Charles Fernando dos Santos

Monogamy in large bee societies: a stingless paradox

High genetic diversity is important for the functioning of large insect societies. Across the social Hymenoptera (ants, bees, and wasps), species with the largest colonies tend to have a high colony-level genetic diversity resulting from multiple queens (polygyny) or queens that mate with multiple males (polyandry). Here we studied the genetic structure of Trigona spinipes, a stingless bee species with colonies an order of magnitude larger than those of polyandrous honeybees. Genotypes of adult workers and pupae from 43 nests distributed across three Brazilian biomes showed that T. spinipes colonies are usually headed by one singly mated queen. Apart from revealing a notable exception from the general incidence of high genetic diversity in large insect societies, our results reinforce previous findings suggesting the absence of polyandry in stingless bees and provide evidence against the sperm limitation hypothesis for the evolution of polyandry. Stingless bee species with large colonies, such as T. spinipes, thus seem promising study models to unravel alternative mechanisms to increase genetic diversity within colonies or understand the adaptive value of low genetic diversity in large insect societies.

Queens become workers: pesticides alter caste differentiation in bees

Bees are important for the world biodiversity and economy because they provide key pollination services in forests and crops. However, pesticide use in crops has adversely affected (decreased) queen production because of increased mortality among larvae. Here, we demonstrated that in vitro-reared queens of a neotropical social bee species (Plebeia droryana) also showed high larval mortality after exposure to an organophosphate pesticide (chlorpyrifos) via larval food. Moreover, most of the surviving larvae that were destined to develop into queens became workers more likely because they ate less food than expected without pesticide skewing thus caste differentiation in this bee species. This adverse effect has not been previously reported for any other social insects, such as honeybees or bumblebees. Queens are essential for breeding and colony growth. Therefore, if our data are applicable to other pantropical social bee species across the globe, it is likely that these bees are at a serious risk of failure to form new colonies.

Polinizadores de Bertholletia excelsa (Lecythidales: Lecythidaceae): interações com abelhas sem ferrão (Apidae: Meliponini) e nicho trófico

This paper presents an analysis of the foraging behavior and interactions of Xylocopa frontalis Olivier (Apidae: Xylocopini) and Eulaema mocsaryi (Friese) (Apidae: Euglossini) in the presence of stingless bees (Apidae: Meliponini) in flowers of Bertholletia excelsa, the Brazilian nut. The palynological load carried by both species was also examined. This study was conducted in the farm Aruanã, Itacoatiara/ Amazonas state, Brazil, during the flowering peak of B. excelsa. The visitation by the main pollinators X. frontalis and E. mocsaryi were influenced by the presence and activities of stingless bees in the flowers of B. excelsa. Meliponini bees did not have any effect on the visits and collection of floral resources by X. frontalis, while negatively affecting the number of visits by E. mocsaryi. The stingless bees presented a variety of strategies to get access to pollen grains of B. excelsa, grouped into two categories: opportunism -Frieseomelitta trichocerata Moure, Tetragona goettei (Friese), and Tetragona kaieteurensis (Schwarz), and stealing -Trigona branneri Cockerell, Trigona fuscipennis Friese, and Trigona guianae Cockerell. The palynological analysis from X. frontalis showed that the bee collected pollen in a few species of plants, but mainly on B. excelsa. The pollen grains of B. excelsa were poorly represented in the pollen shipments of E. mocsaryi, due to its large trophic niche in the locality.

Relatedness and dispersal distance of eusocial bee males on mating swarms

Stingless bee males (Hymenoptera: Apidae) aggregate themselves for reproductive purposes. The knowledge of relatedness among the males attending the aggregations and the distance that they disperse from their natal nests to aggregations may provide important data to effectively conserve these bees. Here, we estimated these properties for Tetragonisca angustula (Latreille, 1811) males. Microsatellite molecular markers were used to genotype bees sampled from local nests and in mating swarms in order to identify the nests of origin of males and maternal genotypes of concerning queens. The distances from assigned nests to the mating swarms allowed us to estimate the distances travelled by males. A genetic relationship analysis was conducted to verify whether T. angustula males were closely related to nests where they aggregated. A pairwise relatedness analysis was also performed among all T. angustula males in each mating swarm. Our results demonstrated that T. angustula mating swarms received dozens to hundreds of males from several colonies (up to 70). Only two of the five mating swarms contained any males that were closely related to the bees from the new nests in construction. The relatedness among males was also extremely low. Yet, dispersal distance of T. angustula males ranged hundreds of meters up to 1.6 km, with evidence of reaching 2.25 km according to their flight radius obtained from their foraging area for locality. These data indicate a highly efficient mating system with minimal inbreeding in this bee species, with a great dispersal capability not previously found for stingless bee males.

A scientific note on diploid males in a reproductive event of a eusocial bee

Departamento de Zoologia, IB, Universidade de São Paulo, Rua do Matão, 321, Travessa 14, 05508-090 São Paulo, SP, Brazil Laboratório de Abelhas, Departamento de Ecologia, IB, Universidade de São Paulo, Rua do Matão, 321, Travessa 14, 05508-090 São Paulo, SP, Brazil Empresa Brasileira de Pesquisa Agropecuária–Amazônia Oriental, travessa Dr. Enéas Pinheiro, s/n, 66095-105 Belém, PA, Brazil Universidade Federal Rural do Semiárido, Km 47-BR110, Mossoró, RN, Brazil Departamento de Genética e Biologia Reprodutiva, IB, Universidade de São Paulo, Rua do Matão 277, 05508-090 São Paulo, Brazil

Eusocial bee male aggregations: spatially and temporally separated but genetically homogenous

Male insects mostly aggregate near sites where sexually reproductive virgin females are found and where mating occur. This reproductive strategy is quite common in Hymenoptera and appears to decrease the chances of inbreeding. In Hymenoptera, inbred mating frequently result in sterile diploid males. Production of diploid males may reach high proportions in small bee populations, and it usually lead to population extinction within a small number of generations. Aggregation of males during a short period of time allow the mixing of local genes. In this paper, we analyzed male aggregations of Tetragonisca angustula (Latreille) (Hymenoptera: Apidae), a eusocial stingless bee, using microsatellite molecular markers. We used population genetic statistics for haplodiploid organisms to address genetic structuring among male aggregations. Our findings indicate that, in general, male aggregations of T. angustula occurring over short time scales and in close proximity are genetically homogeneous as if a single aggregation. We conclude that T. angustula males randomly disperse within a population looking for mating chances rather than settle on a distinct male aggregation. This behavior seems to contribute to the reduction of inbreeding in this species.

Temperature Rise and Its Influence on the Cessation of Diapause in Plebeia droryana, a Eusocial Bee (Hymenoptera: Apidae)

Abstract Climate warming in the coming decades may affect diapause in insect species which use it to survive unfavorable winter conditions. Plebeia droryana (Friese) (Hymenoptera: Apidae: Meliponini) is a highly eusocial bee species that exhibits reproductive diapause and inhabits southern South America where winter temperatures may fall below 10°C, or even below 0°C in extreme years. In this paper, we evaluate whether P. droryana might terminate diapause during winter under laboratory conditions. We initially kept colonies of P. droryana at 8°C in a biochemical oxygen demand chamber, and then raised the temperature by 2°C every 3 d until the cessation of diapause was detected, as indicated by the onset of brood cell building and subsequent egg-laying by queens. We found that the termination of diapause in P. droryana could be achieved at temperatures between 16°C and 22°C, resulting in typical postdiapause brood cell building and egg-laying rates. Our binomial generalized linear mixed model indicated that only temperature, but no time or temperature–time interaction, explained the probability of termination of diapause in P. droryana. Again, only temperature, but no time or temperature–time interaction, significantly affected amount of brood cell built postdiapause in this species. These data suggest that the levels of predicted climate warming in the geographic range of P. droryana over the coming decades will probably result in these populations abandoning diapause behavior. These results have important implications regarding the ecological service of crop and wild plant pollination provided by this species.

Climate Warming May Threaten Reproductive Diapause of a Highly Eusocial Bee

ABSTRACT Climate changes are predicted to affect the diapause of many insect species around the world adversely. In this context, bees are of interest due to their pollination services. In southern Brazil, the highly eusocial bee species Plebeia droryana (Friese) (Hymenoptera: Apidae: Meliponini) exhibits reproductive diapause in response to the regions rigorous winters. That diapause is characterized by a temporary interruption in brood cell construction by nurse bees and egg-laying by the queen, regardless of other internal tasks underway in the nests. In this study, we evaluated whether P. droryana enter diapause under experimental conditions. P. droryana colonies were kept in a germination chamber, and the temperature was progressively reduced from 20°C over a period of a few weeks until diapause was detected. Additionally, we also estimated the environmental conditions in the actual geographic range occupied by P. droryana and modeled it for predicted changes in climate up to the year 2080. Our findings indicate that P. droryana enter diapause between 10 and 8°C. We also found that the current minimum winter temperature (10.1°C, median) in the distributional range of P. droryana will probably rise (13.4°C, median). Thus, if our experimental data are somewhat accurate, ∼36% of the southern Brazilian P. droryana population may be active during the expected milder winter months in 2080. In this scenario, there may be a larger demand for pollen and nectar for that bee species. Greater conservation efforts will be required to preserve P. droryana populations and keep them viable in the coming decades.

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.

The dilemma of agricultural pollination in Brazil: Beekeeping growth and insecticide use

Pollination by bees improves agricultural crop yields and improves the financial outlook of beekeepers because it increases honey production and hive rental revenues. However, in Brazil, with a few exceptions, these benefits have been neglected in recent years because beekeepers are more interested in honey production than in agricultural pollination. The excessive and indiscriminate use of insecticides on agricultural fields in Brazil appears to be one of the principal obstacles preventing partnership between farmers and beekeepers. The goal of this study was therefore to evaluate the most recent situation in Brazil in relation to the use of insecticides, agriculture and to honey production in comparison with other countries. Our results show that Brazil is the largest consumer of insecticides in the world and that consumption has increased by > 150% over 15 years. While countries with a high Human Development Index (i.e., a measure that can also be used to question national policy choices) are reducing their levels of insecticide use in agriculture, Brazil is going in the opposite direction. It is highly likely the increase seen in other countries is a result of alternative methods for pest control rather than a result of the amount of area under agricultural cultivation and their capability to shift their economies from agriculture to other sectors. The number of hives (23%) and the volume of honey production (72%) in Brazil have, however, increased over the same period, raising Brazil to the ninth highest honey producer in the world. Although the data on apiculture are promising, the growth in use of insecticides in Brazil is a cause for concern because they leave residuals on bee products, on crops, and in the environment. Civil society and government in Brazil should encourage reductions in insecticide use and better relations between agricultural farmers and beekeepers.