Pollen diet diversity across bee lineages varies with lifestyle rather than colony size.

The shift to a pollen diet and the evolution of more highly organized societies, i.e., eusocial, were key milestones in bee diversification over their evolutionary history, culminating in a high dependence on feeding broods with a large variety of floral resources. Here, we hypothesized that obligatory eusocial bees have a wider diet diversity than their relatives with solitary lifestyles, and this would be related to colony size. To test both hypotheses, we surveyed diet breadth data (palynological analysis) based on the Shannon-Wiener index (H') for 85 bee taxa. We also obtained colony size for 47 eusocial bee species. These data were examined using phylogenetic comparative methods. The results support the generalist strategy as a derived trait for the bee taxa evaluated here. The dietary diversity of eusocial bees (H': 2.1, on average) was 67.5% higher than that of noneusocial bees (H': 1.21, on average). There was, however, no relationship between diet breadth and colony size, indicating that smaller colonies can harvest a pollen variety as diverse as larger colonies. Taken together, these results provide new insights into the impact of lifestyle on the diversity of collected pollen. Furthermore, this work sheds light on an advantage of living in more highly structured societies irrespective of the size of the colony.

Survivorship and food consumption of immatures and adults of Apis mellifera and Scaptotrigona bipunctata exposed to genetically modified eucalyptus pollen.

Eucalyptus comprises the largest planted area of cultivated production forest in Brazil. Genetic modification (GM) of eucalyptus can provide additional characteristics for increasing productivity and protecting wood yield, as well as potentially altering fiber for a diversity of industrial uses. However, prior to releasing a new GM plant, risk assessments studies with non-target organisms must be undertaken. Bees are prominent biological models since they play an important role in varied ecosystems, including for Eucalyptus pollination. The main goal of this study was to evaluate whether a novel event (Eucalyptus 751K032), which carries the cp4-epsps gene that encodes the protein CP4-EPSPS and nptII gene that encodes the protein NPTII, might adversely affect honey bees (Apis mellifera) and stingless bees (Scaptotrigona bipunctata). The experiments were performed in southern Brazil, as follows: (i) larvae and adults were separately investigated, (ii) three or four different pollen diets were offered to bees, depending on larval or adult status, and (iii) two biological attributes, i.e., survivorship of larvae and adults and food intake by adults were evaluated. The diets were prepared with pollen from GM Eucalyptus 751K032; pollen from conventional Eucalyptus clone FGN-K, multifloral pollen or pure larval food. The insecticide dimethoate was used to evaluate the sensitivity of bees to toxic substances. Datasets were analyzed with Chi-square test, survival curves and repeated measures ANOVA. Results indicated no evidence of adverse effects of Eucalyptus pollen 751K032 on either honey bees or stingless bees assessed here. Therefore, the main findings suggest that the novel event may be considered harmless to these organisms since neither survivorship nor food consumption by bees were affected by it.

Data standardization of plant-pollinator interactions.

BACKGROUND: Animal pollination is an important ecosystem function and service, ensuring both the integrity of natural systems and human well-being. Although many knowledge shortfalls remain, some high-quality data sets on biological interactions are now available. The development and adoption of standards for biodiversity data and metadata has promoted great advances in biological data sharing and aggregation, supporting large-scale studies and science-based public policies. However, these standards are currently not suitable to fully support interaction data sharing. RESULTS: Here we present a vocabulary of terms and a data model for sharing plant-pollinator interactions data based on the Darwin Core standard. The vocabulary introduces 48 new terms targeting several aspects of plant-pollinator interactions and can be used to capture information from different approaches and scales. Additionally, we provide solutions for data serialization using RDF, XML, and DwC-Archives and recommendations of existing controlled vocabularies for some of the terms. Our contribution supports open access to standardized data on plant-pollinator interactions. CONCLUSIONS: The adoption of the vocabulary would facilitate data sharing to support studies ranging from the spatial and temporal distribution of interactions to the taxonomic, phenological, functional, and phylogenetic aspects of plant-pollinator interactions. We expect to fill data and knowledge gaps, thus further enabling scientific research on the ecology and evolution of plant-pollinator communities, biodiversity conservation, ecosystem services, and the development of public policies. The proposed data model is flexible and can be adapted for sharing other types of interactions data by developing discipline-specific vocabularies of terms.

Forensically Relevant Flesh Flies (Diptera, Sarcophagidae, Sarcophaginae) of Southern Brazil.

Flesh flies comprise a large fly family distributed worldwide that has great importance for forensic entomology. A robust and updated checklist of Sarcophaginae flies recorded in Southern Brazil is presented, based on material collected in the Rio Grande do Sul state and on a literature review. The forensic importance (high, moderate, or none) of the recorded flesh flies for estimating the postmortem interval (PMI) or inferring cases of neglect was determined based on their ecological habits. A total of 2,831 specimens representing 38 taxa were collected from three studies. Oxysarcodexia was the most abundant and species-rich genus in all three studies. Dexosarcophaga carvalhoi (Lopes) was registered for the first time in Southern Brazil. The checklist for Southern Brazil comprises 91 species distributed in 19 genera, with Oxysarcodexia, Peckia, and Lepidodexia representing the richest genera. Considering the importance of species for PMI estimation, 10, 42, and 39 species were classified as having high, moderate, or no forensic relevance, respectively. Moreover, five myiasis-causing sarcophagine flies recorded in Southern Brazil were considered to have the potential to reveal cases of neglect or mistreatment. This study revealed that Microcerella halli (Engel) and Peckia (Euboettcheria) australis (Townsend) are the most important species for PMI estimation in Southern Brazil, as they are often found breeding in corpses in this region.

Negative impacts of dominance on bee communities: Does the influence of invasive honey bees differ from native bees?

Invasive species can reach high abundances and dominate native environments. One of the most impressive examples of ecological invasions is the spread of the African subspecies of the honey bee throughout the Americas, starting from its introduction in a single locality in Brazil. The invasive honey bee is expected to more negatively impact bee community abundance and diversity than native dominant species, but this has not been tested previously. We developed a comprehensive and systematic bee sampling scheme, using a protocol deploying 11,520 pan traps across regions and crops for three years in Brazil. We found that invasive honey bees are now the single most dominant bee species. Such dominance has not only negative consequences for abundance and species richness of native bees but also for overall bee abundance (i.e., strong "numerical" effects of honey bees). Contrary to expectations, honey bees did not have stronger negative impacts than other native bees achieving similar levels of dominance (i.e., lack of negative "identity" effects of honey bees). These effects were markedly consistent across crop species, seasons and years, and were independent from land-use effects. Dominance could be a proxy of bee community degradation and more generally of the severity of ecological invasions.

Larvae of stingless bee Scaptotrigona bipunctata exposed to organophosphorus pesticide develop into lighter, smaller and deformed adult workers.

Organophosphorus pesticides such as chlorpyrifos are often used in agriculture due to their broad spectrum of action. However, this insecticide and acaricide is considered highly toxic to the environment and can cause toxicity in nontarget insects such as bees. In addition to adult individuals, immature can also be exposed to residues of this insecticide by larval food. Thus, we investigated the effects of chlorpyrifos concentrations on the larval development of stingless bee Scaptotrigona bipunctata workers reared in vitro. We evaluated four different biomarkers: a) survival, b) development time, c) body mass and d) morphological characteristics (head width, intertegular distance, wing area and proportion of deformed bees). The exposure of the larvae to different doses of chlorpyrifos significantly reduced survival probability but did not cause changes in the development time. Regarding morphometric analysis, bees exposed to chlorpyrifos showed a reduction in body mass and size, and 28% of the emerged adults showed a reduction in wing area and deformations. Therefore, this work shows that S. bipunctata larvae exposed to the sublethal effects of chlorpyrifos are likely to have reduced chances of survival. However, if they emerge, they will be lighter, smaller and less able than equivalent but not exposed workers. These impaired attributes have the potential to compromise the future workforce in colonies exposed to this pesticide.

Factors Affecting the Composition and Succession of Beetles in Exposed Pig Carcasses in Southern Brazil.

Coleoptera is one of the largest taxon among animals and exhibits diverse eating habits. When associated with decaying corpses, beetles can be of great value in estimating the postmortem interval. In order to consolidate a useful database for the forensic field, it is necessary to study the entomological fauna associated with the carcasses in different geographical regions since the diversity of insects varies according to the biogeoclimate zone. Thus, this study aimed to assess the influence of environmental and ecological factors on the composition and succession of beetles associated with pig carcasses exposed in southern Brazil. Collections were carried out during the hot/dry and cold/wet seasons. A total of 415 specimens belonging to 18 Coleoptera families were sampled. The highest total abundance (n = 329) and diversity (n = 44 taxa) were recorded in the cold/wet season, corresponding to approximately 80% of the total sampled from the two seasons. Dermestidae (26.7%) was the family most abundantly sampled. Regarding eating habits, in an increasing order of importance were necrophagous (43.3%), predator (31.6%), and omnivorous (0.05%). In the hot/dry season, there was no faunal succession. In the cold/wet season, the succession was more associated with differences in abundance than to the presence or absence of a specific taxon by decomposition stage. Considering all the factors analyzed in the current study, three species of beetles, Dermestes maculatus DeGeer (Dermestidae), Euspilotus azureus (Sahlberg, 1823) (Histeridae), and Oxelytrum discicolle Brullé, 1840 (Silphidae), could be identified as being of the greatest forensic relevance in this biogeoclimatic zone.

Geographical origin of white honey produced by stingless bees in the Araucaria Forest in Southern Brazil / Origem geográfica do mel branco produzido por abelhas sem ferrão na Floresta de Araucárias no Sul do Brasil

Abstract: Honey produced by native stingless bees in the Araucaria Forest region of Rio Grande do Sul, southern Brazil, specifically the municipality of Cambará do Sul, is highly valued for its characteristic white color, floral odor and taste. In this study, we investigated the botanical origin of white honey stored in colonies of five Meliponini species of the genera Melipona (n = 3) and Plebeia (n = 2). During the production period of white honey, from January to March, flowers were sampled fortnightly along pre-established trails to identify plants used by bees. For all sampled plant species, exsiccates and pollen reference slides were prepared. Honey samples from stingless bees were processed for extraction and preparation of pollen grains for identification of pollen types. In all analyzed honey samples, pollen grains of Clethra scabra (Clethraceae) were predominant (between 46-94%). Pollen grains from other botanical families, including Myrtaceae, Fabaceae and Melastomataceae were frequently identified in honey samples of the Melipona species, while Cunoniaceae was also found in samples of Plebeia species. In this study, we concluded that Clethra scabra is predominantly used by Meliponini bees in the production of white honey in the municipality of Cambará do Sul.

Resumo: Na região da Floresta de Araucária do Rio Grande do Sul, especificamente no município de Cambará do Sul, as abelhas nativas sem ferrão produzem mel característico devido à sua cor branca e gosto apreciado. Neste estudo, investigamos a origem botânica do mel branco armazenado em colônias de cinco espécies de Meliponini dos gêneros Melipona (n = 3) e Plebeia (n = 2). Durante o período de produção do mel branco, de janeiro a março, as flores foram amostradas quinzenalmente ao longo de trilhas pré-estabelecidas, a fim de identificar as espécies utilizadas pelas abelhas. A partir de amostras de plantas foram preparadas exsicatas e lâminas de referência de pólen. As amostras de mel de abelhas sem ferrão foram processadas para extração e preparo dos grãos de pólen para a determinação dos tipos polínicos presentes. Em todas as amostras de méis branco analisadas os grãos de pólen de Clethra scabra (Clethraceae) predominaram (entre 46-94%). Grãos de pólen de outras espécies das famílias botânicas Myrtaceae, Fabaceae e Melastomataceae foram frequentemente identificados nas amostras de méis das espécies de Melipona, enquanto Cunoniaceae também o foi nas amostras das espécies de Plebeia. Neste estudo, nós concluímos que Clethra scabra é predominantemente utilizada pelas abelhas Meliponini na produção de méis branco no município de Cambará do Sul.

Two new species of Tydeidae (Acari: Prostigmata) associated with stingless bees.

Tydeid mites have a cosmopolitan distribution and are associated with diverse substrates such as soil, plants, stored products, and animals like vertebrates and insects. Here we report two new species of tydeid mites living inside stingless bee colonies in Brazil. Lorryia meliponarum n. sp. and Melissotydeus bipunctata n. sp. are described and illustrated, and in addition a key to the species of Melissotydeus is presented.

The virome of an endangered stingless bee suffering from annual mortality in southern Brazil.

Meliponiculture - the management of stingless bee colonies - is an expanding activity in Brazil with economic, social and environmental potential. However, unlike in apiculture, the pathogens that impact on meliponiculture remain largely unknown. In southern Brazil, every year at the end of the summer, managed colonies of the stingless bee Melipona quadrifasciata manifest a syndrome that eventually leads to collapse. Here we characterize the M. quadrifasciata virome using high-throughput sequencing, with the aim of identifying potentially pathogenic viruses, and test whether they are related to the syndrome outbreaks. Two paired viromes are explored, one from healthy bees and another from unhealthy ones. Each virome is built from metagenomes assembled from sequencing reads derived either from RNA or DNA. A total of 40 621 reads map to viral contigs of the unhealthy bees' metagenomes, whereas only 11 reads map to contigs identified as viruses of healthy bees. The viruses showing the largest copy numbers in the virome of unhealthy bees belong to the family Dicistroviridae - common pathogenic honeybee viruses - as well as Parvoviridae and Circoviridae, which have never been reported as being pathogenic in insects. Our analyses indicate that they represent seven novel viruses associated with stingless bees. PCR-based detection of these viruses in individual bees (healthy or unhealthy) from three different localities revealed a statistically significant association between viral infection and symptom manifestation in one meliponary. We conclude that although viral infections may contribute to colony collapses in the annual syndrome in some meliponaries, viruses spread opportunistically during the outbreak, perhaps due to colony weakness.

Looking beyond the flowers: associations of stingless bees with sap-sucking insects.

The main sources of food for stingless bees are the nectar and pollen harvested from flowers, whereas one important kind of nesting material (i.e. wax) is produced by their own abdominal glands. Stingless bees can, nonetheless, obtain alternative resources of food and wax from exudates released by sap-sucking insects as honeydew and waxy cover, respectively. To date, there are no comprehensive studies investigating how diversified and structured the network interactions between stingless bees and sap-sucking insects are. Here, we conducted a survey of the data on relationship between stingless bees and sap-sucking insects to evaluate: (1) which resources are collected by which stingless bee species; (2) how diverse the interaction network is, using species degree and specialisation index as a proxy; and if (3) there would be any phylogenetic signal in the species degree and specialisation indices. Our findings demonstrate that approximately 21 stingless bee species like Trigona spp. and Oxytrigona spp. have been observed interacting with 11 sap-sucking species, among which Aethalion reticulatum is the main partner. From ca. 50 records, Brazil is the country with most observations (n = 38) of this type of ecological interaction. We found also that stingless bees harvest fivefold more honeydew than waxy covers on sap-sucking insects. However, we did not find any phylogenetic signal for the occurrence of this interaction, considering species degree and specialisation indices, suggesting that both traits apparently evolved independently among stingless bee species. We suggest that specific ecological demands may drive this opportunistic behaviour exhibited by stingless bees, because major sources of food are obtained from flowers and these bees produce their own wax.

Pesticide Exposure Assessment Paradigm for Stingless Bees.

Although the importance of bees as the pollinators responsible for maintaining gene flow for many native and cultivated plants in ecosystems around the world is recognized, much of their biodiversity and behavior remains to be discovered. Stingless bees are considered key pollinators for several plant species in tropical and subtropical ecosystems and they also provide pollination services for economically important agricultural crops. Many countries are using the honey bee (Apis mellifera Linnaeus, 1758, Hymenoptera: Apidae) as a surrogate to evaluate the risk of pesticides to all species of bees. However, there is uncertainty regarding the extent to which honey bees can serve as surrogates for non-Apis bee species in the risk assessment for pesticides. This paper provides a short overview of the life history traits relevant in risk assessment of stingless bees. It summarizes what is known about stingless bee exposure to pesticides compared to that of honey bees and presents criteria for potential candidate species from Brazil for use in pesticide risk assessment in tropical environments. This paper also identifies gaps in knowledge of bee biology and pesticide exposure routes not covered by the current honey bee exposure assessment paradigm. Based on these gaps, research is needed on life history traits, estimates of nectar and pollen consumption, mud, resin, and water collection and available protocols to adequately assess toxic effects of pesticides to stingless bees. This review is part of a series of papers on the risk of exposure of non-Apis bees to pesticides.

Queen bee acceptance under threat: Neurotoxic insecticides provoke deep damage in queen-worker relationships.

Virgin queens (gynes) exhibit a range of behaviors in order to be accepted as the leader of colony. However, environmental neurotoxic insecticides as neonicotinoids may affect the social performance of the bees. Here, we evaluated the sublethal effects of neonicotinoid imidacloprid on the larval food of queens from Plebeia droryana, a species of neotropical stingless bee. Several behaviors were analyzed as multivariate response variables in a Hotelling test, as well as generalized additive mixed models. Our findings demonstrate that treated queens perform less wing vibration and trophallaxis with their workers. Furthermore, the treated gynes encounter more harassment (aggression) from their workers, suggesting that workers can differentiate nontreated queens from treated queens most likely by chemical signals. Our data indicate that the behavioral repertoire underlying the queen selection process by the stingless bee P. droryana may be seriously affected by residual doses of imidacloprid in larval food. As a result, such queens are rather undernourished and aggressed by workers, which most likely compromises the viability and permanence of colonies in the long term.

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.

Report on the microbiota of Melipona quadrifasciata affected by a recurrent disease.

Melipona quadrifasciata is an eusocial stingless bee traditionally used for honey production in Brazil. In the last decades, the species disappeared from the wild in Southern Brazil, being kept exclusively in managed colonies for commercial and recreational purposes. Stingless beekeepers from this region report annual losses of their colonies due to a syndrome of yet unknown causes. We investigate whether it is associated to pathogenic microorganisms already known to cause disease in bees. These results provide a starting point for future studies aimed at clarifying the relationship between the microbial community of stingless bees and their colony collapses.

Absence of Leishmaniinae and Nosematidae in stingless bees.

Bee pollination is an indispensable component of global food production and plays a crucial role in sustainable agriculture. The worldwide decline of bee populations, including wild pollinators, poses a threat to this system. However, most studies to date are situated in temperate regions where Apini and Bombini are very abundant pollinators. Tropical and subtropical regions where stingless bees (Apidae: Meliponini) are generally very common, are often overlooked. These bees also face pressure due to deforestation and agricultural intensification as well as the growing use and spread of exotic pollinators as Apis mellifera and Bombus species. The loss or decline of this important bee tribe would have a large impact on their provided ecosystem services, in both wild and agricultural landscapes. The importance of pollinator diseases, which can contribute to decline, has not been investigated so far in this bee tribe. Here we report on the first large pathogen screening of Meliponini species in southern Brazil. Remarkably we observed that there was an absence of Leishmaniinae and Nosematidae, and a very low occurrence of Apicystis bombi. Our data on disease prevalence in both understudied areas and species, can greatly improve our knowledge on the distribution of pathogens among bee species.

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.

Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms.

Ecological intensification, or the improvement of crop yield through enhancement of biodiversity, may be a sustainable pathway toward greater food supplies. Such sustainable increases may be especially important for the 2 billion people reliant on small farms, many of which are undernourished, yet we know little about the efficacy of this approach. Using a coordinated protocol across regions and crops, we quantify to what degree enhancing pollinator density and richness can improve yields on 344 fields from 33 pollinator-dependent crop systems in small and large farms from Africa, Asia, and Latin America. For fields less than 2 hectares, we found that yield gaps could be closed by a median of 24% through higher flower-visitor density. For larger fields, such benefits only occurred at high flower-visitor richness. Worldwide, our study demonstrates that ecological intensification can create synchronous biodiversity and yield outcomes.

Stingless Bees as Alternative Pollinators of Canola.

Alternative pollinators can ensure pollination services if the availability of the managed or most common pollinator is compromised. In this study, the behavior and pollination efficiency of Apis mellifera L. and two species of stingless bees, Plebeia emerina Friese and Tetragonisca fiebrigi Schwarz, were evaluated and compared in flowers of Brassica napus L. 'Hyola 61'. A. mellifera was an efficient pollinator when collecting nectar because it effectively touched the reproductive organs of the flower. In contrast, stingless bees were efficient pollinators only when collecting pollen. The number of pollen grains deposited on the stigma after a single visit by worker bees of the three species was greater than the number of grains resulting from pollination without the bee visits. On average, the three species deposited enough pollen grains to fertilize all of the flower ovules. A. mellifera and P. emerina had similar pollination efficiency because no significant differences were observed in the characteristics of the siliques produced. Although T. fiebrigi is also an effective pollinator, the seed mass produced by their pollination was lower. Native bees promoted similar rates of fruit set compared with A. mellifera. Thus, P. emerina has potential to be used for pollination in canola crops.

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.