South-west Amazonia is one of the world's biologically richest regions in terms of birds, with more than 500 species at some localities (e.g. Terborgh et al. 1984, Parker et al. 1994, Brown & Freitas 2002, Whittaker et al. 2002). The avifauna of the Brazilian state of Acre, which borders Peru, Bolivia and the Brazilian states of Rondônia and Amazonas, is well known, with more than 700 species documented (Guilherme 2016). In addition to species richness, the region is also characterised by high endemism, with many species unique to the Inambari centre of endemism between the Solimões and Madeira Rivers (Haffer 1978, Cracraft 1985, Silva et al. 2019). In Acre, at least 23 species are confined to the Inambari centre, and 12 of these occur in Brazil only in Acre and adjacent parts of Amazonas (Guilherme 2012, 2016). Furthermore, some species are restricted to eastern Acre, including many bamboo specialists (Guilherme & Santos 2009, Guilherme 2012, 2016).

Eastern Acre is also the region most affected by anthropogenic impacts in south-west Amazonia, at the western extreme of the ‘Arc of Deforestation’ in southern Amazonia, where cattle-ranching and cash-cropping are expanding relentlessly (Fearnside 2017). Acre's capital, Rio Branco, is also in this region, which is characterised by a mosaic of many urban and rural forest fragments within an anthropogenic matrix dominated by cattle pasture (Guilherme 2016).

Fragmentation of forest not only impacts avian communities, in particular by eliminating certain ecological guilds (Stouffer & Bierregaard 1995, Bierregaard & Stouffer 1997, Stratford & Stouffer 1999), but may also affect the physiological integrity of individual birds (Hernández-Palma & Stouffer 2018). Long-term studies of bird communities in forest fragments may provide potentially valuable insights into the impacts of fragmentation on community structure vis-à-vis pristine habitats (Rutt et al. 2017).

Although the number of bird surveys has progressively increased in Amazonia, systematic long-term surveys of a given area are still rare (Rutt et al. 2017). We compiled a list of the avifauna of Humaitá Forest Reserve (HFR), a forest fragment owned by the Instituto Nacional de Colonização e Reforma Agrária (INCRA), but which has been ceded to the Universidade Federal do Acre (UFAC) for research purposes. Other inventories available for HFR include medium-sized and large mammals (Botelho et al. 2012) and palms (Pinheiro et al. 2015). In 2009, the ornithological database of the HFR was consolidated during doctoral research by EG (Guilherme 2009). Since then, further work has been conducted in HFR, including by TLS and colleagues (Silva et al. 2015), TNM & EG (Melo & Guilherme 2016), DP & EG (Pedroza & Guilherme 2019) and JL and colleagues (Lima et al. 2019). While ongoing research in HFR over the past ten years has produced an increasingly solid database on its avifauna, no comprehensive list of birds was available for the reserve, until the present study.

Methods

Study area.—Humaitá Forest Reserve (HFR) is in the municipality of Porto Acre (09°45′52″S, 67°38′02″W), Acre, Brazil (Fig. 1), and covers c.2,000 ha (Botelho et al. 2012). The fragment is surrounded by the Humaitá Settlement Project and farms, with the Acre River forming its eastern limit. Climate is tropical humid, with mean annual temperatures of 24–26°C (Alvares et al. 2013) and mean annual rainfall of 1,900 mm (Alvares et al. 2013). Vegetation is a mosaic of open forest with bamboo, and open forest with palms on terra firme and seasonally flooded (várzea) soils (Barroso et al. 2011).

Data collection.—The preliminary bird species list for HFR was based on three published inventories (Guilherme 2009, 2016, Silva et al. 2015). We added unpublished records by other observers, together with those on digital platforms such as Wikiaves and Xeno-canto. Registration numbers of records on Wikiaves (WA) and Xeno-canto are indicated in the species accounts and Appendix. Species were identified via captures in mist-nets, visual observations or their vocalisations. Specimens collected in HFR and deposited in the ornithology laboratory at UFAC, Rio Branco, and the Museu Paraense Emílio Goeldi (MPEG), Belém, were also examined. Voucher specimens and media identification numbers published online were considered as physical evidence of the species' occurrence in HFR.

Species classification.—The list was reviewed to identify migratory, endemic species, habitat specialists, cynegetic and threatened species. Migratory species were classified using Somenzari et al. (2018), while bamboo forest specialists and species associated with patches of Guadua bamboo were identified based on Kratter (1997), Guilherme & Santos (2009), Lebbin (2013) and Guilherme (2012, 2016). Species endemic to the Inambari centre of endemism (sensu Silva et al. 2005, 2019) were identified using Haffer (1978), Cracraft (1985) and Guilherme (2012, 2016). Game (cynegetic) species targeted by subsistence hunters were classified following Ojasti (1993), Sick (1993) and Sigrist (2014). Conservation status follows IUCN (2019).

Figure 1.

Location of the Humaitá Forest Reserve (HFR) in the state of Acre, Brazil, near the city of Rio Branco (red star). The area that corresponds to the HFR, administered by the Federal University of Acre, is outlined by the red polygon.

Figure 2.

Examples of migratory species recorded in the Humaitá Forest Reserve, Acre, Brazil. (A) Broad-winged Hawk Buteo platypterus (Diego Pedroza); (B) Yellow-billed Cuckoo Coccyzus americanus (David P. Guimarães); (C) Rufous Casiornis Casiornis rufus (David P. Guimarães). (D) Swainson's Thrush Catharus swainsoni (Diego Pedroza).

Figure 3.

Three endemic species from the Inambari center associated with patches of Guadua bamboo recorded in the Humaitá Forest Reserve, Acre, Brazil. (A) Rufous-headed Woodpecker Celeus spectabilis (David P. Guimarães). (B) Rufous Twistwing Cnipodectes superrufus (Tomaz N. de Melo). (C) Acre Tody-Tyrant Hemitriccus cohnhafti (Ricardo Plácido).

Feeding guild and foraging stratum of each species was also determined, based on Wilman et al. (2014). Scientific nomenclature follows that of the Comitê Brasileiro de Registros Ornitológicos (Piacentini et al. 2015). In some cases, voucher specimens were collected under ICMBio / SISBio authorisation no. 23269-1, and deposited either at UFAC, Rio Branco, or MPEG, Belém. Some birds were banded using numbered metal rings supplied by CEMAVE (Centro Nacional de Pesquisa e Conservação de Aves Silvestres), under the scope of project 1099, coordinated by EG (senior bird bander, reg. no. 324654).

Results

Compilation of records made in HFR between 2009 and October 2019 revealed the presence of 356 bird species in 60 families and 23 orders (Appendix). Families represented by the largest numbers of species were Thamnophilidae (n = 37 species, 10.3% of the total), Thraupidae (n = 28 species, 7.9%), Tyrannidae (n = 26 species, 7.3%), Rhynchocyclidae (n = 17 species, 4.8%) and Psittacidae (n = 14 species, 3.9%). Overall, 195 species (54.8%) are passerines and 161 (45.2%) non-passerines.

The most species-diverse foraging guilds (Appendix) were the insectivores (196 species), frugivores (56 species) and omnivores (42 species). Most birds forage in the midstorey (84 species), canopy (50 species) or alternate between the understorey and midstorey (40 species).

Thirteen bird species visit HFR on migration (Fig. 2). Slightly more than half of these (53.8%, n = 7) are austral migrants, with the remainder 23.1% (n = 3) being intra-tropical migrants and 23.1% (n = 3) Nearctic migrants. Eleven species (3.1%) are endemic to the Inambari centre of endemism. Eighteen species (5.04%) are either bamboo forest specialists or possess some degree of association with tracts of Guadua bamboo in south-west Amazonia (Fig. 3). Twenty-nine species (8.1%) are considered to be cynegetic (Appendix), including Tinamidae (n = 9 species, 2.5% of the total), Anatidae (n = 1 species, 0.3%) and Cracidae (n = 3 species, 0.8%). Sixteen (4.5%) species are included in higher categories of threat by the IUCN (2019), including nine Near Threatened (2.5%) and seven Vulnerable (2%) (Appendix). Below, we comment on aspects of the biology and distribution of selected species.

Species accounts

Discussion

Bird species richness recorded in HFR (356 species) corresponds to 50.4% of the 708 species currently documented in the state of Acre (Guilherme 2016). This is an impressive number of species, considering that the fragment covers just 2,000 ha. The number of bird species recorded in HFR has progressively increased since 2009, when just 120 species had been recorded in the area based solely on specimens in museums (Guilherme 2009). The increase is due to constant ornithological field work in this forest, together with sporadic visits by amateur birdwatchers in the last ten years. Surveys in HFR prior to 2019 indicate that the site has a similar bird species richness to that in areas of continuous forest inventoried in Acre during shorter term studies, including Rio Acre Ecological Station (Guilherme & Aleixo 2010) and Chico Mendes Extractive Reserve (Mestre et al. 2010). Bird species richness in HFR is also considerably greater than that recorded in isolated fragments inventoried over the long term, e.g., Catuaba Experimental Farm (Rasmussen et al. 2005) (c.36 km from HFR) and the UFAC Zoobotanical Park (Guilherme 2001, 2016) (c.31 km from HFR).

Both of these sites are in eastern Acre and administered by UFAC. Prior to 2001, 150 bird species had been recorded in the Zoobotanical Park (Guilherme 2001), an area of c.100 ha (Meneses-Filho 1995), although this total increased to 196 species over the next 15 years (Guilherme 2016). In the Catuaba Experimental Farm fragment of 1,200 ha (Medeiros et al. 2013), 257 bird species were recorded by Rasmussen et al. (2005), and this number rose to 275 over the next 11 years (Guilherme 2016). Despite the increasing inventory, total richness at both sites is still lower than at HFR. The Zoobotanical Park is a small fragment within an urban matrix and has virtually no connectivity to other forested areas (Guilherme 2001), whereas Catuaba Experimental Farm is much larger, located within a rural matrix, and surrounded by properties with private reserves of forest (as mandated under current Brazilian environmental legislation). In contrast to these sites, HFR is a much larger area of forest, relatively distant from populated areas, and lies within a matrix of pasture and numerous private forest reserves that together with HFR form a single fragment. Although these areas are not directly comparable due to differences in the size and configuration of the fragments, their history of isolation and characteristics of the matrix (Ferraz et al. 2007), the progressive increase in number of species recorded at each site over time indicates that additional species will be recorded in HFR by further surveys.

Approximately 5% of bird species in HFR are associated with bamboo forests of south-west Amazonia (Kratter 1997, Guilherme & Santos 2009, Guilherme 2012, 2016). These species include two of the rarest birds at HFR, Rufous Twistwing and Acre Tody-Tyrant (Tobias et al. 2008, Zimmer et al. 2013, Harvey et al. 2014, Melo et al. 2015). The presence of ecological guilds most sensitive to fragmentation, such as mixed-species flocks of understorey insectivores, terrestrial insectivores and army ant followers, reflects the conservation potential of HFR for birds. The presence of several gamebirds, especially Razor-billed Curassow Pauxi tuberosa, Spix's Guan Penelope jacquacu and large tinamids such as Grey Tinamus tao and Great Tinamous T. major, indicates the viability of their local populations, despite hunting (DP & TNM pers. obs.). These findings are similar to those of Botelho et al. (2012) for medium and large mammals in HFR. Although they tend to become rarer, large cracids appear to be able to persist in areas with moderate hunting pressure (Barrio 2011, Kattan et al. 2016). The presence of Crested Morphnus guianensis and Harpy Eagles Harpia harpyja, which are also targeted by hunters (Trinca et al. 2007, Muñiz-López 2017) is a further indication of the favourable conditions. HFR is almost completely surrounded by cattle pastures, which environment lacks resources for the majority of migratory birds (Saab & Petit 1992), making HFR an important site for migratory species from different regions of the Americas during the year.

HFR is a potentially important area for bird conservation in eastern Acre, given that it has the highest bird species richness recorded anywhere in the state. In addition, it harbours important endemics and habitat specialists, and serves as a strategic stopover for migratory species. Birdwatching, which was initiated in 2013 at HFR by TNM, has attracted people from elsewhere in Brazil and other countries. This type of sustainable tourism has the potential to yield important economic benefits for the region. The proximity to the capital, Rio Branco, and the presence of rare birds such as Ash-throated Gnateater Conopophaga peruviana, Cnipodectes superrufus and Hemitriccus cohnhafti, should attract growing numbers of birders, who in turn can continue to monitor bird populations and add new species to the site list. Some rare species, such as Morphnus guianensis, were already found at HFR by hobby birders. Supervision by competent authorities (e.g., Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis - IBAMA) of this important reserve and continued monitoring of its avifauna should guarantee its role as a safe haven for the biodiversity of a region under increasing anthropogenic pressure.