Bird richness and composition in a Cerrado fragment in the State of São Paulo

Bird species richness is an important measure for monitoring biodiversity changes. We analysed avifauna richness and composition in a 472 ha protected cerrado fragment and surroundings at Fazenda Canchim (RL-CPPSE), São Carlos, in the State of São Paulo (SP). We carried out 95.1 hours of observation (22 visits) at irregular intervals from May 2004 to December 2006. Qualitative surveys were done walking through tracks inside the fragment and on the roads at its edge. We recorded 160 species, six of which were endemic to Cerrado domain, 22 migratory, seven threatened within the State of São Paulo, and two globally threatened. We found 28 species in the cerradão, 110 in the cerrado sensu stricto, 13 in the gallery forest, 26 in the reservoir border, 26 in pasturelands and sugar cane monoculture and 55 in an anthropic area. Most of the species had low frequency of occurrence in all vegetation forms. Insectivores were the major trophic category (46.9%), which is typical in tropical regions, and it is also related to resource availability. Omnivores followed with 19.4%, granivores with 8.8% and frugivores with 7.5%. We conclude that, despite its size and conservation status, our study area has a remarkable bird community and must be considered as a priority conservation area to preserve bird species in Sao Paulo State.


Introduction
Bird species richness is an important measure for monitoring biodiversity changes (Andrén, 1994;Palmer et al., 2008).Bird community inventories, censuses and surveys provide data of great value for conservation purposes (e.g.Tubelis et al., 2004;Marini and Garcia, 2005;Silva, 1997).For instance, these methods allow the recognition of endemic, threatened, keystone, umbrella or surrogate group of species.Because of their restricted distribution, vulnerability, high influence on other species occurrence or important ecological role in ecosystems, registration of these species might strongly influence priority activities in the protection of the natural environment (Stotz et al., 1996;Silva andBates 2002, Loyola et al., 2007;Pinto et al., 2008, Piratelli et al., 2008).
The study of bird species richness also improves the knowledge of community responses in disturbed areas, because richness may be reduced in long-time isolated fragments (Aleixo and Vielliard, 1995;Marini, 2001;Stouffer and Bierregaard, 1995).Small remnants are prone to edge effects, such as nest predation increase (Marini et al., 1995), attraction of exotic predators, diseases and competitors or migratory and dispersal route obstructions (review in Marzluff and Ewing, 2001).All these factors may affect individual chances of reproduction and reduce local species richness (Andrén, 1994).
In addition, bird richness and composition offers valuable data to understand sensitivity and resistance of species to fragmentation (Zanette et al., 2000).Speciesspecific responses to fragmentation are widely diverse among birds (Debinski and Holt, 2000;Watson et al., 2005).For example, local migratory birds and species that need specific nest sites may require extensive areas to find environmental conditions to survive and breed (Sick, 1997).Furthermore, fragmentation may influence the trophic structure of bird communities (Motta-Junior, 1990;Tubelis and Cavalcanti, 2000).For example, specialist groups, such as understory insectivores, are negatively affected in fragmented landscapes because of the reduced suitable pathways connecting multiple foraging areas (Martensen et al., 2008).
Agriculture and pastureland expansions in the Cerrado domain -one of the global biodiversity hotspots (Myers et al., 2000) -have been the major threatening factors to its avifauna biodiversity since the 1970s (Alho and Martins, 1995;Cavalcanti and Joly, 2002).The Cerrado domain has 837 bird species (Silva, 1995), from which 90.7% breed within the domain and the others migrate from the Northern Hemisphere, southern South America and southeast Brazil (Silva, 1995;1997).Endemism in the region is high, but almost 75% of endemic cerrado avifauna is considered at risk (Stotz et al., 1996).Furthermore, although endemic bird areas occur in the Cerrado (Birdlife International, 2003), 20% of endemic and threatened species are outside protected areas (Machado et al., 2004).
In the State of São Paulo, the Cerrado has been reduced to less than 7% of its original cover for the last decades and only 18% of remnants are inside protected areas (São Paulo, 1999).Different from conservation areas of other domains, few Cerrado fragments are greater than 400 ha (Durigan et al., 2003).Considering the high level of degradation of the Cerrado in São Paulo, and regarding its boundary with the Atlantic Forest domain, these remnants should be concerned as important areas for conservation plans (Cavalcanti and Joly, 2002).
Even though some studies of bird communities have been previously carried out in São Paulo (Motta-Junior, 1990;Dias, 2000;Willis and Oniki, 2003;Willis, 2004;Develey et al., 2005;Willis, 2006;Motta-Junior et al., 2008), little is known about the ecology of bird communities in the region.Our aim was to contribute with the knowledge of the avifauna of one fragment in central São Paulo and give data support for future local or regional reaseaches.We studied bird species richness and composition, and identified endemic, threatened and migratory species of a protected cerrado fragment at Fazenda Canchim (RL-CPPSE), São Carlos, SP.

Material and Methods
Our study site is a 472 ha protected cerrado fragment at Fazenda Canchim (Reserva Legal-Embrapa Pecuária Sudeste, RL-CPPSE) and its surroundings, 12 km from São Carlos, in the State of São Paulo (SP) (21° 55' S and 47° 48' W) (Primavesi et al., 1999).This is a transition zone from the Atlantic Forest to Cerrado domain, also characterised as an ecological tension zone, and with a high level of biodiversity (Primavesi et al., 1999).The climate is typical of moist savanna (Cwa, according to Köppen's classification), with a remarkable seasonality: a dry and cold winter from April to September and a wet and warmer summer from October to March (Primavesi et al., 1999).
The reserve is covered by two cerrado physiognomies: cerrado sensu stricto (340 ha), a typical savanna vegetation, and cerradão (130 ha), an almost closed woodland.A gallery forest (1.35 ha) occurs along a stream (Córrego da Lagoa) inside the fragment.The surroundings are composed of a reservoir (Represa do 29) in the north-east of the reserve and between cerrado sensu stricto and a small village; a 120 ha cerrado fragment in the east; pasturelands in the south and south-east and sugar cane monoculture in the north and west of the reserve (Primavesi et al., 1999).
We did qualitative surveys during mornings, from 06:00 to 11:00 AM, and late-afternoon, from 03:00 to 06:00 PM, in 95.1 hours of observation in irregular intervals from 2004 to 2006.The area was visited 22 times: six in 2004 (May, August, November and December), 14 in 2005 (from January to December, except in March, July and August) and two in 2006 (January and December).We sampled all vegetation forms described above walking through 15 km trails or roads, approximately: 1) 3.8 km trail inside the fragment (1.55 km in cerrado sensu stricto, 1.25 km in gallery forest and 1 km in cerradão); 2) 2 km road in the middle of the reserve through cerrado sensu stricto; 3) 6 km road in the northwest edge of the reserve between cerrado sensu stricto and sugar cane monoculture; 4) 2 km road between cerrado sensu stricto and the reservoir, 5) 1.11 km road in the south-east edge of the reserve between cerradão and pastureland and 6) 1 km road that surrounds a small village.We often visited one or more vegetation forms during a single visit.We sampled cerradão on seven visits, cerrado sensu stricto on 22, gallery forest on 10, reservoir border on 14 and anthropic areas on 21.
We used 8 × 40 binoculars for bird identification, and pictures or vocalisation records for comparison and identification according to literature (Meyer de Schauensee, 1982;Sick, 1997;Souza, 1998;Develey and Endrigo, 2004) and to Manoel M. Dias' identification.We carried out a non-standardised method of observation, because our aim was to identify as many individuals as possible.Bird nomenclature follows Comitê Brasileiro de Registros Ornitológicos (2007).Bird species endemic to Cerrado were classified following Silva and Bates (2002), and migratory birds according to Willis (1979), Motta-Junior (1990) andSick (1997).We identified threatened species from official lists [São Paulo, 2008; Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA), 2003; International Union for Conservation of Nature and Natural Resources (IUCN), 2007].We measured the frequency of occurrence (FO) for each spe-cies in each vegetation form, because sample effort was different among them.We calculated FO dividing the total number of records of each species by the total number of visits to each area (Vielliard and Silva, 1990;Aleixo and Vielliard, 1995).Also, we classified species into nine trophic categories according to their principal feeding habits: nectarivores (NEC), carrion-eaters (CAE), carnivores (CAR), frugivores (FRU), granivores (GRA), omnivores (ONI), insectivores (INS), piscivores (PIS) and herbivores (HER), following Motta-Junior (1990), Sick (1997), and also our field observations.
Most of the species had low FO values in all vegetation forms.In five of the six physiognomies, more than 90% of species were registered in less than 25% of the visits.Cerrado sensu stricto was the only one that presented almost 20% of bird species registered in 25.1 to 50% of the visits (Table 2).Insectivores were the major trophic category, followed by omnivores, granivores, piscivores, frugivores, carnivores, nectarivores, carrioneaters and herbivores (Table 3).

Species richness
We found 20.8% of São Paulo avifauna (770 species) (Willis and Oniki, 2003) and 19.1% of Cerrado domain (Silva, 1995).Our results denote that RL-CPPSE has representative species richness if compared with other studies, even though there are few bird studies in São Paulo's cerrado fragments.Twenty years ago, in 4 hours of observation, Willis and Oniki (2003) found 89 species at Fazenda Canchim, in cerrado fragment and semideciduous forest.Other previous studies found 214 bird species in the campus of the Universidade Federal de São Carlos in 9 years of study (Motta-Junior and Vasconcellos, 1996), 302 in Estações Ecológicas de Jataí e Experimental de Luis Antônio in 13 years (Dias, 2000), 231 in Estação Ecológica de Itirapina in 21 years (Willis, 2004) and in 9 years (Motta-Junior et al., 2008), 144 species in Parque Estadual de Vassununga in 1 year (Develey et al., 2005) and 158 and 201 species in two fragments in Estação Experimental de Itirapina in 15 months (Telles and Dias, 2010).In addition, it is important to notice that RL-CPPSE is one of the larger remnants in the region (Primavesi et al., 1999) and could be suitable as a natural corridor or habitat and food source for birds.

Endemic and threatened species
We found 20% (six species) of all endemic species to Cerrado (Silva and Bates 2002); four of them were threatened in São Paulo (São Paulo, 2008).We registered Charitospiza eucosma, which was also recorded at Estação Ecológica de Itirapina, SP (Motta-Junior et al., 2008).Even though this species has been considered as missing or critically endangered in the state (Willis, 2004;São Paulo, 2008), these recent records provide evidence that there are populations breeding within São Paulo.The few Charitospiza eucosma records have been related to habitat loss, since it usually occurs in natural open areas subjected to regular fires (e.g., open savannas) (Willis, 2004), which are now rarely found in the state (Durigan et al., 1987;2003).Furthermore, this species is considered high sensitive to habitat disturbance (Stotz et al., 1996).However, the lack of studies in cerrado fragments in the state may also contribute to C. eucosma threaten status.We suggest, then, more censuses and population monitoring should be conducted in these areas.
Among other endemic and threatened species in the state, we found Melanopareia torquata, which has been rarely studied (e.g.Tubelis and Cavalcanti, 2000).Recently, some population studies have been providing information about their breeding biology and ecology (Gressler and Marini, 2008;Kanegae et al., 2008).Although M. torquata is considered as medium-sensitive species to anthropic disturbance (Stotz et al., 1996), we suggest that it should receive high protection effort in São Paulo.Like M. torquata, A. flammeus is classified as endangered species in São Paulo (São Paulo, 2008).We registered this species only once, flying above pastureland with typical foraging.

Frequency of occurrence
We found low frequency of occurrence (FO) value for most species, which was also reported in other studies in fragments in São Paulo (Aleixo and Vielliard, 1995;Almeida et al., 1999;Donatelli et al. 2007).Few records for species might occur because of the unusual exploitation of the area, for instance feeding habits in the area during a short period of time.Alternatively, migratory and occasional species (see above) or species not easy to detect, such as hummingbirds that are difficult to see or hear, could have also contributed to FO reduced values.We were unable to compare FO between vegetation forms, because the number of visits in each area was not similar.
Migrants that were found indicate this site as an important shelter and food source.We observed both short-and long-distance migratory species, such as Dendrocygna viduata and Tyrannus savana, respectively.However, we did not observe three migratory species, Amazonetta brasiliensis (Gmelin, 1789), Platalea ajaja Linnaeus, 1758 and Rynchops niger Linnaeus, 1758, which used to be observed in the region (Manoel M. Dias, pers. comm.).This may be caused by non-annual site use, to area isolation or to habitat quality decrease in the reserve in recent years.However, our irregular sampling method could also have failed to register more migrant species.

Bird species and vegetation forms
Inside the protected area of cerrado, we found 120 species, 75% of the total recorded.In the cerradão, we registered bird species with canopy foraging habits, such as Dryocopus lineatus, Conirostrum speciosum and Schistochlamys ruficapillus (Stotz et al., 1996).These species had also the highest FO at this habitat.In the cerrado sensu stricto, we found typical species of savanna or similar vegetation forms, e.g.Colaptes campestres, which uses terrestrial and canopy foraging strata, and Melanopareia torquata, with terrestrial and understory habits (Stotz et al., 1996;Sick, 1997).Species with the high FO in this physiognomy were Cyanocorax chrysops, Crypturellus parvirostris, Coryphospingus cuculatus, Thamnophilus doliatus and T. punctatus.In the gallery forest, Cantorchilus leucotis, Antilophia galeata and Basileuterus flaveolus were the most frequent species.Despite the small area of gallery forest, this vegetation type usually shows high biodiversity.Some birds might use different strata (e.g.B. flaveolus, B. leucophrys and B. hypoleucus, Marini and Cavalcanti, 1993) allowing an increase in species richness (Macedo, 2002).
We found 92 species in the surrounding area, including pasturelands, sugar cane monoculture, reservoir border and anthropic area.Ammodramus humeralis, Sicalis flaveola, S. luteola, Sporophila spp.and Volatinia jacarina were typical grassland species found in pastureland borders.Among non-Passeriformes species, Cariama cristata, Syrigma sibilatrix and Bubulcus ibis were frequently found in pasturelands.They are usually benefited by agriculture and pastureland occupation (Sick, 1997).For instance, Bubulcus ibis, was first registered in Brazil almost 40 years ago, and rapidly became abundant (Sick, 1997).Individuals of this species usually follow grazing cattle, improving their ability to find insects for feeding (Sick, 1997).
Swampy species were registered at the reservoir border, such as Certhiaxis cinnamomea, Chrysomus ruficapillus, Fluvicola nengeta and Himantopus melanura, which forage on wet ground.Aquatic species, which are highy dependent of water for fish, aquatic insects or mollusks food items availability, were commonly registered in the area.Ardea alba had the highest FO in this habitat (100%), followed by Mesembrinibis cayennensis (78.6%) and Jacana jacana (71.4%).We found a juvenile individual of Tigrisoma lineatum only once in the reservoir border, which indicates reproduction in the area.
In the anthropic area, including a small village, we frequently found many generalist species, like Pitangus sulphuratus and Furnarius rufus.Most Columbidae species are also highly adapted to anthropic areas and are easily found in these areas.Patagioenas picazuro, P. cayennensis and Zenaida auriculata were uncommon in São Paulo until the 1960's, but since then, they have become abundant in the state (Willis and Oniki 1987).The expansion of mechanical agriculture increases grain availability on the ground and therefore benefits these species' feeding behaviour (Willis and Oniki 1987)

Trophic categories
Species distribution in trophic categories follows similar results found in previous studies (Willis, 1979;Motta-Junior and Vasconcellos, 1996;Krügel and Anjos, 2000;Anjos, 2001;Tellino-Junior et al., 2005).Most species were insectivorous (46.9%), a typical pattern in tropical regions (Sick, 1997;Macedo, 2002), probably related to site resources availability.Omnivorous species followed in the rank (19.4%) and were also significant for the community composition.These species are expected to be less prejudiced in disturbed areas, because they have diverse diets (Willis, 1979;Motta-Junior, 1990).
Granivores were in third position in the categories rank.Such species records are probably related to pas-turelands and crop fields in the surrounding area that provide suitable foraging sites.Frugivores were fewer in number of species in our sample.However, we found small (Antilophia galeata), medium (Amazona aestiva) and large frugivores (Penelope superciliares and Ramphastos toco), which indicates the wide range of food item availability.This group is of great importance in natural area conservation, since it is strongly associated with seed dispersal and vegetation structure maintenance (Pizo, 2001).
Nectarivores were poorly represented in the bird community, and were composed almost entirely of hummingbird species.Most of these species are mutually related to some plant species, as well as frugivores, since they are pollinators.Seed production or germination of many plants species may be affected by the reduction of pollinators in fragmented areas (Murcia, 1996), which denotes the ecological importance of nectarivores.The category of Piscivores was mainly composed of Ardeidae species, which require aquatic environments for enough food availability (Sick, 1997).Therefore, on the RL-CPPSE boundary, Represa do 29 is a representative habitat for this group maintenance.Carnivorous species, such as hawks (Rupornis magnirostris) and owls (Tyto alba) registered in this study, are also critical for community dynamics, because they are top predators (Sick, 1997) and may control the population size of small animals.

Conclusion
We found remarkable data at RL-CPPSE, such as endemic and critically threatened bird species, and high species richness.Species distribution in trophic categories also indicates the area as a suitable environment for the existence of a wide range of birds.Therefore, here we contribute with valuable information for the development of conservation or management plans at a local or regional level.Regarding our results and the area features, such as its size, conservation status and position within the state -between Cerrado and Atlantic Forest -the study site must be considered as a priority conservation area to preserve bird species in the State of São Paulo.

Table 2 .
Frequency of occurrence (%) of bird species in each habitat at RL-CPPSE and surroundings.

Table 3 .
Number of species (% in parentheses) in trophic categories at RL-CPPSE and surroundings.We found 28 species in the cerradão, 110 in the cerrado sensu stricto, 13 in the gallery forest, 26 in the Although we did not see nationally threatened species, we recorded two globally threatened (Table1): Hylocharis chrysura -least concern and C. eucosma near threatened(IUCN, 2007).

Table 1 .
Continued... reservoir border, 26 in the pasturelands and sugar cane monoculture and 55 in the anthropic area (Table