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Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil

Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary... Revista Brasileira de Ornitologia, 24(4), 303–313 ARTICLE December 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil 1,2,4 3 Rômulo Ribon and Miguel Â. Marini Programa de Pós-graduação em Ecologia, Conservação e Manejo de Vida Silvestre, Departamento de Biologia Geral, ICB, Universidade Federal de Minas Gerais, CEP 30161-970, Belo Horizonte, MG, Brazil. Museu de Zoologia João Moojen, Departamento de Biologia Animal, Universidade Federal de Viçosa, CEP 36570-000, Viçosa, MG, Brazil. Departamento de Zoologia, IB, Universidade de Brasília, CEP 70910-900, Brasília, DF, Brazil. Corresponding author: romulo.ribon@ufv.br Received on 18 August 2016. Accepted on 27 December 2016. ABSTRACT: Demographic parameters of birds are essential to understand their ecology and delineate conservation and management plans. This becomes especially important in highly altered biomes such as the Brazilian Atlantic Forest, since the few remaining fragments bear mostly secondary forests where demographic parameters might differ from o ld-growth forests. Few studies about territory sizes and density have been conducted for entire bird communities or groups of species in the Neotropical region, with a bias towards Central America and the Amazon. In this work we determined territories of Atlantic Forest birds in order to assess their size and density. We conducted spot-mapping in a rectangular 40-ha plot within a 384-ha of secondary semideciduous forest fragment in Viçosa region, state of Minas Gerais, Brazil. We identified 260 territories of 30 species of insectivorous bir ds. Mean territory size of all species was 2.4 ha, ranging from 0.5 to 7.5 ha. The mean density for all species was 21.7 pairs/100 ha, ranging from 2.5 to 72.5 pairs. The sizes of the territories of many Atlantic Forest bir ds were by far smaller, and the density higher, than those of conspecific or congeneric species from A mazonian or Central American forests. These geographical differences in territory size and density can be explained by at least two non-exclusive hypotheses: 1) higher primary and secondary productivity in advanced successional secondary forest fragments and; 2) density compensation, given the loss of other competitor species. KEY-WORDS: density compensation, fragmentation, Minas Gerais, Neotropical, secondary forests, territoriality. INTRODUCTION the question whether they will hold viable populations depends on several aspects of birds' biology and their Secondary forests are increasingly replacing pristine knowledge is fundamental for conservation planning and actions. Population viability analyses (Shaffer 1981), forests around the world (ITTO 2002) and are, thus, important for conserving the remaining forest specialist for example, require estimates of a number of traits, species (Wright 2010). Compared to old-growth forests, including population density or territory size (Goldingay secondary forests have lower plant species richness and & Possingham 1995) which might be important for denser and more homogeneous understory (Guariguata management strategies (Beissinger & Westphal 1998, Duca et al. 2009). In addition, the knowledge of the & Ostertag 2001). Compared to secondary forests, Neotropical primary forests have more microhabitats, size and distribution of their territories by habitat types varying from very open understory under a higher and allows a better estimation of their population sizes with more closed canopy cover, to open vine tangles and bushes respect to vegetation characteristics of forest fragments of in older treefall gaps, and even to virtually impenetrable, a given area, and their use in population-based models (Millspaugh & Thompson-III 2009). shaded vine tangles in more recent treefall gaps (Robinson & Terborgh 1995, 1997). This mosaic of thicker and The Atlantic Forest is among the world's top more open understory in primary Neotropical forests biodiversity hotspots (Myers et al. 2000) with only 1% can result in a strikingly different use and distribution by of the original primary (or old-growth) forest remaining. birds in a given area (Robinson & Terborgh 1995, 1997, The current forest cover is estimated at 11–16%, considering forest patches older than 15 years, and Jullien & Thiollay 1998). These secondary forests are also often isolated and comprises thousands of remnants, most of them smaller even more disturbed by further human activities, and than 50 ha, highly isolated, and consisting primarily of Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini forests in secondary succession (Ribeiro et al. 2009). Bird METHODS species richness, and levels of endemic and threatened species (Stotz et al. 1996, Marini & Garcia 2005) are Our study was conducted at Viçosa county, a hilly region extremely high, but their biological parameters, such in southeastern Minas Gerais, Brazil, that consists of a mix as life histories, diets, habitat use, habitat selection and of semideciduous secondary forest fragments, immersed social behavior are largely unknown, as is common for in a matrix of pastures consisting of non-native grasses, many aspects of Neotropical birds (Heming et al. 2013). non-shaded coffee, Euc alyptus plantations, small corn and Furthermore, these Atlantic Forest fragments are already bean plantations, small vegetable gardens and orchards facing local bird extirpations (Ribon et al. 2003), and (≤ 0.5 ha), and narrow linear streams often bordered complete extinction of many species in the biome are by cattail (Typha spp.). Most native forest have been projected for the future although at a rate lower than destroyed along the last 200 years (Brant 2004) and the expected due to a time-lag response (Metzger et al. 2009). remaining patches (mostly secondary vegetation) cover Furthermore, within the Neotropics, there is a mainly hilltops and hillsides. These forest patches are bias in the geographical distribution of the studies mostly < 50 ha in size and the other matrix components describing basic characteristics of bird territories, such occupy the narrow lowlands and ravines (Pereira 1999, as density and size. Although there are some species- Ribon 2003). specific studies from t he Cerrado (savannah) Biome (Marini & Cavalcanti 1992, Ribeiro et al. 2002, Lopes Study area & Marini 2006, Domingues & Rodrigues 2007, Freitas & Rodrigues 2012, Costa & Rodrigues 2013, Duca The observations were made in the largest (384 ha) forest & Marini 2014, Marini et al. 2014) and the Atlantic fragment in an area of 10,000 ha surrounding Viçosa Forest (Willis et al. 1983, Willis & Oniki 2001, Duca county (the Centro de Pesquisas e Educação Ambiental & Marini 2005, Duca et al. 2006, Lima & Roper 2009) Mata do Paraíso – MP, 20°48'07.9''S; 42°51'29.5''W, most of them, including all those more comprehensive 690–870 m a.s.l.). The fragment suffered from strong (i.e. encompassing many species), come from Amazonia selective logging until the middle 1960's and some parts and Central America (Terborgh et al. 1990, Thiollay are regenerating from an unshaded coffee plantation and 1994, Robinson & Terborgh 1997, Robinson et al. 2000, pastureland. The vegetation is nowadays secondary forest Stouffer 2007, Johnson et al. 2011). with small patches of initial, intermediate and advanced Considering that still very little is known about succession stages. The largest forest fragment (~13,000 territoriality of Atlantic Forest birds, and that most of ha) near MP is the Serra do Brigadeiro State Park located the remaining Atlantic Forest is composed by fragments 37 km in straight line to the east. Our study plot reflected of secondary forests, it is very important to know how the topography of the region and included lowlands, bird species that persist in these fragments are distributed ravines, hillsides, and hilltops (sensu Espartel 1977) in different scales if we want to properly manage and within its limits. conserve them. In this study we focused on insectivorous Studies in different parts of the MP have shown birds as they have been reported to be highly vulnerable that areas with vegetation in intermediate and advanced to forest fragmentation and degradation (Stouffer & successional stages have almost half of the number of trees Bierregaard-Jr. 1995, Barlow et al. 2006, but see Anjos and shrubs found in the advanced successional stages 2006). Thus, we studied bird territories in a secondary (Marangon et al. 2003, Pinto et al. 2007). At an initial forest Atlantic Forest fragment to verify territory size and bird stage patch at MP (outside our study plot, but very similar density. Specifically we wanted to know how large are to some of its parts), based on their importance value, the the territories of Atlantic Forest birds still inhabiting a most representative species were Piptadenia gonoacantha secondary forest of a highly fragmented area originally (Mimosaceae), Vernonanthura diffusa (Asteraceae), covered by pristine forest that has suffered many Miconia cinnamomifolia (Melastomataceae), Piptocarpha extinctions (Ribon et al. 2003). Furthermore, we wanted macropoda (Asteraceae) and Luehea grandiflor a (Malvaceae) to determine the abundance and density of territories (Pinto et al. 2007). In the same study, in an advanced of each bird species. Additionally, we also used the few successional stage section, inside our study plot, Euterpe literature accounts on territory sizes of Neotropical birds edulis (Arecaceae), Piptadenia gonoacantha (Mimosaceae), to compare territory sizes and densities with conspecific Nectandra lanceolate (Lauraceae), Myrcia sphaerocarpa or congeneric species from pristine and secondary forests (Myrtaceae) and Guapira opposita (Nyctaginaceae) were from Amazonian or Central American forests as a way the most representative species. Intermediate stage inside to stimulate further studies comparing pristine and our study site is less diverse (Shannon diversity index H' secondary forests across the Neotropic within the same = 3.31) and has higher evenness (Pielou's J' = 0.83) than biome. advanced forest (H' = 3.46; J' = 0.79) (Pinto et al. 2007). Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini Historically, 298 bird species (of which 177 forest E D C B A 11 11 dependent) have been recorded at MP (Ribon et al. 2014), but at least 28 were already extirpated from the Viçosa region, including MP, since 1930's (Ribon et al. 10 2003). Territory mapping 9 We mapped the territories of birds in a 40-ha grid, with eleven 400 m trails intersecting five 1000 m trails 8 every 100 m in the central portion of MP. Roughly half of the grid is covered by native forest at late succession stage (studied by Pinto et al. 2007) with two patches of 7 native bamboo (Merostachys sp. and Olyra sp., Poaceae). The other half is dominated by native forest at early or intermediate succession with small patches of shaded 6 Pteridium (Dennstaedtiaceae) ferns, a half hectare of Corymbia citriodora (Myrtaceae) and one hectare of Pinus eliottii (Pinaceae) (Figure 1). All vegetation types have a dense understory. Because understory and insectivorous birds are often considered as negatively affected by forest fragmentation, destruction, and disturbance (Laurance & Bierregaard- Jr. 1997) we focused our study on the following insectivorous families: Momotidae, Thamnophilidae, Conopophagidae, Dendrocolaptidae, Furnariidae, and Tyrannidae, and in one Cardinalidae, the Red-crowned Ant-tanager (Habia rubica) an omnivorous mixed-species flock leader consuming large amount of invertebrates. To map territories we used territory mapping (or spot-mapping) following guidelines in Bibby et al. (1997) at the 40 ha grid plot described above (details in ED C BA Ribon 2005). The plot had 10-m interval contour lines mapped over a grid that were used to plot bird locations Native forest at early to Corymbia citriodora stand in the field (Ribon 2005). This method by itself suffices intermediate succession to estimate territory sizes and bird densities. Territory Pteridium ferns Bamboo patch (Merostachys, Olyra) mapping only requires that the locations of birds observed and vocalizing, especially simultaneous observations of Pinus elliottii stand Mature forest at late succession singing males, to be recorded. We followed this standard method, but used pairs of singing, calling, or observed FIGURE 1. Schematic representation of the vegetation at the 40 birds to plot territories of some species (Thamnophilidae, ha study grid plot established at Mata do Paraíso Research Station, Furnariidae, and Tyrannidae) because both males and Viçosa, Minas Gerais, Brazil, to map the territories of 30 bird species. females sing (pers. obs.; Sick 1997). Such songs are Letters and numbers indicate the codes of each of the five 1000 m and assumed to be related to territory defense and the limits eleven 400 m trails opened for the territory mapping. of their territories are assumed to lie in the space between singing birds. Even though not required by the territory mapping ICMBio (Permit No. 227) and a combination of two or approach, we also color-banded birds to aid in individual three color bands. identification. We banded 234 individuals of the focus The entire grid was surveyed 10 times to map bird species (85 recaptures) using 6–12 mist nets opened across territories from August to December 2000, each survey our grid (1635 net.h) from August 1999 to October 2000. occurring at each 10–15 days according to weather Nets (12 m × 2.5 m) were placed in different parts of the conditions. Surveys alternated between 1000 m and grid to capture as many individuals as possible. Birds were 400 m trails. As a morning was not enough to sample banded with metallic numbered rings from CEMAVE/ all the five 1000 m or all t he eleven 400 m trails, two Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini or three consecutive mornings were spent to survey all primary forest except Robinson et al. (2000) that worked the longer or all the shorter trails. All territory mapping on more disturbed forest. To allow a comparison of our was conducted from sunrise to 10:30 h, and birds were densities with those from studies conducted in other observed with a Leica Trinovid 10 × 42 mm binocular. Neotropical forests, we estimated the expected number Trails were never left. After 10 visits, we transferred of territories of congeneric species for an area of 100 ha, all the locations of each species to a map of the plot, considering one pair per territory for most species (see mapped the territories according to Bibby et al. (1997), above). We did this based in the structural homogeneity drew each territory contour and further measured them of secondary vegetation and in the assumption that birds using Autocad 1.4. (by Autodesk). For each territory, we in these habitats, as at our study plot, are much more measured its size (in ha). To calculate territory sizes, we evenly distributed than in primary forests (Thiollay used territories entirely inside the plot as well as those 1994, Guariguata & Ostertag 2001, Johnson et al. that partially overlapped the plot. The exact location of 2011). Although we recognize that territory mapping each territory of nine of the species studied along the grid could lead to less accurate estimates of bird density and can be found in Ribon (2003). smaller territory sizes than radio-telemetry (Streby et Among the 76 resident insectivorous bird species al. 2012) or detailed following of banded birds (Lima at the study site (Ribon et al. 2014), we estimated & Roper 2009), we judged it useful for a general territory sizes of 30 species. Among these, 20 species use comparison to mostly existent data on the Neotropical the understory and seldom go higher, while 10 species region (Terborgh et al. 1990, Thiollay 1994, Robinson primarily use the mid-story and canopy (Stotz et al. & Terborgh 1997, Robinson et al. 2000, Johnson et al. 1996, pers. obs.). The sample size for each species varie d 2011) as their data were all based on territory mapping according to its density and possibility of observation. obtained from trail grids. Because of the smaller size of We used a minimum of three locations (either song, our plot relative to other studies, we considered both call, visual, or combination of these) to determine birds with territories entirely inside the plot to calculate the boundaries of bird territories following Bibby et density, and birds with partial territories inside the plot al. (1997). However, only one territory each of three using a correction factor: densities of birds with partial different species had t hree locations, and the general territories inside the plot were proportional to the part average number of points per territory mapped was 13 of territory inside it. For example, for a territory that was (range 3–36). Capture locations and the scarce sightings 50% inside the plot, we assumed a density of 0.5 pairs of banded birds were used to help to solve doubts instead of 1. about territory boundaries obtained after the 10 visits. Recent research suggests that at least 30–40 locations are required for meaningful territory size estimation RESULTS (Anich et al. 2009). Although it is practical to obtain We mapped 260 territories of 30 species (Table 1), most such number of records for species-specific studies (with radio-telemetry or color-banded birds) standard territory of them non-banded. Mean territory size was 2.4 ha mapping still gives accurate estimates and maximize (range 0.5–7.5). Mean number of locations to delineate cost-benefit fieldwork effort when a large number of each territory was 12.9, ranging from three to 36 records species are studied at the same time (Terborgh et al. (Tables 1 and 2). Most territories were smaller than 4 ha (Figure 2). The smallest territory was 0.5 ha (Hangnest 1990, Robinson & Terborgh 1995, 1997). Furthermore, the use of territory mapping to estimate bird densities Tody-tyrant, Hemitriccus nidipendulus; and Greenish is appropriate if one can distinguish one territory from Elaenia Myiopagis viridicata) and the largest was 7.5 ha another. Bird nomenclature and systematic order follow (Gray-hooded Attila, Attila rufus). Remsen-Jr. et al. (2016). Eleven species were rare and had < 5 territories in our plot. Euler's Flycatcher (Lathrotriccus euleri), Rufous Comparison with other Neotropical sites Gnateater (Conopophaga lineata) and Yellow-olive Flycatcher (Tolmomyias sulphurescens) were very abundant, We compared our findings at MP to the few available with the largest number of territories demarcated (29, multispecies territorial studies based on territory 20 and 19 territories in the 40 ha plot, respectively). General average density for all species was 22 pairs/100 mapping in the Neotropics that encompassed several congeneric species found at our study site (Terborgh et ha, ranging from 2 (Sharp-tailed Streamcreeper, Lochmias al. 1990, Thiollay 1994, Robinson & Terborgh 1997, nematura; and Serra Antwren, Formicivora serrana) to 72 Robinson et al. 2000, Johnson et al. 2011). All these pairs/100 ha (Euler's Flycatcher), with 5 species reaching studies have been conducted in >95–100 ha grids of densities of more than 40 pairs/100 ha (Table 3). Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini TABLE 1. Territory sizes of 30 bird species in a 40 ha Atlantic Forest plot at Viçosa, Minas Gerais, Brazil. N - number of territories of each species; n – mean number of points used to map the territories of each species, followed by the range of points. Territory size (ha) Species N (n; range) Range Mean ± SE Rufous-capped Motmot (Baryphthengus ruficapillus) 6 (11.5; 8–14) 1.8–7.8 3.4 ± 0.9 Tufted Antshrike (Mackenziaena severa) 2 (12.5; 7–18) 6.4–6.8 6.6 ± 0.2 Variable Antshrike (Thamnophilus caerulescens) 17 (13.4; 7–22) 0.7–1.7 1.3 ± 0.1 Plain Antvireo (Dysithamnus mentalis) 17 (8.4; 5–13) 0.4–1.6 0.9 ± 0.1 Serra Antwren (Formicivora serrana) 1 (8) -- 1.0 Ferruginous Antbird (Drymophila ferruginea) 3 (17.3; 10–29) 0.8–1.3 1.2 ± 0.2 White-shouldered Fire–eye (Pyriglena leucoptera) 16 (15.2; 8 –36) 0.3–2.5 1.4 ± 0.1 Rufous Gnateater (Conopophaga lineata) 20 (7.7; 4–12) 0.3–1.2 0.6 ± 0.1 Rufous-capped Spinetail (Synallaxis ruficapilla) 14 (13.9; 6–23) 0.8–2.2 1.6 ± 0.1 Gray-bellied Spinetail (Synallaxis cinerascens) 7 (10.9; 4–19) 1.5 –3.5 2.1 ± 0.3 White-collared Foliage-gleaner (Anabazenops fuscus) 9 (18.9; 8–30) 0.7–7.0 3.3 ± 0.6 White-eyed Foliage-gleaner (Automolus leucophthalmus) 3 (21.3; 9–31) 2.1–7.2 5.4 ± 1.6 Streaked Xenops (Xenops rutilans) 4 (15.8; 11–23) 3.7–7.4 6.0 ± 0.8 Sharp-tailed Streamcreeper (Lochmias nematura) 1 (15) -- 2.2 Lesser Woodcreeper (Xiphorhynchus fuscus) 5 (9.6; 5–13) 2.0–4.1 3.3 ± 0.4 Scaled Woodcreeper (Lepidocolaptes squamatus) 8 (9.2; 5–12) 0.7–5.2 2.2 ± 0.5 Black-billed Scythebill (Campylorhamphus falcularius) 5 (9; 3–16) 1.0–4.1 2.8 ± 0.5 Greenish Elaenia (Myiopagis viridicata) 6 (4.6; 3–8) 0.3–1.0 0.5 ± 0.1 Gray Elaenia (Myiopagis caniceps) 3 (7.8; 5–12) 2.0–4.1 3.0 ± 0.6 Sepia-capped Flycatcher (Leptopogon amaurocephalus) 10 (13.5; 9–27) 0.9–3.7 2.3 ± 0.3 Southern Antpipit (Corythopis delalandi) 15 (10.7; 6–19) 0.2–3.0 1.0 ± 0.2 Eared Pygmy-tyrant (Myiornis auricularis) 10 (9.2; 3–16) 0.4 –1.9 1.1 ± 0.2 Hangnest Tody-tyrant (Hemitriccus nidipendulus) 3 (7.5; 5–10) 0.3–0.7 0.5 ± 0.1 Yellow-lored Tody-flycatcher (To dirostrum poliocephalum) 8 (19.8; 16–26) 0.3–2.0 1.5 ± 0.2 Ochre-faced Tody-flycatcher (Poecilotriccus plumbeiceps) 2 (12.5; 10–15) 0.9–2.4 1.7 ± 0.8 Yellow-olive Flycatcher (Tolmomyias sulphurescens) 19 (18.3; 8–27) 0.7–2.9 1.6 ± 0.2 White-throated Spadebill (Platyrinchus mystaceus) 12 (15.1; 6–27) 1.2–2.9 2.0 ± 0.2 Euler's Flycatcher (Lathrotriccus euleri) 29 (13.3; 5–31) 0.2–2.0 0.9 ± 0.1 Gray-hooded Attila (Attila rufus) 2 (18.5; 11–26) 3.2–11.7 7.5 ± 4.3 Red-crowned Ant-tanager (Habia rubica) 3 (17.3; 13–21) 2.4–5.7 4.0 ± 1.0 TABLE 2. Territory sizes (ha) of birds at three Neotropical sites. Atlantic Forest birds are aligned at the left. a b c d Species Viçosa, Brazil Peru Panama Manaus, Brazil Baryphthengus ruficapillus 3.4 B. martii 5–8 Mackenziaena severa 6.6 Thamnophilus caerulescens 1.3 T. aethiops 10 T. schistaceus 8 T. atrinucha 1 T. murinus 5.6 Dysithamnus mentalis 0.9 D. puncticeps <2 Formicivora serrana 1.0 Drymophila ferruginea 1.2 Pyriglena leucoptera 1.4 Conopophaga lineata 0.6 C. aurita 6.3 Synallaxis cinerascens 2.1 S. ruficapilla 1.6 Anabazenops fuscus 3.3 Automolus leucophthalmus 5.4 A. infuscatus 12 10.6 A. ochrolaemus 11 11 A. rubiginosus 13.3 Xenops rutilans 6.0 X. minutus 9 5 13.3 Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini a b c d Species Viçosa, Brazil Peru Panama Manaus, Brazil Lochmias nematura 2.2 Xiphorhynchus fuscus 3.3 X. pardalotus 10.6 Lepidocolaptes squamatus 2.2 L. albolineatus 14 12 Campyloramphus falcularius 2.8 C. procurvoides 24 Myiopagis viridicata 0.5 Myiopagis caniceps 3.0 5–8 6 M. gaimardii 4 5.6 Leptopogon amaurocephalus 2.3 3 Corythopis delalandi 1.0 C. torquata 6 5.7 Myiornis auricularis 1.1 M. ecaudatus 3 M. atricapillus 3 Hemitriccus nidipendulus 0.5 H. zosterops 3 3.9 Todirostrum poliocephalum 1.5 Todirostrum plumbeiceps 1.7 T. crysophataphum 7* Tolmomyias sulphurescens 1.6 T. assimilis 6 4 9.1 T. poliocephalus 56 Platyrinchus mystaceus 2.0 P. coronatus 5 6 3.8 P. platyrhynchos 55 Lathrotriccus euleri 0.9 5 Attila rufus 7.5 A. bolivianus 12 A. spadiceus 12816 Habia rubica 46 H. fuscicauda 25 Average 2.4 7.3 7.1 9.2 a b c d * This study. Territory sizes estimated for 100 ha. Terborgh et al. (1990). Robinson et al. (2000). Johnson et al. (2011). Robinson & Terborgh (1997). TABLE 3. Density of birds (pairs/100 ha) at five Neotropical sites. Atlantic Forest bir ds are aligned at the left. * – number of individuals. a b c d e f Species Atlantic Forest Peru Peru Guyana Manaus Panama Baryphthengus ruficapillus 15 B. martii 24 Mackenziaena severa 5 Thamnophilus caerulescens 42.5 T. aethiops 1 T. schistaceus 10.5 0.5–21 T. doliatus 38 T. murinus 7.75 12.5 T. amazonicus 4 T. punctatus 0.25 T. atrinucha 106 Dysithamnus mentalis 42.5 D. puncticeps 3.5 Formicivora serrana 2.5 Drymophila ferruginea 7.5 Pyriglena leucoptera 40 Conopophaga lineata 50 C. peruviana 3 C. aurita 12 Synallaxis cinerascens 17.5 S. ruficapilla 35 S. gujanensis 53 Anabazenops fuscus 22.5 Automolus leucophthalmus 7.5 A. infuscatus 1.5 4.75 7 A. ochrolaemus 2.5 2–3 1 5 A. rufipileatus 38 A. rubiginosus 1.5 Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini a b c d e f Species Atlantic Forest Peru Peru Guyana Manaus Panama Xenops rutilans 10 4 0.5–4 X. minutus 6 1.5–7.5 6.5 9 27 X. milleri 4.5 Lochmias nematura 2.5 Xiphorhynchus fuscus 12.5 X. pardalotus 18 Lepidocolaptes squamatus 20 L. albolineatus 510 Campyloramphus falcularius 12.5 C. trochilirostris 0.5 C. procurvoides 0.5–9 1.25 3 Myiopagis viridicata 15 5 Myiopagis caniceps 7.5 5 3 M. gaimardii 4 4–20.5 3.25 12.5 11.5 Leptopogon amaurocephalus 25 2.5 2.5–3 1 Corythopis delalandi 37.5 C. torquata 7 3.75 3.5 Myiornis auricularis 25 M. ecaudatus 10 10 4 6 M. atricapillus 3.5 Hemitriccus nidipendulus 7.5 H. zosterops 531 H. minor 6 H. josephinae 2 Todirostrum poliocephalum 20 Todirostrum plumbeiceps 5 T. crysophataphum 3.5 3.5–7.5 T. pictum 3.5 4 T. nigriceps 0.5 Tolmomyias sulphurescens 47.5 T. assimilis 4 4–15 2 17.5 15.5 T. poliocephalus 3 3–10 5 T. flaviventris 4.5–16 0.75 Platyrinchus mystaceus 30 4 P. coronatus 7.5 7.5 15 9.5 10 P. platyrhynchos 66 P. saturatus 53 Latrotriccus euleri 72.5 1.5 L. virescens 24* Attila rufus 5 A. bolivianus 4 4–14 A. spadiceus 4 2–4 4.5 3 7 Habia rubica 7.5 8.5 H. fuscicauda 3* Average 21.7 4.5 12.8 4.3 8.4 15.8 a b c d This study; density extrapolated for 100 ha from data in Table 1. Terborgh et al. (1990). Robinson & Terborgh (1997). Thiollay et al. (1994). e f Johnson et al. (2011). Robinson et al. (2000). > 6.0 0.5–2.0 2.1–4.0 4.1–6.0 Territory size (ha) FIGURE 2. Average territory sizes (ha) of birds at the Atlantic Forest (black bars), Panama (Robinson et al. 2000) (cross-hatched bars), Manaus (Johnson et al. 2011) (grey bars), and Peru (Terborgh et al. 1990) (white bars). Revista Brasileira de Ornitologia, 24(4), 2016 Number of species Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini DISCUSSION mapping is not clearly stated by them as the method used for deriving bird densities. However, their estimates are highly suggestive that the pattern we have found in Viçosa Small territory sizes (< 5 ha) were common among insectivorous birds in the secondary Atlantic Forest can occur also in pristine areas of the Atlantic Forest. It fragment that we studied. Similarly, other species of should be noted, though, that although a small number insectivorous birds found in forested habitats in the Atlantic of large territories in an area often demonstrates low bird density, species with small territories that do not occupy Forest Biome are known to occupy small territories and most of the available habitat also have low densities, as occur at high densities, including, Flavescent Warblers (Basileuterus flaveo lus, 2 ha; Duca & Marini 2005), have been shown for birds with patchy distribution in Variable Antshrikes (Thamnophilus caerulescens, 0.9 ha), primary forests in French Guyana (Thiollay 1994). Plain Antvireos (Dysithamnus mentalis, 0.7 ha), White- The average density at our study site (22 pairs/100 ha) was higher than that for congeneric birds in Guiana shouldered Fire-eyes (Pyriglena leucoptera, 1.4 ha) (Duca (average density = 4.1 pairs/100 ha, Thiollay 1994), et al. 2006), and Black-cheecked Gnateater (Conopophaga melanops, 2.94 ha; Lima & Roper 2009). In addition, Manaus (average density = 8.4 pairs/100 ha, Johnson et the territory sizes of six species of Thamnophilidae in São al. 2011), and the two Peruvian sites (average density = Paulo varied from 0.8 to 3.0 ha (Willis & Oniki 2001). 4.5 pairs/100 ha, Terborgh et al. 1990; average density =12.8 pairs/100 ha, Robinson and Terborgh 1997) As ours, all the above studies, carried out in the Atlantic (Table 3). In Panama the density of 15.7 birds/100 ha Forest, have been conducted in areas that altered by human activities in the past and, thus, had a vegetation was inflated by a very high density of 106 pairs/100 structure similar to that of our study area, although the ha of the hyper-abundant Black-crowned Antshrike understory of the area studied by Duca et al. (2006) was (Thamnophilus atrinucha) which represented almost 50% of all individual birds reported by Robinson et al. (2000). more open because the forest was older (> 150 years) than It should be noted, however, that when compared to ours (c. 50 years). When we compare species among other Neotropical South American forest bird communities, those in Central biomes, the average territory size at our study site (2.4 America have lower species richness, and this could result ha) was smaller than that of congeneric birds in Panama in higher densities of some populations such as at the more disturbed secondary forest in Panama (Robinson (average size = 7.1 ha, Robinson et al. 2000), Peru (average et al. 2000), similarly to our results and to those at size = 7.4 ha, Terborgh et al. 1990), and Manaus (average size = 9.0 ha, Johnson et al. 2011). When comparing successional vegetation in Peru (Robinson & Terborgh congeneric similarly-sized species, 9 of the 11 species in 1997). Only four of the 16 species compared in Panama Panama (Robinson et al. 2000) and all the 20 species in (Robinson et al. 2000) and four of the 18 species in Peru (Robinson & Terborgh 1997) had higher densities than Peru (Terborgh et al. 1990) had larger territories than those in Viçosa. Also, in an additional study conducted those from our Atlantic Forest plot. In Manaus, Stouffer (2007) have found the territories of Conopophaga aurita near Manaus, Amazonia (Stouffer 2007), territories were and Corythopis torquatus were 2 to about 6 times larger larger (average of 13 ha) and densities were lower (average than we found for C. lineata and C. delalandi at MP, of 3.4 pairs/100 ha) than those of Atlantic Forest birds. One important difference among the Neotropical respectively. studies compared here is the successional stage of the As territory sizes were small at our grid, bird densities at MP were high. In their study comparing bird densities forest. The lowest bird densities and larger territory sizes in 5000 ha tract of Atlantic Forest that suffered selective were found in the sites with old-growth primary forest logging 25 years before their study, in Paraguay, Cockle in Peru (Terborgh et al. 1990), Guyana (Thiollay 1994), and Manaus (Johnson et al. 2011). The other study site et al. (2005) applied territory mapping “where possible”. in Peru had an intermediate average density value and They also have found high densities of territories/100 ha for some of the same species that we studied in Viçosa: was carried out along a primary successional gradient Eared Pygmy-tyrant, Myiornis auricularis (c. 68 territories), (Robinson & Terborgh 1997). The second highest bird Rufous-capped Spinetail, Synallaxis ruficapilla ( c. 24 density was observed in Panama (Robinson et al. 2000), at a site of primary forest with plenty of gaps created by territories), Eared Pygmy-tyrant, Myiornis auricularis natural treefalls and storms. All the Atlantic Forest sites (c. 40 territories), Euler's Flycatcher, Lathrotriccus euleri, Gray-bellied Spinetail, Synallaxis cinerascens, have secondary or selectively logged forests, often with White-throated Spadebill, Platyrinchus mystaceus, Plain dense understory. Antvireo, Dysithamnus mentalis and Variable Antshrike, Younger successional vegetation stages have higher productivity allowing higher bird density (Robinson Thamnophilus caerulescens (all t hese five species with c. 10– & Terborgh 1997, Aleixo 1999). Birds density and 20 territories each). These authors have not obtained their data from a grid in the forest area sampled and territory territory size in our study site could be a response to a Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini denser understory and, consequently, a higher abundance the Atlantic Forest to date. Our estimates might be useful of leaves and insects, as indicated by species-specific to future conservation and management studies in the (Bechard 1982, Hunt 1996) or community (Robinson biome. However, a comprehensive determination and & Terborgh 1997, Casenave et al. 1998) studies. In fact, explanation for this proposed pattern in the biome awaits studies conducted in secondary forests in Amazonia further tests. have shown that territory sizes of birds in these habitats are indeed smaller, and bird density higher, than in the ACKNOWLEDGEMENTS primary forests (Kratter 1997, Robinson & Terborgh 1997, Kattan & Beltran 2002). We thank CAPES, CNPq, Programa de Pós-graduação Density compensation, a phenomenon originally em Ecologia, Conservação e Manejo de Fauna Silvestre of described for groups of islands (MacArthur et al. 1972, the Universidade Federal de Minas Gerais, Programa Connor et al. 2000), could be occurring in the small Nacional de Biodiversidade/Ministério do Meio Ambiente/ forest fragments such as MP. Density compensation Banco Interamericano de Desenvolvimento (PROBIO/ results in higher density for those bird species able to MMA/BIRD), Programa Natureza e Sociedade WWF/ colonize islands because of the lack of many species that SUNY (Project CSR 142-00), PROBIO-MMA/GEF/ cannot reach them. The lack of many species would BM (Project Efeitos Espaciais e Temporais da Fragmentação thus trigger “competitor release” and “predator release”, de Hábitats sobre Populações de Insetos e Pássaros), allowing wider niches and much higher densities than in Departamento de Engenharia Florestal (UFV) for the mainland (Stamps & Buechner 1985, Connor et al. financial support. Serra do Cipó National Park (ICMBio) 2000). Although density compensation does not always provided facilities for data analysis. The following helped happens (Connor et al. 2000) it could help to explain the in several stages of the study: E. R. Luiz, A. B. Andrade, territory patterns of the Viçosa region since we studied A. C. Ottoni, F. Stanciola, S. L. Ribeiro (in memorian), territories in a relatively small forest fragment (roughly N. R. Neves, E. C. A. Nieto, H. C. Sari, S. D. Souza, 380 ha) from where several birds have already gone extinct R. F. Fadini. The late C. Bibb y helped to solve doubts (Ribon et al. 2003). The extirpation of species with niches during territory mapping analysis. We appreciate the similar to those that persisted in our area could make it improvements in English usage made by Chandler possible for them to expand their use of resources and Robbins through the Association of Field Ornithologists' achieve higher densities and smaller territories. program of editorial assistance. Two anonymous reviewers Even though territory sizes and bird densities are greatly improved the manuscript. similar among our study and the few other available studies on Atlantic Forest birds, these results should not be generalized to the biome. This is not only because REFERENCES there are many different vegetation subtypes to be studied (e.g. lowland vs. submontane vs. montane forests; Aleixo, A. 1999. Effects of selective logging on a bird community in southern vs. central vs. northeastern forests; old growth the Brazilian Atlantic Forest. 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Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil

Ribon, Rômulo; Marini, Miguel Â.
Ornithology Research , Volume 24 (4) – Dec 1, 2016
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Revista Brasileira de Ornitologia, 24(4), 303–313 ARTICLE December 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil 1,2,4 3 Rômulo Ribon and Miguel Â. Marini Programa de Pós-graduação em Ecologia, Conservação e Manejo de Vida Silvestre, Departamento de Biologia Geral, ICB, Universidade Federal de Minas Gerais, CEP 30161-970, Belo Horizonte, MG, Brazil. Museu de Zoologia João Moojen, Departamento de Biologia Animal, Universidade Federal de Viçosa, CEP 36570-000, Viçosa, MG, Brazil. Departamento de Zoologia, IB, Universidade de Brasília, CEP 70910-900, Brasília, DF, Brazil. Corresponding author: romulo.ribon@ufv.br Received on 18 August 2016. Accepted on 27 December 2016. ABSTRACT: Demographic parameters of birds are essential to understand their ecology and delineate conservation and management plans. This becomes especially important in highly altered biomes such as the Brazilian Atlantic Forest, since the few remaining fragments bear mostly secondary forests where demographic parameters might differ from o ld-growth forests. Few studies about territory sizes and density have been conducted for entire bird communities or groups of species in the Neotropical region, with a bias towards Central America and the Amazon. In this work we determined territories of Atlantic Forest birds in order to assess their size and density. We conducted spot-mapping in a rectangular 40-ha plot within a 384-ha of secondary semideciduous forest fragment in Viçosa region, state of Minas Gerais, Brazil. We identified 260 territories of 30 species of insectivorous bir ds. Mean territory size of all species was 2.4 ha, ranging from 0.5 to 7.5 ha. The mean density for all species was 21.7 pairs/100 ha, ranging from 2.5 to 72.5 pairs. The sizes of the territories of many Atlantic Forest bir ds were by far smaller, and the density higher, than those of conspecific or congeneric species from A mazonian or Central American forests. These geographical differences in territory size and density can be explained by at least two non-exclusive hypotheses: 1) higher primary and secondary productivity in advanced successional secondary forest fragments and; 2) density compensation, given the loss of other competitor species. KEY-WORDS: density compensation, fragmentation, Minas Gerais, Neotropical, secondary forests, territoriality. INTRODUCTION the question whether they will hold viable populations depends on several aspects of birds' biology and their Secondary forests are increasingly replacing pristine knowledge is fundamental for conservation planning and actions. Population viability analyses (Shaffer 1981), forests around the world (ITTO 2002) and are, thus, important for conserving the remaining forest specialist for example, require estimates of a number of traits, species (Wright 2010). Compared to old-growth forests, including population density or territory size (Goldingay secondary forests have lower plant species richness and & Possingham 1995) which might be important for denser and more homogeneous understory (Guariguata management strategies (Beissinger & Westphal 1998, Duca et al. 2009). In addition, the knowledge of the & Ostertag 2001). Compared to secondary forests, Neotropical primary forests have more microhabitats, size and distribution of their territories by habitat types varying from very open understory under a higher and allows a better estimation of their population sizes with more closed canopy cover, to open vine tangles and bushes respect to vegetation characteristics of forest fragments of in older treefall gaps, and even to virtually impenetrable, a given area, and their use in population-based models (Millspaugh & Thompson-III 2009). shaded vine tangles in more recent treefall gaps (Robinson & Terborgh 1995, 1997). This mosaic of thicker and The Atlantic Forest is among the world's top more open understory in primary Neotropical forests biodiversity hotspots (Myers et al. 2000) with only 1% can result in a strikingly different use and distribution by of the original primary (or old-growth) forest remaining. birds in a given area (Robinson & Terborgh 1995, 1997, The current forest cover is estimated at 11–16%, considering forest patches older than 15 years, and Jullien & Thiollay 1998). These secondary forests are also often isolated and comprises thousands of remnants, most of them smaller even more disturbed by further human activities, and than 50 ha, highly isolated, and consisting primarily of Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini forests in secondary succession (Ribeiro et al. 2009). Bird METHODS species richness, and levels of endemic and threatened species (Stotz et al. 1996, Marini & Garcia 2005) are Our study was conducted at Viçosa county, a hilly region extremely high, but their biological parameters, such in southeastern Minas Gerais, Brazil, that consists of a mix as life histories, diets, habitat use, habitat selection and of semideciduous secondary forest fragments, immersed social behavior are largely unknown, as is common for in a matrix of pastures consisting of non-native grasses, many aspects of Neotropical birds (Heming et al. 2013). non-shaded coffee, Euc alyptus plantations, small corn and Furthermore, these Atlantic Forest fragments are already bean plantations, small vegetable gardens and orchards facing local bird extirpations (Ribon et al. 2003), and (≤ 0.5 ha), and narrow linear streams often bordered complete extinction of many species in the biome are by cattail (Typha spp.). Most native forest have been projected for the future although at a rate lower than destroyed along the last 200 years (Brant 2004) and the expected due to a time-lag response (Metzger et al. 2009). remaining patches (mostly secondary vegetation) cover Furthermore, within the Neotropics, there is a mainly hilltops and hillsides. These forest patches are bias in the geographical distribution of the studies mostly < 50 ha in size and the other matrix components describing basic characteristics of bird territories, such occupy the narrow lowlands and ravines (Pereira 1999, as density and size. Although there are some species- Ribon 2003). specific studies from t he Cerrado (savannah) Biome (Marini & Cavalcanti 1992, Ribeiro et al. 2002, Lopes Study area & Marini 2006, Domingues & Rodrigues 2007, Freitas & Rodrigues 2012, Costa & Rodrigues 2013, Duca The observations were made in the largest (384 ha) forest & Marini 2014, Marini et al. 2014) and the Atlantic fragment in an area of 10,000 ha surrounding Viçosa Forest (Willis et al. 1983, Willis & Oniki 2001, Duca county (the Centro de Pesquisas e Educação Ambiental & Marini 2005, Duca et al. 2006, Lima & Roper 2009) Mata do Paraíso – MP, 20°48'07.9''S; 42°51'29.5''W, most of them, including all those more comprehensive 690–870 m a.s.l.). The fragment suffered from strong (i.e. encompassing many species), come from Amazonia selective logging until the middle 1960's and some parts and Central America (Terborgh et al. 1990, Thiollay are regenerating from an unshaded coffee plantation and 1994, Robinson & Terborgh 1997, Robinson et al. 2000, pastureland. The vegetation is nowadays secondary forest Stouffer 2007, Johnson et al. 2011). with small patches of initial, intermediate and advanced Considering that still very little is known about succession stages. The largest forest fragment (~13,000 territoriality of Atlantic Forest birds, and that most of ha) near MP is the Serra do Brigadeiro State Park located the remaining Atlantic Forest is composed by fragments 37 km in straight line to the east. Our study plot reflected of secondary forests, it is very important to know how the topography of the region and included lowlands, bird species that persist in these fragments are distributed ravines, hillsides, and hilltops (sensu Espartel 1977) in different scales if we want to properly manage and within its limits. conserve them. In this study we focused on insectivorous Studies in different parts of the MP have shown birds as they have been reported to be highly vulnerable that areas with vegetation in intermediate and advanced to forest fragmentation and degradation (Stouffer & successional stages have almost half of the number of trees Bierregaard-Jr. 1995, Barlow et al. 2006, but see Anjos and shrubs found in the advanced successional stages 2006). Thus, we studied bird territories in a secondary (Marangon et al. 2003, Pinto et al. 2007). At an initial forest Atlantic Forest fragment to verify territory size and bird stage patch at MP (outside our study plot, but very similar density. Specifically we wanted to know how large are to some of its parts), based on their importance value, the the territories of Atlantic Forest birds still inhabiting a most representative species were Piptadenia gonoacantha secondary forest of a highly fragmented area originally (Mimosaceae), Vernonanthura diffusa (Asteraceae), covered by pristine forest that has suffered many Miconia cinnamomifolia (Melastomataceae), Piptocarpha extinctions (Ribon et al. 2003). Furthermore, we wanted macropoda (Asteraceae) and Luehea grandiflor a (Malvaceae) to determine the abundance and density of territories (Pinto et al. 2007). In the same study, in an advanced of each bird species. Additionally, we also used the few successional stage section, inside our study plot, Euterpe literature accounts on territory sizes of Neotropical birds edulis (Arecaceae), Piptadenia gonoacantha (Mimosaceae), to compare territory sizes and densities with conspecific Nectandra lanceolate (Lauraceae), Myrcia sphaerocarpa or congeneric species from pristine and secondary forests (Myrtaceae) and Guapira opposita (Nyctaginaceae) were from Amazonian or Central American forests as a way the most representative species. Intermediate stage inside to stimulate further studies comparing pristine and our study site is less diverse (Shannon diversity index H' secondary forests across the Neotropic within the same = 3.31) and has higher evenness (Pielou's J' = 0.83) than biome. advanced forest (H' = 3.46; J' = 0.79) (Pinto et al. 2007). Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini Historically, 298 bird species (of which 177 forest E D C B A 11 11 dependent) have been recorded at MP (Ribon et al. 2014), but at least 28 were already extirpated from the Viçosa region, including MP, since 1930's (Ribon et al. 10 2003). Territory mapping 9 We mapped the territories of birds in a 40-ha grid, with eleven 400 m trails intersecting five 1000 m trails 8 every 100 m in the central portion of MP. Roughly half of the grid is covered by native forest at late succession stage (studied by Pinto et al. 2007) with two patches of 7 native bamboo (Merostachys sp. and Olyra sp., Poaceae). The other half is dominated by native forest at early or intermediate succession with small patches of shaded 6 Pteridium (Dennstaedtiaceae) ferns, a half hectare of Corymbia citriodora (Myrtaceae) and one hectare of Pinus eliottii (Pinaceae) (Figure 1). All vegetation types have a dense understory. Because understory and insectivorous birds are often considered as negatively affected by forest fragmentation, destruction, and disturbance (Laurance & Bierregaard- Jr. 1997) we focused our study on the following insectivorous families: Momotidae, Thamnophilidae, Conopophagidae, Dendrocolaptidae, Furnariidae, and Tyrannidae, and in one Cardinalidae, the Red-crowned Ant-tanager (Habia rubica) an omnivorous mixed-species flock leader consuming large amount of invertebrates. To map territories we used territory mapping (or spot-mapping) following guidelines in Bibby et al. (1997) at the 40 ha grid plot described above (details in ED C BA Ribon 2005). The plot had 10-m interval contour lines mapped over a grid that were used to plot bird locations Native forest at early to Corymbia citriodora stand in the field (Ribon 2005). This method by itself suffices intermediate succession to estimate territory sizes and bird densities. Territory Pteridium ferns Bamboo patch (Merostachys, Olyra) mapping only requires that the locations of birds observed and vocalizing, especially simultaneous observations of Pinus elliottii stand Mature forest at late succession singing males, to be recorded. We followed this standard method, but used pairs of singing, calling, or observed FIGURE 1. Schematic representation of the vegetation at the 40 birds to plot territories of some species (Thamnophilidae, ha study grid plot established at Mata do Paraíso Research Station, Furnariidae, and Tyrannidae) because both males and Viçosa, Minas Gerais, Brazil, to map the territories of 30 bird species. females sing (pers. obs.; Sick 1997). Such songs are Letters and numbers indicate the codes of each of the five 1000 m and assumed to be related to territory defense and the limits eleven 400 m trails opened for the territory mapping. of their territories are assumed to lie in the space between singing birds. Even though not required by the territory mapping ICMBio (Permit No. 227) and a combination of two or approach, we also color-banded birds to aid in individual three color bands. identification. We banded 234 individuals of the focus The entire grid was surveyed 10 times to map bird species (85 recaptures) using 6–12 mist nets opened across territories from August to December 2000, each survey our grid (1635 net.h) from August 1999 to October 2000. occurring at each 10–15 days according to weather Nets (12 m × 2.5 m) were placed in different parts of the conditions. Surveys alternated between 1000 m and grid to capture as many individuals as possible. Birds were 400 m trails. As a morning was not enough to sample banded with metallic numbered rings from CEMAVE/ all the five 1000 m or all t he eleven 400 m trails, two Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini or three consecutive mornings were spent to survey all primary forest except Robinson et al. (2000) that worked the longer or all the shorter trails. All territory mapping on more disturbed forest. To allow a comparison of our was conducted from sunrise to 10:30 h, and birds were densities with those from studies conducted in other observed with a Leica Trinovid 10 × 42 mm binocular. Neotropical forests, we estimated the expected number Trails were never left. After 10 visits, we transferred of territories of congeneric species for an area of 100 ha, all the locations of each species to a map of the plot, considering one pair per territory for most species (see mapped the territories according to Bibby et al. (1997), above). We did this based in the structural homogeneity drew each territory contour and further measured them of secondary vegetation and in the assumption that birds using Autocad 1.4. (by Autodesk). For each territory, we in these habitats, as at our study plot, are much more measured its size (in ha). To calculate territory sizes, we evenly distributed than in primary forests (Thiollay used territories entirely inside the plot as well as those 1994, Guariguata & Ostertag 2001, Johnson et al. that partially overlapped the plot. The exact location of 2011). Although we recognize that territory mapping each territory of nine of the species studied along the grid could lead to less accurate estimates of bird density and can be found in Ribon (2003). smaller territory sizes than radio-telemetry (Streby et Among the 76 resident insectivorous bird species al. 2012) or detailed following of banded birds (Lima at the study site (Ribon et al. 2014), we estimated & Roper 2009), we judged it useful for a general territory sizes of 30 species. Among these, 20 species use comparison to mostly existent data on the Neotropical the understory and seldom go higher, while 10 species region (Terborgh et al. 1990, Thiollay 1994, Robinson primarily use the mid-story and canopy (Stotz et al. & Terborgh 1997, Robinson et al. 2000, Johnson et al. 1996, pers. obs.). The sample size for each species varie d 2011) as their data were all based on territory mapping according to its density and possibility of observation. obtained from trail grids. Because of the smaller size of We used a minimum of three locations (either song, our plot relative to other studies, we considered both call, visual, or combination of these) to determine birds with territories entirely inside the plot to calculate the boundaries of bird territories following Bibby et density, and birds with partial territories inside the plot al. (1997). However, only one territory each of three using a correction factor: densities of birds with partial different species had t hree locations, and the general territories inside the plot were proportional to the part average number of points per territory mapped was 13 of territory inside it. For example, for a territory that was (range 3–36). Capture locations and the scarce sightings 50% inside the plot, we assumed a density of 0.5 pairs of banded birds were used to help to solve doubts instead of 1. about territory boundaries obtained after the 10 visits. Recent research suggests that at least 30–40 locations are required for meaningful territory size estimation RESULTS (Anich et al. 2009). Although it is practical to obtain We mapped 260 territories of 30 species (Table 1), most such number of records for species-specific studies (with radio-telemetry or color-banded birds) standard territory of them non-banded. Mean territory size was 2.4 ha mapping still gives accurate estimates and maximize (range 0.5–7.5). Mean number of locations to delineate cost-benefit fieldwork effort when a large number of each territory was 12.9, ranging from three to 36 records species are studied at the same time (Terborgh et al. (Tables 1 and 2). Most territories were smaller than 4 ha (Figure 2). The smallest territory was 0.5 ha (Hangnest 1990, Robinson & Terborgh 1995, 1997). Furthermore, the use of territory mapping to estimate bird densities Tody-tyrant, Hemitriccus nidipendulus; and Greenish is appropriate if one can distinguish one territory from Elaenia Myiopagis viridicata) and the largest was 7.5 ha another. Bird nomenclature and systematic order follow (Gray-hooded Attila, Attila rufus). Remsen-Jr. et al. (2016). Eleven species were rare and had < 5 territories in our plot. Euler's Flycatcher (Lathrotriccus euleri), Rufous Comparison with other Neotropical sites Gnateater (Conopophaga lineata) and Yellow-olive Flycatcher (Tolmomyias sulphurescens) were very abundant, We compared our findings at MP to the few available with the largest number of territories demarcated (29, multispecies territorial studies based on territory 20 and 19 territories in the 40 ha plot, respectively). General average density for all species was 22 pairs/100 mapping in the Neotropics that encompassed several congeneric species found at our study site (Terborgh et ha, ranging from 2 (Sharp-tailed Streamcreeper, Lochmias al. 1990, Thiollay 1994, Robinson & Terborgh 1997, nematura; and Serra Antwren, Formicivora serrana) to 72 Robinson et al. 2000, Johnson et al. 2011). All these pairs/100 ha (Euler's Flycatcher), with 5 species reaching studies have been conducted in >95–100 ha grids of densities of more than 40 pairs/100 ha (Table 3). Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini TABLE 1. Territory sizes of 30 bird species in a 40 ha Atlantic Forest plot at Viçosa, Minas Gerais, Brazil. N - number of territories of each species; n – mean number of points used to map the territories of each species, followed by the range of points. Territory size (ha) Species N (n; range) Range Mean ± SE Rufous-capped Motmot (Baryphthengus ruficapillus) 6 (11.5; 8–14) 1.8–7.8 3.4 ± 0.9 Tufted Antshrike (Mackenziaena severa) 2 (12.5; 7–18) 6.4–6.8 6.6 ± 0.2 Variable Antshrike (Thamnophilus caerulescens) 17 (13.4; 7–22) 0.7–1.7 1.3 ± 0.1 Plain Antvireo (Dysithamnus mentalis) 17 (8.4; 5–13) 0.4–1.6 0.9 ± 0.1 Serra Antwren (Formicivora serrana) 1 (8) -- 1.0 Ferruginous Antbird (Drymophila ferruginea) 3 (17.3; 10–29) 0.8–1.3 1.2 ± 0.2 White-shouldered Fire–eye (Pyriglena leucoptera) 16 (15.2; 8 –36) 0.3–2.5 1.4 ± 0.1 Rufous Gnateater (Conopophaga lineata) 20 (7.7; 4–12) 0.3–1.2 0.6 ± 0.1 Rufous-capped Spinetail (Synallaxis ruficapilla) 14 (13.9; 6–23) 0.8–2.2 1.6 ± 0.1 Gray-bellied Spinetail (Synallaxis cinerascens) 7 (10.9; 4–19) 1.5 –3.5 2.1 ± 0.3 White-collared Foliage-gleaner (Anabazenops fuscus) 9 (18.9; 8–30) 0.7–7.0 3.3 ± 0.6 White-eyed Foliage-gleaner (Automolus leucophthalmus) 3 (21.3; 9–31) 2.1–7.2 5.4 ± 1.6 Streaked Xenops (Xenops rutilans) 4 (15.8; 11–23) 3.7–7.4 6.0 ± 0.8 Sharp-tailed Streamcreeper (Lochmias nematura) 1 (15) -- 2.2 Lesser Woodcreeper (Xiphorhynchus fuscus) 5 (9.6; 5–13) 2.0–4.1 3.3 ± 0.4 Scaled Woodcreeper (Lepidocolaptes squamatus) 8 (9.2; 5–12) 0.7–5.2 2.2 ± 0.5 Black-billed Scythebill (Campylorhamphus falcularius) 5 (9; 3–16) 1.0–4.1 2.8 ± 0.5 Greenish Elaenia (Myiopagis viridicata) 6 (4.6; 3–8) 0.3–1.0 0.5 ± 0.1 Gray Elaenia (Myiopagis caniceps) 3 (7.8; 5–12) 2.0–4.1 3.0 ± 0.6 Sepia-capped Flycatcher (Leptopogon amaurocephalus) 10 (13.5; 9–27) 0.9–3.7 2.3 ± 0.3 Southern Antpipit (Corythopis delalandi) 15 (10.7; 6–19) 0.2–3.0 1.0 ± 0.2 Eared Pygmy-tyrant (Myiornis auricularis) 10 (9.2; 3–16) 0.4 –1.9 1.1 ± 0.2 Hangnest Tody-tyrant (Hemitriccus nidipendulus) 3 (7.5; 5–10) 0.3–0.7 0.5 ± 0.1 Yellow-lored Tody-flycatcher (To dirostrum poliocephalum) 8 (19.8; 16–26) 0.3–2.0 1.5 ± 0.2 Ochre-faced Tody-flycatcher (Poecilotriccus plumbeiceps) 2 (12.5; 10–15) 0.9–2.4 1.7 ± 0.8 Yellow-olive Flycatcher (Tolmomyias sulphurescens) 19 (18.3; 8–27) 0.7–2.9 1.6 ± 0.2 White-throated Spadebill (Platyrinchus mystaceus) 12 (15.1; 6–27) 1.2–2.9 2.0 ± 0.2 Euler's Flycatcher (Lathrotriccus euleri) 29 (13.3; 5–31) 0.2–2.0 0.9 ± 0.1 Gray-hooded Attila (Attila rufus) 2 (18.5; 11–26) 3.2–11.7 7.5 ± 4.3 Red-crowned Ant-tanager (Habia rubica) 3 (17.3; 13–21) 2.4–5.7 4.0 ± 1.0 TABLE 2. Territory sizes (ha) of birds at three Neotropical sites. Atlantic Forest birds are aligned at the left. a b c d Species Viçosa, Brazil Peru Panama Manaus, Brazil Baryphthengus ruficapillus 3.4 B. martii 5–8 Mackenziaena severa 6.6 Thamnophilus caerulescens 1.3 T. aethiops 10 T. schistaceus 8 T. atrinucha 1 T. murinus 5.6 Dysithamnus mentalis 0.9 D. puncticeps <2 Formicivora serrana 1.0 Drymophila ferruginea 1.2 Pyriglena leucoptera 1.4 Conopophaga lineata 0.6 C. aurita 6.3 Synallaxis cinerascens 2.1 S. ruficapilla 1.6 Anabazenops fuscus 3.3 Automolus leucophthalmus 5.4 A. infuscatus 12 10.6 A. ochrolaemus 11 11 A. rubiginosus 13.3 Xenops rutilans 6.0 X. minutus 9 5 13.3 Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini a b c d Species Viçosa, Brazil Peru Panama Manaus, Brazil Lochmias nematura 2.2 Xiphorhynchus fuscus 3.3 X. pardalotus 10.6 Lepidocolaptes squamatus 2.2 L. albolineatus 14 12 Campyloramphus falcularius 2.8 C. procurvoides 24 Myiopagis viridicata 0.5 Myiopagis caniceps 3.0 5–8 6 M. gaimardii 4 5.6 Leptopogon amaurocephalus 2.3 3 Corythopis delalandi 1.0 C. torquata 6 5.7 Myiornis auricularis 1.1 M. ecaudatus 3 M. atricapillus 3 Hemitriccus nidipendulus 0.5 H. zosterops 3 3.9 Todirostrum poliocephalum 1.5 Todirostrum plumbeiceps 1.7 T. crysophataphum 7* Tolmomyias sulphurescens 1.6 T. assimilis 6 4 9.1 T. poliocephalus 56 Platyrinchus mystaceus 2.0 P. coronatus 5 6 3.8 P. platyrhynchos 55 Lathrotriccus euleri 0.9 5 Attila rufus 7.5 A. bolivianus 12 A. spadiceus 12816 Habia rubica 46 H. fuscicauda 25 Average 2.4 7.3 7.1 9.2 a b c d * This study. Territory sizes estimated for 100 ha. Terborgh et al. (1990). Robinson et al. (2000). Johnson et al. (2011). Robinson & Terborgh (1997). TABLE 3. Density of birds (pairs/100 ha) at five Neotropical sites. Atlantic Forest bir ds are aligned at the left. * – number of individuals. a b c d e f Species Atlantic Forest Peru Peru Guyana Manaus Panama Baryphthengus ruficapillus 15 B. martii 24 Mackenziaena severa 5 Thamnophilus caerulescens 42.5 T. aethiops 1 T. schistaceus 10.5 0.5–21 T. doliatus 38 T. murinus 7.75 12.5 T. amazonicus 4 T. punctatus 0.25 T. atrinucha 106 Dysithamnus mentalis 42.5 D. puncticeps 3.5 Formicivora serrana 2.5 Drymophila ferruginea 7.5 Pyriglena leucoptera 40 Conopophaga lineata 50 C. peruviana 3 C. aurita 12 Synallaxis cinerascens 17.5 S. ruficapilla 35 S. gujanensis 53 Anabazenops fuscus 22.5 Automolus leucophthalmus 7.5 A. infuscatus 1.5 4.75 7 A. ochrolaemus 2.5 2–3 1 5 A. rufipileatus 38 A. rubiginosus 1.5 Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini a b c d e f Species Atlantic Forest Peru Peru Guyana Manaus Panama Xenops rutilans 10 4 0.5–4 X. minutus 6 1.5–7.5 6.5 9 27 X. milleri 4.5 Lochmias nematura 2.5 Xiphorhynchus fuscus 12.5 X. pardalotus 18 Lepidocolaptes squamatus 20 L. albolineatus 510 Campyloramphus falcularius 12.5 C. trochilirostris 0.5 C. procurvoides 0.5–9 1.25 3 Myiopagis viridicata 15 5 Myiopagis caniceps 7.5 5 3 M. gaimardii 4 4–20.5 3.25 12.5 11.5 Leptopogon amaurocephalus 25 2.5 2.5–3 1 Corythopis delalandi 37.5 C. torquata 7 3.75 3.5 Myiornis auricularis 25 M. ecaudatus 10 10 4 6 M. atricapillus 3.5 Hemitriccus nidipendulus 7.5 H. zosterops 531 H. minor 6 H. josephinae 2 Todirostrum poliocephalum 20 Todirostrum plumbeiceps 5 T. crysophataphum 3.5 3.5–7.5 T. pictum 3.5 4 T. nigriceps 0.5 Tolmomyias sulphurescens 47.5 T. assimilis 4 4–15 2 17.5 15.5 T. poliocephalus 3 3–10 5 T. flaviventris 4.5–16 0.75 Platyrinchus mystaceus 30 4 P. coronatus 7.5 7.5 15 9.5 10 P. platyrhynchos 66 P. saturatus 53 Latrotriccus euleri 72.5 1.5 L. virescens 24* Attila rufus 5 A. bolivianus 4 4–14 A. spadiceus 4 2–4 4.5 3 7 Habia rubica 7.5 8.5 H. fuscicauda 3* Average 21.7 4.5 12.8 4.3 8.4 15.8 a b c d This study; density extrapolated for 100 ha from data in Table 1. Terborgh et al. (1990). Robinson & Terborgh (1997). Thiollay et al. (1994). e f Johnson et al. (2011). Robinson et al. (2000). > 6.0 0.5–2.0 2.1–4.0 4.1–6.0 Territory size (ha) FIGURE 2. Average territory sizes (ha) of birds at the Atlantic Forest (black bars), Panama (Robinson et al. 2000) (cross-hatched bars), Manaus (Johnson et al. 2011) (grey bars), and Peru (Terborgh et al. 1990) (white bars). Revista Brasileira de Ornitologia, 24(4), 2016 Number of species Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini DISCUSSION mapping is not clearly stated by them as the method used for deriving bird densities. However, their estimates are highly suggestive that the pattern we have found in Viçosa Small territory sizes (< 5 ha) were common among insectivorous birds in the secondary Atlantic Forest can occur also in pristine areas of the Atlantic Forest. It fragment that we studied. Similarly, other species of should be noted, though, that although a small number insectivorous birds found in forested habitats in the Atlantic of large territories in an area often demonstrates low bird density, species with small territories that do not occupy Forest Biome are known to occupy small territories and most of the available habitat also have low densities, as occur at high densities, including, Flavescent Warblers (Basileuterus flaveo lus, 2 ha; Duca & Marini 2005), have been shown for birds with patchy distribution in Variable Antshrikes (Thamnophilus caerulescens, 0.9 ha), primary forests in French Guyana (Thiollay 1994). Plain Antvireos (Dysithamnus mentalis, 0.7 ha), White- The average density at our study site (22 pairs/100 ha) was higher than that for congeneric birds in Guiana shouldered Fire-eyes (Pyriglena leucoptera, 1.4 ha) (Duca (average density = 4.1 pairs/100 ha, Thiollay 1994), et al. 2006), and Black-cheecked Gnateater (Conopophaga melanops, 2.94 ha; Lima & Roper 2009). In addition, Manaus (average density = 8.4 pairs/100 ha, Johnson et the territory sizes of six species of Thamnophilidae in São al. 2011), and the two Peruvian sites (average density = Paulo varied from 0.8 to 3.0 ha (Willis & Oniki 2001). 4.5 pairs/100 ha, Terborgh et al. 1990; average density =12.8 pairs/100 ha, Robinson and Terborgh 1997) As ours, all the above studies, carried out in the Atlantic (Table 3). In Panama the density of 15.7 birds/100 ha Forest, have been conducted in areas that altered by human activities in the past and, thus, had a vegetation was inflated by a very high density of 106 pairs/100 structure similar to that of our study area, although the ha of the hyper-abundant Black-crowned Antshrike understory of the area studied by Duca et al. (2006) was (Thamnophilus atrinucha) which represented almost 50% of all individual birds reported by Robinson et al. (2000). more open because the forest was older (> 150 years) than It should be noted, however, that when compared to ours (c. 50 years). When we compare species among other Neotropical South American forest bird communities, those in Central biomes, the average territory size at our study site (2.4 America have lower species richness, and this could result ha) was smaller than that of congeneric birds in Panama in higher densities of some populations such as at the more disturbed secondary forest in Panama (Robinson (average size = 7.1 ha, Robinson et al. 2000), Peru (average et al. 2000), similarly to our results and to those at size = 7.4 ha, Terborgh et al. 1990), and Manaus (average size = 9.0 ha, Johnson et al. 2011). When comparing successional vegetation in Peru (Robinson & Terborgh congeneric similarly-sized species, 9 of the 11 species in 1997). Only four of the 16 species compared in Panama Panama (Robinson et al. 2000) and all the 20 species in (Robinson et al. 2000) and four of the 18 species in Peru (Robinson & Terborgh 1997) had higher densities than Peru (Terborgh et al. 1990) had larger territories than those in Viçosa. Also, in an additional study conducted those from our Atlantic Forest plot. In Manaus, Stouffer (2007) have found the territories of Conopophaga aurita near Manaus, Amazonia (Stouffer 2007), territories were and Corythopis torquatus were 2 to about 6 times larger larger (average of 13 ha) and densities were lower (average than we found for C. lineata and C. delalandi at MP, of 3.4 pairs/100 ha) than those of Atlantic Forest birds. One important difference among the Neotropical respectively. studies compared here is the successional stage of the As territory sizes were small at our grid, bird densities at MP were high. In their study comparing bird densities forest. The lowest bird densities and larger territory sizes in 5000 ha tract of Atlantic Forest that suffered selective were found in the sites with old-growth primary forest logging 25 years before their study, in Paraguay, Cockle in Peru (Terborgh et al. 1990), Guyana (Thiollay 1994), and Manaus (Johnson et al. 2011). The other study site et al. (2005) applied territory mapping “where possible”. in Peru had an intermediate average density value and They also have found high densities of territories/100 ha for some of the same species that we studied in Viçosa: was carried out along a primary successional gradient Eared Pygmy-tyrant, Myiornis auricularis (c. 68 territories), (Robinson & Terborgh 1997). The second highest bird Rufous-capped Spinetail, Synallaxis ruficapilla ( c. 24 density was observed in Panama (Robinson et al. 2000), at a site of primary forest with plenty of gaps created by territories), Eared Pygmy-tyrant, Myiornis auricularis natural treefalls and storms. All the Atlantic Forest sites (c. 40 territories), Euler's Flycatcher, Lathrotriccus euleri, Gray-bellied Spinetail, Synallaxis cinerascens, have secondary or selectively logged forests, often with White-throated Spadebill, Platyrinchus mystaceus, Plain dense understory. Antvireo, Dysithamnus mentalis and Variable Antshrike, Younger successional vegetation stages have higher productivity allowing higher bird density (Robinson Thamnophilus caerulescens (all t hese five species with c. 10– & Terborgh 1997, Aleixo 1999). Birds density and 20 territories each). These authors have not obtained their data from a grid in the forest area sampled and territory territory size in our study site could be a response to a Revista Brasileira de Ornitologia, 24(4), 2016 Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil Rômulo Ribon and Miguel Â. Marini denser understory and, consequently, a higher abundance the Atlantic Forest to date. Our estimates might be useful of leaves and insects, as indicated by species-specific to future conservation and management studies in the (Bechard 1982, Hunt 1996) or community (Robinson biome. However, a comprehensive determination and & Terborgh 1997, Casenave et al. 1998) studies. In fact, explanation for this proposed pattern in the biome awaits studies conducted in secondary forests in Amazonia further tests. have shown that territory sizes of birds in these habitats are indeed smaller, and bird density higher, than in the ACKNOWLEDGEMENTS primary forests (Kratter 1997, Robinson & Terborgh 1997, Kattan & Beltran 2002). We thank CAPES, CNPq, Programa de Pós-graduação Density compensation, a phenomenon originally em Ecologia, Conservação e Manejo de Fauna Silvestre of described for groups of islands (MacArthur et al. 1972, the Universidade Federal de Minas Gerais, Programa Connor et al. 2000), could be occurring in the small Nacional de Biodiversidade/Ministério do Meio Ambiente/ forest fragments such as MP. Density compensation Banco Interamericano de Desenvolvimento (PROBIO/ results in higher density for those bird species able to MMA/BIRD), Programa Natureza e Sociedade WWF/ colonize islands because of the lack of many species that SUNY (Project CSR 142-00), PROBIO-MMA/GEF/ cannot reach them. The lack of many species would BM (Project Efeitos Espaciais e Temporais da Fragmentação thus trigger “competitor release” and “predator release”, de Hábitats sobre Populações de Insetos e Pássaros), allowing wider niches and much higher densities than in Departamento de Engenharia Florestal (UFV) for the mainland (Stamps & Buechner 1985, Connor et al. financial support. Serra do Cipó National Park (ICMBio) 2000). Although density compensation does not always provided facilities for data analysis. The following helped happens (Connor et al. 2000) it could help to explain the in several stages of the study: E. R. Luiz, A. B. Andrade, territory patterns of the Viçosa region since we studied A. C. Ottoni, F. Stanciola, S. L. Ribeiro (in memorian), territories in a relatively small forest fragment (roughly N. R. Neves, E. C. A. Nieto, H. C. Sari, S. D. Souza, 380 ha) from where several birds have already gone extinct R. F. Fadini. The late C. Bibb y helped to solve doubts (Ribon et al. 2003). The extirpation of species with niches during territory mapping analysis. We appreciate the similar to those that persisted in our area could make it improvements in English usage made by Chandler possible for them to expand their use of resources and Robbins through the Association of Field Ornithologists' achieve higher densities and smaller territories. program of editorial assistance. Two anonymous reviewers Even though territory sizes and bird densities are greatly improved the manuscript. similar among our study and the few other available studies on Atlantic Forest birds, these results should not be generalized to the biome. This is not only because REFERENCES there are many different vegetation subtypes to be studied (e.g. lowland vs. submontane vs. montane forests; Aleixo, A. 1999. Effects of selective logging on a bird community in southern vs. central vs. northeastern forests; old growth the Brazilian Atlantic Forest. 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Journal

Ornithology Research – Springer Journals

Published: Dec 1, 2016

Keywords: density compensation; fragmentation; Minas Gerais; Neotropical; secondary forests; territoriality

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