Microsoft Word - 29-Bio_23072 1885 Original Article Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 DIVERSITY OF REPRODUCTIVE ECOLOGICAL GROUPS IN SEMIDECIDUOUS SEASONAL FORESTS DIVERSIDADE DE GRUPOS ECOLÓGICOS REPRODUTIVOS EM FLORESTAS ESTACIONAIS SEMIDECIDUAIS Filipe Ferreira de DEUS¹;Vagner Santiago do VALE 2 ; Ivan SCHIAVINI 3 ; Paulo Eugênio OLIVEIRA 4 1. Biologist, Ms., Ecology and Conservation of Natural Resources, Federal University of Uberlandia – UFU, Uberlandia, MG, Brazil. filipefdedeus@yahoo.com.br; 2. Dr., Ecology and Conservation of Natural Resources - UFU, Uberlandia, MG, Brazil; 3. Professor, Dr., Institute of Biology – INBIO - UFU Uberlandia, MG, Brazil; 4 Professor, Dr., Institute of Biology – INBIO - Uberlandia, MG, Brazil. poliveira@ufu.br ABSTRACT: Ecosystem degradation leads to loss of interactions between animals and plants, and changes in frequency of pollination systems, dispersal modes and sexual systems of plants. The objective of the present work was to compare the reproductive ecological groups of tree species among semideciduous seasonal forests remnants in the Triangulo Mineiro, Brazil, and to understand the organization of those plant communities. We analyzed the reproductive biology of 243 tree species found in 10 fragments, which showed different levels of disturbance. The occurrence and relative density of the species were used to estimate the importance of each reproductive feature. The study was based on a compilation of data present in specialized works and community surveys conducted in the region. We aggregated the species of these communities in ecological groups according to their reproductive characteristics. The frequency of species in each reproductive ecological group was, to a certain extent, similar between remnants. The pollination by small insects (small bees, wasps and flies) represented 42%, dispersal by birds 35%, and hermaphrodite sexual system 54% of the species. Clearer differences among fragments were found on the relative densities of each reproductive ecological group. Relatively specialized bat and moth pollination, as well as wind dispersal were common in the most disturbed fragment. But generalist reproductive characteristics predominated in the studied fragments. KEYWORDS: Pollination system. Dispersal system. Sexual system. Forest fragments. INTRODUCTION The Cerrado Biome has a high diversity of plant physiognomies intensively explored by man for livestock, agriculture, and sugar cane cultivation (KLINK; MACHADO, 2005), and has been reduced to a fraction of the original vegetation. These disturbances contributed to changes in the natural processes of communities, because the composition and abundance of species are affected by degradation (NUNES et al., 2003). The semideciduous seasonal forest (sensu IBGE 2012), also referred as dry semideciduous forests (RIBEIRO; WALTER, 2008), is one of the Cerrado phytophysiognomies, which trees elements loose between 20 and 50% of their leaves during the dry season (RIBEIRO; WALTER, 2008). Many of these formations are characterized by a large floristic diversity, including species of the Amazon, Atlantic Forest and Cerrado flora (OLIVEIRA-FILHO; FONTES, 2000). The plant diversity identified in the remnants of seasonal forests suggests an intricate network of interactions with animals. Hence, the process of pollination as well as the dispersal of fruits and seeds are fundamentally dependent on biotic vectors, especially birds and mammals (TALORA; MORELLATO, 2000). Over 90% of the world Angiosperms are pollinated by animals (BUCHMANN; NABHAN, 1996), so pollination is essential for the maintenance of biodiversity in forest ecosystems in general (VAMOSI et al., 2006) and in these forests in particular (OLIVEIRA; PAULA, 2001). With the degradation and forest fragmentation, many of the animal-plant interactions may disappear, since many species of animals cannot find enough resources to feed or reproduce efficiently in fragments (FRANCHESCHINELLI et al., 2003). Fragmentation processes of Atlantic forest areas in Northeastern Brazil have prompted a shift in the frequency of certain pollination systems and reproductive features, leading to a simplification of the reproductive process and breakdown of the interdependence between animals and plants (GIRÃO et al., 2007). With the change of plant-pollinator interactions, the species reproductive success is affected, disturbing the processes of seed dispersal and germination, reducing the size of populations and often promoting local extinctions (HARRIS; JOHNSON, 2004). Received: 03/07/13 Accepted: 15/06/14 1886 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 Considering that each forest fragment has a history of disturbance and occupation by different plant species (LOPES, 2010), we expected to find variation in the occurrence of pollination systems, fruit and seed dispersal modes, and sexual systems between fragments. The basic idea is that well preserved forests tend to have species with more specialized reproductive features and which depend more broadly on animal pollinators and dispersers. Furthermore, the conservation status and the possibility of recovery of these areas are dependent on biotic interactions and reproductive requirements of the plant species in these communities. Therefore, the objective of the present work was to compare the reproductive ecological groups of tree species among fragments of semideciduous seasonal forests of Triangulo Mineiro, Brazil, and to understand the organization of plant communities, using those reproductive characteristics. MATERIAL AND METHODS We here compiled and supplemented information on the reproductive biology and ecology of tree species found in ten fragments of semideciduous seasonal forests (sensu IBGE 2012) of the Triangulo Mineiro region, in Central Brazil (Table 1). These ten forests were studied in phytosociological surveys conducted by Lopes (2010). The relative density data in each area for each species, obtained from that study, were used to estimate similarities and/or differences in the pollination systems, dispersal and sexual system. The species information about the flowering phenology and fruiting was also compiled from herbarium data and specific literature, when available. Data on sexual system, pollination and reproduction systems were obtained from literature or other community studies conducted in the region (OLIVEIRA; GIBBS, 2000; PINHEIRO; RIBEIRO, 2001). Table 1. Information of the ten fragments of semideciduous seasonal forest (sensu IBGE 2012) in Triangulo Mineiro region used in the data collection analyzed in this work, Minas Gerais, Brazil. According to the study of Lopes (2010). MASL – Meters above sea level. Fragment City Watersheed Area(h a) Latitude( S) Longitude( W) Altitud e (MAS L) Tree density (ind.ha-1) Água Fria Araguari Rio Paranaíba 200 18°29'50" 48°23'03" 680 839 Ipiaçu Ipiaçu Rio Paranaíba 40 18°43'39" 49°56'22" 530 837 Monte Carmelo Monte Carmelo Rio Paranaíba 119 18°44'59" 47°30'56" 910 798 Uberaba Uberaba Rio Grande 70 19°40'35" 48°02'12" 790 805 Cruzeiro Uberlândia Rio Paranaíba 17,5 18°40'26" 48°24'32" 600 1233 Glória Uberlândia Rio Paranaíba 30 18°57'03" 48°12'22" 880 976 Irara Uberlândia Rio Paranaíba 22,3 19°08'39" 48°08'46" 930 945 Panga Uberlândia Rio Paranaíba 16 19°10'04" 48°23'41" 800 1292 Pereira Uberlândia Rio Paranaíba 35 18°51'35" 48°03'51" 890 1144 São José Uberlândia Rio Paranaíba 20 18°29'50" 48°13'53" 890 1063 Data were compiled and organized into a spreadsheet of Excel 2007, following some of the categories and parameters used in previous studies (PAULA; OLIVEIRA, 2001; GIRÃO et al., 2007). The categories used for pollination systems were: SMI - small insects (small bees, flies and wasps); LGB - large bees; WIN - wind; VSI - very small insects; BUT - butterflies; BAT - bats; MOT - moths; BTL - beetles; NID - not identified. For fruit and seed dispersal modes, the categories were: ORN 1887 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 - birds; MAM - non-flying mammals; CHI - bats; ANE - wind, AUT - autochory; NID – not identified. And for the sexual systems the categories were: DIO: dioecious; MON: monoecious; HER: hermaphrodite; NID – not identified. Each of these categories for pollination system, dispersal system and sexual system were considered reproductive ecological groups. The species richness and relative density of the species in each of the studied areas and reproductive ecological group were calculated. The relative density was calculated based on the density of each species divided by the total tree density in each area (Table 1). The sum of the relative densities of species within each reproductive ecological group was used as an estimator of the relative importance of each group. Since there were species that could not be classified into a reproductive group, the relative density used in the analyses was the percentage of the effectively classified species, excluding the non-classified plants (NID –not identified). We compared the similarity between areas based on the reproductive features with a hierarchical cluster analysis, the similarity index Morisita-Horn, based on the group average (UPGMA = unweighted Pair- Groups Method using Arithmetic Averages) (SNEATH; SOKAL, 1973) using the FITOPAC 1.6 (SHEPHERD, 2004). RESULTS Species general analysis – Some 243 tree species were found in semideciduous seasonal forest fragments, of which only three were not identified (see a complete list in Appendix 1). The species were distributed in 163 genera and 58 families. We found information on pollination system for 76.5% of the species (186 spp.) Out of the total of species, some 103 (42%) were pollinated by small insects, such as bees, wasps and flies, 22 (9%) by large bees, and 18 (7%) by moths (Figure 1A). As for dispersal mode, 78% of species (189 spp.) were classified. We observed a high percentage of zoochory as a whole (46%), and 33% were bird dispersed (81 spp). Wind dispersal accounted for 25% of the species (60 spp.) (Figure 1B). Sexual system was defined for 79.2% of species (190 spp.), of which the hermafroditism represented 54% (130 spp.), dioecy 15% (37 spp.), and monoecy 9% (23 spp.) (Figure 1C). Species and relative density – Number of species with each pollination systems showed little variation among the analyzed areas. Some 40% of the trees were predominantly pollinated by small insects (bees, wasps and flies small) (Figure 2A). Yet when considering the sum of the relative density for each pollination system, the results were more contrasting, with pollination by small insects showing large variations among the ten areas (Figure 2B). For example, this pollination system accounted for about 27% of individuals in São José area while in Água Fria it represented 69% of individuals (Figure 2B). In Ipiaçu fragment, pollination by moths and bats seemed to be more important, representing respectively 22% and 25% of the relative density and differing from other areas where between 2% to 14% were pollinated by moths and 1% to 4% pollinated by bats (Figure 2B). Panga, Monte Carmelo and Água Fria were the only fragments with species pollinated by non-flying mammals, although with very low densities (0.1%, 0.3% and 0.6% respectively). Pollination involving very small insects (VSI) had reduced values, when considering the number of plant species with this system (Figure 2B). However, when the relative density of these species was analyzed, we observed much higher importance for this type of pollination system in most areas, except Ipiaçu. Such differences in relative density of species in the areas of São José and Ipiaçu explain the separation of these two areas in the similarity analysis based on pollination systems (Figure 2C). Dispersal modes – The analysis about the ecological groups demonstrated the occurrence of many zoochorous species, and more specifically many ornithochorous species in semideciduous seasonal forests (Figure 3A). Bird dispersal showed no marked differences in the frequency of species among the ten fragments. But Ipiaçu was the fragment with the lowest representation of this dispersal system with 23% (Figure 3A). However, when analyzing species relative density, we observed that ornithochory showed greater importance in the natural processes of some fragments such as Água Fria, Irara, Monte Carmelo, Glória and Pereira reaching values of 74%, 61%, 54 %, 48% and 47%, respectively (Figure 3B). Panga, Cruzeiro and São José showed respectively 32%, 29% and 37% of individuals dispersed by non- flying mammals (Figure 3B). In the Ipiaçu fragment, the most representative dispersal modes were anemochory and autochory, with values between 37% and 23% of individuals, respectively. The Uberaba fragment also stood out by presenting approximately 36% of individuals with autochory (Figure 3B). These differences in the relative density of autochorous species in Ipiaçu and Uberaba areas explain the separation of these two areas in the similarity analysis (Figure 3C). 1888 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 Sexual systems – The sexual systems analysis showed low values of dioecy and monoecy when compared with the frequency of hermaphroditism (Figure 4A). However, considering the relative density of individuals, the importance of dioecy increased in six of the areas, indicating the importance of this process in such environments (Figure 4B). Fragments such as Irara, Glória, Monte Carmelo and Pereira showed highest relative density of dioecious individuals and dispersal by animals, when compared to other areas (Figure 4B). The similarity analysis for the sexual system using the relative density of individuals (Figure 4C), highlighted the Irara fragment with the highest relative density of monoecious and dioecious species. Figure 1. Number of species found in each ecological reproductive groups found in ten fragments of semideciduous forests of Triangulo Mineiro, Minas Gerais, Brazil. (A) Pollination systems: SMI – small insects (small bees, flies and wasps); MOT – moths; BAT – bats; VSI – very small insects; BTL – beetles; BUT – butterflies; MAM – non-flying mammals; LGB – large bees; WIN – wind; NID – not identified. (B) - Dispersal systems: ANE – wind; ORN – birds; MAM – non-flying birds; CHI – bats; AUT – autochory; NID – not identified. (C) - Sexual systems: DIO – dioecious; MON – monoecious; HER – hermaphrodite; NID – not identified. (A) (B) (C) N um b er o f sp ec ie s 1889 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 Figure 2. Pollination system in ten fragments of semideciduous seasonal forests of Triangulo Mineiro, Minas Gerais, Brazil. (A) Percentage of the number of species in each pollination system. Number of species analyzed in each area on the top of the column, (B) Percentage of the relative density represented by the sum of the species density in each pollination system; and (C) Cluster of similarity based on the relative density of the pollination systems using the UPGMA method. WIN – wind; VSI – very small insects; SMI – small insects (small bees, flies and wasps); MOT – moths; MAM – non-flying mammals; LGB – large bees; BUT – butterflies; BTL – beetles; BAT – bats; NID – not identified. % o f sp ec ie s 77 48 98 85 73 87 96 88 101 79 % o f re la ti v e d en si ty (C) (B) (A) 1890 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 Figure 3. Dispersal system in ten fragments of semideciduous seasonal forests of Triangulo Mineiro, Minas Gerais, Brazil. (A) Percentage of the number of species in each dispersal system. Number of species analyzed in each area on the top of the column, (B) Percentage of the relative density represented by the sum of the species density in each dispersal system; and (C) Cluster of similarity based on the relative density of the dispersal systems using the UPGMA method. ORN – birds; MAM – non-flying birds; CHI – bats; AUT – autochory; ANE – wind; NID – not identified. % o f sp ec ie s 76 48 96 82 73 86 93 86 100 79 % o f re la ti v e d en si ty (C) (B) (A) 1891 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 Figure 4. Sexual system in ten fragments of semideciduous forests of Triangulo Mineiro, Minas Gerais, Brazil. (A) Percentage of the number of species in each sexual system. Number of species analyzed in each area on the top of the column, (B) Percentage of the relative density represented by the sum of the species density in each sexual system, and (C) Cluster of similarity based on the relative density of the sexual systems using the UPGMA method. MON – monoecious; HER – hermaphrodite; DIO – dioecious; NID – not identified. % o f sp ec ie s 77 48 98 85 73 87 96 88 101 79 % o f re la ti v e d en si ty (C) (B) (A) 1892 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 DISCUSSION The semideciduous seasonal forests studied here showed varied frequencies of pollination systems, despite the relatively high frequency for some systems. In plant communities with high abundance of flowers, the quality and quantity of resources offered varies from species to species, so that pollinators may select some species over others. However there are pollinator species, especially bees, flies and wasps, which can use plant species with different floral traits (GEBER; MOELLER, 2006). Therefore, pollination by these groups can be considered generalist. In the ten studied areas these pollinators were the most important. For gallery forests (sensu RIBEIRO; WALTER 2008) in the Cerrado region, this pollination system represents 45% of species (PAULA; OLIVEIRA, 2001), in typical cerrado s.s. formations (sensu RIBEIRO; WALTER 2008) it represents 44% (OLIVEIRA; GIBBS, 2000), but in a rainforest in Costa Rica it represents only 18% (KRESS; BEACH, 1994). Therefore, the main pollinators for the cerrado s.s., gallery forests and semideciduous seasonal forests in the region are the animals included in this small insects group, different from moist rain forest areas, which have distinct, perhaps more specialized pollinators. As for the dispersal systems, almost half of the studied species in forest remnants was dispersed by animals (46%), but this value is likely to be even higher due to 22% of non–classified species. For semideciduous forests in the Atlantic forest region, zoochory represented 70% of plant species (CARVALHO et al., 2006), and in the cerrados and semideciduous forests in the region of Mato Grosso zoochory was about 58% (TAKAHASI; FINA, 2004). In the forests of the Cerrado region as a whole, zoochory represents 67%, and in gallery forests up to 71% of the species (OLIVEIRA; PAULA, 2001). Thus, zoochorous dispersal mode is the most common among arboreal plants, and the Cerrado birds stand out as the main seed and fruit dispersers (GOTTSBERGER; SILBERBAUER- GOTTSBERGER, 2006). The ornithochory was present in 33% of species in fragments of semideciduous forests here studied. The dispersal by birds is very common in the region forests, and may include up to 57% (OLIVEIRA; PAULA, 2001) or even 70% of gallery forest species (PINHEIRO; RIBEIRO, 2001). Despite the dominance of zoochory in the studied semideciduous seasonal forest fragments, abiotic seed and fruit dispersal by wind and gravity (anemochory and autochory respectively) represent important process in some of these forests. Especially anemochory is a common dispersal mechanism on seasonal environments, since drought facilitates the carrying of propagules to longer distances. In the ten forest fragments the hermaphroditism was the predominant sexual system (54%) followed by dioecy (15%) and monoecy (9.5%). In a rainforest in Costa Rica, 65.5% of the species are hermaphrodites, 23.1% and 11.4% are respectively monoecious and dioecious (BAWA et al., 1985b). For the cerrado savanna physiognomies (sensu RIBEIRO; WALTER 2008) in a reserve of CPAC - Agricultural Research Center, 88% of the species are hermaphrodites, and 7% and 5% are monoecious and dioecious respectively (RIBEIRO et al., 1985). Thus, hermaphroditism was the predominant sexual system in tropical forests, cerrado physiognomies and semideciduous forests. The ten areas were more similar in terms of the number of species in each of the reproductive ecological groups than in terms of relative density of individuals in each group. This means that the differences between areas are less related to species turnover and more related to the species relative importance, which changes from area to area. The relative density may indicate more quickly the interactions between species and environmental conditions of the forests remnants, including degradation (LOPES, 2010). Ipiaçu was the most distinct area due to the relative density of species pollinated by bats and moths. This difference may be associated with the historical use of the area, which allowed the establishment of species with specialized pollination agents, but it is somewhat surprising since this is clearly the most degraded fragment. The Ipiaçu fragment presented occupation by pastureland and annual crops in the surrounding area, and signals of selective logging, forming gaps where vegetation consisted of shrub species and juveniles, with few large individuals (LOPES, 2010). Despite degradation, high relative density values were found for plants pollinated by relatively specialized moths and bats, both in the canopy and understory layers. The species Hymenaea courbaril and Luehea divaricata pollinated by bats and Piptadenia gonoacantha by moths, had the highest relative densities in this disturbed fragment. Studies conducted in the Atlantic Forest in Pernambuco (GIRÃO et al., 2007) indicated a reduction in specialized pollination systems in small and degraded forest fragments. The idea is that fragmentation and disturbance would select generalist pollination systems as small insect (SMI) 1893 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 and very small insects (VSI). But those systems seems to be the most common and widespread in both semideciduous seasonal forests and gallery forests in the region (OLIVEIRA; PAULA, 2001) and we could not find a clear relationship between disturbance and the frequency of these systems, as described for the Atlantic Forest in Pernambuco (GIRÃO et al., 2007). According to a study conducted in a floodplain dipterocarp forest in Sarawak, Malaysia, the flowers present in open areas, as forest gaps, have characteristics that attract specialized pollinators (MOMOSE et al., 1998). These forest gaps are formed by a smaller number of species and present low productivity. These characteristics are similar to those observed in Ipiaçu fragment and may help to understand pollination systems found in this area. As for the dispersal modes, Uberaba and Ipiaçu differed more than other areas in the similarity analysis, presenting the highest relative importance for species dispersed by wind and gravity. Autochory has been associated with pioneering species and arid regions (PIJL, 1969). This dispersal mode is considered, therefore, a limiting process in closed forests, as can be seen in the gallery forest where only 3% of the plants have this type of dispersal (PINHEIRO; RIBEIRO, 2001). Although the Uberaba fragment showed the highest percentage of autochorous species, the vegetation of this area is in an advanced stage of succession, with large individuals (LOPES, 2010). In this fragment, species of Galipea jasminiflora and Micrandra elata are dispersed by autochory, and present high relative density in the understory and canopy, respectively. Therefore, autochory seems to be important even in better conserved forests in the region. As for anemochory, some authors consider this type of dispersion associated with open habitats (OLIVEIRA; MOREIRA, 1992), this system tends also to decrease in denser environments, because they prevent the action of wind (PINHEIRO; RIBEIRO, 2001). But in Ipiaçu fragment, anemochory and autochory systems had higher percentages when compared with the zoochory. As the Ipiaçu fragment is the most open area, probably a result of disturbance and gaps, wind dispersed species have better chances to spread their diaspores in this area. However, despite differences in Uberaba and Ipiaçu, dispersal by birds and non- flying mammals predominated in most semideciduous forest studied. Irara fragment differed by the relatively high abundance of dioecious and monoecious plants, while other areas showed lower values. The dioecy and monoecy can be seen as sexual systems associated with pollination by small insects and dispersal by animals, which can be most directly affected by environmental changes in forests (OLIVEIRA, 1996). On the other hand, dioecy has been associated also with vegetation in isolated islands or where pollination may be somewhat limited (BAWA et al., 1985b). For the semideciduous seasonal forests of Triangulo Mineiro, we observed that more than 50% of species pollinated by small insects were hermaphrodites, 21% were dioecious and 15% were monoecious. The guild of small insects is very diverse and is commonly considered the most important group of pollinators of dioecious plants (OLIVEIRA, 1996). In the rainforests of Costa Rica, 66% of species pollinated by small insects are dioecious (BAWA et al., 1985a,b). This means that there is a predominance of dioecy in rainforests, probably due to the diversity of pollinators and environmental stability of these forests. This stability allows the maintenance of viable dioecious plant populations pollinated by small insects, and contrasts with seasonal and degraded environments such as semideciduous season forests studied here. However this small insect pollination system, is not well defined in many cases and tends to be subdivided in plants adapted to different groups of pollinators, as small bees, flies, and wasps, which may exhibit specialized and distinct requirements for the pollination process (KRESS; BEACH, 1994). The predominance of certain systems such as hermaphroditism and small insect pollination may represent an effect of fragmentation and degradation in these areas, influencing the loss of diversity of ecological groups. The predominance of generalist pollinators may also lead to increased frequency of self-compatible hermaphrodites plants (GIRÃO et al., 2007). CONCLUSION The study points out to a great diversity of reproductive ecological groups in the semidecidous seasonal forests in the Triangulo Mineiro. We observed a trend of generalist reproductive characteristics, which seem to be associated with the poorly conserved forest fragments studied. This is even clearer when using the relative density of the species, which may indicate that changes in environmental conditions affected species density and relative importance well before they affect species turnover. But some reproductive 1894 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 characteristics associated with more pristine habitats, as e.g. moth and bat pollination, are still present even in the most disturbed remnants. ACKNOWLEDGMENTS We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq for financial support to this research. CAPES provided a Post-doctoral grant to V.S. Vale. Part of the analyses and manuscript preparation was carried out with support of the PELD project (CNPq/FAPEMIG 403733/2012-0). RESUMO: A degradação dos ecossistemas gera a perda das interações entre animais e plantas e a mudança na frequência de sistemas de polinização, modos de dispersão e sistema sexual das plantas. O objetivo do estudo foi comparar os grupos ecológicos reprodutivos de árvores entre remanescentes de florestas estacionais semideciduais no Triângulo Mineiro, Brasil, e entender a organização destas comunidades. Foi analisada a biologia reprodutiva de 243 espécies arbóreas encontradas em 10 fragmentos que apresentavam diferentes níveis de perturbação ambiental. A ocorrência e densidade relativa das espécies foi utilizada para estimar a importância de cada característica reprodutiva. O estudo baseou-se na compilação de dados presentes em trabalhos especializados e estudos comunitários realizados na região. As espécies dessas comunidades foram agregadas em grupos ecológicos reprodutivos de acordo com suas características. A frequência das espécies foi, até certo ponto, semelhante entre os fragmentos. A polinização por pequenos insetos (abelhas, moscas e vespas pequenas) representou 42% no total das espécies, a dispersão pelas aves foi de 35% e o sistema sexual que se destacou foi o hermafroditismo com 54%. Diferenças mais evidentes foram encontradas entre as densidades relativas de cada grupo ecológico reprodutivo. Polinização por morcegos e mariposas, relativamente especializadas, bem como dispersão pelo vento foram comuns na área com maior perturbação. No entanto, características reprodutivas consideradas generalistas prevaleceram nos fragmentos. PALAVRAS-CHAVE: Sistema de polinização. Sistema de dispersão. Sistema sexual. Fragmentos florestais. REFERENCES BAWA, K. S., BULLOCK, S. H., PERRY, D. R., COVILLE, R. E.; GRAYUM, M. H. 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In: Simpósio sobre recursos naturais e sócio-econômicos do Pantanal, 4o, 2004, Corumbá, Anais do IV Simpósio sobre recursos naturais e sócio-econômicos do Pantanal Corumbá: Embrapa, 2004. p.1-7. TALORA, D. C., MORELLATO, P. C. Fenologia de espécies arbóreas em uma floresta de planície litorânea do sudeste do Brasil. Revista Brasileira de Botânica, São Paulo, v. 23, n. 1, p. 13-26, 2000. VAMOSI, J. C., KNIGHT, T. M., STEETS J. A., MAZER S. J.; BURD, M., ASHMAN, T. L. Pollinations decays in biodiversity hotspots. Proceeding of the National Academy of Sciences, Boston, v. 103, n. 4, p. 956-961, 2006. 1897 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 Appendix 1 – Woody species observed in semideciduous forests remnants of the Triangulo Mineiro region and their reproductive ecological groups. The categories used for pollination systems were: SMI - small insects (small bees, flies and wasps); LGB - large bees; WIN - wind; VSI - very small insects; BUT - butterflies; BAT - bats; MOT - moths; BTL - beetles; NID - not identified. For the sexual systems the categories were: DIO: dioecious; MON: monoecious; HER: hermaphrodite; NID – not identified. And for fruit and seed dispersal systems, the categories were: ORN - birds; MAM - non-flying mammals; CHI - bats; ANE - wind, AUT - autochory; NID – not identified. *Allien species spontaneous in the region. Families Species Pollination systems Sexual systems Dispersal systems Anacardiaceae Astronium fraxinifolium Schott NID DIO ANE Anacardiaceae Astronium nelson-rosae D.A. Santin SMI DIO ANE Anacardiaceae Myracrodruon urundeuva Allemão SMI DIO ANE Anacardiaceae Lithrea molleoides (Vell.) Engl. SMI DIO ORN Anacardiaceae Tapirira guianensis Aubl. SMI DIO ORN Anacardiaceae Tapirira obtusa ( Benth.) J.F. Mitch SMI DIO ORN Annonaceae Annona cacans Warm. BTL HER MAM Annonaceae Annona montana Macfad. NID NID NID Annonaceae Cardiopetallum calophyllum Schlecht. BTL HER ORN Annonaceae Duguetia lanceolata St. Hil. BTL HER MAM Annonaceae Guatteria australis A. St.-Hil. BTL NID NID Annonaceae Porcelia macrocarpa (Warm.) R.E.Fr. BTL NID NID Annonaceae Rollinia sylvatica (A.St.-Hill.) Mart. BTL MON ORN Annonaceae Unonopsis lindmanii R.E.Fr. SMI HER ORN Annonaceae Xylopia aromatica (Lam.) Mart. VSI HER ORN Annonaceae Xylopia brasiliensis Spreng. BTL MON ORN Annonaceae Xylopia sericea St. Hil. BTL HER ORN Apocynaceae Aspidosperma cuspa (H.B.K.) S.F. Blake MOT HER ANE Apocynaceae Aspidosperma cylindrocarpum M.Arg. MOT HER ANE Apocynaceae Aspidosperma discolor A. DC. MOT HER ANE Apocynaceae Aspidosperma olivaceum M.Arg MOT HER ANE Apocynaceae Aspidosperma parvifolium A. DC. MOT HER ANE Apocynaceae Aspidosperma polyneuron Müll. Arg. MOT NID ANE Apocynaceae Aspidosperma subincanum Mart. ex A. DC. MOT HER ANE Aquifoliaceae Ilex cerasifolia Reissek NID NID NID Araliaceae Aralia warmingiana (Marchal) J. Wen SMI HER ORN Araliaceae Dendropanax cuneatum (DC.) Decne. et Planch SMI DIO ORN Araliaceae Schefflera morototoni (Aubl.) Maguire et al. SMI HER MAM Arecaceae Acrocomia aculeata (Jacq.) Lodd. BTL MON MAM Asteraceae Piptocarpha macropoda Baker SMI HER ANE Bignoniaceae Handroanthus impetiginosus (Mart. Ex DC.) Mattus LGB HER ANE Bignoniaceae Jacaranda cuspidifolia Mart. Ex A.DC. NID HER ANE Bignoniaceae Jacaranda macrantha Cham. NID HER ANE Bignoniaceae Tabebuia roseo-alba (Ridley) Sandwith LGB HER ANE Bignoniaceae Tabebuia serratifolia (Vahl) Nicholson LGB HER ANE Boraginaceae Cordia alliodora Cham. MOT HER ANE Boraginaceae Cordia sellowiana Cham. SMI HER MAM Boraginaceae Cordia superba Cham. SMI NID MAM 1898 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 Boraginaceae Cordia trichotoma SMI NID ANE Burseraceae Protium heptaphyllum (Aubl.) March. SMI DIO ORN Cannabaceae Celtis iguanaea (Jacq.) Sargent. SMI NID ORN Cannabaceae Trema micrantha (L.) Blume NID NID NID Cardiopteridaceae Citronella paniculata (Mart) R.A.Howard NID NID NID Caricaceae Jacaratia spinosa (Aubl) A.DC MOT DIO AUT Celastraceae Cheiloclinium cognatum (Miers.) A.C.Sm. VSI HER MAM Celastraceae Maytenus floribunda Reiss. NID NID NID Celastraceae Maytenus robusta Reissek NID NID NID Celastraceae Maytenus sp. NID NID NID Celastraceae Salacia elliptica (Mart.ex Schult.) G.Don SMI MON MAM Chrysobalanaceae Hirtella glandulosa Spreng. BUT HER ORN Chrysobalanaceae Hirtella gracilipes (HooK f.) Prance BUT HER ORN Chrysobalanaceae Hirtella racemosa Lam. BUT NID ORN Clusiaceae Calophyllum brasiliense Cambess SMI DIO CHI Clusiaceae Garcinia brasiliensis Mart. NID NID NID Combretaceae Terminalia argentea Mart. & Zucc. SMI HER ANE Combretaceae Terminalia glabrescens C. Zucc. SMI HER ANE Combretaceae Terminalia phaeocarpa Eichl. SMI HER ANE Cunoniaceae Lamanonia ternata Vell. SMI HER ANE Ebenaceae Diospyros hispida A. DC. VSI DIO MAM Elaeocarpaceae Sloanea hirsuta (Schott) Planch. ex Benth NID HER MAM Erythroxylaceae Erythroxylum daphnites Mart. SMI HER ORN Erythroxylaceae Erythroxylum deciduum St. Hil. SMI HER ORN Euphorbiaceae Acalypha gracilis (Spreng.) Müll. Arg. WIN NID AUT Euphorbiaceae Alchornea glandulosa Poepp. & Endl. VSI DIO ORN Euphorbiaceae Mabea fistulifera Mart. BAT MON AUT Euphorbiaceae Maprounea guianensis Aubl. SMI MON ORN Euphorbiaceae Micrandra elata Müll. Arg. NID NID AUT Euphorbiaceae Pera glabrata (Schott.) Baill. SMI DIO NID Euphorbiaceae Sapium glandulosum (L.) Morong NID NID NID Fabaceae Acacia polyphilla DC. SMI HER ANE Fabaceae Albizia niopoides (Spruce ex. Benth.) Brukat MOT HER AUT Fabaceae Albizia polycephala (Benth.) Killip SMI MON AUT Fabaceae Anadenanthera colubrina (Vell) Brenan SMI HER AUT Fabaceae Andira fraxinifolia Benth. SMI HER NID Fabaceae Andira ormosioides Benth. NID HER NID Fabaceae Apuleia leiocarpa (Vog.) Macbr. LGB HER ANE Fabaceae Bauhinia rufa (Bong.) Steud BAT HER AUT Fabaceae Bauhinia ungulata L. BAT HER AUT Fabaceae Calliandra foliolosa Benth MOT HER AUT Fabaceae Cassia ferruginea Schrad. ex DC. LGB HER ANE Fabaceae Centrolobium tomentosum Guillem. ex Benth. LGB HER ANE Fabaceae Copaifera langsdorffii Desf. SMI HER ORN Fabaceae Dipterix alata Vogel SMI HER MAM Fabaceae Enterolobium contortisiliquum (Vell.) Morong SMI HER MAM 1899 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 Fabaceae Hymenaea courbaril L. var. stilbocarpa (Hayne) Lee & Lang. BAT HER MAM Fabaceae Inga laurina (Sw.) Willd MOT HER MAM Fabaceae Inga marginata Willd. SMI MON CHI Fabaceae Inga sessilis (Vell.)Mart. BAT HER CHI Fabaceae Inga vera Willd. SMI MON ORN Fabaceae Lonchocarpus cultratus (Vell.)Az.-Tozzi & H.C.Lima SMI HER AUT Fabaceae Machaerium acutifolium Vog. SMI HER ANE Fabaceae Machaerium brasiliense Vogel NID HER ANE Fabaceae Machaerium hirtum (Vell.) Stellfeld SMI HER ANE Fabaceae Machaerium nictitans (Vell.) Benth. SMI HER ANE Fabaceae Machaerium opacum Vogel NID HER NID Fabaceae Machaerium stipitatum Vog. SMI MON ANE Fabaceae Machaerium villosum Vog. SMI HER ANE Fabaceae Myroxylon peruiferum L.F. SMI MON ANE Fabaceae Ormosia arborea (Vell.) Harms SMI MON AUT Fabaceae Peltophorum dubium (Spreng.) Taub. SMI HER ANE Fabaceae Piptadenia gonoacantha (Mart.) Macbride MOT HER AUT Fabaceae Platyciamus regnellii Benth. LGB HER ANE Fabaceae Platypodium elegans Vog. LGB HER ANE Fabaceae Pterodon emarginatus Vogel NID HER NID Fabaceae Sclerolobium paniculatum Vog. var rubiginosum (Tul.) Benth. SMI HER ANE Fabaceae Sweetia fruticosa Spreng. SMI HER ANE Fabaceae Vatairea macrocarpa (Benth.)Ducke NID HER NID Fabaceae Zollernia ilicifolia(Brongn.)Vogel NID HER AUT Lacistemataceae Lacistema aggregatum (Berg.) Rusby NID HER ORN Lamiaceae Aegiphila sellowiana Cham. SMI DIO ORN Lamiaceae Vitex polygama Cham. LGB HER ORN Lauraceae Ocotea corymbosa (Meissn.) Mez. SMI DIO ORN Lauraceae Cryptocaria aschersoniana Mez. SMI HER MAM Lauraceae Endlicheria paniculata (Spreng.) Macbride SMI HER ORN Lauraceae Nectandra cissiflora Nees. SMI HER ORN Lauraceae Nectandra megapotamica (Spreng.) Mez VSI MON ORN Lauraceae Nectandra membranacea ssp cuspidata Ness Rower SMI MON ORN Lauraceae Ocotea minarum (Nees.) Mez. SMI NID ORN Lauraceae Ocotea pulchella (Ness.) Mez. SMI DIO ORN Lauraceae Ocotea spixiana (Nees) Mez. SMI DIO ORN Lecythidaceae Cariniana estrellensis (Raddi) O. Kuntze LGB HER ANE Lythraceae Lafoensia pacari A.ST.-Hil. (syn. L. densiflora Pohl) NID NID NID Malpighiaceae Byrsonima laxiflora Griseb. LGB HER ORN Malvaceae Apeiba tibourbou Aubl. LGB HER ORN Malvaceae Ceiba speciosa (A.St.-Hil) Ravenna BUT HER ANE Malvaceae Eriotheca candolleana (K. Sch.) A. Robyns LGB HER ANE Malvaceae Eriotheca gracilipes (K. Sch.) A. Robyns LGB HER ANE 1900 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 Malvaceae Eriotheca pubescens (Mart. & Zucc) Schott&Endl. LGB HER ANE Malvaceae Guazuma ulmifolia Lam. SMI HER ORN Malvaceae Luehea divaricata Mart. LGB HER ANE Malvaceae Luehea grandiflora Mart. & Zucc. BAT HER ANE Malvaceae Luehea paniculata Mart. LGB HER ANE Malvaceae Pseudobombax longiflorum (Mart. & Zucc) A. Robyns BAT HER ANE Malvaceae Pseudobombax tomentosum (Mart.& Zucc) A.Robyns MAM HER ANE Malvaceae Quararibea turbinata (Sw.) Poir. MAM NID CHI Melastomataceae Miconia cuspidata Naud. SMI HER ORN Melastomataceae Miconia latecrenata (DC.) Naudim SMI NID ORN Melastomataceae Miconia minutiflora (Bonpl.) DC. NID NID NID Meliaceae Guarea guidonia (L.) Sleumer BUT DIO ORN Meliaceae Cabralea canjerana (Vell) Mart. SMI DIO ORN Meliaceae Cedrella fissilis Vell. MOT HER ANE Meliaceae Guarea kunthiana A. Juss. BUT DIO ORN Meliaceae Trichilia catigua A. Juss SMI NID ORN Meliaceae Trichilia claussenii C. DC. SMI NID ORN Meliaceae Trichilia elegans A. Juss. SMI NID ORN Meliaceae Trichilia pallida Sw. SMI NID ORN Monimiaceae Mollinedia widgrenii A. DC. NID NID NID Moraceae Sorocea bomplandii (Baill.) W. Burg. NID DIO ORN Moraceae Ficus clusiifolia Schott VSI NID NID Moraceae Ficus guaranitica Chodat VSI NID CHI Moraceae Ficus obtusiuscula (Miq.) Miq VSI NID NID Moraceae Ficus pertusa L.F. VSI NID CHI Moraceae Ficus trigona L.F. SMI NID NID Moraceae Ficus sp1 VSI NID NID Moraceae Ficus sp2 VSI NID NID Moraceae Maclura tinctoria D. Don. Ex Stend. VSI MON CHI Moraceae Pseudolmedia laevigata Troc. SMI DIO ORN Myristicaceae Virola sebifera Aubl. VSI DIO ORN Myrsinaceae Ardisia ambigua Mez SMI NID ORN Myrsinaceae Myrsine coriacea R.Br. SMI DIO ORN Myrsinaceae Myrsine leuconeura Mart. NID NID NID Myrsinaceae Myrsine umbellata Mart. SMI DIO ORN Myrtaceae Psidium sartorianum (Berg.) Nied. NID HER NID Myrtaceae Calyptranthes clusiifolia O.Berg. NID NID NID Myrtaceae Calyptranthes widgreniana Berg. SMI HER ORN Myrtaceae Campomanesia guazumifolia (Cambess.)O.Berg. SMI HER ORN Myrtaceae Campomanesia velutina Berg. SMI HER ORN Myrtaceae Eugenia florida DC. SMI HER ORN Myrtaceae Eugenia involucrata DC. SMI HER ORN Myrtaceae Eugenia ligustrina (Sw.) Willd. NID HER ORN Myrtaceae Eugenia subterminalis DC. NID HER NID Myrtaceae Gomidesia lindeniana Berg. SMI HER ORN 1901 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 Myrtaceae Myrcia splendens (Sw.)DC. SMI HER ORN Myrtaceae Myrcia tomentosa (Aubl.) DC. SMI HER ORN Myrtaceae Myrciaria glanduliflora (Kiaersk.) Mattos & D.Legrand NID NID NID Myrtaceae Myrciaria tenella (DC.) Berg. SMI HER ORN Myrtaceae Psidium longipetiolatum D.Legrand NID HER NID Myrtaceae Psidium rufum DC. NID HER NID Myrtaceae Siphoneugena densiflora Berg. SMI HER ORN Myrtaceae Syzygium jambos (L.) Aston.* NID NID NID Myrtaceae Myrtaceae 1 NID NID NID Myrtaceae Myrtaceae 2 NID NID NID Nyctaginaceae Guapira opposita (Vell.)Reitz SMI DIO NID Nyctaginaceae Guapira venosa (Choisy)Lundell SMI DIO ORN Nyctaginaceae Neea hermaphrodita Sp. Moore VSI DIO ORN Ochnaceae Ouratea castaneifolia DC. Engl. LGB HER ORN Olacaceae Heisteria ovata Benth. NID HER CHI Oleaceae Chionanthus trichotomus (Vell.) P.S.Green NID HER CHI Opiliaceae Agonandra brasiliensis Miers. NID DIO MAM Phyllanthaceae Margaritaria nobilis L.F. NID DIO AUT Phyllanthaceae Phyllanthus acuminatus Vahl. NID NID NID Piperaceae Piper amalago L. SMI MON NID Piperaceae Piper arboreum Aubl. SMI MON CHI Polygonaceae Coccoloba mollis Cass. NID HER ORN Proteaceae Roupala brasiliensis Klotz. MOT HER ANE Rhamnaceae Rhamnidium elaeocarpum Reiss. SMI HER ORN Rubiaceae Amaioua guianensis Aubl. MOT DIO MAM Rubiaceae Chomelia pohliana M.Arg. NID HER ORN Rubiaceae Cordiera sessilis (Vell.) Kuntze SMI DIO MAM Rubiaceae Coussarea hydrangeaefolia (Benth.) B. & H. MOT HER ORN Rubiaceae Coutarea hexandra (Jacq.) K. Schum. NID HER ANE Rubiaceae Faramea hyacinthina Mart. SMI HER ORN Rubiaceae Genipa americana L. SMI HER NID Rubiaceae Guettarda viburnioides Cham. & Schl. SMI HER ORN Rubiaceae Ixora brevifolia Benth. NID HER NID Rubiaceae Machaonia brasiliensis (Hoffmanss. Ex Humb.)Cham.&Schltdl. NID HER NID Rubiaceae Rudgea viburnioides (Cham.) Benth. NID HER ORN Rubiaceae Simira sampaioana (Standl.)Steyerm. SMI HER ANE Rubiaceae Tocoyena formosa (Cham.& Schltdl.) K.Schum. MOT HER NID Rutaceae Galipea jasminiflora (A.St.-Hill)Engl. NID NID AUT Rutaceae Metrodorea nigra A. St.-Hill. NID NID NID Rutaceae Metrodorea stipularis Mart. SMI HER ORN Rutaceae Pilocarpus spicatus A.St.-Hil. NID NID NID Rutaceae Zanthoxylum riedelianum Engl. SMI DIO ORN Salicaceae Casearia gossypiosperma Briquet. SMI HER ANE Salicaceae Casearia grandiflora Camb. SMI HER ORN Salicaceae Casearia rupestris Eichl. NID HER ORN 1902 Diversity of reproductive… DEUS, F. F. et al. Biosci. J., Uberlândia, v. 30, n. 6, p. 1885-1902, Nov./Dec. 2014 Salicaceae Casearia sylvestris Sw. SMI HER ORN Salicaceae Prockia crucis P.Browne ex L. NID NID NID Salicaceae Xylosma cf. prockia (Turcz.) Turcz. NID NID NID Sapindaceae Allophyllus edulis (A.St.-Hil., Cambess.& A.Juss.) Radlk. SMI MON AUT Sapindaceae Allophyllus racemosus Sw SMI NID ORN Sapindaceae Cupania vernalis Camb. BUT MON ORN Sapindaceae Dilodendron bipinatum Radlk. SMI NID NID Sapindaceae Magonia pubescens A. St.-Hil. NID NID ANE Sapindaceae Matayba elaegnoides Radlk. SMI MON ORN Sapindaceae Matayba guianensis Aubl. SMI MON ORN Sapotaceae Chrysophyllum gonocarpum (Mart.& Eichler) Engl. VSI DIO ORN Sapotaceae Chrysophyllum marginatum (Hook & Corn.) Radlk. SMI HER MAM Sapotaceae Micropholis venulosa (Mab. & Eichl.) Pierri VSI HER MAM Sapotaceae Pouteria gardneri (Gartn. F.) Ducke NID MON MAM Sapotaceae Pouteria torta (Mart.) Radlk. SMI MON MAM Siparunaceae Siparuna guianensis Aubl. VSI DIO ORN Styracaceae Styrax camporum Pohl. LGB HER ORN Symplocaceae Symplocos pubescens klotzsh. ex Benth. NID DIO ORN Urticaceae Urera baccifera (L.) Gaudich. Ex Benth. NID NID ORN Verbenaceae Aloysia virgata (Ruiz & Pav) A.Juss. SMI NID ANE Vochysiaceae Callisthene major Mart. SMI HER ANE Vochysiaceae Qualea dichotoma (Mart.) Warm. LGB HER ANE Vochysiaceae Qualea jundiahy Warm. SMI HER ANE Vochysiaceae Vochysia magnifica Warm. LGB HER ANE Vochysiaceae Vochysia tucanorum (Spr.) Mart. LGB HER ANE Urticaceae Cecropia pachystachya Troc. SMI DIO CHI