). Cattle pastures provided some habitat for forest species (27%
and 17% of species shared with primary and secondary forest habitats in PGM and
STM respectively), but the majority of cattle pastures in our sample are unimproved
and often contain large numbers of shrubs and scattered trees providing habitat
resources and cover for birds. On the other hand, plantations forestry in Paragominas
retained very little avian biodiversity harbouring just 7% of the regional pool of forest
species.
Interpretation of simple percentages of shared species should be treated with
caution (Barlow et al. 2010) as the frequency of occurrence of these forest birds in any
given production area was also very low: 15% of all forest species from PGM and STM
were recorded on less than five occasions across all agricultural areas. Occasional
detections of nominally forest species, such as Black-and-white Hawk-eagle (Spizaetus
melanoleucus) utilising non-forest habitats, does not necessarily indicate that these
species can persist in the absence of neighbouring forest patches, and many such
detections might be better considered to be the result of gap-crossing events (Lees and
Peres 2009) or occasional foraging sorties. However, even such rare events may have
important implications for landscape dynamics given the importance of birds as seed
dispersers assisting in regeneration processes (Silva et al. 1996, Cole et al, 2010).
4.2 Secondary forests
Secondary or regenerating forests are becoming an increasingly dominant type
of land cover in the tropics (Neef et al. 2006, FAO 2012) and as such are likely to have
a very important future role in safeguarding the persistence of forest species in some
regions (Chazdon et al. 2009, Gardner et al. 2009). Combining all secondary forests
age groups together, this land cover harboured intermediate levels of forest species
richness (242 species, 73% of all forest birds recorded in both regions) and species
composition between that of primary forests (332 species in total, 70% overlap with
secondary forests) (Fig. 2.5 and Table 2.5 and 2.6) and production land-use systems
(88 species, 26% forest species).
52
Table 2.5 Percentage of total species and forest birds (in parentheses) shared between landuse system in PGM and STM.
PGM
Forest
Secondary
Pasture
Plantation
Exclusive
55(76)
13(39)
27(54)
13(38)
16(25)
28(43)
16(31)
18(26)
18(28)
13(20)
25(96)
2(67)
0
6(13)
0
Forest
Secondary
Pasture
Small-Holder
Exclusive
Forest
Secondary
Pasture
Small-Holder
53(85)
20(64)
14(54)
22(54)
19(41)
18(67)
-
26(100)
5(20)
4(0)
1(0)
Mechanised
7(58)
10(38)
13(31)
9(35)
2(0)
Forest
Secondary
Plantation
Pasture
Mechanised
STM
Table 2.6 Percentage of all species and forest birds (in parentheses) shared between different
forest degradation classes in PGM and STM.
PGM
Undisturbed
Logged
Logged&burnt
Secondary
STM
Undisturbed
Logged
Burnt
Logged&burnt
Secondary
Undisturbed
Logged
Logged&burnt
34(98)
31(98)
25(98)
58(88)
47(84)
Undisturbed
Logged
Burnt
Logged&burnt
Exclusive
44(98)
36(96)
42(98)
32(100)
41(92)
50(93)
39(95)
43(88)
40(82)
47(87)
3(92)
3(90)
2(86)
2(63)
9(46)
51(76)
Exclusive
2(100)
5(89)
3(50)
8(23)
However, it is also clear that secondary forests do not provide adequate habitat for
many forest-associated species. For example, 18% of forest species were absent from
secondary forests in PGM and 23% were absent from secondary forests in STM, including the
Great Jacamar (Jacamerops aureus) and Uniform Woodcreeper (Hylexetastes uniformis), which
were only found in primary forest. Although we recorded many of the species listed by Parker et
al. (1996) as disturbance-sensitive in secondary forests, many of these species were much
more infrequently recorded in primary than secondary forests. For instance, the nuclear
understorey flock-leading Cinereous Antshrike (Thamnomanes caesius) was recorded in 66% of
primary forest transects and just 23% of secondary forest transects and the canopy-dwelling
Red-billed Pied Tanager (Lamprospiza melanoleuca) was recorded in 28% of primary forest
transects and 1.5% of secondary forest transects. This reduction in species richness is
53
especially pronounced in relatively young secondary forests which dominate much of the
eastern Amazon, Fig. 2.5), and these are often returned to agricultural production within less
than ten years in the Amazon region (Neef et al. 2006).
4.3 Disturbed primary forests
Like other studies, we found consistently more species in undisturbed primary forest
than in forests disturbed by logging and burning (e.g. Barlow et al. 2007a, Gibson et al. 2011).
Nevertheless, we also found that primary forests disturbed by fire and logging retained relatively
high numbers of forest species (86% of the total regional species pool were found in logged
forest and 78% in logged&burnt forests in PGM; with 59% of species in burnt, 74% in
logged&burnt and 74% in logged forests in STM). Despite these differences in species totals,
we did not find statistically significant differences in the average number of species per site
when comparing between primary forests characterised by different levels of historical
disturbance. This may be partly because of the high level of natural environmental variation
(due to factors such as soil type and topography) or because forests are grouped within the
same degradation class that may mask differences in the time-since or severity of disturbance
event(s) or distance to source populations (Dunn 2004b, Barlow et al. 2006, Edwards et al.
2011, Mestre et al. 2013). Finally, our comparisons may also be biased because areas selected
for timber harvesting are often of higher than average tree basal area (and thus perhaps higher
faunal species richness) (Henriques et al. 2008, Barlow et al. 2006). These kinds of difficulties
in interpretation highlight the limitations of using species richness, rather than species
composition to understand the ecological effects of land-use and landscape change (Barlow et
al. 2007a, Devictor et al. 2010).
Species richness was similar in all types of primary forest irrespective of the level of
disturbance, yet some species (4% in PGM and STM) were entirely restricted to the relatively
few undisturbed forest transects. These included Brown-winged (Psophia dextralis) and Darkwinged (P. obscura) Trumpeters, Variegated Antpitta (Grallaria varia) and Musician Wren
(Cyphorhinus arada). Even small canopy disturbance events, such as the felling of a single tree,
may alter understorey microclimatic conditions and hence ground cover of the forest floor
rendering it unsuitable for some terrestrial species (Lees and Peres 2010). Although some
disturbance sensitive understorey species, such as Bare-eyed Antbird (Rhegmatorhina
gymnops), Rufous-capped Antthrush (Formicarius colma) and Black-tailed Leaftosser
(Sclerurus caudacutus), were occasionally detected in some burnt forest transects, our data
support the conclusion by Barlow et al. (2006) in suggesting that areas exposed to fire are more
dissimilar to primary forests regarding their avian biota compared to those that have only been
logged (see also Fig. 2.7). Our findings also reinforce the conclusions of other studies from
elsewhere in the tropics that disturbed primary forests are able to effectively conserve many
forest-dependent species (Putz and Redford 2010, Edwards et al. 2011, Gibson et al. 2011), at
least in Amazonian landscapes that maintain high forest land-cover.
54
4.4 Effects of landscape scale forest loss on avian diversity
The total amount of remaining primary forest at the catchment (landscape)
scale was an important predictor of forest species richness, confirming the conclusions
of the small number of previous landscape-scale studies (e.g. Bennet et al. 2006 in
Australia and Pardini et al. 2010 in the Atlantic forest of Brazil). We were not able to
detect any meaningful thresholds in the relationship between changes in forest cover
and changes in avian diversity in either region. Nevertheless, these results point
strongly to the importance of adopting a landscape-scale (as opposed to property-level)
approach to maintaining and enhancing the conservation status of multiple use
landscapes in tropical forest regions.
We found that rates of species turnover changed consistently along a gradient
of increasing forest disturbance and land-use intensity. Alpha diversity became
increasingly important in explaining total levels of diversity as land was subject to more
intensive human use (see Fig. 6); indicating lower levels of turnover as a result of an
impoverished species pool characterised by a smaller number of species that can
survive or proliferate in anthropogenic habitats; i.e. the process of
biotic
homogenisation which is already characterising many Neotropical forest habitats (e.g.
Lôbo et al. 2011, Melo et al. 2013). In comparison, transect-scale beta diversity made a
more important contribution to landscape diversity in forest areas, and to undisturbed
forest sites in particular - where the avian assemblage is composed of a large number
of habitat specialists that are often found at low densities (Terborgh et al. 1990,
Tylianakis et al. 2006).
5.
Conclusions
The data presented in this paper represent what is arguably the largest-scale
field assessment of the impacts of land-use change on tropical avifaunas to date. We
found that 1) there is no evidence for a significant role of production areas in
conserving Amazonian forest bird biodiversity; 2) secondary forest landscapes
conserve significant bird biodiversity but differ markedly in assemblage composition
from primary forests; 3) primary forests disturbed by fragmentation, logging and fire
retain a high proportion of forest bird species but still lack some of the most sensitive
taxa, with burnt forests appearing more affected than forests that have been logged but
not burnt, 4) primary forest cover is an important predictor of total diversity for each
catchment, and 5) that the distribution of species diversity across multiple spatial
scales is highly influenced by the level of habitat modification, with beta-diversity
55
consistently declining with increasing land-use intensity. The broad patterns of species
richness and loss across the gradient of land-use between these two regions located
800 km apart in biogeographically different Amazonian interfluvial regions were similar,
suggesting that conclusions on responses of Amazonian avifaunal communities to
forest loss and degradation can be generalised.
As most of our fieldwork was conducted on private lands, our results reinforce
the importance of conservation through private forest reserves in Brazil and the need to
enforce current forest legislation and promote coordinated conservation strategies
across neighbouring properties to safeguard regional biodiversity in the Amazon. In
considering priorities for the protection of regional forest avifauna in eastern Amazonia,
perhaps the most important implication of our results is the urgent need (ahead of
costly investments in the restoration of cleared land) to protect and restore the
varyingly disturbed and degraded primary forests that dominate much of eastern
Amazonia, and which remain vulnerable to further timber extraction and recurrent fire
events.
56
Capítulo 3
Idiosyncratic responses of forest-associated Amazonian birds
to disturbance and land-use changes
Nárgila G. Moura, Alexander C. Lees, Alexandre Aleixo, Jos Barlow, Erika Berenguer,
Joice Ferreira, Ralph MacNally, Jim R. Thomson, Toby A. Gardner
Abstract
As land-use change intensifies across the tropics, it is imperative to understand what
environmental characteristics mediate biodiversity persistence in human-modified
landscapes. Yet most studies investigating avian responses to habitat modification are
focused on community-wide response or narrow guilds such as understory
insectivores, and they rarely compare the relative impacts of the full gamut of
environmental variation. Here we investigated species-specific responses to land-use
change and forest disturbance in 36 drainage catchments distributed across two large
regions of the eastern Brazilian Amazon of 30 focal forest-associated species with
varying life histories. We investigated patterns of occupancy in a gradient of land use
change from undisturbed forest to mechanized agriculture and then explored
relationships between species persistence and local, landscape and historical
environmental factors in 171 primary forest transects. We found that our focal species
universally declined along the gradient of human impact, being consistently rarer in
secondary forests and absent from agricultural land-uses. Within undisturbed and
degraded primary forest transects we found that distance to forest edge and the
biomass of large trees were the most important predictors driving the occupancy of
focal species. However, these ubiquitous responses belie huge individual variation in
focal species response to different environmental determinants, sometimes even
between both of our study regions. We were able to model the responses of suboscine
passerines better than most other groups and some species e.g. Lipaugus vociferans,
Herpsilochmus rufimarginatus and Myiornis ecaudatus are extremely reliable indicators
of high basal forests. We advocate using species-level analysis to complement
community-wide responses, as the latter often mask huge idiosyncratic variation in
species’ responses to environmental change.
Keywords: forest species, Neotropical birds, Brazil, human-modified landscape,
variable importance, random forest
57
1.
Introduction
Land-use change and agricultural expansion is the preeminent threat to tropical
biodiversity (Laurance et al. 2014). A significant body of research has assessed
patterns of biodiversity persistence in tropical deforestation frontiers. However, this
work has been predominantly focussed on a subset of common objectives, including;
patterns of species occupancy in variable-sized forest remnants (e.g. Uezu et al. 2005,
Newmark and Stanley 2011), the influence of the surrounding matrix on species
persistence in areas of native habitat (e.g. Umetsu and Pardini 2007, Perfecto and
Vandermeer 2002), and patterns of species persistence in production systems (e.g.
Daily et al. 2000, Phalan et al. 2011), or native vegetation subject to a specific type of
disturbance such as logging (e.g Wunderle et al. 2006, Edwards et al. 2011), fire (e.g.
Uhl 1998, Mestre et al. 2013), and over-hunting (Wright 2003, Terborgh et al. 2008).
Comparatively few studies have explored the full gamut of land-use types and
disturbance regimes that characterise many frontier regions, or assess changes in
community composition at different spatial scales (Gardner et al. 2010, Moura et al.
2013). As such our understanding of the distribution of individual species across
human-modified landscapes and the relative importance of different environmental
variables in determining observed patterns, is often very poor or non-existent
(Tylianakis et al. 2006) with the generality of many studies being compromised by
problems of sample size and spatial extent (Gardner et al. 2009, Peres et al. 2010).
The Brazilian Amazon represents a global priority for biodiversity conservation
efforts. Between 1988-2013, 8% (402 000 km²) of forest cover was lost and at least
64,000 km² of forest was degraded by fire and logging events between 2007-2010
(INPE 2014a,b). Therefore, conservationist biologists are charged with trying to
understand the impacts of land use change on biodiversity associated with an
expanding agricultural frontier (Gardner et al. 2009, Laurance et al. 2011). Birds are
one of the species groups most commonly studied to understand the ecological effects
of human disturbances to such tropical forest ecosystems (Tscharntke 2008, Karp et al.
2011, Newbold et al. 2013). However, the vast majority of these studies have been
limited to examining the pooled responses of entire avian communities through
measures of species richness, diversity and community structure (e.g. Aleixo 1999,
Barlow et al. 2006a, Lees and Peres 2006, Sodhi et al. 2008). Because tropical forest
species assemblages have very high levels of alpha diversity (c.270 bird species in
typical Amazonian terra firme forests Cohn-Haft et al. 1997), such studies risk masking
important species-specific response patterns given the myriad of different life histories,
58
even between closely related taxa (Elmqvist et al. 2003, Ferraz et al. 2007). Such
masking effects may result in misleading conclusions regarding the sensitivity of
biodiversity to disturbance, and the kinds of species that are most at risk of extinction.
Different avian function groups are known to respond differentially to land-use
change and habitat disturbance. For instance, understory insectivorous birds (including
ant-followers, terrestrial foragers, and obligate mixed-flock species) are considered a
particularly vulnerable group (Stouffer and Bierregaard 1995, Castelletta et al. 2000),
being highly sensitive to edges (Wong et al. 1998, Develey and Stouffer 2001), and
forest fragmentation (Stratford and Stouffer 1999, Lees and Peres 2008) and known to
avoid non-forest matrix habitat (Antongiovanni and Metzger 2005, Mahood et al. 2012).
By comparison, some frugivores (especially small-bodied species) may be more
tolerant to anthropogenic habitat disturbance (Gomes et al. 2008) owing to their higher
vagility (Lees and Peres 2009).
Here we employ occupancy data for 30 widely-distributed Amazonian forest bird
species with differing diets, feeding strategies and flocking responses, representative of
the terra firme forest bird community, to investigate species-specific responses to landuse change and forest disturbance across two regions in the eastern Brazilian Amazon.
We used the focal species approach (Lambeck 1997) where a small group of species
are used to represent discrete environment requirements and their persistence define
the attributes that must be present to guarantee their occurrence, without studying all
the species individually.
We analysed data collected from two regions with different histories of use and
occupation, with 361 transects distributed in a nested fashion across 18 randomlychosen catchments per region covering a gradient of human disturbance from
undisturbed forest through forest varyingly disturbed by fire and logging, forests
regenerating on cleared land to cattle pastures and mechanized agriculture.
Specifically, we investigated a) how species-specific occupancy patterns changed
across the different land-uses; b) how the individual species respond to primary forest
disturbance; c) and we assess the extent to which individual species responses to
forest disturbance can be partly determined by their life history traits or response to
broader land-use changes.
59
2.
Materials and methods
2.1 Study regions and experimental design
This study was conducted in two municipalities in Brazilian state of Pará in the
eastern Amazon (Fig. 3.1): Paragominas (hereafter PGM) and Santarém/Belterra
(hereafter STM). Both are biophysically distinct , experienced the loss of at least one
third of their native forest cover yet are distinguished by significant differences in their
historical trajectory of colonization and both past and present land-uses and also have
ongoing sustainable land use initiatives strongly supported by local government
(Gardner et al. 2013).
Paragominas (1.9 Mha) was sampled between July and November 2010 and
again in May 2011 and is located in north-east Pará state 300 km south of the state
capital Belém. The municipalities of Santarém/Belterra (sampled area equal to
approximately 1 Mha), both sampled between October 2010 and February 2011, lie
immediately south-east of the confluence of the Amazonas and Tapajós rivers (for
more details see Gardner et al. 2013).
Both municipalities were divided into approximately evenly-sized catchments (c.
4000 ha), which were delineated using a digital elevation model and SWAT (Soil and
Water Assessment Tool) for ARCGIS 9.3. Eighteen catchments were selected for each
region capturing the full gradient of deforestation (6-100% forest cover in Paragominas;
10-100% forest cover in Santarém for 2010), whilst also ensuring adequate
representation of current land-use practices, the spatial distribution of the rural
population, and major soil types.
In each catchment between eight and twelve 300 m transects were allocated
(depending on differences in catchment size) and distributed using a stratified-random
sampling design to increase the likelihood that they would capture important
heterogeneities in habitat condition in either forest and/or production systems (using an
even density of 1 transect per 400 ha). The distance between each transect was at
least of 1.5 km, helping to ensure sample independence. In total we sampled 196
transects in PGM and 165 in STM.
The transects were classified a posteriori into six land-use types (see Table
3.1), using 2010 Landsat images and a decision tree classification algorithm (Gardner
et al. 2013), as (i) primary forest - the region’s original climax physiognomy that has
never been clear-felled for agriculture (although may have been extensively degraded
60
by disturbance from logging, fire and other forms of exploitation); (ii) secondary forests
- forests that have developed after complete clearance (Putz and Redford 2010); (iii)
tree plantations - in this case commercial plantations, typically of Eucalyptus sp., teak
(Tectona grandis) or paricá (Schizolobium parahyba var. amazonicum); (iv) cattle
pasture; (v) mechanised agriculture - typically soybean fields or rice; and (vi) smallholder agriculture - farms typically smaller than 100 ha and consisting of small-scale
manioc plantations and/or fruit trees. Primary forest transects were further subclassified in four classes of disturbance based on ground-truthed observations of past
disturbance events (Gardner et al. 2013): ‘undisturbed’ for which no evidence of recent
human-induced degradation was apparent, ‘selectively logged’ for forests which have
undergone detectable logging, ‘burned’ for forests in which fire scars were found on
trees and charcoal deposits detected on the ground and ‘logged&burned’ for those
forests exposed to both of these disturbances.
Figure 3.1 Map of Paragominas (a) and Santarém/Belterra (b) showing the location of the 18
catchments surveyed in each municipality. Two example catchments are presented for each
municipality in (c) showing the location of transects and transects design and positioning of
point count stations and vegetation plots (d).
61
Table 3.1 Total number of transects allocated to each land-use type in both study regions
Land-use type
Primary forest
Paragominas
Santarém
Undisturbed
9
17
Logged only
44
25
Burnt only
0
9
Logged&burned
Secondary forest
44
25
23
43
Plantation
9
0
Pasture
53
25
Mechanised agriculture
12
16
Small-holder agriculture
0
7
196
165
Total
2.2 Bird surveys
In each transect three point count (PC) stations were located at 0, 150 and 300
m. We carried out two repetitions of three 15 minute, 75 m fixed-width PCs per
transect, recording all species seen or heard. Repetitions ensured that temporal
variation in avian vocal activity was minimized. A total of 1083 PCs were conducted
across both regions. For more details on survey methodology, full species lists and
links to digital vouchers see Lees et al. (2012, 2013a). We recorded 467 species in
both regions of which 336 were forest-dependent species (forest birds), with 359
species (252 forest birds) in PGM and 377 (286 forest birds) in STM. Forest-associated
species are those that occur in undisturbed terra firme forests but are not necessarily
restricted to those habitats (for more details see Moura et al. 2013). As our
experimental design focused on maximising spatial extent of sampling, trading-off
against temporal repetition, we have not corrected for potential differences in
detectability, which we here assume to be uniform between species and habitats
(Welsh and Lougheed 1996)
We reduced our choice of candidate focal species for the analysis by first
selecting all forest birds occurring in both municipalities with records from at least 20
point counts per region, thus excluding any rare species. This left a short list of 47
species which we classified with respect to four life-history traits: diet, flocking
62
behaviour and forest strata occupied (based on Stotz et al. 1996, Cohn-Haft et al.
1997, Stouffer and Bierregaard 1995, 2007, del Hoyo et al. 2014). Our final selection
comprised 10 species of insectivores, 9 species of frugivores and 11 species of
omnivores (Table 3.2).
63
Table 3.2 Focal species and their respective life strategies such as diet, flocking behaviour and forest strata occupied. PGM and STM represent Paragominas
and Santarém-Belterra study regions respectively.
Species
English name
Diet
Flocking behaviour
Strata
Patagioenas plumbea
Piaya cayana
Plumbeous Pigeon
Squirrel Cuckoo
67
54
42
24
Frugivore
Omnivore
Solitary
Flock dropout
Canopy
Canopy/ Midstory
Trogon viridis
Ramphastos tucanus
Ramphastos vitellinus
Pteroglossus aracari
White-tailed Trogon
White-throated Toucan
Channel-billed Toucan
Black-necked Aracari
48
69
65
65
91
77
60
29
Omnivore
Frugivore
Frugivore
Frugivore
Flock dropout
Monospecific flock
Monospecific flock
Monospecific flock
Midstory
Canopy
Canopy
Canopy
Brotogeris chrysoptera
Pionus menstruus
Amazona farinosa
Myrmotherula longipennis
Golden-winged Parakeet
Blue-headed Parrot
Mealy Parrot
Long-winged Antwren
48
115
72
36
59
55
62
29
Frugivore
Frugivore
Frugivore
Insectivore
Monospecific flock
Monospecific flock
Monospecific flock
Flock obligate
Canopy
Canopy
Canopy
Understory
Thamnomanes caesius
Herpsilochmus
rufimarginatus
Cinereous Antshrike
134
82
Insectivore Flock obligate
Understory
Rufous-winged Antwren
White-shouldered
Antshrike
68
41
Insectivore Flock dropout
Canopy
96
54
Understory
294
62
241
69
Insectivore Solitary
Midstory
Understory
Glyphorynchus spirurus
Automolus paraensis
Tyranneutes stolzmanni
Ceratopipra rubrocapilla
Schiffornis turdina
Gray Antbird
Plain-brown Woodcreeper
Wedge-billed
Woodcreeper
Para Foliage-gleaner
Dwarf Tyrant-Manakin
Red-headed Manakin
Thrush-like Schiffornis
112
27
87
72
27
98
22
110
79
23
Insectivore
Insectivore
Omnivore
Frugivore
Omnivore
Flock dropout
Flock obligate
Solitary
Solitary
Solitary
Understory
Understory
Midstory
Understory
Midstory
Pachyramphus marginatus
Black-capped Becard
20
33
Omnivore
Flock dropout
Canopy
Thamnophilus aethiops
Cercomacra cinerascens
Dendrocincla fuliginosa
Nº of records
PGM
STM
64
Species
English name
Lipaugus vociferans
Querula purpurata
Myiornis ecaudatus
Lophotriccus galeatus
Zimmerius acer
Ornithion inerme
Attila spadiceus
Lamprospiza melanoleuca
Saltator grossus
Screaming Piha
Purple-throated Fruitcrow
Short-tailed Pygmy-Tyrant
Helmeted Pygmy-Tyrant
Guianan Tyrannulet
White-lored Tyrannulet
Bright-rumped Attila
Red-billed Pied Tanager
Slate-colored Grosbeak
Nº of records
PGM
STM
103
49
49
195
66
72
44
36
51
190
36
62
138
81
21
42
25
53
Diet
Flocking behaviour
Strata
Omnivore
Omnivore
Insectivore
Insectivore
Omnivore
Omnivore
Frugivore
Omnivore
Omnivore
Flock dropout
Monospecific flock
Solitary
Flock dropout
Flock dropout
Solitary
Flock dropout
Flock dropout/monospecific flock
Flock dropout
Midstory
Canopy
Canopy
Midstory
Canopy
Canopy
Canopy
Canopy
Canopy
65
2.3 Environmental variables
We used 14 environmental variables which we a-priori judged to be relevant in
influencing patterns of occupancy of forest birds in primary forest transects in both
regions. These variables were divided into three categories: local, landscape and
historical.
2.3.1 Local variables
Variables related to forest structure are known to affect the presence of many
forest species (e.g. Bueno et al. 2012, Cintra and Naka 2012, Stratford and Stouffer
2013). For instance the leaf litter depth may affect understorey birds (Pearson 1975)
and availability of dead trees may be important for species which use them for foraging
or nesting/roosting (Skutch 1961, Cornelius et al. 2008). Edaphic variables are also
known to influence avian community composition (Pomara et al. 2012)
Forest structure. Vegetation sampling was undertaken in 10x250 m plots (0.25
ha) where all trees and palms (alive or dead) > 10 cm diameter at 1.3 m height were
measured (Fig. 3.1). Smaller individual plants (2 to 10 cm diameter) were sampled in
five 5 x 20 m subplots. Lianas (woody vines) followed the same sampling design as
trees and palms, but the diameter was measured at 1.3 m from the main root, located
inside the plot (for large individuals) or inside the subplots (for smaller individuals). All
living individuals were identified to species level by experienced parabotanists, with
herbarium samples collected whenever appropriate and fertile specimens registered at
the IAN herbarium in Belém, Brazil, with these data being compiled to give a total
richness of tree, palm and liana species (TPL). Understory density (UD) was measured
by counting the number of stems between 2-10 cm diameter in the 100m² subplots.
We measured the biomass of dead trees > 10 cm diameter (BDT10) which
pertained to stumps, fallen trunks, fallen branches and fallen palms and lianas (with >
10 cm diameter of at least one of its extremities) sampled in five 5x20 m subplots
located 30 m apart in each transect (Fig. 3.1). The length and diameter of all individual
pieces were measured at both extremities (if branched, both parts were measured
separately). Each piece of dead wood was subdivided into five decomposition classes
(Harmon and Sexton 1996); ranging from ‘recently dead’ to ‘completely soft, rotten
crumbling wood’. Samples sometimes had severe structural damage so we recorded
four damage categories for each sample: 0-25, 25-50, 50-75 and >75%.
66
Leaf litter biomass (BLL) comprising fallen leaves, fine twigs, fruits and seeds
was sampled every 50 m along the transect in 50x50 cm quadrats at both 5 and 10 m
perpendicular to the main transect line to avoid human trampling (Fig.2.1). Samples
were taken to a laboratory and oven-dried to calculate their weight.
Edaphic variables. Soil was sampled at five points separated by 50 m along
each transect where individual samples were collected at three different depths (0-10,
10-20 and 20-30 cm, Fig. 3.1). Soil analyses were carried out at the Embrapa
Amazônia Oriental Soil Laboratory in Belém. Here we used variables of pH (following
EMBRAPA 1997) and clay content as a measure of soil texture, determined using a
densimeter (Camargo et al. 1986).
2.3.2 Landscape variables
Topographic variables elevation (ELEV) and slope (SLOPE) were obtained
using SRTM images (90 m resolution; National Aeronautics and Space Administration).
A remote sensing analysis was performed using a 30 m (900 m²) pixel resolution
Landsat image time-series from 1988-2010 in Paragominas and 1990-2010 in
Santarém with ArcGIS 9.3 software. The images were classified using a decision tree
algorithm after being corrected for atmospheric haze and smoke interferences (see
Gardner et al. 2013). Mean distances to forest edge (primary forest + secondary forest
>10 years mapped in 2010) were calculated within a buffer of 100 m immediately
surrounding each transect (EdgePS).The classification of primary forest disturbance for
each transect was based on evidence from a combination of both field observations
and a visual inspection of degradation scars from remote-sensing images, providing
measures of both the number of times each transect was logged (NTL) and burnt
(NTB). In addition, we used the semi-supervised classification of degraded forest pixels
to estimate the percentage of forest pixels degraded (PFD) at least once in the time
series within a 100 m buffer around each transect.
2.3.3 Historical variables
Historical land-use trajectory may also affect community composition in humanmodified tropical landscapes (Gaston 2000, Thompson et al. 2002, Gardner et al.
2009). We calculated the deforestation curvature profile (DPC) within a 500 m buffer,
by transect, in mature forest (primary forest and old secondary forest [>20 years]),
based on data on deforestation during the last two decades. The DPC is the maximum
deviation of the deforestation curve in relation to the line linking initial and final forest
proportion. The DPC is unit-less and will be positive if the deforestation curve is mainly
67
below average deforestation line, and negative if it is mainly above it (see Ferraz et al.
2009).
2.4 Data analysis
In order to visually assess how focal species responded to different land-uses
we measured the percentage occupancy of transects within each land use type for
PGM and STM respectively. Then, to investigate the relative importance of each
candidate predictor variable for each focal species, we used Random Forest decision
trees. The Random Forest (hereafter RF) was performed using 2000 decision trees,
using the package ‘extendedForest’ (Ellis et al, 2012) conducted in R version 2.15.1 (R
Core Development Team 2011). We modified the RF fitting and cross validation
procedure to account for spatial-autocorrelation of transects sampled within the same
catchment using a variant of the residual autocovariate method (RAC, Crase et al.
2012). Specifically, for each catchment in turn, we used data from all other catchments
to predict occupancy within the held-out catchment, and calculated the mean residual.
We then included the catchment mean residuals as an additional predictor variable
(analogous to a catchment level random intercept) in a final RF model fitted with all
data combined. Following Ellis et al (2012) we calculated R 2 weighted mean
importance values for each predictor variable, which indicate the relative importance of
each variable in predicting the assemblage as a whole. After modelling we discarded
poorly-modelled species with r² ≤ 0.4 and then plotted a cluster heat map, using the
‘heatmap.2’ function, also in R, to visualize differences in species-environment
relationships across both individual species and variables.
3. Results
3.1 Species occupancy patterns
Across the full range of land-use types, our 30 focal forest species are all rare
or extinct outside of forest habitats (Fig. 3.2). Only one species, Pionus menstruus, was
encountered with any regularity in non-forest habitats in both regions, as was Amazona
farinosa in PGM only. Both are large canopy frugivores and many detections involved
birds simply flying over non-forest landscapes.
The responses of species occupancy patterns in forested areas differed among
different forest types and between regions. We identified five broad response
categories among our focal species (Fig. 3.2). The first response category involved
species such as Automolus paraensis and Schiffornis turdina which exhibited a rapid
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decline in occupancy from undisturbed to disturbed forest (either logged, burned, or
both). The second response category included species such as Thamnomanes caesius
and Lamprospiza melanoleuca that showed a gradual decline with increasing forest
disturbance. The third response category included those species whose occupancy
was relatively similar despite a reduction in forest quality (e.g. Thamnophilus aethiops
and Lophotriccus galetaus). The fourth category included species (e.g. Patagioenas
plumbea and Pteroglossus aracari) that were more frequently encountered in disturbed
forests. A few species e.g. Piaya cayana and Trogon viridis exhibited marked
differences in responses between regions, which was our fifth category. Most species
were either absent or rarely encountered in secondary forest transects, with the
exception of Trogon viridis in STM, which was the only species that was more
frequently encountered in secondary than in primary forests.
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Figure 3.2 Focal species (in taxonomic order) occupancy of different land use types in the municipalities of Paragominas (filled circles) and Santarém (empty
circles).Illustrations reproduced with the permission of Lynx Edicions.
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3.2 Importance of predictor variables
In pooling analyses for all focal species, the most important predictors of
species occurrence in primary forest transects in PGM were the biomass of large trees
(BT10), the distance to the forest edge (EdgePS), and the percentage of degraded
primary forest in an adjacent buffer area (PFD) (Fig. 3.3). The same pattern of
response to tree biomass and edge effects was found in STM (Fig. 3.3) but there,
elevation was the third most important variable, albeit without an obvious or consistent
pattern of effect.
The partial dependence plots (Fig. 3.4) for BT10 indicated a near-linear
increase in the probability of occurrence of species with increasing tree biomass until
an asymptote is reached at around 300 Mg/ha. The probability of occurrence of forest
species increased with increasing distance from the forest edge up to c. 1000 m, after
which there was no pattern. Species occupancies also declined with an increase in the
percentage
of
degraded
forest
around
the
transects .
Figure 3.3 Distribution of the weighted importance values of environmental variables in primary
forest for the 30 focal species in PGM and STM. NTL: number of times the transect was logged;
NTB: number of times the transect was burned; EdgePS: Average distances to forest edges
(primary forest +secondary forest >10 years); PFD: percentage of forest pixels degraded; TPL:
total number of tree, palm and liana species; UD: understory density; BLL: biomass of leaf litter;
BT10: biomass of trees with circumference >10 cm; BDT: biomass of dead trees; DPC:
deforestation curvature profile; ELEV: Elevation
71
Figure 3.4 Partial dependence plot for the three most important variables from random forest
analysis in Paragominas (top panel) and Santarém (bottom panel). BT10: biomass of trees with
circumference >10 cm. EdgePS: Average distances to forest edges (primary forest +secondary
forest >10 years); PFD: percentage of forest pixels degraded.
72
Figure 3.5 Ranked goodness-of-fit (pseudo-R²) models for each focal species in Paragominas
and Santarém.
We assumed that species with goodness-of-fit higher than 0.4 to be well
modelled using the Random Forest approach (Fig. 3.5) and restricted interpretation of
variable importance to these species. Of the 10 species satisfactorily modelled in PGM
(Fig. 3.6) nine were suboscine passerines: four insectivores (H. rufimarginatus, A.
paraensis, C. cinerascens and and M. ecaudatus), five omnivores (Z. acer, T.
stolzmanni, L. vociferans and S. turdina, Q. purpurata) and one frugivores (P.
menstruus - the only non-passerine). In STM the eleven (Fig. 3.7) satisfactorily
modelled species comprised three insectivores (C. cinerascens, L. galeatus and M.
ecaudatus), four omnivores (P. cayana, S. turdina, L. vociferans and L. melanoleuca,)
and four frugivores (all large-bodied - P. plumbea, P. aracari, A. farinosa and P.
menstrus). Of these 21 species, five species were common to both municipalities: P.
menstruus, C. cinerascens, M. ecaudatus, L. vociferans and S. turdina.
In the region of PGM the species with highest weighted importance values (R²)
for NTL were: S. turdina, P. menstruus and A. paraensis; for NTB: C. cinerascens, M.
ecaudadtus and L. vociferans; for EdgePS: M. ecaudatus, P. menstruus, and L.
vociferans. For PFD were S. turdina A. paraensis and Q. purpurata; for ELEV variable
were A. paraensis, Q. purpurata and M. ecaudatus. For t SLOPE variable were C.
cinerascens, Q. purpurata and L. vociferans; for TPL were, Z. acer, L. vociferans and
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T. stolzmanni; for UD were S. turdina, Z. gracilipes, C. cinerascens, for BLL were H.
rufimarginatus, T. stolzmanni and Z. acer, for BT10 H. rufimarginatus, L. vociferans
and S. turdina, for the BDT were Z. acer, S. turdina and A. paraensis, for clay M.
ecaudatus, Q. purpurata and A.paraensis for pH were T. stolzmanni, L. vociferans
and H. rufimarginatus and finally for DPC were, Z. acer, C. cinerascens and Q.
purpurata.
Figure 3.6 R² weighted importance by species in PGM for each environmental variable NTL:
number of time the transect was logged; NTB: number of time the transect was burned;
EdgePS: Average distances to forest edges (primary forest +secondary forest >10 years); PFD:
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percentage of forest pixels degraded; TPL: total number of tree, palm and liana species; UD:
understory density; BLL: biomass of leaf litter; BT10: biomass of trees with circumference
>10cm; BDT: biomass of dead trees; DPC: deforestation curvature profile, ELEV: Elevation.
In STM the species which presented higher importance value for NTL: L.
melanoleuca, P. menstruus and M. ecaudatus; for the NTB were P. cayana, P. aracari
and M. ecaudatus; for EdgePS: P. aracari, L. vocirerans and L. melanoleuca; for PFD:
L. galeatus; L. vociferans and M. ecaudatus; for the ELEV
were S. turdina, L.
melanoleuca; A. farinosa; for SLOPE were L. melanoleuca, A. farinosa and L. galeatus;
for the TPL were P. aracari, M. ecaudatus and L. vociferans; for the UD were C.
cinerascens, L. vociferans and P. cayana; for the BLL were P. aracari, A. farinosa, and
L. vociferans; for BT10 were L. vociferans, M. ecaudatus and P. cayana; for BDT were
M. ecaudatus and S. turdina; to the Clay variable were S. turdina, P. aracari and P.
cayana; for the pH were P. acaraci, P. menstruus and C. cinerascens; finally for DPC
were C. cinerascens, L. vociferans and P. plumbea.
The cluster heat-map illustrates the overall pattern of relationships between
focal species and environmental variables modelled with RF (Fig. 3.8). There do not
appear to be clear species groupings or a common influence of similar life history
strategies on associations with similar environmental disturbance responses.
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Figure 3.7 R² weighted importance by species in STM for each environmental variable. NTL:
number of time the transect was logged; NTB: number of time the transect was burned;
EdgePS: Average distances to forest edges (primary forest +secondary forest >10 years); PFD:
percentage of forest pixels degraded; TPL: total number of tree, palm and liana species; UD:
understory density; BLL: biomass of leaf litter; BT10: biomass of trees with circumference
>10cm; BDT: biomass of dead trees; DPC: deforestation curvature profile; ELEV: Elevation.
76
Figure 3.8 Cluster heat-map of species with goodness-of-fit ≥ 0.4 after RF modelling for both Paragominas and Santarém. Each cell is coloured based on the
R² weighted values generated by RF. The cluster on the left side of each heat-map groups species with similar response patterns according to their
relationship with different predictor variables. Table legend: F- frugivores, O- omnivore, I- insectivore; Flock: SO- solitary, MF- monospecific flock, FD- flock –
dropout; Strata: M- midstory, C- canopy, U- understory. Environmental variables: NTL: number of time the transect was logged; NTB: number of time the
transect was burned; EdgePS: Average distances to forest edges (primary forest +secondary forest >10 years); PFD: percentage of forest pixels degraded;
TPL: total number of tree, palm and liana species; UD: understory density; BLL: biomass of leaf litter; BT10: biomass of trees with circumference >10cm; BDT:
biomass of dead trees; DPC: deforestation curvature profile; ELEV: Elevation.
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4. Discussion
4.1 Patterns of avian species occupancy
To our knowledge this is the first study examining species-specific responses of
Amazonian forest birds to local, landscape and historical factors across a broad gradient of
human disturbance. Our 30 focal forest species universally declined along the gradient of
human impact and were almost invariably absent from agricultural land-uses. Previously we
had found that 43% and 38% of forest associated-species (e.g. Ramphocelus carbo,
Tangara palmarum and Coereba flaveola) in PGM and STM respectively occurred at least
occasionally in production areas (Moura et al. 2013). However, given our small sample size
of undisturbed forest transects in Paragominas (n = 9) and STM (n = 17) we were unable to
model the most disturbance-sensitive forest species as these were rarely recorded. This bias
towards more disturbance-tolerant forest birds should be remembered in interpreting our
results.
Although all our focal species declined across the full land-use gradient, individual
species responded idiosyncratically to fine-scale patterns of forest disturbance. Those
showing the most rapid decrease in occupancy as the land use was intensified, e.g. A.
paraensis and M. longipennis, were typically insectivorous flock obligate species of the forest
mid and understorey, known to exhibit low tolerance to forest fragmentation and disturbance
(Henriques et al. 2008, Moura et al. 2013). Not all flock-following species responded in this
way however, T. caesius, a nuclear flock leader (Powell 1985) known to be sensitive to
forest disturbance (e.g. Stouffer and Bierregard 1995, Barlow et al. 2002, Lees and Peres
2010), declined less rapidly, indicating a greater resilience to forest disturbance. In logged,
burnt and secondary forests this species typically leads flocks composed of facultative flockfollowers such as Myrmotherula axillaris, Glyphorhynchus spirurus and Xenops minutus
(Powell et al. 2013)
Canopy flocking species such as L. melanoleuca also declined gradually across the
full land-use gradient. Canopy species are known to be more tolerant to the degradation
(Cohn-Haft and Sherry 1994) are well adapted to long distance movements (Karr and James
1975), since the food resources fluctuated and therefore selective logging may be more
detrimental to understorey species owing to micro-climatic changes than canopy species
whose habitat structure is less affected (Wong 1985, Mason and Thiollay 2001). Some
species such as T. aethiops C. cinerascens and L. galeatus exhibited similar patterns of
occupancy in all levels of disturbed primary forest, and this tolerance likely related to their
preference for dense forest understorey or vine tangle habitats which persist or proliferate in
disturbed forests. Some species were more frequently recorded in disturbed primary forests,
principally large-bodied canopy frugivores such as P. plumbea and P. aracari. These species
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are both highly vagile (Lees and Peres 2009) and may benefit from an increase in fruit
production seen in some tree species in once-burned forests (Barlow and Peres 2006b). Not
all species exhibited similar patterns between regions, for instance in PGM P. cayana slowly
decreased in abundance with increasing forest disturbance whilst in STM the opposite was
true. We interpret this difference as potentially being due to a release from competition with
its sister species, the congeneric P. melanogaster (not modelled and absent from PGM),
which was restricted to undisturbed and logged forests. It seems likely that P. cayana is
competitively excluded from less disturbed forest habitats by the canopy-specialist P.
melanogaster (Pearson 1971).
4.2 Species-environment relationships
Overall, we found that distance to forest edge and the biomass of large trees were the
most important variables driving patterns of occupancy of focal species in varyinglydegraded primary forests in our study regions. Edge effects are among the most studied
disturbance types, with proximity to edges typically resulting in marked patterns of species
turnover with increases in gap-specialist species and a loss of forest-interior specialists (e.g.
Terborgh et al. 1990, Laurance 2004). That we were able to uncover evidence for edgeeffects stretching up to 1000 m into forests is further evidence for the pervasive effects of
edges on forest bird distributions. In a remote-sensing investigation of canopy water content
Briant et al. (2010) found that desiccating edge effects may penetrate 1-2.7 km into
fragmented forests. Not all species responded strongly to edges however; medium to largebodied species frugivores (e.g. Psittacids and Ramphastids) are less affected, given their
natural affinity for edges and good gap-crossing ability (Lees et al. 2008, 2009).
Biomass of large trees closely reflects patterns of historical logging frequency and
intensity, with the removal of large emergent tree species altering the canopy structure and
hence understorey micro-climate and vegetative composition (Uhl and Vieira 1989) to the
detriment of specialist understory species, such as Psophia dextralis and P. obscura,
Grallaria varia and Cyphorhinus arada only recorded in undisturbed forests (Moura et al.
2013).
Variation in Amazonian soils can be responsible for the heterogeneity of lowland forest
physiognomies (Tuomisto et al. 1995) with consequences for avian distribution patterns and
community structuring (Bueno et al 2012, Pomara et al. 2012). Soil variables such as clay
content and pH are important determninants of the occurrence of species among primary
forest classes, affecting species with different life strategies, including canopy insectivores
e.g. H. rufimarginatus, midstory omnivores e.g. T. stolzmanni and canopy frugivores e.g. P.
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aracari echoing the results of Cintra and Naka (2012) who also found that clay content
mediated avian community structure in central Amazonia.
We did not uncover any clear patterns of congruence between our environmental
predictor variables and different functional groups (diet, flocking behavior or association with
different forest strata) of our focal species. These divergent responses to the same
environment variables may reflect subtle differences in realized niches that allow microsymaptry between these different species. In addition some species, particularly largebodied birds in STM, were poorly-modelled by our environmental variables, and it is of
course possible that observed occupancy patterns are being driven by similar or different
factors that we did not measure, including biotic interactions such as inter-specific
competition, predation or parasitism (Connel and Orias 1964, Cody 1985, Robinson and
Terborgh 1995).
We were able to model the occurrence of some species much better than others and
given the strong response of some of these to primary forest disturbance, we can
recommend their use as indicator species of good-quality forest habitat. Example indicator
species include H. rufimarginatus (R² = 0.4 in PGM), M. ecaudatus (R² = 0.7 and 0.4 in PGM
and STM respectively), S. turdina (R² = 0.6 and 0.5 in PGM and STM respectively) and L.
vociferans (R² = 0.6 and 0.7 in PGM and STM respectively). The fact that L. vociferans, a
mid-storey omnivore, was well-modelled in both regions responding strongly to edge effects,
as well as differences in tree species richness and biomass and understory density is
particularly notable given that this species is one of the loudest birds on Earth (Nemeth
2004) and thus may make an easily-detectable proxy for forest-quality based on its
dependence affinity for forests with high basal area and edge avoidance. That suboscine
passerines were better-modelled than most other phylogenetic groups again reinforces their
importance as study systems in ecological enquiries (Tobias et al. 2013).
5.
Conclusions
This study offers a set of more nuanced insights as to the effects of land-use change
and forest disturbance on a tropical forest avian bird community than is possible from typical
community-wide studies. We found that many focal species were highly sensitive to humanmodification of their forest habitats, with only two species using agricultural areas. We
uncovered a remarkably diverse set of species responses to individual environmental
variables although the basal area of large trees and distance to forest edges were shown to
be consistently important. Our study highlights the ubiquity of species-specific responses to
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habitat degradation and indicates the extent to which highly divergent disturbance response
signatures may be masked by community studies.
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Capítulo 4
Two hundred years of local avian extinctions in Eastern Amazonia
Publicado como: Moura, N. G., Lees, A. C., Aleixo, A., Barlow, J. Dantas, S. M., Ferreira, J.,
Lima, M. F. C., and Gardner, T. A. 2014. Two hundred years of local avian extinctions in
Eastern Amazonia. Conservation Biology. In press.
Abstract
Local, regional, and global extinctions caused by habitat loss, degradation, and
fragmentation have been widely reported for the tropics. The patterns and drivers of this loss
of species are now increasingly well known in Amazonia, but there remains a significant gap
in understanding of long-term trends in species persistence and extinction in anthropogenic
landscapes. Such a historical perspective is critical for understanding the status and trends
of extant biodiversity as well as for identifying priorities to halt further losses. We searched
for evidence of local extinctions of a terra firma rainforest avifauna over 200 years in a 2,500
km² eastern Amazonian region around the Brazilian city of Belém using extensive historical
data sets of specimen records and contemporary surveys. This region has the longest
history of ornithological fieldwork in the entire Amazon basin and lies in the highly-threatened
Belém Centre of Endemism. We also compared our historically inferred extinction events
with extensive data on species occurrence in a sample of catchments in a nearby
municipality (Paragominas) that encompass a gradient of past forest loss. We found
evidence for the possible extinction of 47 species (14% of the regional species pool) that
were unreported from 1980 to 2013 (80% last recorded between 1900 and 1980).
Seventeen species appear in the red list of the International Union for Nature Conservation
(IUCN), many of which are large-bodied species. The species lost from the region
immediately around Belém are similar to those which are currently restricted to well-forested
catchments in Paragominas. Although we anticipate the future rediscovery or recolonization
of some species inferred to be extinct by our calculations, we also expect that there are likely
to be additional local extinctions, not reported here, given the on-going loss and degradation
of remaining areas of native vegetation across eastern Amazonia.
Keywords: sighting record, colonization, forest dependency, urban conservation, IUCN Red
List, avifauna
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1.
Introduction
Determining if and when a species becomes locally, regionally, or globally extinct is
never easy because the rarer a species gets, the more difficult it is to find and study. The
ecological literature contains many cases whereby species once considered extinct have
been rediscovered decades or even centuries later (e.g. Crowley et al. 2011). Such cases
indicate the necessity for thorough field surveys before declaring a species to be extinct (e.g.
Butchart et al. 2006). These problems are most severe in the tropics, where biodiversity is
richest, extinction (and rediscovery) rates are highest (Costello et al. 2013), and land-use
change is currently most acute (e.g. Sodhi et al. 2004). Furthermore, a persistent lack of
time-series data means that estimating extinction risk is often only possible through a spacefor-time substitution. For example, one might compare current species persistence in heavily
forested areas with patterns of persistence in adjacent recently deforested areas (Pickett
1989). However, it is possible that many short-term studies may not be able to capture longterm patterns of species survival because extinction debts may be paid over a very long
period for species with long generation times and insulation from real-world threats (in
experimental landscapes or over short periods), such as hunting and trapping, may lead to
underestimates of extinction risk (e.g. Peres et al. 2010). Thus, understanding what
constitutes the baseline of biodiversity prior to recent large-scale landscape change and
resource extraction by humans is fraught with difficultly for many parts of the world.
One of the most robust approaches to estimating past extinctions and current
extinction risk is to combine data from current field surveys with historical data from museum
specimens (e.g. Kattan et al. 1994, Patten et al. 2010). This powerful approach is only
possible for regions of the world where extensive natural history fieldwork has been
conducted over long periods. Here, we present such a case study for the region around the
city of Belém, the longest-studied area of the entire Amazon basin.
Amazonia is subject to the highest absolute rates of loss of tropical forest on the
planet (Hansen et al. 2013). Despite substantial reductions in deforestation rates in the
Brazilian Amazon during the last decade (INPE 2013), this loss and fragmentation of forests
threaten many species with global extinction (e.g. Bird et al. 2011). Local extinctions caused
by habitat loss, fragmentation, and disturbance from fire and logging are relatively well
studied in Amazonia (Peres et al. 2010), and the longest-running study, the Biological
Dynamics of Forest Fragments Project, dates back only to 1979 (Laurence et al. 2011).
Thus, a major knowledge gap relating to the conservation of Amazonian biota is an
understanding of long-term trends in species persistence and extinction in the humanmodified landscapes that increasingly characterize the region.
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Arguably the most threatened region of Amazonia is the 243,000 km² Belém Center
of Endemism (BCE) in northeastern Pará and western Maranhão states. This area has the
longest history and highest proportion of forest loss of any Amazonian interfluve and retains
24% of its original primary forest cover (Almeida and Vieira 2010). Most of this remaining
forest is heavily fragmented and degraded by recurrent selective-logging and fire events, as
well as over-extraction of game animals and other non-timber forest resources (Almeida and
Vieira 2010, Amaral et al. 2012). Although 11 of the 160 threatened avian taxa on the
current Brazilian Red List are strictly Amazonian, 10 of these are restricted to the BCE
(Machado et al. 2008). A further 12 species occurring in but not necessarily restricted to the
BCE are also considered globally threatened (IUCN 2013), of which 7 do not appear on the
Brazilian Red List (Machado et al. 2008). Quantitative data on the responses to land-use
change and persistence in fragmented landscapes for many of these threatened taxa are
generally lacking (Portes et al. 2011).
The state capital Belém (Belém do Grão Pará) was founded by the Portuguese in
1616 and by 1752 was already a hub of Amazonian biodiversity research (Teixeira et al.
2010). Many renowned naturalists (including Henry Walter Bates, Alfred Russel Wallace,
and Johann Baptist von Spix among others) collected thousands of bird (among other)
specimens that were deposited in museums across the world (Novaes and Lima 2009). This
wealth of specimen data has, until now, been untapped for use in conservation research, yet
offers invaluable insights into the history of local avifaunal extinctions in this unique corner of
Amazonia (e.g. Burgman et al. 1995).
In stark contrast to most of Amazonia, where
substantial forest losses have only occurred in the last fifty years, the Metropolitan region of
Belém (MRB) was already heavily deforested and defaunated more than a century ago
(Vieira et al. 2007).
Our goal was thus to investigate long-term trends in local extinction and persistence
of Amazonian birds in a highly fragmented and degraded forest region (MRB) that
characterizes the BCE. We searched for evidence of local extinctions from 1812 to 1980 in
the MRB by examining museum records and estimating the persistence probabilities and
likely extinction dates for species unrecorded since 1980. We compared these historical data
with field data on local extinctions from the most extensively forested region left in the BCE the municipality of Paragominas, which was subject to a recent exhaustive biodiversity
inventory (Lees et al. 2012, Gardner et al. 2013, Moura et al. 2013). We then determined if
current patterns of threat recognized at the regional, national, and international levels agreed
with our findings of which species were most threatened with extinction in both our historical
and contemporary data sets.
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2.
Methods
2.1 Study site
The 2,537 km² MRB (~1ºS, 48º'W, Fig. 4.1), a conurbation of 2.2 million people, is in
northeastern Brazil at the mouth of the Guamá River in Pará state and is divided into 6
municipalities: Belém, Ananindeua, Marituba, Benevides, Santa Isabel, and Santa Bárbara
do Pará. Local soils are typically deep oxisoils, well-drained with low natural fertility, and the
natural climax vegetation is dense ombrophilous terra firma and várzea (seasonally flooded)
forests (Novaes and Lima 2009).
The regional climate is classified as Af following the Köppen terminology; hot with
annual mean temperatures ranging from 23 to 31°C and very humid with mean relative air
humidity is 80%. There is no pronounced dry season, although it rains less between June
and November with mean annual precipitation ranging from 2,500 to 3,000 mm (Novaes and
Lima 2009).
Figure 4.1 Map indicating the position of the study regions MRB and Paragominas in Brazil (a) and
the state of Pará (b); extent of remaining forest cover in the MRB (forest as dark pixels, urban and
agricultural areas in white) (c) and one of two specimens of Rufous-rumped Foliage-gleaner (Philydor
85
erythrocercum) collected by Sir Alfred Russel Wallace at ‘Pará’ (old name for Belém) in May 1849 and
deposited at the Natural History Museum, Tring, England (A. C. Lees © Natural History Museum,
Tring) (d). This latter species was last reported in the MRB in 1965, but according to the Solow
2
calculations is potentially still extant. It is most likely to persist in the 6,367 km Refúgio de Vida
Silvestre Metrópole da Amazônia, the largest area of contiguous primary forest left in the MRB.
Since its founding on 12 January 1616 the city and its environs have undergone over
4 centuries of forest loss and degradation, catalyzed by the construction of the Estrada Real
from 1616 onwards, a highway that connects Belém to São Luís in Maranhão state, and later
associated with the construction of the Bragança railway, between 1883-1908 aimed at
developing eastern Pará (Vieira et al. 2007). Present day forest cover in the MRB is
approximately 43.5% of the original pre-Columbian extent (INPE 2013). There are 6
protected areas (6,399 km2), most of which are severely degraded due to on-going
disturbance events such as fire, selective-logging, and illegal hunting (Leão et al. 2007).
2.2 Data collection
Novaes and Lima (2009) list 490 bird species for the MRB, of which 329 (67%) are
present in unflooded terra firma forest. We compiled a baseline list of those species reliably
recorded in the region and represented either by specimen records or archived documented
observations (voucher images or sound recordings). The principle source of specimen data
came from digitized records of study skins deposited at the Museu Paraense Emílio Goeldi
(MPEG) and from 9 North American institutions with data from the MRB archived on the
ORNIS database (www.ornisnet.org/). The databases of many avian collections are
undigitized, so we also conducted an exhaustive search of secondary sources to locate
additional historical records (e.g. Sclater and Salvin 1867, Hellmayr 1905, Stone 1928) from
which we extracted collection dates directly or used to direct targeted visits to other
collections (e.g. the Natural History Museum at Tring). To ascertain the contemporary
presence of species in the region, in addition to specimen data we also accepted digital
voucher images and sound recordings.
Through the compilation of data from multiple sources, we compiled a sighting record
for each species. Data sources :North American Institutions with specimen data for the MRB
housed on the ORNIS site are as follows: Museum of Comparative Zoology (MCZ),
American Museum of Natural History (AMNH), California Academy of Sciences (CAS),
Cornell University-Museum of Vertebrates (CUMV), Field Museum of Natural History
(FMNH), Los Angeles County Museum of Natural History (LACM), University of Nebraska
State Museum (USNM), Royal Ontario Museum (ROM), University of Michigan, Museum of
Zoology (UMMZ ). Collecting localities were located using Paynter and Traylor (1991). We
86
also searched for images archived on the Brazilian avian photo data base WikiAves
(http:www.wikiaves.com.br), sound-recordings deposited on the global avian soundrecording database xeno-canto (http://www.xeno-canto.org/) and records from recent
surveys conducted by ornithologists based at the MPEG.
2.3 Data analyses
We considered 1980 the cut-off year for analysis. Species unrecorded since 1980
were candidates for local extinction because the last really rigorous inventories were finished
in the 1970s (e.g. Lovejoy 1971, Novaes 1973).To infer extinction dates, we used the
formulas of Solow (1993, 2005). These formulas assume a uniform distribution of sightings
(non-stationary Poisson, which also assumes the records are independent). We organized
the records as t1<t2<…<tn, where n represents the number of times a species was sighted
during the study period, ordered from the earliest to latest, starting with t 1= 0. To determine if
a species was likely to be extinct, we used the formula p = (tn/T) n-1, where T is the difference
between the first sighting and the target year 2013 (which is the endpoint of the study period
that corresponds to the present time). If p<0.05, then the species was considered likely to be
extinct (Solow 1993, 2005). We used the following equation to estimate extinction dates: T̂E
= (n+1/n)tn , where the expected year of extinction is T̂E and the first record is t1 (for species
with at least 4 independent records). The confidence interval for T̂E was calculated as TEU =
tn/α1/n, where α = 0.05.
Because the Solow equation is heavily dependent on the initial number of sightings
(tn), calculating the sighting rate (sensu McInerny et al. 2006) is also useful because it allows
for greater comparability between taxa if there is disparity in the period of initial sighting or
discovery. The sighting rate is calculated with p = (1-(n/tn)(T-tn)). We present both measures
for greater confidence in our inferred candidates for extinction.
To assess the generality of extinction patterns, we compared them with the results of
a 2010-2011 survey investigating patterns of avian persistence in 18 catchments (of
approximately 5,000 ha) in the municipality of Paragominas (2° S, 47° W), which is 307 km
south of the MRB and has a baseline avifauna that is nearly identical to that of the MRB
(Lees et al. 2012, Gardner et al. 2013). The 18 catchments studied were delineated using a
digital elevation model and SWAT (Soil and Water Assessment Tool) for ARCGIS 9.3 and
represented a gradient of accumulated forest loss (based on classified 2010 Landsat images
[Gardner et al. 2013]) from 94% (6% remaining primary forest cover) to 0% (100% forest
cover). Between 7 and 12 (300 m) transects were stratified (forest, non-forest) across each
87
catchment. Three point count stations were allocated to each transect (see Lees et al. [2012]
and Gardner et al. [2013] for more details on experimental design and avian survey
protocols).
We compiled a list of avian taxa classified as threatened on the state (Pará) (Aleixo
2006), national (Brazilian) (Machado et al. 2008), and international (IUCN) red lists (IUCN
2013) (evaluations at the state and national level also considered taxa below the species
level, in some cases pending taxonomic upgrades) currently or historically occurring in the
MRB. We then compared all species that we inferred to be extinct in the MRB and all
species listed as threatened on state, national, and international lists with the total number of
records, catchment occupancy, land-use breadth (number of land uses sampled from
primary and secondary forest, pasture, silviculture, and mechanized agriculture), and the
minimum percentage of forest cover within each occupied catchment in Paragominas. To
assess potential traits of birds vulnerable to local extinction, we compared the threats
compiled for each species and species’ life history attributes, such as mass and forest
dependency, by Birdlife International (2013). Finally, we adapted the framework of Butchart
et al. (2006) and used it to assess the conservation status of species either already listed or
deemed to be regionally threatened based on our analyses of species persistence in the
MRB. For species last recorded quite recently there needs to be greater confidence that the
last individual has died in order for the species to be considered extinct.
3. Results
3.1 Possible extinctions in the MRB
We traced 10,147 specimens of 329 terra firma species from 8 collections from which
we were able to construct a sighting record. These indicated that 47 terra firma species
(14%) were unrecorded in the MRB over the last 33 years, a loss of 0.28 species/year.
Probable extinctions were inferred to have occurred over the course of the entire period
1800-2000. However, more occurred in the 20 th century; 80% of candidate extinctions were
recorded between 1900 and 1980 (Table 4.1). In addition we infer the undocumented
'Centinelan' sensu Wilson (1992) extinctions of the following species from the region Gray
Tinamou Tinamus tao, Bare-faced Currasow Crax fasciolata pinima, Crested Eagle
Morphnus guianensis and Variegated Antpitta Grallaria varia which likely occurred in the
region but were never recorded by ornithologists. Gray Tinamou was historically collected
along the rio Capim to the south of the region (Griscom and Greenway 1941) as was the
Bare-faced Currasow (Goeldi 1903) and both are extremely vulnerable to local extinction
because of hunting. The currasow is now on the brink of global extinction (Lees et al. 2012).
88
Crested Eagles occur throughout the Neotropics and have been recorded 18 km south of
Belém at Barcarena (Vilar 2013) and in forest remnants around Tailândia (Silveira 2006)
where Variegated Antpittas have also been recorded, both there and at other sites in the
BCE (Portes et al. 2011, Lees et al. 2012). We excluded three unvouchered terra firme
species listed in Novaes and Lima (2009) from our analysis; White Bellbird Procnias albus,
Chestnut-fronted Macaw Ara severus and Bar-breasted Piculet Picumnus aurifrons which we
deem biogeographically unlikely to occur in the region and are not represented by voucher
documentary material (specimens, photographs, sound-recordings).
We were able to estimate extinction probabilities for 26 (for which number of records
was ≥ 4). Ten species were considered likely to be extinct based on the Solow equation;
extinction dates ranged from 1918 to 1978 (95% confidence intervals between 1952 and
2004, Fig. 4.2), and 16 species were presumed to be still extant. Of the 21 species for which
it was not possible to calculate the extinction probability, 9 were unrecorded after 1900. We
were reasonably confident that these species have become locally extinct (Fig. 4.2) because
all are susceptible to local extinction following habitat loss and hunting (e.g. Peres et al.
2000) and all are large-bodied (> 350 g) easy to survey species which are very unlikely to
have remained undetected for over a century. The sighting rate calculations for 26 species
suggested that 17 species were likely to be extinct in the MRB, including 8 species that were
highly likely to be extant based on the Solow equation (Table 4.1).
89
Table 4.1 Species unrecorded in the last 33 years in the Metropolitan region of Belém.
Scientific name
a
English common name
Last record
b
n
c
tn
d
T
e
Solow
Estimated
extinction year
Upper
95%
bound
Sighting rate Mean weight (g)
Penelope pileata
White-crested Guan
1870
2
-
-
-
-
-
-
1260
Aburria cujubi
Red-throated Piping-Guan
1835
1
-
-
-
-
-
-
1407
Pauxi tuberosa
Razor-billed Curassow
1959
6
124
178
0.164
-
-
0.108
2813
Odontophorus gujanensis
Marbled Wood-Quail
1906
7
71
178
0.004
1918
1952
0.991
314
Sarcoramphus papa
King Vulture
1898
1
-
-
-
-
-
-
3337
Accipiter poliogaster
Gray-bellied Hawk
1915
3
-
-
-
-
-
-
420
Accipter superciliosus
Tiny Hawk
1968
6
133
178
0.233
-
-
0.178
104
Harpia harpyja
Harpy Eagle
1894
2
-
-
-
-
-
-
6550
Spizaetus melanoleucus
Black-and-white Hawk-Eagle
1962
1
-
-
-
-
-
-
751
Spizaetus ornatus
Ornate Hawk-Eagle
1812
1
-
-
-
-
-
-
1215
Daptrius ater
Black Caracara
1848
1
-
-
-
-
-
-
352
Micrastur mirandollei
Slaty-backed Forest-Falcon
1835
1
-
-
-
-
-
-
517
Micrastur semitorquatus
Collared Forest-Falcon
1968
2
-
-
-
-
-
-
631
Psophia obscura
Anodorhynchus
hyacinthinus
Dark-winged Trumpeter
1922
9
87
178
0.003
1931
1956
0.000
1071
Hyacinth Macaw
1812
1
-
-
-
-
-
-
1565
Ara macao
Scarlet Macaw
1900
4
88
201
0.084
-
-
0.020
1245
Ara chloropterus
Red-and-green Macaw
1906
6
94
104
0.523
-
-
0.491
1479
Guarouba guarouba
Golden Parakeet
1848
3
-
-
-
-
-
-
260
Pyrrhura lepida
Pearly Parakeet
1968
4
156
201
0.468
-
-
0.417
75
Touit huetii
Scarlet-shouldered Parrotlet
1969
4
71
115
0.235
-
-
0.150
60
Deroptyus accipitrinus
Red-fan Parrot
1912
4
100
201
0.123
-
-
0.046
255
Neomorphus geoffroyi
Rufous-vented Ground-Cuckoo
1912
4
100
201
0.123
-
-
0.046
363
Lophornis gouldii
Dot-eared Coquette
1967
9
55
101
0.008
1974
1992
0.001
2
Calliphlox amethystina
Amethyst Woodstar
1926
1
-
-
-
-
-
-
2
Piculus chrysochloros
Golden-green Woodpecker
1963
6
62
112
0.052
-
-
0.015
66
90
Scientific name
a
English common name
Last record
b
n
c
tn
d
T
e
Solow
Estimated
extinction year
Upper
95%
bound
Sighting rate Mean weight (g)
Celeus torquatus
Ringed Woodpecker
1968
1
-
-
-
-
-
-
124
Hylopezus macularius
Spotted Antpitta
1968
6
133
178
0.233
-
-
0.178
40
Sclerurus caudacutus
Black-tailed Leaftosser
1967
5
42
88
0.052
-
-
0.010
38
Sclerurus rufigularis
Short-billed Leaftosser
1972
18
60
101
0.000
1976
1984
0.000
22
Dendrocincla merula
White-chinned Woodcreeper
1968
6
5
50
0.00
1969
1972
0.00
53
Deconychura longicauda
Long-tailed Woodcreeper
1968
3
-
-
-
-
-
-
26
Dendroxestastes rufigula
Cinnamon-throated Woodcreeper
1936
1
-
-
-
-
-
-
70
Berlespchia rikeri
Point-tailed Palmcreeper
1935
4
34
112
0.028
1946
1993
0.001
35
Philydor ruficaudatum
Rufous-tailed Foliage-gleaner
1968
1
-
-
-
-
-
-
27
Philydor erythrocercum
Rufous-rumped Foliage-gleaner
1965
6
86
134
0.109
-
-
0.000
25
Myiobius atricaudus
Black-tailed Flycatcher
1968
6
96
141
0.146
-
-
0.090
10
Phoenicircus carnifex
Guianan Red-Cotinga
1930
10
72
95
0.083
-
-
0.046
84
Gymnoderus foetidus
Bare-necked Fruitcrow
1912
1
-
-
-
-
-
-
283
Platyrinchus platyrhynchos
White-crested Spadebill
1968
9
56
101
0.009
1975
1993
0.001
13
Platyrinchus saturatus
Cinnamon-crested Spadebill
1972
12
60
101
0.003
1977
1981
0.000
13
Piprites chloris
Wing-barred Piprites
1965
2
-
-
-
-
-
-
19
Corythopis torquatus
Ringed Antpipit
1972
11
124
165
0.057
-
-
0.032
17
Hylophilus ochraceiceps
Tawny-crowned Greenlet
1969
8
66
110
0.028
1978
2004
0.007
15
1965
8
130
178
0.111
-
-
0.070
35
Dacnis lineata
Black-faced Dacnis
1926
6
47
134
0.005
1935
1965
0.000
11
Periporphyrus erythromelas
Red-and-black Grosbeak
1905
1
-
-
-
-
-
-
48
Euphonia minuta
White-vented Euphonia
1960
3
-
-
-
-
-
-
9
a
Our taxonomy follows the checklist of Brazilian birds compiled by the Comitê Brasileiro de Registros Ornitológicos (CBRO 2011).
Number of records.
c
The interval between the first and last record.
d
The time interval between the year of the first sighting and the target year (2013).
e
The p values shown are based on the Solow equation (Solow 1993, 2005).
b
91
Figure 4.2 Last record, extinction date (year), and confidence intervals for 47 species unrecorded in
the Metropolitan region of Belém, Brazil, after 1980 (gray squares, last record of species presumed
extinct but for which there are insufficient records to use the Solow equation (n<4); white triangles,
last record for species considered extant based on Solow equation; black circles, date of last record
for species considered extinct based on Solow equation; white circles, extinction date inferred based
on Solow equation; semi-filled diamond, species extant based on Solow equation and extinct based
on sighting rate; semi-filled circle, species extinct based on Solow equation and extant based on
sighting rate; crosses, 95% confidence interval for extinct species based on Solow equation).
92
3.2 Forest dependency of threatened species
In comparing our historical analysis with contemporary avian surveys in the
municipality of Paragominas, we found that 6 species recorded as extinct (since 1980) in the
MRB were also unrecorded in Paragominas. Thirty-nine species considered extinct in the
MRB persisted in Paragominas, although 6 of these are likely to be rare given that they were
not recorded during our comprehensive 2010 survey and reported only by Portes et al.
(2011). Ten of 11 threatened (from any list) species that were still extant in the MRB were
also recorded in Paragominas (Table 4.2).
Forest dependency of individual threatened or extinct species in Paragominas
(measured as the minimum percentage forest cover at the catchment scale from which a
species was recorded) ranged from 34% to 100%; the number of catchments occupied
ranged from 1 to 15 (of 18 catchments surveyed). The number of catchments occupied in
Paragominas and the date of the last record in the MRB were weakly and positively related
(Fig. 4.3, non-linear exponential model r² = 0.16; p<0.05). Species recorded in fewer
catchments were more susceptible to local extinction (last recorded longer ago). Among the
47 species with a high extinction probability in the MRB, 9 were recorded once in
Paragominas, indicating parallel patterns of rarity. However, this was not the case for all
species. For example, the Red-billed Pied Tanager (Lamprospiza melanoleuca) was
recorded on 37 occasions from 12 catchments in Paragominas (Table 4.2).
Figure 4.3 Relationship between inferred extinction date in the Metropolitan region of Belém and
occupancy of catchments in Paragominas, Brazil (r² = 0.16, p < 0.05).
93
3.3 Reassessment of species threat status
Seventeen (36%) of the 47 species unrecorded since 1980 are categorized as
threatened; 12 of these species are on the Pará list, 6 are on the Brazilian list, and 12 are on
the IUCN list (Table 4.2). Ten species listed as regionally threatened are still extant in the
MRB (Table 4.2). All 47 species we considered to have a high probability of extinction in the
MRB, together with the species currently considered to be endangered in Pará (12 species),
are threatened by habitat loss, degradation, and fragmentation, and 19 of these species
were only recorded from primary forests in Paragominas, of which 3 species were found
exclusively in remnant fragments of undisturbed forests (Dark-winged Trumpeter [Psophia
obscura], Guianan Red-Cotinga [Phoenicircus carnifex], and Tawny-crowned Greenlet
[Hylophilus ochraceiceps rubrifrons]). Fifteen species occupied both primary and secondary
forest and 3 - Scarlet Macaw, Red-and-green Macaw and Golden Parakeet were also
recorded in non-forest (agricultural) areas (Fig. 4. 2). Of the species considered threatened
in Pará, only Black-spotted Bare-eye (Phlegopsis nigromaculata paraensis) was restricted to
primary forest around Paragominas (although it occurs in old secondary forests [>50 years]
elsewhere in the MRB). Nine other species were also recorded in secondary forests, and 4
species considered likely to be extinct in the MRB and listed as endangered on the IUCN list
were also threatened by hunting and the wild bird trade. Seven of the 10 species last
recorded before 1900 were either large-bodied (>1 kg) game birds, raptors, or psittacids of
high commercial value (Table 4.2).
94
Table 4.2 Principle threats and Red List evaluations of threatened taxa at the State (Pará), national (Brazil) and global (IUCN) level and status of of the
species in the MRB and Paragominas.
Species
English name
Species
persistence
a
in the MRB
Species
persistence in
Paragominas
b
(PGM)
Low total
cover(%)
No. of
catchments
with records
in PGM
Number of
records from
PGM
Habitat
types
occupied
in PGM
Pará
Red
List
Brazilian
Red List
IUCN
Principle
Red List threats
Penelope pileata
White-crested Guan
0
1
92
1
2
2,4
LC
LC
VU
1, 2
Aburria cujubi
Red-throated PipingGuan
0
1
56
2
1
2
LC
LC
LC
1, 2
Pauxi tuberosum
Razor-billed Curassow
0
1
73
3
7
1,2,5
LC
LC
LC
1, 2
Odontophorus gujanensis
Marbled Wood-Quail
0
1
56
4
5
2
LC
LC
NT
1, 2
Sarcoramphus papa
King Vulture
0
1
72
2
1
2,6
LC
LC
LC
1, 2
Accipiter poliogaster
Gray-bellied Hawk
0
0
-
-
-
-
LC
LC
LC
1, 2
Accipter superciliosus
Tiny Hawk
0
0*
-
-
-
-
LC
LC
LC
1, 2
Harpia harpyja
Harpy Egle
0
0*
-
-
-
-
LC
LC
NT
1, 2
Spizaetus melanoleucus
Black-and-white HawkEagle
0
1
76
1
1
5
LC
LC
LC
1, 2
Spizaetus ornatus
Ornate Hawk-Eagle
0
1
92
1
1
-
NT
LC
NT
1, 2
Daptrius ater
Black Caracara
0
1
58
1
1
-
LC
LC
LC
1, 2
Slaty-backed ForestFalcon
0
1
63
1
1
-
LC
LC
LC
2
Psophia obscura
Dark-winged Trumpeter
0
1
100
1
1
1
End
End
End
1, 2
Collared Forest-Falcon
0
1
63
2
2
4
LC
LC
LC
2
Anodorhynchus
hyacinthinus
Hyacinth Macaw
0
0
-
-
-
-
VU
VU
1,2,3
Ara macao
Scarlet Macaw
0
1
51
10
16
3,4,5,6
LC
LC
LC
1,2,3
Ara chloropterus
Red-and-green Macaw
0
1
56
9
21
2,4,6
LC
LC
LC
1,2,3
Guarouba guarouba
Golden Parakeet
0
1
51
13
41
1,2,4,5,6,7
VU
VU
End
1,2,3
Pyrrhura lepida
Pearly Parakeet
0
1
56
9
28
1,2,4,5
End
End
VU
1,2,3
Pyrilia vulturina
Vulturine Parrot
1
0*
-
-
-
-
LC
LC
VU
1,2,3
Touit huetii
Scarlet-shouldered
Parrotlet
0
0
-
-
-
-
LC
LC
VU
1,2,3
VU
95
Species
English name
Species
persistence
a
in the MRB
Species
persistence in
Paragominas
b
(PGM)
Low total
cover(%)
No. of
catchments
with records
in PGM
Number of
records from
PGM
Habitat
types
occupied
in PGM
Pará
Red
List
Brazilian
Red List
IUCN
Principle
Red List threats
Pionites leucogaster
White-bellied Parrot
1
1
34
13
23
1,2,4
LC
LC
VU
1,2,3
Red-fan Parrot
0
1
51
11
19
2,4
LC
LC
LC
1,2,3
Neomorphus geoffroyi
Rufous-vented GroundCuckoo
0
0*
-
-
-
-
LC
LC
LC
2, 4
Threnetes leucurus
Pale-tailed Barbthroat
1
0
-
-
-
-
End
LC
LC
2
Lophornis gouldii
Dot-eared Coquette
0
0*
-
-
-
-
LC
LC
VU
2
Amethyst Woodstar
0
1
57
4
5
2,4,6
LC
LC
LC
2
Pteroglossus bitorquatus
Red-necked Aracari
1
1
51
10
22
1,2,4,5
VU
LC
NT
2
Celeus torquatus
Ringed Woodpecker
0
0
-
-
-
-
End
LC
LC
24
0
0
-
-
-
-
VU
LC
LC
24
1
1
34
15
99
1,2,4,5
VU
LC
LC
2,4
Piculus chrysochloros
Golden-green
Woodpecker
White-shouldered
Antshrike
Phlegopsis nigromaculata
Black-spotted Bare-eye
1
1
51
6
8
1,2,4
End
LC
LC
2, 4
Hylopezus macularius
Spotted Antpitta
0
1
80
2
2
1,4
LC
LC
LC
2, 4
Black-tailed Leaftosser
0
1
72
5
12
1,2,4,5
LC
LC
Short-billed Leaftosser
0
1
70
1
1
2
LC
LC
LC
2, 4
Dendroxestastes rufigula
Cinnamon-throated
Woodcreeper
0
1
56
5
8
2,4
End
End
LC
2,4
Deconychura longicauda
Long-tailed Woodcreeper
0
1
55
4
4
2,4
VU
LC
NT
2,4
1
1
63
6
6
2,4,5
End
End
LC
2,4
1
1
55
10
24
1,2,4,5
End
LC
LC
2,4
1
1
55
11
19
2,3,4,5
End
LC
LC
2,4
0
0
-
-
-
-
LC
LC
LC
2,4
0
1
63
7
8
1,2,3
LC
LC
LC
24
Dendrocincla merula
Dendrocolaptes certhia
Synallaxis rutilans
Berlespchia rikeri
White-chinned
Woodcreeper
Amazonian BarredWoodcreeper
Ruddy Spinetail
Cinnamon-throated
Woodcreeper
Rufous-tailed Foliagegleaner
LC
2, 4
2,4
Rufous-rumped Foliagegleaner
0
1
68
7
24
1,2,3
LC
LC
LC
96
Species
English name
Species
persistence
a
in the MRB
Species
persistence in
Paragominas
b
(PGM)
Low total
cover(%)
No. of
catchments
with records
in PGM
Number of
records from
PGM
Habitat
types
occupied
in PGM
Pará
Red
List
Brazilian
Red List
IUCN
Principle
Red List threats
Lepidothrix iris
Opal-crowned Manakin
1
1
63
2
2
1,2
LC
LC
VU
2,4
Myiobius atricaudus
Black-tailed Flycatcher
0
0
-
-
-
-
LC
LC
LC
2,4
Gymnoderus foetidus
Bare-necked Fruitcrow
0
0
-
-
-
-
LC
LC
LC
2,4
Guianan Red-Cotinga
0
1
100
1
1
1
LC
LC
LC
2,4
Tolmomyias assimilis
Yellow-margined
Flycatcher
1
1
34
14
47
1,2,4,5
End
LC
LC
2,4
Xipholena lamellipenis
White-tailed Cotinga
1
1
69
6
19
1,2,3,5
LC
LC
NT
2,4
Platyrinchus platyrhynchos
White-crested Spadebill
0
1
55
4
14
1,2,3
LC
LC
LC
2,4
Golden-crowned
Spadebill
0
1
55
4
4
2
LC
LC
LC
2,4
Piprites chloris
Wing-barred Piprites
0
1
56
9
34
1,2,4,5
VU
LC
LC
2,4
Ringed Antpipit
0
1
72
3
8
1,2,5
LC
LC
LC
2,4
Hylophilus ochraceiceps
Tawny-crowned Greenlet
0
1
100
1
5
1
LC
LC
2,4
0
1
56
12
37
1,2,4,5
LC
LC
LC
2,4
Dacnis lineata
Black-faced Dacnis
0
0*
-
-
-
-
LC
LC
LC
24
Periporphyrus
erythromelas
Red-and-black Grosbeak
0
1
72
4
6
1,2
LC
LC
NT
2,4
Euphonia minuta
White-vented Euphonia
0
1
-
-
-
-
LC
LC
LC
2,4
LC
† Evaluated at the subspecies level.
a
0 = extinct; 1 = extant
b
0 = not recorded by Lees et al. (2012), if marked with an asterisk then recorded by Portes et al. 2011; 1 = recorded by Lees et al. (2012)
c
Habitat types: 1Undisturbed; 2 Logged; 3 Burned; 4 Logged & burned; 5 Secondary forest; 6 Pasture; 7 Plantations; 8 Mechanized agriculture.
97
A combined analysis of sighting records, threat status, and estimates of the ease of
detection revealed 16 extinct species for which we are very confident of local extinction, 19
probably extinct species and 13 possibly extinct species for which we have lower confidence
in their extinction (Fig. 4.4).
Figure 4.4 Schematic of framework illustrating how time since last record interacts with confidence of
extinction (bold, globally threatened species [IUCN 2013]; asterisk, included on the regional red list).
The framework can be used to determine how species can be classified locally as possibly extinct,
probably extinct or extinct (adapted from Butchart et al. [2006]).
4.
Discussion
We found evidence for the possible local extinction of 47 terra firma species in the
MRB since 1812, all of which remained undetected from 1980 to 2013. Gradual local and
regional extinctions have been reported throughout the Neotropics (Table 4.3), but we
conducted the first study illustrating the long-term (>160 years) erosion of an Amazonian bird
community. Rate of loss was estimated at 0.28 species/year in the MRB. By comparison,
Robinson et al. (2001) found that Barro Colorado Island, Panama, lost 13.5% of its avifauna
in 25 years (1.1 species extinction/year) and Patten et al. (2010) found that Palenque,
Mexico, lost 9.5% of its avifauna in 109 years (0.21 extinctions/year).
98
Table 4.3 Long term species loss from Neotropical forest regions
Number of extinct
species, total species
richness, community
regionally extinct (%)
47, 360, 14.5
12, 122, 9.8
23, 240, 9.5
27, 200, 13.5
Study
Region
Biome
Period (years), No.
years
Species loss/
year
This study
Shaw et al. 2013
Patten et al. 2010
Robinson et al. 2001
Metropolitan region of Belém, Pará, Brazil
Sierra de Los Tuxtlas, Veracruz, Mexico
Palenque, Chiapas, Mexico
Barro Colorado Island, Panama
Amazonia
Central America
Central America
Central America
1812-1980, 168
1973-2004, 30
1900-2009, 109
1970-1996, 25
Renjifo 1999
Ribon et al. 2003
Christiansen and Pitter
2003
west slope, Cordillera Central, Colombia
Viçosa, Minas Gerais, Brazil
Andes
Atlantic Forest
1911-1997, 86
1932-1999, 67
6, 139, 4.3
28, 221, 13
0.06
0.42
Lagoa Santa, Minas Gerais, Brazil
Atlantic Forest
1870-1987, 117
13, 107, 12.1
0.11
0.28
0.40
0.21
1.08
99
These results suggest that short-term studies of avian extinctions from
Amazonian forest landscapes may yield very conservative results because extinction
debts may be paid over a long period and species present in the current landscape
may not be part of viable populations (e.g. Brooks et al. 1999, Metzger et al. 2009). Our
results therefore reinforce the critical importance of establishing (when historical
records are available) an accurate local baseline for a given biota to avoid
underestimating levels of species losses associated with cumulative land-use change
and synergistic interactions between multiple threats (Gardner et al. 2009, Lees et al.
2012). Our results should also be viewed through a conservative lens, given potential
historical collecting biases that we believe makes it more likely that our analysis
underestimated rather than overestimated change. Many species may not have been
represented in the pre-disturbance samples that constituted our baseline due to the
difficulty of collecting small-bodied canopy species relative to understory species and
the fact that collecting effort is neither temporally nor spatially constant (Burgman et al.
1995, McCarthy 1998).
4.1 Patterns of local extinction in the MRB avifauna
Extinction proneness in Amazonian birds is typically linked to life history
characteristics such as body-size, feeding behavior, and dispersal ability (Lees and
Peres 2009, Lees and Peres 2010, Stouffer et al. 2011). Our findings are consistent
with those of previous studies (e.g. Owens and Bennett 2000) which found that largebodied species are particularly extinction prone. For example, we report the purported
loss of 6 large-bodied (>1 kg) species from the MRB, of which 4 - Dark-winged
Trumpeter (Psophia obscura), White-crested Guan (Penelope pileata) Red-throated
Piping-Guan (Aburria cujubi) and Razor-billed Curassow (Pauxi tuberosa) - are
gamebirds highly sought after for bushmeat (e.g. Peres 2000). Eight of the largebodied species were unrecorded after 1900. The mean mass of species that went
extinct from 1800 to 1900 was 1772 g, in contrast to a mean of 270 g after 1901. Given
this information, the most parsimonious explanation for this first wave of local
extinctions from the MRB is hunting of large-bodied species for food, although local
forest loss also began to gain momentum in the same period and was most severe
after 1880 (Vieira et al. 2007).
Trade and persecution may also have driven some species to extinction. For
example, other large-bodied species such as Scarlet Macaw (Ara macao), Red-andgreen Macaw (Ara chloropterus) and Hyacinth Macaw (Anodorhynchus hyacinthinus)
were harvested for the wild bird trade in the MRB (Alves et al. 2013). The same is true
100
of the Golden Parakeet (Guarouba guarouba), which we (NGM & ACL) found persisting
in the neighboring fragmented landscapes of Moju, Paragominas, and Tailândia but
which remains a target for the (now illegal) wild bird trade (Alves et al. 2013). Large
raptors, such as Harpy Eagle (Harpia harpyja), Crested Eagle (Morphnus guianensis),
and Ornate Hawk-Eagle (Spizaetus ornatus) are also particularly threatened in
fragmented landscapes from hunting, which may be triggered by human-wildlife
conflicts when raptors are suspected of killing small livestock (e.g. Trinca et al. 2008).
Many of the other probable extinctions we found are more likely to be related to
forest loss and disturbance than direct persecution. A wave of extinctions of smallerbodied species occurred after 1900, and the mean bodyweight of species assumed to
go extinct between 1900 and 1980 was 270 g (an 85% drop in body size compared
with losses observed during the previous century). This second wave of extinctions
may be linked to habitat loss and degradation associated with the construction of the
railway in 1883-1908 (Vieira et al. 2007) and the subsequent increase in human
population and the size of settlements in Belém after the construction of the BelémBrasília road in the 1960s. The disappearance of both medium and small-bodied
primary-forest dependent frugivores such as the Guianan Red-Cotinga (Phoenicircus
carnifex) and Wing-barred Piprites (Piprites chloris griseicens) is consistent with results
of other studies (e.g. Lees and Peres 2008, Española et al. 2013) and may reflect loss
of food resources or access to adequate nest sites. The absence of many such species
was observed by early naturalists. For example, in 1926 J. Bond failed to find Red-andBlack Grosbeak (Periporphyrus erythromelas) in the MRB, remarking that it was “found
only in the virgin forest at Castanhal” 50 km from Belém (Stone 1928).
Insectivorous species have also been disproportionately affected by habitat
loss, degradation, and fragmentation, including both flock-following under and midstory
primary-forest
dependent
species
such
as
Long-tailed
Woodcreeper
(Deconychura longicauda zimmeri) and terrestrial solitary species such as Spotted
Antpitta (Hylopezus [macularius] paraensis) which appear intolerant even to lowintensity selective-logging activities (Lees and Peres 2010, Moura et al. 2013). The
potential lack of cavity trees could have contributed to population collapses in the MRB
because many of the species inferred to be locally extinct are either primary
(woodpeckers) or secondary cavity nesters (e.g., forest falcons, parrots, woodcreepers)
for which habitat may be reduced in selectively logged and secondary forests (e.g.
Cockle et al. 2010) which typically offer far fewer cavities given reductions in the
number of large live trees, dead snags, and trees with dead limbs (Cockle et al. 2010).
A lack of dead wood and other preferred foraging substrates for woodpeckers,
101
combined with a lack of trees large enough to construct nests for the larger species
could lead to cascade effects for secondary cavity nesters given their dependency on
woodpeckers for creating suitable cavities (Drever et al. 2008).
This local extinction (or ecological extinction, in the case of species now very
rare) likely results in the impairment of important ecosystem processes such as seed
dispersal by large frugivores which may result in cascade effects on vegetative
composition as has already been convincingly demonstrated for the Atlantic forest (e.g.
Galetti et al. 2013, and reviewed in Şekercioḡlu 2006).
4.2 Colonization of MRB by non-forest bird species
Most studies documenting long-term extinctions in formerly forested tropical
landscapes also report on colonization events by non-forest taxa (e.g. Patten et al.
2010). Several ‘new’ species have also been reported from the MRB in the last few
decades including Guira Cuckoo Guira guira which was unrecorded in the MRB prior to
1982 and Ashy-headed Greenlet Hylophilus pectoralis unrecorded before 2005
(Novaes and Lima 2009). These species have likely spread along corridors of nonforest habitat from surrounding savannah-like formations, although-long distance
colonization events from further afield cannot be ruled out (Silva and Oren 1990).
These species are likely to continue to spread throughout the region from neighboring
non-forest habitats. However, these marginal gains in new species do not compensate
for the losses, as the few colonizing species are not of conservation concern,
reinforcing the notion that maintenance and protection of well-preserved primary forest
habitats is a prerequisite for both local (Moura et al. 2013) and global avian biodiversity
conservation (Gibson et al. 2011).
4.3 The future of the MRB avifauna
We anticipate that some of the species we have considered to be extinct may
yet be rediscovered in the region. For example the lack of recent records of Point-tailed
Palmcreeper Berlepschia rikeri and Amethyst Woodstar Calliphlox amethystina is
surprising as they are not typically restricted to primary forest habitats (Parker et al.
1996) and occur patchily in disturbed forest habitats elsewhere in the region (ACL,
NGM, unpubl. data). Some primary-forest dependent species (e.g. Dot-eared Coquette
Lophornis gouldii, Black-faced Dacnis Dacnis lineata and White-vented Euphonia
Euphonia minuta) may have been recently missed because of their cryptic canopy
habits. Some taxa listed as regionally threatened such as Red-necked Aracari
Pteroglossus bitorquatus bitorquatus, Amazonian Barred Woodcreeper Dendrocolaptes
102
certhia medius, White-shouldered Antshrike Thamnophilus aethiops incertus and
Black-spotted Bare-eye Phlegopsis nigromaculata paraensis persist both in degraded
forest landscapes (including in some cases old secondary forest) around the MRB and
in Paragominas (Table 4.2) and their Red List status may warrant re-evaluation.
Most studies documenting long-term extinctions in formerly forested tropical
landscapes also report on colonization events by non-forest taxa (e.g. Patten et al.
2010). However, these marginal gains in new species do not compensate for the
losses because the few colonizing species are not of conservation concern. Thus,
maintenance and protection of well-preserved primary forest habitats is a prerequisite
for both local (Moura et al. 2013) and global avian biodiversity conservation (Gibson et
al. 2011).
Future records of mobile large-bodied species may more likely represent
recolonization rather than low-level persistence throughout the survey period. On 28
April 2013 we recorded a trio of Red-throated Caracaras Ibycter americanus at the
Parque Estadual do Utinga which was apparently the first documented MRB record
since 1958 (Lees 2013a), and there is also a recent (2011) undocumented but reliable
record of Crimson Fruitcrow Haematoderus militaris (G. Thom in litt.) which represents
the first published report in the region since 1919. We have also had documented
sightings of two globally threatened and locally extinct woodpeckers from close to the
study region. On 28 July 2013 we (ACL, NGM and I. Thompson) photographed and
sound-recorded a single Golden-green Woodpecker Piculus chrysochloros paraensis
on the left bank of the Rio Guamá (opposite the study region) in the municipality of
Acará (Lees 2013b), the first documented record globally since 1998, and on 8 August
2013 ACL sound-recorded a Ringed Woodpecker Celeus torquatus pieteroyensi (Lees
2013c) in old secondary forest bordering várzea in the municipality of Vigia (~40 km
from the MRB), hinting at the possible future rediscovery of both species in the MRB.
Larger-bodied (often frugivorous) species with high dispersal capacity are more
likely to be recorded as occasional vagrants or colonizing individuals than smallerbodied (often insectivorous) species with lower dispersal capacity (Lees and Peres
2009). Although this could be grounds for guarded optimism, biotic impoverishment
driven by fragmentation, unsustainable forest management, wildfires, and hunting is
still on-going in the region (Amaral et al. 2012). Given these impacts, coupled with the
lack of an adequate protected area network in the MRB, we anticipate that the number
of local extinctions will continue to rise and result in an ever more impoverished
avifauna in this biologically unique corner of the world’s largest remaining tropical
forest. Our ability to catalogue the long-term erosion of biological diversity in the MRB
103
was made possible only due to the long history of natural history research in the region.
It is likely that similar, hitherto unrecorded, processes of erosion and species extinction
are happening elsewhere in Amazonian deforestation frontiers and across the tropics.
104
Capítulo 5
Conclusão geral
A grande inovação trazida pelo desenho experimental do RAS envolvendo
múltiplas escalas espaciais em um gradiente de perturbação em duas regiões distintas
(Gardner et al. 2013) proporcionou um melhor entendimento das respostas da
avifauna às mudanças de uso da terra na Amazônia. A seguir serão apresentados os
principais resultados relativos ao valor de conservação das florestas primárias,
secundárias e dos sistemas de produção estudados na Amazônia Oriental.
A
C
D
B
E
A
A
A
F
G
H
Figura 5.1 Gradiente de perturbação em Paragominas e Santarém/Belterra . (A)
floresta primária intacta, (B) floresta primária que sofreu corte seletivo, (C) floresta
primária que sofreu corte seletivo e queimada, (D) floresta secundária, (E) plantação
de eucalipto, (F) agricultura familiar, (G) pastagem e (H) agricultura mecanizada. Fotos
C, D e F. A.C. Lees e fotos A, B,E, G e H N. Moura.
105
1. A importância das florestas primárias
As florestas primárias em Paragominas e Santarém apresentaram a maior
riqueza de espécies, entretanto, as florestas primárias não perturbadas por exploração
de madeira e/ou fogo tiveram uma riqueza maior e estrutura da comunidade ainda
diferente das demais classes de floresta primária (com apenas corte seletivo, apenas
queimada e com corte e queima). Esta diferença foi ainda mais acentuada quando
consideradas apenas as espécies florestais (Fig. 2.5, Cap. 2). Além disso,
porcentagem de cobertura florestal é um importante preditor para riqueza de espécies
florestais, mostrado claramente no Capítulo 2. Cobertura e qualidade da floresta
também podem ser consideradas como uma das causas para as prováveis extinções
das 47 espécies na região metropolitana de Belém nos últimos 180 anos (Capítulo 4),
visto que as unidades de proteção ambiental regionais estão continuamente sofrendo
um processo de degradação e perda de floresta (Leão et al. 2007).
Figura 5.2 Guaruba guarouba (ararajuba). Espécie extinta na região metropolitana de Belém
(A) (A.C.Lees). O último registro foi de A. Wallace em 1848 (B) (A. C. Lees © Natural History
Museum, Tring).
Contudo, as florestas primárias degradadas que sofreram apenas corte seletivo
tiveram maior riqueza do que as demais classes e foram significativamente
semelhantes às florestas não perturbadas. Esse resultado foi também encontrado em
outros lugares na Amazônia (Barlow et al. 2006), na Mata Atlântica (Aleixo 1999) e em
outras florestas tropicais e.g. Bornéo (Edwards et al. 2011). Dessa forma, um longo
ciclo de exploração madeireira e proteção ao fogo poderá preservar a maior parte da
biodiversidade local nas florestas públicas e privadas. No entanto, as florestas
primárias não perturbadas são insubstituíveis para algumas espécies, sendo as aves
um dos grupos mais sensíveis a essas mudanças no uso da terra (Gibson et al. 2011)
106
e portanto, podem ser utilizadas como espécies indicadoras de qualidade florestal
(Capítulo 3).
2. Valor da conservação das florestas secundárias
As áreas de florestas secundárias são crescentes nas florestas tropicais (Neef
et al. 2006, FAO 2012), porém a importância das florestas secundárias para a
conservação da biodiversidade é pouco conhecido (Gardner et al. 2007). Em
Paragominas e Santarém, as florestas secundárias apresentaram valor intermediário e
significativamente diferente na riqueza de espécies entre florestas primárias e áreas
agrícolas (Fig. 2.5, Cap. 2). A estrutura e composição da comunidade também foram
diferentes, mesmo para as florestas secundárias mais antigas (>20 anos) (Fig. 2.6,
Cap. 2), por não fornecerem habitat adequado para muitas espécies que foram apenas
associadas às florestas primárias não perturbadas como, por exemplo, Psophia
dextralis (Jacamim-de-costas-marrom), Odontorchilus cinereus (Cambaxirra-cinzenta)
e Grallaria varia (Tovacuçu) em STM e Psophia obscura (Jacamim-de-costasescuras), Hylophilus ochraceiceps (Vite-vite uirapuru) e Haematoderus militaris
(Anambé militar) em PGM. Entre as diferentes classes de idades que as florestas
secundárias foram separadas em PGM, não houve diferença na riqueza de espécies
entre as florestas antigas e as intermediárias (entre 5-20 anos), apenas na estrutura e
composição enquanto, em STM houve diferença significativa (Fig. 2.8, Cap. 2). Ainda
em STM, as florestas secundárias jovens tiveram riquezas significativamente
semelhantes com as pastagens, ao contrário de PGM.
107
B
A
Figura 5.3 Espécies registradas em áreas de floresta primária e secundária. (A) Philydor
erythrocercum (limpa-folha-de-sobre-ruivo), (B) Willisornis poecilinotus (rendadinho), (C) Ibycter
americanus (gralhão) e (D) Taeniotriccus andrei (maria-bonita) N. Moura.
Quando utilizado espécies focais, no capítulo 3, as espécies apresentaram
diferentes de respostas às mudanças de uso da terra, porém das 30 espécies
analisadas
apenas
uma
C
(Trogon
viridis
D
[Surucuá-grande-de-barriga-amarela])
aumentou a porcentagem de ocupação nas florestas secundárias, mostrando que o
uso das florestas secundárias ainda é limitante para muitas espécies. Powell et al.
(2013) avaliou o tempo que as espécies de sub-bosque levaram para transitar na
matriz de floresta secundária entre os fragmentos isolados de floresta primária. Em
média, as espécies levaram 26 anos após o isolamento para serem recapturadas e
algumas aves terrestres como Hylopezus macularius (Torom-carijó) e Grallaria varia
(Tovaçu) não foram capturada nessas áreas 1 . Essas mesmas espécies só foram
registras em áreas de floresta primária em PGM e STM.
1
Hylopezus macularius foi recentemente dividida em quarto espécies- Hylopezus paraensis, H.
macularius, H. whittakeri e H. dilutus pelo CBRO [2014] baseado em Carneiro et al. (2012)1
108
Por propiciar habitats adequados para algumas espécies florestais (Cap 1, 2,
Stratford e Stouffer, 2013), as florestas secundárias podem ser importantes na
formação de corredores entre fragmentos de florestas primárias, dessa forma,
funcionado como uma matriz permeável para diversas espécies e agir como um buffer
(Chazdon et al. 2009), e fornecer importantes serviços de ecossistema como o
sequestro de carbono (Martin et al. 2013) e evapotranspiração, que pode amortecer
possíveis mudanças climáticas regionais. Os resultados apresentados nessa tese
também têm ajudado a quantificar o valor da biodiversidade das diferentes idades das
florestas secundárias orientando na política florestal regional, distinguindo áreas de
florestas secundárias que poderiam ser convertidas em áreas de produção (áreas com
idade < 5 anos de idade), das áreas recomendadas para conservação (entre 5 e 20
anos de idade) (Instrução Normativa 02 /2014, Apêndice 2).
3.
Áreas agrícolas
De acordo com a previsão de Tilman et al. (2011), 1 bilhão de hectares de
florestas serão convertidos, globalmente, até 2050 em áreas agrícolas, crescendo
assim a preocupação com biodiversidade e a manutenção dos serviços de
ecossistema, como, por exemplo, a regulação do ciclo da água, dos nutrientes do solo
e do regime climático. A biodiversidade em áreas agrícolas é muito menor do que nas
áreas de floresta (Capítulo 2), ocasionada pela simplificação do ecosistema, tornando
a ambiente inadequado principalmente para espécies dependentes de floresta. Por
exemplo, das espécies modeladas no Capítulo 3, apenas Amazona farinosa
(papagaio-moleiro) e Pionus fuscus (maitaca-roxa) foram detectadas fora das áreas
florestais, pois são espécies que possuem grande mobilidade, sendo capazes de
cruzarem longas distâncias entre fragmentos de floresta (Lees e Peres 2009). Mahood
et al. 2012, na paisagem fragmentada de Alta Floresta (MT), registraram apenas 30%
das espécies nas áreas agrícolas, enquanto que em PGM e STM foi registrado 43% e
38% espécies, respectivamente. Os resultados dessa tese indicam que mesmo em
áreas de agricultura não intensiva, poucas espécies florestais com significativo
interesse para conservação, persistem. Portanto, considerando-se que as espécies
ocupantes das paisagens de produção e das terras abandonadas, ou seja, sem uso,
são geralmente de baixo interesse de conservação, o aumento da produtividade
agrícola nessas áreas que já foram defaunadas e a fiscalização efetiva, poderiam
diminuir a pressão para abertura de novas fronteiras agrícolas (Green, et al. 2005,
Phalan et al. 2011), reduzindo, assim, a pressão nas áreas de floresta primária.
109
A
C
B
D
A
Figura 5.4 Espécies registradas nas paisagens agrícolas de Paragominas e Santarém/Belterra.
(A) Columbina passerina (rolinha-cinzenta), (B) Anthus lutescens (caminheiro-zumbidor),
Melanerpes candidus (pica-pau-branco) e (D) Crotophaga ani (anu-preto) N. Moura
4.
Conservação na Amazônia dentro e fora das áreas de proteção
As crescentes demandas por novas terras agrícolas e concomitantes
mudanças de uso da terra estão aumentando a pressão nas florestas tropicais,
ameaçando a integridade da biodiversidade. Na Amazônia, apesar da exploração dos
recursos terem começado no século XVI, (retirada de guaraná, resinas, pimenta etc.) a
expansão agrícola começou com a exploração da borracha entre 1840-1915 (Bentes
2004). Atualmente, a fronteira agrícola na Amazônia ‘Arco do Desmatamento’,
considerada uma das mais ativas do mundo (FAO 2005), é expandida principalmente
para criação de pastos (Arima et al. 2005), plantio de soja (Morton et al. 2006) e mais
recentemente plantio de dendê (Lees e Vieira 2013) e cana-de-açúcar (Nepstad et al.
2008). Empreendimentos como construção de hidroelétricas também tem ameaçado
de maneira preocupante os remanescentes florestais do bioma, inundando imensas
áreas de floresta, alterando ciclos hidrológicos, afetando centenas de comunidades
indígenas (Fearnside 2005) e impactando pesadamente a biodiversidade (Fearnside
2014).
A criação e manutenção de um mosaico de áreas protegidas são fundamentais
para a conservação da biodiversidade nas florestas tropicais (Bruner et al. 2001,
Rodrigues et al. 2004, Peres 2005), especialmente quando são áreas representativas
110
da diversidade biológica (Margules e Pressey 2000). A Amazônia legal possui 43,9%
do território protegidos em unidades de conservação e terras indígenas (Fig. 5.5).
Contudo, essas áreas protegidas por si só não garantem a persistência a longo prazo
de muitas espécies (Brooks et al. 2004, Rodrigues et al. 2004), principalmente quando
se tornam cada vez mais isoladas (DeFries et al. 2005). Entre os anos de 1995 e
2013, 2,5 milhões de ha foram retirados de 38 unidades de conservação, o que
corresponde à 1% do território protegido, principalmente para a construção de usinas
hidroelétricas (Veríssimo et al. 2011). Atualmente tramita no Congresso Nacional um
projeto de lei (PL 3.682/2012) para diminuição das unidades de conservação em 10%
para exploração de minérios alterando também Sistema Nacional de Unidades de
Conservação (SNUC Lei 9.985/2000).
Figura 5.5 Áreas protegidas na Amazônia até 2010 (Veríssimo et al. 2011).
Todas essas alterações vão na contramão do que pesquisadores que
argumentam para a necessidade de megareservas (Terborgh e Soule 1999, Peres
2005, Laurence 2005) que poderiam garantir a preservação e a persistência de um
conjunto completo de unidades evolutivas de espécies ecologicamente viáveis e
funcionais em longo prazo (Peres 2005). Além disso, nem todas as espécies estão
protegidas dentro das unidades de conservação (Fernandes 2013, Whitney e CohnHaft 2013)) e, portanto, as propriedades privadas passam a oferecer uma grande
oportunidade para preservar (Soares-Filho et al. 2006 Ferreira et al. 2013) o que já é
conhecido e o que ainda poderá ser descoberto.
111
5. O futuro da Amazônia
Mesmo que sejam crescentes as pesquisas para entender como as mudanças
no uso da terra afetam a biodiversidade e os serviços de ecossistema nas florestas
tropicais, muitos processos ainda precisam ser aprofundados, por exemplo, como
produzir alimentos sem devastar? Phalan et al. (2011) propõe duas estratégias como
um trade-off entre a agropecuária e a conservação. A primeira seria compartilhamento
de terra (land sharing) em que há intensificação do cultivo e a manutenção de uma
área específica para preservação, como os sistemas agroflorestais. Bhagwat e
colaboradores (2008) defendem que os sistemas agroflorestais são importantes para
conservação da biodiversidade local, e apontam três razões: 1) proteção de espécies
e habitats fora das unidades de conservação, funcionando como corredores, por
exemplo, 2) mantêm a heterogeneidade nas escalas de locais e de paisagem e 3) as
árvores nas paisagens agroflorestais reduzem a pressão sobre as reservas, pois a
diversidade do sistema agroflorestal diminuirá a dependência dos produtores das
áreas florestadas. Porém, só funciona para as espécies que podem crescer à sobra
das agroflorestas, como café e cacau.
A segunda estratégia economia de terra (land sparing) o que integra a
produção e a conservação na mesma área . Os mesmos autores em Phalan et al.
2014 defendem que economia de terra pode ser mais promissor, principalmente para
as aves dependentes de habitats naturais, pois a intensificação nas áreas já utilizadas
para fins agrícolas diminuirá a pressão nas áreas ainda florestadas.
6.
Pesquisas futuras
Essa tese procurou avaliar a perda de espécies em um gradiente de
perturbação (Capítulo 2), entender como algumas espécies estavam distribuídas nos
diferentes tipos de uso da terra (Capítulo 3) e quais as evidências para a extinção
histórica das espécies de terra firme ao logo de quase 200 anos de pesquisa na
Amazônia (Capítulo 4). Outras variáveis como características edáficas, interações com
plantas (Pomara et al. 2012) e outros fatores podem também estar relacionados com
as respostas da avifauna à essas alterações humanas. Para melhor embasar políticas
de conservação também é preciso entender os padrões de sobrevivência das espécies
nos diferentes tipos de uso, buscando relações entre a topografia, vegetação e aves,
também é importante conhecer os processos de recolonização das áreas de florestas
em regeneração.
112
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136
Anexo 1
Tabela com as espécies registradas em Paragominas e Santarém nos diferentes tipos de uso da terra. Segue classificação CBRO 2014.
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Tinamidae
Tinamus tao
1
0
2
0
0
0
0
0
0
2
2
2
0
0
0
0
Tinamus guttatus
1
0
1
0
0
0
0
0
8
6
0
0
5
0
0
0
Crypturellus cinereus
1
0
0
1
2
0
0
0
4
0
1
6
3
0
0
0
Crypturellus soui
0
1
6
17
11
0
0
0
1
3
7
7
32
3
2
0
Crypturellus obsoletus
1
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
Crypturellus strigulosus
1
0
5
8
5
0
0
0
1
0
0
5
4
0
0
0
Crypturellus parvirostris
0
0
0
3
0
5
32
3
0
0
2
0
12
16
16
6
Crypturellus variegatus
1
10
7
0
2
0
0
0
11
4
4
4
1
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
Cairina moschata
0
0
0
1
0
0
3
0
0
0
0
0
0
0
0
0
Amazoneta brasiliensis
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
Penelope superciliaris
1
0
1
8
0
0
0
0
0
0
0
0
2
0
0
0
Penelope jacquacu
1
0
0
0
0
0
0
0
3
7
0
5
6
0
0
0
Penelope pileata
1
0
1
1
0
0
0
0
0
2
1
4
4
0
0
0
Aburria cujubi
1
0
2
0
0
0
0
0
3
3
0
0
0
0
0
0
Ortalis superciliaris
0
0
0
2
2
2
4
0
0
0
0
0
0
0
0
0
Ortalis motmot
0
0
0
0
0
0
0
0
0
1
0
0
4
0
1
0
Pauxi tuberosa
1
1
5
0
1
0
0
0
0
2
1
0
0
0
0
0
Odontophoridae
Odontophorus
gujanensis
1
0
5
0
0
0
0
0
1
2
1
0
0
0
0
0
Anhimidae
Anhima cornuta
Anatidae
Cracidae
Ciconiidae
137
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
familiar
Agricultura
mecanizada
0
0
0
4
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
Theristicus caudatus
0
0
0
0
0
0
0
0
0
1
0
0
Platalea ajaja
0
0
1
0
0
0
0
0
0
0
0
0
Cathartes aura
0
1
29
6
0
1
0
1
12
24
5
12
Cathartes burrovianus
0
0
0
0
0
0
0
0
2
3
3
8
4
0
0
2
0
1
0
0
0
2
0
0
0
1
4
9
2
52
7
0
1
0
1
9
23
12
9
1
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
1
0
2
1
0
0
1
0
0
0
0
1
2
0
0
0
0
0
0
0
0
0
3
1
0
0
0
0
0
0
0
0
Elanus leucurus
0
0
0
0
0
0
4
0
0
0
0
0
0
0
0
0
Harpagus bidentatus
1
0
0
0
0
0
0
0
0
0
0
2
0
0
0
0
Accipiter superciliosus
Heterospizias
meridionalis
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
1
0
0
Urubitinga urubitinga
1
0
0
0
0
0
1
0
0
1
0
1
0
0
0
0
Rupornis magnirostris
0
0
0
0
3
4
7
2
0
0
0
1
9
4
2
0
Pseudastur albicollis
Geranoaetus
albicaudatus
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
1
2
0
0
0
0
3
2
4
2
Leucopternis kuhli
1
1
4
0
0
0
0
0
1
1
1
0
3
0
0
0
Buteo nitidus
Geranoaetus
albicaudatus
1
0
0
3
5
2
2
0
0
0
0
3
4
4
0
0
0
0
0
0
0
0
1
2
0
0
0
0
3
2
4
2
Corte
seletivo
Cortado e
queimado
0
0
1
Butorides striata
0
0
Bubulcus ibis
0
Ardea alba
Pasto
Agricultura
mecanizada
Floresta primária
Floresta
secundária
Não
perturbada
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
0
0
0
0
2
0
0
0
0
1
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
2
5
0
0
0
0
Cathartes melambrotus
1
0
2
Coragyps atratus
0
0
Sarcoramphus papa
1
0
Accipitridae
Chondrohierax
uncinatus
1
Elanoides forficatus
Gampsonyx swainsonii
Mycteria americana
Ardeidae
Threskiornithidae
Cathartidae
138
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Leucopternis kuhli
1
1
4
0
0
0
0
0
1
1
1
0
3
0
0
0
Buteo nitidus
1
0
0
3
5
2
2
0
0
0
0
3
4
4
0
0
Buteo brachyurus
0
0
0
0
0
0
2
0
0
0
0
0
2
0
0
0
Buteo albonotatus
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
Spizaetus tyrannus
Spizaetus
melanoleucus
1
0
1
0
1
0
0
0
0
0
0
0
1
0
0
0
1
0
0
0
1
0
0
0
0
0
0
0
0
1
0
0
Spizaetus ornatus
1
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
Psophia dextralis
1
0
0
0
0
0
0
0
2
1
0
0
0
0
0
0
Psophia obscura
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
Aramides cajanea
0
0
0
0
0
0
0
0
1
0
0
0
0
1
0
0
Laterallus viridis
Laterallus
melanophaius
0
0
1
3
5
4
34
3
0
0
0
0
6
7
5
1
0
0
0
0
1
0
1
0
0
0
0
0
0
0
0
0
Laterallus exilis
0
0
0
0
0
0
0
0
0
0
0
0
0
6
0
1
Neocrex erythrops
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
Porphyrio martinica
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
0
0
0
0
1
0
15
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
4
0
0
0
0
0
0
0
0
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
Columbina passerina
0
0
0
0
4
9
60
8
0
0
0
1
10
38
24
26
Columbina minuta
0
0
0
0
0
0
0
0
0
0
0
0
0
3
1
0
Columbina talpacoti
0
0
1
1
17
6
67
14
0
0
0
0
7
12
8
8
Psophiidae
Rallidae
Charadriidae
Vanellus chilensis
Scolopacidae
Tringa solitaria
Jacanidae
Jacana jacana
Sternidae
Phaetusa simplex
Columbidae
139
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecaniza
da
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Columbina squammata
0
0
0
0
0
0
4
0
0
0
0
0
0
0
0
0
Claravis pretiosa
0
0
0
2
0
0
0
0
0
0
0
0
0
0
0
0
Columba livia
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
Patagioenas speciosa
1
0
5
5
16
1
9
0
0
0
1
0
5
1
1
0
Patagioenas picazuro
Patagioenas
cayennensis
0
0
0
0
2
2
15
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
2
0
0
0
0
1
4
0
1
Patagioenas plumbea
Patagioenas
subvinacea
1
11
44
12
1
0
0
0
9
8
5
20
6
0
0
0
1
0
3
4
0
0
0
0
4
3
5
3
4
0
0
0
Zenaida auriculata
0
0
0
0
0
0
1
0
0
0
0
0
0
13
0
7
Leptotila verreauxi
0
0
0
12
18
0
23
2
0
2
1
0
9
8
10
4
Leptotila rufaxilla
1
0
4
13
3
3
0
0
1
6
6
8
30
0
1
0
Geotrygon montana
1
0
4
7
2
0
0
0
4
4
1
2
1
0
0
0
Coccycua minuta
0
0
0
1
0
0
2
0
0
0
0
0
1
0
0
0
Piaya cayana
1
5
19
30
14
0
3
0
1
5
4
14
19
4
0
0
Piaya melanogaster
1
0
0
0
0
0
0
0
6
3
0
0
1
0
0
0
Crotophaga major
0
0
0
0
0
0
1
0
0
0
0
0
2
0
0
0
Crotophaga ani
0
0
1
1
2
7
86
4
0
0
0
0
15
67
20
21
Guira guira
Dromococcyx
phasianellus
Dromococcyx
pavoninus
0
0
0
0
0
0
3
0
0
0
0
0
0
0
0
0
1
0
0
8
5
0
1
0
0
0
0
1
2
0
0
0
1
0
1
3
2
0
0
0
0
0
0
0
0
0
0
0
Tapera naevia
0
0
0
0
1
0
12
1
0
0
0
0
0
0
0
0
Megascops choliba
0
0
0
1
1
0
0
0
0
0
0
1
3
1
0
0
Megascops usta
1
0
0
0
0
0
0
0
2
5
2
1
3
0
0
0
Lophostrix cristata
1
1
0
2
0
0
0
0
0
0
0
1
0
0
0
0
Pulsatrix perspicillata
1
0
1
1
0
0
0
0
0
0
1
0
0
0
0
0
Strix huhula
1
0
0
0
0
0
0
0
1
0
1
1
0
0
0
0
Strix virgata
1
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
Cuculidae
Strigidae
140
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Floresta primária
Agricultura
mecanizada
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Glaucidium hardyi
1
0
2
0
0
0
0
0
4
12
2
6
5
0
0
0
Athene cunicularia
0
0
0
0
0
2
11
4
0
0
0
0
0
1
0
0
Asio clamator
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
Nyctibius griseus
0
0
1
0
0
0
0
0
0
0
1
0
4
0
0
0
Nyctibius aethereus
1
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
Nyctibius leucopterus
1
2
0
0
0
0
0
0
0
2
0
0
0
0
0
0
Nyctibiidae
Caprimulgidae
1
Nyctiphrynus ocellatus
1
0
1
1
2
0
0
0
1
0
0
1
1
0
0
0
Antrostomus rufus
Antrostomus
sericocaudatus
1
0
0
0
1
0
0
0
0
0
0
0
1
0
0
0
1
0
0
0
0
0
0
0
1
5
0
1
0
0
0
0
Lurocalis semitorquatus
1
1
4
2
0
0
0
0
12
17
1
10
6
0
0
0
Hydropsalis nigrescens
1
0
3
2
1
0
0
0
0
2
1
1
2
0
0
0
Hydropsalis albicollis
1
0
1
6
3
0
1
0
0
0
0
0
4
1
0
0
Cypseloides senex
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
Chaetura spinicaudus
1
0
19
21
10
0
7
1
8
4
6
3
7
8
0
0
Chaetura chapmanii
1
0
1
0
1
0
0
0
0
0
1
0
1
0
0
0
Chaetura brachyura
1
0
8
21
4
1
22
2
1
0
1
0
10
22
3
6
Tachornis squamata
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
1
Glaucis hirsutus
1
0
18
12
7
3
1
0
0
0
1
4
8
0
0
0
Phaethornis rupurumii
Phaethornis
aethopygus
1
0
0
0
0
0
0
0
0
0
0
1
7
0
0
0
1
0
0
0
0
0
0
0
8
8
0
3
2
0
0
0
Phaethornis ruber
Phaethornis
superciliosus
1
11
151
177
89
5
8
0
2
9
10
12
31
1
0
0
1
8
37
18
3
0
0
0
6
12
7
14
27
0
0
0
Phaethornis bourcieri
Campylopterus
largipennis
1
0
0
0
0
0
0
0
1
1
0
2
1
0
0
0
1
2
24
10
4
0
2
0
0
0
0
0
0
0
0
0
Florisuga mellivora
1
0
1
1
1
0
0
0
0
0
2
0
0
0
0
0
Apodidae
Trochilidae
141
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
familiar
Agricultura
mecanizada
8
0
1
5
4
4
0
0
0
2
0
1
0
0
0
0
0
0
5
3
0
0
5
8
2
0
0
0
0
17
6
0
0
0
0
0
0
0
0
0
0
0
4
1
0
6
5
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
Amazilia fimbriata
1
0
3
0
0
1
0
0
4
4
0
0
Heliomaster longirostris
1
0
0
0
0
0
0
0
0
0
0
0
1
Heliothryx auritus
1
0
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
Trogon melanurus
0
0
0
0
6
11
3
17
8
0
0
0
15
4
0
0
0
15
32
15
29
55
0
0
0
5
0
0
0
0
5
10
4
13
6
0
0
0
3
4
5
0
0
0
0
0
0
0
1
0
0
0
3
7
3
0
0
0
0
14
11
1
8
2
0
0
0
0
0
1
1
2
0
2
0
0
0
0
0
0
1
0
1
Chloroceryle americana
1
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
Chloroceryle inda
1
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
Baryphthengus martii
1
0
0
0
0
0
0
0
1
1
1
0
1
0
0
0
Momotus momota
1
3
30
18
10
0
1
0
4
1
3
7
21
0
0
0
4
28
25
1
0
0
0
1
2
2
3
0
0
0
0
Corte
seletivo
Cortado e
queimado
1
0
9
0
0
0
Thalurania furcata
1
3
Hylocharis cyanus
1
Polytmus theresiae
Amazilia versicolor
Pasto
Agricultura
mecanizada
Floresta primária
Floresta
secundária
Não
perturnada
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
0
0
1
0
0
0
0
0
0
0
8
3
0
0
0
0
9
4
77
8
2
0
0
0
3
0
0
0
0
5
0
0
0
1
1
0
0
4
4
0
1
3
15
6
Trogon viridis
1
7
26
Trogon ramonianus
1
3
15
Trogon curucui
1
0
Trogon rufus
1
Megaceryle torquata
Anthracothorax
nigricollis
Chrysolampis
mosquitus
Trogonidae
Alcedinidae
Momotidae
Galbulidae
Brachygalba lugubris
1
0
0
0
0
0
2
0
0
0
0
0
0
0
0
0
Galbula dea
1
3
7
1
0
0
0
0
8
9
3
7
4
0
0
0
Jacamerops aureus
1
2
11
3
0
0
0
0
4
6
2
3
0
0
0
0
Bucconidae
Notharchus
hyperrhynchus
1
0
7
4
0
0
0
0
9
12
2
8
3
0
0
0
142
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Notharchus ordii
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
Notharchus tectus
1
3
10
12
1
0
0
0
1
4
0
3
5
0
0
0
Bucco tamatia
1
3
4
2
3
0
0
0
1
1
0
0
0
0
0
0
Bucco capensis
1
2
8
2
0
0
0
0
6
7
3
4
3
0
0
0
Nystalus torridus
1
1
7
9
1
0
0
0
0
0
0
0
0
0
0
0
Nystalus maculatus
0
0
0
0
0
0
0
0
0
0
0
0
1
4
4
0
Malacoptila rufa
1
6
5
2
4
0
0
0
6
4
1
1
5
0
0
0
Monasa nigrifrons
1
0
0
2
0
0
0
0
0
0
0
0
0
0
0
0
Monasa morphoeus
1
11
20
19
0
0
0
0
10
13
7
17
10
0
0
0
Chelidoptera tenebrosa
1
0
0
0
0
0
0
0
1
0
1
0
3
0
0
0
Ramphastos tucanus
1
8
38
23
2
0
0
0
22
23
4
28
8
1
0
0
Ramphastos vitellinus
1
3
36
26
8
0
0
0
13
23
11
13
15
1
0
0
Selenidera gouldii
1
0
17
8
2
0
0
0
1
5
6
2
3
0
0
0
Pteroglossus inscriptus
Pteroglossus
bitorquatus
1
0
9
3
0
0
1
0
0
3
0
6
7
1
0
0
1
2
12
7
1
0
0
0
1
5
0
3
0
0
0
0
Pteroglossus aracari
1
1
33
31
8
0
1
0
5
9
5
10
12
2
0
0
Picumnus aurifrons
1
0
0
0
0
0
0
0
0
0
1
0
2
2
1
0
Picumnus exilis
1
0
6
6
0
0
0
0
0
0
0
0
0
0
0
0
Picumnus pygmaeus
0
0
0
0
1
1
1
0
0
0
0
0
0
0
0
0
Melanerpes candidus
0
0
0
1
1
0
9
1
0
0
0
0
0
0
0
0
Melanerpes cruentatus
1
0
2
6
1
0
1
1
4
12
3
12
8
2
1
0
Veniliornis affinis
1
2
20
11
1
0
0
0
1
5
0
6
8
1
0
0
Piculus flavigula
1
3
16
7
0
0
0
0
2
6
0
1
1
0
0
0
Piculus laemostictus
1
0
0
0
0
0
0
0
2
2
1
0
2
0
0
0
Colaptes melanochloros
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
Celeus undatus
1
7
17
0
1
0
0
0
0
0
0
0
0
0
0
0
Celeus grammicus
1
0
0
0
0
0
0
0
9
10
4
2
4
0
0
0
Ramphastidae
Picidae
143
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Celeus elegans
1
0
0
0
0
0
0
0
0
1
1
2
7
0
0
0
Celeus flavus
1
1
1
1
0
0
0
0
2
7
0
2
2
0
0
0
Celeus torquatus
1
0
0
0
0
0
0
0
1
6
1
2
0
0
0
0
Dryocopus lineatus
0
0
5
20
5
0
8
0
2
10
2
7
18
9
3
0
Campephilus rubricollis
Campephilus
melanoleucus
1
4
15
8
0
0
1
0
8
9
2
10
6
0
0
0
1
0
0
0
0
0
0
0
0
1
0
1
1
0
0
0
Daptrius ater
1
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
Ibycter americanus
1
1
13
9
0
0
0
0
6
8
0
4
4
0
0
0
Caracara plancus
0
0
0
1
1
2
10
2
0
0
0
0
2
5
2
5
Milvago chimachima
Herpetotheres
cachinnans
0
0
0
0
0
0
1
0
0
0
0
0
1
8
0
1
1
0
1
3
1
0
4
1
1
2
0
1
3
4
0
0
Micrastur ruficollis
1
0
13
8
5
0
0
0
4
2
1
5
1
0
0
0
Micrastur mintoni
1
5
9
3
0
0
0
0
7
4
1
2
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
2
0
0
0
0
1
0
0
2
0
0
0
0
0
1
1
0
0
0
0
0
Falco rufigularis
1
0
1
2
0
0
3
0
0
1
0
1
0
3
0
0
Falco femoralis
0
0
0
0
0
0
0
0
0
0
0
0
0
1
3
1
Psittacidae
Anodorhynchus
hyacinthinus
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
Ara ararauna
1
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
Ara macao
1
0
5
6
3
0
1
0
2
5
0
0
4
1
0
0
Ara chloropterus
1
0
9
9
0
0
3
0
6
4
1
1
0
0
0
0
Ara severus
1
0
0
0
0
0
0
0
4
10
1
8
19
10
4
3
Orthopsittaca manilatus
1
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
Guaruba guarouba
Psittacara
leucophthalma
1
1
12
11
9
1
5
0
0
0
0
0
0
0
0
0
1
0
2
0
3
0
8
1
0
0
4
3
11
11
2
4
Aratinga jandaya
0
0
1
5
7
2
14
0
0
0
0
0
0
0
0
0
Eupsittula aurea
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
Falconidae
144
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Pyrrhura lepida
1
3
16
7
2
0
0
0
0
0
0
0
0
0
0
0
Pyrrhura amazonum
1
0
0
0
0
0
0
0
2
8
5
5
3
0
0
0
Forpus passerinus
1
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
Forpus xanthopterygius
0
0
0
0
0
0
3
0
0
0
0
0
0
0
0
0
Brotogeris versicolurus
1
0
0
0
0
0
0
0
0
1
3
2
7
14
10
5
Brotogeris chrysoptera
1
2
29
17
2
0
3
0
16
12
5
26
8
1
0
0
Touit huetii
1
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
Pionites leucogaster
1
4
9
10
0
0
0
0
2
2
0
0
0
0
0
0
Pyrilia vulturina
1
0
0
0
0
0
0
0
4
2
1
1
1
0
0
0
Pionus menstruus
1
0
58
57
17
1
14
2
14
21
9
11
19
2
0
1
Pionus fuscus
1
9
35
15
4
0
3
0
2
5
1
3
6
0
0
0
Amazona farinosa
1
4
37
31
2
1
6
3
13
24
6
19
15
0
0
0
Amazona amazonica
1
0
26
51
28
2
31
2
3
5
2
9
23
7
0
4
Amazona ochrocephala
1
0
7
8
1
1
4
1
1
6
0
4
4
2
2
2
1
0
13
6
0
0
0
0
2
0
0
3
1
0
0
0
Microrhopias quixensis
1
0
0
0
0
0
0
0
1
1
0
2
2
0
0
0
Pygiptila stellaris
Epinecrophylla
leucophthalma
Myrmotherula
brachyura
1
3
6
3
0
0
0
0
6
9
1
9
2
0
0
0
1
0
0
0
0
0
0
0
5
9
0
1
3
0
0
0
1
0
0
0
0
0
0
0
22
23
4
12
4
0
0
0
Myrmotherula sclateri
Myrmotherula
multostriata
1
0
0
0
0
0
0
0
9
9
1
11
0
0
0
0
1
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
Myrmotherula axillaris
Myrmotherula
longipennis
Myrmotherula
menetriesii
1
9
49
54
13
0
0
0
8
11
15
28
74
0
0
0
1
11
13
12
1
0
0
0
9
13
1
6
1
0
0
0
1
9
35
23
1
0
0
0
13
11
3
9
2
0
0
0
Formicivora grisea
0
0
7
49
73
2
86
4
0
0
0
0
24
11
13
0
Isleria hauxwelli
1
5
33
19
2
0
0
0
5
0
2
1
2
0
0
0
Thamnomanes caesius
1
15
65
54
14
0
0
0
21
23
8
30
15
0
0
0
Dysithamnus mentalis
1
7
30
7
4
0
0
0
0
0
0
0
0
0
0
0
Thamnophilidae
145
Espécies/Família
Herpsilochmus
rufimarginatus
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
1
18
31
19
4
0
0
0
9
14
5
13
0
0
0
0
Thamnophilus palliatus
Thamnophilus
schistaceus
1
0
6
8
21
0
8
0
0
0
0
2
8
0
0
0
1
0
0
0
0
0
0
0
36
48
16
37
56
0
0
0
Thamnophilus
amazonicus
1
7
50
39
3
0
0
0
10
19
5
20
13
0
0
0
1
5
49
57
48
0
0
0
0
0
0
0
5
0
0
0
Cymbilaimus lineatus
1
0
0
0
0
0
0
0
25
48
9
14
11
0
0
0
Taraba major
Hypocnemoides
maculicauda
0
0
0
4
15
1
23
1
0
0
0
2
23
4
9
0
1
0
0
0
1
0
0
0
0
1
0
0
0
0
0
0
Hylophylax naevius
1
0
0
0
0
0
0
0
11
1
2
2
0
0
0
0
Hylophylax punctulatus
1
0
0
0
0
0
0
0
2
2
0
0
0
0
0
0
Sclateria naevia
Myrmoborus
myiotherinus
1
0
0
0
0
0
0
0
0
2
0
0
1
0
0
0
1
0
0
0
0
0
0
0
8
13
6
6
30
0
0
0
Pyriglena leuconota
Sciaphykax
hemimelaena
Cercomacra
cinerascens
1
4
85
77
24
0
0
0
3
2
0
5
3
0
0
0
1
0
0
0
0
0
0
0
5
14
9
17
48
0
1
0
1
23
161
110
10
0
0
0
45
108
23
65
38
1
0
0
Cercomacra laeta
1
1
44
60
18
0
0
0
0
0
0
0
0
0
0
0
Cercomacra nigrescens
Hypocnemis
hypoxantha
1
0
0
0
0
0
0
0
0
9
3
5
28
3
6
0
1
0
0
0
0
0
0
0
2
1
5
7
2
0
0
0
Hypocnemis striata
1
0
0
0
0
0
0
0
13
18
6
22
15
0
0
0
Willisornis vidua
Phlegopsis
nigromaculata
Rhegmatorhina
gymnops
1
13
22
12
3
0
0
0
7
13
7
11
17
0
0
0
1
3
4
1
0
0
0
0
5
10
2
2
12
0
0
0
1
0
0
0
0
0
0
0
3
1
1
0
0
0
0
0
Conopophaga aurita
1
0
0
0
0
0
0
0
1
3
0
5
0
0
0
0
Conopophaga roberti
1
0
34
21
4
0
0
0
0
0
0
0
0
0
0
0
Grallaria varia
1
4
1
0
0
0
0
0
2
0
0
0
0
0
0
0
Hylopezus paraensis
1
1
0
1
0
0
0
0
0
0
0
0
0
0
0
0
Hylopezus whittakeri
1
0
0
0
0
0
0
0
6
1
3
1
0
0
0
0
Conopophagidae
Grallariidae
146
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
familiar
Agricultura
mecanizada
0
0
0
0
0
0
0
0
0
0
0
5
2
0
0
22
2
0
0
0
5
2
0
0
0
0
1
0
0
0
2
18
5
4
0
2
2
0
0
0
0
1
1
1
0
0
0
0
0
1
0
0
0
1
0
1
0
2
1
1
0
0
0
0
0
1
2
7
0
0
2
0
0
1
0
0
0
Dendrocincla fuliginosa
1
9
0
0
16
27
7
19
26
0
0
0
Dendrocincla merula
Deconychura
longicauda
Sittasomus
griseicapillus
Certhiasomus
stictolaemus
1
0
0
0
4
1
1
2
1
0
0
0
0
0
0
0
2
0
0
0
0
0
0
0
0
0
0
0
8
7
0
3
3
0
0
0
1
0
0
0
0
0
0
0
0
2
0
0
0
39
17
0
0
0
30
35
11
22
47
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
47
37
3
0
0
0
28
52
6
35
13
0
2
0
22
15
4
0
1
0
10
10
0
2
6
0
0
0
0
0
0
0
0
0
4
1
0
1
0
0
0
0
0
2
10
16
0
6
0
0
0
1
2
17
13
9
0
7
25
34
3
0
0
0
5
1
2
2
2
0
0
0
1
0
7
1
0
0
0
0
1
4
1
2
1
0
0
0
Dendrocolaptes medius
Dendrocolaptes
ridgwayi
Dendrocolaptes
picumnus
1
3
14
6
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
18
13
8
15
10
0
0
0
1
0
0
0
0
0
0
0
10
21
1
10
7
0
0
0
Hylexetastes uniformis
Xiphocolaptes
promeropirhynchus
1
0
0
0
0
0
0
0
12
16
5
8
4
0
0
0
1
0
0
0
0
0
0
0
2
4
0
6
3
0
0
0
Corte
seletivo
Cortado e
queimado
1
0
0
1
0
0
Formicarius colma
1
2
Formicarius analis
1
Sclerurus macconnelli
Pasto
Agricultura
mecanizada
Floresta primária
Floresta
secundária
Não
perturnada
Corte
seletivo
Queimado
1
0
0
9
12
7
0
1
0
0
0
0
3
2
0
0
0
0
0
0
0
0
2
1
0
0
29
24
1
0
0
3
2
1
1
0
3
1
1
0
0
0
1
0
1
Glyphorynchus spirurus
Xiphorhynchus
obsoletus
1
20
53
1
0
Xiphorhynchus guttatus
1
17
Xiphorhynchus spixii
Campylorhamphus
cardosoi
1
12
1
0
Dendroplex picus
0
Lepidocolaptes . layardi
1
Dendrexetastes rufigula
Hylopezus berlepschi
Myrmothera
campanisona
Não
perturnada
Cortado e
queimado
Formicariidae
Scleruridae
Dendrocolaptidae
147
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
familiar
Agricultura
mecanizada
45
12
0
0
5
8
0
0
0
0
0
0
0
0
4
0
0
0
0
0
0
0
0
13
9
5
2
0
1
1
8
0
0
0
9
2
5
2
0
0
0
0
7
4
0
0
0
1
5
0
0
0
1
6
14
0
3
4
0
0
3
0
0
0
Philydor erythropterum
1
5
Philydor pyrrhodes
1
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
1
0
0
0
2
3
0
1
0
0
0
0
Synallaxis albescens
4
4
164
11
0
0
0
0
0
5
0
0
9
2
0
0
0
0
0
0
3
4
0
0
0
2
16
0
11
0
0
0
0
0
1
4
2
0
49
21
3
0
0
0
19
33
21
37
22
0
0
0
5
44
23
11
0
0
0
12
25
11
31
35
0
0
0
1
1
0
0
0
0
0
16
14
3
10
11
0
0
0
0
0
1
7
37
0
0
0
0
0
0
2
26
0
0
0
1
0
0
0
0
0
0
0
0
1
0
0
1
0
0
0
Chiroxiphia pareola
1
0
0
5
4
0
0
0
0
3
14
27
80
0
0
0
Dixiphia pipra
1
2
10
4
6
0
0
0
0
0
0
0
0
0
0
0
Onychorhynchidae
Onychorhynchus
coronatus
Terenotriccus
erythrurus
1
0
11
6
3
0
0
0
1
1
0
0
2
0
0
0
1
0
24
24
4
0
0
0
1
0
1
1
3
0
0
0
Myiobius barbatus
1
0
5
4
0
0
1
0
0
0
1
0
0
0
0
0
Schiffornis turdina
1
13
10
4
3
0
0
0
9
1
6
7
0
0
0
0
Laniocera hypopyrra
1
6
0
0
0
0
0
0
3
3
1
0
0
0
0
0
Corte
seletivo
Cortado e
queimado
1
6
42
Ancistrops strigilatus
1
0
Automolus ochrolaemus
1
Automolus paraensis
1
Automolus rufipileatus
1
Pasto
Agricultura
mecanizada
Floresta primária
Floresta
secundária
Não
perturnada
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
0
3
2
3
0
0
3
1
0
0
0
1
0
0
0
6
4
0
0
0
4
0
0
0
6
2
0
0
1
0
0
0
1
3
4
0
0
0
0
0
Synallaxis rutilans
1
0
7
Synallaxis gujanensis
0
0
0
Tyranneutes stolzmanni
1
17
Ceratopipra rubrocapilla
1
Lepidothrix iris
1
Manacus manacus
Machaeropterus
pyrocephalus
Xenopidae
Xenops minutus
Furnariidae
Pipridae
Tityridae
148
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Iodopleura isabellae
1
0
0
1
1
0
0
0
1
0
0
0
0
0
0
0
Tityra inquisitor
1
0
2
3
0
0
0
0
0
0
0
0
0
0
0
0
Tityra cayana
1
2
19
17
4
0
0
0
0
0
0
0
0
0
0
0
Tityra semifasciata
1
0
0
0
0
0
0
0
0
3
1
6
4
0
0
0
Pachyramphus viridis
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
Pachyramphus rufus
Pachyramphus
castaneus
Pachyramphus
polychopterus
Pachyramphus
marginatus
0
0
0
0
3
0
6
0
0
0
0
0
6
17
6
1
1
0
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
3
0
2
0
0
0
0
0
0
1
2
0
1
0
1
0
12
8
0
0
0
0
6
13
3
11
3
0
0
0
Pachyramphus minor
1
0
6
5
3
0
0
0
2
2
2
2
2
0
0
0
Pachyramphus validus
0
0
0
0
2
0
0
0
0
0
0
0
0
0
0
0
Lipaugus vociferans
1
26
66
11
2
0
0
0
57
67
20
46
12
0
0
0
Xipholena lamellipennis
1
6
5
5
3
0
0
0
4
1
1
2
1
0
0
0
Cotinga cotinga
1
0
1
0
0
0
0
0
0
0
0
0
1
0
0
0
Cotinga cayana
1
1
0
0
0
0
0
0
0
0
0
0
4
0
0
0
Haematoderus militaris
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
Querula purpurata
1
0
37
12
3
0
0
0
9
15
6
6
5
0
0
0
1
1
0
0
0
0
0
0
6
1
2
3
0
0
0
0
1
3
28
2
1
0
0
0
3
7
2
2
0
0
0
0
1
0
3
1
0
0
0
0
1
1
0
1
0
0
0
0
1
8
3
3
0
0
0
0
11
4
0
5
0
0
0
0
Taeniotriccus andrei
1
0
12
5
6
0
0
0
0
0
0
0
0
0
0
0
Mionectes oleagineus
0
0
0
2
1
0
0
0
0
0
0
0
10
0
0
0
Mionectes macconnelli
1
2
10
1
1
0
0
0
1
0
3
0
0
0
0
0
Cotingidae
Pipritidae
Piprites chloris
Platyrinchidae
Platyrinchus
platyrhynchos
Rhynchocyclidae
149
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
1
2
5
0
1
0
0
0
2
1
1
0
0
0
0
0
Phylloscartes virescens
Rhynchocyclus
olivaceus
Tolmomyias
sulphurescens
1
3
3
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
2
2
1
0
0
0
0
7
1
3
6
0
0
0
1
0
2
4
2
0
0
0
0
0
0
0
0
0
0
0
Tolmomyias assimilis
Tolmomyias
poliocephalus
1
3
23
18
2
0
0
0
6
4
2
5
1
0
0
0
1
0
1
10
6
0
0
0
11
13
15
17
24
1
2
0
Tolmomyias flaviventris
0
0
21
50
46
12
26
2
0
7
2
4
43
6
12
0
Todirostrum cinereum
Todirostrum
chrysocrotaphum
0
0
3
2
10
9
73
6
0
0
0
0
0
0
0
0
1
0
4
3
1
0
0
0
0
2
0
2
1
0
0
0
Poecilotriccus fumifrons
0
0
0
10
31
2
41
3
0
0
0
0
0
0
0
0
Poecilotriccus sylvia
0
0
13
31
33
0
3
0
0
0
0
0
0
0
0
0
Myiornis ecaudatus
1
20
26
3
0
0
0
0
22
18
6
16
15
0
0
0
Hemitriccus minimus
1
0
0
0
0
0
0
0
1
3
0
2
7
0
0
0
Hemitriccus striaticollis
0
0
0
0
0
0
0
0
0
0
1
0
15
13
3
0
1
12
97
86
29
0
0
0
31
55
18
34
34
0
0
0
Zimmerius acer
1
9
36
21
6
0
0
0
17
22
15
27
48
0
0
0
Ornithion inerme
1
5
32
35
2
0
0
1
6
3
1
11
5
0
0
0
Hemitriccus minimus
1
0
0
0
0
0
0
0
1
3
0
2
7
0
0
0
Hemitriccus striaticollis
0
0
0
0
0
0
0
0
0
0
1
0
15
13
3
0
1
12
97
86
29
0
0
0
31
55
18
34
34
0
0
0
Zimmerius acer
1
9
36
21
6
0
0
0
17
22
15
27
48
0
0
0
Ornithion inerme
Camptostoma
obsoletum
1
5
32
35
2
0
0
1
6
3
1
11
5
0
0
0
0
0
4
21
31
1
51
4
0
0
3
2
8
2
4
0
Elaenia flavogaster
0
0
12
16
30
16
147
7
0
0
1
1
28
60
22
0
Elaenia cristata
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
Myiopagis gaimardii
1
7
40
58
13
1
3
0
16
15
12
41
57
2
3
0
Myiopagis caniceps
1
1
5
3
0
0
1
0
3
1
0
0
2
0
0
0
Tyrannidae
Tyrannidae
150
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Myiopagis flavivertex
1
0
0
0
0
0
0
0
0
1
0
5
0
0
0
0
Myiopagis viridicata
1
0
0
1
0
0
0
0
0
0
2
0
0
0
0
0
Tyrannulus elatus
1
1
18
7
11
0
2
0
8
10
7
15
19
6
9
0
Capsiempis flaveola
0
0
0
0
0
0
0
0
0
0
0
0
2
0
0
0
Attila cinnamomeus
1
1
1
1
1
0
0
0
0
0
0
2
2
2
0
0
Attila spadiceus
1
6
24
14
1
0
0
0
10
16
3
13
14
0
0
0
Legatus leucophaius
Ramphotrigon
megacephalum
1
0
8
10
17
0
3
0
0
2
2
0
2
5
0
0
1
0
2
0
0
0
0
0
0
0
0
0
0
0
0
0
Ramphotrigon ruficauda
1
0
4
3
1
0
0
0
1
0
3
5
2
0
0
0
Myiarchus tuberculifer
1
2
24
19
4
0
0
0
3
6
0
7
5
0
0
0
Myiarchus ferox
0
0
5
8
13
2
24
0
0
0
1
0
4
8
2
0
Myiarchus tyrannulus
0
0
0
0
0
0
0
0
0
0
1
1
5
10
3
0
Rhytipterna simplex
1
6
36
16
1
0
0
0
12
38
7
20
15
0
0
0
Casiornis fuscus
0
0
1
0
3
0
1
0
0
0
0
0
0
0
0
0
Pitangus sulphuratus
0
0
3
8
18
11
65
7
0
0
1
0
20
29
9
2
Philohydor lictor
Myiodynastes
maculatus
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
4
3
0
8
0
0
0
0
0
8
4
7
0
Tyrannopsis sulphurea
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
Megarynchus pitangua
1
0
2
4
9
0
4
1
0
0
0
2
10
13
5
0
Myiozetetes cayanensis
0
0
14
16
34
6
39
3
0
1
1
0
21
17
9
3
Myiozetetes luteiventris
Tyrannus
melancholicus
1
0
0
0
0
0
0
0
1
1
1
2
0
0
0
0
0
0
8
17
24
31
142
28
0
0
0
1
18
70
19
14
Tyrannus savana
Griseotyrannus
aurantioatrocristatus
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
4
1
0
2
0
0
0
0
0
0
0
0
0
0
0
0
0
Empidonomus varius
1
0
0
6
5
2
12
1
0
0
0
1
5
12
8
1
Conopias trivirgatus
1
0
0
0
0
0
0
0
1
1
4
5
2
0
0
0
Colonia colonus
1
1
7
2
0
0
0
0
0
0
0
0
0
0
0
0
Myiophobus fasciatus
0
0
0
2
5
6
94
9
0
0
0
1
4
13
0
1
Cnemotriccus fuscatus
0
0
0
1
18
0
0
0
0
0
0
0
0
0
0
0
151
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
Floresta
secundária
SANTARÉM
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Lathrotriccus euleri
1
0
3
10
1
0
0
0
0
0
0
0
0
0
0
0
Phaeomyias murina
0
0
1
7
31
20
155
5
0
0
0
0
20
41
28
3
Cyclarhis gujanensis
1
4
15
14
16
0
9
0
1
2
0
0
15
7
6
2
Vireolanius leucotis
1
0
0
0
0
0
0
0
16
24
4
10
2
0
0
0
Vireo olivaceus
Hylophilus
semicinereus
1
0
2
1
5
0
0
0
0
5
5
11
82
22
14
2
1
0
16
33
16
0
3
1
0
0
1
1
24
2
6
0
Hylophilus pectoralis
0
0
0
0
16
2
7
2
0
0
2
0
21
7
8
0
Hylophilus hypoxanthus
Hylophilus
ochraceiceps
1
0
0
0
0
0
0
0
21
26
7
21
6
0
0
0
1
5
0
0
0
0
0
0
2
3
1
0
0
0
0
0
Atticora tibialis
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
Stelgidopteryx ruficollis
0
0
1
9
16
9
73
16
0
0
0
0
1
3
0
2
Progne chalybea
1
0
9
43
30
23
130
32
1
0
5
2
15
36
6
9
Tachycineta albiventer
0
0
0
0
0
0
7
0
0
0
0
0
0
1
0
0
Riparia riparia
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
Hirundo rustica
0
0
0
0
1
0
11
8
0
0
0
0
0
8
0
9
Troglodytidae
Microcerculus
marginatus
1
5
8
0
0
0
0
0
6
10
2
6
3
0
0
0
Odontorchilus cinereus
1
0
0
0
0
0
0
0
6
0
0
0
0
0
0
0
Troglodytes musculus
Campylorhynchus
turdinus
Pheugopedius
genibarbis
0
0
0
5
10
10
144
10
0
0
0
0
7
89
15
10
1
0
0
0
0
0
0
0
5
3
0
2
5
1
0
0
1
8
110
120
97
0
16
1
0
0
0
0
0
0
0
0
Pheugopedius coraya
1
0
0
0
0
0
0
0
12
58
22
53
122
4
4
0
Cantorchilus leucotis
0
0
0
0
0
0
0
0
0
0
0
1
28
19
17
2
Cyphorhina arada
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
1
3
0
0
0
0
0
0
0
0
0
Vireonidae
Hirundinidae
Donacobiidae
Donacobius atricapilla
Polioptilidae
0
0
152
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Ramphocaenus
melanurus
1
9
50
81
24
0
0
0
1
15
10
20
21
1
0
0
Polioptila plumbea
0
0
0
9
7
0
6
0
0
0
0
0
0
0
0
0
Polioptila paraensis
1
2
2
1
0
0
0
0
2
1
0
0
0
0
0
0
Turdus leucomelas
0
0
5
10
17
4
17
1
0
0
0
0
8
8
2
0
Turdus fumigatus
1
1
3
0
0
0
0
0
1
6
0
0
0
0
0
0
Turdus albicollis
1
0
2
0
0
0
0
0
2
0
0
0
0
0
0
0
0
0
0
0
1
10
16
46
0
0
0
0
0
1
1
21
Ammodramus aurifrons
Ammodramus
humeralis
0
0
0
0
2
2
9
5
0
0
0
0
0
0
0
0
0
0
0
0
0
3
20
9
0
0
0
0
0
0
0
0
Arremon taciturnus
1
0
8
7
12
0
1
0
1
0
0
4
2
0
0
0
Parulidae
Geothlypis
aequinoctialis
0
0
0
0
5
2
73
2
0
0
0
0
0
0
0
0
Phaeothlypis rivularis
1
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
Psarocolius viridis
1
2
16
5
0
0
0
0
10
24
3
8
0
0
0
0
Psarocolius decumanus
1
0
0
0
0
0
0
0
2
1
1
0
6
3
0
0
Psarocolius bifasciatus
1
0
3
1
2
0
0
0
4
7
2
3
1
0
0
0
Cacicus haemorrhous
1
1
7
2
5
0
0
0
0
0
0
3
0
0
0
0
Cacicus cela
1
0
7
4
7
0
0
0
6
7
5
3
26
6
0
1
Icterus cayanensis
1
0
4
2
0
0
0
0
0
0
0
0
0
0
0
0
Icterus jamacaii
0
0
0
0
0
0
2
0
0
0
0
0
0
0
0
0
Molothrus oryzivorus
0
0
0
0
0
0
1
0
0
0
0
0
1
7
0
1
Molothrus bonariensis
0
0
0
0
0
3
7
1
0
0
0
0
0
3
1
1
Sturnella militaris
0
0
0
0
5
22
143
26
0
0
0
0
0
16
0
11
Mitrospingidae
Lamprospiza
melanoleuca
1
6
19
11
0
0
0
0
13
4
4
4
1
0
0
0
Turdidae
Motacillidae
Anthus lutescens
Passerellidae
Icteridae
153
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Thraupidae
Coereba flaveola
1
30
103
118
31
0
30
0
2
0
1
1
11
4
2
0
Saltator azarae
0
0
0
2
6
1
16
1
0
0
0
0
1
0
0
0
Saltator grossus
1
1
30
20
1
0
0
0
6
16
10
21
10
0
0
0
Saltator maximus
Parkerthraustes
humeralis
0
0
19
47
58
1
30
1
0
1
0
0
20
7
5
0
1
0
0
2
0
0
0
0
0
0
0
0
0
0
0
0
Nemosia pileata
1
0
1
0
0
0
1
0
0
0
0
0
0
0
0
0
Tachyphonus rufus
0
0
1
8
14
5
58
3
0
0
0
0
1
16
17
0
Ramphocelus carbo
1
1
58
92
95
11
136
9
1
2
4
4
65
52
24
1
Lanio luctuosus
1
2
6
8
0
0
0
0
1
0
1
0
7
0
0
0
Lanio versicolor
1
0
0
0
0
0
0
0
1
3
0
1
0
0
0
0
Lanio surinamus
1
6
4
0
0
0
0
0
0
2
0
1
0
0
0
0
Lanio cristatus
1
3
13
10
2
0
0
0
2
1
1
0
0
0
0
0
Lanio cucullatus
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
Tangara gyrola
1
3
12
4
2
0
0
0
0
0
0
0
0
0
0
0
Tangara mexicana
1
0
1
8
1
0
0
0
0
1
0
0
4
0
2
0
Tangara velia
1
2
3
3
1
0
0
0
1
0
0
1
0
0
0
0
Tangara varia
1
0
0
0
0
0
0
0
2
1
0
1
0
0
0
0
Tangara punctata
1
3
12
5
0
0
0
0
0
0
0
0
1
0
0
0
Tangara palmarum
1
1
10
14
9
2
20
2
2
0
3
10
37
42
16
4
Tangara episcopus
1
1
24
22
34
12
3
7
0
0
1
7
50
44
22
6
Cissopis leverianus
Schistochlamys
melanopis
0
0
0
2
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
3
0
30
1
0
0
0
0
0
0
0
0
Tersina viridis
1
1
4
1
0
0
0
0
0
0
0
0
0
0
0
0
Dacnis lineata
1
0
0
0
0
0
0
0
1
0
0
1
0
0
0
0
Dacnis cayana
1
1
4
6
1
0
0
0
0
0
2
0
2
0
0
0
Chlorophanes spiza
1
0
3
0
0
0
0
0
0
0
0
0
0
0
0
0
Hemithraupis guira
1
9
11
23
2
0
0
0
1
0
0
0
1
0
0
0
Cyanerpes caeruleus
1
0
0
2
0
0
0
0
0
0
0
0
0
0
0
0
154
Espécies/Família
Espécies
florestais
(1-sim, 0não)
PARAGOMINAS
Floresta primária
Não
perturnada
Corte
seletivo
Cortado e
queimado
SANTARÉM
Floresta
secundária
Silvicultura
Pasto
Agricultura
mecanizada
Floresta primária
Não
perturnada
Corte
seletivo
Queimado
Cortado e
queimado
Floresta
secundária
Pasto
Agricultura
familiar
Agricultura
mecanizada
Cyanerpes cyaneus
1
0
0
2
1
0
0
0
0
0
0
0
0
0
0
0
Emberizoides herbicola
0
0
0
0
0
0
2
1
0
0
0
0
0
0
0
0
Volatinia jacarina
0
0
0
1
7
11
106
9
0
0
0
0
15
71
33
35
Sporophila americana
0
0
0
0
5
2
20
3
0
0
0
0
0
0
1
0
Sporophila lineola
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
Sporophila nigricollis
0
0
0
0
2
1
5
0
0
0
0
0
1
7
7
10
Sporophila minuta
0
0
0
1
0
0
15
2
0
0
0
0
0
3
0
2
Sporophila angolensis
0
0
0
1
3
0
13
0
0
0
0
0
4
15
11
0
Granatellus pelzelni
1
0
26
6
2
0
0
0
3
1
1
0
4
0
0
0
Habia rubica
Caryothraustes
canadensis
Periporphyrus
erythromelas
1
0
0
0
0
0
0
0
1
0
1
2
1
0
0
0
1
2
27
26
4
0
0
0
0
0
0
0
0
0
0
0
1
5
5
0
0
0
0
0
1
0
0
0
0
0
0
0
Cyanoloxia rothschildii
1
1
5
10
1
0
1
0
0
3
3
6
11
0
0
0
Euphonia violacea
0
0
0
0
0
0
2
0
0
0
0
1
4
1
0
0
Euphonia rufiventris
1
0
0
0
0
0
0
0
0
2
2
0
1
0
0
0
Euphonia chrysopasta
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
Euphonia cayennensis
1
3
6
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
Cardinalidae
Fringillidae
Passer domesticus
155
ANEXO 2
Outros resultados
1)
Paragominas: a Quantitative Baseline Inventory of an Eastern
Amazonian Avifauna.
Publicado como: A.C. Lees, N.G. Moura, A. Santana, A. Aleixo, J. Barlow, E.
Berenguer, J. Ferreira, & T.A. Gardner. 2012. Paragominas: a Quantitative Baseline
Inventory of an Eastern Amazonian Avifauna. Revista Brasileira de Ornitologia 20, 7–
32.
Abstract
We present the results of a five-month survey of the birds of Paragominas, Pará, a
municipality in eastern Brazilian Amazonia that lies within the Belém center of
endemism. We recorded 440 species, sampling habitats across a gradient of
disturbance, ranging from ‘undisturbed’ primary forest, through logged and burnt forest,
patches of varyingly aged secondary forest, cattle pastures and intensive mechanized
agriculture. Given the potential for species miss-identifications in avian inventories, we
paid special attention to obtaining voucher documentation (photographs and sound
recordings) and here provide a unique collection of publically-accessible digital
vouchers for 418 species recorded (95% of the total). Many of the species reported
here are poorly- known or represent notable range-extensions, and we present data on
their status and distribution, both within the municipality and elsewhere in the Belém
center of endemism. Notable amongst these include the first records for Pará and
Amazonia of Spotted Piculet (Picumnus pygmaeus), trans-Tocantins range-extensions
for Large-headed Flatbill (Ramphotrigon megacephalum) and Yellow-shouldered
Grosbeak (Parkerthraustes humeralis) and multiple observations of the threatened
paraensis subspecies of Cinnamon- throated Woodcreeper (Dendrexetastes rufigula).
Keywords: Amazon; bird survey; conservation; digital voucher; range-extension.
2)
One hundred and thirty five years of avifaunal surveys around
Santarém, central Brazilian Amazon
156
Publicado como: Lees, A.C., Moura, N.G., Andretti, C.B., Davis, J.W., Lopes, E.V.,
Henriques, M.P., Aleixo, A., Barlow, J. Ferreira, J., & Gardner, T.A., 2013. One
hundred and thirty five years of avifaunal surveys around Santarém, central Brazilian
Amazon. Revista Brasileira de Ornitologia 21, 16–57.
Abstract
We present an updated annotated avifaunal checklist for the Santarém region of
central Pará state, Brazil, an area that has one of the oldest histories of ornithological
exploration in South America. We combine data from a five month quantitative survey
of the birds of the municipalities of Santarém and Belterra (east of the Tapajós River)
between 2010 and 2011 with an exhaustive search of material in museum collections
worldwide and digital vouchers deposited online. Our own survey sampled habitats
across a gradient of disturbance ranging from ‘undisturbed’ primary forest, through
logged and burnt forest, patches of secondary forest, cattle pastures and intensive
mechanized agriculture. Given the potential for species misidentifications in avian
inventories, we paid special attention to obtaining voucher documentation. Here we
present a collection of publicly accessible digital vouchers for all of the new species, in
addition to providing museum catalogue numbers for all old records. We added 24
species to the regional list, principally species associated with anthropogenic landuses, but also including seven species restricted to primary forest habitats which were
missed from both recent published inventories and over the course of two centuries of
intensive collecting efforts. The regional list now stands at 583 species for which
voucher documentation is available, with an additional 26 undocumented species.
Many of the species reported here are poorly known or represent notable range
extensions, and we present new data on their status and distribution.
Keywords: bird survey, Amazonia, conservation, range extension, digital voucher.
3)
A social and ecological assessment of tropical land-uses at multiple
scales: the sustainable amazon network
Publicado como:
Gardner, T.A., Ferreira, J., Barlow, J., Lees, A.C., Parry, L., Vieira, I.C.G., Berenguer,
E., Abramovay, R., Aleixo, A., Andretti, C., Aaragao, L.E.O., Araujo, I., Souza de Avila,
W., Bardgett, R.D., Batistella, M., Begotti, R.A., Beldini, T., Ezzine de Blas, D., Braga,
R.F., de Lima Braga, D., de Brito, J.G., de Camargo, P.B., Campos dos Santos, F.,
Campos de Oliveira, V., Cordeiro, A.C.N., Cardoso, T.M., de Carvalho, D.R., Castelani,
157
S.A., Chaul, J.C.M., Cerri, C.E., De Assis Costa, F., da Costa, C.D.F., Coudel, E.,
Coutinho, A.C., Cunha, D., D’Antona, A., Dezincourt, J., Dias-Silva, K., Durigan, M.,
Esquerdo, J.C.D., Feres, J., de Barros Ferraz, S.F., de Melo Ferreira, A.E., Fiorini,
A.C., da Silva, L.V.F., Frazao, F.S., Garrett, R., dos Santos Gomes, A., da Silva
Goncalves, K., Guerrero, J.B., Hamada, N., Hughes, R.M., Igliori, D.C., da Conceição
Jesus, E., Juen, L., Junior, M., de Oliveira Junior, J.M.B., de Oliveira Junior, R.C.,
Junior, C.S., Kaufmann, P., Korasaki, V., Leal, C.G., Leitao, R., Lima, N., de Fatima
Lopes Almeida, M., Lourival, R., Louzada, J., Mac Nally, R.C., Marchand, S., Maues,
M.M., Moreira, F.M.S., Morsello, C., Moura, N., Nessimian, J., Nunes, S., Oliveira,
V.H.F., Pardini, R., Pereira, H.C., Pompeu, P.S., Ribas, C.R., Rossetti, F., Schmidt,
F.A., da Silva, R., da Silva, R.C.V., da Silva, T.F.M., Silveira, J., Siqueira, J.V., de
Carvalho, T.S., Solar, R.R.C., Tancredi, N.S.H., Thomson, J.R., Torres, P.C Vaz-de
Mello, F.Z., Veiga, R.C.S., Venturieri, A., Viana, C., Weinhold, D., Zanetta, R., Zuanon,
J., 2013. A social and ecological assessment of tropical land uses at multiple scales:
the Sustainable Amazon Network. Phil. Trans. R. Soc. B 368 (1619), 20120166.
Abstract
Science has a critical role to play in guiding more sustainable development trajectories.
Here, we present the Sustainable Amazon Network (Rede Amazônia Sustentável,
RAS): a multidisciplinary research initiative involving more than 30 partner
organizations working to assess both social and ecological dimensions of land-use
sustainability in eastern Brazilian Amazonia. The research approach adopted by RAS
offers three advantages for addressing land-use sustainability problems: (i) the
collection of synchronized and co-located ecological and socioeconomic data across
broad gradients of past and present human use; (ii) a nested sampling design to aid
comparison of ecological and socioeconomic conditions associated with different land
uses across local, landscape and regional scales; and (iii) a strong engagement with a
wide variety of actors and non-research institutions. Here, we elaborate on these key
features, and identify the ways in which RAS can help in highlighting those problems in
most urgent need of attention, and in guiding improvements in land-use sustainability in
Amazonia and elsewhere in the tropics. We also discuss some of the practical lessons,
limitations and realities faced during the development of the RAS initiative so far.
Keywords: Tropical forests, land use, sustainability, trade-offs, interdisciplinary
research, social-ecological systems.
158
4) Instrução Normativa 02/2014 para classificação de florestas
secundárias para diferenciar áreas de produção e conservação no
Estado do Pará
Publicada no Diário Oficial do Estado do Pará. Caderno 5 , 28 de fevereiro de 2014, pp
6.
Autores: Gardner A. T.,
Ferreira, J., Barlow, J., Vieira, I.C.G., Chazdon, R.
Berenguer, E., Brancallion,P., Brondizio, E., Ferraz, S., Lees, A. C., Louzada, J.,
Mac Nally, R., Moura, N.G., Oliveira, V.H., Parry, L., Salomão,R.,
Solar, R.,
Thomson, J.
Instituições: constam no final do documento
20 de Fevereiro de 2014
Sumário
1
Descrição o problema
2
Sumário executivo da proposta
2 (i)
Evidências científicas para a elaboração da proposta
2(ii)
Vantagens da presente proposta
2(iii) Desvantagens e limitações da presente proposta
2(iv) Áreas de trabalho adicional necessário para implementar a proposta
2(v)
Áreas de trabalho adicional necessário para melhorar a proposta
3
Dados utilizados no estudo
4
Resumo das análises e resultados
5
Recomendações para os próximos passos e expansão do estudo das florestas
em regeneração para levar em conta fatores regionais e de paisagem
6
Autores e instituições
7
Agradecimentos
159
Tabela ou Figura
Tabela 1
Figura 1
Figura 2
Descrição
Número de áreas de florestas secundárias estudadas em
cada município e mesorregião do Pará
Distribuição da frequência de idade das áreas de
vegetação de florestas secundárias
Relação entre idade das áreas de floresta e riqueza
de espécies de árvores grandes (≥10 cm de DAP) e
pequenas (<10 cm de DAP)
Figura 3
Relação entre idade das áreas de floresta e riqueza de
espécies florestais de aves e besouros
Figura 4
Importância relativa dos fatores que regulam a
abundância de espécies de árvores grandes (≥ 10 cm de
DAP)
Figura 5
Figura 6
Relação entre área basal e biomassa acima do solo
Importância relativa dos fatores que regulam
presença de espécies florestais de aves e besouros
Figura 7
Relação entre a idade da floresta e área basal em
áreas de florestas secundárias em diferentes regiões do
Pará
Área basal total de árvores grandes em áreas de
vegetação de florestas secundárias que têm <5 anos,
entre 5-20 anos e > 20 anos de idade comparadas à
área basal total em áreas de floresta primária no estado
do Pará
Figura 8
Figura 9
Figura 10
a
Relação entre área basal e 1) cobertura do dossel 2)
densidade do sub- bosque em parcelas de vegetação de
floresta secundária em Santarém e Paragominas
Relação entre idade e área basal para parcelas de
vegetação de florestas secundárias entre 5 e 20 anos de
idade
1. Descrição do problema
A legislação do estado do Pará recomenda que em áreas designadas como
"zonas de consolidação agrícola" as propriedades rurais com menos de 80, mas
acima de 50 % de cobertura florestal, as florestas secundárias em estágio médioavançado de regeneração devem ser conservadas (Lei 7.398, Capitulo II, III, Artigo
4). Para implementar esta regulação, para fins de autorização de supressão de
160
vegetação nativa, entretanto, é necessário definir a forma de identificar o ponto de
separação entre as florestas em estágios iniciais de regeneração daquelas que
podem ser demonstradas em estágios intermediário a avançado de regeneração.
Para realizar esta definição um grupo de pesquisa multi-institucional elaborou a
proposta aqui apresentada a partir da realização de análises de um amplo banco de
dados de florestas secundárias para o Estado do Pará
.2. Sistema de decisão para classificação de florestas secundárias no estado do Pará
A proposta consiste em um processo simples de classificação em duas
etapas, baseado primeiramente na idade da floresta secundária sob avaliação, e em
segundo, lugar na combinação da cobertura de floresta primária do munícipio em
que está localizado o empreendimento e na medição do DAP (diâmetro do tronco
medido a 1,30m do solo) de todas as árvores com DAP ≥ 10cm nas parcelas da
floresta secundária sob avaliação para geração da área basal, onde:
1) Áreas demonstradas serem abaixo de 5 anos de idade podem ser
convertidas em áreas de produção sem necessidade de qualquer avaliação
de campo. Áreas demonstradas serem acima de 20 anos de idade são
recomendadas para proteção sem a necessidade de qualquer avaliação de
campo
2) Áreas demonstradas serem entre 5 e 20 anos de idade (incluindo 20) são
recomendadas para conservação se tiverem área basal igual ou acima de (a)
10 m2 ha-1 em municípios com mais de 50% de cobertura de floresta
primaria, e (b) 5 m2 ha-1 em municípios com menos de 50% de cobertura de
floresta primária.
2 (i). Evidências científicas para a elaboração da proposta

A idade é um forte indicador positivo da riqueza de espécies arbóreas e das
respectivas abundâncias na floresta (Figs. 2 e 4).

A estrutura, medida aqui pela área basal de árvores com DAP ≥ 10cm (um
parâmetro de estrutura da floresta muito simples e fácil de calcular, a partir
da medição do diâmetro, Fig. 6), é um indicador forte da riqueza de espécies
161
da fauna da floresta e da ocorrência de espécies arbóreas climáticas (clímax)
(Fig. 6)

Uma combinação da idade da floresta em regeneração e da sua área basal
fornece uma discriminação efetiva do estágio ecológico da floresta em
regeneração, levando-se em conta a diversidade de espécies da flora e
fauna.

Um limite de idade inferior a 5 anos separa áreas que consistentemente têm
baixa área basal total de árvores (DAP ≥ 10cm ) - 100% de 10 sítios de
estudo têm menos de 10 m2 ha-1) e podem ser licenciadas para serem
convertidas
à
produção
agrícola,
sem amostragens de campo da
vegetação, usando somente as imagens de satélite (Fig. 7).

Um
limite
de
idade
superior
a
20
anos
separa
áreas
que
consistentemente têm uma alta área basal total de árvores (DAP ≥10cm)
2
-1
- 89% dos 43 sítios de estudo são maiores do que 10 m ha ) e podem
ser recomendadas para conservação, sem amostragens de campo
adicionais, mas somente com as séries temporais das imagens de satélite
(Fig. 7 ).

Áreas em regeneração acima de 20 anos têm uma área basal
significativamente maior do que áreas de 5-20 anos de idade e são mais
semelhantes às florestas primárias (Fig.8)

Não existe uma relação clara entre a idade da floresta e área basal para
as parcelas entre 5 e 20 anos de idade (Fig. 7 ), mas o limite de área basal
de 10 m 2 ha-1 (árvores com DAP ≥ 10cm) está associada com um limite de
fechamento do dossel ( <20% de fração de abertura) e diminuição da
densidade da vegetação do sub-bosque (< 4.000 indivíduos por hectare),
indicando uma fase mais madura da regeneração que é menos dominada
por espécies pioneiras (Fig. 8).

Existe uma tendência nas regiões mais antropizadas do Estado, devido a
degradação do solo e da baixa conectividade florestal, para florestas
secundárias, mesmo de idades mais avançadas terem menos de 10 m2 ha1 de área basal (Fig. 10). Portanto, nos municípios com menos de 50%
cobertura de floresta primária (do ultimo ano antes do pedido de corte,
que sejadisponível nas imagens de PRODES) recomenda-se o uso de um
limite de 5 m2 ha-1 para autorização de supressão de vegetação nativa, ao
invés de 10 m2 ha-1. Tal medida mais conservadora oferece uma
162
salvaguarda essencial para a proteção dos serviços ecossistêmicos
prestados por estas florestas (Fig. 7 e 10).
2 ( ii) As vantagens do sistema de decisão aqui proposto incluem:
1. É simples e de baixo custo e evita a subjetividade quando na tomada de
decisão suprime/não suprime a vegetação. Observando-se que a idade
deverá ser avaliada por meio de análises de séries temporais de imagens de
satélite.
2. Oferece
uma
garantia
mínima
da
condição
ecológica
das
áreas
recomendadas para conservação com base em evidências de campo
3. Minimiza custos de transação e atrasos ao excluir parte das áreas dentro
dos limites máximo e mínimo de idades. Além do mais áreas com menos de
cinco anos de idade também correspondem à definição da Lei Federal para
pousio.
4.
Assegura
a proteção
proporcionando
de florestas em regeneração
benefícios
significativos
de
que já
conservação
e
estão
serviços
ambientais para o estado do Pará e que não tenham participado do sistema
de produção por pelo menos 20 anos consecutivos. Isso também inclui
áreas de floresta onde (apesar de terem pelo menos 20 anos de idade) a
regeneração foi impedida devido a motivos diversos como solo de baixa
fertilidade ou de uso intensivo no passado (por exemplo, os cinco locais na
Fig. 7, que têm acima de 20 anos, mas possuem uma área basal de < 10 m2
ha-1)
5. Depende de apenas uma medida objetiva e repetida da estrutura da floresta
(DAP ou Diâmetro a Altura do Peito) e não necessita de medidas estruturais
mais difíceis de coletar (como a altura da árvore) ou qualquer identificação
taxonômica das espécies.
6. Se não é possível avaliar a idade da área por sensoriamento remoto (por
exemplo, devido à cobertura excessiva de nuvem em anos consecutivos nas
séries temporais de imagem de satélite), então uma decisão suprime /não
suprime a vegetação pode ser feita com base apenas em uma pesquisa de
campo sobre a estrutura da vegetação (determinação da área basal).
163
7. Assegura a proteção de florestas
proporcionando
benefícios
em regeneração
significativos
de
que
conservação
já
e
estão
serviços
ecossistêmicos para os municípios do estado do Pará que têm uma baixa
quantidade de remanescentes de floresta primária, e histórico de uso da
terra intensivo (indicado por aqueles municípios com menos de 50% de
cobertura florestal primária)
2 (iii) As desvantagens e limitações do sistema de decisão proposto incluem:
1. Exige uma amostragem de campo da vegetação para fazer uma avaliação
de área basal nas áreas que têm entre 5 e 20 anos de idade.
2. Qualquer avaliação do estágio de regeneração com base em medidas de
estrutura da floresta poderia ser manipulada por proprietários de terra por
meio do corte seletivo de árvores de grande porte para reduzir a área basal
total abaixo do limite de 10 m2 ha-1. Neste sentido, qualquer evidência de
corte recente ou queimada nessas florestas tem que ser anotado e
comunicado ao Ibama.
3. Uma amostragem (inventário) tendenciosa da vegetação secundária poderia
alocar as parcelas naquelas áreas onde se têm os menores valores de área
basal.
2(iv) Áreas de trabalho adicional necessário para implementar o sistema de decisão
proposto
1.Definição de fontes de dados e imagens, e um protocolo para avaliar a
idade das florestas secundárias usando uma série temporal de imagens
Landsat
2. Definição de um protocolo de pesquisa de vegetação padronizado para
avaliar a área basal de árvores com DAP ≥ 10cm, incluindo:
a) Área total a ser amostrada
b) Tamanho padronizado da parcela
c) Densidade padronizada de parcelas
164
d) Protocolo padronizado para determinar a distribuição de parcelas de
vegetação dentro de uma dada área.
e) Definição do tamanho mínimo da área de floresta em regeneração que
necessita de licenciamento para liberação de conversão para agricultura.
f) Definição de critérios regulatórios adicionais para assegurar que os
proprietários rurais não sejam capazes de manipular as áreas de regeneração
florestal para colocá-las abaixo do limiar de 5 ou 10 m2ha-1 dependendo do
município
2 (v) Análises futuras recomendadas para facilitar a aplicação do sistema de
decisão desta proposta:
1. Mapeamento de idades de florestas secundárias em todo o estado do Pará
feita pelo órgão público de fiscalização- modelo DETER, que auxilie o Ibama
a checar o desflorestamento quando ele acontece - para fornecer uma fonte
de dados definitiva (atualizada em uma base anual) que permita avaliar a
idade das áreas dentro de uma determinada propriedade rural. Isso requer
uma análise de séries temporais de dados do Landsat para os últimos 20
anos para identificar a idade de cada pixel de floresta secundária com base
no histórico de desmatamento e uso. Este mapa facilitaria enormemente a
avaliação rápida e defensável para saber se uma determinada área é
imediatamente recomendada para conservação (> 20 anos) ou pode ter a
vegetação suprimida sem necessidade de qualquer amostragem de campo
(inferior a cinco anos de idade), ou requer avaliação da área basal antes que
qualquer decisão possa ser feita (entre 5 e 20 anos de idade). O mesmo
mapa também permitiria uma avaliação dos benefícios regionais de
conservação
(aumento
da
área
de
floresta
e
conectividade entre
fragmentos) e custos de oportunidade agrícola para garantir a proteção de
todas as florestas > 20 anos de idade . No momento, as avaliações de idade
das áreas em regeneração precisariam ser realizadas com base em análises
específicas para cada propriedade individual.
2. Mapeamento da área basal da vegetação arbórea para todo o Pará. Isso
pode ser feito usando dados RADAM e, também, dos novos inventários
florestais programados pelo Serviço Florestal Brasileiro para o estado em
uma modelagem espacial para produzir
165
um mapa da área basal de árvores com DAP ≥10cm para todo o estado.
3. Teste da aplicação de técnicas adicionais de datação da idade das florestas
secundárias que não precisam utilizar dados de satélite. Uma alternativa
possível é a contagem de nós ao longo do caule para datar as árvores d do
gênero Cecropia (embaúba). Esta técnica foi desenvolvida e publicada em
trabalhos científicos.
Dados usados na presente análise
Dois conjuntos de dados foram utilizados na análise da presente proposta
para fornecer as recomendações aqui apresentadas
1. Dados do Projeto Rede Amazônia Sustentável (RAS), uma parceria entre
vários projetos no âmbito do INCT-MPEG, EMBRAPA, Universidade de
Lancaster e Universidade de Cambridge para avaliar a relação entre a idade
das áreas de florestas secundárias, área basal e outros atributos de
estrutura e composição de espécies da flora e fauna. Este conjunto de
dados é composto por um total de 60 áreas de florestas secundárias (20 em
Paragominas e 40 em Santarém), bem como 30 áreas de florestas primárias
não perturbadas, usadas como condição de referência.
2. Um banco de dados de florestas secundárias para diferentes regiões do
estado composto de dados de campo de quatro projetos
a. RAS (Santarém e Paragominas) =
61
sítios
b.
Ima
Vieira
(vários
municípios) = 38 sítios
c. Eduardo Brondizio (vários municípios) = 36
sítios d. Jos Barlow (Almeirim) = 5 sítios
e. Total = 140 sítios
Para ser qualificado na inclusão da meta-análise do Estado, os dados dos
projetos individuais deveriam conter (a) a idade da floresta secundária avaliada, (b)
as medidas de DAP por indivíduo, e (c) a identificação em nível de espécie para
cada indivíduo. Nos dados do projeto RAS, um conjunto de florestas secundárias
foram
identificadas
nas
imagens
de satélite desde as primeiras medições
registradas pelo INPE (1988). Desta forma, não se pôde determinar a idade exata
destas florestas, mas apenas inferir que as mesmas teriam mais de 22 anos
166
durante o período das medidas de campo, sendo a idade destas florestas então
registrada como desconhecida.
No total, nós conseguimos reunir dados de 140 sítios de florestas secundárias,
abrangendo 22 municípios em cinco das seis meso-regiões do Pará (não havia
dados disponíveis para a região metropolitana de Belém) (Tabela 1).
Tabela 1: Dados das pesquisas em florestas secundárias incluídos na metaanálise para o estado do Pará.
Município ou região
Mesorregião
Número de sítios
Abaetetuba
Nordeste Paraense
2
Abel Figueiredo
Sudeste Paraense
1
Acará
Nordeste Paraense
1
Almeirim
Baixo Amazonas
5
Altamira
Sudoeste Paraense
11
Aurora do Pará
Nordeste Paraense
1
Bom Jesus do Tocantins
Sudeste Paraense
1
Capitão Poço
Nordeste Paraense
6
Dom Eliseu
Sudeste Paraense
2
Igarapé-Açu
Nordeste Paraense
10
Ipixuna do Pará
Nordeste Paraense
2
Irituia
Nordeste Paraense
1
Jacundá
Sudeste Paraense
2
Moju
Nordeste Paraense
1
Paragominas
Sudeste Paraense
21
Ponta de Pedras
Marajo
4
Rondon do Pará
Sudeste Paraense
2
Santarém
Baixo Amazonas
41
167
São Francisco do Pará
Nordeste Paraense
11
Tailândia
Nordeste Paraense
2
Tome-acu
Nordeste Paraense
11
Ulianópolis
Sudeste Paraense
2
22 (de 144)
5 (de 6)
140
Os sítios de estudo estão distribuídos em um amplo gradiente de idade variando
entre 1-70 anos (Fig. 2).
Figura 1. Distribuição da frequência de idade dos sítios de pesquisa utilizados nas
análises. Notar que 26 sítios (projeto RAS) têm apenas uma estimativa mínima
idade determinada por séries temporais imagens de satélite ( ≥ 22 anos) .
Análises e resultados
As análises realizadas atenderam dois objetivos principais:
1. Avaliação da utilidade da idade e da estrutura da floresta (área basal) como
critérios mínimos baseados no local para classificar as florestas em
regeneração no Pará. [utilizando apenas dados da RAS]
2. Identificação de limiares da idade da floresta e da estrutura da vegetação
para orientar recomendações de decisões de suprimir/não suprimir a
168
vegetação para o estado do Pará [usando tanto dados da RAS quanto dados
de outros projetos para diferentes regiões do estado]
OBJETIVO 1: Avaliação da utilidade da idade e estrutura da floresta como critérios
mínimos baseados no local para classificar a regeneração de florestas no Pará
Esta análise avaliou a evidência para o uso da idade da floresta e da estrutura
da vegetação (área basal) como indicadores da condição ecológica, medida em
termos de diversidade de espécies da floresta.
Resultados-chave

A idade da floresta secundária é um indicador positivo da riqueza e
abundância de espécies de árvores (DAP < 10cm) (Fig. 2a); assim como da
proporção entre árvores com DAP ≥10cm e árvores com DAP <10cm ( Fig.
2b ). No entanto, a idade não foi um bom indicador do número de espécies da
fauna (aves e besouros) dependentes da floresta ( Fig. 3).

A idade da floresta secundária é o mais importante indicador de mudanças na
abundância de espécies de árvores com DAP ≥ 10cm Fig. 4).

A área basal de árvores com DAP ≥10cm é um forte indicador positivo da
biomassa aérea e , por conseguinte, dos estoques de carbono da floresta (Fig.
5).

A estrutura da área (medida pela biomassa aérea) e a composição florística da
vegetação são os fatores mais importantes que atuam na regulação da
presença de espécies de aves e besouros (Fig. 6)
Resumo das recomendações com base nos resultados
A combinação da idade da floresta secundária e da estrutura da vegetação,
medida em termos de área basal de árvores (DAP ≥10cm) (em si um bom indicador
da biomassa total acima do solo), explica uma quantidade significativa da variação
na diversidade de espécies de árvores, aves e besouros. A combinação destes
parâmetros pode, portanto, ser utilizada como indicador mínimo (sem medidas
adicionais de condição da paisagem, história local e tipo de solo), porém adequado
para indicar a condição ecológica das florestas em regeneração.
OBJETIVO 2: Identificação de limiares de idade da floresta e de estrutura da
vegetação para orientar as recomendações da decisão desmata/não desmata para o
estado do Pará
169
Resultados-chave

Um limite de idade inferior a 5 anos separa áreas que têm consistentemente
baixa área basal (< 10 m2 ha-1) e, um limite de idade superior a 20 anos
separa áreas que têm consistentemente alta área basal (>10 m2 ha-1) ( Fig.
7)

As três classes de idade de florestas em regeneração (<5 , 5-20 e > 20 anos)
são significativamente diferentes entre si em termos de área basal para
árvores com DAP ≥ 10 cm. Os sítios com mais de 20 anos de idade têm
áreas basais significativamente maiores do que aqueles entre 5-20 anos, e as
florestas primárias (em diferentes regiões do Pará) têm área basal total
significativamente maior que sítios com mais de 20 anos de idade (Fig. 8).

Não existe uma relação clara entre a idade da floresta secundária e a área
basal para as áreas entre 5 e 20 anos de idade (Fig. 7 ), mas o limite de
2
-1
área basal de 10 m ha (DAP ≥ 10cm) está associado com um limite de
fechamento do dossel (<20% fração de abertura) e diminuição da densidade
da vegetação do sub-bosque (< 4.000 indivíduos por hectare), indicando uma
fase mais madura da regeneração que é menos dominada por espécies
pioneiras (Fig. 8)

A maior área basal no sudoeste do Pará (região de solos férteis, mais
recentemente colonizada, com 100 % dos sítios com área basal superior a 10
m2 ha-1) em comparação com o nordeste do Pará (a mais antiga região de
ocupação na Amazônia brasileira, com baixa nível de remanescentes
florestais, 68 % dos sítios com área basal inferiores a 10 m2 ha-1),
independentemente da idade para florestas entre 5 e 20 anos de idade (Fig.
10). Assim, assumindo uma limiar de 5 m2 ha-1 (a metade de 10 m2 ha-1)
para aqueles municípios que têm menos de 50% de cobertura florestal
primária ajudaria compensar essa importante tendência (Fig. 7 e10).
Resumo das recomendações com base nos resultados
O limite inferior e superior de 5 e 20 anos de idade, separa respectivamente,
áreas que têm consistentemente baixa e alta área basal e pode, portanto, ser usado
170
para determinar as áreas de florestas secundárias que podem ser licenciadas para
conversão ou recomendadas para a conservação sem a necessidade de avaliação
adicional de campo. Para áreas entre 5 e 20 anos de idade a decisão suprimir/não
suprimir a vegetação pode ser feita com base em uma avaliação de campo para
cálculo da área basal, na qual áreas que tenham área basal superior a 10 m2 ha-1
seriam recomendadas para a conservação.
Deve ser reconhecido que qualquer avaliação dependente apenas de critérios
baseados na escala local vai deixar de considerar devidamente as variações
regionais nas taxas de regeneração devido a diferenças naturais (por exemplo, na
fertilidade do solo) bem como as diferenças na condição da paisagem (por exemplo,
ausência virtual de áreas de floresta primária vizinha ou extremamente fragmentada)
ou a intensidade do uso do solo no passado. Consequentemente, qualquer critério de
área basal que seja utilizado para determinar a decisão de desmatar/não desmatar
resultará em um viés em favor da conservação de florestas regenerando em áreas
mais férteis que sofreram menor impacto humano (por exemplo, paisagens jovens
perto da fronteira de desmatamento) e um viés em favor de permitir a conversão de
florestas regenerando em áreas inférteis ou altamente degradadas (veja Fig.10).
2
-1
.Assim propomos o uso de dois limiares de área basal: 5 m ha para municípios
com menos de 50% de cobertura de florestas primárias (das imagens de PRODES do
ultimo ano disponível antes do pedido de supressão de vegetação nativa), e 10
2
-1
m ha para os municípios com mais de 50% cobertura de floresta primária.
171
Figura 2. Relação entre idade das florestas secundárias e riqueza de espécies
florestais de árvores grandes (≥ 10 cm de DAP ) e pequenas ( <10 cm de DAP ).
Fonte de dados: Projeto RAS.
Figura 3. Relação entre idade das florestas secundárias e riqueza de espécies
de aves e besouros. Fonte de dados: Projeto RAS.
172
Figura 4. Importância relativa dos fatores que regulam a distribuição de 88 espécies
florestais de árvores grandes (≥ 10 cm de DAP ) (valores médios de importância das
variáveis a partir de árvores de regressão Random Forests para cada espécie ).
Fonte de dados: Projeto RAS.
Figura 5. Relação entre área basal e biomassa acima do solo. Equações de
biomassa padronizadas para todos os sítios e descritas em Gardner et al. 2012,
Phil. Trans. R. Soc. B 2013 368, 20120166). Fonte de dados: Projeto RAS.
173
Figura 6. Importância relativa dos fatores que regulam a presença de espécies
florestais de aves e besouros. Fonte de dados: Projeto RAS.
Figura 7. Idades das áreas de floresta secundária e área basal para 140 áreas de
florestas secundárias em diferentes regiões do Pará . Os pontos cinza representam
locais onde se conhece apenas que tenham pelo menos 22 anos de idade. As linhas
verticais vermelhas tracejadas representam os limites de idade propostos para
separar consistentemente as áreas de baixa ( 100% dos sítios) e alta (89% dos
174
sítios) área basal em relação ao limiar de 10 m2 ha-1 de área basal. Fonte de
dados: Diversos projetos para diferentes regiões do Pará.
Figura 8. Área basal total de árvores grandes em sítios de floresta secundária < 5
anos, 5-20 anos e > 20 anos de idade, bem como áreas de floresta primária (em
diferentes regiões do Pará). Existem diferenças significativas (p < 0,001) entre
todas as comparações (Teste Tukey de diferença significativa). Fonte de dados:
Diversos projetos para diferentes regiões do Pará.
175
Figura 9. Relação (e ajuste de curva não-linear), entre área basal e cobertura do
dossel de floresta e área basal e densidade do sub-bosque em 60 áreas de floresta
em regeneração em Santarém e Paragominas . Fonte de dados: Projeto RAS.
176
Figura 10. Relação entre a idade e área basal para áreas de florestas secundárias
entre 5 e 20 anos de idade. Os sítios em vermelho são no nordeste paraense e em
verde são do Sudoeste paraense. O restante das regiões estão em cinza.
6. Lista de Autores e respectivas instituições

Toby Gardner. Universidade de Cambridge, Reino Unido
 Joice Ferreira. Embrapa Amazônia Oriental, Brasil
 Jos Barlow. Universidade de Lancaster , Reino Unido
 Ima Vieira. Museu Paraense Emílio Goeldi, Brasil
 Robin Chazdon. Universidade de Connecticut, Estados Unidos
 Erika Berenguer. Universidade de Lancaster , Reino Unido

Pedro Brancallion. Univ. de São Paulo, Escola Superior de Agricultura
"Luiz de Queiroz", Brasil
 Eduardo Brondizio. Universidade de Indiana, Estados Unidos
 Silvio Ferraz. Univ. de São Paulo, Escola Superior de Agricultura "Luiz de
Queiroz", Brasil
 Alexander Lees. Museu Paraense Emílio Goeldi, Brasil
 Julio Louzada. Universidade Federal de Lavras, Brasil
 Ralph MacNally. Universidade Monash, Austrália
 Nárgila Moura. Museu Paraense Emílio Goeldi, Brasil
 Victor Oliveira. Universidade Federal de Lavras, Brasil

Luke Parry. Universidade de Lancaster , Reino Unido
 Rafael Salomão. Museu Paraense Emílio Goeldi, Brasi
 Ricardo Solar. Universidade Federal de Viçosa, Brasil
 Jim Thomson. Universidade Monash, Austrália
7. Agradecimentos
A Rede Amazônia Sustentável (RAS) é uma iniciativa multi-institucional focada
na avaliação da sustentabilidade social e ecológica dos sistemas de uso da terra na
Amazônia
Oriental
e
envolve
mais
de
30
organizações
parceiras
(ver
www.redeamazoniasustentavel.org). A Rede Amazônia Sustentável (RAS) é grata
pelo apoio financeiro às seguintes instituições: Instituto Nacional de Ciência e
Tecnologia - Biodiversidade e Uso da Terra na Amazônia (CNPq 574008/20080), Empresa Brasileira de Pesquisa Agropecuária - Embrapa
(SEG:
02.08
.06.005.00), Iniciativa Darwin do governo do Reino Unido (17-023), TNC-The Nature
Conservancy e Conselho Britânico de Pesquisa do ambiente natural (NERC)
(NE/F01614X/1 e NE/G000816/1). A Rede Amazônia Sustentável também é grata a
Embrapa, TNC, LBA- Experimento de Grande Escala da Biosfera-Atmosfera na
Amazônia, Universidade Federal d'Oeste do Pará, Universidade Estadual do Pará e
aos sindicados dos agricultores e sindicatos dos trabalhadores rurais de Santarém,
Belterra e Paragominas e a todos os produtores rurais por seu apoio no campo.
178

Moura, N. 2014 - Sustainable Amazon

Transcription

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