The Value of Crop Production and Pollination Services in the Eastern Amazon.

Nature safeguards living organisms and the ecosystem functions and services delivered by them. Animal pollination is an important Ecosystem Service since it plays a key role for achieving the sustainable development goals by safeguarding worldwide food production. Thus, conservation of pollination services is a major priority for guaranteeing global food security in the long term. Here we evaluate the crop pollination services in Pará state (Eastern Amazon, Brazil) focusing on two questions: (1) What is the economic value of crop production and pollination service in Pará? (2) Which municipalities are most dependent on pollination services considering local economies? We found 36 crops produced in the state; 20 (55%) crops are dependent on animal pollinators. In 2016, crop production value (CPV) for Pará state was US$ 2.95 billion and total pollination service value (PSV) was US$ 983.2 million, corresponding to 33% of CPV in Pará. Highest PSV value crops were açaí palm (US$635.6 million), cocoa (US$187.6 million), soybean (US$98.4 million), and watermelon (US$26.1 million), accounting for 96% of Pará's PSV. Two municipalities (Medicilândia and Igarapé Miri) presented more than 50% of their GDP based on pollination services. In general, we found low crop diversity in the municipalities of Pará, suggesting an economic rural vulnerability for the state, mainly supported by the high productions of soy and açaí. Pollinator conservation and ecological intensified farming practices are urgent for supporting sustainable development for the state.

Stingless Bees (Melipona subnitida) Overcome Severe Drought Events in the Brazilian Tropical Dry Forest by Opting for High-Profit Food Sources.

In the Brazilian Tropical Dry Forest, the Caatinga, stingless bees (Apidae, Meliponini) need to adjust their foraging behavior to a very short and unpredictable blooming period. Melipona subnitida Ducke 1910 is one of the few meliponine species adapted to the environmental peculiarities of this biome. To get an insight into how these highly eusocial bees are able to maintain their perennial colonies despite extended periods of food scarcity, we asked the following questions: (1) At which plant species do colonies of M. subnitida collect their food during the rainy season? And (2) are there any plant species during the dry season, from which the colonies may profit for replenishing their food stores? During 1 year, we collected monthly honey and pollen samples from recently built storage pots of five colonies of M. subnitida and identified the botanical origin of the collected resources. In the course of our study, the colonies foraged at native trees, shrubs, and herbaceous species, demonstrating the importance of all plant strata for the bees' diet. Profitable plants, which bloom mainly during the rainy season and usually produce a great number of flowers, were frequently sampled in new pots throughout the entire study, even during the dry season. From our results, we compiled a list of the most important plant species providing floral resources for bees throughout the year, including periods of drought. We recommend these plants for restoration areas to improve the conservation of native bee species and local beekeeping in the Brazilian Tropical Dry Forest.

The Dependence of Crops for Pollinators and the Economic Value of Pollination in Brazil.

Food production is challenged by changes in climate and land use and expanding human population growth. Proper pollination can increase the production and quality of fruit, nut, oil, and fiber crops. We reviewed crop dependence on pollinators and estimated the economic value of pollination per year for each crop in Brazil. We analyzed 141 crops and found that 85 depend on pollinators. Almost one-third of these crops have an essential or great dependence on pollinators. The economic contribution of pollinators totals ∼30% (∼US$12 billion) of the total annual agricultural income of the dependent crops (totalizing almost US$45 billion). However, half of these figures includes soybean crop (US$5.7 billion of pollinators' contribution and US$22 billion of annual income). Soybean was considered as having a modest dependence on pollinators, but this remains controversial because pollinator dependence might vary among different varieties cultivated in Brazil. Moreover, we have no information about pollinator dependence regarding some important crops, showing the urgent need for basic research into reproductive biology and pollination ecology.

Behavioral suites mediate group-level foraging dynamics in communities of tropical stingless bees.

Competition for floral resources is a key force shaping pollinator communities, particularly among social bees. The ability of social bees to recruit nestmates for group foraging is hypothesized to be a major factor in their ability to dominate rich resources such as mass-flowering trees. We tested the role of group foraging in attaining dominance by stingless bees, eusocial tropical pollinators that exhibit high diversity in foraging strategies. We provide the first experimental evidence that meliponine group foraging strategies, large colony sizes and aggressive behavior form a suite of traits that enable colonies to improve dominance of rich resources. Using a diverse assemblage of Brazilian stingless bee species and an array of artificial "flowers" that provided a sucrose reward, we compared species' dominance and visitation under unrestricted foraging conditions and with experimental removal of group-foraging species. Dominance does not vary with individual body size, but rather with foraging group size. Species that recruit larger numbers of nestmates (Scaptotrigona aff. depilis, Trigona hyalinata, Trigona spinipes) dominated both numerically (high local abundance) and behaviorally (controlling feeders). Removal of group-foraging species increased feeding opportunities for solitary foragers (Frieseomelitta varia, Melipona quadrifasciata and Nannotrigona testaceicornis). Trigona hyalinata always dominated under unrestricted conditions. When this species was removed, T. spinipes or S. aff. depilis controlled feeders and limited visitation by solitary-foraging species. Because bee foraging patterns determine plant pollination success, understanding the forces that shape these patterns is crucial to ensuring pollination of both crops and natural areas in the face of current pollinator declines. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00040-009-0055-8) contains supplementary material, which is available to authorized users.

The queen is dead--long live the workers: intraspecific parasitism by workers in the stingless bee Melipona scutellaris.

Insect societies are well known for their high degree of cooperation, but their colonies can potentially be exploited by reproductive workers who lay unfertilized, male eggs, rather than work for the good of the colony. Recently, it has also been discovered that workers in bumblebees and Asian honeybees can succeed in entering and parasitizing unrelated colonies to produce their own male offspring. The aim of this study was to investigate whether such intraspecific worker parasitism might also occur in stingless bees, another group of highly social bees. Based on a large-scale genetic study of the species Melipona scutellaris, and the genotyping of nearly 600 males from 45 colonies, we show that approximately 20% of all males are workers' sons, but that around 80% of these had genotypes that were incompatible with them being the sons of workers of the resident queen. By tracking colonies over multiple generations, we show that these males were not produced by drifted workers, but rather by workers that were the offspring of a previous, superseded queen. This means that uniquely, workers reproductively parasitize the next-generation workforce. Our results are surprising given that most colonies were sampled many months after the previous queen had died and that workers normally only have a life expectancy of approximately 30 days. It also implies that reproductive workers greatly outlive all other workers. We explain our results in the context of kin selection theory, and the fact that it pays workers more from exploiting the colony if costs are carried by less related individuals.

Hygienic behavior of the stingless bee Plebeia remota (Holmberg, 1903) (Apidae, Meliponini).

We investigated hygienic behavior in 10 colonies of Plebeia remota, using the pin-killed method. After 24 h the bees had removed a mean of 69.6% of the dead brood. After 48 h, the bees had removed a mean of 96.4% of the dead brood. No significant correlation was found between the size of the brood comb and the number of dead pupae removed, and there was no apparent effect of the origin and the condition of the colony on the hygienic behavior of the bees. Plebeia remota has an efficiency of hygienic behavior superior to that of three of the other four stingless bee species studied until now.

Pollen foraging in colonies of Melipona bicolor (Apidae, Meliponini): effects of season, colony size and queen number.

We evaluated the ratio between the number of pollen foragers and the total number of bees entering colonies of Melipona bicolor, a facultative polygynous species of stingless bees. The variables considered in our analysis were: seasonality, colony size and the number of physogastric queens in each colony. The pollen forager ratios varied significantly between seasons; the ratio was higher in winter than in summer. However, colony size and number of queens per colony had no significant effect. We conclude that seasonal differences in pollen harvest are related to the production of sexuals and to the number of individuals and their body size.

Production of workers, queens and males in Plebeia remota colonies (Hymenoptera, Apidae, Meliponini), a stingless bee with reproductive diapause.

Queen, male and worker production was studied during one year in three Plebeia remota colonies from Atlantic Rainforest in Cunha, São Paulo State, and two from a subtropical Araucaria forest in Prudentópolis, Paraná State. All the colonies were kept in São Paulo city during our study. Plebeia remota has reproductive diapause during autumn and winter, which makes its biology of special interest. Brood production begins before spring, renewing the colony cycle. We sampled brood combs monthly in these five colonies. The number of cells in each comb varied significantly with time of the year; the smallest brood combs appear to be a consequence of reduced food availability. However, worker, queen and male frequencies did not differ significantly in time, and this presumably is due to the fact that they all are necessary for the growth, maintenance and reproduction of the colony. Although some molecular, morphological and behavioral differences have been detected in several studies comparing populations from Cunha and from Prudentópolis, we did not find significant differences between the colonies from these two localities in number of brood cells and worker, queen and male production.

The number of reproductive workers in highly eusocial Hymenoptera: monogyny and monandry.

Haplodiploidy results in relatedness asymmetries between colony members of highly eusocial Hymenoptera. As a consequence, queen and reproductive workers are more related to their own sons than to each other's male offspring. Kin selection theory predicts multiple optima in male parentage: either the queen or the workers should produce all the males. Nevertheless, shared male parentage is common in highly eusocial hymenopterans. An inclusive fitness model was used to analyze the effect of the number of reproductive workers on male parentage shared by the queen and laying workers by isolating the male component from an inclusive fitness equation using the equal fitness through male condition for each pairwise combination of the three female classes comprised of the queen, laying workers and non-laying workers. The main result of the theoretical analyses showed that the fraction of males produced by workers increases asymptotically with the number of laying workers at an increasingly diminishing rate, tending to an asymptotic value of 0.67. In addition, as the number of laying workers increases, the share of male parentage converges to that of non-laying workers. The diminishing return effect on male parentage share depending on the number of reproductive workers leads us to expect the number of reproductive workers to be relatively small in a stingless bee colony, even in the absence of productivity costs. The available data confirms this hypothesis, as there is an unusually small number of reproductive workers in stingless bee colonies.

Spatial patterns in the brood combs of Nannotrigona testaceicornis (Hymenoptera: Meliponinae): male clusters.

Genetic models of sex and caste determination in eusocial stingless bees suggest specific patterns of male, worker and gyne cell distribution in the brood comb. Conflict between queen and laying workers over male parentage and center-periphery gradients of conditions, such as food and temperature, could also contribute to non-random spatial configuration. We converted the positions of the hexagonal cells in a brood comb to Cartesian coordinates, labeled by sex or caste of the individuals inside. To detect and locate clustered patterns, the mapped brood combs were evaluated by indexes of dispersion (MMC, mean distance of cells of a given category from their centroid) and eccentricity (DMB, distance between this centroid and the overall brood comb centroid) that we developed. After randomizing the labels and recalculating the indexes, we calculated probabilities that the original values had been generated by chance. We created sets of binary brood combs in which males were aggregated, regularly or randomly distributed among females. These stylized maps were used to describe the power of MMC and DMB, and they were applied to evaluate the male distribution in the sampled Nannotrigona testaceicornis brood combs. MMC was very sensitive to slight deviations from a perfectly rounded clump; DMB detected any asymmetry in the location of these compact to fuzzy clusters. Six of the 82 brood combs of N. testaceicornis that we analyzed had more than nine males, distributed according to variations in spatial patterns, as indicated by the two indexes.

Gender identification of five genera of stingless bees (Apidae, Meliponini) based on wing morphology.

Currently, the identification of pollinators is a critical necessity of conservation programs. After it was found that features extracted from patterns of wing venation are sufficient to discriminate among insect species, various studies have focused on this structure. We examined wing venation patterns of males and workers of five stingless bee species in order to determine if there are differences between sexes and if these differences are greater within than between species. Geometric morphometric analyses were made of the forewings of males and workers of Nannotrigona testaceicornis, Melipona quadrifasciata, Frieseomelitta varia, and Scaptotrigona aff. depilis and Plebeia remota. The patterns of males and workers from the same species were more similar than the patterns of individuals of the same sex from different species, and the patterns of both males and workers, when analyzed alone, were sufficiently different to distinguish among these five species. This demonstrates that we can use this kind of analysis for the identification of stingless bee species and that the sex of the individual does not impede identification. Computer-assisted morphometric analysis of bee wing images can be a useful tool for biodiversity studies and conservation programs.

Comparative study in stingless bees (Meliponini) demonstrates that nest entrance size predicts traffic and defensivity.

Stingless bees (Meliponini) construct their own species-specific nest entrance. The size of this entrance is under conflicting selective pressures. Smaller entrances are easier to defend; however, a larger entrance accommodates heavier forager traffic. Using a comparative approach with 26 species of stingless bees, we show that species with greater foraging traffic have significantly larger entrances. Such a strong correlation between relative entrance area and traffic across the different species strongly suggests a trade-off between traffic and security. Additionally, we report on a significant trend for higher forager traffic to be associated with more guards and for those guards to be more aggressive. Finally, we discuss the nest entrance of Partamona, known in Brazil as boca de sapo, or toad mouth, which has a wide outer entrance but a narrow inner entrance. This extraordinary design allows these bees to finesse the defensivity/traffic trade-off.

Chemical basis for inter-colonial aggression in the stingless bee Scaptotrigona bipunctata (Hymenoptera: Apidae).

Inter-colonial aggression was tested using three colonies of Scaptotrigona bipunctata in a natural setting when their nests were moved and by artificial contact between individuals. Examination of the cuticular lipids of individuals from two colonies kept under identical conditions showed clear differences in their cuticular hydrocarbon profiles. The cuticular lipids were a mixture of hydrocarbons (saturated and unsaturated alkanes and alkenes) within the range of C23-C29. The use of multivariate analysis (PCA and discriminant analysis) showed that seven of the identified surface compounds are enough to separate workers from colonies A and B from each other.

Thermal evidence of the invasion of a stingless bee nest by a mammal

Melipona bicolor, an inhabitant of the Atlantic Rainforest, nidifies in hollows of live or dead trees. In order to study thermoregulation of a nest of this species, a temperature data logger was installed inside a hollow tree. After this, an intruder dug a hole, invaded the nest, and probably consumed its honey, pollen and bees, having remained there during three days. Thermal evidence and its behavior allowed the delimitation of a small number of suspects, wich we analized here. The intruder was a small mammal, predominantly nocturnal, that takes shelter in burrows, probably the yellow armadillo (Euphractus sexcinctus). Other evidence, if collected immediately after invasion, could precisely indicate precisely the species.

Thermal evidence of the invasion of a stingless bee nest by a mammal.

Melipona bicolor, an inhabitant of the Atlantic Rainforest, nidifies in hollows of live or dead trees. In order to study thermoregulation of a nest of this species, a temperature data logger was installed inside a hollow tree. After this, an intruder dug a hole, invaded the nest, and probably consumed its honey, pollen and bees, having remained there during three days. Thermal evidence and its behavior allowed the delimitation of a small number of suspects, which we analyzed here. The intruder was a small mammal, predominantly nocturnal, that takes shelter in burrows, probably the yellow armadillo (Euphractus sexcinctus). Other evidence, if collected immediately after invasion, could precisely indicate precisely the species.

Responses to climatic factors by foragers of Plebeia pugnax Moure (in litt.) (Apidae, Meliponinae).

Flight activity of Plebeia pugnax Moure (in litt.) was studied in six colonies coming from Cunha, SP, from July to October 1994. Twice a week, from 8:00 a.m. to 6:00 p.m., for 5 minutes every half-hour, all the bees entering and leaving the hives were counted. Six hundred counts were made and the materials that foragers carried were recorded. Data were analysed in relation to temperature, relative humidity, light intensity and day time. Foragers' flight activity was relatively constant in a wide range of temperature, from 22 degrees C to 34 degrees C. The minimum temperature for the beginning of flight activity was 14 degrees C. Effective flight activity (when foragers of all colonies were leaving the hives) occurred at 15 degrees C. These bees also flew within a wide range of relative humidity, from 30% to 100%, decreasing slowly after 50%. Flight activity increased as light intensity rose and it has also increased as the hours passed by, reaching a peak around midday and decreasing gradually afterwards. Pollen was collected all day long, while resin collection was relatively constant and debris transportation was slightly higher after 10:00 h. From all known Plebeia species, this one flew on the lowest temperature ever registered for this genus.

Responses to climatic factors by foragers of Plebeia pugnax Moure (in litt.) (Apidae, Meliponinae)

Flight activity of Plebeia pugnax Moure (in litt.) was studied in six colonies coming from Cunha, SP, from July to October 1994. Twice a week, from 8:00 a.m. to 6:00 p.m., for 5 minutes every half-hour, all the bees entering and leaving the hives were counted. Six hundred counts were made and the materials that foragers carried were recorded. Data were analysed in relation to temperature, relative humidity, light intensity and day time. Foragers' flight activity was relatively constant in a wide range of temperature, from 22 C to 34 C. The minimum temperature for the beginning of flight activity was 14 C. Effective flight activity (when foragers of all colonies were leaving the hives) occurred at 15 C. These bees also flew within a wide range of relative humidity, from 30 percent to 100 percent, decreasing slowly after 50 percent. Flight activity increased as light intensity rose and it has also increased as the hours passed by, reaching a peak around midday and decreasing gradually afterwards. Pollen was collected all day long, while resin collection was relatively constant and debris transportation was slightly higher after 10:00 h. From all known Plebeia species, this one flew on the lowest temperature ever registered for this genus