Ibis (2004), 146, 114 –124 Species poor but distinct: bird assemblages in white sand vegetation in Jaú National Park, Brazilian Amazon Blackwell Publishing Ltd. SÉRGIO HENRIQUE BORGES* Museu Paraense Emílio Goeldi, Departamento de Zoologia, Avenida Perimetral 1901/1907, 66077–530, Belém, PA, Brazil There have been few studies of the fauna of the distinctive vegetation that grows on sandy soil in Amazonia. Leached and nutrient-poor sandy soil is associated with a vegetation type that varies in structure from open fields (campinas) to low canopy forests (campinaranas). During a bird inventory in sandy soil vegetation at Jaú National Park (JNP), I recorded 128 bird species, with 55 in campina and 94 in campinarana. Estimates suggested only 150 bird species should be expected to occur in these habitats, a reduced species diversity compared with other vegetation types in the Amazon region. This low species diversity is probably linked to the low productivity of this habitat and its relatively simple vegetation structure. Despite the relatively low diversity, at least 14 bird species (3% of the entire avifauna) appear to be restricted to white sand vegetation in JNP. In Amazonia as a whole, some 37 bird species are associated with vegetation in sandy soils. Biological inventories of other taxa are needed to understand the contribution of white sandy vegetation to the faunal distribution in Amazonia. The vegetation of the Amazon region is generally classified as tropical rainforest. This broad classification encompasses a heterogeneous mosaic of physiognomies, including forests and non-forest vegetation, such as black-water and white-water flooded forests, terra firme forests, savannas and sandy soil vegetation (Pires & Prance 1985). One such vegetation type is that which grows over sandy soil (Rodriques 1961, Anderson 1981). The physiognomy of this habitat varies from open fields to low-canopy forests and, although widespread in the Amazon, is most typical of the Negro river basin, especially in its middle to upper course (Anderson 1981). This vegetation grows in the areas of very leached and nutrient-poor sandy soils distributed in ‘islands’ isolated by terra firme forest, which are found on more clay-dominated soils. This patchy distribution and the peculiar ecological conditions make this habitat poor in plant species diversity, but high in rates of plant endemism (Anderson 1981). In the central Amazon, for example, most (54.5%) of the vascular plants of sandy soil vegetation occur exclusively in this habitat *Present address: Fundação Vitória Amazônica, Avenida Djalma Batista, 440 fundos, Nossa Senhora das Graças, Manaus, AM, Brazil, 69080 –060. Email: sergio@fva.org.br © 2004 British Ornithologists’ Union (Anderson 1978). Furthermore, several researchers have called attention to the importance of sandy soil vegetation for landscape heterogeneity and the distribution of biodiversity in the Peruvian forests (Tuomisto & Ruokolainen 1994, Tuomisto et al. 1995, Whitney & Alvarez 1998). The biodiversity of Amazonian sandy soil vegetation has been studied by botanists and plant ecologists (Takeuchi 1960, Rodrigues 1961; Anderson et al. 1975, Braga & Braga 1975, Lisbôa 1975, Anderson 1978, 1981, Tuomisto & Ruokolainen 1994). By contrast, only a few studies have reported on the faunal composition of this habitat. These have included birds (Oren 1981, Díaz et al. 1995, Stiles et al. 1995), monkeys (Kinzey & Gentry 1979, Boubli 1999) and some invertebrate groups (Marco 1998, Adis et al. 1989a, 1989b). Because of the high rates of endemism of the faunal communities of sandy soil (at least when compared with plants), research on these sites suggests that they are important in understanding patterns of distribution of biodiversity in the Amazon region. I studied the bird assemblages of two sites of sandy soil vegetation in Jaú National Park (JNP), Amazonas, Brazil. I describe the species diversity and composition of these sites to evaluate the importance of the avifauna of sandy soil vegetation to local and regional Bird assemblages in white sand vegetation diversity. In addition, the results of this study were compared with other bird studies conducted in JNP (Borges et al. 2001) and other regions in the Amazon (Silva et al. 1997, Silva 1998). STUDY SITES The study was carried out in JNP (1°50′10″S 61°35′11″W), one of Brazil’s largest national parks at 22 720 km2. The Park is located approximately 200 km north-west of Manaus on the western margin of the Negro River. The major vegetation types found in JNP are non-flooded terra firme forests and igapó forests, which are seasonally inundated by blackwater rivers (Ferreira 1997, Ferreira & Prance 1998, Fundação Vitória Amazônica 1998). The sandy soil vegetation is concentrated mostly in the eastern section of the Park. Although the actual amount of land-cover of this vegetation type is unknown, the area occupied by it probably does not exceed 0.5% of the JNP area (Fundação Vitória Amazônica 1998). The terminology applied to sandy soil vegetation in the Amazon basin has often been confusing (see review in Anderson 1981). Part of this confusion is 115 explained by the high heterogeneity in the physiognomy of these habitats. Throughout this paper I use the term ‘campinarana’ to mean a low-canopy forest (7–20 m) with an understorey dominated by smalldiameter trees. Most trees of the campinarana in JNP (e.g. Pradosia schomburgiana, Aldina cf. heterophyla) are restricted to this vegetation (A. Vicentini pers. comm.). By contrast with campinarana, ‘campina’ is a shrubby vegetation with sparse trees, most of which are less than 5 m tall. Campina is typified by the presence of the palms Mauritia carana and Bactris campestris. Fieldwork was conducted in two localities, hereafter called Patauá and Seringalzinho (Fig. 1). In both regions, campinas are surrounded by campinarana and terra firme forests. The campina in the Patauá region occupies approximately 900 ha, whereas the campina in Seringalzinho occupies only 20 ha. The campina in Seringalzinho is dense shrub with a few more open fields (see Borges & Almeida 2001 for vegetation measurements). By contrast, campina in the Patauá region is much more open. In JNP, campinas and campinaranas are seasonally saturated by water. Campinas and campinaranas are easily identified from Landsat satellite images (Fig. 1) owing to Figure 1. Landsat image (only band 1 is shown) of the eastern part of Jaú National Park showing the regions where the fieldwork was conducted. White areas represent campinas, dark grey campinaranas and light grey the terra firme forest. The arrow points to a specific type of igapó with vegetation structure similar to campinas. © 2004 British Ornithologists’ Union, Ibis, 146, 114–124 116 S. H. Borges their typical landscape features (low canopy, seasonally saturated and sandy soil). MATERIALS AND METHODS The bird inventory was conducted in four field sessions as follows: August/September 1998 (Patauá region, 15 field days), March 1999 (Seringalzinho region, five field days), August 1999 (Seringalzinho, five field days) and March 2000 (Seringalzinho, five field days). In each field session birds were sampled by mist-net (36 mm mesh, 12 × 2 m), field observation and the use of tape recordings to document bird vocalizations (see below). At Patauá, I ran four mist-net lines in campinarana with eight and seven nets grouped in continuous straight lines. Nets were kept open from 06:00 to 12:00 hours for two consecutive days. In Seringalzinho I ran two lines with 12 and nine mist-nets, respectively. Seven mist-net lines (three in Patauá and four in Seringalzinho) with eight nets each were set in campina vegetation. The mist-nets in campina were kept open from 06:00 to 10:00 hours because, after this time, the nets were more visible and birds avoided them. In order to compare understorey bird communities of campinarana and campina with terra firme forest, I randomly selected data from nine net lines from a larger database of bird captures in JNP. The distances between capture sites ranged from 200 m to 20 km. The capture schedule resulted in 2312 net-hours (one net open for 1 h = 1 net-hour) in 22 capture sites as follows: 612 net-hours in six sites in campinarana, 800 net-hours in seven sites in campina and 900 net-hours in nine sites in terra firme forest. Mist-nets give a biased view of the bird community because only a portion of the birds present in a site are sampled (Karr 1981). To complete the analyses, all bird species detected by observation or vocalization were also recorded. I used a Marantz PMD 222 recorder and a Senheiser ME-66 microphone to record bird vocalizations. In most cases I performed play-back tests to obtain a better view of the birds. The identification of recorded voices of birds was aided by more experienced ornithologists (see Acknowledgements). In addition to general observations, I performed a standard census consisting of recording all birds detected during 1 h of walking the trails that cross each habitat sampled. There were 20 h of census accumulated in both campinarana and terra firme forest and 5 h of census in the campina. This standard census was performed only in the Patauá region. © 2004 British Ornithologists’ Union, Ibis, 146, 114–124 Data analysis To analyse habitat use, I tested whether the proportion of captures (abundance) and number of sites (site fidelity) of particular species differed among habitats using a chi-squared test. For this analysis I merged campina and campinarana into the same category to increase the sample size and selected only species with at least 10 captures in six sites. The relationships of species composition among sites were analysed by a non-metric dimension scaling (NMDS) using presence and absence data from mistnet captures and standard censuses. Sorensen’s coefficient was used as a distance measure to run NMDS and only species recorded in at least three sampling units (net-line or census-hour) were considered. The analyses followed the general procedures suggested by McCune and Mefford (1995). The species richness of birds was estimated by a first-order Jackknife estimator using each field day as a sampling unit. This non-parametric measure is considered to be one of the best estimators in the ecological literature (Palmer 1990, Colwell & Coddington 1994). To evaluate the contribution made by birds of the Amazonian sandy soil vegetation to the local and regional avifaunas, I compared the checklist of birds of campina and campinarana with bird inventories performed in terra firme forest, igapó flooded forest (Borges et al. 2001) and savanna vegetation (Silva et al. 1997, Silva 1998). There are several limitations in comparing bird checklists, including unequal sampling effort, the definition of the core avifauna to be compared and differences in the methodology employed for the bird inventory (Remsen 1994). The following criteria were adopted to maximize the comparability among the checklists: (1) birds observed more frequently in flight (Cathartidae, Psittacidae, Apodidae, Hirundinidae) and aquatic birds (Ardeidae, Charadriidae) were omitted from comparison; (2) species marked with habitat codes 4 (campina forest) and 7 (Curatella americana/ Byrsonima crassifolia campo) in Silva (1998), S (terra firme savannas) in Silva et al. (1997), TF (terra firme forest) and IG (igapó flooded forest) in Borges et al. (2001) were included in the comparisons. RESULTS Number of species I recorded 128 bird species: 55 in campina and 94 in campinarana (Appendix 1). The estimate of bird species richness in campinarana was around Bird assemblages in white sand vegetation 113 species, whereas approximately 66 species are expected to occur in campina (Fig. 2). Curves of cumulative species by sampling effort suggested that the inventory was near 80% complete in both habitats (Fig. 2). Standard comparisons show that more species were detected in terra firme forest (mean = 14.4, sd = ±2.2 species/h) than in white sand vegetation (mean = 9, sd = ±0.9 species/ h) (U = 38.5, P < 0.05). Species composition at the local scale Species composition differed strongly among the habitats considered (Fig. 3). The same pattern of greater similarity between the two types of forests (campinarana and terra firme forests) than between them and the campina was revealed by both sampling methods (Fig. 3a & 3b). This pattern can be partially explained by the more closed vegetation structure in the two forest types. The best represented guild in campina/campinarana was the frugivore–insectivores, with four species (Xenopipo atronitens, Tachyphonus phoenicius, Pipra erythrocephala and Elaenia ruficeps) responsible for 53.5% of total mist-net captures in the campina (Table 1). However, in the terra firme forests, insectivorous birds (Hylophylax naevia, Thamnomanes caesius and Pithys albifrons) were the best represented group (Table 1). From 87 species recorded in standard censuses, 13 were exclusively recorded in campina, 22 in campinarana and 30 in terra firme forest. Several bird species show tendencies in habitat association, 117 including Galbula leucogastra, Hemitriccus minimus, Hylophilus brunneiceps (recorded only in the campinarana census), Hylophylax naevia, Tyranneutes stolzmanni, Galbula dea (terra firme forest census), and Formicivora grisea, Schistochlamys melanopis and Emberizoides herbicola (campina census – Fig. 4). Species composition at the regional scale The similarity in bird species composition among the habitats was generally low (Table 2). The campinarana was more similar to terra firme forest than expected given the connectivity of these forests (Table 2). By contrast, bird species composition in the campinas is very distinct from the forested sites. A large proportion (46%) of bird species recorded in campina/campinarana were also found in black-water inundated forest or igapó forest (e.g. Myrmotherula cherriei, Hemitriccus minimus, Galbula leucogastra). In fact, the similarity between campina /campinarana and igapó forest is greater than between these habitats and Amazonian savannas (Table 2). This is surprising because the sandy soil vegetation in JNP is separated from igapó forest by several kilometres of terra firme forest (Fig. 1), and these birds are not recorded in the latter habitat. In recent fieldwork, I sampled birds in a specific type of igapó with vegetation physiognomy very similar to campinas that occur in patches along the Jaú river (Fig. 1). In this type of open igapó I recorded several birds typically associated with campinas, such as Myrmeciza disjuncta and Dolospingus fringilloides. Figure 2. Bird species cumulative curves (observed and estimated) by sampling effort in campina and campinarana habitats. The firstorder Jackknife estimator was used to construct the estimated curves. The position of the sampling units was resampled 1000 times. © 2004 British Ornithologists’ Union, Ibis, 146, 114–124 118 S. H. Borges Figure 3. Ordination of sampling units in non-metric dimension scaling (NMDS) similarity space based on (a) captures and (b) standard censuses. Table 1. Number of individuals and number of sites (in parentheses) where selected species were captured in the three habitats studied at Jaú National Park. The expected value in a chi-squared test was based on total captures (n = 439) and sites sampled (n = 22). Bird species Dendrocincla merula Thamnomanes caesius Myrmotherula axillaris Hylophylax naevia Hylophylax poecilinota Pithys albifrons Gymnopithys leucaspis Phlegopsis erythroptera Elaenia ruficeps Schiffornis turdinus Xenopipo atronitens Pipra coronata Pipra pipra Pipra erythrocephala Tachyphonus phoenicius Guild Terra firme forest Campinarana Campina Insectivore (ant-follower) Insectivore (mixed-flocks) Insectivore (mixed-flocks) Insectivore (solitary) Insectivore (solitary) Insectivore (ant-follower) Insectivore (ant-follower) Insectivore (ant-follower) Frugivore–insectivore Frugivore–insectivore Frugivore–insectivore Frugivore–insectivore Frugivore–insectivore Frugivore–insectivore Frugivore–insectivore 8 (5) 13 (6) 3 (3) 12 (6) 12 (6) 13 (5) 18 (7) 5 (4) 0 (0) 8 (5) 0 (0) 9 (6) 4 (3) 0 (0) 0 (0) 14 (4) 0 (0) 7 (4) 0 (0) 12 (6) 3 (1) 10 (4) 7 (2) 0 (0) 8 (4) 13 (5) 0 (0) 3 (2) 0 (0) 2 (2) 1 (1) 0 (0) 3 (2) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 14 (4) 0 (0) 35 (4) 1 (1) 4 (3) 16 (4) 18 (5) © 2004 British Ornithologists’ Union, Ibis, 146, 114–124 P value Abundance P value Site fidelity NS 0.0001 NS 0.0001 NS 0.002 0.01 NS NS 0.01 NS 0.01 NS 0.02 0.21 NS NS 0.0001 0.003 NS NS 0.03 0.004 NS 0.0006 0.07 Bird assemblages in white sand vegetation 119 Table 2. Similarity in bird-species composition (based on Jaccard index) between sandy soil vegetation and other vegetation types in the Amazon region. Number of species shared by the habitats being compared is given in parentheses. Campina Campinarana Savanna (RR) Savanna (AP) Igapó forest Campinarana Savanna (RR)* Savanna (AP)† Igapó forest‡ Terra-firme forest‡ 15.38% (18) 11.21% (13) 0.62% (1) 7.50% (9) 0.62% (1) 30% (36) 14.36% (26) 25% (48) 7.34% (16) 7.83% 17 7.02% (20) 25.65% (69) 1.53% (5) 1.53% (5) 22.75% (76) *Bird checklist from savannas of Roraima (Silva 1998). †Bird checklist from savannas of Amapá (Silva et al. 1997). ‡Bird checklist from Borges et al. (2001). Figure 4 Examples of birds typically associated with white sandy vegetation in the Amazon: (a) Dolospingus fringilloides male, found in campinas and campinaranas; (b) Myrmeciza disjuncta male, a small antbird found in shrubby campinas; (c) Neopipo cinnamomea, a rare small insectivorous bird captured in campina; (d) Xenopipo atronitens male, a frugivore – insectivore very common in campinarana and shrubby campina. The avifauna of campina differs from that of other open habitats in the Amazon (Table 2). Some bird species that occur in campinas have wide distributions in Amazonian savannas, such as Emberizoides herbicola, Caprimulgus rufus and Formicivora grisea (Silva et al. 1997, Stotz 1997, Bates et al. 1998). However, some species are truly associated with campinas (e.g. Myrmeciza disjuncta, Dolospingus fringilloides). Another good example of a distinction between campinas and Amazonian savannas concerns the birds of the genus Sporophila. No species of this group was found in campinas, but at least six Sporophila species have been recorded in savannas in the states of Roraima and Amapá (Silva et al. 1997, Stotz 1997, Silva 1998). Comparisons between different campinas are complicated because there is no published checklist of birds of this habitat. Therefore, I compare only the avifauna of Seringalzinho and Patauá campinas. The similarity between these two sites was 50% (based on the Jaccard index), with 11 and 15 species recorded only in Patauá and Seringalzinho, respectively. The distributions of some species are probably associated with vegetation structure in campinas. For example, the species Myrmeciza disjuncta and Dolospingus fringilloides were only recorded in the more shrubby and dense Seringalzinho campina, whereas Emberizoides herbicola and Chordeiles pusillus were much more common in the Patauá campina, which has more open and extensive fields. Although very preliminary, these results suggest that the highly variable vegetation structure of campinas can affect the local bird assemblages. DISCUSSION Species richness Studies of the sandy soil vegetation avifauna in other sites in Amazonia have indicated that the number of bird species in this habitat can vary from 77 to 111 (Oren 1981, Stiles et al. 1995). The species richness estimates in this study suggest that no more than 150 bird species are found in white sandy vegetation in Amazonia. In the JNP only disturbed vegetation has fewer species (Borges et al. 2001). Terra firme forest in the central Amazon holds more than twice as many bird species as do the campinas and campinaranas (Cohn-Haft et al. 1997, Borges et al. 2001). These numbers indicate that the avian assemblages in white sandy vegetation are depauperate in species richness compared with other Amazonian vegetation types. This pattern of low species diversity is similar to that found in plant communities (Anderson 1981). Similarly, general observations indicate that © 2004 British Ornithologists’ Union, Ibis, 146, 114–124 120 S. H. Borges the fauna of sandy soil vegetation in several tropical regions is also extremely species-poor (Janzen 1974, Emmons 1984). The low species richness can ultimately be related to the low productivity of the soils that sustain the campinas and campinaranas. A relationship between soil productivity and biological diversity has been demonstrated in other studies (see review in Rosenzweig & Abramsky 1993), and the low productivity of some soil types has been correlated with the low species diversity in plants and small mammals at some sites in Amazonia (Emmons 1984, Gentry & Emmons 1987). A more proximate cause of the low diversity of bird species in campinas and campinaranas is the vegetation structure, which is much more open and has a lower canopy than is found in other habitats (e.g. terra firme forest, igapó flooded forest). For example, some birds of mixed-species flocks, which are an important component of Neotropical bird species richness (Powell 1989), probably avoided the campinarana because of the open structure resulting from the small diameter of understorey trees and shrubs. Species composition Although poor in species, the avifauna of campinas and campinaranas has a distinct composition (Oren 1981, Stotz et al. 1996, this study), a pattern that is similar to that found in plant communities (Anderson 1981). In particular, comparison with savanna vegetation (Table 2) suggests that in the context of Amazon open vegetation, the campina avifauna represents a relatively well-delimited group. In JNP at least 14 species, or 3% of the avifauna recorded in the region, appear restricted to campinas and campinaranas (Borges et al. 2001, author’s unpubl. data). Moreover, some species, although not restricted to campinas and campinaranas, are much more abundant in these habitats (e.g. Neopelma chrysocephalum, Xenopipo atronitens). In the Amazon region approximately 37 bird species are known to have some level of association with white sand vegetation (Appendix 2). The biology of most of these species is poorly known, rendering the categorization presented in Appendix 2 as very preliminary. However, the number of species associated with sandy soil vegetation will probably increase with more detailed ecological and systematic studies, because several subspecies and even some recently described species are probably endemic to white sandy soil vegetation (Oren 1981, © 2004 British Ornithologists’ Union, Ibis, 146, 114–124 Whitney & Alvarez 1998, Alvarez & Whitney 2001, Isler et al. 2001). Conservation The conservation of the biodiversity of campinas and campinaranas is favoured by nutrient-poor soils that are inadequate for agriculture. However, the soils are also responsible for the low resilience to disturbance of this vegetation. Owing to their isolated nature and poor soil, the recovery of vegetation is slow after disturbance (Anderson 1981). Since the 1980s, anthropogenic disturbance affecting white sandy vegetation includes the removal of the sand for building around Manaus (Anderson 1981, author’s pers. obs.). Another source of disturbance in campinas is fire. Approximately 25% of the campina in the Patauá region was burned in 1995. If the populations and distribution of bird species in campina and campinarana are as reduced as some studies suggest (Oren 1981), even small-scale disturbances can affect the biodiversity of this ecosystem. Fortunately, the vegetation on sandy soils in the Brazilian Amazon has been little affected by deforestation (INPE 2000). Moreover, most of this vegetation type is concentrated in the Rio Negro basin, one of the less disturbed regions of the Brazilian Amazon with a high concentration of protected areas (Borges & Pinheiro 2001). Studies on birds and plants suggest that other faunal elements of campina and campinarana will also be distinct from those of other vegetation types. Further biological inventories are needed to understand the importance of this habitat to the distribution of animal species in the region. These inventories can benefit from the use of modern geoprocessing techniques (Tuomisto et al. 1994) for mapping the distribution of white sand soil vegetation and its peculiar biota. I am grateful to Ricardo Afonso, Marcelo Tonini, Marcela Santamaria, Marcela Nascimento and Mario Cohn-Haft for helping with fieldwork in Jaú National Park. Special thanks go to Mario Cohn-Haft, who taught me several aspects of the natural history of birds of campinas and campinaranas. Mario Cohn-Haft, Bret Whitney and Andrew Whittaker helped with bird identification from voice recordings. The staff of Fundação Vitória Amazônica, especially Célio Ribeiro, Fernando Oliveira, Lindalva, Conceição and Isdale provided logistical support during the field expeditions. The manuscript was improved by discussions and corrections from Emílio Bruna, Philip Stouffer and Alberto Vicentini. J.V. 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Tinamidae Crypturellus cinereus (cp,ig) Crypturellus soui (cp,c,tf,dv) Crypturellus cf. erythropus (c) Crypturellus variegatus (cp,tf) Cathartidae Cathartes aura (c) Accipitridae Elanoides forficatus (c,tf,s) Asturina nitida (c,cp,ig) Rupornis magnirostris (cp,c,tf,ig,dv,s) Falconidae Daptrius ater (cp,ig) Cracidae Penelope jacquacu (cp,tf) Psophiidae Psophia crepitans (cp,tf) Columbidae Columba speciosa (cp,dv,ig) Columba cayennensis (c,ig,dv,s) Columba subvinacea (cp,tf) Columba plumbea (cp,tf) Geotrygon montana (cp,tf) Psittacidae Ara ararauna (cp,tf,ig) Aratinga pertinax (cp,ig) Pyrrhura melanura (cp,tf,ig) Brotogeris chrysopterus (cp,tf,ig) Pionites melanocephala (cp,tf) Pionopsitta barrabandi (cp,tf,ig) Amazona amazonica (cp,c,ig) Amazona farinosa (cp,tf) Cuculidae Piaya melanogaster (cp,tf) Tapera naevia (c,s) Tytonidae Tyto alba (c,dv) Strigidae Otus choliba (cp,ig,dv) O. watsonii (cp,tf) Strix huhula (cp,tf,ig) Asio stygius (c,ig) Nyctibiidae Nyctibius griseus (cp,tf,ig) Caprimulgidae Chordeiles pusillus (c,s) Caprimulgus rufus (cp,c) Caprimulgus cayennensis (c,s) Caprimulgus nigrescens (c,dv) Trochilidae Phaethornis superciliosus (cp,c,tf,ig) Phaethornis ruber (cp,c,tf,dv) Thalurania furcata (cp,c,tf,ig,dv) Hylocharis cyanus (cp,c,ig,dv) Hylocharis sapphirina (c,tf,dv) Chlorostilbon mellisugus (c,ig,dv,s) Polytmus theresiae (c) Topaza pyra (cp,c) Trogonidae Trogon melanurus (cp,tf,ig,dv) Trogon viridis (cp,tf,ig,dv) Galbulidae Galbula leucogastra (cp,ig) Galbula dea (cp,tf,ig) Jacamerops aurea (cp,tf) Bucconidae Bucco tamatia (cp,tf,ig) Capitonidae Capito niger (cp,tf,ig) Ramphastidae Ramphastos vitellinus (cp,tf,ig) Ramphastos tucanus (cp,tf,ig) Picidae Celeus elegans (cp,tf,ig) Celeus grammicus (cp,tf,ig) Celeus torquatus (cp,tf,ig) Dendrocolaptidae Dendrocincla fuliginosa (cp,tf,ig,dv) Dendrocincla merula (cp,c,tf,ig) Sittasomus griseicapillus (cp,tf,ig) Dendrocolaptes certhia (cp,tf,ig) Xiphorhynchus ocellatus (cp,c,tf) Furnariidae Xenops minutus (cp,tf,ig) Automolus infuscatus (cp,tf) Thamnophilidae Thamnophilus murinus (cp,tf) Thamnophilus amazonicus (cp,ig,dv) Thamnomanes caesius (cp,tf,ig) Herpsilochmus dorsimaculatus (cp,tf,ig) Myrmotherula brachyura (cp,tf,ig) Myrmotherula cherriei (cp,c,ig) Myrmotherula axillaris (cp,c,tf,ig,dv) Formicivora grisea (c,s) Myrmoborus myotherinus (cp,tf,dv) Hylophylax naevia (cp,tf) Hylophylax poecilinota (cp,tf,ig) Myrmeciza disjuncta (c,ig) Pithys albifrons (cp,tf) Gymnopithys leucaspis (cp,tf,ig) Rhegmatorhina cristata (cp,tf) Phlegopsis erythroptera (cp,tf) Formicariidae Formicarius colma (cp,tf,ig) Tyrannidae Elaenia ruficeps (c) Myiopagis gaimardii (cp,tf,ig,dv) Tyrannulus elatus (cp,tf,ig,dv) Zimmerius gracilipes (cp,tf,ig,dv) Mionectes oleagineus (cp,c,tf,ig) continued © 2004 British Ornithologists’ Union, Ibis, 146, 114–124 124 S. H. Borges Appendix 1. Continued Hemitriccus zosterops (cp,tf) Hemitriccus minimus (cp,c,ig) Corythopis torquata (cp,tf,ig) Ramphotrigon ruficauda (cp,tf,ig) Terenotriccus erythrurus (cp,tf) Cnemotriccus fuscatus (cp,c,ig) Attila citriniventris (cp) Rhytipterna simplex (cp,tf,ig) Rhytipterna immunda (c) Myiarchus ferox (c,ig,dv) Myiarchus tuberculifer (c,ig,dv) Conopias parva (cp,tf) Legatus leucophaius (cp,tf,ig,dv) Tyrannus melancholicus (c,ig,tf,s) Pipridae Schiffornis turdinus (cp,tf,dv) Tyranneutes stolzmanni (cp,tf) Neopelma chrysocephalum (cp,tf,ig) Neopipo cinnamomea (c) Xenopipo atronitens (cp,c,ig) Pipra coronata (c,tf,ig,dv) Pipra pipra (cp,c,tf,ig,dv) Pipra erythrocephala (cp,c,tf,dv) Cotingidae Xipholena punicea (cp,tf,ig) Lipaugus vociferans (cp,tf,ig) APPENDIX 2. Bird species that are indicators of campinas and campinaranas in Amazonia following Oren (1981), Stotz et al. (1996), Whitney and Alvarez (1998), Alvarez and Whitney (2001), Isler et al. (2001) and this study. The habitat association categories were based on Borges et al. (2001), Borges and Carvalhaes (2000), Stotz (1997), Silva et al. (1997), Bates et al. (1998), Cohn-Haft et al. (1997), Zimmer and Hilty (1997), Prum et al. (1996), Tostain et al. (1992) and Hilty and Brown (1986). Category a (n = 6 species): species probably restricted to campinas and campinaranas. Crypturellus cf. erythropus, Crypturellus duidae, Percnostola arenarum, Herpsilochmus gentryi, Zimmerius villarejoi, Neopipo cinnamomea. Hirundinidae Progne chalybea (c,ig) Hirundo rustica (c,ig) Troglodytidae Thryothorus coraya (cp,c,tf,dv) Troglodytes aedon (c,ig,dv,s) Sylviidae Microbates collaris (cp,tf) Vireonidae Vireo olivaceus (cp,ig,dv) Hylophilus brunneiceps (cp,ig) Hylophilus hypoxanthus (cp,tf) Thraupidae Schistochlamys melanopis (c,s) Tachyphonus phoenicius (c) Dacnis cayana (cp,tf,ig,dv) Coerebidae Coereba flaveola (c,ig,dv,s) Icteridae Sturnella militaris (c,s) Icterus chrysocephalus (c,tf,ig) Cacicus cela (c,ig) Cardinalinae Caryothraustes canadensis (cp,tf) Emberezinae Oryzoborus angolensis (c,ig,dv) Dolospingus fringilloides (c,ig) Emberizoides herbicola (c,s) Heterocercus flavivertex, Hylophilus brunneiceps, Dolospingus fringilloides. Category c (n = 11 species): species recorded in campinas and Amazonian savannas. Hylocharis cyanus, Polytmus theresiae, Thamnophilus punctatus, Formicivora grisea, Formicivora rufa, Elaenia cristata, Elaenia ruficeps, Rhytipterna immunda, Schistochlamys melanopis, Tachyphonus phoenicius, Zonotrichia capensis. Category d (n = 5 species): species recorded in campinas and campinaranas but also associated with a variety of habitats, including terra firme forest and disturbed vegetation. Cyanocorax cayanus, Caprimulgus nigrescens, Hemitriccus zosterops, Neopelma chrysocephalum, Turdus ignobilis. Category b (n = 10 species): species characteristic of campinas and campinaranas, but also found in black-water inundated forests (igapó forests). Category e (n = 5 species): species found in campinas and campinaranas, but with uncertain association with other habitats. Aratinga pertinax, Galbula leucogastra, Xiphorhynchus obsoletus, Myrmotherula cherriei, Myrmeciza disjuncta, Hemitriccus minimus, Xenopipo atronitens, Cyanocorax heilprini, Picumnus pygmaeus, Hemitriccus striaticollis, Neopelma pallescens, Heterocercus aurantiivertex. © 2004 British Ornithologists’ Union, Ibis, 146, 114–124