Searching for bioindicators of forest fragmentation: passerine birds in the Atlantic forest of southeastern Brazil/Busca por bioindicadores de fragmentacao florestal: aves Passeriformes na Floresta Atlantica do Sudeste do Brasil.
Ecological indicators have been used to detect changes in nature for the last 40 years, and currently, they are mainly used to assess the condition of the environment (Niemi and McDonald, 2004), and one of the aspects that have been evaluated by ecological indicators is the landscape fragmentation (O'Neill et al., 1988).
Fragmentation is a serious threat for the Brazilian Atlantic forest, and today it is estimated only 7% remains (Mittermeier et al., 1999), mostly in small fragments. The Atlantic Forest harbors 688 breeding species of birds (Goerck, 1997), only one bird species is truly registered as extinct in this ecosystem, but many species are now endangered (Collar et al., 1992). In the state of Rio de Janeiro, the most important remnants of this ecosystem are in the mountains, and mainly restricted to fragments. This state hosts 653 taxa of birds, including 82 threatened, 38 probably threatened and 25 without enough data for evaluation of their status (Alves et al., 2000).
One of the primary goals of research on bioindicators is to identify species or other taxonomic units that would indicate disturbances in the environment, reflecting the responses of other species (Rainio and Niemela, 2003). When searching for bioindicators, one has to find groups of species which respond quickly to environmental changes, being these answers clearly distinct from those generated by natural fluctuations (Furness and Greenwood, 1993). Birds have been used as bioindicators for having particular characteristics, as good taxonomic and systematic knowledge (Furness and Greenwood, 1993; Bierregaard and Stouffer, 1997), several species occupying higher levels on food chain (Bierregaard, 1990) and sensibility to habitat losses and fragmentation (Terborgh, 1977; Turner, 1996).
In fragmented landscapes, a regular process is the substitution of rare-specialized species for abundant-generalist ones, more adapted to open and clear-cut areas (Willis, 1979; Restrepo and Gomez, 1998; Willis and Oniki, 2002a); thus we can associate the presence/ absence of some species to environmental quality. In general, Suboscines Passerine birds are more closely-related to forested landscapes, and Oscines usually are more linked to open areas (Willis, 1979; Sick, 1997). If those assumptions are natural processes, some species usually would be more easily found in continuous forests; meanwhile other groups will appear mainly in open and fragmented areas. Therefore, this non-random distribution would be a clue for evaluating environmental quality.
Our goal in this study is to verify non-random distribution of some Passerine bird species in areas with different levels of disturbance at the Serra do Mar sub region of Atlantic Forest. Thus we intend to detect which species are more closed-related to each site (indicator species), investigating their potential as bioindicators of forest fragmentation.
2. Material and Methods
In order to estimate the potential of some Passerine birds as bioindicators of forest fragmentation in the Atlantic forest, we have conducted this research in the mountains of Rio de Janeiro state, southeastern Brazil, from October 2001 to July 2005. We used mist nets for sampling Passerine birds in six sites, including four small fragments (4, 9, 23 and 64 ha) in agricultural areas in Teresopolis municipality (22[degrees] 17' 22" S and 42[degrees] 52' 3 " W and 22[degrees] 16' 35" S and 42[degrees] 51' 49" W), a second-growth forest (Igapira Farm440 ha) in the vicinity of Miguel Pereira (22[degrees] 30' S and 42[degrees] 23' W) and a continuous forest (10,600 ha) in Teresopolis municipality (Serra dos Orgaos National Park; 22[degrees] 24' 36" S and 42[degrees] 58' 48" W; from now SONP).
The vegetation in the four smaller fragments, from now named F1 to F4 (from smaller to larger), is second-growth forest. They are surrounded by pastureland for raising cattle (which usually is seen inside the fragments), and agricultural activities (in which pesticides are used). Excepted for F1 (where only one net line was operated), we performed a two-net lines protocol with from 6 to 10 mist nets in each fragment. In every fragment, one net line was close to the border and the other was located inside the forest. Every fragment and net line was sampled at least every two months, with the same sample effort in all studied sites.
Igapira Farm is a 910 hectares private farm in the municipality of Miguel Pereira. It is estimated that 440 hectares are covered by second-growth montane pluvial forest, and the remnant are buildings and large area of pasturelands for cattle and buffalo. The dominant native covering is montane semideciduous Atlantic Forest (Rizzini, 1997), with trees between 20 and 30 m, and emergent reaching up to 40 m. For sampling birds, eight to ten mist nets were operated every month in two sites (800 and 1,100 m high)
The vegetation in SONP is second-growth Atlantic pluvial forest, with palm trees, epiphytes and tall trees. It has 10 peaks higher than 2000 m and six other peaks over 1500 m high. The highest peak is Pedra do Sino at 2263 m, and the lowest is located in the relatively flat municipality of Mage, at 145 m. The average temperature at 1000 m is 17 [degrees]C (Wikipedia, 2006). We sampled two sites, located at 1000 m high and about 2 km far from each other. From 6 to 10 mist nets were used in each site, which was sampled every two months.
Due to different mist netting efforts (net-hours) in the six sampled areas (850 in each fragment, 2680 in Igapira Farm and 1800 in SONP), before using our data we divided captures by net-hours x 100; thereby we were able to compare our results of relative proportion of captures in these sites. Mist nets are probably free of biases associated with the observer (Bierregaard and Stouffer, 1997); however introduction biases themselves in that birds of different sizes and with differing behavior patterns, whose capture probabilities are distinct (Remsen and Good, 1996). Nevertheless, their use has provided satisfactory results in many studies (e.g., Bierregaard and Stouffer, 1997; Blake and Loiselle, 2001; Wang and Finch, 2002; Piratelli and Blake, 2006), and this methodology can be an useful tool for comparing bird communities of several sites when used in a similar sampling effort.
The Indicator Species analysis (Dufrene and Legendre, 1997) and a Monte Carlo test were run using the package PCOrd 4.01 (McCune and Mefford, 1997) to verify non-random species distribution in the sampled sites. We only considered species with 10 or more captures, a minimum of 30% of perfect indication and a significant value for the statistical test. We then assumed that those species more closely related to a given sampled site would be more specialized and probably more sensitive to the degradation of their habitats. Next, we searched in the literature for their biological characteristics, based on descriptions of their occurrence. Finally, we matched our results with previous descriptions in order to find the best bioindicators, and to test the use of Indicator Species analysis for detecting bioindicators.
A total of 71 Passerine bird species from 11 families were sampled, and 30 had at least 10 captures, from which twenty (66.7%) were Suboscine, and 10 (33.4%) Oscine Passerines. The most well-represented families were Emberizidae (n = 15) and Tyrannidae and Furnariidae (n = 13), and the most common trophic guilds were understory insectivores (n = 27) and omnivores (n = 12) (Table 1).
Due to their association to the largest area (SONP), we have linked Sclerurus scansor (Menetries, 1835), Mionectes rufiventris (Cabanis, 1846), Chiroxiphia caudata (Shaw & Nodder, 1793) and Habia rubica (Vieillot, 1817) to that site. Five species were further captured not by chance in the 440 ha secondgrowth (Igapira farm), suggesting some preference to that forest: Conopophaga melanops (Vieillot, 1818), Myiobius barbatus (Gmelin, 1789), Myrmeciza loricata (Lichtenstein, 1823), Philydor atricapillus (Wied, 1821) and Schiffornis virescens (Lafresnaye, 1838). No species were related to any small fragment (Table 2). All of these species excepted H. rubica and M. barbatus are endemic of Atlantic Forest (Brooks et al., 1999) and only Habia rubica is Oscine (Emberizidae, Thraupinae). Most ( seven) of these nine species were understory insectivores; two (Myiobius barbatus and Schiffornis virescens) were classified as understory omnivores (see Table 1).
In this analysis some species, even with an expressive higher relative abundance in a given sampled site were not considered as indicator, due to their low frequencies of captures. This is the case of Euphonia pectoralis (Latham, 1801) and Saltator similis d'Orbigny & Lafresnaye, 1837 for SONP (Table 3).
According to Indicator Species analysis, Sclerurus scansor, Mionectes rufiventris, Chiroxiphia caudata and Habia rubica were indicators for the largest area (SONP); and Conopophaga melanops, Myiobius barbatus, Myrmeciza loricata, Philydor atricapillus, and Schiffornis virescens for the medium-size site (410 ha, Igapira).
Sclerurus scansor usually is found on or near ground in humid lowland and montane forests (Brooks et al., 1999), nesting in holes in banks inside the forest (Develey and Endrigo, 2004). It has been considered a rare, specialized (Goerck, 1997) and highly sensitive species (Ribon et al., 2003), commonly as a member of fixed flocks (Develey and Peres, 2000). There are records of S. scansor in a 230 ha patch of semideciduous forest in cane fields of central Sao Paulo (Willis and Oniki, 2002b). These last authors did not find this species in further samplings, suggesting its disappearance due to loss of the few individuals present earlier. Even though it has already been observed in very small fragments by D'Angelo-Neto et al. (1998) in Minas Gerais (5 to 8 ha) and in Rio Grande do Sul, foraging on the ground (I. Accordi, p. comm.), its abundance estimate was affected by logging in Sao Paulo, occurring mainly in a primary forest (Aleixo, 1999).
Mionectes rufiventris is a common species in lower growth of humid forest, secondary woodland and borders of southeastern Brazil (Ridgely and Tudor, 1994a) occurring in mixed flocks (Develey and Peres, 2000) both in lowland (Machado and Fonseca, 2000) and montane evergreen forests (Brooks et al., 1999). Aguilar et al. (2000) found 19 nests of this species in two of the three fragments (50, 200 and 300 ha) that they studied in Minas Gerais; however, they did not specify in which fragment the nests were found. All nests were constructed over water, fixed to tree roots under stream beds; the authors considered this species as nest-site specialist. Pizo and Aleixo (1998) has described its leck behavior in a 2000 ha protected area in Sao Paulo. There are records for this species in antropized areas in Minas Gerais (Manhaes and Ribeiro, 2005) as well as in larger patches in Rio Grande do Sul (I. Accordi, p. comm.).
Chiroxiphia caudata is a common species in lower and middle growth of humid forest, secondary woodland, and borders (Brooks et al., 1999; Ridgely and Tudor, 1994a). It has been reported in a large fragment (21,840 ha) (Donatelli et al., 2004), and in smaller ones in Sao Paulo (Willis and Oniki, 2002b; Poza and Pires, 2003) and Minas Gerais (D'Angelo-Neto et al., 1998; Ribon et al., 2004). In this last state, there are reports up to 500 m high in the Rio Doce Valley (Machado and Fonseca, 2000), and from 800 to 1,000 m high in Serra do Cipo ( Mello-Junior et al., 2001). It was not affected by logging in Sao Paulo, occurring both in a primary forest and in a logged area (Aleixo, 1999).
Habia rubica lives in lower growth of humid forest and forest borders, usually in mixed flocks (Ridgely and Tudor, 1994b). It is a low specialized species (Develey and Peres, 2000) having medium sensitivity (Ribon et al., 2003). There are records of this species in a 21,840 ha forest (Donatelli et al., 2004), and in smaller fragments (Willis and Oniki, 2002b) in Sao Paulo. It is currently seen as a nuclear species of mixed flocks in Rio Grande do Sul (I. Accordi, p. com.).
Those four species, regardless of their records in small fragments, have some ecological characteristics (e.g. rarity status, needs for nesting, foraging in mixed flocks, sometimes as nuclear species) which would limit their occurrence and/or their nesting activities, leading them to prefer less altered areas. Thus, their indication for the largest area (SONP) in our analysis has matched their ecological specialization.
Conopophaga melanops is a usual member of mixed flocks (Develey and Peres, 2000) in lowland forests (Brooks et al., 1999). Machado and Fonseca (2000) captured this species up to 500 m high in the Rio Doce Valley, Minas Gerais. It also was not affected by logging in Sao Paulo, occurring in the same areas described before for C. caudata (Aleixo, 1999).
Myiobius barbatus is an uncommon to fairly common species in lower growth of humid forest and mature secondary woodlands (Ridgely and Tudor, 1994a). Machado and Fonseca (2002) sampled this species in the highest area of Rio Doce Valle. Its estimate of abundance was affected by logging in Sao Paulo, occurring mainly in a primary forest (Aleixo, 1999).
Myrmeciza loricata is a lowland and montane forest species (Brooks et al., 1999), living, for example, in the lower area of the Rio Doce Valle. (Machado and Fonseca, 2000) and having medium sensitivity (Ribon et al., 2003).
Philydor atricapillus is an inconspicuous bird in lower growth of humid forest and mature secondary woodland (Ridgely and Tudor, 1994a). It is a medium-sensibility species (Ribon et al., 2003) typical of mixed-flocks (Develey and Peres, 2000). These last authors have reported young individuals in an 80,000 ha protected area in Sao Paulo; in this state it also was not affected by logging (Aleixo, 1999). It is critically endangered in Rio Grande do Sul, occurring only in a few fragments of lowland forests in Northeastern, following Habia rubica (I. Accordy, p. com.).
Schiffornis virescens is common in montane secondary forest (Brooks et al., 1999) and in mature secondary woodlands (Ridgely and Tudor, 1994a). It was recorded in Sao Paulo (Willis and Oniki, 2002b; Donatelli et al., 2004) in areas ranging in size from 230 to over 21,000 ha). Aleixo (1999) detected the influence of logging in this species in that state.
The last five species also have some characteristics (e.g. foraging in mixed flocks, medium sensibility, reports for very large areas, been affected by logging) that would restrict their occurrence to medium to large area and/or mature secondary woodlots. Again Indicator Species analysis has detected some sensitive species.
Because indicator species analysis combines both species relative abundance and frequency of occurrence (Dufrene and Legendre, 1997), it can indicate which species are more closely associated to specifics habitats not by chance. Ecological indicators should trade off two potential endpoints; they should be sensitive enough to react in a detectable way when a system is affected by anthropogenic stress and they should also remain reasonably predictable in unperturbed ecosystems (Niemy and McDonald, 2004).
In accordance with Stotz et al. (1996), who have suggested that for guiding principles for bird conservation in the Neotropics, one might focus on assemblages of endemics and habitat specialists rather than on sheer number of species, we do suggest using Indicator Species analysis as a clue for detecting groups of Passerine bird species that would be bioindicators. This could be a valuable tool for a quick and primarily evaluation of the environmental quality (mainly focusing on habitat fragmentation) and for bird conservation as well.
Acknowledgements--We thank Sandro Von Matter and Rafael Kiffer for help with data collecting; CNPq for scholarships, BMBF and Fazenda Igapira for field support, IBAMA, Cristina Santos, and farmers from Teresopolis for permission to conduct this research. For valuable comments, we thank Iury Accordi.
Received April 28, 2006--Accepted October 25, 2006--Distributed May 31, 2008
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Piratelli, A. (a*), Sousa, SD. (b), Correa, JS. (b), Andrade, VA. (b), Ribeiro, RY. (b), Avelar, LH. (b) and Oliveira, EF. (b)
(a) Campus Sorocaba, Universidade Federal de Sao Carlos--UFSCar, Rodovia Joao Leme dos Santos, Km 110, Itinga, CEP 18052-780, Sorocaba, SP, Brasil
(b) Programa de Pos-Graduacao em Biologia Animal, Departamento de Biologia Animal, Instituto de Biologia, Universidade Federal Rural do Rio de Janeiro, BR 465, Km 07, CEP 23890-000, Seropedica, RJ, Brazil
* e-mail: email@example.com
Table 1. All Passerine birds (by Families) sampled in six sites at Atlantic Forest in the state of Rio de Janeiro, Brazil, their capture rates--(captures/net-hour) x 100 and trophic guilds (according to Willis. Families Species F1 F2 THAMNOPHILIDAE Mackenziana severa - - Thamnophilus caerulescens 0.24 0.35 Thamnophilus punctatus - - Dysithamnus mentalis - - Dysithamnus stictothorax - - Dysithamnus xanthopterus - - Myrmotherula gularis - - Drymophila ochropyga - - Pyriglena leucoptera 0.47 0.71 Myrmeciza loricata - - FORMICARIIDAE Chamaeza campanisona - - Grallaria varia - - CONOPOPHAGIDAE Conopophaga lineata 0.24 0.59 Conopophaga melanops - - FURNARIIDAE/ SYNALLAXINAE Synallaxis ruficapilla 0.35 - FURNARIIDAE/ Anabazenops fuscus 0.12 - PHILYDORINAE Philydor atricapillus - - Syndactyla rufosuperciliata - 0.35 Anabacerthia amaurotis - - Automolus leucophthalmus - - Philydor lichtensteini - - Philydor rufus - 0.12 Heliobletus contaminatus - - Xenops minutus - - Xenops rutilans - - Sclerurus scansor - - Lochmias nematura - 0.12 DENDROCOLAPTIDAE Dendrocincla fuliginosa - - Sittasomus griseicapillus - 0.24 Xiphocolaptes albicollis - - Lepidocolaptes fuscus 0.24 0.47 Campylorhamphus falcularius - 0.12 TYRANNIDAE/ Mionectes rufiventris - - ELAENIINAE Leptopogon amaurocephalus - - Phylloscartes difficilis - - Phylloscartes ventralis - - Hemitriccus diops - - Todirostrum plumbeiceps - 0.12 Rhynchocyclus olivaceus - - Tolmomyias sulphurescens - 0.24 Platyrinchus mystaceus - 0.12 TYRANNIDAE/ Myiobius barbatus - - FLUVICOLINAE Lathrotriccus euleri 0.24 0.35 TYRANNIDAE/ Attila rufus - - TYRANNINAE Myiarchus swainsoni 0.12 - PIPRIDAE Chiroxiphia caudata - 0.59 Ilicura militaris - - Schiffornis virescens - - COTINGIDAE Carpornis cucullatus - - MUSCICAPIDAE/ Platycichla flavipes - - TURDINAE Turdus leucomelas 0.12 0.71 Turdus rufiventris 0.94 1.53 Turdus amaurochalinus - 0.35 Turdus albicollis - - VIREONIDAE Cyclarhis gujanensis - - Hylophilus poicilotis - - EMBERIZIDAE/ Basileuterus culicivorus 0.24 0.12 PARULINAE Basileuterus leucoblepharus - - EMBERIZIDAE/ COEREBINAE Coereba flaveola - - EMBERIZIDAE/ Tachyphonus cristatus - - THRAUPINAE Tachyphonus coronatus 0.59 0.94 Tachyphonus rufus - - Trichothraupis melanops 0.59 0.47 Habia rubica - - Thraupis sayaca - - Euphonia pectoralis - - Tangara desmaresti - - EMBERIZIDAE/ Haplospiza unicolor - - EMBERIZINAE Arremon taciturnus 0.35 0.47 EMBERIZIDAE/ Pitylus fuliginosus - - CARDINALINAE Saltator similis - - Families F3 F4 Igapira THAMNOPHILIDAE 0.12 0.12 - 0.24 0.24 - - - 0.04 - 0.12 0.26 - - 0.15 - - 0.07 - - 0.30 - - 0.04 1.65 1.29 1.01 - - 0.45 FORMICARIIDAE - - 0.11 - - - CONOPOPHAGIDAE 0.82 0.71 0.56 - - 0.26 FURNARIIDAE/ SYNALLAXINAE 0.35 0.24 0.11 FURNARIIDAE/ 0.24 0.12 0.22 PHILYDORINAE - - 0.34 - 0.12 0.41 - 0.24 - - - 0.22 - - 0.04 - - 0.04 - - - - - 0.15 - 0.12 - - - 0.56 - - - DENDROCOLAPTIDAE - - 0.04 0.12 - 0.37 - - 0.15 0.24 0.94 0.52 0.12 - 0.07 TYRANNIDAE/ 0.12 0.12 0.56 ELAENIINAE 0.12 0.12 0.26 - - 0.37 - - 0.04 0.47 - - - - - - - 0.04 0.12 - - 0.12 0.47 0.52 TYRANNIDAE/ - - 0.30 FLUVICOLINAE - 0.35 0.04 TYRANNIDAE/ - - 0.11 TYRANNINAE - - - PIPRIDAE 0.59 0.71 1.27 - - 0.07 - - 0.22 COTINGIDAE - - - MUSCICAPIDAE/ - - - TURDINAE 0.12 0.35 - 1.76 0.59 - 0.35 - 0.04 0.47 0.35 0.49 VIREONIDAE 0.24 0.12 - 0.12 - 0.07 EMBERIZIDAE/ 0.24 0.35 0.26 PARULINAE - - - EMBERIZIDAE/ COEREBINAE - - 0.04 EMBERIZIDAE/ - - 0.04 THRAUPINAE 0.35 0.47 0.19 - - 0.04 0.82 0.59 0.60 - - -0.11 0.12 - - - - -0.34 0.12 - - EMBERIZIDAE/ - - -0.11 EMBERIZINAE 0.12 - -0.04 EMBERIZIDAE/ - - -0.04 CARDINALINAE - - -0.37 Families SONP Trophic guilds THAMNOPHILIDAE - Bamboo or forest tangles insectivores - Understory insectivores - Understory insectivores 0.17 Understory insectivores - Understory insectivores - Understory insectivores 0.11 Understory insectivores - Bamboo or forest tangles insectivores 0.11 understory insectivores - Understory insectivores FORMICARIIDAE - Understory insectivores 0.06 Ground insectivore CONOPOPHAGIDAE 0.11 Understory insectivores - Understory insectivores FURNARIIDAE/ SYNALLAXINAE - Understory insectivores FURNARIIDAE/ - Understory insectivores PHILYDORINAE - Understory insectivores 0.06 Understory insectivores 0.33 Understory insectivores - Understory insectivores - Understory insectivores 0.11 Understory insectivores 0.17 Understory insectivores - trunk and twig insectivores - Trunk and twig insectivores 0.33 Understory insectivores 0.17 Understory insectivores DENDROCOLAPTIDAE - Trunk and twig insectivores 0.11 Trunk and twig insectivores - Understory insectivores 0.39 Trunk and twig insectivores - Trunk and twig insectivores TYRANNIDAE/ 0.61 Understory insectivores ELAENIINAE - Understory insectivores - Canopy insectovores - Canopy insectovores - Bamboo or forest tangles insectivores - Bamboo or forest tangles insectivores - Understory insectivores - Understory omnivores 0.06 Understory omnivores TYRANNIDAE/ - Understory omnivores FLUVICOLINAE - Understory omnivores TYRANNIDAE/ 0.11 Understory omnivores TYRANNINAE - Treetop insectivores PIPRIDAE 0.89 Understory omnivores - Understory omnivores - Understory omnivores COTINGIDAE 0.06 Canopy frugivores MUSCICAPIDAE/ 0.28 Edge omnivores TURDINAE - Edge omnivores 0.28 Edge omnivores 0.06 Edge omnivores 0.56 Understory omnivores VIREONIDAE - Treetop insectivores - Edge insectivores EMBERIZIDAE/ - Understory insectivores PARULINAE 0.11 Understory insectivores EMBERIZIDAE/ COEREBINAE - Nectar and insect eaters EMBERIZIDAE/ - Edge omnivores THRAUPINAE 0.06 Edge omnivores - Edge omnivores 0.39 Understory omnivores 0.28 Understory omnivores - Understory omnivores - Edge omnivores - Edge frugivores EMBERIZIDAE/ 0.06 Edge seedaters EMBERIZINAE - Edge seedaters EMBERIZIDAE/ - Edge seedaters CARDINALINAE - Edge omnivores F1 = fragment 1 (4 ha); F2 = fragment 2 (9 ha); F3 = fragment 3 (23 ha); F4 = fragment 4 (64 ha); Igapira = Igapira Farm (440 ha); and SONP = Serra dos Orgaos National Park (10,600 ha). Table 2. Indicator values (% of perfect red in this analysis. Species F1 F2 F3 F4 Dysithamnus mentalis - - - 3 Myrmotherula gularis - - - - Pyriglena leucoptera 4 4 26 13 Myrmeciza loricata - - - - Conopophaga lineata 2 5 13 12 Conopophaga melanops - - - - Synallaxis ruficapilla 15 - 8 4 Anabazenops fuscus 3 - 5 2 Philydor atricapillus - - - - Syndactyla rufosuperciliata - 8 - 1 Sclerurus scansor - - - - Sittasomus griseicapillus - 2 2 3 Lepidocolaptes fuscus 2 4 2 13 Mionectes rufiventris - - 1 1 Phylloscartes difficilis - - - - Platyrinchus mystaceus - 1 1 7 Myiobius barbatus - - - - Lathrotriccus euleri 7 7 1 10 Chiroxiphia caudata - 3 6 7 Schiffornis virescens - - - - Turdus leucomelas 2 16 4 5 Turdus rufiventris 10 12 16 2 Turdus albicollis - - 7 4 Basileuterus culicivorus 6 3 2 9 Tachyphonus coronatus 14 12 7 4 Trichothraupis melanops 8 3 13 7 Habia rubica - - - - Euphonia pectoralis - - - - Arremon taciturnus 17 13 1 - Saltator similis - - - - Species Igapira SONP F Dysithamnus mentalis 9 11 0.346 Myrmotherula gularis 23 8 0.035 Pyriglena leucoptera 7 - 0.125 Myrmeciza loricata 42 - 0.002 * Conopophaga lineata 7 1 0.648 Conopophaga melanops 31 - 0.008 * Synallaxis ruficapilla 1 - 0.226 Anabazenops fuscus 2 - 0.894 Philydor atricapillus 35 - 0.004 * Syndactyla rufosuperciliata 26 1 0.026 Sclerurus scansor 18 46 0.001 * Sittasomus griseicapillus 11 - 0.501 Lepidocolaptes fuscus 7 12 0.760 Mionectes rufiventris 11 33 0.014 * Phylloscartes difficilis 27 - 0.011 Platyrinchus mystaceus 28 1 0.002 Myiobius barbatus 38 - 0.002 * Lathrotriccus euleri - - 0.402 Chiroxiphia caudata 10 39 0.004 * Schiffornis virescens 38 - 0.003 * Turdus leucomelas - - 0.132 Turdus rufiventris - 3 0.300 Turdus albicollis 7 26 0.056 Basileuterus culicivorus 2 - 0.692 Tachyphonus coronatus 1 - 0.441 Trichothraupis melanops 2 9 0.548 Habia rubica 1 34 0.002 * Euphonia pectoralis 15 - 0.149 Arremon taciturnus - - 0.107 Saltator similis 15 - 0.149 F1 = fragment 1 (4 ha); F2 = fragment 2 (9 ha); F3 = fragment 3 (23 ha); F4 = fragment 4 (64 ha); Igapira = Igapira Farm (440 ha); and SONP = Serra dos Orgaos National Park (10,600 ha). Table 3. Relative abundance, frequency of captures (in parenthesis) and percentile of perfect indication (when statistically significant) of birds with tenor more captures in six sites at Atlantic Forest in the state of Rio de Janeiro, Brazil. Species F1 F2 Dysithamnus mentalis 0 (0) 0 (0) Myrmotherula gularis 0 (0) 0 (0) Pyriglena leucoptera 9 (38) 9 (33) Myrmeciza loricata 0 (0) 0 (0) Conopophaga lineata 7 (25) 14 (25) Conopophaga melanops 0 (0) 0 (0) Synallaxis ruficapilla 34 (38) 0 (0) Anabazenops fuscus 17 (13) 0 (0) Philydor atricapillus 0 (0) 0 (0) Syndactyla rufosuperciliata 0 (0) 16 (25) Sclerurus scansor 0 (0) 0 (0) Sittasomus griseicapillus 16 (0) 53 (8) Lepidocolaptes fuscus 6 (25) 9 (33) Mionectes rufiventris 0 (0) 0 (0) Phylloscartes difficilis 0 (0) 0 (0) Platyrinchus mystaceus 0 (0) 4 (8) Myiobius barbatus 0 (0) 0 (0) Lathrotriccus euleri 26 (25) 26 (25) Chiroxiphia caudata 0 (0) 6 (25) Schiffornis virescens 0 (0) 0 (0) Turdus leucomelas 20 (13) 39 (42) Turdus rufiventris 19 (50) 22 (50) Turdus albicollis 0 (0) 0 (0) Basileuterus culicivorus 20 (25) 13 (17) Tachyphonus coronatus 25 (50) 27 (42) Trichothraupis melanops 16 (38) 8 (25) Habia rubica 0 (0) 0 (0) Euphonia pectoralis 0 (0) 0 (0) Arremon taciturnus 42 (38) 37 (33) Saltator similis 0 (0) 0 (0) Species F3 F4 Dysithamnus mentalis 0 (0) 12 (10) Myrmotherula gularis 0 (0) 0 (0) Pyriglena leucoptera 31 (67) 21 (50) Myrmeciza loricata 0 (0) 0 (0) Conopophaga lineata 22 (44) 17 (50) Conopophaga melanops 0 (0) 0 (0) Synallaxis ruficapilla 30 (22) 18 (20) Anabazenops fuscus 31 (11) 14 (10) Philydor atricapillus 0 (0) 0 (0) Syndactyla rufosuperciliata 0 (0) 6 (10) Sclerurus scansor 0 (0) 0 (0) Sittasomus griseicapillus 11 (11) 20 (10) Lepidocolaptes fuscus 6 (22) 21 (40) Mionectes rufiventris 4 (11) 3 (10) Phylloscartes difficilis 0 (0) 0 (0) Platyrinchus mystaceus 5 (11) 20 (20) Myiobius barbatus 0 (0) 0 (0) Lathrotriccus euleri 12 (11) 32 (30) Chiroxiphia caudata 10 (33) 9 (40) Schiffornis virescens 0 (0) 0 (0) Turdus leucomelas 17 (22) 24 (20) Turdus rufiventris 33 (44) 9 (20) Turdus albicollis 12 (33) 8 (30) Basileuterus culicivorus 18 (11) 24 (30) Tachyphonus coronatus 18 (33) 16 (20) Trichothraupis melanops 22 (44) 13 (40) Habia rubica 0 (0) 0 (0) Euphonia pectoralis 0 (0) 0 (0) Arremon taciturnus 12 (11) 9 (0) Saltator similis 0 (0) 0 (0) Species Igapira SONP Dysithamnus mentalis 42 31 46 25 Myrmotherula gularis 75 35 25 25 Pyriglena leucoptera 25 77 5 13 Myrmeciza loricata 100 42 0 0 Conopophaga lineata 32 50 7 13 Conopophaga melanops 100 31 0 0 Synallaxis ruficapilla 17 19 0 0 Anabazenops fuscus 38 15 0 0 Philydor atricapillus 100 35 0 0 Syndactyla rufosuperciliata 69 58 8 13 Sclerurus scansor 48 46 52 75 Sittasomus griseicapillus 5 42 0 0 Lepidocolaptes fuscus 27 50 32 50 Mionectes rufiventris 28 58 65 50 Phylloscartes difficilis 100 27 0 0 Platyrinchus mystaceus 65 73 6 13 Myiobius barbatus 100 38 0 0 Lathrotriccus euleri 4 4 0 0 Chiroxiphia caudata 27 65 46 100 Schiffornis virescens 100 38 0 0 Turdus leucomelas 0 0 0 0 Turdus rufiventris 0 0 16 38 Turdus albicollis 21 54 59 50 Basileuterus culicivorus 25 19 0 0 Tachyphonus coronatus 9 19 5 13 Tiichothraupis melanops 18 27 22 63 Habia rubica 0 12 87 38 Euphonia pectoralis 100 15 0 0 Arremon taciturnus 9 4 0 0 Saltator similis 100 15 0 0 Species (%) of perfect F indication Dysithamnus mentalis - 0.346 Myrmotherula gularis - 0.035 Pyriglena leucoptera - 0.125 Myrmeciza loricata 42 (Igapira) 0.002 * Conopophaga lineata - 0.648 Conopophaga melanops 31(Igapira) 0.008 * Synallaxis ruficapilla - 0.226 Anabazenops fuscus - 0.894 Philydor atricapillus 35 (Igapira) 0.004 * Syndactyla rufosuperciliata - 0.026 Sclerurus scansor 46 (SONP) 0.001 * Sittasomus griseicapillus - 0.501 Lepidocolaptes fuscus - 0.76 Mionectes rufiventris 33 (SONP) 0.014 * Phylloscartes difficilis - 0.011 Platyrinchus mystaceus - 0.002 Myiobius barbatus 38 (Igapira) 0.002 * Lathrotriccus euleri - 0.402 Chiroxiphia caudata 39 (SONP) 0.004 * Schiffornis virescens 38 (Igapira) 0.003 * Turdus leucomelas - 0.132 Turdus rufiventris - 0.300 Turdus albicollis - 0.056 Basileuterus culicivorus - 0.692 Tachyphonus coronatus - 0.441 Trichothraupis melanops - 0.548 Habia rubica 34 (SONP) 0.002 * Euphonia pectoralis - 0.149 Arremon taciturnus - 0.107 Saltator similis - 0.149 F1 = fragment 1 (4 ha); F2 = fragment 2 (9 ha); F3 = fragment 3 (23 ha); F4 = fragment 4 (64 ha); Igapira = Igapira Farm (440 ha); and SONP = Serra dos Orgaos National Park (10,600 ha).