Bird communities in two fragments of Cerrado in Itirapina , Brazil

The Cerrado domain is a mosaic of vegetation types at the local scale, and this environmental heterogeneity leads to high regional bird diversity. Therefore, we aimed to survey quantitative and qualitatively the bird fauna of two fragments of Cerrado and to compare them with an adjacent protected area (Estação Ecológica de Itirapina), in order to assess the heterogeneity of bird diversity in the region. The present study was conducted during 12 months from October 2006 to September 2007 in the municipality of Itirapina, Southeastern Brazil. Altogether we recorded 210 bird species. Fifty-six of them had never been detected in Estação Ecológica de Itirapina, and eleven species are new records for the whole Itirapina region. The list also includes six species that are endangered in Sao Paulo State and five endemic species of the Cerrado domain. Most species were recorded in less than 50% of the visits and exhibited low relative abundance. Primarily insectivorous species were the most common, followed by omnivores. Frugivorous birds were poorly represented. Carnivores were more abundant than usually observed in fragments. The similarity among fragments was higher than between fragments and the protected area. Considering the vegetation heterogeneity in the Cerrado domain, our results reinforce the importance of conserving fragments in order to sample this diversity.


Introduction
Detecting environmental quality and monitoring biodiversity is important for the conservation of natural areas.In that sense, bird inventories are commonly used for this purpose (Vielliard, 2000;Marini, 2001;Antunes, 2005;Piratelli et al., 2008).Conservation strategies of natural areas require knowledge on the distribution and abundance of species, and studies on bird communities can provide suitable data (Naeve et al., 1996).
Studies on Cerrado demonstrate high biodiversity (Klink and Machado, 2005).The domain is formed of a mosaic of different vegetation forms that varies from grasslands ('campo limpo') to forests ('cerradão'), including gallery forests (Coutinho, 2006).This environmental heterogeneity is important to keep high levels of species richness and endemic species (Machado et al., 2004).However, the Cerrado is one of the world's threatened biodiversity hotspots (Myers et al., 2000).About 60% of its vegetation has already been removed (Machado et al., 2004) and the remaining areas are isolated in forest fragments (Durigan et al., 2007).
While grasslands are predominant in EEI (Motta-Junior et al., 2008;Granzinolli, 2009) more forested areas prevail in these two fragments.Therefore, this paper aimed to accomplish qualitative and quantitative bird surveys of the two fragments, as well as to compare the results with those from EEI.Such outcomes could be used in future wildlife monitoring and to better understand the influence of fragmentation on bird communities (Palmer et al., 2008).This study also proposes some local management strategies for biodiversity conservation.

Study area
We have studied two fragments: A (22° 13' S and 47° 48' W) and B (22° 14' S and 47° 49' W), inside the Estação Experimental de Itirapina.This area is basically used for the extraction of Eucalyptus spp.(Myrtaceae) and resin from Pinus spp.(Pinacea).Fragment A, of 150 ha, is composed predominantly of 'cerrado sensu stricto', 'cerradão' (a tall woodland) and gallery forest (Delgado et al., 2004).Fragment B, of 350 ha, is more heterogeneous, concerning the vegetation.It is a more forested fragment than A, being composed of 'cerradão', 'cerrado sensu stricto', gallery forests (Delgado et al., 2004), Eucalyptus spp. with native understory and regeneration areas with native and exotic species (pers.obs.).Fragments A and B are about 1.5 km and 2 km, respectively, distant from EEI, that is of 2,300 ha.Both fragments are surrounded by pine and eucalyptus plantations and are 750 m apart from each other.
Itirapina region has a Cwa climate according to the Köppen system (Zanchetta, 2006), with annual rainfall average of 1,459 mm.The rainy season is usually from October to March and the dry period occurs from April to September.The average annual temperature is 21.9 °C.The hottest months are January and February and the coolest, June and July.The altitude of the region is about 740 m (Zanchetta, 2006).

Methods
Qualitative and quantitative methods were performed.The qualitative survey was done to generate the fullest species list possible that occur in the area (Vielliard and Silva, 1990) and was conducted during 12 months (October 2006to September 2007).For this purpose we walked on pre-existent tracks during mornings (6:00 to 11:00 AM), evenings (3:00 to 6:00 PM) and nights (6:00 to 9:00 PM) recording all bird species, through auditory and/or visual contacts, without standardising the vegetation types.Sampling effort during the qualitative survey in fragment B (61 visits) was higher than in fragment A (30 visits) because of its size and vegetation heterogeneity.Rarefaction curves were plotted using the statistical package EstimateS 8.0 (Colwell, 2006).The same program was used to estimate fragment richness using the first-order Jackknife richness estimator (Heltshe and Forrester, 1983).Species composition in the fragments, compared with that from EEI, was analysed using Jaccard's similarity index (Krebs, 1999).Bird lists from EEI were extracted from data review by Motta-Junior et al. (2008).Species frequency of occurrence (FO) was calculated from Vielliard and Silva (1990) and the analysis of trophic structure was done using species groups based on Motta-Junior (1990) and Sick (1997).
The quantitative survey was also carried out over 12 months (October 2006 to September 2007) using the point counts method, developed by Blondel et al. (1970) and adapted by Vielliard and Silva (1990) for Neotropical studies.For this purpose, 18 sampling points were chosen in each fragment in pre-existing tracks, each containing four or five points, with the minimum distance of 200 m from each other (Vielliard and Silva, 1990).In each of these sampling places all auditory and/or visual contacts with individuals within a 100 m range were recorded over 20 minutes.Points were visited during morning (6:00 to 11:00 PM), starting minutes before sunrise.On each day, eight to ten random points were visited in each fragment, totalising 216 samples in each area (18 points visited for 12 months).

Results
During the qualitative survey, 210 species of birds distributed in 51 families, were recorded (see Table 1).In 91 days of field visits (476 hours of observation) 158 species in the fragment A and 201 in B were recorded (see Table 1).First-order Jackknife estimated a richness of 186 ± 7.22 species to fragment A and 223.61 ± 5.3 species to fragment B. Rarefaction curves from both fragments indicate a similar pattern (see Figures 1 and 2).The similarity among species composition of fragments was 70.95%, while the similarity between fragments and EEI was 53.66%.
Species frequency of occurrence ranged from 3.1% (one contact) to 96.9% (31 contacts) in fragment A and 1.5% (one contact) to 90.8% (59 contacts) in B (see Table 1).In both fragments, most of the species were recorded in up to 50% of the field visits (see Table 2), namely 119 species in A (75.3% of the total recorded in the fragment) and 158 species in B (78.61%), however some species were recorded in only one visit.This occurred with 30 species (18.9%) in A and 22 (13.92%) in B. Species with frequency of occurrence over 75% were considered residents in the studied areas (Almeida et al., 1999).This frequency was 19 species (12.03%) for fragment A and 14 species (6.97%) for B (see Table 1).
In both fragments, results were similar in relation to the distribution of trophic categories (see Table 3).Predominantly insectivorous birds were more representative both in A and B (49.37 and 48.26% respectively), followed by predominantly omnivorous (17.72 and 16.42%, respectively).The other categories, in order of prevalence piscivores, detritivores, malacophages, carnivores, nectarivores and gramnivores -were poorly represented and together summed only 27.21% of birds in fragment A and 29.36% in B. The predominantly frugivorous birds were represented by only 5.70% of species in A and 5.97% in B.
During quantitative surveys, 111 species of birds in A and 120 in B were recorded, in 3,647 and 3,474 contacts, respectively (see Table 1).PIA ranged from 0.005 (one contact) to 1.282 (277 contacts) in A and 0.005 (one contact) to 1.023 (221 contacts) in B (see Figures 3 and 4).In A, 26 species (23.42% of the total registered during quantitative survey) had PIA values lower than 0.019 (less than four contacts), and the same occurred with 36 species (29.75%) in B, where values lower than 0.014 represent less than three contacts.
Lower similarity between fragments and EEI, compared to the similarity among fragments, may be related to size and vegetation differences among areas and also the presence of a large number of exclusive bird species in each one of them.The fragments have 56 exclusive species, which happens to 77 species recorded only in EEI.Belonging to this group of birds apparently sensitive to environmental changes, there is a group that includes endemic species to the Cerrado and/or threatened ones, occurring in more open vegetation forms, as Rhea americana, Culicivora caudacuta, Alectrurus tricolor and Polystictus pectoralis.Differences between study duration, frequency of visits and sampling method may also explain the disparity of results.For example Willis's survey (2004) was conducted over 21 years in contrast to the 12 months of this study.

Frequency of occurrence
The high percentage of species with low FO is commonly found in other studies (Almeida et al., 1999;Donatelli et al., 2007).Almeida et al. (1999) attribute the results to the occurrence of wandering, occasional or migratory species.Concerning the fragments studied, especially due to the considerable species number recorded in up to 25% of visits, this explanation can be attributed to some groups, such as diurnal raptors, represented by nine of the 11 species with low frequency in A and 13 of the 14 species in B. Low FO values can also be related to the reduced detection of certain species.This was true to some hummingbird species: nine of the 11 species showed low frequencies (seven species with up to 25% of frequency) in fragment A and the same happened with 13 of the 14 species recorded (9 species below 25% of frequency) in B. Species with inconspicuous vocalisations (Conirostrum speciosum, Eucometis penicillata, Piranga flava and Nemosia pileata) and/or which were recorded in low relative abundance in study areas (Penelope superciliaris, Piaya cayana and Tapera naevia) may also explain these results (Aleixo and Vielliard, 1995).Only 26 species (see Table 1) are resident (FO values higher than 75%, according to Almeida et al., 1999) to the studied areas and ten of them occur in both fragments.Turdus leucomelas, Pitangus sulphuratus, Patagioenas picazuro, Cyclarhis gujanesis and Zonotrichia capensis can be included in this group because they are species adapted to disturbed registered species (Chiroxiphia caudata and Habia rubica) are bioindicators (Piratelli et al., 2008).According to these authors, both species have some ecological characteristics (e.g.needs for nesting and foraging in mixed flocks) that lead them to prefer less altered areas.
Some species (n = 56) had never been registered in EEI (review by Motta-Junior et al., 2008) (see Table 1), but one (Leucochloris albicollis) had already been registered during a brief visit to fragment B (Willis and Oniki, 2003).This number represents a considerable increase to the bird list for the protected areas (EEI and Estação Experimental de Itirapina), now with a total of 287 species.Some species may not have been previously recorded as they are difficult to detect or even occur in the region in low relative abundance (low FO and/or low PIA values).This is the case, for example, of the five records of hummingbirds (Anthracothorax nigricollis, Thalurania glaucopis, Hylocharis sapphirina, Heliomaster squamosus, Calliphlox amethystina).
However, some of the new species recorded were found only in forested habitats, which are scarce in EEI (Granzinolli, 2009) and very important for birds in Cerrado (Piratelli and Blake, 2006).These species possibly would not be detected in more open vegetation areas, which prevail in EEI.In this group there are thirteen Atlantic Forest endemics (Brooks et al., 1999) (see Table 1).There were also, while not restricted, other species associated with forest habitats (Sick, 1997), like Eucometis penicillata, Habia rubica, Leptopogon amaurocephalus and Pachyramphus polychopterus.These results reinforce the importance of keeping forest fragments and environmental heterogeneity for the conservation of local biodiversity, especially for Cerrado.This contributes to bird conservation in a landscape scale (Bakker et al., 2002).
Within the list, there are eleven species (see Table 1) registered for the first time for the whole Itirapina region (Willis, 2003a;Willis and Oniki, 2003;Motta-Junior et al., 2008): Rostramus sociabilis, Micrastur semitorquatus, Leptotila rufaxilla, Hylocharis sapphirina, Elaenia spectabilis, Legatus leucophaius, Pachyramphus castaneus, Cantorchilus leucotis, Polioptila dumicola, Eucometis penicillata and Haplospiza unicolor.Even when a specific area is visited for a long time, recording new species is common in bird surveys, as shown by some other authors (Rodrigues et al., 2005;Motta-Junior et al., 2008).Despite the intensive sampling effort, rarefaction curves did not stabilize (see Figures 1 and 2).Jackknife estimator data indicate that bird richness is probably higher than observed for both studied areas.In light of that, new visits to the fragments are likely to allow for additional records.

Similarities among areas
The similarity among bird communities of fragments is probably explained by the similarities in vegetation and proximity between areas, which may favour the displacement of individuals.The matrix can also play an important role, since the occurrence of a similar matrix in distinct areas selects similar communities (Sisk et al., 1997).In addition, a considerable portion of the species common to both areas is often found in forest fragments  areas and also occurred in high frequencies in other studies (Donatelli et al., 2007).

Trophic categories
Almost 50% of registered species were classified as predominantly insectivores and omnivores represented just over 15% of species (see Table 3).The percentage of birds considered frugivores was low for both fragments, corroborating studies conducted in fragments in Sao Paulo State (Motta-Junior, 1990;Manica et al., 2010).Frugivores are among the most sensitive groups to forest fragmentation (Willis, 1979) because they need large areas to reach their food needs (Pizo, 2001).The higher percentage of predominantly insectivorous birds was also recorded by Motta-Junior (1990), Donatelli et al. (2004Donatelli et al. ( , 2007)); and Manica et al. (2010).However Motta-Junior (1990) and Donatelli et al. (2007) found frugivores as the second more representative category.Omnivores were more abundant than frugivores, as observed in Motta-Junior (1990) andManica et al. (2010) and this appears to be a common pattern in fragments (Willis, 1979).Apparently, a more varied diet (e.g.omnivory) tends to be favoured in disturbed environments.
Although with low values, the importance of carnivores in both fragments was high when compared to other studies (Motta-Junior, 1990;Donatelli et al., 2007;Manica et al., 2010).Raptor birds have a large range (Del Hoyo et al., 1994) and probably the proximity to EEI allowed the record of most species.Therefore, these birds must use both Itirapina protected areas, which again highlight the importance of the fragments to the local avifauna.The presence of 17 carnivore species in the fragments can indicate its quality.They are top predators (Sick, 1997) and thus need a structured environment, concerning trophic chains.
Gramnivores were ranked in the fourth position, probably because both fragments have large amounts of exotic herbaceous species, used by these birds (pers.obs).Nectarivores occupied the fifth place, which can be partially attributed to the presence of Pyrostegia venusta (Ker Gawl.)Miers (Bignoniaceae), which produces flowers visited by this category (hummingbirds, mainly).However, the importance of this plant species for nectarivorous birds must be observed in other areas.Flowers of Eucalyptus spp.were also apparently important for these birds, but also requires more observations, although Willis (2002Willis ( , 2003b) ) has already reported the importance of the resource.Nectarivores are important in natural areas because some species are flower pollinators.Impacts on pollinator populations can affect all communities' structure (Murcia, 1996).

Ponctual index of abundance
For the PIA values, a pattern similar to other studies that have used the same methodological standards (e.g.time in each sampling point) was observed (Vielliard and Silva, 1990;Aleixo and Vielliard, 1995;Almeida et al., 1999).The results indicated the presence of few species with high values and many species with medium to low values.Some birds had high and similar values in both fragments, such as Patagioenas picazuro, Tangara cayana, Cyclarhis gujanensis, Turdus leucomelas, Thraupis sayaca and Pitangus sulphuratus, common species in disturbed environments (Sick, 1997) and with long or constant vocalisation scope (Almeida et al., 1999).The PIA of P. picazuro was higher than 1.0, data also found by Almeida et al. (1999) and Donatelli et al. (2007).This species has been expanding in Sao Paulo State, aided by deforestation (Willis and Oniki, 1987) and is currently one of the most common birds in eastern Brazil (Oniki and Willis, 2000).There is difference in PIA values of some species when the fragments are compared (see Table 1).This is the case, for example, of Tolmomyias sulphurescens, Thamnophilus caerulescens, Euphonia chlorotica, Turdus rufiventris, Conopophaga lineata and Lathrotriccus euleri, which occurred in higher relative abundance in B, and to Coryphospingus cucullatus, Casiornis rufa, Colaptes campestris, Synallaxis frontalis and Tyrannus savanna, which occurred at higher relative abundance in A. These differences may be related to the occurrence of certain birds in forest vegetation areas, which occur in B, and species associated with more open environments, such as those with highest relative abundance in A. This highlights the importance of keeping the Cerrado mosaic, since species are related to certain vegetation types (Boecklen, 1986).

Final Considerations and Recommendations
To improve the quality of the studied areas, this paper suggests the establishment of an ecological corridor between fragments, given the short distance that separates them, and the similarity among bird communities.It includes the use of native plant species that produce fruits.Frugivorous birds, including the largest ones, still occur within Sao Paulo State, but they need large areas to reach their food needs.So, in addition to these corridors between fragments, it could also attract frugivorous bird species, currently rare, to these fragments.Moreover, these fragments can act as a damping area to the Estação Ecológica de Itirapina, reducing the disruption in this area.
This paper also proposes discussing the withdrawal of native understory in Pinus spp.plantation, used by birds.Certain areas of forest adjacent to the fragments show native understory which is, at least apparently, important for certain bird populations.The testing of this hypothesis is therefore suggested.In case of positive results, lack of removal of native vegetation can be a simple way of management in areas of planting pine species.

Conclusion
Our results reinforce the importance of forest fragments for certain populations of birds and therefore for the conservation of birds locally.Environmental heterogeneity is an important factor for the conservation of biodiversity and therefore, is essential to the maintenance of forest fragments in areas of activities affecting the soil cover.Moreover, the results also highlight that forest fragments are important to research, since they contribute to understanding species distribution on a landscape scale, providing data for management strategies.

Figure 2 .
Figure 2. Rarefaction curve from fragment B during the qualitative survey conducted between October 2006 and September 2007 in Itirapina, Sao Paulo State, Brazil.

Figure 1 .
Figure 1.Rarefaction curve from fragment A during the qualitative survey conducted between October 2006 and September 2007 in Itirapina, Sao Paulo State, Brazil.

Figure 3 .
Figure 3. Ponctual Index of Abundance (PIA) in descending order of the bird species recorded during the quantitative survey conducted between October 2006 and September 2007 in fragment A in Itirapina, Sao Paulo State, Brazil.

Figure 4 .
Figure 4. Ponctual Index of Abundance (PIA) in descending order of the bird species recorded during the quantitative survey conducted between October 2006 and September 2007 in fragment B in Itirapina, Sao Paulo State, Brazil.

Table 2 .
Frequency of occurrence (FO) classes percentage of bird species in fragments A and B, Itirapina, Sao Paulo State, during 91 visits to areas in 12 months of study (October 2006 to September 2007).

Table 3 .
Number of species and relative percentage of nine trophic categories to the fragments studied (A and B) and analysed