Diversity of birds and mammals in the forest reserves of the Agropalma Group, in

Tailândia municipality, state of Pará, Brazil

Final Report

Prof. Dr. Luís Fabio Silveira

Universidade de São Paulo - USP

General Coordinator and Birds Project

M.Sc. Líliam Patrícia Pinto

PPG Ecology - UNICAMP

Mammals Project

São Paulo, October 2004

EXECUTIVE SUMMARY

The West region of Maranhão state as well as the Eastern region of the

Pará state are among the areas most strongly impacted by anthropic actions in

the whole Amazonian region. Illegal loggers’ actions plus colonization fronts

actually began in this region, resulting in the Eastern part of the so-called “Arch

of Deforestation”, stretching over to the South and the West, towards the State of

Rondônia. The formerly extensive forests, located East of the Gurupi River and

West of the Tocantins River provide shelter for hundreds of vertebrate and

invertebrate taxa, many of which endemic, that is, only found in this region.

Forest remnants of the Tailândia and Moju regions are located in such

highly degraded matrix. Such forests can be indicated as potentially very

important to the study of diversity and conservation, once they provide habitat for

many endemic species to East Amazon, many of which, rare or endangered.

Within this context of both high biological importance and anthropic impact, forest

reserves of the Agropalma Group should be considered as fundamental areas to

increase knowledge of the diversity of birds and mammals, especially those

regarded as endangered.

During two periods in 2004 – from January 18 to February 05 and from

August 28 to September 06 - preliminary surveys of birds and mammals were

performed, with special emphasis given to primates, in the forest reserve areas

of the Agropalma Group, located in Tailândia, State of Pará.

During fieldwork, 338 birds species were recorded. This minimum number

of species found in the forest reserves of the Agropalma Group should be viewed

as highly expressive, once these 338 recorded species nearly represent 64%

of the whole avifauna of Eastern Pará. Such number of species is even more

relevant when considering that the area regarded as “Eastern Pará”

encompasses about 140.000 km2. Besides the meaningful number of registered

species, one of the most important results - indeed impressive - was the

recording of six taxa listed by IBAMA as endangered. Such number corresponds

to about 60% of all taxa of endangered birds in the whole Brazilian Amazonian

region.

Overall, 27 species of medium and large-size mammals were

recorded (Table 3). Among them, five are considered endangered. The

Black-bearded Saki, Chiropotes satanas, is a highly demanding primate

regarding forest quality (Figure 27). This species is endemic to Eastern Pará and

known to occur East of the Tocantins River, all the way up to the border of the

Pre-Amazonian region of Maranhão state. The Cebus kaapori (Ka’apor Capuchin

Monkey), described by scientists not long ago, is considered by IBAMA as

critically threatened.

An area of 119 km was surveyed during the two phases of the census

work on mammals and other cynegetic species. 269 animals were recorded and

93,7% of which belong to the Class Mammalia. Primates were the most sighted

species. For each ten kilometers surveyed, an average of seven tamarins were

sighted. The Black-bearded Saki, C. satanas, showed a density of 1,2 ind/10 km.

In the total sample, 22,6 ind/10 Km were recorded.

It is important to highlight that the richness of birds and mammals in

addition to the expressive number of endangered species – eleven according to

IBAMA, with special emphasis given to the Golden Parakeet, the Black-bearded

Saki and the tamarins – adds a huge value to the forest fragments within the

Agropalma Group’s property.

Therefore, we recommend specific studies on endangered species

detected in the area, especially the Golden Parakeet, the Black-bearded Saki

and the Ka’apor Capuchin Monkey – searching for new places where these

species also occur, within the company’s reserves. And, moreover, the

assurance that threatened fragments and species will be effectively protected

against hunters and wild animals illegal traders.

1. INTRODUCTION

Detailed studies on richness and density of animal species are important

to evaluate the conservation status of a forest. For instance, high densities of

certain species groups, such as top predators, frugivorous or cynegetic species,

indicate that the ecological dynamics of such environment are balanced, and that

the area suffers little or none habitat disturbance.

Frugivorous species (feed primarily on fruit) have a key role in the forest

natural regeneration, once they spread seeds of ingested fruit, therefore helping

to keep the diversity of plants. Top predators, such as the Jaguar (Panthera

onca), the Crested Eagle (Morphnus guianensis) or the Harpy Eagle (Harpya

harpyja), are responsible for regulating populations of frugivorous and

herbivorous species. Cynegetic species, hunted by men, include mainly medium

and large size mammals, such as agoutis, collared peccary and deer, as well as

birds, such Curassows and guans, and reptiles, such as tortoises and turtles.

The absence or low density of such indicative species is a symptom of habitat

and ecological impoverishing processes.

Many factors may contribute for the decline of animal population in a

given region. Thou, major threats to natural population are linked to human

impact, through habitat modification, hunting or introduction of exotic species.

(Peres, 1990, 1997; Cowlishaw & Dunbar, 2000).

Following habitat change, hunting is the second major factor, which

critically threatens the survival of medium and large size species (weighing over

1,5 kg). It causes severe impact on populations, profoundly decreasing its

densities and, frequently, causing local extinction of certain species.

Northern Maranhão and Eastern Pará are among the areas which most

suffered with anthropic actions in the whole Amazonian region. Extensive

forests, classified as dense ombrophylous forest and located below 100 m high,

which used to cover the whole region, are now very fragmented. Illegal loggers’

actions plus colonization fronts actually began in this region, resulting in the

Eastern part of the so-called “Arch of Deforestation”, stretching over to the South

and the West, towards the State of Rondônia. Many municipalities of Eastern

Pará already present 100% of its area completely altered by human actions.

(MMA 2001; Figures 1 and 2).

�

�

�

�

�

Figure 1: Illegal logging area in Eastern Pará and Western Maranhão. The study area is marked with a circle with a dot. Capitals of Brazilian states are marked with black dots.

Figure 2: Deforested area in Brazilian Amazon (according to MMA 2003). A circle with a dot represents the study area.

These formerly extensive forests, located East of the Gurupi River and

West of the Tocantins River provide shelter for hundreds of vertebrate and

invertebrate taxa, many of which endemic, that is, found only in this region.

Though this is one of the most important areas related to the Amazon vertebrate

diversity, and despite its high biogeographical value, there is no Conservation

Unities and most of the areas still forested are under control of big corporations

or land owners, who very often, clear great portions of the forest for cattle

pasture purposes. (MMA 2001; Figure 3).

�

�

�

�������������� �����������

��������������

����������������

������������������������� �

�����������!��� �

�������!�������� "� ��

��#�����������

Figure 3: Conservation Unities System (State and Federal) near the study area (circle with a dot). In yellow, direct use Conservation Unities, in green indirect use CU’s. REBIO – Biologic Reserve; FLONA – National Forest; PES – State Park; APA – Environment Protected Area.

Forest remnants of the Tailândia and Moju regions are located in such

highly degraded matrix. Such forests when analyzed within a regional – or even

national – context, can be indicated as potentially very important to the study of

diversity and conservation, once they provide habitat for many endemic species

to East Amazon, many of which, rare or endangered. We may refer to, for

instance, the Black-bearded Saki (Chiropotes satanas), the Ka'apor Capuchin

Monkey (Cebus kaapori) and the Golden Parakeet (Guarouba guarouba). It is

also important to highlight that, according to IBAMA (2003), ten of the eleven

taxa of Amazonian birds, regarded as endangered, could be found in the area

between the rivers Gurupi and Tocantins, which shows, per se, how extreme

important is the study and preservation of the remaining forest of this region.

Among this context of high biological importance and high anthropic

impact, forest reserves of the Agropalma Group could be seen as extremely

important areas for the increase of knowledge of birds and mammals diversity,

especially those regarded as endangered.

During two periods in 2004 – from January 18 to February 05 and from

August 28 to September 06 - preliminary surveys of birds and mammals were

performed, with emphasis given to primates, in the forest reserve areas of the

Agropalma Group, located in Tailândia, State of Pará. The survey sampled the

major blocks of the company’s forest areas, dedicating more time to those better

preserved.

The areas were chosen on day 19.i.2004, during the first phase of the

work, when the most meaningful fragments in terms of size were identified,

based on the property satellite images. In addition to that, many interviews were

conducted with workers, who knew the area well, in order to get proper and

updated information about the preservation status of each selected fragment.

Finally, from January 19 on, the selected blocks were surveyed by the birds

team, while the primates team focused on the block considered by all interviewed

workers as the best preserved (6; Agropalma Forest Reserve). Therefore, the

following locations were sampled (Table 1; see also Figure 4):

Table 1: Locations sampled in the present work, and respective geographical coordinates. See also Figure 4.

Location Latitude degree

Latitude minutes

Longitude degree

Longitude minutes

1) Maçaranduba 2 36 48 47

2) Maxixe 2 38 48 55

3) Águas Claras 2 33 48 53

4) Amapalma 2 40 48 55

5) Amapalma, line 67 2 24 48 49

6) Agropalma Forest Reserve 2 36 48 44

7) Agropalma – Trail II 2 37 48 44

8) Dendê 2 38 48 48

9) Aiu-açu 2 33 48 53

r

r

r

r

r

r

r

r

r r

r

1

2

3

4

5

67

89

Figure 4: Locations sampled in the present work. The dark line represents Road PA150, while gray lines represent the limits of Tailândia and Moju municipalities. Numbers eight and nine are close to the Aiu-Açu River, a tributary of the Acará River.

Objectives and methodologies used to sample diversity of birds and

mammals, in general, and primates, in particular, are described bellow.

2. AVIFAUNA

2.1. Objectives

The present project aimed to survey, through different specific

methodologies, bird communities in the best-preserved forest fragments kept by

the Agropalma Group. Besides that, special attention was given to the presence

of species designated as endangered by IBAMA (2003).

2.2. Material and Methods

In order to obtain a more efficient sampling of the avifauna, which inhabits

the region, different methodologies were used and listed below. The use of

varied simultaneous sampling methods enables a fast and reliable survey, with

special emphasis on documentation of each found species. Obviously, no

survey is complete, once many species migrate, seasonally occupy different

kinds of habitat, might have discrete habits or simply are not detectable through

the used methods. Therefore, the list on Appendix 1 refers to the minimum

number of species found in the area and, as studies and habitat samples

increase, certainly this number will increase as well, although in lower intensity.

Visual and auditory recordings were carried out throughout the whole area

within the Agropalma Group’s forests, while sample collection was concentrated

in the selected areas, listed above.

Bird species were visually identified with the help of binoculars 10x40 and

8,5x45. The variety of sounds emitted by the birds was recorded in analogical

format, in cassette tape (tape recorder Sony TCM 5000 EV and microphone

Sennheiser ME 66) and in digital format, in minidisks (recorder Sharp MD DR7

and microphone Sennheiser ME 66).

Birds were captured with mist nets, which had been previously spread

along open transects in the chosen areas (Figure 5). In order to sample large-

size birds as well birds that inhabit higher strata of vegetation, thus more difficult

to be captured with mist nets, caliber .22, .28 and .36 rifles were used.

Collected birds were preserved and stuffed in characteristic positions for

systematic studies, and some individuals, collected in duplicate, were fixed in 4

% formol and latter, preserved in 70 % ethanol, as well as all carcasses of the

preserved birds.

Biometric data (total mass and length) and the color of bare parts were

also recorded for each collected specimen. Tissue samples (pectoral muscles)

were removed from all collected birds, and will be used for further genetic

studies. All collected material is deposited at the Museu de Zoologia da

Universidade de São Paulo (MZUSP), where after publication of survey results,

will be available for consultation to the scientific community in general.

Copies of all recordings will be deposited at the Arquivo Sonoro Elias

Coelho - ASEC - at the Universidade Federal do Rio de Janeiro, and the Arquivo

Sonoro do Departamento de Zoologia da Universidade de São Paulo (USP). The

original recordings belong to the author and will be kept at the Departamento de

Zoologia da USP.

It’s important to point out that all collections were authorized by the

Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis

(IBAMA – DF) (Brazilian Institute of Environment and Renewable Natural

Resources (IBAMA – DF), and no animal – designated as endangered by IBAMA

(2003) was collected. Furthermore, transportation and use of firearms (riffles) for

the birds survey as well as ammunition purchase were properly authorized by the

Federal Police and the Brazilian Army.

Figure 5: Line of nets spread out inside the forest.

Daily activities began at about 5 am and would continue as late as 8 pm to

enable night birds sighting, totaling about 500 hours of fieldwork (not considering

raining periods). Mist nets were kept open from 6 am to 6 pm. Overall, 15 nets

were set (12 meters long by 2,40 m high - 36 mm mesh) on line, covering an

area 180 m long, in open transects of the chosen locations, during twenty days,

totaling about 3.500 hours/net.

2.4. Results

During fieldwork, 338 species of birds were registered (Appendix 1). In

order to properly evaluate how expressive is the diversity of birds within the

Agropalma Group forest areas, it would be necessary to compare our results to

another authors’ works of the same region. The most important reference work

for Eastern Pará is Roma (1996), who made a compilation of all recordings and

all scientific publications related to existing birds in Eastern Pará.

Eastern Pará was delimited by this author as “All regions of the Pará state

located between the right bank of the Tocantins river and the left bank of the

Gurupi river, having as Northern limits the waters of the Marajó Bay and the

Atlantic Ocean, and as Southern limits the politic-administrative bordering with

neighboring Maranhão state” (Figure 6). Such division was adopted in the

present work, aiming to fit the survey’s results within the context of its regional

biodiversity and, in a more restricted biogeographically context, in order to

facilitate further diversity comparisons.

Besides the results by Roma (1996), we may also cite Novaes and Lima

(1998), who compiled all birds in the regions of Belém and Ananindeua, which

might be also compared to the results of the present work.

Figure 6: Eastern Pará region (gray area), according to Roma’s definition (1996). The circle with a dot indicates the area of the present study and the black dot indicates the city of Belém, capital of Pará State.

Roma (1996) lists 529 species for the whole Eastern Pará region and

Novaes & Lima (1998) list 482 species for the great Belém region (which

includes Ananindeua). Its important to emphasize that both works are

compilations involving the results of dozens – in some cases hundreds – of years

of intense collection in this region, performed by different researchers and

professional collectors. In some cases, we may mention species, which were

registered only once, such as the Hyacinth Macaw (Anodorhynchus

hyacinthinus), and never again sighted by any other researcher. Besides that,

both compilations also include birds species which live in other ecosystems

either not included in this survey - like beaches, coastal areas and mangrove

lands - or poorly represented in the region, such as flooded igapó forest or open

fields.

The minimum number of species found in the forest reserves of the

Agropalma Group should be viewed as highly expressive, once these 338

recorded species nearly represent 64% of the whole avifauna of Eastern Pará.

Such number of species is even more relevant when considering that the area

defined as “Eastern Pará” by Roma (1996) encompasses about 140.000 km2.

Besides the meaningful number of registered species, one of the most

important results - indeed impressive - was the recording of six taxa listed by

IBAMA as endangered. Such number accounts for about 60% of all endangered

taxa of birds in the whole Brazilian Amazonian region. Regardless of being

recorded in densities lower than expected for such extensive areas, like the

surveyed ones, just their occurrence already makes the forest fragments within

the Agropalma Group’ property, one of the most important places for the

preservation of such taxa which are, in their majority, exclusive of the endemic

“Centro Belém”, which encompasses the whole Eastern Pará.

Furthermore, all our local woodsman (mateiros) and guides, who have

been hunters in the past, were unanimous in confirming, in the region, the

occurrence – although very rare due to intense hunting pressure - of the Dark

winged Trumpeter (Psophia viridis obscura) and the Bare-faced Curassow (Crax

fasciolata pinima). These two taxa are also regarded as endangered, and the

Bare-faced Curassow, which is the rarest species of the Cracidae (family of birds

which includes Curassows, guans, chachalacas, and piping guans) in Brazil, has

not been confirmed sighted or identified since the 60’s. A focused and specific

effort must be done to confirm these recordings in the area of the Agropalma

Group. The presence of such species will include these forest fragments amidst

the most important (if not one of the very few) of the whole Amazonian region for

conservation of endangered birds, being imperative its maintenance and

management, in order to ensure these birds’ long-term survival. Its very

important to point out that, in case Curassows and trumpeters indeed occur in

the region, the percentage of Amazonian endangered birds within the reserves of

the Agropalma Group will increase to 90%, that alone showing the singular

importance of these fragments for birds conservation.

Table 2. Threatened birds’ species and locations where they were recorded in the surveyed area.

Scientific name Popular name Location of record

Guarouba guarouba Golden Parakeet Road to the Moju and

Maçaranduba harbor.

Pyrrhura lepida lepida Pearly Parakeet Road to the Moju

harbor, Areal

Pteroglossus

bitorquatus bitorquatus Red-necked Aracari (Figure 7)

Águas Claras,

Maçaranduba

Dendrocincla merula

badia White-chinned Woodcreeper Amapalma

Dendrocolaptes certhia

medius

Amazonian Barred-

Woodcreeper Amapalma

Phlegopsis

nigromaculata

paraensis

Black Spotted Bare Eye

(Figure 8) Maçaranduba

Figure 7: Red-Necked Aracari, Pteroglossus bitorquatus bitorquatus, endemic to Eastern Pará and recorded in Águas Claras and Maçaranduba (photo by Edson Endrigo).

Besides the six endangered taxa, there is a remarkable presence of

different species which suffer very intense pressure in other Amazonian regions.

Among such species, emphasis should be given to representatives of Family

Psittacidae, which includes the parrots, macaws and parakeets. Large-sized

birds, like macaws, were encountered in small number, although parrots and

parakeets were common in the area.

Figure 8: Black-Spotted Bare Eye, Phlegopsis nigromaculata paraensis, recorded in the Maçaranduba region.

The Mealy Parrot, Amazona farinosa (Figure 9) had the highest number of

encounters, together with the Orange-winged Parrot (Amazona amazonica),

while macaws, like the Scarlet Macaw (Ara macao, Figure 10), were very rare in

the surveyed area. Plausible explanations for such low encounter rates of larger

species, like macaws, could be the loss and destruction of the habitat (such as

the cutting of trees with holes compatible to these birds’ size and where they

might reproduce) as well as illegal capture for the trade of wild animals –

individuals of this and other species of macaws were seen in many houses in

Vila dos Palmares and other houses located in farther places. Among the

Psittacidae, the occurrence of the Pearly Parakeet, Pyrrhura l. lepida, must be

highlighted, once this endemic taxon is designated as endangered species. Many

groups of these birds were sighted feeding on fruit trees in the forest, as well as

Miconia, encountered in the roads edges. The taxonomic status of these species

icomplex is now under study by Fernando José Belmonte.

Figure 9: Mealy Parrot, Amazona farinosa, the most common species of parrot encountered within the forest areas of the Agropalma Group.

Figure 10: Scarlet Macaw, Ara macao, species that, although rare in all surveyed fragments, is found in the houses of local inhabitants, thus indicating a pressure for wild animals illegal trade which affect native population.

Understory birds are also a good indication of the fragments’ preservation

status. Many species regarded as army ants followers plus mixed-species

understory flocks were observed. Among them, the White Chinned Woodcreeper Dendrocincla merula badia, the Amazonian Barred Woodcreeper, Dendrocolaptes certhia medius, and the Black-Spotted Bare-eye, Phlegopsis

nigromaculata paraensis, must be pointed out once they are all considered

endangered species. The Hooded Gnateater, Conopophaga aurita (Figure 11)

and the Rufous-capped Antthrush, Formicarius colma (Figure 12) are understory

species which eventually join mixed-species flocks.

Figure 11: Hooded Gnateater, Conopophaga roberti, common in the understory of all fragments.

The Rufous-capped Antthrush (Figure 12) is a little more rare than its

congener, Formicarius analis, which is one of the most common species in all

fragments, either in very degraded areas or where no signal of tree cutting could

be seen. The existence of two species, which occupy similar habitats and have

similar habits, encountered in the same location, but with such different densities

could be an interesting theme for further studies related to both species’ ecology

and environmental needs.

Figure 12: Rufous-capped Antthrush, Formicarius colma, typical inhabitant of well-

preserved areas.

The White-backed Fire Eye, Pyriglena leuconota (Figure 13) is always

present in mixed-species flocks, sometimes in many pairs. Easily found by their

vocalization, they prefer more shadowed areas of the understory. This is a

relatively common species in all surveyed fragments.

Figure 13: White-backed Fire Eye, Pyriglena leuconota, always recorded following the army ants.

Eagles or falcons – inhabitants of the interior of the forest, which hunt

specially in understory or sub canopy - were observed and recorded at low rate.

Among the very few recorded, the Barred Forest-Falcon, Micrastur ruficollis

(Figure 14) was one of the most common, both in well-preserved and degraded

fragments.

Figure 14: Barred Forest-Falcon, Micrastur ruficollis, a common species in all fragments.

The Pearl Kite, Gampsonyx swainsonii (Figure 15) is the smallest hawk

species in Brazil, typical of open areas. It was not rare, especially in the forest

edges, where it stays, alone or in pairs, on the watch for prey - small vertebrates

and insects.

Figure 15: Pearl kite, Gampsonyx swainsonii, typical of open areas.

Another extremely common species found in the survey was the Blue-

crowned Motmot, Momotus momota (Figure 16). This species lives in the middle

strata of the forest and feed on small vertebrates and fruits. It’s also a widely

spread species throughout Brazil, occurring only in forested areas.

Figure 16: Blue-crowned Motmot, Momotus momota, one of the most common species in all fragments.

The family with the highest number of representatives recorded in the

survey was the Tyrannidae, with 41 species. Birds of this Family – which includes

Great Kiskadees, Tropical Kingbirds and flycatchers in general – are very

diversified especially in the Amazon. Among the recorded species, the Royal

Flycatcher (Figures 17 e 18) and the White-crested Spadebill distinguish

themselves (Figure 19). The first one is considered one of the most exotic bird

species of the Neotropical region, occurring only in the Amazon (there is another

species in Brazil, which occurs in the Atlantic Forest and it is now restrict to a few

Conservation unities).

Figure 17: Royal Flycatcher, Onychorhynchus coronatus, male, a common species in the Amazonian region, although almost unknown.

Figure 18: Royal Flycatcher, Onychorhynchus coronatus, female.

Among the granivorous, usually not so plentiful and diversified in

extensive forested areas, like the Amazonian region, the Chestnut-bellied Seed-

finch, Oryzoborus angolensis, once although common, is easily found as

domestic birds in houses of the local population. We even registered a capture

within the preservation areas of the Agropalma Group. The Blue-black Grosbeak (Figure 20), less desirable as pet birds, was extremely abundant in some

fragments, and accounts for most of the granivorous recordings.

Figure 19: White-crested Spadebill, Platyrinchus platyrynchos.

The diversity of hummingbirds’ species - family Trochilidae- was very

meaningful, with an overall of 13 registered species. The most common among

them, was the Fork-tailed Woodnymph (Figure 21), found in all fragments.

Among the hummingbirds, we may also highlight the presence of the Crimson

Topaz, Topaza pella and the Racket-tailed Coquette, Discosura longicauda, a

virtually unknown species.

Figure 20: Blue-black Grossbeak, Passerina cyanoides.

The number of hummingbirds’ species seems to be still underestimated.

Many species might experience some occasional migration when seeking out

flowering plants. Certainly, the number of representatives of this family, which is

already high, could increase as the frequency of studies also increases together

with proper follow-up on some tree species’ flowering period.

Figure 21: Fork-tailed Woodnymph, Thalurania furcata.

Nevertheless, among all recorded species, the most distinguished is the

Golden Parakeet, Guarouba guarouba. Endemic to Pará and Western Maranhão,

this stunning Psittacidae (Figure 22) appears in the list of endangered Brazilian

species (IBAMA 2003) and is also considered as globally threatened (Collar et al.

1992; BirdLife 2000). Its distribution area was largely reduced due to loss of

habitat (see Appendix 2), plus the fact that the Golden Parakeet has always been

one of the most desirable species by rare birds smugglers. Its natural populations

currently are restricted to very few protected areas, and the ones, which are not

in such areas, face intense capture pressure. (See below).

Figure 22: Golden Parakeets, Guarouba guarouba, kept in captivity. The massive destruction of its original habitat combined with great pressure by the illegal trade of wild birds in Brazil and abroad, contributed for its almost-extinction from Nature.

It was a very pleasant and big surprise to find, in the middle of the “Trans-

Moju” road, an active nest of Golden Parakeets (Figures 23 e 24). The nest was

located in a tree of about 40 meters high, and its entrance at about 30m high

(Figure 25). Ten individuals were sighted and monitored during eight days, and

their feeding, social and breeding behavior were registered and will be eventually

published (see Appendix 2). The place chosen for nidification could not be more

interesting - a very busy location with cars and people constantly passing by.

Figure 23: Golden Parakeets’ nest, Guarouba guarouba, on the “angelim” Dinizia excelsa (Leg. Mimosoideae). The arrow shows the approximate location of the nest. Please note the tree height in relation to the observers, on the left of the picture.

Figure 24: Detail of the Golden Parakeet’s nest, Guarouba guarouba, on the angelim.

Nevertheless, the Golden Parakeets’ situation in that region is far from

safe. Besides the illegal trade for the big cities, this species is also very desirable

as domestic bird by local population (Figures 25 and 26), and usually kept in

extremely bad conditions. Nestlings taken away from the nests (Figure 26) are

bred in captivity by local people, who, in order to capture these birds, cut nest

trees. Such procedure have a doubly deleterious effect, first it takes the nestlings

away from their reproductive station as well as eliminates a nidification site.

Natural tree holes are a highly disputed resource by dozens of birds and

mammals species in Neotropical forests, and their absence may cause severe

effects in the reproduction and recruitment rate of such species.

The presence of Golden Parakeets in the forest fragments of the

Agropalma Group should be viewed very carefully, because its disclosure,

without proper protection of the sites where the species was recorded (Table 2),

could lead to their capture by birds illegal traders, once they still reach

considerably high prices in the national - and illegal - market of captive birds.

One pertinent suggestion is that Agropalma adopt the Golden Parakeet as a

symbol of the company, thus making all employees feel somehow responsible for

its preservation. Another suggestion for the long-term maintenance of this

species in the reserve area is the implementation of a program of monitoring and

basic studies on the species’ and its almost unknown biology. These low-costs

studies certainly would bring many benefits for the Company’s image, besides

yielding a large amount of data, which could be used in management plans for

this species in other areas where they also occur.

Figure 25: Golden Parakeet, Guarouba guarouba, kept in semi-captivity in Vila dos Palmares.

Figure 26: Nestling of Golden Parakeet, Guarouba guarouba, kept in captivity, near Vila dos Palmares. This nestling was taken away from the nest on day 04.i.2004, and already presented signs of dehydration and malnutrition. A skin of ocelot, Leopardus pardalis can be seen hanging on the back.

3. MAMMALS AND CYNEGETIC SPECIES

3.1. Objectives

The study on mammals and cynegetic species is divided in two main

parts. In the first section, the inventory of mammals species is presented and, in

the second, a quantitative survey of mammals and cynegetic species.

1.1. QUALITATIVE SURVEY OF MAMMALS

1.1.1. Objectives

• Supply with a list of medium and large size mammals fauna found in the

forest reserves of the Agropalma Group, special attention given to

primates and endangered species;

• Watch vertebrates’ species which use the palm crops to obtain resources.

1.1.2. Material and Methods

The present study was performed in two phases – the first one between

January 18 and February 05 of 2004 and, the second, between August 28 and

September 06 of the same year. Data obtained in both field trips were gathered

and are here presented in a combined way.

In order to elaborate the list of medium and large size mammals found in

the study areas, the field team in charge of the terrestrial mammals surveyed the

forest reserves of the Agropalma Group, recording all sightings, vocalizations,

footprints and other vestiges.

The Agropalma Forest Reserve was the area where the work was mostly

focused, due to the census work performed there. The Agropar Forest Reserve

and Mata da Galiléia were the least investigated forests.

1.1.3. Results

Overall, 27 species of medium and large size mammals were recorded

(Table 3). Five of them are endangered species. The Black-bearded Saki,

Chiropotes satanas, is a highly demanding primate regarding forest quality

(Figure 27). This species is endemic to Eastern Pará and known to occur East of

the Tocantins River, stretching to the border of the Pre-Amazonian region of

Maranhão state. They are primates of diurnal habits, medium size and weigh

about 3 kg when adults. This species is unmistakable because of its long fur and

very thick beard (van Roosmalen et al., 1981). On top of its head, the fur is

divided in two big bunches.

C. satanas live in large groups with more than 20 individuals, with

subgroups divided along the day, gathering again after feeding sessions (Ayres,

1981; van Roosmalen et al., 1981, 1988). They basically feed on immature seeds

and ripe fruit, and their presence in the area is an indicative sign that fruit

production is high at such location. This could be easily observed in the area, as

you walk through the forest, a great amount of fruit can be seen lying on the floor

(Figure 28).

The Black-bearded Saki was not sighted in the second phase of the study,

which does not mean that it has disappeared from the forest. This species uses

large portions of forest and is found at low density, which in fact, makes its

detection to be rare.

Figure 27. Chiropotes satanas, Black-bearded Saki, endangered primate species sighted three times in the Agropalma Forest Reserve.

Figure 28. “Breu” fruit (Protium sp., Burseraceae) lying on the forest ground.

Another very interesting species, the Cebus kaapori (Ka’apor Capuchin

Monkey), was found only once at Trail I, on August 28,2004. This species,

described only a while ago by scientists (Queiroz, 1992), is considered by IBAMA

(2003) as critically threatened. It’s an omnivorous primate, whose diet is basically

composed of fruit and insects. Two sighted individuals ran away rapidly without

vocalizing, which didn’t allow us to confirm the presence of other individuals in

the group.

Besides the Black-bearded Saki and the Ka’apor Capuchin Monkey, three

threatened felines were also observed – the Oncilla, Leopardus tigrinus (Figure

29a), the Margay, Leopardus wieddi (Figure 29b), and the Jaguar, Panthera

onca.

(a) L. tigrinus (b) L. wieddi

Figure 29. Oncilla (a) and Margay (b), two threatened felines sighted in the studied area.

Between the forest edge and the palm plantation of Block G (02°34’52”N;

48°46’32”W), feces of a feline containing bones and fur were found. In order to

identify both animal and the prey, feces were collected and washed to separate

fur from bones’ fragments (Figure 30). The material analysis detected the

presence of Jaguar fur, which – similar to any other feline - have the habit of lick

itself and, as consequence, swallows grate amount of its own fur. Bones and

other type of fur present in the feces belonged to a Nine-banded armadillo

(Dasypus novemcinctus; Figure 31).

The Jaguar is the largest predator of Neotropical forests, where it hunts

large mammals, such as deer, capybaras, collared peccary as well as smaller

animals, like agoutis, birds and tortoises. In locations where its habitat is reduced

due replacement of forests for cattle pasture, this large size feline suffers with

reduction of its prey, which leads it to attack cattle. Consequently, they are

intensively hunted by farmers.

The presence of the Puma (Puma concolor) was also recorded through

indirect evidences in both phases of the work. Footprints were found in the

edges of the Agropalma Forest Reserve (Figure 32), in two locations: the

entrance of Trail I (02°36’15”S; 48°45’55”W) and near Trail II (02°38’40”N;

48°48’28”W), where footprints of two such animals walking side by side were

found. Similar to the Jaguar, the Puma also need great areas to obtain

resources. Its diet is composed of medium and large size vertebrates, like

agoutis, collared peccary and deer.

Animals living in forests contiguous to roads are prone to being run over,

especially if such animals need large territories and move around a lot searching

for food. Agropalma Forest Reserve is located near Road PA 150, and six

animals run over were recorded, among them a Grison (Galictis vittata) and two

Lesser anteaters (Tamandua tetradactyla, Figure 33).

Figure 30. The washing process of carnivorous’ feces aiming the separation of bones and fur for identification.

Figure 31. Washed feces of a Jaguar presenting fur and bones of armadillo, besides its own fur.

Figure 32. Puma footprint (Puma concolor) recorded on 29/01/04 in the Agropalma Forest Reserve.

Figure 33. Lesser anteater, locally known as “mambira”, killed by a car at Km 75 of the Road PA 150.

Many vertebrate species were observed using the palm crops searching

for food. Many Crab-eating foxes were sighted crossing the crops (Figure 34),

and analysis of their feces shows that the palm fruit (Elaeis guineensis) is an

important item of their diet (Figure 35). Moreover, as Crab-eating foxes are

omnivorous animals, they certainly feed themselves on many rodents and other

small vertebrates, which also live in the crops. These Canidae may also live in

the crops’ shelters, just like the Armadillos (Figure 36) and the Boa (Boa

constrictor). The presence of Boa constrictors is certainly a benefit for the crops,

once these reptiles are very important in helping to control rodents’ population

(Figure 37).

Figure 34. Crab-eating Fox (Cerdocyon thous) footprint found on Avenida 5, Block G.

Figure 35. Crab-eating Fox (C. thous) feces, containing palm fruit fibers. A fruit palm partially eaten by this animal was also found near the feces.

Figure 36. Nine-banded Armadillo (Dasypus novemcinctus) footprint, found in the palm crops near the Agropalma Forest Reserve.

Figure 37. Boa (Boa constrictor) found in the palm crops near the Agropalma Forest Reserve.

Coatis (Figure 38) and tamarins also use the crops to obtain food. Besides the

palm fruit, the tamarins could feed on butterflies and other insects’ larvae, found

in these palm trees. Vestiges left by the Puma show that this animal uses the

crops as passage to other forests, which is probably, the same case of the

Jaguar and many other animals (Figure 39).

Figure 38. Coati (Nasua nasua) footprints found in the palm crops near Agropalma Forest Reserve, close to Trail II.

Table 3. Qualitative survey of medium and large size mammals of the Agropalma Group’s forest areas. ORDER Type of Recording:

Family Vi = visualization; Ve = vestiges; Species Common Name Local** Vo = vocalization

MARSUPIALIA Didelphidae

Monodelphis americana Opossum 8 Capture

XENARTHRA Myrmecophagidae

Tamandua tetradactyla Lesser anteater 6; 11 Run over animal Bradypodidade

Bradypus variegatus Three-toed tree sloth 5; 8 Vi; Ve (bones) Choloepus didactylus Two-toed tree sloth 5 Vi

Dasypodidae Dasypus novemcinctus Nine-banded Armadillo 2; 3; 9 Vi; Ve (footprints, fur and bones)

PRIMATES

Callitrichidae Saguinus midas niger Tamarin 1; 2; 3; 4; 5; 6 Vi; Vo

Cebidae Aotus infulatus Night monkey Local people statments Saimiri sciureus sciureus Squirel monkey 1 Vi Cebus apella Capuchin Monkey 1; 2 Vi, Vo Cebus kaapori * Ka’apor Capuchin Monkey 1 Vi

ORDER Type of Recording:

Family Vi = visualization; Ve = vestiges; Species Common Name Local** Vo = vocalization

Pithecidae Chiropotes satanas* Black-bearded Saki 1 Vi

Atelidae Alouatta belzebul belzebul Red Howler monkey 1; 2; 3; 4; 5; 6; 7; 8. Vi; Vo; Ve (feces)

CARNIVORA

Canidae Cerdocyon thous Crab-eating fox 8; 9 Vi; Ve (footprints and feces)

Procyonidae Nasua nasua Coati 1; 2 Vi

Mustelidae Galictis vittata Grison 11 Vi Eira barbara Tayra 1 Vi

Felidae Leopardus wiedii* Margay 2 Ve (footprints) Leopardus tigrinus* Oncilla 1 Vi Panthera onca Jaguar 1 Ve (feces) Puma concolor Puma, Mountain Lion 1 Ve (footprints)

ORDER Type of Recording:

Family Vi = visualization; Ve = vestiges; Species Common Name Local** Vo = vocalization

PERISSODACTYLA Tapiridae

Tapirus terrestris Tapir 2 Ve (footprints)

ARTIODACTYLA Tayassuidae

Tayassu tajacu Collared peccary 1 Ve (footprints; bones) Cervidae

Mazama americana Bush deer 1; 2 Vi; Ve (footprints, feces) Mazama gouazoubira Brocket deer 1; 6 Vi

RODENTIA Sciuridae

Sciurus aestuans 1 Vi Hydrochaeridae

Hydrochaeris hydrochaeris Capybara 6 Ve (footprints, feces) Agoutidae

Agouti paca Agouti 1 Ve (footprints) Dasyproctidae

Dasyprocta agouti Agouti 1 Vi; Vo

* Threatened species. ** Locations: 1 – Agropalma Forest Reserve – Trail I (02°36’15”S; 48°45’55”W).

2 – Agropalma Forest Reserve – Trail II (02°38’40”S; 48°48’28”W).

3 – Agropar Forest Reserve I (Trans-Moju) (02°31’18”S; 48°52’19”W) (Figure 33).

4 – Agropar Forest Reserve II (Maxixe) (02°33’19”S; 48°53’53”W).

5 – Palmares Forest Reserve (02°36’00”S; 48°44’00”W).

6 – Amapalma Forest Reserve (02°38’00”S; 48°55’00”W).

7 – Galiléia (02°31’11”S; 48°42’09”W).

8 – Surroundings of Vila da Agropalma (02°32’34”S; 48°45’48”W).

9 – Vicinal road between the woods of the Agropalma Forest Reserve and the palm crops - block G (02°34’52”S; 48°46’32”W).

10 – Palm crops - block F/G (02°34’41”S; 48°46’17”W). 11 – Road PA150, Km 75.

Figure 39. View of the forest edge of the Agropar Forest Reserve – Trans-Moju, where a group of tamarins, Saguinus midas niger, was sighted.

A Tayra (Eira barbara) was sighted at the margins of the igarapé

Jacareteu (02°37’03”S; 48°45’55”W) in the Agropalma Forest Reserve, on

August 31, 2004. This species has diurnal, omnivorous habits, with diet

composed of fruit, small vertebrates and insects.

None of the two species of Collared peccary were sighted. Although,

the Collared peccary caititu (Tayassu tajacu) had its presence confirmed by

the detection of footprints near the bottom of the fruit tree ”cutitiribá” (Pouteria

venosa, Sapotaceae) and also by a piece of jaw donated by a former hunter

of the region (Figure 40).

Figure 40. Jaw of a Collared peccary (Tayassu tajacu) hunted more than five years ago in the region’s forest.

1.2. QUANTITATIVE SURVEY OF MAMMALS AND CYNEGETIC SPECIES

(CENSUS)

1.2.1. Objectives

• Measure the density of mammals and other cynegetic species;

• Analyze the environment quality of the Agropalma Group forest

reserves.

1.2.2. Census Methodology

The quantitative survey was performed using standard line transects

methodology, indicated for this type of study (Peres, 1993; Peres, 1999;

Buckland et al., 2001). Such procedure consists in traverse linear trails of 4 to

6 km long in the interior of the forest, searching for animal, which are focus of

the present study.

In the first five days of work, six local woodsmen open, within the

Agropalma Forest Reserve, a trail of 5.516 m long, named “Trail I”. Besides

that, another preexisting trail was also used in one of the limits of the same

forest, named “Trail II”. Trail II is 2.400 m long and is located about 5.000 m

far from Trail I.

In order to facilitate event mapping, such transects were marked with

colorful tapes at each 25 m, where distances were measured in relation to the

beginning of the trail (Figure 20).

Trail I was surveyed in 11 mornings between January 18 and February

05 of 2004 and, again, in 10 mornings between August 28 and September 06

of 2004. Trail II was visited only in three mornings in the first phase of the

work. There was no census work on rainy days. The average speed was

approximately 1,25 km/hour, with brief stops at each 25 m, in order to better

listen to the sounds of the forest.

For each detected group, the following information were written down:

hour, species, number of individuals, social composition, distance from the

beginning of transect. By the end of the first phase of the work, 68 km of

census had taken place. In the second phase, 51 km were surveyed.

Figure 41. Measurement and marking work in Trail I for the performance of the mammals and cynegetic species census.

1.2.3. Results Overall, 119 km were surveyed in both phases of the work of mammals and

other cynegetic species census. 269 animals were recorded, 93,7% of which

belong to the Class Mammalia. Primates were the most sighted (67%) (Figure

42), and tamarins the most common species (30,5%). For each ten kilometers

surveyed, an average of seven tamarins were sighted. The density of the

Black-bearded Saki, C. satanas, was of 1,2 ind/10 km (Figure 43). In the total

sample, 22,6 ind/10 Km were detected.

The predominance of primates in the quantitative census was expected,

because – except for the Night monkey (Aotus spp.) - primates have diurnal

habits and live in groups, consequently are easily sighted.

other mammals

27%

birds6%

primates67%

Figure 42. Percentage of individuals which belong to the different animal groups recorded in the mammals and cynegetic species census.

0

10

20

30

Mammals Primates Tamarim Saki

Ind/

10K

m s

urve

yed

Figure 43. Number of individuals sighted for each 10 km surveyed.

Along the 119 km surveyed, 127 individuals, who belong to cynegetic

species, were sighted (Figure 44) – a low density when compared to protected

non-hunting areas. For instance, the flesh of Giant tortoises (Geochelone

spp.) is very appreciated by the Amazon population; hence they are frequently

hunted. Within the study area, only one individual of the species G. carbonaria

(Figure 45) was found.

0

30

60

90

120

150

Non-huntedMammals

Mammals Birds TurtleCynegetic species

Num

ber o

f ind

ivid

uals

Figure 44. Proportion of cynegetic animals in the survey.

Figure 45. Young Geochelone carbonara individual, the only red foot tortoise sighted in the cynegetic animals’ census.

4. DISCUSSION AND CONCLUSIONS

Except for a few species, such as Owls, Nightjars and Night monkeys

(Aotus spp.), all birds and primates species have diurnal habits, thus

facilitating the study and generating a large amount of data.

Interest in the study of mammals and birds has increased significantly

over the last three decades, partly due to the threat to their survival. The main

factors which contribute for the disappearance of natural population of

mammals are destruction of habitat, hunting for food purposes and – which is

common in the case of primates and birds – capture of live animals to be used

as pets or sold to the traffic.

One of the main reasons medium and large size mammals and birds

are used in forest quality assessment is the fact that such animals easily

respond to alterations in their environments. Furthermore, this group has a

high number of cynegetic species, which indicates the intensity of hunting they

are submitted.

Similar to the birds, mammals also play an important role in ecological

processes, pollination and the wide dispersion of seeds. Primates, especially,

help to disperse a great number of seeds of many species and therefore are

considered fundamental for the forests diversity maintenance.

With diet basically composed of fruit, the Black-bearded Saki and the

Ka’apor Capuchin Monkey, two primates found in the Agropalma Group

forest, are also considered as important contributors of the forest integrity

maintenance and the recovery of disturbed areas.

Once they need well preserved forests in order to maintain viable

populations and due to their relevant ecologic services, C. satanas and C.

kaapori are regarded as special species by people and institutions linked to

environment protection. It is possible that – in a near future - the Agropalma

Group Forest reserves will be one of the few forest extensions in the Moju

River region, large enough to shelter viable populations of these two

endangered primates, which would lead the company to have a prominent

role in their preservation. In addition to that, the presence of a high number of

birds species, (~64% of the whole avifauna already recorded in Eastern Pará)

plus the presence of 60% (maybe 90%) of the endangered avifauna of the

Brazilian Amazon, places the forest reserves protected by the Agropalma

Group amidst the most important of the Amazon region in general and,

particularly, of Eastern Pará.

Regarding the fragments, some important measures may be

suggested, such as:

Try to connect the different fragments, thus facilitating the transit

of animals and increasing the genetic flux among the

populations;

Increase vigilance in the fragments, especially in the limits of the

reserve area, therefore avoiding a possible illegal logging

activity, plus essential and continuous ban on hunting.

It is important to highlight that the richness of birds and mammals in

addition to the expressive number of endangered species – according to

IBAMA, with special emphasis given to the Golden Parakeet, the Black-

bearded Saki and the tamarins – adds great value to the forest fragments in

the Agropalma Group’s property. Hence, we strongly recommend:

Performance of specific studies on endangered species

detected in the area, especially the Golden Parakeet, the Black-

bearded Saki and the Ka’apor Capuchin Monkey – searching for

new places where these species also occur, within the

company’s reserves. And effectively protect these species

against hunters and wild animals illegal traders.

Development of a monitoring program, especially directed to the

Golden Parakeet, the Black-bearded Saki and the Ka’apor

Capuchin Monkey, threatened species and highly sensitive to

anthropic alterations;

Execution of an specific survey in order to verify the possible

existence of populations of the Bare-faced Curassow (Crax

fasciolata pinima) and the Dark-winged Trumpeter (Psophia

viridis obscura), which are among the two most threatened bird

species in the whole Amazon region. Their presence was

emphatically confirmed by local woodsmen and sentinels, even

though their genuine rarity was unanimous. c It’s fundamental to

identify possible remnant populations of these taxa;

Survey the diversity of other groups of terrestrial and aquatic

vertebrates (fishes, amphibians, reptiles, small mammals and

bats), which could help in the elaboration of a more precise and

complete environment diagnosis. Many of these groups (e. g.

small mammals and bats) also play a very important role in the

forest regeneration processes;

Construction of two observation towers in the company’s forest

areas – especially in the Agropalma Group Forest Reserve and

in the Águas Claras region. These towers are fundamental for a

monitoring program of primates and canopy birds, and may very

well serve as an assistant for the environmental education

activities developed by the company;

In case there is a need for the Agropalma Group to acquire new

forest areas in order to constitute their legal reserve system as

well as permanent preservation area, such new locations must

contemplate, preferably, sites where birds and primates

communities are still rich, especially where endangered species

could still be found - with emphasis on the Golden Parakeet, the

Black-bearded Saki and the Ka’apor Capuchin Monkey.

The presence of endemic and globally threatened species could bring

great benefits to the company’s environmental campaigns, plus undeniable

benefits for environment education programs. Some initiatives may be

suggested, such as:

Transform endangered species, especially the Golden Parakeet

and the Black-bearded Saki, in a reason for the company to be

proud of. In addition to being considered endangered, these two

species only occur in this region, and catch a lot of attention.

Their presence in the Agropalma Group Forest Reserve could

be transformed in a key piece for the company’s campaigns, and

employees may feel stimulated to be part of the process of

preservation and conservation of forest remnants;

Use these species (the Golden Parakeet and the Black-bearded

Saki, especially) in the company’s marketing pieces, aiming to

expand to new markets. The presence of endangered species

plus the participation of the company in environment

preservation projects could be a differential in an industry where

non-financial values increasingly make a difference;

Use endangered species as keys in programs, such as

environment education and awareness of employees and

populations who live near the company;

Show that the company effectively preserves endangered

species through promotion of conservation affirmative actions.

Construction of observation towers.

5. ACKNOWLEDGEMENTS

The work team, composed by Luís Fábio Silveira, Líliam Patrícia Pinto,

Fernando José Belmonte, Paulo César Balduíno and Carolina Mello, thank

the Agropalma Group for the great support and confidence given throughout

the present project. We especially thank Hilário Freitas, Marcelo Britto and

Agenilson Silva (São Paulo), César and Olaviano Neto (Belém), Gil Muner,

Stanley Silva, Sebastião Sinimbu, Flávio, Adauto, Elias, Célio and Mara

(Agropalma – Tailândia) for the warm reception and given help. To our field

team - drivers, local woodmen and securities - who were tireless in order to

accomplish all tasks the best possible way. Celso Sant´Anna (São Paulo), for

his always-present critical spirit and incentive. Our results, definitively, would

not be so expressive and meaningful without such fundamental support.

6. REFERENCES

BirdLife International (2000) Threatened birds of the world. Barcelona and

Cambridge, UK: Lynx Editions and BirdLife International.

Buckland, S.T., Anderson, D.R., Burnham, K.P., Laake, J.L., Borchers, D.L.

and Thomas, L. 2001. Introduction to Distance Sampling. Oxford

University Press, London.

Collar, N. J.; Gonzaga, L. A. P.; Krabbe, N.; Madroño Nieto, A.; Naranjo, L.

G.; Parker, T. A. and Wege, D. C. (1992) Threatened birds of the Americas:

the ICBP/IUCN Red Data Book. Cambridge, U. K., International Council for

Bird Preservation.

Cowlishaw, G. & Dunbar, R. 2000. Primate Conservation Biology. Chicago:

University of Chicago Press. 498p.

Novaes, F. C. & Lima, M. F. C. 1998. Aves de Belém. Belém: Museu

Paraense Emílio Goeldi, 415 p.

Peres, C. A. 1990. Effects of hunting on western Amazonian primates

communities. Biol. Cons. 54:47-59.

Peres, C. A. 1997. Effects of habitat quality and hunting pressure on arboreal

folivore densities in Neotropical forests: a case study of howler monkeys.

Folia Primatol. 68:199-222.

Peres, C.A. 1999. General guidelines for standardizing line-transect surveys

of tropical forest primates. Neotropical Primates 7(1):11-16.

Roma, J. C. 1996. Composição e vulnerabilidade da avifauna do leste do

Estado do Pará, Brasil. Dissertação apresentada ao Curso de Pós-

Graduação da Universidade Federal do Pará, 204 p.

Queiroz, H. L. 1992. A new species of Capuchin Monkey, genus Cebus

Erxleben 1977 (Cebidae, Primates), from eastern Brazilian Amazonia.

Goeldiana Zoologia (15): 1-3.

van Roosmalen, M.G.M.; Mittermeier, R.A. & Milton, K. 1981. The bearded

Sakis, genus Chiropotes. In Coimbra-Filho, A.F. & Mittermeier, R.A. (eds.).

Ecology and behavior of neotropical primates, vol. 1. Rio de Janeiro:

Academia Brasileira de Ciências. pp. 419-441.

van Roosmalen, M.G.M.; Mittermeier, R.A. & Fleagle, J.G. 1988. Diet of the

northern bearded Saki (Chiropotes satanas chiropotes): a neotropical seed

predator. Am. J. Primatol. 14:11-35.

7. APPENDIXES

Appendix 1: List of recorded birds in the foret areas of the Agropalma Group, Tailândia, Pará (total: 338 species).

x ORDER Popular name English name x Family (n. of species) Scientific Name x TINAMIFORMES * * x Tinamidae (7) * * Tinamus tao azulona Gray Tinamou

Tinamus major inhambu-de-cabeça-vermelha Great Tinamou

Crypturellus cinereus inhambu-preto Cinereous Tinamou Crypturellus soui tururim Little Tinamou Crypturellus variegatus chororão Variegated Tinamou Crypturellus strigulosus inhambu-relógio Brazilian Tinamou Crypturellus parvirostris inhambu-chororó Small-billed Tinamou x PELECANIFORMES * * x Phalacrocoracidae (1) * * Phalacrocorax brasilianus biguá Neotropic Cormorant x Anhingidae (1) * * Anhinga anhinga anhinga Anhinga x CICONIIFORMES * * x Ardeidae (6) * * Casmerodius albus garça-branca-grande Great Egret Egretta thula garça-branca-pequena Snowy Egret Bubulcus ibis garça-vaqueira Cattle Egret Butorides striatus socozinho Striated Heron Pilherodius pileatus garça-real Capped Heron Tigrisoma lineatum socó-boi Rufescent Tiger-Heron x Cochleariidae (1) * * Cochlearius cochlearius arapapá Boat-billed Heron x Threskiornithidae (1) * * Mesembrinibis cayennensis corocoró Green Ibis x Cathartidae (5) * * Sarcoramphus papa urubu-rei King Vulture Coragyps atratus urubu-de-cabeça-preta Black Vulture Cathartes aura urubu-de-cabeça-vermelha Turkey Vulture

Cathartes burrovianus urubu-de-cabeça-amarela Lesser Yellow-headed Vulture

Cathartes melambrotus urubu-da-mata Greater Yellow-headed Vulture

x ANSERIFORMES * * x Anatidae (3) * * Dendrocygna viduata irerê White-faced Whistling-

Duck

Amazonetta brasiliensis pé-vermelho Brazilian Teal Cairina moschata pato-do-mato Muscovy Duck x FALCONIFORMES * * x Accipitridae (16) * * Elanus leucurus peneira White-tailed Kite Gampsonyx swainsonii gaviãozinho Pearl Kite Elanoides forficatus gavião-tesoura Swallow-tailed Kite Leptodon cayanensis gavião-de-cabeça-cinza Gray-headed Kite Harpagus diodon gavião-bombachinha Rufous-thighed Kite Ictinia plumbea sovi Plumbeous Kite Rostrhamus sociabilis caramujeiro Snail Kite Accipiter bicolor gavião-bombachinha-grande Bicolored Hawk Buteo brachyurus gavião-de-cauda-curta Short-tailed Hawk Asturina nitida gavião-pedrês Gray Hawk Rupornis magnirostris gavião-carijó Roadside Hawk Leucopternis albicollis gavião-pombo-da-Amazônia White Hawk Leucopternis kuhli gavião-vaqueiro White-browed Hawk Busarellus nigricollis gavião-belo Black-collared Hawk Morphnus guianensis uiraçu-falso Crested Eagle Geranospiza caerulescens gavião-pernilongo Crane Hawk x Falconidae (11) * * Herpetotheres cachinnans acauã Laughing Falcon Micrastur semitorquatus gavião-relógio Collared Forest-Falcon Micrastur ruficollis gavião-caburé Barred Forest-Falcon Micrastur mintoni gavião-mateiro Lined Forest-Falcon Daptrius ater gavião-de-anta Black Caracara Daptrius americanus gralhão Red-throated Caracara Milvago chimachima carrapateiro Yellow-headed Caracara Caracara plancus caracará Southern Caracara Falco rufigularis cauré Bat Falcon Falco femoralis falcão-de-coleira Aplomado Falcon Falco sparverius quiriquiri American Kestrel x GALLIFORMES * * x Cracidae (4) * * Ortalis superciliaris aracuã-de-sobrancelhas Buff-browed Chachalaca Penelope superciliaris jacupemba Rusty-margined Guan Penelope pileata jacu-de-cocuruto-branco White-crested Guan Mitu tuberosa mutum-cavalo Razor-billed Curassow x Phasianidae (1) * * Odontophorus gujanensis corcovado Marbled Wood-Quail x GRUIFORMES * * x Aramidae (1) * * Aramus guarauna carão Limpkin x Rallidae (5) * * Aramides cajanea três-potes Gray-necked Wood-Rail Porzana albicollis sanã-carijó Ash-throated Crake Laterallus melanophaius pinto-d'água-comum Rufous-sided Crake Laterallus viridis siricora-mirim Russet-crowned Crake Gallinula chloropus frango-d'água-comum Common Moorhen x Eurypygidae (1) * * Eurypyga helias pavãozinho-do-Pará Sunbittern x CHARADRIIFORMES * * x Jacanidae (1) * * Jacana jacana jaçanã Wattled Jacana

x Charadriidae (2) * * Vanellus chilensis quero-quero Southern Lapwing Hoploxypterus cayanus batuíra-de-esporão Pied Lapwing x Scolopacidae (5) * * Tringa solitaria maçarico-solitário Solitary Sandpiper Tringa flavipes maçarico-de-perna-amarela Lesser Yellowlegs

Tringa melanoleuca maçarico-grande-de-perna-amarela Greater Yellowlegs

Actitis macularia maçarico-pintado Spotted Sandpiper Gallinago paraguaiae narceja South American Snipe x COLUMBIFORMES * * x Columbidae (9) * * Columba speciosa pomba-trocal Scaled Pigeon Columba cayennensis pomba-galega Pale-vented Pigeon

Columba subvinacea pomba-amargosa-da-Amazônia Ruddy Pigeon

Columba plumbea pomba-amargosa Plumbeous Pigeon Columbina passerina rolinha-cinzenta Common Ground-Dove Columbina talpacoti rola Ruddy Ground-Dove Leptotila verreauxi juriti White-tipped Dove Leptotila rufaxilla gemedeira Gray-fronted Dove Geotrygon montana pariri Ruddy Quail-Dove x PSITTACIFORMES * * x Psittacidae (15) * * Ara macao arara-canga Scarlet Macaw Ara chloroptera arara-vermelha-grande Red-and-green Macaw Guaruba guarouba guaruba Golden Parakeet Pyrrhura lepida tiriba-pérola Pearly Parakeet Forpus passerinus tuim-santo Green-rumped Parrotlet Brotogeris versicolurus periquito-de-asa-branca Canary-winged Parakeet Brotogeris chrysopterus tuipara-de-asa-laranja Golden-winged Parakeet Pionites leucogaster marianinha White-bellied Parrot Pionopsitta vulturina curica-urubu Vulturine Parrot Graydidascalus brachyurus curica-verde Short-tailed Parrot Pionus menstruus maitaca-de-cabeça-azul Blue-headed Parrot Pionus fuscus maitaca-roxa Dusky Parrot Amazona amazonica curica Orange-winged Parrot Amazona farinosa papagaio-moleiro Mealy Parrot Deroptyus accipitrinus anacã Red-fan Parrot x CUCULIFORMES * * x Cuculidae (6) * * Piaya cayana alma-de-gato Squirrel Cuckoo Piaya minuta chincoã-pequeño Little Cuckoo Crotophaga ani anu-preto Smooth-billed Ani Crotophaga major anu-coroca Greater Ani Tapera naevia saci Striped Cuckoo Dromococcyx pavoninus peixe-frito Pavonine Cuckoo x STRIGIFORMES * * x Tytonidae (1) * * Tyto alba suindara Barn Owl x Strigidae (6) * * Otus choliba corujinha-do-mato Tropical Screech-Owl

Otus usta corujinha-orelhuda NorthernTawny-bellied Screech-Owl

Lophostrix cristata coruja-de-carapuça Crested Owl

Pulsatrix perspicillata murucututu Spectacled Owl Glaucidium hardyi caburé-da-Amazônia Amazonian Pygmy-Owl Ciccaba virgata coruja-do-mato Mottled Owl x CAPRIMULGIFORMES * * x Nyctibiidae (2) * * Nyctibius aethereus mãe-da-lua-parda Large-tailed Potoo Nyctibius griseus urutau Common Potoo x Caprimulgidae (5) * * Nyctidromus albicollis curiango Pauraque Nyctiphrynus ocellatus bacurau-ocelado Ocellated Poorwill Caprimulgus rufus joão-corta-pau Rufous Nightjar Caprimulgus parvulus bacurau-pequeno Little Nightjar Caprimulgus nigrescens bacurau-de-lajeado Blackish Nightjar x APODIFORMES * * x Apodidae (2) * * Chaetura spinicauda andorinhão-de-sobre-branco Band-rumped Swift Reinarda squamata tesourinha Fork-tailed Palm-Swift x Trochilidae (13) * * Glaucis hirsuta balança-rabo-de-bico-torto Rufous-breasted Hermit

Phaethornis superciliosus besourão-de-rabo-branco Eastern Long-tailed Hermit

Phaethornis ruber besourinho-da-mata Reddish Hermit

Campylopterus largipennis asa-de-sabre Gray-breasted Sabrewing

Florisuga mellivora beija-flor-azul-de-rabo-branco White-necked Jacobin

Anthracothorax nigricollis beija-flor-preto Black-throated Mango Discosura longicauda bandeirinha Racket-tailed Coquette Thalurania furcata beija-flor-tesoura-verde Fork-tailed Woodnymph

Hylocharis sapphirina beija-flor-safira Rufous-throated Sapphire

Hylocharis cyanus beija-flor-roxo White-chinned Sapphire

Polytmus theresiae beija-flor-dourado-de-bico-curvo

White-tailed Goldenthroat

Topaza pella beija-flor-brilho-de-fogo Crimzon Topaz Heliothryx aurita beija-flor-de-bochecha-azul Black-eared Fairy x TROGONIFORMES * * x Trogonidae (4) * * Trogon melanurus surucuá-de-cauda-preta Black-tailed Trogon

Trogon viridis surucuá-grande-de-barriga-amarela White-tailed Trogon

Trogon rufus surucuá-de-barriga-amarela Black-throated Trogon Trogon violaceus surucuá-miudinho Violaceous Trogon x CORACIIFORMES * * x Alcedinidae (4) * * Ceryle torquata martim-pescador-grande Ringed Kingfisher Chloroceryle amazona martim-pescador-verde Amazon Kingfisher Chloroceryle americana martim-pescador-pequeno Green Kingfisher

Chloroceryle inda martim-pescador-da-mata Green-and-rufous Kingfisher

x Momotidae (1) * * Momotus momota udu-de-coroa-azul Blue-crowned Motmot x PICIFORMES * * x Galbulidae (3) * * Galbula cyanicollis ariramba-da-mata Blue-cheeked Jacamar

Galbula dea ariramba-do-paraíso Paradise Jacamar

Jacamerops aurea ariramba-grande-da-mata-virgem Great Jacamar

x Bucconidae (8) * * Notharchus macrorhynchus capitão-do-mato White-necked Puffbird Notharchus tectus capitão-do-mato-pequeno Pied Puffbird Bucco tamatia rapazinho-carijó Spotted Puffbird Nystalus striolatus rapazinho-estriado Striolated Puffbird

Malacoptila rufa barbudo-de-pescoço-ferrugem Rufous-necked Puffbird

Monasa nigrifrons bico-de-brasa Black-fronted Nunbird

Monasa morphoeus bico-de-brasa-de-testa-branca White-fronted Nunbird

Chelidoptera tenebrosa urubuzinho Swallow-wing x Ramphastidae (4) * * Pteroglossus aracari araçari-de-bico-branco Black-necked Aracari

Pteroglossus bitorquatus araçari-de-pescoço-vermelho Red-necked Aracari

Ramphastos vitellinus tucano-de-bico-preto Channel-billed Toucan

Ramphastos tucanus tucano-grande-de-papo-branco Red-billed Toucan

x Picidae (8) * * Piculus flavigula pica-pau-bufador Yellow-throated

Woodpecker

Piculus chrysochloros pica-pau-dourado-escuro Golden-green Woodpecker

Celeus undatus pica-pau-barrado Waved Woodpecker Dryocopus lineatus pica-pau-de-banda-branca Lineated Woodpecker

Melanerpes cruentatus benedito-de-testa-vermelha Yellow-tufted Woodpecker

Veniliornis affinis pica-pauzinho-avermelhado Red-stained Woodpecker

Campephilus melanoleucos pica-pau-de-topete-

vermelho Crimson-crested

Woodpecker

Campephilus rubricollis pica-pau-de-barriga-vermelha

Red-necked Woodpecker

x PASSERIFORMES * * x Thamnophilidae (22) * * Taraba major choro-boi Great Antshrike

Thamnophilus palliatus choca-listrada Chestnut-backed Antshrike

Thamnophilus nigrocinereus choca-preta-e-cinza Blackish-gray Antshrike

Thamnophilus aethiops choca-lisa White-shouldered Antshrike

Thamnophilus amazonicus choca-canela Amazonian Antshrike Pygiptila stellaris choca-cantadora Spot-winged Antshrike Dysithamnus mentalis choquinha-lisa Plain Antvireo Thamnomanes caesius ipecuá Cinereous Antshrike Myrmotherula axillaris choquinha-de-flanco-branco White-flanked Antwren

Myrmotherula hauxwelli choquinha-de-garganta-clara Plain-throated Antwren

Myrmotherula longipennis choquinha-de-asa-comprida Long-winged Antwren

Myrmotherula menetriesii choquinha-de-garganta-cinza Gray Antwren

Herpsilochmus chororozinho-de-asa- Rufous-winged Antwren

rufimarginatus vermelha Formicivora grisea papa-formigas-pardo White-fringed Antwren Cercomacra cinerascens chororó-pocuá Gray Antbird Cercomacra laeta chororó-didi Willis’ Antbird Pyriglena leuconota papa-taoca White-backed Fire-eye

Myrmoborus leucophrys papa-formigas-de-sobrancelha White-browed Antbird

Hypocnemoides maculicauda solta-asa Band-tailed Antbird

Sclateria naevia papa-formigas-do-igarapé Silvered Antbird Hylophylax poecilinota rendadinho Scale-backed Antbird Phlegopsis nigromaculata mãe-de-taoca Black-spotted Bare-eyex Formicariidae (2) * * Formicarius colma galinha-do-mato Rufous-capped

Antthrush Formicarius analis pinto-da-mata-de-cara-preta Black-faced Antthrush x Conopophagidae (1) * * Conopophaga roberti chupa-dente-de-capuz Hooded Gnateater x Furnariidae (9) * * Synallaxis albescens uipí Pale-breasted Spinetail Synallaxis gujanensis joão-teneném-becuá Plain-crowned Spinetail Certhiaxis cinnamomea curitié Yellow-chinned Spinetail

Philydor erythrocercus limpa-folha-de-sobre-ruivo Rufous-rumped Foliage-gleaner

Philydor ruficaudatus limpa-folha-de-cauda-ruiva Rufous-Tailed Foliage-gleaner

Automolus paraensis barranqueiro-pardo Olive-backed Foliage-gleaner

Xenops minutus bico-virado-miúdo Plain Xenops Xenops rutilans bico-virado-carijó Streaked Xenops

Sclerurus mexicanus vira-folha-de-peito-vermelho Tawny-throated Leaftosser

x Dendrocolaptidae (11) * * Dendrocincla fuliginosa arapaçu-pardo Plain-brown

Woodcreeper

Dendrocincla merula arapaçu-da-taoca White-chinned Woodcreeper

Deconychura longicauda arapaçu-rabudo Long-tailed Woodcreeper

Deconychura stictolaema arapaçu-de-garganta-pintada

Spot-throated Woodcreeper

Glyphorhynchus spirurus arapaçu-de-bico-de-cunha Wedge-billed Woodcreeper

Dendrexetastes rufigula arapaçu-canela Cinnamon-throated Woodcreeper

Dendrocolaptes certhia arapaçu-barrado Amazonian Barred-Woodcreeper

Xiphorhynchus picus arapaçu-de-bico-branco Straight-billed Woodcreeper

Xiphorhynchus guttatus arapaçu-de-garganta-amarela

Buff-throated Woodcreeper

Xiphorhynchus obsoletus arapaçu-riscado Striped Woodcreeper Xiphorhynchus spixii arapaçu-de-Spix Spix's Woodcreeper x Tyrannidae (41) * * Ornithion inerme poiaeiro-de-sobrancelha White-lored Tyrannulet

Camptostoma obsoletum risadinha Southern Beardless-Tyrannulet

Phaeomyias murina bagageiro Mouse-colored Tyrannulet

Tyrannulus elatus maria-te-viu Yellow-crowned Tyrannulet

Myiopagis gaimardii maria-pechim Forest Elaenia

Elaenia flavogaster guaracava-de-barriga-amarela Yellow-bellied Elaenia

Mionectes oleagineus supi Ochre-bellied Flycatcher Mionectes macconnelli abre-asa-da-mata MacConnell's Flycatcher Corythopis torquata estalador-do-norte Ringed Antpipit

Myiornis ecaudatus caçula Short-tailed Pygmy-Tyrant

Lophotriccus galeatus caga-sebinho-penacho Helmeted Pygmy-Tyrant Hemitriccus minor maria-sebinha Snethlage's Tody-Tyrant Poecilotriccus andrei maria-bonita Black-chested Tyrant Todirostrum maculatum ferreirinho-estriado Spotted Tody-Flycatcher

Todirostrum sylvia ferreirinho-da-capoeira Slate-headed Tody-Flycatcher

Tolmomyias sulphurescens bico-chato-de-orelha-preta Yellow-olive Flycatcher

Tolmomyias flaviventris bico-chato-amarelo Yellow-breasted Flycatcher

Platyrinchus platyrhynchos patinho-de-coroa-branca White-crested Spadebill

Platyrinchus saturatus patinho-escuro Cinnamon-crested Spadebill

Onychorhynchus coronatus maria-leque Royal Flycatcher Terenotriccus erythrurus papa-moscas-uirapuru Ruddy-tailed Flycatcher Myiobius barbatus assanhadinho Whiskered Flycatcher Attila spadiceus capitão-de-saíra-amarelo Bright-rumped Attila Rhytipterna simplex vissiá Grayish Mourner Laniocera hypopyrra chorona-cinza Cinereous Mourner Myiarchus ferox maria-cavaleira Short-crested Flycatcher Philohydor lictor bem-te-vizinho-do-brejo Lesser Kiskadee Pitangus sulphuratus bem-te-vi Great Kiskadee Megarynchus pitangua nei-nei Boat-billed Flycatcher

Myiozetetes cayanensis bem-te-vizinho-de-asa-ferrugínea

Rusty-margined Flycatcher

Myiodynastes maculatus bem-te-vi-rajado Streaked Flycatcher Legatus leucophaius bem-te-vi-pirata Piratic Flycatcher Empidonomus varius peitica Variegated Flycatcher Tyrannus melancholicus suiriri Tropical Kingbird

Pachyramphus polychopterus caneleiro-preto White-winged Becard

Pachyramphus marginatus caneleiro-bordado Black-capped Becard Pachyramphus validus caneleiro-de-chapéu-negro Crested Becard Pachyramphus rufus caneleiro-cinzento Cinereous Becard

Tityra cayana anambé-branco-de-rabo-preto Black-tailed Tityra

Tityra semifasciata anambé-branco-de-máscara-negra Masked Tityra

Tityra inquisitor anambé-branco-de-bochecha-parda Black-crowned Tityra

x Pipridae (7) * * Pipra rubrocapilla cabeça-encarnada Red-headed Manakin

Pipra pipra cabeça-branca White-crowned Manakin Pipra fasciicauda uirapurú-laranja Band-tailed Manakin Chiroxiphia pareola tangará-falso Blue-backed Manakin Manacus manacus rendeira White-bearded Manakin Tyranneutes stolzmanni uirapuruzinho Dwarf Tyrant-Manakin Schiffornis turdinus flautim-marrom Thrush-like Schiffornis x Cotingidae (5) * * Cotinga cayana anambé-azul Spangled Cotinga Xipholena lamellipennis anambé-de-rabo-branco White-tailed Cotinga Lipaugus vociferans cricrió Screaming Piha

Querula purpurata anambé-una Purple-throated Fruitcrow

Piprites chloris papinho-amarelo Wing-barred Piprites x Hirundinidae (4) * * Tachycineta albiventer andorinha-do-rio White-winged Swallow Phaeoprogne tapera andorinha-do-campo Brown-chested Martin Progne chalybea andorinha-doméstica-grande Grey-breasted Martin

Stelgidopteryx ruficollis andorinha-serrador Southern Rough-winged Swallow

x Troglodytidae (5) * * Donacobius atricapillus japacanim Black-capped

Donacobius Thryothorus genibarbis garrinchão-pai-avô Moustached Wren

Thryothorus leucotis garrinchão-de-barriga-vermelha Buff-breasted Wren

Troglodytes musculus corruíra Southern House-Wren Microcerculus marginatus uirapuru-veado Scaly-breasted Wren x Muscicapidae * * x Sylviinae (2) * * Ramphocaenus melanurus bico-assovelado Long-billed Gnatwren

Polioptila plumbea balança-rabo-de-chapéu-preto Tropical Gnatcatcher

x Turdinae (3) * * Turdus leucomelas sabiá-barranco Pale-breasted Thrush Turdus fumigatus sabiá-da-mata Cocoa Thrush Turdus albicollis sabiá-coleira White-necked Thrush x Vireonidae (3) * * Cyclarhis gujanensis pitiguari Rufous-browed

Peppershrike Hylophilus semicinereus verdinho-da-várzea Gray-chested Greenlet Hylophilus pectoralis vite-vite-de-cabeça-cinza Ashy-headed Greenlet x Emberizidae * * x Parulinae (1) * * Phaeothlypis rivularis pula-pula-ribeirinho Neotropical River

Warbler x Coerebinae (1) * * Coereba flaveola cambacica Bananaquit x Thraupinae (24) * * Schistochlamys melanopis sanhaço-de-coleira Black-faced Tanager Lamprospiza melanoleuca pipira-de-bico-vermelho Red-billed Pied Tanager Cissopis leveriana tietinga Magpie Tanager Hemithraupis guira saíra-de-papo-preto Guira Tanager

Lanio versicolor pipira-de-asa-branca White-winged Shrike-Tanager

Tachyphonus cristatus tiê-galo Flame-crested Tanager

Tachyphonus surinamus tem-tem-de-topete-ferrugíneo Fulvous-crested Tanager

Tachyphonus rufus pipira-preta White-lined Tanager Ramphocelus carbo pipira-vermelha Silver-beaked Tanager Thraupis episcopus sanhaço-da-Amazônia Blue-gray Tanager Thraupis palmarum sanhaço-do-coqueiro Palm Tanager

Euphonia chlorotica fi-fi-verdadeiro Purple-throated Euphonia

Euphonia minuta gaturamo-de-barriga-branca White-vented Euphonia Euphonia cayennensis gaturamo-preto Golden-sided Euphonia Tangara mexicana cambada-de-chaves Turquoise Tanager Tangara punctata negaça Spotted Tanager Tangara gyrola saíra-de-cabeça-castanha Bay-headed Tanager Tangara cayana saíra-amarelo Burnished-buff Tanager Tangara velia saíra-diamante Opal-rumped Tanager Dacnis lineata saí-de-máscara-preta Black-faced Dacnis Dacnis cayana saí-azul Blue Dacnis Chlorophanes spiza saí-verde Green Honeycreeper Cyanerpes caeruleus saí-de-perna-amarela Purple Honeycreeper

Cyanerpes cyaneus saí-azul-de-pernas-vermelhas

Red-legged Honeycreeper

x Emberizinae (12) * * Zonotrichia capensis tico-tico Rufous-collared Sparrow Ammodramus aurifrons cigarrinha-do-campo Yellow-browed Sparrow

Sicalis columbiana canário-do-Amazonas Orange-fronted Yellow-finch

Emberizoides herbicola canário-do-campo Wedge-tailed Grass-Finch

Volatinia jacarina tiziu Blue-black Grassquit Sporophila plumbea patativa-verdadeira Plumbeous Seedeater Sporophila americana gola Wing-barred Seedeater Sporophila nigricollis baiano Yellow-bellied Seedeater

Sporophila minuta caboclinho-lindo Ruddy-breasted Seedeater

Sporophila castaneiventris caboclinho-de-faixa Chestnut-bellied Seedeater

Oryzoborus angolensis curió Chestnut-bellied Seed-Finch

Arremon taciturnus tico-tico-do-mato-de-bico-preto Pectoral Sparrow

x Cardinalinae (6) * * Caryothraustes canadensis furriel Yellow-green Grosbeak Periporphyrus erythromelas bicudo-encarnado Red-and-black Grosbeak Pitylus grossus bico-encarnado Slate-colored Grosbeak Saltator maximus tempera-viola Buff-throated Saltator Saltator coerulescens sabiá-gongá Grayish Saltator Passerina cyanoides azulão-da-Amazônia Blue-black Grosbeak x Icterinae (6) * * Psarocolius viridis japu-verde Green Oropendola Cacicus cela xexéu Yellow-rumped Cacique Icterus cayanensis inhapim Epaulet Oriole

Agelaius ruficapillus garibaldi Chestnut-capped Blackbird

Leistes militaris polícia-inglesa-do-norte Red-breasted Blackbird Molothrus bonariensis chopim Shiny Cowbird

x Passeridae (1) * * Passer domesticus pardal House Sparrow

Appendix 2: Article in press in the scientific journal Ararajuba – Revista Brasileira de Ornitologia.

Breeding behaviour and general habits of the Golden Parakeet,

Guarouba guarouba, in Tailândia municipality, Pará, Brazil.

Luís Fábio Silveira 1 e Fernando José Belmonte 2

1. Departamento de Zoologia, Universidade de São Paulo, São Paulo. Rua do

Matão, Travessa 14, no 101, Cidade Universitária, São Paulo, SP, Brazil.

Cep-05508-900; Seção de Aves, Museu de Zoologia da Universidade de São

Paulo (MZUSP). Caixa Postal 42494, Cep 04218-970, São Paulo, SP, Brasil.

E.mail: lfsilvei@usp.br

2. Graduação em Ciências Biológicas, Universidade de São Paulo, São

Paulo. Rua do Matão, Travessa 14, no 101, Cidade Universitária, São Paulo,

SP, Brazil. Cep-05508-900. E.mail: febelmonte@yahoo.com.br

ABSTRACT. Breeding behavior and general habits of the Golden

Parakeet, Guarouba guarouba, in Tailândia municipality, Pará, Brazil.

The Golden Parakeet, Guarouba guarouba is a threatened species, endemic

from Brazil and found only in the states of Maranhão, Pará, Mato Grosso and

Rondônia. Little is known about its habits and breeding behavior. We

monitored an active nest of this species with two nestlings in the municipality

of Tailândia, Pará State for about 80 hours (between 27.i. and 05.ii.2004). The

nest was located in an angelim (Dinizia excelsa, Leg. Mimosoideae) about 30

m from the ground. Copulation and searching for nest sites were observed.

The nestlings were attended by four different individuals, on average eight

times a day. No adult bird spent the night with the nestlings during the period

the nest was monitored. The Golden Parakeets defended the nest site

aggressively, the whole group attacking species of the families Cathartidae,

Accipitridae, Falconidae, Psittacidae and Ramphastidae in a coordinated way,

but not the mainly insectivore Plumbeous Kite, Ictinia plumbea. The main

threats for the Golden Parakeets in the area are the loss of habitat and the

caught of nestlings for the illegal domestic pet trade.

KEY WORDS: Psittacidae, Golden Parakeet, Guarouba guarouba, breeding

behaviour, Brazil.

Introduction

The Golden Parakeet, Guarouba guarouba is a medium-size - ranging

from 34 to 36 cm total length - Psittacidae, which inhabits mainly “terra firme”

forests in the Brazilian states of Maranhão and Pará, with recent records also

in the states of Mato Grosso and Rondônia (BirdLife International 2004). It’s

considered as globally endangered species due to the rapid loss of its habitat,

especially in the North of the so-called “Amazonian Arch of Deforestation”,

located in Northern Maranhão and Eastern Pará (figure 1). In addition to that,

the Golden Parakeet has always been a very desirable species by illegal birds

traders, which also significantly contributed for the decrease of its population

in nature. (Oren e Novaes 1986, IBAMA 2003, BirdLife International 2004).

Little is known about the species’ breeding habits and behaviour and

most part of information about it was collected by Oren and Novaes (1986).

Breeding recordings are concentrated between November and February,

although there also records on birds breeding in October (Collar et al. 1992).

On 25.i.2004 we observed a group of ten Golden Parakeets in a

location in Eastern Pará. Watching an intense movement of four individuals to

the tree’s lower strata, an active nest with two fully feathered nestlings was

found, located in one of the highest angelim of this group. Our observations

about the breeding habits and behaviour of Golden Parakeets are based on

monitoring such nest.

Area Description and Methods

Observations about the Golden Parakeet breeding habits and

behaviour were taken during the performance of the bird survey in the forest

reserve of the Agropalma Group (c. 02°31’S; 48°52’W, figure 1), in the

municipality of Tailândia, Pará state. Work was performed between January

19 and February 05 of 2004.

Forest fragments, which compose the company’s legal reserve (about

50.000 ha), have different size and preservation status, as well as some

connectivity among some of them. The largest part of the preserved area is

composed of dense ombrophylous forest interspersed with wet, open, natural

fields. As a result of selective tree cutting in the past, in most part of the area,

emergent and other large size trees are rare and only a few are higher than

35 m. A good amount of trees with fruit was observed, for example

Tetragastris and Protium (Burseraceae). The understory is open and a few

small tributary streams, known as igarapés, cut the fragments.

Observations were made from a selected fixed point, on the ground,

located in front of the nest about 6 meters far from the tree where it was

located. Monitoring started at about 05:00 h, still in the dark, and the watcher

only left the place at night, after 18:30 h. Nest monitoring began on day

27.i.2004 and ended on day 05.ii.2004, in a total of approximately 80 hours of

observation. Behaviour aspects considered relevant, as well as the time spent

in each activity of the group were recorded and are here presented in topics.

The nest’s characteristics were recorded, whenever possible, according to

recommendations by Guedes and Seixas (2002).

We searched for marks in the plumage, which could individualize each

bird, especially those attending the nestlings. Only two birds, which didn’t take

care of the nestlings, were clearly identified based on the degree of wearing of

the tail feathers. Observations were done with the help of binoculars 8x40 and

10x50 mm, and many individuals were photographed in order to find less

conspicuous marks. Plumage of observed adults and nestlings were

compared to individuals deposited in collections of the Museu de Zoologia da

Universidade de Sao Paulo (MZUSP) and Museu Paraense Emílio Goeldi

(MPEG).

Many vocalizations were recorded (recorder Sony TCM 5000EV and

microphone Sennheiser ME66) and compared to available ones (e. g.

Whitney et al. 2002). All recordings were tentatively identified within their

behavior context (contact calls, nestlings’ begging, etc) in order to facilitate

further comparative studies on vocal repertoire. Such vocalizations will be

deposited at the Arquivo Sonoro Elias Coelho at the Universidade Federal do

Rio de Janeiro (ASEC - UFRJ).

Results and discussion

General behavior: two groups of Golden Parakeets were located within the

study area. A smaller group (six individuals) was sighted flying over “terra

firme” forest at a location known as Maçaranduba, about 15 km from the

second sighted group. Such second group, which nest was monitored, was

composed of ten adults and two nestlings, which in the beginning of the study

had not left the nest yet. Groups of Golden Parakeets may range from three to

thirty individuals (Oren and Novaes 1986, Oren and Parker 1997) and, more

recently (May 2003), F. Olmos and J. F. Pacheco (pers. comm.) observed a

group of 18 birds at Novo Progresso city, in Pará state. The groups monitored

by us, used only “terra firme” forests. According to local inhabitants these

birds are resident in such habitat and do not present a nomadic behavior,

local disappearance nor seasonally movement towards flooded forests

“várzeas”, as stated by Oren and Novaes (1986). Groups were easily located

through their unique vocalization and because they always landed on

emergent trees. While the rest of group foraged or took other activities, one or

two individuals stayed on the highest branches, as sentinels. The monitored

group was tolerant to our presence, allowing approaches as near as 5 meters,

especially when they were landed on the tree where the nest was located.

Nest location: the nest was located on an angelim tree (Dinizia excelsa, Leg.

Mimosoideae). This tree was 41 m high and was part of a group of four trees

of the same species, still alive and isolated from the rest of the forest by a

road. The entrance of the nest was located at 30 m high, on a thick branch,

which presented an angle of approximately 30° with the trunk. Its opening had

about 30 cm diameter and was located to the North (figure 2). Our

observations were similar to the ones made by Oren and Novaes (1986), who

verified similar heights for nests and didn’t observed any preference, by the

birds, for nidification or resting sites on live or dead trees. It was not possible

for us to estimate the depth of the monitored nest. Oren and Novaes (1986)

recorded very deep cavities, with the egg laid farther than 2 meters from the

nest entrance, which was continuously excavated by the adults. According to

these authors, such cameras located in deep cavities could be a strategy

against toucans, considered by them as one of the major predators of this

species’ eggs and nestlings (see below). Apparently, the choice for nest

location depends primarily on the existence of emergent trees. Trees,

presenting holes large enough to shelter the flock and eventual nestlings of

Golden Parakeet, are found mainly in forests with old growth and well-

developed trees. The angelim tree is one of the most searched places by the

Golden Parakeets as night shelter and nidification place, therefore the

presence of such trees is fundamental for the species. (C. Yamashita

pers.comm.).

Copulation and search for nidification sites: copulation in the morning (08:10

h) of day 01.ii.04 was observed. One couple flew to an isolated place on the

angelim crown, and after taking care of each other’s plumage, copulated for

about two minutes. Soon after mating, the couple flew down to one of the

angelim trees nearby and began exploiting two cavities, which had entrances

located at an approximately 45° angle, ten meters from the ground. In the

following days, two Golden Parakeets were observed exploiting, at least three

times a day, these same cavities, spending an average of 15 or 20 minutes

each time. One of such individuals spent most of the time inside one of these

cavities, while the other stayed on the entrance or carried out quick incursions

to the inside of it. Probably, this was the selected place for nidification,

although we have no further information about the success of this supposedly

couple breeding.

Care with nestlings: cooperation from other members of the flock in breeding

is very little documented for Psittacidae in general, but is eventually related to

the lack nest sites. Golden Parakeet is the only species whose observation of

nest helpers is quite well documented (Collar 1997), thou there are

statements of pairs which took care of their nestlings by themselves (Oren

and Novaes 1986). During the monitoring period the nest was attended by

only four individuals which we were not able – due to the lack of identification

marks - to determine if they were always the same ones or different members

of the flock, although our experience point to the first choice.

The group always arrived on the tree crown where the nest was located

between 6:10 and 6:30 h, always vocalizing. As soon as they perceived the

flock’s approach, the nestlings moved towards the nest’s entrance also

vocalizing. Individuals, which attended nestlings, stayed on the top of the tree

for another ten minutes, before coming down to feed them. On the average

adults attended nestlings eight times a day, staying with them around four

minutes each session.

Both observed nestlings were already fledged, although apparently,

they were of different ages (see below, figure 2). During the study period,

nestlings showed up on the nest edge about 14 times a day, for about eight

minutes each time, watching the surroundings, most of the time in silence. It

was not observed any relation between the time spent on the nest edge and

the environmental temperature, but related with the presence of adults groups

in the surroundings.

The group of Golden Parakeets went to the angelim trees about eight

times a day. While four adults attended the nestlings, the others took care of

plumage, besides keeping contact with the partner. Usually, when arriving on

the angelim trees, the group segregated in pairs or groups of up to four

individuals, always on the same tree, where they stayed for about 35 minutes

each visit.

Differently from expected, no adult individual stayed overnight with the

nestlings in the nest during the monitoring period. Between 18:15 and 18:35 h,

already at sundown, the whole group used to move to a nearby tree, located

about 60 m from the nest, where they spent the night and only returned in the

morning. Golden Parakeets are known for their gregarious behaviour, where

all members of the group spend the night together in the same cavity (Oren

and Novaes 1986). A possible explanation for this observation might be the

large size of nestlings and the size of the nest itself, which didn’t seem large

enough to shelter the whole group. Further observations including the hollow’s

measurement, would be necessary to confirm such hypothesis.

Nestlings leave the nest: on day 29.i. we observed the first flight of one of the

nestlings. At about 17:00 h one of the nestlings got near the nest edge and,

stimulated by the rest of the flock, which strongly vocalized, left in a rectilinear

flight towards the forest. In this flight the nestling was followed by the rest of

the flock, returning to the angelim crown about five minutes later. During the

next 20 minutes, the nestling stayed on the tree crown, always surrounded by

four adults, who fed it and took care of its plumage. The nestling returned to

the nest at 17:25 h, not flying again this day. In the following days, the nestling

left the nest an average of three times a day, staying outside for about 40 min

each time, thou always returning to sleep in the nest. The whole group was

very sociable with the nestling, following it in all flights. The other nestling,

apparently younger, didn’t leave the nest during the monitoring period.

The nestling, by the time it left the nest, already presented similar

posture and plumage to adult birds, although it presented more green feathers

on its head than the adults (figures 2-3). Juniper and Parr (1998) described

and illustrated the immature of such species as olivaceous-brown with dark

green dorsal grooves. There is no correspondence between the description

given by these authors and what was observed in the field or the skins

deposited in MZUSP and the MEPG, and there is no other indication, by these

authors, of the individual, which such description was based on. Immature

description presented by Forshaw and Cooper (1989) and Collar (1997) is

more appropriate and suitable with the observed in the fields and museums.

Reaction to the presence of other species: Golden Parakeets aggressively

defended nidification place as well as the group of three trees near the nest.

Individual or small groups of the following were observed - Cathartes aura, C.

burrovianus, C. melambrotos, Asturina nitida, Herpetotheres cachinnans,

Pyrrhura l. lepida, Pionites l. leucogaster, Pionus fuscus, P. m. menstruus,

Amazona f. farinosa, A. amazonica, Deroptyus accipitrinus fuscifrons,

Pteroglossus b. bitorquatus, P. a. aracari, Ramphastos vitellinus ariel and R. t.

tucanus flying at low altitude or landed on trees near the nest.

Representatives of the mentioned species were immediately attacked by the

Golden Parakeets, which presented territory defence behaviour similar in all

occasions. As soon as they noticed the presence of these birds anywhere

near the nest, the group of Golden Parakeets simultaneously flew into their

direction, usually dividing themselves in two smaller groups, attacking from

the sides and from the back, while intensively vocalizing. Twenty two flights of

territory defence were recorded, and in all of them, the intruders were rapidly

expelled, being still pursued in flight for a couple dozens meters. Despite the

fact that the group kept many species of Falconiformes away from the nest,

no reaction was observed to the presence of the Ictinia plumbea, which

landed and vocalized, in different occasions, on the same tree where the nest

was located, and furthermore, very close to it (< 4 meters). Golden Parakeets

did not show any reaction also to the presence of representatives of Picidae

and Passeriformes. Other natural cavities present in the same group of four

angelim trees also served as shelter for Strix virgata, Chaetura brachyura and

for at least two bats species, which were not molested by the Golden

Parakeets. Oren and Novaes (1986), based on third parties’ information,

pointed R. tucanus and R. vitellinus as major predators of Golden Parakeets’

eggs and nestlings, besides relating monkeys, tayras (Eira barbara,

Mammalia: Mustelidae) and snakes as possible predators of nest in forested

areas. These authors also stated, again based on third parties information,

that Golden Parakeet vigorously defended the nest from toucans.

Threats and final considerations: a large part of the natural landscape of the

Tomé-Açu micro-region is severely altered. Nowadays, threats to the few left

fragment are restricted to illegal loggers - who search for trees of lower

commercial value - and to colonization projects, where they eliminate native

vegetal cover in order to make cattle pasture. There are no federal or state

Conservation unities in that region of Pará state, which is considered of

extremely high biological value (MMA 2001). During our inventory, around 300

birds species were recorded and, besides the Golden Parakeet, we recorded

seven of the nine taxa designated as endangered and endemic to the Centers

“Pará and Belém (Maranhão)”, like Phlegopsis nigromaculata paraensis,

Dendrocincla merula badia and Dendrocolaptes certhia medius (IBAMA

2003). Therefore, conservation of the 50.000 ha of the forest which compose

the company’s legal reserve - even though discontinuous and with different

degrees of regeneration - have considerable importance both at regional and

national levels.

Besides the continuous loss of its habitat, Golden Parakeets’ nestlings

being taken away by wild animals smugglers could still be seen in the region.

During fast visits to the houses of local inhabitants, we could witness the

presence of three captive individuals. Two of them, which were bought while

nestlings, presented one of the wings with badly consolidated fractures,

resulting from falling during the nest tree-cutting. A third one (figure 2) was

taken away the same way on 04.i.2004. This nestling was been fed by hand,

with a mixture of manioc flour and water, plus fruit like banana and guava.

Also, we had knowledge of nestlings and adults sales to illegal traders of wild

animals based in Belém. Apparently, all individuals taken from the wild are

destined to Brazilian breeders, with no convincing evidence of international

traffic, and, unfortunately, the situation today does not look much different

from the one described by Oren and Novaes (1986). The cutting of trees

where the shelter or nest is located is the most usual means to obtain the

Golden Parakeet in the region. Such trees cutting, besides the obvious loss

which represents in the recruitment of new individuals, decreases the number

of available shelter and breeding sites, not only for the Golden Parakeet, but

also for other species which depend on natural cavities. The studied group

was composed by ten adults, and only two nestlings were successfully raised,

which suggests a low recruitment rate.

Although they occur in some conservation unities and other protected

areas, the Golden Parakeet’s situation in nature is far from secure. These

birds are still going through illegal wild animals trade, and are commonly

found in control operations conducted by environment protection official

bodies throughout the country. The fast and proper destination of such

apprehended specimen should be done by IBAMA, following an oriented

program of population in captivity management. Captive breeding of Golden

Parakeets in breeding facilities and zoos does not seem to be a difficult task,

and apparently has been happening since 1939, when a couple reproduced in

a private breeding facility in Sri Lanka (Hill 1939). An incentive to creation and

reproduction in captivity, besides an increase on control operations which will

effectively protect habitats and remnant populations of this species, could be

suitable tools which will guarantee preservation of this endemism so unique

and symbolic.

Acknowledgments

We are thankful to the Agropalma Group, for allowing access to the area as

well as for the infra structure made available to us, especially in the name of

Mr. Hilário de Freitas, Mr. Marcelo Britto and Mr. Gil Muner. Also to Celso

Sant´Anna, for the constant incentive. Líliam Patrícia Pinto, who helped in the

fieldwork. Edson Endrigo, who kindly provided the nice picture of the couple

and nestling. Carlos Yamashita, Fábio Olmos and Fábio Amaral for the

constructive suggestions on the manuscript.

Bibliographic references

BirdLife International (2004). Threatened birds of the world 2004. CD-Rom.

Cambridge, UK: BirdLife International.

Collar, N. J. (1997). Family Psittacidae, p. 280-479 Em: J. del Hoyo, A. Elliott e

J. Sargatal (eds.) Handbook of the Birds of the World. Barcelona: Lynx

Editions.

Collar, N. J., L. A. P. Gonzaga, N. Krabbe, A. Madroño Nieto, L. G. Naranjo,

T. A. Parker e D. C. Wege (1992) Threatened birds of the Americas: the

ICBP/IUCN Red Data Book. Cambridge: International Council for Bird

Preservation.

Forshaw, J. M. e W. T. Cooper. (1989) Parrots of the World. Willoughby:

Lansdowne Editions.

Guedes, N. M. R. e G. H. F. Seixas (2002). Métodos para estudos de

reprodução de psitacídeos, p. 123-140. Em: Galetti, M. e M. A. Pizo (eds.)

Ecologia e conservação de psitacídeos no Brasil. Belo Horizonte:

Melopsittacus Publicações Científicas.

Hill, W. C. O. (1939) Breeding of the Queen of Bavaria´s Conure in captivity.

Avicultural Magazine: 387-389.

Juniper, T. e M. Parr (1998) Parrots – a Guide to Parrots of the World. New

Haven: Yale University Press.

Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis

(IBAMA) (2003). Instrução Normativa n° 03, de 27 de maio de 2003 - Lista

das Espécies da Fauna Brasileira Ameaçadas de Extinção.

Ministério do Meio Ambiente (2001). Avaliação e identificação de ações

prioritárias para a conservação, utilização sustentável e repartição dos

benefícios da biodiversidade na Amazônia brasileira. Brasília: MMA/SBF.

Oren, D. C. e F. C. Novaes (1986) Observations on the Golden Parakeet

Aratinga guarouba in Northern Brazil. Biological Conservation 36: 329-337.

Oren, D. C. e T. A. Parker III (1997) Avifauna of the Tapajós National Park

and vicinity, Amazonian Brazil. Ornithological Monographs 48: 493-525.

Whitney, B. M., T. A. Parker III, G. F. Budney, C. A. Munn e J. W. Bradbury

(2002) Voices of New World Parrots. Compact Disc, Macaulay Library of

Natural Sounds.

Figure 1. Distribution of the Golden Parakeet, Guarouba guarouba, throughout the

states of Pará and Maranhão. Circle with dot: study area. Black circles: locations where

the species was recorded in the last 20 years. Asterisks indicate sites where the

species is only known for museum specimens. Golden Parakeet is considered extinct

in locations in Northeast Pará and Northwest Maranhão (modified from Oren and

Novaes 1986). Gray circles indicate the area affected by logging in the region (MMA

2001).

Figure 2. Golden Parakeet’s nest Guarouba guarouba, with one of the nestlings (photo

by Edson Endrigo).

Figure 3. Golden Parakeet (Guarouba guarouba) nestling taken away

from the nest on day 04.i.2004 and kept in captivity in the municipality of

Tailândia, Pará state.