Two Hundred Years of Local Avian Extinctions in Eastern Amazonia

Contributed Paper
Two Hundred Years of Local Avian Extinctions
in Eastern Amazonia
NÁRGILA G. MOURA,∗ ALEXANDER C. LEES,†‡‡ ALEXANDRE ALEIXO,† JOS BARLOW,†‡
SIDNEI M. DANTAS,† JOICE FERREIRA,§ MARIA DE FÁTIMA C. LIMA,†
AND TOBY A. GARDNER¶∗∗ ††
∗
Curso de Pós-Graduação de Zoologia, Universidade Federal do Pará/Museu Paraense Emı́lio Goeldi, Caixa Postal 399, CEP 66040-170,
Belém, Pará, Brazil
†Coordenação de Zoologia, Museu Paraense Emı́lio Goeldi, Caixa Postal 399, CEP 66040-170, Belém, Pará, Brazil
‡Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, United Kingdom
§Embrapa Amazônia Oriental, Trav. Dr. Enéas Pinheiro s/n, CP 48, CEP 66095–100 Belém, PA, Brazil
¶Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, United Kingdom
∗∗
International Institute for Sustainability, Rio de Janeiro, CEP 22460-320, Brazil
††Stockholm Environment Institute, 87D Linegatan, Stockholm, Sweden
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.
Using extensive historical data sets of specimen records and results of contemporary surveys, we searched
for evidence of local extinctions of a terra firma rainforest avifauna over 200 years in a 2500 km2 eastern
Amazonian region around the Brazilian city of Belém. 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 occurrences 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 on the International
Union for Conservation of Nature Red List, and many of these are large-bodied. 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 ongoing loss and degradation of remaining areas of native vegetation across eastern
Amazonia.
Keywords: avifauna, colonization, forest dependency, IUCN Red List, sighting record, urban conservation
Doscientos Años de Extinciones Locales de Aves en la Amazonia Oriental
Resumen: Las extinciones locales, regionales y globales causadas por la pérdida, degradación y fragmentación de hábitat se han reportado ampliamente para los trópicos. Los patrones y conductores de esta
pérdida de especies son ahora muy conocidos en la Amazonia, pero aún persiste un vacı́o significativo
en el entendimiento de las tendencias a largo plazo en la persistencia de las especies y la extinción en
terrenos antropogénicos. Dicha perspectiva histórica es crı́tica para entender el estado y las tendencias de
la biodiversidad existente ası́ como para identificar prioridades que detengan las pérdidas futuras. Al usar
‡‡ Address
correspondence to A. C. Lees, email [email protected]
Paper submitted October 30, 2013; revised manuscript accepted January 26, 2014.
1
Conservation Biology, Volume 00, No. 0, 1–11
C 2014 Society for Conservation Biology
DOI: 10.1111/cobi.12300
2
Avian Extinctions in Amazonia
juegos de datos históricos extensivos de registros de especı́menes y resultados de sondeos contemporáneos,
buscamos evidencias de extinciones locales de avifauna en una selva de tierra firme a lo largo de 200 años
en una región de 2, 500 km2 en la Amazonia oriental, cerca de la ciudad brasileña de Belém. Esta región
tiene la mayor historia de trabajo de campo ornitológico en toda la cuenca del Amazonas y yace en el
altamente amenazado Centro de Endemismo de Belém. También comparamos nuestros eventos de extinción
inferidos históricamente con los datos extensos de la ocurrencia de especies en una muestra de zonas de
influencia en una municipalidad cercana (Paragominas) que engloba un gradiente de pérdidas pasadas de
bosque. Encontramos evidencias de la extinción posible de 47 especies (14% del acervo regional de especies)
que no se reportaron de 1980 a 2013 (80% fue reportado por última vez entre 1900 y 1980). Diecisiete
especies aparecen en la Lista Roja de la UICN, y muchas de estas son de gran tamaño. Las especies perdidas
en la región inmediata a Belém son similares a aquellas que actualmente están restringidas a zonas de
influencia con bosques bien desarrollados en Paragominas. Aunque anticipamos el futuro redescubrimiento
o recolonización de algunas especies que se infiere están extintas de acuerdo a nuestros cálculos, también
esperamos que probablemente existan extinciones locales adicionales, no reportadas aquı́, dada la pérdida y
degradación continua de las áreas restantes de vegetación nativa a lo largo de la Amazonia oriental.
Palabras Clave: avifauna, colonización, conservación urbana, dependencia de bosque, Lista Roja de la UICN,
registro de avistamientos
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
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 space-for-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 long-term 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 field-
Conservation Biology
Volume 00, No. 0, 2014
work 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 (Laurance et al.
2011). Thus, a major knowledge gap relating to the conservation of Amazonian biota is an understanding of longterm trends in species persistence and extinction in the
human-modified landscapes that increasingly characterize the region.
Arguably the most threatened region of Amazonia is
the 243,000 km2 Belém Center of Endemism (BCE) in
northeastern Pará and W 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 & Vieira 2010). Most of
this remaining forest is heavily fragmented and degraded
by recurrent selective-logging and fire events, as well as
overextraction of game animals and other nontimber forest resources (Almeida & 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
Moura et al.
3
70°0'W
60°0'W
50°0'W
40°0'W
0
250
500 Km
0°0'
0°0'
1.
2.
10°0'S
10°0'S
20°0'S
20°0'S
a)
30°0'S
b)
0
5
10 Km
c)
30°0'S
70°0'W
60°0'W
50°0'W
40°0'W
30°0'W
Figure 1. (a) The state of Pará in Brazil, (b) position of the study areas (1, metropolitan region of Belém (MRB);
2, Paragominas in Pará), and (c) the extent of remaining forest cover in the MRB (black, forest; dark gray,
secondary forest; light gray, urban; white agricultural; hatched, water).
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 it was
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 & 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 50 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.
Methods
Study Site
The 2537 km2 MRB (approximately 1°S, 48°ʹW, Fig. 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 & Lima 2009). Local climate
details are in Supporting Information.
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 onward, a highway that connects
Belém to São Luı́s in Maranhão state, and later associated
with the construction of the Bragança railway, between
1883 and 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 (6399 km2 ), most of
which are severely degraded due to ongoing disturbance
events such as fire, selective-logging, and illegal hunting
(Leão et al. 2007).
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
Conservation Biology
Volume 00, No. 0, 2014
Avian Extinctions in Amazonia
4
source of specimen data came from digitized records
of study skins deposited at the Museu Paraense Emı́lio
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 & 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 (Supporting Information).
Through the compilation of data from multiple sources,
we compiled a sighting record for each species. A full
compilation of our data sources is listed in Supporting
Information.
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 (nonstationary 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
t1 = 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 TE U = tn /α 1/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 5000 ha) in the municipality of Paragomi-
Conservation Biology
Volume 00, No. 0, 2014
nas (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, nonforest)
across each 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 before the species can be considered
extinct.
Results
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 20th century; 80% of candidate extinctions were recorded between 1900 and 1980 (Table 1).
We were able to estimate extinction probabilities for 26
(for which number of records was ࣙ4). Ten species were
Moura et al.
5
Table 1. Species unrecorded in the last 33 years in the metropolitan region of Belém.
Scientific namea
English common name
Penelope pileata
Aburria cujubi
Pauxi tuberosa
Odontophorus gujanensis
Sarcoramphus papa
Accipiter poliogaster
Accipter superciliosus
Harpia harpyja
Spizaetus melanoleucus
Spizaetus ornatus
Daptrius ater
Micrastur mirandollei
Micrastur semitorquatus
Psophia obscura
Anodorhynchus hyacinthinus
Ara macao
Ara chloropterus
Guarouba guarouba
Pyrrhura lepida
Touit huetii
Deroptyus accipitrinus
Neomorphus geoffroyi
Lophornis gouldii
Calliphlox amethystina
Piculus chrysochloros
Celeus torquatus
Hylopezus macularius
Sclerurus caudacutus
Sclerurus rufigularis
Dendrocincla merula
Deconychura longicauda
Dendrexetastes rufigula
Berlespchia rikeri
Philydor ruficaudatum
Philydor erythrocercum
Myiobius atricaudus
Phoenicircus carnifex
Gymnoderus foetidus
Platyrinchus platyrhynchos
Platyrinchus saturatus
Piprites chloris
Corythopis torquatus
Hylophilus ochraceiceps
Lamprospiza melanoleuca
Dacnis lineata
Periporphyrus erythromelas
Euphonia minuta
White-crested Guan
Red-throated Piping-Guan
Razor-billed Curassow
Marbled Wood-Quail
King Vulture
Gray-bellied Hawk
Tiny Hawk
Harpy Eagle
Black-and-white Hawk-Eagle
Ornate Hawk-Eagle
Black Caracara
Slaty-backed Forest-Falcon
Collared Forest-Falcon
Dark-winged Trumpeter
Hyacinth Macaw
Scarlet Macaw
Red-and-green Macaw
Golden Parakeet
Pearly Parakeet
Scarlet-shouldered Parrotlet
Red-fan Parrot
Rufous-vented Ground-Cuckoo
Dot-eared Coquette
Amethyst Woodstar
Golden-green Woodpecker
Ringed Woodpecker
Spotted Antpitta
Black-tailed Leaftosser
Short-billed Leaftosser
White-chinned Woodcreeper
Long-tailed Woodcreeper
Cinnamon-throated Woodcreeper
Point-tailed Palmcreeper
Rufous-tailed Foliage-gleaner
Rufous-rumped Foliage-gleaner
Black-tailed Flycatcher
Guianan Red-Cotinga
Bare-necked Fruitcrow
White-crested Spadebill
Cinnamon-crested Spadebill
Wing-barred Piprites
Ringed Antpipit
Tawny-crowned Greenlet
Red-billed Pied Tanager
Black-faced Dacnis
Red-and-Black Grosbeak
White-vented Euphonia
a Our taxonomy follows the checklist of
b Number of records.
c The interval between the first and last
d The time interval between the
e The p values shown are based
Last
record nb
1870
1835
1959
1906
1898
1915
1968
1894
1962
1812
1848
1835
1968
1922
1812
1900
1906
1848
1968
1969
1912
1912
1967
1926
1963
1968
1968
1967
1972
1968
1968
1936
1935
1968
1965
1968
1930
1912
1968
1972
1965
1972
1969
1965
1926
1905
1960
2
1
6
7
1
3
6
2
1
1
1
1
2
9
1
4
6
3
4
4
4
4
9
1
6
1
6
5
18
6
3
1
4
1
6
6
10
1
9
12
2
11
8
8
6
1
3
tn c
Td
Solowe
124
71
133
87
88
94
156
71
100
100
55
62
133
42
60
5
34
86
96
72
56
60
124
66
130
47
-
178
178
178
178
201
104
201
115
201
201
101
112
178
88
101
50
112
134
141
95
101
101
165
110
178
134
-
0.164
0.004
0.233
0.003
0.084
0.523
0.468
0.235
0.123
0.123
0.008
0.052
0.233
0.052
0.000
0.00
0.028
0.109
0.146
0.083
0.009
0.003
0.057
0.028
0.111
0.005
-
Estimated
Upper
Sighting
Mean
extinction year 95% bound
rate
weight (g)
1918
1931
1974
1976
1969
1946
1975
1977
1978
1935
-
1952
1956
1992
1984
1972
1993
1993
1981
2004
1965
-
0.108
0.991
0.178
0.000
0.020
0.491
0.417
0.150
0.046
0.046
0.001
0.015
0.178
0.010
0.000
0.00
0.001
0.000
0.090
0.046
0.001
0.000
0.032
0.007
0.070
0.000
-
1260
1407
2813
314
3337
420
104
6550
751
1215
352
517
631
1071
1565
1245
1479
260
75
60
255
363
2
2
66
124
40
38
22
53
26
70
35
27
25
10
84
283
13
13
19
17
15
35
11
48
9
Brazilian birds compiled by the Comitê Brasileiro de Registros Ornitológicos (CBRO 2011).
record.
year of the first sighting and the target year (2013).
on the Solow equation (Solow 1993, 2005).
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. 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. 2) because all are susceptible to
local extinction following habitat loss and hunting (e.g.,
Peres 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 1).
Forest Dependency of Threatened Species
In comparing our historical analysis with contemporary
avian surveys in the municipality of Paragominas, we
found that 8 species recorded as extinct (since 1980)
in the MRB were also unrecorded in Paragominas. Thirtynine species considered extinct in the MRB persisted in
Paragominas, although 5 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.
Conservation Biology
Volume 00, No. 0, 2014
6
Avian Extinctions in Amazonia
Figure 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; half-filled diamond, species
extant based on Solow equation and extinct based on sighting rate; half-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).
(2011). Eight of 11 threatened (from any list) species
that were still extant in the MRB were also recorded in
Paragominas (Supporting Information).
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
Conservation Biology
Volume 00, No. 0, 2014
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. 3, nonlinear exponential model r2 = 0.16; p < 0.05). Species
recorded in fewer catchments were more susceptible
to local extinction (last recorded longer ago). Among
Moura et al.
7
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. Thirteen of the 15 species last recorded before
1900 were either large-bodied (>1 kg) game birds, raptors, or psittacids of high commercial value (Supporting
Information).
A combined analysis of sighting records, threat status,
and estimates of the ease of detection revealed 15 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).
Figure 3. Relationship between inferred extinction
date (year) in the Metropolitan region of Belém and
number of catchments occupied in Paragominas,
Brazil (r2 = 0.16, p < 0.05).
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 (Supporting
Information).
Reassessment of Species Threat Status
Fifteen (31%) of the 47 species unrecorded since 1980
are categorized as threatened; 10 of these species are on
the Pará list, 6 are on the Brazilian list, and 10 are on the
IUCN list (Supporting Information). Ten species listed as
regionally threatened are still extant in the MRB (Supporting Information). 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 (Ara macao),
Red-and-green Macaw (Ara chloropterus), and Golden
Parakeet (Guarouba guarouba)—were also recorded in
nonforest (agricultural) areas (Fig. 3). 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
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 2), 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
(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).
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 landuse 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 predisturbance
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).
Conservation Biology
Volume 00, No. 0, 2014
Avian Extinctions in Amazonia
8
High
Accipiter poliogaster
Spizaetus melanoleucus
Dendrexetastes rufigula*
G
Phoenicircus carnifex
Hylophilus ochraceiceps
Dacnis lineata
Micrastur semitorquatus
Touit huetii
Lophornis gouldii
Celeus torquatus*
Philydor erythrocercum
Phylidor ruficaudatum
Myiobius atricaudus
Platyrinchus platyrhynchos
Lamprospiza melanoleuca
Daptrius ater
Micrastur mirandollei
Deroptyus accipitrinus
≈30
POSSIBLY
EXTINCT
Calliphlox amethystina
Piculus chrysochloros*
Berlespchia rikeri
Euphonia minuta
PROBABLY
E
EXTINCT
Low
Accipter superciliosus
Pyrrhura lepida*
Hylopezus macularius
Sclerurus caudacutus
Sclerurus rufigularis
Dendrocincla merula
Deconychura longicauda*
Platyrinchus saturatus
Corythopis torquatus
Piprites chloris*
EXTINCT
Confidence
of
E
extinction
Penelope pileata
Aburria cujubi
Odontophorus gujanensis
Sarcoramphus papa
Harpia harpyja
Spizaetus ornatus*
Anodorhynchus hyacinthinus*
Ara macao
Guarouba guarouba*
Neomorphus geoffroyi
Gymnoderus foetidus
Periporphyrus erythromelas
Pauxi tuberosa
Psophia obscura*
>100
E
≈50
E
Number of years since last record
Figure 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]).
Table 2. Long-term species loss from Neotropical forest regions.
Study
Region
This study
metropolitan region of
Belém, Pará, Brazil
Shaw et al. 2013
Sierra de Los Tuxtlas,
Veracruz, Mexico
Patten et al. 2010
Palenque, Chiapas,
Mexico
Robinson 2001
Barro Colorado Island,
Panama
Renjifo 1999
west slope, Cordillera
Central, Colombia
Ribon et al. 2003
Viçosa, Minas Gerais,
Brazil
Christiansen & Pitter 1997 Lagoa Santa, Minas
Gerais, Brazil
Biome
Amazonia
1812–1980, 168
47, 360, 14.5
0.28
Central America
1973–2004, 30
12, 122, 9.8
0.40
Central America 1900–2009, 109
23, 240, 9.5
0.21
Central America
1970–1996, 25
27, 200, 13.5
1.08
Andes
1911–1997, 86
6, 139, 4.3
0.06
Atlantic Forest
1932–1999, 67
28, 221, 13
0.42
Atlantic Forest
1870–1987, 117
13, 107, 12.1
0.11
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 & Peres
2009, 2010; Stouffer et al. 2011). Our findings are con-
Conservation Biology
Volume 00, No. 0, 2014
Number of extinct species,
total species richness,
community regionally
Species
extinct (%)
loss/year
Period (years),
no. of
years
sistent with those of previous studies (e.g., Owens &
Bennett 2000), which found that large-bodied 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,
Moura et al.
White-crested Guan (Penelope pileata), Red-throated
Piping-Guan (Aburria cujubi), and Razor-billed Curassow (Pauxi tuberosa)—are game birds 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, Red-and-green Macaw,
and Hyacinth Macaw (Anodorhynchus hyacinthinus)
were harvested for the wild bird trade in the MRB (Alves
et al. 2013). The same is true of the Golden Parakeet,
which we (N.G.M. and A.C.L.) 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
were more likely related to forest loss and disturbance
than direct persecution. A wave of extinctions of smaller
bodied 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 Belém–Brası́lia road in the 1960s.
The disappearance of both medium and small-bodied
primary-forest dependent frugivores such as the Guianan
Red-Cotinga and Wing-barred Piprites (Piprites chloris
griseicens) is consistent with results of other studies (e.g.,
Lees & 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-and-Black 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 affected disproportionately by habitat loss, degradation, and fragmentation, including both flock-following under and mid-story
primary-forest dependent species such as Long-tailed
9
Woodcreeper (Deconychura longicauda zimmeri) and
terrestrial solitary species such as Spotted Antpitta (Hylopezus [macularius] paraensis), which appear intolerant even to low-intensity selective-logging activities (Lees
& 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,
and woodcreepers) for which habitat may be reduced
in selectively logged and secondary forests (e.g., Cockle
et al. 2010; Supporting Information).
The Future of the MRB Avifauna
Most studies documenting long-term extinctions in formerly forested tropical landscapes also report on colonization events by nonforest 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 (examples in
Supporting Information). Large-bodied (often frugivorous) species with high dispersal capacity are more likely
to be recorded as occasional vagrants or colonizing individuals than small-bodied (often insectivorous) species
with lower dispersal capacity (Lees & Peres 2009). Although this could be grounds for guarded optimism,
biotic impoverishment driven by fragmentation, unsustainable forest management, wildfires, and hunting is still
ongoing 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 catalog the long-term erosion of
biological diversity in the MRB 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.
Acknowledgments
We thank the Instituto Nacional de Ciência e
Tecnologia—Biodiversidade e Uso da Terra na Amazônia
(CNPq 574008/2008-0), the National Environment
Conservation Biology
Volume 00, No. 0, 2014
10
Research Council (NE/G000816/1), the Darwin Initiative (17-023), the Coordenação de Aperfeiçoamento de
Pessoal de Nı́vel Superior-CAPES, Lancaster University,
Embrapa Amazonia Oriental (SEG: 02.08.06.005.00), and
The Nature Conservancy for funding and The Nature
Conservancy for access to detailed land-use maps of the
municipality. We are very grateful to all the farmers
and landowners of Paragominas for collaborating in the
project, particularly Mauro Lúcio de Castro Costa and the
Sindicato dos Produtores Rurais de Paragominas. N.G.M.
was supported by a CNPq doctoral studentship, A.C.L.
thanks CNPq for funding, and A.A. thanks CNPq for a
research productivity fellowship. We thank P. Cerqueira,
M. Henriques, W. Overal, and I. Vieira for sharing data
and discussions on local land-use change history. We also
thank M. A. Patten and one anonymous referee whose
comments helped to improve the manuscript. This paper
is number 22 in the Rede Amazônia Sustentável publication series.
Supporting Information
Detailed information on the study site and data sources
used to compile the sighting records (Appendix S1), additional literature (Appendix S2), threats, Red List evaluations and status of the species in the study regions
(Appendix S3), and body mass of species unrecorded
in the MRB after 1980 (Appendix S4) are available online. The authors are solely responsible for the content
and functionality of these materials. Queries (other than
absence of the material) should be directed to the corresponding author.
Literature Cited
Aleixo, A. 2006. Oficina de trabalho “Discussão e elaboração da lista
de espécies ameaçadas de extinção do estado do Pará Relatório
Técnico.” Museu Paraense Emı́lio Goeldi. Available from http://
www2.museu-goeldi.br/biodiversidade/biota (accessed May 2013).
Almeida, S. A., and I. C. G. Vieira. 2010. Centro de Endemismo Belém:
Status da Vegetação Remanescente e Desafios para a Conservação
Biológica e Restauração Ecológica. Revista de Estudos Universitários
36:95–111.
Alves, R. R. N., J. R. D. F. Lima, and H. F. P Araújo. 2013. The live bird
trade in Brazil and its conservation implications: an overview. Bird
Conservation International 23:53–65.
Amaral, D. D., I. C. G. Vieira, R. P. Salomão, S. S. Almeida, and M. A. G.
Jardim. 2012. The status of conservation of urban forests in eastern
Amazonia. Brazilian Journal of Biology 72:257–265.
Bird, J. P., G. M. Buchanan, A. C. Lees, R. P. Clay, P. F. Develey, I.
Yépez, and S. H. Butchart. 2011. Integrating spatially explicit habitat
projections into extinction risk assessments: a reassessment of Amazonian avifauna incorporating projected deforestation. Diversity and
Distributions 18:273–281.
Birdlife International. 2013. World bird database. Available from
www.birdlife.org/datazone (accessed May 2013).
Conservation Biology
Volume 00, No. 0, 2014
Avian Extinctions in Amazonia
Brooks, T. M., S. L. Pimm, and J. O. Oyugi. 1999. Time lag between
deforestation and bird extinction in tropical forest fragments. Conservation Biology 13:1140–1150.
Burgman, M., R. Grimson, and S. Ferson. 1995. Inferring threat from
scientific collections. Conservation Biology 9:923–928.
Butchart, S. H. M., A. J. Stattersfield, and T. M. Brooks. 2006. Going
or gone: defining “Possibly Extinct” species to give a truer picture
of recent extinctions. Bulletin of the British Ornithologists’ Club
126:7–24.
Christiansen, M. B., and E. Pitter. 1997. Species loss in a forest bird
community near Lagoa Santa in southeastern Brazil. Biological Conservation 80:23–32.
CBRO (Comitê Brasileiro de Registros Ornitológicos). 2011. Listas das
aves do Brasil. Available from www.cbro.org.br (accessed May
2013).
Cockle, K. L., K. Martin, and M. C. Drever. 2010. Supply of tree-holes
limits nest density of cavity-nesting birds in primary and logged
subtropical Atlantic forest. Biological Conservation 143:2851–
2857.
Costello, M. J., R. M. May, and N. E. Stork. 2013. Can we name Earth’s
species before they go extinct? Science 339:413–416.
Crowley, B. E. 2011. Extinction and rediscovery: where the wild things
are. Journal of Biogeography 38:1633–1634.
Española, C. P., N. J. Collar, and S. J. Marsden. 2013. Are populations
of large-bodied avian frugivores on Luzon, Philippines, facing imminent collapse? Animal Conservation 16:467–479.
Gardner, T. A., J. Barlow, R. L. Chazdon, R. Ewers, C. A. Harvey, C. A.
Peres, and N. Sodhi. 2009. Prospects for tropical forest biodiversity
in a human-modified world. Ecology Letters 12:561–582.
Gardner, T. A., et al. 2013. A social and ecological assessment of
tropical land uses at multiple scales: the Sustainable Amazon Network. Philosophical Transactions of the Royal Society B 368(1619):
20120166.
Gibson, L., et al. 2011. Primary forests are irreplaceable for sustaining
tropical biodiversity. Nature 478:378–381.
Hansen, M. C., et al. 2013. High-resolution global maps of 21st-century
forest cover change. Science 342:850–853.
Hellmayr, C. E. 1905. Notes on a collection of birds, made by Mons.
A. Robert in the District of Pará, Brazil. Novitates Zoologicae 12:
269–305.
INPE (Instituto Nacional de Pesquisas Espaciais). 2013. Monitoramento
da floresta amazônica por satélite: Projeto Prodes, São José dos
Campos, São Paulo. Available from http://www.obt.inpe.br/prodes/
index/html (accessed August 2013).
IUCN (International Union for Conservation of Nature). 2013. The
IUCN red list of threatened species. Version 2013.2. Available from
http://www.iucnredlist.org (accessed May 2013).
Kattan, G. H., H. Alvarez-López, and M. Giraldo. 1994. Forest fragmentation and bird extinctions: San Antonio eighty years later. Conservation Biology 8:138–146.
Laurance, W. F., et al. 2011. The fate of Amazonian forest fragments: a
32-year investigation. Biological Conservation 144:56–67.
Leão, N., C. Alencar, and A. Verı́ssimo. 2007. Belém Sustentável 2007.
Imazon, Belém.
Lees, A. C., and C. A. Peres. 2008. Avian life-history determinants of local
extinction risk in a hyper-fragmented Neotropical forest landscape.
Animal Conservation 11:128–137.
Lees, A. C., and C. A. Peres. 2009. Gap-crossing movements predict
species occupancy in Amazonian forest fragments. Oikos 118:
280–290.
Lees, A. C., and C. A. Peres. 2010. Habitat and life history determinants of antbird local extinction in variable-sized Amazonian forest
fragments. Biotropica 42:614–621.
Lees, A. C., N. G. Moura, A. Santana, A. Aleixo, J. Barlow, E. Berenguer, J.
Ferreira, and T. A. Gardner. 2012. Paragominas: a quantitative baseline inventory of an eastern Amazonian avifauna. Revista Brasileira
de Ornitologia 20:93–118.
Moura et al.
Lovejoy, T. E. 1971. Diversity and abundance patterns of lower Amazonian rain forest birds. PhD thesis, Yale University, New Haven,
Connecticut.
Machado, A. B. M., G. M. Drummond, and A. P. Paglia. 2008. Livro
vermelho da fauna brasileira ameaçada de extinção. 1st edition.
MMA; Belo Horizonte, MG: Fundação Biodiversitas, Brası́lia, DF.
McCarthy, M. A. 1998. Identifying declining and threatened species
with museum data. Biological Conservation 83:9–17.
McInerny, G. J., D. L. Roberts, A. J. Davy, and P. J. Cribb. 2006. Significance of sighting rate in inferring extinction and threat. Conservation Biology 20:562–567.
Metzger, J. P., A. C. Martensen, M. Dixo, L. C. Bernacci, M. C. Ribeiro,
A. M. G. Teixeira, and R. Pardini. 2009. Time-lag in biological responses to landscape changes in a highly dynamic Atlantic forest
region. Biological Conservation 142:1166–1177.
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.
Novaes, F. C. 1973. Aves de uma vegetação secundária na foz do Amazonas. Publicação Avulsa Museu Paraense Emilio Goeldi 21:1–88.
Novaes, F. C., and M. D. F. C. Lima. 2009. Aves da grande Belém:
municı́pios de Belém e Ananindeua, Pará. PR/McT/Cnpq.
Owens, I. P., and P. M. Bennett. 2000. Ecological basis of extinction
risk in birds: habitat loss versus human persecution and introduced
predators. Proceedings of the National Academy of Sciences of the
United States of America 9:12144–12148.
Patten, M. A., H. G. Silva, and B. D. Smith-Patten. 2010. Long-term
changes in the bird community of Palenque, Chiapas, in response
to rainforest loss. Biodiversity and Conservation 19:21–36.
Peres, C. A. 2000. Effects of subsistence hunting on vertebrate community structure in Amazonian forests. Conservation Biology 14:
240–253.
Peres, C. A., T. A. Gardner, J. Barlow, J. Zuanon, F. Michalski, A. C. Lees,
I. C. G. Vieira, F. M. S. Moreira, and K. J. Feeley. 2010. Biodiversity
conservation in human-modified Amazonian forest landscapes. Biological Conservation 143:2314–2327.
Pickett, S. T. 1989. Space-for-time substitution as an alternative to longterm studies. Pages 110–135 in G. E. Likens, editor. Long-term studies in ecology: approaches and alternatives. Springer-Verlag, New
York.
Portes, C. E. B., L. S. Carneiro, F. Schunck, M. S. S. Silva, K. J. Zimmer, A.
Whittaker, F. Poletto, L. F. Silveira, and A. Aleixo. 2011. Annotated
checklist of birds recorded between 1998 and 2009 at nine areas in
11
the Belém area of endemism, with notes on some range extensions
and the conservation status of endangered species. Revista Brasileira
de Ornitologia 19:167–184.
Renjifo, L. M. 1999. Composition changes in a subandean avifauna after long-term forest fragmentation. Conservation Biology 13:1124–
1139.
Ribon, R., J. E. Simon, and G. T. Mattos. 2003. Bird extinctions in
Atlantic forest fragments of the Viçosa region, southeastern Brazil.
Conservation Biology 17:1827–1839.
Robinson, W. D. 2001. Changes in abundance of birds in a Neotropical
forest fragment over 25 years: a review. Animal Biodiversity and
Conservation 24:51–65.
Sclater, P. L., and O. Salvin. 1867. List of birds collected by Mr. Wallace
on the lower Amazons and Rio Negro. Proceedings of the Zoological
Society of London 1867:566–596.
Shaw, D. W., P. Escalante, J. H. Rappole, M. A. Ramos, R. J. Oehlenschlager, D. W. Warner, and K. Winker. 2013. Decadal changes and
delayed avian species losses due to deforestation in the northern
Neotropics. PeerJ 1. DOI:10.7717/peerj.179.
Sodhi, N. S., L. H. Liow, and F. A. Bazzaz. 2004. Avian extinctions
from tropical and subtropical forests. Annual Review of Ecology
and Systematics 35:323–345.
Solow, A. R. 1993. Inferring extinction from sighting data. Ecology
74:962–964.
Solow, A. R. 2005. Inferring extinction from a sighting record. Mathematical Biosciences 195:47–55.
Stone, W. 1928. On a collection of birds from the Pará region, eastern
Brazil (with field notes by J. Bond and R. Meyer de Schauensee).
Proceedings of the Academy of Natural Sciences of Philadelphia
80:149–176.
Stouffer, P. C., E. I. Johnson, R. O. Bierregaard Jr., and T. E. Lovejoy. 2011. Understory bird communities in Amazonian rainforest
fragments: species turnover through 25 years post-isolation in recovering landscapes. PLoS ONE 6:e20543.
Teixeira, D. M., N. Papavero, and L. B. Kury. 2010. As aves do Pará
segundo as “memórias” de Dom Lourenço Álvares Roxo de Potflis
(1752). Arquivos de Zoologia 41:97–131.
Trinca, C. T., S. F. Ferrari, and A. C. Lees. 2008. Curiosity killed the
bird: arbitrary hunting of Harpy Eagles (Harpia harpyja) on an
agricultural frontier in southern Brazilian Amazonia. Cotinga 30:
12–15.
Vieira, I. C. G., P. M. Toledo, and A. Almeida. 2007. Análise das
modificações da Paisagem da Região Bragantina, no Pará. Integrando
diferentes escalas de tempo. Ciência e Cultura 59:27–30.
Conservation Biology
Volume 00, No. 0, 2014