Bombus Pauloensis Research Articles

The Gut Microbiome of Two Wild Bumble Bee Species Native of South America: Bombus pauloensis and Bombus bellicosus

South America is populated by a wide range of bumble bee species that represent an important source of biodiversity, supporting pollination services in natural and agricultural ecosystems. These pollinators provide unique specific microbial niches, populated by a wide number of microorganisms such as symbionts, environmental opportunistic bacteria, and pathogens. Recently, it was demonstrated how microbial populations are shaped by trophic resources and environmental conditions but also by anthropogenic pressure, which strongly affects microbes’ functionality. This study is focused on the impact of different land uses (natural reserve, agroecosystem, and suburban) on the gut microbiome composition of two South American bumble bees, Bombus pauloensis and Bombus bellicosus. Gut microbial DNA extracted from collected bumble bees was sequenced on the Illumina MiSeq platform and correlated with land use. Nosema ceranae load was analyzed with qPCR and correlated with microbiome data. Significant differences in gut microbiome composition between the two wild bumble bee species were highlighted, with notable variations in α- and β-diversity across study sites. Bombus bellicosus showed a high abundance of Pseudomonas, a genus that includes environmental saprobes, and was found to be the second major taxa populating the gut microbiome, probably indicating the vulnerability of this host to environmental pollution. Pathogen analysis unveils a high prevalence of N. ceranae, with B. bellicosus showing higher susceptibility. Finally, Gilliamella exhibited a negative correlation with N. ceranae, suggesting a potential protective role of this commensal taxon. Our findings underscore the importance of considering microbial dynamics in pollinator conservation strategies, highlighting potential interactions between gut bacteria and pathogens in shaping bumble bee health.

Pollination efficiency and foraging behavior of Bombus pauloensis (Hymenoptera: Apidae) on two highbush blueberry cultivars (Vaccinium corymbosum)

Bombus pauloensis Friese is a promising managed bumblebee that can pollinate crops in South America. Highbush blueberry (Vaccinium corymbosum L.) is a recently introduced and economically promising crop cultivated in open fields or greenhouses in Colombia. Although this crop is known to be pollinator-dependent, the efficiency of local pollinators in this geographic area has yet to be established. This study aimed to establish the pollination effectiveness and foraging behavior of B. pauloensis in two of the most common cultivars of highbush blueberries planted in a high Andean region of Colombia. We hand-reared and located B. pauloensis colonies in two different plantations of Sharpblue (open field) and Biloxi (greenhouse) cultivars. The time spent per flower and the number of flowers visited per minute of 300 foragers were registered to characterize the foraging behavior in both cultivars. Pollen analysis was performed once from corbicular loads, larvae, larval cells, and colony feces to identify the pollen sources collected by colonies located in the Sharpblue crop. Analysis of fruit quality was performed to establish the effect of B. pauloensis pollination. Foragers visited blueberry flowers with a corolla aperture of more than 3mm in both cultivars but spent more time visiting Biloxi than Sharpblue flowers. B. pauloensis pollination reduced the ripening time and increased the fresh and dry weight and the number of true seeds in both cultivars. Our results provide evidence that B. pauloensis pollination can improve the fruit quality in the blueberry cultivars evaluated here in Colombia, making it an efficient native pollinator for a promising commercial species.

A first approach in the correlation of pathogens load affecting Bombus pauloensis to the land use in Buenos Aires Province

Bombus pauloensis is a native bumble bee species widely distributed over South America and a key pollinator for native plants and commercial crops. This species is affected by pathogens such as Nosema ceranae, Crithidia bombi and Apis mellifera Filamentous Virus (AmFV). This work aims to document the presence and intensity of exogenous pathogens on the native bumble bee B. pauloensis in different periods of the year during spring and summer. Bumble bees were sampled in four study areas with contrasting land uses to preliminary evaluate if anthropization levels can be related to the presence and intensity of pathogens. DNA was isolated from twenty individuals per sampling site and N. ceranae, C. bombi and AmFV pathogens load were quantified by quantitative PCR. The results showed a wide and ubiquitous prevalence of N. ceranae and C. bombi pathogens in all the sampled bumble bees throughout the year, with a pathogens load that did not differ significantly among the sampling sites. AmFV was undetected in any of the individuals analyzed in any sampling site. This suggests that human activities could equally impact all habitats populated by B. pauloensis. Honey bees were detected with a relevant abundance in all the sampling sites and could be one of the main anthropogenic drivers of pathogens spread and host switches in the analyzed sampling sites. This study analyzes the general occurrence of the prevalence and intensity of the pathogens in a native Argentinian bumble bee species and attempts the correlation with the land use

Occurrence of chlorpyrifos and organochlorine pesticides in a native bumblebee (Bombus pauloensis) living under different land uses in the southeastern Pampas, Argentina

Pollinators such as Apidae bees are vital for ecosystems and food security. Unfortunately, their populations have declined due to several factors including pesticide use. Among them, the organophosphate insecticide chlorpyrifos, poses a global threat, while legacy compounds like organochlorine pesticides (OCPs) easily bioaccumulate, increasing the concern. Bombus pauloensis, a widely distributed native bee in Argentina, is used for commercial pollination; however, information regarding their health status is scarce. This study assessed chlorpyrifos and OCP levels in B. pauloensis (workers and males) and related environmental matrices living from three different land uses schemes, by means of GC-ECD and GC–MS. The ornamental horticulture field (OP) showed the highest total pesticide concentrations in workers (13.1 ng/g), flowers and soils, whereas the organic agriculture field (OA) exhibited the lowest. Chlorpyrifos was the most abundant compound, accounting for at least 20 % of pesticide load across all matrices. The food production horticulture field (FH) had the highest chlorpyrifos concentration in workers, males and soils (5.0, 4.4 and 3.3 ng/g, respectively), suggesting a local greater usage, whereas OA showed the lowest. Regarding OCPs groups, Drins and DDTs were predominant in most matrices, with FH males registering the highest levels (4.0 and 2.5 ng/g, respectively), closely followed by OP. However, metabolites' contribution indicated historical use and atmospheric inputs in all sites. Multivariate analyses confirmed the significance of site and bumblebee sex to explain pesticide composition. Males from all sites exhibited higher chlorpyrifos levels than workers and this trend was similar for some OCP groups. Overall, OA differed from FH and OP, indicating a correlation between production modes and pesticide profiles. This study demonstrates the value of B. pauloensis as a pesticide biomonitor but also offers insights into its populations' health in the area. In this sense, this information could be useful towards the preservation of this crucial pollinator.

Arthropods associated with a Bombus pauloensis (Hymenoptera: Apidae: Bombini) nest in the Sabana of Bogotá (Colombia)

Bumblebees are important natural pollinators due to their services to wild and cultivated plants. They commonly nest in cavities in the ground where they are exposed to numerous organisms or interact with them. One Bombus pauloensis nest in the Sabana of Bogotá (Colombia) was transferred to an artificial nest and relocated close to a honeybee apiary after the original nest was threatened by an intentional fire. The objective was to preserve the colony and simultaneously identify arthropods associated with a bumblebee nest as this is poorly studied in Colombia. Samples of the organisms found in the bumblebees’ nest were collected for taxonomic identification. Several commensal, scavenger and parasitic organisms were found, including Antherophagus sp. (Coleoptera: Crytophagidae), wireworm beetles (Coleoptera: Elateride), Fannia canicularis (Diptera: Fanniidae), and mites of genera Parasitellus and Pneumolaelaps. This is the first report of other organisms besides Antherophagus from a B. pauloensis nest in Colombia.

Managed honeybees and South American bumblebees exhibit complementary foraging patterns in highbush blueberry

Despite Apis mellifera being the most widely managed pollinator to enhance crop production, they are not the most suitable species for highbush blueberries, which possess restrictive floral morphology and require buzz-pollination. Thus, the South American bumblebee Bombus pauloensis is increasingly managed as an alternative species in this crop alongside honeybees. Herein, we evaluated the foraging patterns of the two species, concerning the potential pollen transfer between two blueberry co-blooming cultivars grown under open high tunnels during two seasons considering different colony densities. Both managed pollinators showed different foraging patterns, influenced by the cultivar identity which varied in their floral morphology and nectar production. Our results demonstrate that both species are efficient foragers on highbush blueberry and further suggest that they contribute positively to its pollination in complementary ways: while bumblebees were more effective at the individual level (visited more flowers and carried more pollen), the greater densities of honeybee foragers overcame the difficulties imposed by the flower morphology, irrespective of the stocking rate. This study supports the addition of managed native bumblebees alongside honeybees to enhance pollination services and emphasizes the importance of examining behavioural aspects to optimize management practices in pollinator-dependent crops.

Classical olfactory conditioning promotes long-term memory and improves odor-cued flight orientation in the South American native bumblebee Bombus pauloensis.

Fil: Nery, Denise. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Oficina de Coordinacion Administrativa Ciudad Universitaria. Instituto de Fisiologia, Biologia Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiologia, Biologia Molecular y Neurociencias; Argentina

Spatio-temporal dynamics of landscape use by the bumblebee Bombus pauloensis (Hymenoptera: Apidae) and its relationship with pollen provisioning.

Understanding how bees use resources at a landscape scale is essential for developing meaningful management plans that sustain populations and the pollination services they provide. Bumblebees are important pollinators for many wild and cultivated plants, and have experienced steep population declines worldwide. Bee foraging behavior can be influenced by resource availability and bees’ lifecycle stage. To better understand these relationships, we studied the habitat selection of Bombus pauloensis by tracking 17 queen bumblebees with radio telemetry in blueberry fields in Entre Ríos province, Argentina. To evaluate land use and floral resources used by bumblebees, we tracked bees before and after nest establishment and estimated home ranges using minimum convex polygons and kernel density methods. We also classified the pollen on their bodies to identify the floral resources they used from the floral species available at that time. We characterized land use for each bee as the relative proportion of GPS points inside of each land use. Bumblebees differed markedly in their movement behavior in relation to pre and post nest establishment. Bees moved over larger areas, and mostly within blueberry fields, before nest establishment. In contrast, after establishing the nest, the bees preferred the edges near forest plantations and they changed the nutritional resources to prefer wild floral species. Our study is the first to track queen bumblebee movements in an agricultural setting and relate movement changes across time and space with pollen resource availability. This study provides insight into the way bumblebee queens use different habitat elements at crucial periods in their lifecycle, showing the importance of mass flowering crops like blueberry in the first stages of queen’s lifecycle, and how diversified landscapes help support bee populations as their needs changes during different phases of their lifecycle.

Chronic bee paralysis virus (CBPV) in South American non-Apis bees.

Chronic bee paralysis virus (CBPV) is a positive single-stranded RNA virus that exhibits a worldwide distribution. Although the effects of this virus on honeybees' health are well known, its presence in other bee species has not been fully studied. In this work, CBPV was detected in several native bees from Argentina, including Bombus pauloensis, Halictillus amplilobus, Peponapis fervens, and members of the genus Xylocopa. Here, we report for the first time the presence of CBPV in native bees from South America.

The melittofauna and its floral associations in a natural riparian forest in Buenos Aires province, Argentina

This study estimates the diversity, abundance and floral associations of native wild bees present in a nature reserve in Buenos Aires, Argentina. The study included monthly sampling from September to April for two consecutive seasons (2011–2013). Bees were collected using entomological nets and pan traps along transects in the reserve area. A total of 1102 specimens belonging to 87 wild bee species/morphospecies in 37 genera of five families were collected. The families with the highest numbers of species were Apidae, followed by Halictidae and Megachilidae. A total of 63 species/morphospecies of plants belonging to 20 families were visited by bees. Asteraceae received the most visits, followed by Fabaceae and Onagraceae. Wild bee/plant interactions were studied through niche breadth and niche overlap. The highest values for niche breadth were found in two social species (Bombus pauloensis and Augochlora amphitrite) and niche overlap was predominantly low among bee species. Our results suggest that the nature reserve “Reserva Natural Integral Punta Lara” in northeastern Buenos Aires Province, Argentina, is an important natural area that supports a diverse community of wild bees.

Parasites and pathogens associated with native bumble bees (Hymenoptera: Apidae: Bombus spp.) from highlands in Bolivia and Peru

ABSTRACT Bumble bees of the genus Bombus spp. play a key role as effective pollinators in the biodiversity rich Central Andean region; however, parasites and pathogens may negatively influence their abundance and population numbers. In this study, we aimed at verifying the occurrence of these natural enemies in the Andes regions of Bolivia and Peru. Workers and males of Bombus funebris, Bombus opifex and Bombus pauloensis were collected in three localities from highlands at ~1,700 m.a.s.l. Analyses by both optical and molecular techniques revealed the presence of the Apis mellifera filamentous virus (AmFV), the microsporidium Vairimorpha ceranae, the flagellates Crithidia bombi and Lotmaria passim, and five species of mites in the genera Parasitellus Willmann, Pneumolaelaps Berlese, Proctolaelaps Berlese, Tyrophagus Oudemans, and Kuzinia Zachvatkin. Given the potential entry of the allochthonous bumble bee Bombus terrestris to the region, this information is essential to evaluate autochtonous biodiversity conservation strategies.

Broad Geographic and Host Distribution of Apis mellifera Filamentous Virus in South American Native Bees

Abstract Apis mellifera filamentous virus (AmFV) is a large double stranded DNA virus of honey bees and its prevalence and relationship with other parasites is poorly known. Samples consisted of fifty-one adult bees belonging to eight native species collected using entomological nets in six provinces of Argentina, from 2009 to 2018. Total genomic DNA was extracted from individual bees and a 551 bp fragment of the Bro-N gene of AmFV was amplified by qPCR. In the present work we have reported for the first time both the presence and the wide geographic distribution of AmFV in Argentinian species of native bees. This is the first report of the presence of this virus associated with Xylocopa atamisquensis, X. augusti, X. frontalis, X. spendidula, Bombus pauloensis and Peponapis fervens. Detecting pathogens that could threaten native bee health is of outmost importance to generate both conservation and management strategies.

Temporal drop of genetic diversity in Bombus pauloensis

Bumblebees are economically important insects which perform essential pollination tasks in natural and managed ecosystems. Recent research studying Neotropical bumblebee species in Brazil showed a clear decrease in genetic diversity over time in Bombus pauloensis. A new temporal assessment of genetic diversity is needed to know whether this was a location-specific result, or a more general phenomenon. This knowledge is essential to be able to prioritize conservation and management needs. Here, the genetic variability of B. pauloensis populations in Argentina was investigated over time using museum collection specimens from 1933 to 2016, and compared with reanalyzed data from Brazilian populations. Furthermore, specific time series were made for two Argentinean locations, Candelaria and La Plata, and compared with the time series of Porto Alegre (Brazil). All collected specimens were genotyped with 16 microsatellite loci to estimate genetic diversity parameters. Our results showed no drop in either allelic richness or expected heterozygosity over all Argentinean populations. However, a clear drop in genetic diversity was observed in two out of three location-specific time series. This loss of diversity will have negative impacts on population survival, especially over longer periods of time. Furthermore, the use and release of mass-reared specimens of B. pauloensis, which may be inbred and specifically selected for certain commercial but non-adaptive traits, could further diminish the genetic pool. Thus, our result implies the urgent need for regional conservation policies of B. pauloensis in South Brazil and North Argentina.

Entomofauna and potential pollinators of strawberry crop under semi-hydroponic conditions

ABSTRACT Strawberry cultivation under semi-hydroponic conditions has increased in the Southern region of Brazil since it facilitates management, besides avoiding weather adversities, pests and diseases. However, protected environment can hamper the access of pollinator insects, essential for crop productivity. This work aimed to know the entomofauna associated with strawberry cultivar Albion cultivated under semi-hydroponic conditions and to identify potential species of native pollinating bees. Insects were captured at different times of the day (9:30 a.m., 12:30 p.m. and 3:30 p.m.) in three commercial crops located in Bento Gonçalves and Farroupilha, Rio Grande do Sul. In each study area, three days of sampling were carried out during January 2017. The flowers were visited by 47 species of insects. Apis mellifera (Hymenoptera: Apidae) was the most abundant, constant, dominant and frequent species. Twelve species of native bees were identified: Tetragonisca fiebrigi, Tetrapedia sp., Trigona spinipes, Schwarziana quadripunctata, Plebeia emerina, P. remota, Bombus pauloensis (Hymenoptera: Apidae), Dialictus sp.1, Dialictus sp.2, Augochloropsis sp.1, Augochloropsis sp.2, and Augochlora sp.1 (Hymenoptera: Halictidae). All these species are potential pollinators of the crop. The native species T. fiebrigi, P. emerina and P. remota present potential for directed pollination of the strawberry under protected cultivation due to abundance and ease of management.

Bees Diversity on Flowers of Eremanthus spp. (Asteraceae)

ABSTRACT Bees are considered important pollinators due to their fidelity to plants, enabling the maintenance of gene flow between plant species. The objective of this study was to recognize the visit of bees in two Candeia species, Eremanthus erythropappus and Eremanthus incanus (Asteraceae), as well as to analyze the pollen content carried by bees in a regeneration area. Nine samplings were taken in each plant species using entomological nets. The pollen grains were obtained in 338 bees from their legs and bodies. The species Trigona spinipes, Apis mellifera, and Bombus pauloensis were most frequent. Candeias are essential in the study area because they have high adaptive potential, but besides them, other plants are also important for attracting bees searching for pollen and/or nectar.

Diversity of bees and their interaction networks with Ludwigia sericea (Cambessides) H. Hara and Ludwigia peruviana (L.) H. Hara (Onagraceae) flowers in a swamp area in the Brazilian Atlantic Foresteae) flowers in Atlantic Forest Area in Southern Brazil

In Southern Brazil the great diversity of bees is due to the richness of ecosystems in the region and when studies attribute the processes for identification of the floral resources used by bees we can get important steps for the elaboration of management and conservation plans of the species involved. Based on this setting and considering that the study area is a "várzea" (swamp) with a large concentration of flowers of Ludwigia sericea and Ludwigia peruviana, important sources of resources for bees, the aim of this study was to find out about the floral visitor bees and through palynological studies and interaction networks, understand the role of these plants as providers of pollengrains to bees and how the bees interact with them and other plants, also found in this habitat. Ludwigia sericea, Ludwigia peruviana and the other plant species are presented as generalist in the interactions with the bee species, and the same occurs for most of the bee species in relation to these plants. Generalist bee species (Bombus pauloensis, Apis mellifera, Augochlora amphitrite and Melissoptila paraguayensis) tend to be more abundant and more resistant to disturbances than the specialist species. It was the first time that Plebeia emerina, Centris varia, Mourella caerulea and Augochlorella ephyra were recorded on the Ludwigia flowers in Brazil. Based on the results presented in this study, these plants are important for maintaining the bee community in the region of the Atlantic Forest in Southern Brazil, because they provide resources (nectar and pollen) to bee species that only occur in this region.

Floral biology, nectar secretion pattern and fruit set of a threatened Bignoniaceae tree from Brazilian tropical forest

Zeyheria tuberculosa, a Bignoniaceae tree that occurs in a broad latitudinal range in Brazilian forests, is a threatened species of seasonal tropical forest. It is crucial to enhance the knowledge on this species’ floral biology, since interactions related to reproduction of plants are critical for the long term maintenance of their populations. Thus, we investigated the sexual reproduction and floral biology of Z. tuberculosa, including nectar features, aiming to understand the ecological processes associated to this mutualistic plant-animal interaction in the current modified landscape. For this, we performed experiments under natural conditions and in the laboratory. All the evaluated plants were self-incompatible. Zeyheria tuberculosa was pollinated by Bombus pauloensis, a medium-sized bee, and offered hexose-rich nectar as resource. Flowers were also visited by small-sized bee species, Trigona spinipes, that acted as pollen thief, and Pseudoaugochlora pandora and P. graminae that acted as nectar thieves. These three bee groups exhibited temporal separation in the peak of visits throughout the day. The peak of pollinator visits occurred firstly, which may allow the pollinator to access nectar and pollen loads before they are exploited by thieves. However, bee pollinator visits were scarce, and this fact, associated to the self-incompatibility of Z. tuberculosa, may explain the low fruit set registered in the studied plants. It could be of special concern for this threatened species maintenance in the medium and long term, which depends on the offspring originated by sexual reproduction.

Effects of pollen origin on apomixis in Zygopetalum mackayi orchids

Reproductive and pollination biology studies are crucial to understand processes of diversification in plants. The facultative apomictic orchid Zygopetalum mackayi comprises a potential model in the Neotropics to understand the role of asexuality in the reproductive success of plants. Adventive embryogenesis is the main mechanism behind the production of clonal embryos in Z. mackayi and it has been associated with polyembryony. Previous studies suggested all seeds (mono-/polyembryonic) to be of apomictic origin. If so, we expect to find no difference in seed viability from self- and cross-pollinations, considering monoembryonic and polyembryonic seeds. To test this prediction, we estimated how pollen origin affects fruit set and seed viability. We also investigated if reproduction is dependent on pollinators and described how pollination is achieved. We collected phenological and pollination data in one natural population and sampled five additional populations for studies of the reproductive system. To access seed viability, we stained seeds with a tetrazolium solution. Z. mackayi is a generalized food-deceptive species pollinated by Bombus pauloensis. This species is also dependent on pollinators for reproduction as individuals are unable to perform spontaneous self-pollination. Self- and cross-pollination treatments yielded mainly monoembryonic seeds, but crossed flowers produced more viable monoembryonic seeds than self-pollinated ones. Sexual reproduction is dominant in Z. mackayi because monoembryonic seeds are more frequent in both cross- and self-pollinated flowers and more viable when pollen comes from a different individual. Self-pollinated flowers set more polyembryonic seeds than crossed ones, although there were no differences in seed viability between treatments considering all types of seeds produced. We hypothesize that embryo abortion by inbreeding depression in self-pollinated flowers is compensated by apomictic reproduction in Z. mackayi, as polyembryonic seeds are a common outcome of apomixis. We propose polyploidy, not pollen limitation, is responsible for the evolution of apomixis in this orchid species.

Inferring sex and caste seasonality patterns in three species of bumblebees from southern Brazil using biological collections.

Biological collections may often be an important source of information about natural history, behavioral habits, and ecology as they contain samples of organisms collected in different places and moments in times. In here, we used museum specimens to examine how populations of three species of Bombus-Bombus bellicosus Smith, Bombus morio (Swederus), and Bombus pauloensis Friese-vary over time with respect to abundance and biomass of each sex and caste. The study included all specimens of these three bumblebee species deposited in the insect collection of the Federal University of Parana that were collected in eastern Paraná, in southern Brazil. Seasonality is most noticeable in the peak of queen activity (number of individuals in collections) in early spring, after dormancy during the winter. Queens then founded nests, and workers and males began to become more abundant during spring and summer. Worker abundance peaked at the end of summer and beginning of fall and may correspond to increasing activity for production of new males and gynes. Male abundance peaks are during the reproductive period. Thus, we show with these data and analyses that museum collections can be very useful tools to examine temporal and ecological processes. We recommend greater use of museum accessions to explore these kinds of patterns that may otherwise go unnoticed.

A comparative study of the antennal sensilla in corbiculate bees

SummarySensilla are the basic structures that allow the perception of environmental cues that play a role as mechanoreceptors, chemoreceptors, thermoreceptors and hygroreceptors associated with their morphology. Because bees have different degrees of sociability, they are a good model for the study of sensilla types and distribution linked with behaviour. This work identifies the types of sensilla in the antennae of bees with different degrees of sociability. The antennae of 18 species of bee were analysed with a scanning electron microscope. Trichoid and placoid sensilla are present in all antennomers of the species studied. The honey bee Apis mellifera and bumble bee Bombus pauloensis workers have higher diversity and sensillum distribution in comparison with males. In stingless bees, species of Meliponaare representative of a homogeneous group for sensilla types and distribution. The types and distribution of sensilla in the antennae of bees seems to be associated with the degree of sociability.