Bird records from the rural landscape of Igarapé-Açu municipality, Northeastern Pará Registros de aves na paisagem rural do município de Igarapé-Açu, nordeste paraense

This paper reports on bird records from the little studied Bragantina region, in the densely populated Northeastern Amazon. This region was a center of human colonization in the last century, resulting in the nearly complete replacement of rainforests by a dynamic, mosaic-like rural landscape pattern. From February 1999 to January 2001, I surveyed birds at three sites: a 25-ha smallholding farm, and around two small lakes, in the municipality of Igarapé-Açu. Bird species were recorded along 36 days during an agricultural experiment. As would be expected, species lists from these sites show reduced bird diversity in comparison to primary forests. They also reveal a preponderance of robust, widespread generalists, such as Crotophaga ani (Linnaeus, 1758), Ramphocelus carbo (Pallas, 1764), and Columbina passerina (Linnaeus, 1758). However, endemic Xipholena lamellipennis (Lafresnaye, 1839), Tachybaptus dominicus (Linnaeus, 1766), and Primolius maracana (Vieillot, 1816) (high count of 34 at one time), were also observed. In all, 110 bird species (representing 95 genera and 40 families) are listed with information about abundance and habitat. More detailed surveys of this region are recommended, which should focus on gallery forests that might serve as refuges for some forest species.


INTRODUCTION
There are huge areas in Central and Western Amazonia, which are still in a 'primary' state, and which have never been visited by ornithologists (Oren & Albuquerque, 1991).Since these areas are still mainly forested, they are expected to be species-rich and might reasonably include species that are rare, endangered, endemic, or even new to science (e.g.Silva & Pimentel Neto, 1997;Pacheco et al., 2007).Exploration of such areas is a logical priority for biologists, particularly those in the conservation community.
Conversely, rural landscapes in Amazonia have received little attention from ornithologists and birdwatchers.Densely settled rural landscapes, which contain a significantly reduced avifauna in comparison to primary forests, are typically dominated by widespread common invaders and well-known neotropical generalists, and hence, attract little attention from the ornithological and conservation biology societies.A case in point is provided by the Bragantina region of Northeastern Pará State.The region is delineated to the west and the east by respectively the cities of Castanhal and Bragança, and to the north and south by the Atlantic Ocean and the river Guamá.Biogeographically, it belongs to the drier easternmost frontier of the Amazon, usually referred to as the 'Belém'-area of endemism (Haffner, 1969;Bates et al., 1998;Silva et al., 2005).As the Bragantina region was a center of colonization during the last century, human population density increased to an extraordinary high level for the Amazon of 38.9 inhabitants km -² in 1996 (IBGE, 2008).From the beginning of the last century, forested areas were assigned to settlers along the railroad Belém-Bragança, who turned the land use of their lots into extensive and fallowbased agricultural use.As a consequence, the ancient natural vegetation, the evergreen tropical rain forest, was almost completely converted into agricultural lands (Egler, 1961;Metzger, 2002).Because the common agricultural systems are based on slash-and-burn activities, the sustainability is based on the forest fallows, which are nationally called 'capoeira', in Brazil (Denich, 1991).Thus, the region mainly consists of a mosaic of maize, bean and cassava fields, and especially of extended capoeiras of various ages (Metzger, 2003).In the last decades, many of these areas were turned into more intensive agriculture.Capoeira fallows were shortened or completely replaced by permanent and semi-permanent land use systems like passion fruit, black pepper, or oil palm plantations (e.g.Silva et al., 1998;IBGE, 2008;Metzger, 2002Metzger, , 2003)).Also, since the 1980s, cattle husbandry became popular and large areas, even on smallholdings, were turned into pastures, a process called 'pecuarização' of the Bragantina region (Serrão & Toledo, 1992).The municipality of Igarapé-Açu typifies the Bragantina region and is classified as a rural region of middle to high demographic density with a tessellated landscape structure of various land use types (Nepstad et al., 1996;IBGE, 2008;Metzger, 2002;MMA, 2006).From the former rain forest, only small fragments remained, mainly as gallery forests along creeks (igapós), where no other use is possible.The climate of the region belongs to the humid warm tropics (Lauer et al., 1996), with a mean annual temperature of 27.6 °C and an average yearly rainfall of 2.469 mm.The 'Marcelino' climate station in Igarapé-Açu (Embrapa), in comparison to Belém, shows a prolonged dry season, which lasts from July until January (Denich, 1991;Hohnwald, 2002).
While investigations into the avifauna of the Belém area have a long scientific history (Novaes & Lima, 1998), there is only some basic information about the avifauna of Pará State in general (Novaes, 1980;Oren & Henriques, 1994;Nepstad et al., 1996) or the Bragantina region hinterland itself.However, one checklist includes major parts of adjacent areas east of Belém and gives an overview and an estimation of the abundance of species, but does not cover the whole region (Forrester, 1993).Detailed field observations were carried out in savannas, capoeiras, and mangroves in the municipality of Vigia (Novaes & Lima, 1992), which will be used as a reference in this study.There is no explicit publication concerning the avifauna of Igarapé-Açu itself.Therefore, the objective of this paper is to report the most important bird observations and to enhance the knowledge of the avifauna of an ornithologically poorly known region.

STUDy SITES
A two-year stay during the bilateral German-Brazilian SHIFT (Studies of Human Impact on Forests and Floodplains in the Tropics) project in the rural landscape of Igarapé-Açu, provided the opportunity to note some bird observation data besides fieldwork on a typical smallholder property.
The main observation location was a 25 ha smallholding (1 lot) in the vicinity of the village Nova Olinda at 47° 30' 18.46" W / 1° 2' 54" S in the northeast of the municipality of Igarapé-Açu, at the 'estrada velha Igarapé-Açu -Maracanã' (= road PA-426), at km 9 (site 1).The land use of the smallholding shows the typical mosaic pattern of a smallholder farm (Figure 1) with fruit trees and garden like plantations around the house located next to the road.Behind that home garden, a rural mosaic of cassava fields of up to two hectares, passion fruit and pepper plantations, as well as one to five hectare Brachiaria-pastures can be found.Furthermore, it also incorporates several small two-to-13 years old capoeira vegetation (up to 10 m high), and an on average 15 m high mature igapó forest along the Pupuca creek, in the back of the lot.Because fields, pastures, and plantations were not clearly separated from each other there often were young capoeira hedgerows between the units.The location also included the experimental site of the SHIFT-Pecuária project, where a 3.2 ha pasture of Brachiaria humidicola (Rendle) Schweick.(quicuio-da-Amazônia) was planted (Figure 1).The experiment incorporated treatments with bushy components in the pastures, e.g. a grass-capoeira pasture in which up to 30% cover of the re-sprouting capoeira re-growth is tolerated, a bushy grass-legume pasture, and nine 100 m² capoeira islands (Hohnwald, 2002;Hohnwald et al., 2006).
At site 1, birds were checked on 36 days: 21 days during the rainy season (six in 1999, seven in 2000, eight in 2001), and 15 days during the dry season (seven in 1999, eight in 2000), respectively.Observations were carried out during the agricultural field work, which lasted usually from approximately 8:00 to 16:00 hours.For data calculation, some single bird observations from other days were added to the next respective daily checklist.
The second location was a small pond (site 2) at km 2 of the PA-426 road, at 47° 32' 03.52" W / 1° 06' 34.22" S.This pond reaches a maximum size of 500 m² during the rainy season in March, but regularly dries completely out during the dry season, usually from October until the end of January.Its borders are mainly covered by three to six year old capoeira vegetation, but cattle trampling also leads to open and sandy lake borders.Due to its small size and also due to lack of time this location was only shortly checked during ten days, usually some minutes around 7:30 and at 16:15 hours.Additionally, some single bird observations of up to 1 km distance from site 2 along the road were added to this checklist.
The third site is the lake at the southern border of the city of Igarapé-Açu at 47° 37' 13.60" W / 1° 08' 36.56"S (site 3).This lake was visited seven times, usually at around 17:30 until dusk.The lake is extensively covered with water hyacinths (Eichhornia crassipes (Mart.)Solms, Pontederiaceae) and its border consisted of up to three years old capoeira.
Besides these three locations, additional observations from Igarapé-Açu municipality are also included in this paper, giving scientific family and species names, locations, remarks, and observation dates.Some records of noteworthy species which occur in Table 1 are further specified in the text.

OBSERVATIONS AND DATA EVALUATION
All bird observations, including the single ones in the text, were recorded between March 1999 and January 2001 in the municipality of Igarapé-Açu.Records were made through visual observations using 7 x 50 mm-binoculars.Some species, e.g. the Rallidae, were mainly identified by their voices and are marked with a '(v)' in the table.For species determination, mainly Ridgely & Tudor (1989;1994), Hilty & Brown (1986), and Novaes & Lima (1998) were used.
Daily checklists of site 1 were evaluated for abundance and frequency of each species.According to the frequency, species were categorized sensu Novaes & Lima (1992) namely as: abundant (present in > 80% of the days), common (61-80%), regular (41-60%), occasional (20-40%), and rare (< 20%).Bird records were also evaluated for wet (January-June) and dry season (July-December).Taxonomy follows Pacheco et al. (2007) and CBRO (2008), while assessment of species vulnerability follows Stattersfield & Capper (2000).The total species number is calculated by adding all species of Table 1 to the free-living species mentioned in the text.
None of the bird species found on any of the three sites is considered to be globally endangered, but Primolius maracana, found at site 1, is classified as 'vulnerable' (Stattersfield & Capper, 2000).1. Classification of the recorded bird species on a smallholding at Nova Olinda (site 1, Igarapé-Açu municipality) in five classes (Aabundant > 80% of the days, B -common 61-80%, C -regular 41-60%, D -occasional 20-40%, and E -rare < 20%, n = 36 days of observation).Habitat abbreviations: A = pasture, B = breeding on smallholding, C = capoeira (> 2 years old), E = experiment (grasscapoeira pasture), F = cassava fields, G = garden, H = hedgerows, young capoeira (≤ 2 years old), tall grasses, I = igapó forests, O = overflight, P = pepper fields.In the fourth column, the abundance of bird species of a capoeira in Vigia is listed, according to the same classes (A -E, Novaes & Lima, 1992).* = among the twenty most abundant capoeira species in Vigia.In the last two columns, the presence of species at site 2 and 3 is marked qualitatively.(v) = mainly identified by voice.The only North-American migrants recorded were five individuals of Hirundo rustica noted on spring migration on 3, 9, and 22 January (two individuals), and 5 February 2001, which is much earlier than the record of 9 April from Vigia (Novaes & Lima, 1992).
Mixed flocks of over 40 individuals of Sporophila minuta, Sporophila nigricollis, Sporophila americana, and Volatinia jacarina were frequent around site 1 during the dry season, mainly feeding on cassava fields and pastures.Some of them might be inner-Brazilian migrants from semi-arid Northeastern Brazil.One mixed-species flock of five Ramphocelus carbo, three Thraupis episcopus, four Saltator maximus, and two Schistochlamys melanopsis were observed at site 1, on 27 September 2000.
In general, the results show the same species spectrum found by Novaes & Lima (1992) in the capoeiras, savannas and mangroves of Vigia.For instance, if compared with the twenty most abundant bird species of the capoeira (Novaes & Lima, 1992: Table 3), seven species are also found among the 'abundant' species in this study (Table 1).However, Campylopterus largipennis (Boddaert, 1783), Myiobius barbatus (Gmelin, 1789), and Hylophilus semicinereus (Sclater & Salvin, 1867) were not observed in Igarapé-Açu.On the other hand, there are Lathrotriccus euleri, Leucopternis albicollis, Caracara plancus, Todirostrum chrysocrotaphum, Legatus leucophaius, Coryphospingus cucullatus which were not mentioned by Novaes & Lima (1992), although 'regularly' found in Igarapé-Açu (Table 1).These species might have been overlooked by Novaes & Lima (1992) probably just due to their limited observation times.Also, Crotophaga ani and Columbina passerina seem to be much more common in Igarapé-Açu than in Vigia.The main differences can be explained by the different survey methods, slightly different habitats, e.g.pure capoeiras, savannas, mangroves in contrast to a rural landscape mosaic, and different study times.
Besides abundant neotropical generalists, there are some noteworthy observations in Igarapé-Açu, such as that of Xipholena lamellipennis, Tityra semifasciata, Chiroxiphia pareola, Cacicus haemorrhous, Pipra rubrocapilla, Trogon viridis, Spizaetus tyrannus, Picumnus cirratus, and Ramphocaenus melanurus.These observations indicate that the mosaic-like rural landscape might still host more rare forest bird species than expected.The more so probably if major forest patches and tree islands would be protected (Nepstad et al., 1996).As species conservation strategies should not just concentrate on protected areas alone, smallholders have a considerable responsibility for the conservation of the local avifauna.Compensation payments might be an option for farmers to help maintain larger forest patches on smallholdings.
Xipholena lamellipennis is classified as a rare to locally uncommon forest bird species, living in humid tropical forest canopies and at forest borders (Ridgely & Tudor, 1994).As this species is endemic to the Lower Amazon, south of the river Amazon (Ridgely & Tudor, 1994), its survival must be seen as critical for the eastern half of its range to Maranhão is already densely settled and heavily deforested.However, as it was occasionally found in Vigia (Novaes & Lima, 1992) and the fact that both sexes have been observed at site 1 indicates that the species might be able to survive in forest islands of the Bragantina region.Primolius maracana is qualified as worldwide 'vulnerable' because of rapid decline in population due to exploitation, habitat loss, and degradation (Stattersfield & Capper, 2000;Snyder et al., 2000).The isolated island population of Northeast Pará (Juniper & Parr, 1998;Stattersfield & Capper, 2000) must also be considered critical in that context.However, large flocks of up to 34 individuals and regular observations of pairs all around Igarapé-Açu municipality and other common observations within the Bragantina region (Novaes & Lima, 1992) suggests that the population is stable in the region.But, as the species is said to feed partly on maize and beans, some farmers regard them as a pest (personal interview with three farmers).On the other hand, there were no signs that Primolius maracana is hunted or trapped for cage-bird trading.The species also obviously like to feed on bacuri trees (Platonia insignis Mart., Clusiaceae), which can be frequently found on smallholdings.
Guira guira is declared as 'scarce' in the Belém hinterland (Forrester, 1993), which seems either a printing error, a rough underestimation, or it might have become more common in the region with increasing deforestation in the last decades.Based on permanent observations at the Embrapa Amazônia Oriental in Belém, but also along the roads between Belém and Castanhal (BR 316), between Castanhal and Igarapé-Açu, and within the municipality of Igarapé-Açu the species should be clearly declared as a normal 'resident'.However, it seems that Guira guira is more abundant around Belém than in Igarapé-Açu.Besides the character bird species Croptophaga ani of the rural landscape, the other member of the Cuculidae family Tapera naevia seems to be almost as abundant as Guira guira in the rural landscape of Igarapé-Açu.
Besides bats and monkeys, birds are the most important seed dispersers in the Neotropics and play a major ecological role as facilitator species in the recolonization of capoeira tree species on degraded lands (Vieira et al., 1994).As the capoeira is still the ecological basis of fallow-based agriculture on smallholdings (Denich, 1991), these species are also agronomically important for the rural Bragantina region.Fortunately, most seed-dispersing bird species such as Ramphocelus carbo, Thraupis episcopus, Thraupis palmarum, Sporophila minuta, Sporophila nigricollis, Volatinia jacarina, Coereba flaveola, Tachyphonus rufus, Ammodramus aurifrons, and Saltator maximus are still quite common in the rural landscape (Table 1; classes A-B) so that the capoeira recuperation abilities seem to be unlimited.
The innovative agro-silvo-pastoral system of a grass-capoeira pasture (Hohnwald, 2002;Hohnwald et al., 2006) seems to offer attractive habitats for some rural bird species, e.g.Crotophaga ani, Ramphocelus carbo, and especially Columbina passerina, whose nests were found exactly in the middle of grass-capoeira pastures.
The presented bird observations were collected alongside field work of an agricultural field trial and thus surely will not be as complete as intensive mist-netting or other intense inventories.In many cases there was simply no time to track down bird vocalizations or other short appearances so that shy, rare, hidden or nocturnal species are probably underrepresented or overlooked in this study.This fact makes it also difficult to compare the results with other studies.However, an advantage of this study is that observations have been carried out over a rather long period of time, which often provides more accurate data than intensive studies for a short time (Bibby et al., 1992).
However, many common species (Forrester, 1993) of the Northeastern Amazon were not observed in the study area and might simply have been overlooked, e. Land use changes constantly take place in the rural landscape of the Bragantina region, following changing market prices of various products (Metzger, 2002;IBGE, 2008).As birds are specialized in their ecological niches, but also are able to quickly react to the environmental changes by simply flying to more suitable areas, the bird composition might be as dynamic as the changes in agroecosystems.Fortunately for bird life, most smallholder production systems are still extensively carried out and often based on capoeira fallows so that bird diversity stayed remarkably high in Igarapé-Açu.However, huge areas of the Eastern Amazon are already clear-cut and look worse than the investigated rural landscape.As deforestation of the Amazon continues, it is probable that a species-poor 'unattractive' bird community of generalist species will soon also be found in other parts of the Amazon, although in other bio-geographical zones these communities might contain slightly different species.Unfortunately, there are no local bird associations or even clubs, offering to publish annual bird reports and species lists, and usually infra-structure for international tourists or birdwatchers are lacking.Nevertheless, it should be interesting enough for scientists to observe which bird species keep pace with the dynamic land use changes in the Amazon.

Figure 1 .
Figure 1.Aerial view to the south on the studied smallholding at Nova Olinda (site 1): the typical rural landscape mosaic of the Bragantina region can be seen which consists of cassava fields, pastures, gardens, and capoeira.Around the Pupuca creek (right hand) dense gallery forests (igapó) can be seen, which turn into approximately 13 years old capoeiras further left (e.g.broad forest stripe behind road).At the centre of the photo, the pasture experiment of the SHIFT-project with its six dark capoeira spots is visible.The road on the left hand is the 'estrada velha Igarapé-Açu -Maracanã, PA-426', at km 9.The road at the bottom is the travessa 9. Photo: Wickel & Vielhauer, 15 April 2000.

Figure 2 .
Figure 2. Smooth-billed Ani (Crotophaga ani) is the most common character bird species of the mosaic-like rural landscape in Igarapé-Açu municipality.

found only at site 2 and site 3
Taxonomy follows CBRO (2008).