Abstracts

Introduction

One of the main positive interactions between plants and animals is seed dispersal by frugivores. Plants benefit from the dispersal of their propagules away from the parent plant because this reduces competition and predation (Howe & Smallwood 1982HOWE, H.F. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13(1):201-228, 10.1146/annurev.es.13.110182.001221.
https://doi.org/10.1146/annurev.es.13.11... ) and increases gene flow between populations. In return, animals that consume fruits receive nutritional benefits (Howe & Primack 1975HOWE, H.F. & PRIMACK, R.B. 1975. Differential seed dispersal by birds of the tree Casearia nitida (Flacourtiaceae). Biotropica 7(4):278-283, 10.2307/2989740.
https://doi.org/10.2307/2989740... , Snow 1981SNOW, D.W. 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13(1):1-14.).

The interactions between fruiting plants and frugivorous birds in a community define a pattern comprising a few bird species that interact with many plant species and a few plants that interact with many birds. This makes the dependence between bird and plants species essential to the stability of the ecological processes of a community (Fadini & De Marco 2004FADINI, R.F. & DE MARCO, P. 2004. Interações entre aves frugívoras e plantas em um fragmento de Mata Atlântica de Minas Gerais. Ararajuba 12(2):97-103.).

Birds stand out as seed dispersers due to the high abundance and frequency with which they feed on fruits and their great ability to move between environments (Jordano 1994JORDANO, P. 1994. Spatial and temporal variation in the avian-frugivore assemblage of Prunus mahaleb: patterns and consequences. Oikos 71(3):479-471, 10.2307/3545836.
https://doi.org/10.2307/3545836... ). Frugivorous birds represent 56% of the world’s avian families and, in Neotropical forests, 25 to 30% of the avifauna includes fruits in their diet (Pizo & Galetti 2010Pizo, M.A. & GALETTI, M. 2010. Métodos e perspectivas do estudo da frugivoria e dispersão de sementes por aves. In Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento (Accordi, I., Straube, F.C & Von Matter, S. orgs). Technical Books Rio de Janeiro, p. 492-504.). According to Jordano (1987)JORDANO, P. 1987. Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Am. Nat. 129(5):657-677, 10.1086/284665.
https://doi.org/10.1086/284665... , studies of frugivory by birds in tropical forests are relatively well reported (e.g., Snow 1981SNOW, D.W. 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13(1):1-14., Jordano 1987JORDANO, P. 1987. Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Am. Nat. 129(5):657-677, 10.1086/284665.
https://doi.org/10.1086/284665... , Galetti & Pizo 1996GALETTI, M. & PIZO, M.A. 1996. Fruit eating by birds in a forest fragment in southeastern Brazil. Ararajuba 4(2):71-79., Medellín & Gaona 1999MEDELLĺN, R.A. & GAONA, O. 1999. Seed dispersal by bats and birds in forest and disturbed habitats of Chiapas, México. Biotropica 31(3):478-485, 10.1111/j.1744-7429.1999.tb00390.x.
https://doi.org/10.1111/j.1744-7429.1999... , Silva & Tabarelli 2000SILVA, J.M.C. & TABARELLI, M. 2000. Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature 404(6773):72-74, 10.1038/35003563.
https://doi.org/10.1038/35003563... , Bascompte et al. 2003BASCOMPTE, J., JORDANO, P., MELIÁN, J. & OLESEN, J.M. 2003. The nested assembly of plant-animal mutualistic networks. PNAS 100(16):9383-9387, 10.1073/pnas.1633576100.
https://doi.org/10.1073/pnas.1633576100... , Saracco et al. 2005SARACCO, J.F., COLLAZO, J.A., GROOM, M.J. & CARLO, T.A. 2005. Crop size and fruit neighborhood effects on bird visitation to fruiting Schefflera morototoni trees in Puerto Rico. Biotropica 37(1):81-87, 10.1111/j.1744-7429.2005.04040.x.
https://doi.org/10.1111/j.1744-7429.2005... , Galetti et al. 2013GALETTI, M.R., GUEVARA, R., CÔRTES, M.C., FADINI, R., VON MATTER, S., LEITE, A.B., LABECCA, F., RIBEIRO, T., CARVALHO, C.S., COLLEVATTI, R.G., PIRES, M.M., GUIMARÃES JR, P.R., BRANCALION, P.H., RIBEIRO, M.C. & JORDANO, P. 2013. Functional extinction of birds drives rapid evolution changes in seed size. Science 340(6136):1086-1090, 10.1126/science.1233774.
https://doi.org/10.1126/science.1233774... ). It is estimated that 50 to 90% of tree species in tropical forests produce zoochorous fruit (Howe & Smallwood 1982HOWE, H.F. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13(1):201-228, 10.1146/annurev.es.13.110182.001221.
https://doi.org/10.1146/annurev.es.13.11... ). In contrast, in tropical savannas, despite the wide geographical distribution and rich biodiversity, few studies have addressed the frugivory and seed dispersal by birds (e.g., Dean et al. 1999Dean, W.R.J., MILTON, S.J. & JELTSCH, F. 1999. Large trees, fertile islands, and birds in arid savanna. J. Arid Environ. 41(1):61-78, 10.1006/jare.1998.0455.
https://doi.org/10.1006/jare.1998.0455... , Hovestadt et al. 1999HOVESTADT, T., YAO, P. & LINSENMAIR, K.E. 1999. Seed dispersal mechanisms and the vegetation of forest islands in a West African forest-savanna mosaic (Comoé National Park, Ivory Coast). Plant Ecol. 144(1):1-25, 10.1023/A:1009764031116.
https://doi.org/10.1023/A:1009764031116... , Wütherich et al. 2001WÜTHERICH, D., AZ=CAR, A., GARCĺA-NUÑEZ, C. & SILVA, J.F. 2001. Seed dispersal in Palicourea rigida, a common treelet species from Neotropical savannas. J. Trop. Ecol. 17(3):449-458, 10.1017/S0266467401001304.
https://doi.org/10.1017/S026646740100130... , Faustino & Machado 2006FAUSTINO, T.C. & MACHADO, C.G. 2006. Frugivoria por aves em uma área de campo rupestre na Chapada Diamantina, BA. Rev. Bras. Ornitol. 14(2):137-143., Christianini & Oliveira 2009CHRISTIANINI, A. & OLIVEIRA, P.S. 2009. The relevance of ants as seed rescuers of a primarily bird-dispersed tree in the Neotropical cerrado savanna. Oecologia 160(4):735-745, 10.1007/s00442-009-1349-2.
https://doi.org/10.1007/s00442-009-1349-... , Pascotto et al. 2012PASCOTTO, M.C., CATEN, H.T. & OLIVEIRA, J.P.F. 2012. Birds as potential seed dispersers of Curatella americana L. in the Brazilian Cerrado. Ornitol. Neotrop. 23(1):583-593., Maruyama et al. 2013MARUYAMA, P.K., BORGES, M.R., SILVA, P.A., BURNS, K.C. & MELO, C. 2013. Avian frugivory in Miconia (Melastomataceae): contrasting fruiting times promote habitat complementary between savanna and palm swamp. J. Trop. Ecol. 29(2):99-109, 10.1017/S0266467413000138.
https://doi.org/10.1017/S026646741300013... ).

Savannas are defined primarily by their seasonal climate and fire regime, with vegetation characterized by an herbaceous stratum dominated by grasses and a discontinuous woody shrub stratum (Skarpe 1992SKARPE, C. 1992. Dynamics of savanna ecosystems. J. Veg. Sci. 3(3):293-300, 10.2307/3235754.
https://doi.org/10.2307/3235754... ). The Brazilian Cerrado, the largest savanna in the world, is represented by a mosaic of phytophysiognomic formations such as Fields, Cerrado sensu stricto, Semideciduous Forests and Gallery Forests (Silva & Bates 2002SILVA, J.M.C. & BATES, J.M. 2002. Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot. BioScience 52(3):225-233, 10.1641/0006-3568(2002)052[0225:BPACIT]2.0.CO;2.
https://doi.org/10.1641/0006-3568(2002)0... ). The climate is represented by two well-defined seasons (one warm and wet and the other cool and dry), due to the changes in temperature and precipitation over the year (Eiten 1972EITEN, G. 1972. The cerrado vegetation of Brazil. Bot. Rev. 38(2):201-341, 10.1007/BF02859158.
https://doi.org/10.1007/BF02859158... ).

With about 12000 plant species (Mendonça et al. 2008MENDONÇA, R.C., FELFILI, J.M., WALTER, B.M., SILVA-JUNIOR, M.C., REZENDE, A.B., FILGUEIRAS, T.S., NOGUEIRA, P.E. & FAGG, C.W. 2008. Flora vascular do bioma Cerrado: checklist com 12.356 espécies. In Cerrado: ecologia e flora (Sano, S.M., Almeida, S.P. & Ribeiro J.F., eds). Embrapa Informação Tecnológica, Brasília, v 2, p. 421-1279.) and 837 bird species (Myers et al. 2000MYERS N., MITTERMEIER, R.A., MITTERMEIER, C.G., FONSECA, G.A.F. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403(6772):853-858, 10.1038/35002501.
https://doi.org/10.1038/35002501... ) catalogued, it is estimated that about half of the plant species in the Cerrado need animals to disperse their seeds, and birds are the main group of dispersers (Gottsberger & Silberbauer-Gottsberger 1983GOTTSBERGER, G. & SILBERBAUER-GOTTSBERGER, I. 1983. Dispersal and distribuition the Cerrado vegetation of Brazil. Sonderb. Naturwiss. Ver. Hamburg 7(1):315-352., Pinheiro & Ribeiro 2001PINHEIRO, F. & RIBEIRO, J.F. 2001. Síndromes de dispersão de sementes em Matas de Galeria do Distrito Federal. In Cerrado: caracterização e recuperação de Matas de Galeria (Ribeiro, J.F., Fonseca, C.E.L. & Sousa-Silva, J.C, eds). Embrapa Cerrados. Planaltina, p. 333-376., Kuhlmann 2012KUHLMANN, M. 2012. Frutos e sementes do Cerrado atrativos para fauna: guia de campo. Rede de Sementes do Cerrado, Brasília.). The proportion of zoochorous plant species is high in both savanna and forest physiognomies of the Cerrado. In the Cerrado sensu stricto of Central Brazil, for example, the proportion of zoochorous plant species ranges from 51 to 68% (Vieira et al. 2002VIEIRA, D.L.M., AQUINO, F.G., BRITO, M.A., FERNANDES-BULHÃO, C. & HENRIQUES, R.P.B. 2002. Síndromes de dispersão de espécies arbustivo-arbóreas em cerrado sensu stricto do Brasil Central e savanas amazônicas. Rev. Bras. Bot. 25(2):215-220, 10.1590/S0100-84042002000200009.
https://doi.org/10.1590/S0100-8404200200... ). On the other hand, in the Gallery Forests of Central and Southeastern Brazil, 63 to 89% of the plants have zoochorous dispersion and more than half of them are ornithochorous (Pinheiro & Ribeiro 2001PINHEIRO, F. & RIBEIRO, J.F. 2001. Síndromes de dispersão de sementes em Matas de Galeria do Distrito Federal. In Cerrado: caracterização e recuperação de Matas de Galeria (Ribeiro, J.F., Fonseca, C.E.L. & Sousa-Silva, J.C, eds). Embrapa Cerrados. Planaltina, p. 333-376., Motta-Junior & Lombardi 2002MOTTA-JUNIOR, J.C & LOMBARDI, J.A. 2002. Ocorrência de zoocoria em florestas de galeria no Complexo do Cerrado, Brasil. Biotemas 15(1):59-81.).

The fruit production of most Cerrado sensu stricto zoochorous species follows a seasonal pattern, with a peak in fruit ripening in the rainy season (Silberbauer-Gottsberger 2001SILBERBAUER-GOTTSBERGER, I. 2001. A hectare of Cerrado. II. Flowering and fruiting of thick-stemmed woody species. Phyton 41(1):129-158., Lenza & Klink 2006, Pirani et al. 2009PIRANI, F.R., SANCHEZ, M. & PEDRONI, F. 2009. Fenologia de uma comunidade arbórea em cerrado sentido restrito, Barra do Garças, MT, Brasil. Acta Bot. Bras. 23(4):1096-1109, 10.1590/S0102-33062009000400019.
https://doi.org/10.1590/S0102-3306200900... , Camargo et al. 2013CAMARGO, M.G.G., CAZETTA, E., SCHAEFER, H.M. & MORELLATO, L.P.C. 2013. Fruit color and contrast in seasonal habitats - a case study from a cerrado savanna. Oikos 122(9):1335-1342, 10.1111/j.1600-0706.2013.00328.x.
https://doi.org/10.1111/j.1600-0706.2013... ). The same pattern has been observed in Gallery Forests (Oliveira & De Paula 2001OLIVEIRA, P.E.A.M. & DE PAULA, F.R. 2001. Fenologia e biologia reprodutiva de plantas de Matas de Galeria. In Cerrado: caracterização e recuperação de Matas de Galeria (Ribeiro, J.F, Fonseca, C.E.L. & Sousa-Silva, J.C., eds). Embrapa Cerrados, Planaltina, p. 303-332.). However, the fruit of most abundant species in the two phytophysiognomies ripen in the dry season (Gouveia & Felfili 1998GOUVEIA, G.P. & FELFILI, J.M. 1998. Fenologia de comunidades de cerrado e de Mata de Galeria no Brasil Central. Rev. Árvore 22(4):443-450.).

Knowing that seed dispersal is an important ecological process that acts in the maintenance of diversity and that frugivory is the first step in studying this event (Cordeiro & Howe 2001CORDEIRO, N.J. & HOWE, H.F. 2001. Low recruitment of trees dispersed by animals in African forest fragments. Conserv. Biol. 15(6):1733-1741, 10.1046/j.1523-1739.2001.99579.x.
https://doi.org/10.1046/j.1523-1739.2001... ), our objectives were (i) to identify the interactions between frugivorous birds and plants and the most important species in the community (sensu importance Murray 2000MURRAY, K.G. 2000. The importance of different bird species as seed dispersers. InMonteverde: ecology and conservation of a tropical cloud forest (Nadkarni, N.M, & Wheelwright, N.T. eds) Oxford University Press, New York, p. 294-295.), and (ii) to evaluate the potential of seed dispersal, number of feeding records, number of interactions and composition of frugivorous bird species in savanna and forest formations of the Cerrado, considering the dry and rainy seasons. We tested the hypothesis that forest formations have higher numbers of feeding records and interactions, since most of the zoochorous plants of the Cerrado are concentrated in forests (Pinheiro & Ribeiro 2001PINHEIRO, F. & RIBEIRO, J.F. 2001. Síndromes de dispersão de sementes em Matas de Galeria do Distrito Federal. In Cerrado: caracterização e recuperação de Matas de Galeria (Ribeiro, J.F., Fonseca, C.E.L. & Sousa-Silva, J.C, eds). Embrapa Cerrados. Planaltina, p. 333-376., Kuhlmann 2012KUHLMANN, M. 2012. Frutos e sementes do Cerrado atrativos para fauna: guia de campo. Rede de Sementes do Cerrado, Brasília.), and that the records of feeding and interactions show higher values during the rainy season, because there is greater availability of ripe fruit in the Cerrado during this season (Silberbauer-Gottsberger 2001SILBERBAUER-GOTTSBERGER, I. 2001. A hectare of Cerrado. II. Flowering and fruiting of thick-stemmed woody species. Phyton 41(1):129-158., Lenza & Klink 2006, Pirani et al. 2009PIRANI, F.R., SANCHEZ, M. & PEDRONI, F. 2009. Fenologia de uma comunidade arbórea em cerrado sentido restrito, Barra do Garças, MT, Brasil. Acta Bot. Bras. 23(4):1096-1109, 10.1590/S0102-33062009000400019.
https://doi.org/10.1590/S0102-3306200900... , Camargo et al. 2013). Our second hypothesis is that the composition of frugivorous bird species does not differ between savanna and forest formations or between the dry and rainy seasons, since most of the bird species of the Cerrado occur in both vegetation formations (Silva 1997SILVA, J.M.C. 1997. Endemic bird species and conservation in the Cerrado Region, South America. Biodivers. Conserv. 6(3):435-450, 10.1023/A:1018368809116.
https://doi.org/10.1023/A:1018368809116... , Bagno & Marinho-Filho 2001BAGNO, M.A. & MARINHO-FILHO, J. 2001. A avifauna do Distrito Federal: uso de ambientes abertos e florestais e ameaças. In Cerrado: caracterização e recuperação de Matas de Galeria (Ribeiro J.F., Fonseca C.E.L. & Sousa-Silva J.C., eds). Embrapa Cerrados, Planaltina, p. 493-528.).

Material and Methods

Study area - This study was conducted in Serra Azul State Park (15°52’S and 51°16’W), located in the municipality of Barra do Garças, in the region of the Araguaia Valley, in the eastern part of the state of Mato Grosso. With an area of about 11,000 ha, this is an important Conservation Unit in the Cerrado containing a variety of phytophysiognomies typical to this biome, including savanna and forest formations (Ribeiro & Walter 2008RIBEIRO, J.F. & WALTER, B.M.T. 2008. As principais fitofisionomias do Bioma Cerrado. In Cerrado: ecologia e flora (Sano, S.M., Almeida, S.P. & Ribeiro, J.F., eds). Embrapa Informação Tecnológica, Brasília, p. 151-212.). The average altitudes in the region range from 600 to 700 m and its soils are classified as clayey dystrophic red-yellow latosol (oxisol) (Pirani et al. 2009PIRANI, F.R., SANCHEZ, M. & PEDRONI, F. 2009. Fenologia de uma comunidade arbórea em cerrado sentido restrito, Barra do Garças, MT, Brasil. Acta Bot. Bras. 23(4):1096-1109, 10.1590/S0102-33062009000400019.
https://doi.org/10.1590/S0102-3306200900... ).

According to the Köppen classification the region has an Aw type climate, hot and humid, with two well-defined seasons, a rainy summer (October to March) and dry winter (April to September). The average annual temperature is 25.5°C and annual average rainfall is 1,528 mm (Pirani et al. 2009PIRANI, F.R., SANCHEZ, M. & PEDRONI, F. 2009. Fenologia de uma comunidade arbórea em cerrado sentido restrito, Barra do Garças, MT, Brasil. Acta Bot. Bras. 23(4):1096-1109, 10.1590/S0102-33062009000400019.
https://doi.org/10.1590/S0102-3306200900... ).

Data collection - Sampling was conducted from August 2009 to October 2010 (first period) and from November 2011 to August 2012 (second period). In the first period, we used four preestablished trails, each approximately 2 km in length, two of which passed through savanna formations (rocky outcrop Cerrado - Cerrado Rupestre and Typical Cerrado - Cerrado Típico) and two through forest formations (Gallery Forest and Semideciduous Forest). In the second period we sampled the module that follows the RAPELD model (Magnusson et al. 2005MAGNUSSON, W.E., LIMA, A.P., LUIZÃO, R., LUIZÃO, F., COSTA, F.R.C., CASTILHO, C.V. & KINUPP, V.F. 2005. RAPELD: a modification of the Gentry method for biodiversity surveys in long-term ecological research sites. Biota Neotrop. 5(2):1-6. http://www.biotaneotropica.org.br/v5n2/pt/abstract?point-of-view+bn01005022005 (último acesso em 02/05/2014), 10.1590/S1676-06032005000300002
http://www.biotaneotropica.org.br/v5n2/p... ), in which two parallel 5-km-long trails, one kilometer apart from each other, pass through different Cerrado phytophysiognomies, such as Shrubby Grassland Cerrado (Cerrado Ralo), Typical Cerrado, Semideciduous Forest and Gallery Forest (sensuRibeiro & Walter 2008RIBEIRO, J.F. & WALTER, B.M.T. 2008. As principais fitofisionomias do Bioma Cerrado. In Cerrado: ecologia e flora (Sano, S.M., Almeida, S.P. & Ribeiro, J.F., eds). Embrapa Informação Tecnológica, Brasília, p. 151-212.).

The interactions were recorded using the line transect method (Bibby et al. 2000BIBBY, C.J., BURGESS, N.D., HILL, D.A. & MUSTOE, S.H. 2000. Bird census techniques. 2 ed. Academic Press, London.), with adaptations for frugivory studies (Pizo & Galetti 2010Pizo, M.A. & GALETTI, M. 2010. Métodos e perspectivas do estudo da frugivoria e dispersão de sementes por aves. In Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento (Accordi, I., Straube, F.C & Von Matter, S. orgs). Technical Books Rio de Janeiro, p. 492-504.). In addition to the line transect method, focal observations were made involving twelve plant species chosen mainly because of their large individual fruit production and the easy visibility of the crown (Byrsonima sericea DC. - Malpighiaceae, Cecropia pachystachya Trécul - Urticaceae, Copaifera langsdorffii Desf. - Fabaceae, Lasiacis ligulata Hitchc. & Chase - Poaceae, Miconia staminea (Desr.) DC. - Melastomataceae, Myrcia multiflora (Lam.) DC. - Myrtaceae, Myrsine umbellata Mart. - Primulaceae, Norantea guianensins Aubl. - Marcgraviaceae, Rudgea viburnoides (Cham.) Benth. - Rubiaceae, Schefflera morototoni (Aubl.) Maguire et al. - Araliaceae, Xylopia aromatica (Lam.) Mart. e Xylopia sericea A. St.-Hil. - Annonaceae). Focal observations of the same plant were made on non-consecutive days, with an average of three observers per sampling. Three hours of focal observations were made for each plant species and only complete observations were considered, in which a frugivore was observed from its arrival on the plant until its departure, without losing sight of the bird during its entire visit (Silva et al. 2002SILVA, W.R., DE MARCO, P., HASUI, E. & GOMES, V.S.M. 2002. Patterns of fruit-frugivore interactions in two Atlantic forest bird communities of south-eastern Brazil: implications for conservation. In Seed dispersal and frugivory: ecology, evolution and conservation (Levey, D.J., Silva, W.R. & Galetti, M. eds). CABI Publising, Oxon, p. 423-436.).

Each time a bird was observed eating fruit the feeding event was recorded, regardless of the number of fruits consumed and the duration of the visit. In the case of flocks of birds foraging at the same time on the same plant, an individual feed record was made of the fruit consumed by each bird in the flock (Pizo & Galetti 2010Pizo, M.A. & GALETTI, M. 2010. Métodos e perspectivas do estudo da frugivoria e dispersão de sementes por aves. In Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento (Accordi, I., Straube, F.C & Von Matter, S. orgs). Technical Books Rio de Janeiro, p. 492-504.). Records of feeding events by a bird species on a plant species corresponded to an interaction. Thus, an interaction indicated that a particular bird species consumed fruits of a particular plant species, regardless of the number of recorded feeding events.

In each recorded feeding event, we noted the consumer bird species, the plant species whose fruits were consumed, the phytophysiognomy and the date of the record. The mode of fruit consumption by the birds was also evaluated, including the portion of fruit consumed (pulp, aril, seed, and/or entire fruit) and the fruit’s ripeness. Birds observed consuming whole propagules or taking them away from the parent plant were considered potential seed dispersers. The species that ate unripe fruits or that shredded the seeds were considered seed predators (Howe & Smallwood 1982HOWE, H.F. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13(1):201-228, 10.1146/annurev.es.13.110182.001221.
https://doi.org/10.1146/annurev.es.13.11... , Moermond & Denslow 1985MOERMOND, T.C. & DENSLOW, J.S. 1985. Neotropical avian frugivores: patterns of behavior, morphology, and nutrition, with consequences for fruit selection. Ornithological Monographs 36(1):865-897, 10.2307/40168322.
https://doi.org/10.2307/40168322... ).

Weekly visits to the field were made in the first period, so that each phytophysiognomy was sampled at least once a month by the line transect method. Two to three weekly field visits were made in the second period, so that each vegetation type would also be sampled at least once a month by the line transect method, ensuring that the number of samplings in savanna and forest formations would be as similar as possible. Samplings were conducted between 6:00 AM and 1:00 PM., totaling 284 hours of sampling work by the line transect (248 hours) and focal methods (36 hours).

A frugivore was considered based on the criteria of Moermond & Denslow (1985MOERMOND, T.C. & DENSLOW, J.S. 1985. Neotropical avian frugivores: patterns of behavior, morphology, and nutrition, with consequences for fruit selection. Ornithological Monographs 36(1):865-897, 10.2307/40168322.
https://doi.org/10.2307/40168322... ), according to which a frugivorous bird is one that includes fruits in its diet at least during some season or stage of life, but does not feed exclusively on fruits. To separate the frugivorous birds into feeding guilds, we used the criteria adopted by Vieira et al. (2013VIEIRA, F.M., PURIFICAÇÃO, K.N., CASTILHO, L.S. & PASCOTTO, M.C. 2013. Estrutura trófica da avifauna de quatro fitofisionomias do Cerrado no Parque Estadual da Serra Azul. Ornithologia 5(2):43-57.) for the avifauna of Serra Azul State Park. The taxonomic classification and nomenclature of bird species was based on the proposal of the Brazilian Ornithological Records Committee (CBRO 2014COMITÊ BRASILEIRO DE REGISTROS ORNITOL=GICOS -CBRO. 2014. Lista das aves do Brasil. 11a ed. http://www.cbro.org.br/CBRO/pdf/AvesBrasil2014.pdf (último acesso em 02/05/2014).
http://www.cbro.org.br/CBRO/pdf/AvesBras... ) and of plant species on the List of Brazilian Flora Species (2014LISTA DE ESPÉCIES DA FLORA DO BRASIL. 2014. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (último acesso em: 02/05/ 2014).
http://floradobrasil.jbrj.gov.br/... ).

Data analysis - The importance index (I) was calculated for each bird species considered a potential seed disperser. This index denotes the contribution of a bird species compared with the other bird species to each of the plants with which it interacts. The index is characterized by assigning a weight to the species with many interactions, which include many exclusive interactions (Murray 2000MURRAY, K.G. 2000. The importance of different bird species as seed dispersers. InMonteverde: ecology and conservation of a tropical cloud forest (Nadkarni, N.M, & Wheelwright, N.T. eds) Oxford University Press, New York, p. 294-295.), and is given by the following formula: Ij = Σ[(Cij/Ti)/S] where Ti is the total number of bird species that fed on the fruit of plant i, S is the total number of sampled plants species, and Cij is equal to 1 if the bird species j consumed the fruits of the plant species i or 0 if it did not. The value of I varies between 0 and 1, with 0 corresponding to avian species that did not interact with any plant and 1 corresponding to those that consumed fruits from all the plants contained in the sample. The same index was use to calculate the plant species whose fruits were eaten by the birds. In this case, i corresponded to the bird species and j to the plant species.

We used the chi-square test (χ²) by means of contingency tables (Zar 1999ZAR, J.H. 1999. Biostatistical analysis. Prentice-Hall, New York.) to test our first hypothesis, i.e., to ascertain if there are more records of feeding events and interactions (consumed/did not consume) in forest formations than in savanna formations, and to determine how these values are distributed between the dry and rainy seasons. The composition of frugivorous bird species between savanna and forest formations and between the dry and rainy seasons (second hypothesis) was compared based on a multivariate analysis of similarity (ANOSIM) (Clarke & Green 1988CLARKE, K.R. & GREEN, R.H. 1988. Statistical design and analysis for a 'biological effects' study. Mar. Ecol. Prog. Ser. 46(1):213-226, 10.3354/meps046213.
https://doi.org/10.3354/meps046213... ), using the Jaccard similarity coefficient. The significance of the test (p) was obtained after 9,999 permutations and sequential Bonferroni correction (Legendre & Legendre 1998LEGENDRE, P. & LEGENDRE, E. 1998. Numeral Ecology. Elsevier Science B.V., Amsterdam.). The analyses were performed using the R-2.13.0 software program (R Development Core Team 2011R DEVELOPMENT CORE TEAM. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, http://www.R-project.org/.
http://www.R-project.org/... ).

Results

A total of 348 feeding events were recorded (average of 1.22 events per hour) and 187 interactions involving 44 plant species (26 families) and 60 bird species (19 families). Of the 60 bird species observed consuming fruit, 47 belong to the order Passeriformes, and are distributed in 12 families. Among them, the most numerous in terms of species were Thraupidae (16) and Tyrannidae (11). Among the non-passerines (13 species), the Psittacidae family was the most well represented (5 species) (Figure 1A). The plant families with the highest species richness were Myrtaceae (4), Melastomataceae (3) and Malpighiaceae (3) (Figure 1B).

Figure 1
. Specific richness of the avian (A) and plant (B) families that presented interactions in frugivory events in Serra Azul State Park, Mato Grosso, Brazil.

The bird species that interacted with the largest number of plants were Turdus leucomelas Vieillot, 1818 (15 interactions) and Dacnis cayana (Linnaeus, 1766) (n = 12), followed by Tangara cayana (Linnaeus, 1766) (n = 9) and Cyanocorax cyanopogon (Wied, 1821) (n = 9). Considering only forest formations, Turdus leucomelas (n = 12), Dacnis cayana (n = 8) and Saltator maximus (Statius Muller, 1776) (n = 8) were the bird species that interacted with the largest number of plant species. In the savanna formations, Dacnis cayana and Tangara sayaca (Linnaeus, 1766) stood out with five interactions each, and Hemithraupis guira (Linnaeus, 1766) and Elaenia chiriquensis Lawrence, 1865, with four interactions each.

The plant species that interacted with the largest number of bird species were Miconia staminea (23 interactions), Cecropia pachystachya (n = 12) and Dilodendron bipinnatum Radlk. (n = 12). In the forest formations, 35% of the observed interactions involved Miconia staminea (n = 23), Dilodendron bipinnatum (n = 12) and Schefflera morototoni (n = 10). On the other hand, about 40% of the interactions in the savanna formations involved Cecropia pachystachya (9 interactions), Curatella americana L. (n = 9) and Copaifera langsdorffii (n = 7).

As for the importance index, Turdus leucomelas (I = 0.107), Cyanocorax cyanopogon (I = 0.066) and Trogon curucui Linnaeus, 1766 (I = 0.054) were the most important bird species in the entire community (Figure 2A). The most important bird species in the forests were Turdus leucomelas (I = 0.116), Trogon curucui (I = 0.078) and Saltator maximus (I = 0.071). In the savanna formations, the bird species with the highest levels of importance were Volatinia jacarina (Linnaeus, 1766) (I = 0.080), Turdus leucomelas (I = 0.065), Tangara sayaca (I = 0.065) and Myiodynastes maculatus (Statius Muller, 1776) (I = 0.065).

Figure 2
Indices of importance of the ten avian (A) and plant (B) species that presented the highest values in Serra Azul State Park, Mato Grosso, Brazil. The number of recorded interactions are shown in parentheses.

Among plants, Miconia staminea (I = 0.162), Cecropia pachystachya (I = 0.083) and Rudgea viburnoides (I = 0.063) were the most important in the community (Figure 2B). The plants that stood out in the forest formations were Miconia staminea (I = 0.255), Rudgea viburnoides (I = 0.089) and Xylopia sericea (I = 0.084). The most important plants in the savanna formations were Cecropia pachystachya (I = 0.170), Curatella americana (I = 0.165) and Copaifera langsdorffii (I = 0.111).

Among the observed interactions, 77% showed a potential for dispersal. Of the 60 bird species, 49 (82%) were considered potential dispersers of all the plant species with which they interacted. Seed predators, represented mainly by species of the Psittacidae family, accounted for 12% of the observed bird species. Besides parrots, only Cyclarhis gujanensis (Gmelin, 1789), Nemosia pileata (Boddaert, 1783), Neothraupis fasciata (Lichtenstein, 1823), Tersina viridis (Illiger, 1811), Zonotrichia capensis (Statius Muller, 1776) and Gnorimopsar chopi (Vieillot, 1819) were not considered potential seed dispersers of any plant species (Table 1).

The seeds of nine plant species were not dispersed by any bird species. The seeds of four of these plant species [Brosimum gaudichaudii Trécul, Caryocar brasiliense Cambess., Cordia sellowiana Cham. and Pseudobombax tomentosum (Mart. & Zucc.)] were shredded by parrots. Added to these plant species, the fruits of Mezilaurus crassiramea (Meisn.) Taub. ex Mez and Indeterminate 1 were consumed only in the unripe stage. The consumption of pulp was observed only in Buchenavia tomentosa Eichler, Diospyros brasiliensis Mart. ex Miq. and Mangifera indica L. (Table 1).

Most of the feeding events (70% of total) were recorded in forest formations and during the dry season (73%) (χ² = 39.529; gl= 1; p < 0.001). As for the number of interactions (consumed/did not consume), about 70% of them were recorded in the forest formations and also during the dry season (75%). However, this result was not significant (χ² = 15.975; gl = 1; p = 0.06). Of total number of frugivorous birds recorded, 75% occurred in forest formations and 52% in savanna formations, indicating that the composition of frugivorous bird species differed between the two types of vegetation (ANOSIM, R = 0.238, p < 0.001). The bird species composition also differed between seasons (ANOSIM, R = 0.223, p < 0.001). About 80% of the species were recorded during the dry season, while approximately 50% were recorded eating fruits in the rainy season. Twenty- nine bird species were recorded consuming fruits exclusively in forests, 15 exclusively in savanna formations, and 16 in both environments (Table 1).

Discussion

Bird species of the Thraupidae and Tyrannidae families (Passeriformes) were found to be the main potential seed dispersers. In frugivory studies conducted in the Cerrado (Francisco & Galetti 2002FRANCISCO, M.R. & GALETTI, M. 2002. Aves como potenciais dispersores de sementes de Ocotea pulchella Mart. (Lauraceae) numa área de vegetação de cerrado do sudeste brasileiro. Rev. Bras. Bot. 25(1):11-17., Cazetta et al. 2002CAZETTA, E., RUBIM, P., LUNARDI, V.O., FRANCISCO, M.R. & GALETTI, M. 2002. Frugivoria e dispersão de sementes de Talauma ovata (Magnoliaceae) no sudeste brasileiro. Ararajuba 10(2):199-206., Melo et al. 2003MELO, C., BENTO, E.C. & OLIVEIRA, P.E. 2003. Frugivory and dispersal of Faramea cyanea (Rubiaceae) in cerrado woody plant formations. Braz. J. Biol. 63(1):75-82, 10.1590/S1519-69842003000100010.
https://doi.org/10.1590/S1519-6984200300... , Marcondes-Machado & Rosa 2005MARCONDES-MACHADO, L.O. & ROSA, G.A.B. 2005. Frugivoria por aves em Cytharexyllum myrianthum Cham. (Verbenaceae) em áreas de pastagens de Campinas, SP. Ararajuba 13(1):113-115., Pascotto 2006PASCOTTO, M.C. 2006. Avifauna dispersora de sementes de Alchornea glandulosa (Euphorbiaceae) em uma área de mata ciliar no estado de São Paulo. Rev. Bras. Ornitol. 14(3):291-296., 2007PASCOTTO, M.C. 2007. Rapanea ferruginea (Ruiz & Pav.) Mez. (Myrsinaceae) como uma importante fonte alimentar para as aves em uma mata de galeria no interior do Estado de São Paulo. Rev. Bras. Zool. 24(3):735-741., Francisco et al. 2007FRANCISCO, M.R., LUNARDI, V.O. & GALETTI, M. 2007. Bird attributes, plant characteristics, and seed dispersal of Pera glabrata (Schott, 1858), (Euphorbiaceae) in a disturbed cerrado area. Braz. J. Biol. 67(4):627-634, 10.1590/S1519-69842007000400006.
https://doi.org/10.1590/S1519-6984200700... , Christianini & Oliveira 2009, Allenspach & Dias 2012ALLENSPACH, N. & DIAS, M.M. 2012. Frugivory by birds on Miconia albicans (Melastomataceae), in a fragment of cerrado in São Carlos, southeastern Brazil. Braz. J. Biol. 72(2):407-413, 10.1590/S1519-69842012000200024.
https://doi.org/10.1590/S1519-6984201200... , Pascotto et al. 2012PASCOTTO, M.C., CATEN, H.T. & OLIVEIRA, J.P.F. 2012. Birds as potential seed dispersers of Curatella americana L. in the Brazilian Cerrado. Ornitol. Neotrop. 23(1):583-593., Maruyama et al. 2013MARUYAMA, P.K., BORGES, M.R., SILVA, P.A., BURNS, K.C. & MELO, C. 2013. Avian frugivory in Miconia (Melastomataceae): contrasting fruiting times promote habitat complementary between savanna and palm swamp. J. Trop. Ecol. 29(2):99-109, 10.1017/S0266467413000138.
https://doi.org/10.1017/S026646741300013... ), species of the aforementioned families also stood out as the main potential seed dispersers, with Tangara sayaca, Tangara cayana (Thraupidae), Pitangus sulphuratus (Linnaeus, 1766) and Myiodynastes maculatus (Tyrannidae) standing out as the most frequently recorded species.

Species of the tanager family are very important to seed dispersal in the Cerrado, as well as throughout the Neotropics (Snow & Snow 1971SNOW, B.K. & SNOW, D.W. 1971. The ecology of tanagers and honeycreepers in Trinidad. The Auk 88(2):291-322.). According to Francisco & Galetti (2002), tanagers stand out especially in the dispersal of seeds from plants with small fruit (< 0.4 cm). In the case of larger fruits, seed dispersal is compromised because the seeds fall under the parent plants (Levey 1987LEVEY, D. 1987. Seed size and fruit-handling techniques of avian frugivores. Am. Nat. 129(4):471-485, 10.1086/284652.
https://doi.org/10.1086/284652... , Sick 1997SICK, H. 1997. Ornitologia Brasileira: uma introdução. Nova Fronteira, Rio de Janeiro., Francisco & Galetti 2002). Despite the importance of tanagers as potential seed dispersers in this study, we observed that in the case of larger seeds (> 0.5 cm, personal observation), the potential for seed dispersal was really compromised, confirming the findings of Francisco & Galetti (2002). Tanagers also were less efficient in the dispersal of arilled seeds (Table 1). According to Sick (1997)SICK, H. 1997. Ornitologia Brasileira: uma introdução. Nova Fronteira, Rio de Janeiro., species of this group commonly eat only the aril and discard the seeds under the plant.

On the other hand, tyrant flycatchers, which are known for their predominantly insectivorous diet, include many species that feed on a mixed diet of insects and fruits (Sick 1997SICK, H. 1997. Ornitologia Brasileira: uma introdução. Nova Fronteira, Rio de Janeiro.). Some studies have shown that species that supplement their diet with fruits, as in the case of this family, have stood out as major seed dispersers in forest (Melo et al. 2003MELO, C., BENTO, E.C. & OLIVEIRA, P.E. 2003. Frugivory and dispersal of Faramea cyanea (Rubiaceae) in cerrado woody plant formations. Braz. J. Biol. 63(1):75-82, 10.1590/S1519-69842003000100010.
https://doi.org/10.1590/S1519-6984200300... , Pascotto 2006PASCOTTO, M.C. 2006. Avifauna dispersora de sementes de Alchornea glandulosa (Euphorbiaceae) em uma área de mata ciliar no estado de São Paulo. Rev. Bras. Ornitol. 14(3):291-296., 2007PASCOTTO, M.C. 2007. Rapanea ferruginea (Ruiz & Pav.) Mez. (Myrsinaceae) como uma importante fonte alimentar para as aves em uma mata de galeria no interior do Estado de São Paulo. Rev. Bras. Zool. 24(3):735-741.) and savanna formations (Faustino & Machado 2006, Pascotto et al. 2012PASCOTTO, M.C., CATEN, H.T. & OLIVEIRA, J.P.F. 2012. Birds as potential seed dispersers of Curatella americana L. in the Brazilian Cerrado. Ornitol. Neotrop. 23(1):583-593., Maruyama et al. 2013MARUYAMA, P.K., BORGES, M.R., SILVA, P.A., BURNS, K.C. & MELO, C. 2013. Avian frugivory in Miconia (Melastomataceae): contrasting fruiting times promote habitat complementary between savanna and palm swamp. J. Trop. Ecol. 29(2):99-109, 10.1017/S0266467413000138.
https://doi.org/10.1017/S026646741300013... ) in the Cerrado. Generally, bird species with non-specialized diets also lack habitat specificity, making them important in seed dispersal among different environments (Melo et al. 2003MELO, C., BENTO, E.C. & OLIVEIRA, P.E. 2003. Frugivory and dispersal of Faramea cyanea (Rubiaceae) in cerrado woody plant formations. Braz. J. Biol. 63(1):75-82, 10.1590/S1519-69842003000100010.
https://doi.org/10.1590/S1519-6984200300... ). Thus, in environments characterized by a mosaic of vegetation types, such as the Cerrado (Silva & Bates 2002SILVA, J.M.C. & BATES, J.M. 2002. Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot. BioScience 52(3):225-233, 10.1641/0006-3568(2002)052[0225:BPACIT]2.0.CO;2.
https://doi.org/10.1641/0006-3568(2002)0... ), opportunistic frugivores are extremely important from the standpoint of seed dispersal potential, at least with regard to plants that are little specialized and to the quantitative component (Schupp 1993SCHUPP, E.W. 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107/108(1):15-29.). However, it is worth investigating how seeds are treated after being ingested by these birds.

Miconia staminea and Cecropia pachystachya stood out as the most important plants. These species are characterized by their abundant production of small fruits and seeds (Kuhlmann 2012KUHLMANN, M. 2012. Frutos e sementes do Cerrado atrativos para fauna: guia de campo. Rede de Sementes do Cerrado, Brasília.). Like most of the plant species observed here, they belong in the low investment model (Howe & Smallwood 1982HOWE, H.F. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13(1):201-228, 10.1146/annurev.es.13.110182.001221.
https://doi.org/10.1146/annurev.es.13.11... ). In this model, plants produce copious amounts of fruits which are not very nutritious and small seeds, attracting a large variety of opportunistic birds willing to take advantage of a superabundant resource, but of little nutritional value. Based on the bird species observed consuming fruits (Table 1), we suggest that our results strongly fit this model, since most of the interactions were performed by opportunistic frugivores.

We found that 82% of the frugivorous bird species were considered potential seed dispersers. This was expected, since ornithochory is the main seed dispersal syndrome of tree species in the Brazilian Cerrado, in both forest and savanna environments (Gottsberger & Silberbauer-Gottsberger 1983, Pinheiro & Ribeiro 2001PINHEIRO, F. & RIBEIRO, J.F. 2001. Síndromes de dispersão de sementes em Matas de Galeria do Distrito Federal. In Cerrado: caracterização e recuperação de Matas de Galeria (Ribeiro, J.F., Fonseca, C.E.L. & Sousa-Silva, J.C, eds). Embrapa Cerrados. Planaltina, p. 333-376.). Species of the Psittacidae family, widely known as predators of seeds, which are usually shredded when ingested, stood out among the bird species that did not act as seed dispersers (Sick 1997SICK, H. 1997. Ornitologia Brasileira: uma introdução. Nova Fronteira, Rio de Janeiro.). Plants with larger fruits (> 2.5 cm), such as Buchenavia tomentosa and Diospyros brasiliensis, were only visited by pulp-eaters or seed predators (Table 1).

An analysis of the records of feeding events, number of interactions and composition of frugivorous bird species indicated that higher numbers were recorded in forested areas, confirming our hypotheses. A recent study by Kuhlmann (2012)KUHLMANN, M. 2012. Frutos e sementes do Cerrado atrativos para fauna: guia de campo. Rede de Sementes do Cerrado, Brasília. in the central portion of the Cerrado, involving 150 plant species with fruit attractive to fauna, revealed that about 80% were dispersed by birds and about 60% occurred in forested areas. Seed dispersal by animals in forest environments is more advantageous for plants than dispersal by abiotic processes, since animals, particularly birds, are more likely to disperse seeds over longer distances (Hovestadt et al. 1999HOVESTADT, T., YAO, P. & LINSENMAIR, K.E. 1999. Seed dispersal mechanisms and the vegetation of forest islands in a West African forest-savanna mosaic (Comoé National Park, Ivory Coast). Plant Ecol. 144(1):1-25, 10.1023/A:1009764031116.
https://doi.org/10.1023/A:1009764031116... ).

Kuhlmann (2012)KUHLMANN, M. 2012. Frutos e sementes do Cerrado atrativos para fauna: guia de campo. Rede de Sementes do Cerrado, Brasília. states that the majority of fruiting plants of the Cerrado ripen predominantly in the rainy season. Oliveira & De Paula (2001OLIVEIRA, P.E.A.M. & DE PAULA, F.R. 2001. Fenologia e biologia reprodutiva de plantas de Matas de Galeria. In Cerrado: caracterização e recuperação de Matas de Galeria (Ribeiro, J.F, Fonseca, C.E.L. & Sousa-Silva, J.C., eds). Embrapa Cerrados, Planaltina, p. 303-332.) reported a similar finding, stating that the fruit of most zoochorous plant species of gallery forests in central Brazil ripen in the rainy season. The same phenomenon has been observed in savanna formations (Silberbauer-Gottsberger 2001SILBERBAUER-GOTTSBERGER, I. 2001. A hectare of Cerrado. II. Flowering and fruiting of thick-stemmed woody species. Phyton 41(1):129-158., Lenza & Klink 2006, Pirani et al. 2009PIRANI, F.R., SANCHEZ, M. & PEDRONI, F. 2009. Fenologia de uma comunidade arbórea em cerrado sentido restrito, Barra do Garças, MT, Brasil. Acta Bot. Bras. 23(4):1096-1109, 10.1590/S0102-33062009000400019.
https://doi.org/10.1590/S0102-3306200900... , Camargo et al. 2013). Based on this information about fruiting phenology, we expected to record more numerous feeding events and interactions during the rainy season since, according to the above cited authors, more fruits ripen during this period. However, our assumption was not confirmed.

We believe that the large number of records of feeding events and of interactions during the dry season stems from the high production of fruits by species such as Rudgea viburnoides, Schefflera morototoni and Miconia staminea. According to Snow (1981SNOW, D.W. 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13(1):1-14.), species of these three genera are very important in the diet of frugivorous birds in the Neotropics, because their fruits are eaten by specialist and generalist frugivores. Firstly, the three species have small fruits (< 1 cm), which enables them to be eaten by frugivores of all sizes. Rudgea viburnoides and Miconia staminea belong to the two most important families of plants for tropical frugivorous birds (Rubiaceae and Melastomataceae, respectively) and, because their fruits are succulent, they are appreciated by a variety of frugivorous birds, especially the small ones that feed in the lower strata of the vegetation (Snow 1981SNOW, D.W. 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13(1):1-14., Maruyama et al. 2013MARUYAMA, P.K., BORGES, M.R., SILVA, P.A., BURNS, K.C. & MELO, C. 2013. Avian frugivory in Miconia (Melastomataceae): contrasting fruiting times promote habitat complementary between savanna and palm swamp. J. Trop. Ecol. 29(2):99-109, 10.1017/S0266467413000138.
https://doi.org/10.1017/S026646741300013... ). On the other hand, the fruit of Schefflera morototoni is rich in lipids and proteins (Snow 1971SNOW, B.K. & SNOW, D.W. 1971. The ecology of tanagers and honeycreepers in Trinidad. The Auk 88(2):291-322.), and therefore also attracts a wide variety of frugivores ranging from the smallest to the largest (Saracco et al. 2005SARACCO, J.F., COLLAZO, J.A., GROOM, M.J. & CARLO, T.A. 2005. Crop size and fruit neighborhood effects on bird visitation to fruiting Schefflera morototoni trees in Puerto Rico. Biotropica 37(1):81-87, 10.1111/j.1744-7429.2005.04040.x.
https://doi.org/10.1111/j.1744-7429.2005... , Parrini et al. 2013PARRINI, R., RAPOSO, M.A., DEL HOYO, J. & SILVA, A.R. 2013. Schefflera morototoni (Araliaceae) como importante recurso alimentar para as aves durante a estação seca na Amazônia central. Cotinga 35(1):1-4.).

It should also be noted that highly abundant species such as Turdus leucomelas, which alone accounted for 25% of the recorded feeding events, may have influenced the high number of feeding events recorded in the forests during the dry season, which may explain the fact that we found no difference in the qualitative matrix of interactions. Thus, we emphasize that it is important to consider the abundance of frugivores, as well as the number of recorded feeding events, and not only the presence/absence of interactions. During the dry season, for example, the number of feeding events recorded for Turdus leucomelas in forest areas was about 90% higher than in the rainy season. Most of the species recorded in forests also showed a remarkable increase in recorded feeding events in the dry season. This may be due to temporal and spatial variations in food resources, such as lower abundance of invertebrates and ripe fruits in open areas in the dry season (Macedo 2002MACEDO, R.H.F. 2002. The avifauna: ecology, biogeography, and behavior. In The Cerrados of Brazil: ecology and natural history of a Neotropical savanna (Oliveira, P.S. & Marquis, R.J. eds). Columbia University Press, New York, p. 242-265.). These factors are extremely important and can influence the movement of birds between forest and savanna habitats.

We observed that the composition of frugivorous birds differs between savanna and forest formations. This contradicted our hypothesis since, according to Bagno & Marinho-Filho (2001), most bird species in the Cerrado occur in both savanna and forest formations. However, this does not seem to apply when only frugivorous birds are involved (Vieira et al. 2013VIEIRA, F.M., PURIFICAÇÃO, K.N., CASTILHO, L.S. & PASCOTTO, M.C. 2013. Estrutura trófica da avifauna de quatro fitofisionomias do Cerrado no Parque Estadual da Serra Azul. Ornithologia 5(2):43-57.), probably due to the dependence of mandatory frugivores [e.g., Ramphastos vitellinus Lichtenstein, 1823 and Antilophia galeata (Lichtenstein, 1823)] on forest environments.

Based on the composition of avian frugivores (Table 1), it was found that the diet of approximately 80% of the recorded bird species is not based on fruits, but that they simply complement their diet with this type of resource. Thus, we believe that during the dry season, when there is a scarcity of other food items [such as small arthropods (Macedo 2002, Manhães 2003MANHÃES, M.A. 2003. Variação sazonal da dieta e do comportamento alimentar de traupíneos (Passeriformes: Emberezidae) em Ibitipoca, Minas Gerais, Brasil. Ararajuba 11(1):45-55.)], there is an increase in fruit consumption. Moreover, in situations of water deficit, consuming fruit is one of the main ways to obtain water (Argel-de-Oliveira 1998ARGEL-DE-OLIVEIRA, M.M. 1998. Aves que plantam: frugivoria e dispersão de sementes por aves. Boletim CEO 13(1):9-21.). Thus, species that do not usually consume fruits begin to use this resource in the dry season, which may explain the increase in the records of feeding events and bird-plant interactions during this period.

Our findings suggest that there is a shift of frugivorous bird species and particularly of individuals between savanna and forest formations in response to fluctuations in food resources, which are influenced by the strong climate seasonality of the Cerrado (Macedo 2002, Manhães 2003MANHÃES, M.A. 2003. Variação sazonal da dieta e do comportamento alimentar de traupíneos (Passeriformes: Emberezidae) em Ibitipoca, Minas Gerais, Brasil. Ararajuba 11(1):45-55.). Future studies to evaluate temporal and spatial fluctuations in the composition and abundance of bird species in the different vegetation formations of the Cerrado, as well as the availability of food resources, may complement and strengthen our findings. However, we already have strong evidence that forests represent important foraging areas for frugivorous birds during the dry season. Thus, the conservation of forest areas in predominantly savanna-like ecosystems such as the Cerrado is extremely important for frugivorous birds, thus ensuring the preservation of frugivore-plant interactions.

Acknowledgments

The authors thank the Secretaria de Estado de Meio Ambiente (SEMA-MT) for authorizing the fieldwork in the Parque Estadual da Serra Azul (PESA). We also gratefully acknowledge the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), for granting a master scholarship to the first author; and Fundação de Amparo è Pesquisa do Estado de Mato Grosso (FAPEMAT) (Process Nos. 873/2006 and 738702/2008) and the project SISBIOTA/Rede ComCerrado (Proc. CNPq 563134/2010-0) for their financial support. In addition, we are indebted to the following people for their assistance: the team of the Laboratório de Ornitologia UFMT/CUA for their assistance in the field work; Leandro Maracahipes and Maryland Sanchez for their help in identifying several plant species; Renato Goldenberg for identifying Miconia staminea and M. macrothyrsa; and Dilermando P. Lima Junior and Rudi R. Laps for their insightful suggestions.

References

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