FLOWERING AND POLLINATORS OF THREE DISTYLOUS SPECIES OF Psychotria (Rubiaceae) CO-OCCURRING IN THE BRAZILIAN ATLANTIC FOREST1

ABSTRACT This study investigates the flowering and pollinators of the floral morphs of three co-occurring distylous species, Psychotria conjugens Müll, P. hastisepala Müll. Arg. and P. sessilis Vell., in two consecutive flowering seasons in an Atlantic Forest fragment in southeastern Brazil. The species have diurnal, cream-colored, tubular, nectariferous flowers and their flowering occurs in the rainy season, from September to April, with little or no overlapping between species, characterizing a staggered flowering. The flowering of the long-and short-styled floral morphs of each species was synchronous, but the number of open flowers per day per morph tended to vary in each flowering season. These numbers were higher in P. sessilis and P. conjugens and, probably, resulted in higher total numbers of visits on its flowers (up to 1084 visits in P. sessilis and 756 in P. conjugens), compared to that observed in P. hastisepala (up to 71). There was a higher frequency of visits to long-styled flowers of all species. The bee Ariphanarthra palpalis was a common pollinator to all species. This bee is native to Brazil, solitary, considered relatively rare and its host plants were unknown. Other native bees (Melipona spp.) also visited the flowers of the Psychotria species. The availability of flowers with similar floral features over eight months, the staggered flowering and common pollinators appear to be part of a strategy to attract floral visitors, minimizing the competition for pollinators and then favoring the legitimate pollination of these plants.

Observations on flower visitors to Bertholletia excelsa H.B.K. and Couratari tenuicarpa A.C. Sm. (Lecythidaceae)

Bees visiting flowers of Bertholletia excelsa. (Brazil Nut tree) and Couratari tenuicarpa were collected, their behavior described and the pollen found clinging to their dorsal thorax and stored on their legs was identified. Female bees of Xylocopa frontalis(Olivier) and males of Eulaema mocsaryi (Friese) are apparently effective pollinators of Couratari in igapó near Manaus. Female bees of Euplusia seabrai Moure in litt., Epicharis umbraculata (Fabricius), Epicharis rustica (Olivier) and Eulaema nigrita(Lepeletier), as well as male bees of Eulaema cingulata(Fabricius) and Eulaema nigrita are apparently effective pollinators of adult Brazil Nut trees in the Aleixo plantation near Manaus. Only large bees capable of uncurling the floral androecium can effectively pollinate Couratari or Bertholletia.Pollen analysis indicated that all bees captured carried pollen of the host tree in question and had been foraging on flowers of plant species common in secondary growth. Secondary growth near the Aleixo plantation supports a bee guild which appeared to effectively pollinate almost every flower on the Brazil Nut tree studied. Proximity to primary forest (and to those Euglossine bee species which occur only in primary forest) therefore does not appear to be necessary for pollination of Brazil Nut trees.In the Aleixo plantation chronic low fruit set is probably due to some factor other than pollination. Since natural occurrences of Brazil Nut trees to the north and south of Manaus are associated with a higher soil fertility, low production at the Aleixo plantation may be due to deficiencies of the soil.

Reproductive biology of Bellucia (MELASTOMATACEAE)

The reproductive biology of five of the seven species of Bellucia (Melastomataceae), a genus of shrubs and small trees, was investigated in Amazonia. Sucessful fruit-set by Bellucia requires floral visitation by bees. The flowers are produced continuously all year, and are visited by a wide variety of female bees, the principal pollinators being Xylocopa, Centris, Ptilotopus, Epicharis, Eulaema, Bombus, and Oxaea. The floral attractants are color and the odor produced by the pollen, stamens, and petals; the reqard is pollen. Three species of Bellucia are self-incompatible. Indiscriminate visitor behavior and lack of phenological, morphological, or genetic barriers lead to hybridization between sympatric species of Bellucia, and no more than two species occupy the same habitat at anu one locality. Bellucia produces berries with numerous small seeds, and is dispersed by birds, bats, monkeys, tapirs, turtles, and ants. Seedling establisment requires full sunlight, and occurs on a variety of soil types. The reproductive strategy is interpreted as that of a pioneer species.

Heliconia acuminata reproductive success is independent of local floral density

Reproductive plants in tropical forests are patchily distributed, with some in large aggregations of reproductive consepecifics while others are relatively isolated. This variation in floral density is hypothesized to have a major effect on plant reproductive success, since individuals in higher density neighborhoods can attract more or higher quality pollinators. We experimentally tested this hypothesis with populations of the understory herb Heliconia acuminata in central Amazonia. We created replicated plots in which reproductive plant density spanned the range of naturally occurring floral neighborhood size, then measured three surrogates of plant fitness in focal plants in each array. There was no significant difference between any of the three floral neighborhood treatments in total seed production, fruit set, or the number of seeds produced per fruit. Pollinator visitation rates to plants in all treatments were extremely low, with many plants not visited at all during the observation period. This could be because H. acuminata's hummingbird pollinators are unable to find the widely scattered reproductive plants, however this hypothesis appears unlikely. Instead, natural flowering plant densities may simply be below the threshold value at which neighborhood effects become important, even in "high-density" aggregations. Nutrient limitation, selective fruit abortion, and reproduction via male rather than female function may also be playing a role. We argue the absence of neighborhood effects may be a general phenomenon in central Amazonian forests, though additional experiments with other plant-pollinator systems are needed to determine the extent to which this hypothesis is supported.

Flowering levels, harvest season and yields of cupuassu (Theobroma grandiflorum)

Cupuassu (Theobroma grandiflorum), a specie native to Amazonia, has been planted commercially in Brazil to satisfy the demand for the flavorful juice obtained from the pulp around its seeds. The trees are notorious for low and irregular fruit production. Data gathered over two seasons from trees in a germplasm collection in Pará, Brazil, showed that some of them fruited more regularly than others. Differences in fruit production correlated to differences in flower production. Tree-to-tree variation in flower production, fruit production, and consistency of both over time suggest considerable scope for improving yields by selection. Hand pollinations resulted in a much higher frequency of fruit set than open pollinations, indicating that lack of effective pollination is also a reason for low yield. However, attempts to increase the level of effective pollination are handicapped by low knowledge about the pollinators of cupuassu and their behavior.

Interactions between carpenter bees and orchid bees (Hymenoptera: Apidae) in flowers of Bertholletia excelsa Bonpl. (Lecythidaceae)

Competition between two species of bees for the same type of floral resource may generate antagonistic behavior between them, especially in cultivated areas where food resources are limited, seasonally and locally. In this study, was tested the hypothesis of antagonism between two solitary bee species of the family Apidae, Eulaema mocsaryi (Euglossini) and Xylocopa frontalis (Xylocopini), visiting the Brazil nut flowers (Bertholletia excelsa: Lecythidaceae) in a central Amazonia agricultural area. The visitation time was analyzed to detect the possible temporal overlap in the foraging of these bees. Furthermore, was analyzed their interspecific interactions for manipulating flower species visited by an opponent species, as well as attempts to attack this opponent. The individuals of Xylocopa frontalis visited the Brazil nut flowers before Eulaema mocsaryi, although the peak visitation of both did not presented significant differences. Neither of the species manipulated flowers recently visited by opponent species, and there were practically no antagonistic interactions between them. Thus, X. frontalis and E. mocsaryi shared the same food source in the flowers of B. excelsa due to differences in their time of visits and non-aggressive way of interacting with the opponent. This result has important implications for pollinating the Brazil nut, and a possible management of X. frontalis and E. mocsaryi, since these two were the most abundant pollinators in the studied locality.

Reproductive biology of Amasonia obovata Gleason (Laminaceae)

Floral mechanisms that ensure seed production via autogamy are more likely to occur in species growing in environments where pollination is scarce. Amasonia obovata was studied in the State of Mato Grosso-Brazil, from 2009 to 2012, to analyze the morphological and reproductive characteristics, aside from investigating the association of the reproductive success with the pollinator frequency and identity. The flowering and fruiting of A. obovata was concentrated in a period of five months during the rainy season. The dichogamy in flowers of A. obovata is not clearly defined, since the sexual functions were overlapped in the male and female phases. The species is self-compatible and not apomictic. The fruiting percentage obtained by hand self-pollination did not differ from cross-breeding (F = 0.74, P =0.39). In the observations from 2010 to 2012, a hummingbird (Thalurania furcata) legitimate visited 20-100% of the flowers in the male and female phases on different A. obovata plants. Due to the high frequency, this hummingbird was considered the single potential pollinator of the species. These findings show that a limited availability of pollinators may select for floral traits and plant mating strategies that lead to a system of self-fertilization.

Composition and structure of the fig wasp community in Amazonia

An understanding of the complex ecological interaction between fig wasps and their host plants in Amazonia requires previous knowledge of their distribution and diversity. The objective of this study was to describe the composition and structure of the wasp community associated with four species of Ficus in the municipal area of Manaus, Amazonas, Brazil. A total of 600 syconia from four species were collected. The study species were: Ficus obtusifolia Kunth; Ficus citrifolia Mill; F. americana subspecies guianensis Desv. form mathewsii; and F. americana subspecies guianensis Desv. form parkeriana. Statistical analyses were used to examine the relationship between fig wasp diversity and syconium diameter, and the effect of non-pollinating wasps on numbers of pollinators and seeds. Forty three species of fig wasp were identified, distributed across seven genera (Pegoscapus, Idarnes, Aepocerus, Physothorax, Anidarnes, Heterandrium , Eurytoma). Idarnes (carme group) was the wasps genus non-pollinator with greatest number of individuals with the greatest number of infested syconia (7409 wasps in 376 syconia). Analysing non-pollinating wasp diversity in relation to fig diameter, a significant difference was observed between the four fig species. Ficus citrifolia and F. americana subspecies guianensis form mathewsii had the smallest diameter but the greatest diversity of fig wasp. Ficus obtusifolia was the only species in which the non-pollinating wasps had a significant negative effect on the number of Pegoscapus sp. and on seed production.

Polinização de Passiflora edulis f. flavicarpa (Passiflorales, Passifloraceae), por abelhas (Hymenoptera, Anthophoridae) em Campos dos Goytacazes, Rio de Janeiro

The yellow passion Passiflora edulis f. flavicarpa Deg. is allogamous, self incompatible, and it depends of insects pollinators to disseminate the pollen grains. The field work was conducted at Campos dos Goytacazes, Rio de Janeiro, Brazil, from October 17 to November 9 and December 12 to 21, 1995. It was analyzed 1565 flower buds, from which 423 showed well developed ovaries, five days after opening, this represents 27% of fruit set by natural pollination. It was observed 76,86 % of completely curved flowers, 21,22 % of partially curved flowers, and 1,92 % flowers without curvature. Five species of bees where observed on the flowers, from which two were the effective pollinator of yellow passion flower: Xylocopa (Megaxylocopa) frontalis (Olivier, 1789) and X. (Neoxylocopa) ordinaria Smith, 1874.

Floral biology of Stachytarpheta maximiliani Scham. (Verbenaceae) and its floral visitors

This study describes the reproductive system of Stachytarpheta maximiliani (Verbenaceae), including its floral biology, nectar and pollen availability and insect foraging patterns, identifying whose species act as pollinators. It was carried out in a Brazilian Atlantic rain forest site. Observations on the pollination biology of the Verbenaceae S. maximiliani indicate that their flowering period extends from September through May. Anthesis occurs from 5:30 a.m. to 5:00 p.m. and nectar and pollen are available during all the anthesis. Many species of beetles, hemipterans, flies, wasps, bees and butterflies visit their flowers, but bees and butterflies are the most frequent visitors. The flowers are generally small, gathered in dense showy inflorescences. A complex of floral characteristcs, such as violet-blue color of flowers, long floral tubes, without scents, nectar not exposed, high concentration of sugar in nectar (about 32%), allowed identification of floral syndromes (melittophily and psicophily) and function for each visitor. The bees, Bombus morio, B. atratus, Trigonopedia ferruginea, Xylocopa brasilianorum and Apis mellifera and the butterflies Corticea mendica mendica, Corticea sp., Vehilius clavicula, Urbanus simplicius, U. teleus and Heraclides thoas brasiliensis, are the most important pollinators.

Nest distribution and nesting habits of Xylocopa ordinaria Smith (Hymenoptera, Apidae) in a restinga area in the northern Rio de Janeiro State, Brazil

This paper aims to study the distribution of natural nests of Xylocopa ordinaria and characterize its nesting habits in the restinga of Grussai/Iquipari (RJ), supporting future studies on the pollinators management in the northern Rio de Janeiro state. The data obtained from Aug/2003 to Dec/2004, in an area of 11.6ha, were related to the nest distribution, substrate identification and dimensions, emergence, sex ratio, nest structure (n= 23 nests) and pollen content analysis of provisioning masses and feces. X. ordinaria nests were abundant and presented a clustered distribution. These bees do not present taxonomical affinity for nesting substrates, but preferences for wood availability and characteristics, being Pera glabrata the main substrate. X. ordinaria is a multivoltine species that tolerates co-specifics in their nests. These bees were generalist on their nectar and pollen consumption, but presented floral constancy while provisioning brood cells. These behaviors, activity along the year, flights throughout the day, and legitimate visits to flowers indicate the importance of X. ordinaria on the pollination of plants in the restinga.

Pollinator guild organization and its consequences for reproduction in three synchronopatric species of Tibouchina (Melastomataceae)

Pollinator guild organization and its consequences for reproduction in three synchronopatric species of Tibouchina (Melastomataceae). In co-flowering plant species, pollinator sharing can result in interspecific pollen transfer and fecundity reduction. Competition will be relaxed whenever there is a large amount of initial pollen supply or if each plant species occupies different habitat patches. Reproduction in Tibouchina cerastifolia (Naudin) Cogn., T. clinopodifolia (DC.) Cogn. and T. gracilis (Bonpl.) Cogn. was studied in an area of Atlantic rainforest to examine whether synchronopatry induces time partitioning among pollinator species. Eleven bee species comprised the pollinator guild. Among pollinators, there were overlaps in bee species composition and in flower visitation time. Direct competition for pollen in Tibouchina Aubl. at the study site seems to lead to different activity periods among the bee species, in which Bombus pauloensis Friese,1913 was most active earlier, while the other species were active later in the day. Bombus pauloensis, the largest bee species recorded on Tibouchina flowers, was the most important and efficient pollinator. This species harvested pollen before the other species and had the shortest handling time. The plants reproduced sexually by selfing or outcrossing, and hybridization was not avoided by incompatibility reactions at the style. The avoidance of direct competition for pollen and no pollinator partitioning among the synchronopatric species of Tibouchina may reflect a facilitative interaction among these pioneer plants.

Effect of Citrus floral extracts on the foraging behavior of the stingless bee Scaptotrigona pectoralis (Dalla Torre)

Effect of Citrus floral extracts on the foraging behavior of the stingless bee Scaptotrigona pectoralis (Dalla Torre). Stingless bees have an important role as pollinators of many wild and cultivated plant species in tropical regions. Little is known, however, about the interaction between floral fragrances and the foraging behavior of meliponine species. Thus we investigated the chemical composition of the extracts of citric (lemon and orange) flowers and their effects on the foraging behavior of the stingless bee Scaptotrigona pectoralis. We found that each type of flower has its own specific blend of major compounds: limonene (62.9%) for lemon flowers, and farnesol (26.5%), (E)-nerolidol (20.8%), and linalool (12.7%) for orange flowers. In the foraging experiments the S. pectoralis workers were able to use the flower extracts to orient to the food source, overlooking plates baited with hexane only. However, orange flower extracts were seemingly more attractive to these worker bees, maybe because of the particular blend present in it. Our results reveal that these fragrances are very attractive to S. pectoralis, so we can infer that within citric orchards they could be important visitors in the study area; however habitat destruction, overuse of pesticides and the competitive override by managed honeybees might have put at risk their populations and thus the ecological services they provide to us.

Euglossine bee communities in small forest fragments of the Atlantic Forest, Rio de Janeiro state, southeastern Brazil (Hymenoptera, Apidae)

Euglossine bee communities in small forest fragments of the Atlantic Forest, Rio de Janeiro state, southeastern Brazil (Hymenoptera, Apidae). Euglossine bees are important pollinators in forests and agricultural areas. Although the structure of their communities is critically affected by anthropogenic disturbances, little is known about these bees in small forest fragments. The objectives of this study were to analyze the composition, abundance, and diversity of euglossine bee species in nine small fragments of different phytophysiognomies of the Atlantic Forest in southeastern Brazil, and to identify the environmental variables that may be related to the species composition of these communities. Males were sampled quarterly from May 2007 to May 2009 with aromatic traps containing methyl cinnamate, vanillin, eucalyptol, benzyl acetate, and methyl salicylate. A total of 1558 males, belonging to 10 species and three genera of Euglossina were collected. The richness ranged from five to seven species per fragment. Euglossa cordata, E. securigera, Eulaema nigrita e E. cingulata were common to all fragments studied. The diversity differed significantly among areas, ranging from H' = 1.04 to H' = 1.65. The precipitation, phytophysiognomy, and altitude had the highest relative importance over the species composition variation. The results presented in this study demonstrate that small forest fragments are able to support populations of euglossine bee species, most of which are widely distributed and reportedly tolerant to open and/or disturbed areas and suggest that the conservation of such areas is important, particularly in areas that are regenerating and in regions with agricultural matrices where these bees can act as important pollinators

Bee assemblage in habitats associated with Brassica napus L.

ABSTRACTAssessments in agricultural crops indicate that alterations in the landscape adjacent to the crops can result in reduced productivity due to loss or low abundance of pollinating agents. In the canola crop, production is partially dependent on insect pollination. Therefore, knowledge of the faunal diversity within and near crop fields is key for the management of these insects and consequently for the increase in productivity. This study aimed to determine and compare the diversity of bees in habitats associated with canola fields in southern Brazil. Bees were captured in four agricultural areas using pan traps in three habitat classes: (1) flowering canola crop, (2) forest remnant, and (3) grassland vegetation. The highest abundance of bees was observed in the grassland vegetation (50%) and in the flowering canola field (47%). Eight species common to the three habitat classes were recorded, four of which are represented by native social bees. In addition, a single or a few individuals represented species that were exclusive to a specific habitat class; eight species were collected exclusively in the interior of the canola field, 51 in the grassland vegetation, and six in the forest remnant. The majority of the rare species recorded exhibits subsocial or solitary behaviour and inhabit open places. The composition of bee groups differed between the habitats showing the importance of maintaining habitat mosaics with friendly areas for pollinators, which promote the pollination service for canola flowers.