Native Bumblebees Research Articles

First records of the Common Eastern Bumble Bee, Bombus impatiens Cresson (Hymenoptera: Apidae, Apinae, Bombini) from the Prairies Ecozone in Canada.

BackgroundIn Canada, the Common Eastern Bumble Bee (Bombus impatiens Cresson) is native to southern Ontario and Quebec, but since being developed as a managed commercial pollinator, it has been exported to several other provinces for use in greenhouse and field crop settings. This has enabled this species to become established outside its natural range and it is now established in eastern Canada (New Brunswick, Nova Scotia, Prince Edward Island) and British Columbia. To date, the species has not been detected via field capture in the prairie provinces.New informationHere we report on recent captures of B. impatiens workers and males from south-eastern Alberta and suggest that these specimens escaped from nearby commercial greenhouses. The risk that the presence and looming establishment of this species has on native bumble bees in the Canadian prairies is discussed.

Phoretic mites associated to Bombus pauloensis and Bombus bellicosus (Hymenoptera: Apidae) from Uruguay

Bumble bees (Bombus spp.), considered as important angiosperm pollinators, harbor several mite species associated with their nests. In the present study, 403 bumble bees – B. pauloensis (n = 285) and B. bellicosus (n = 118) – were surveyed at five departments from Uruguay: Canelones, Colonia, Montevideo, Florida and Soriano. The mite species Kuzinia spp. Pneumolaelaps longanalis, P. longipilus, Scutacarus acarorum, and Tyrophagus putrescentiae were found associated with both bumble bee species. At least one mite was present on 30% of the bumble bees. We compared the mite prevalence, abundance, intensity and Simpson’s diversity index between bumble bee species and castes. Bumble bee caste was the most influential factor on mite presence, and also on the composition of the phoretic mite community. The assemblages described here could be relevant for future studies focusing on potential threatens for native bumble bees. In combination with a pathogen screening, this data could be proposed as a relevant approach for monitoring native pollinators, especially in areas where they are threatened. The establishment of descriptive indices for threatened and healthy populations would be then of great value for species conservation.

Contrasting occurrence patterns of managed and native bumblebees in natural habitats across a greenhouse landscape gradient

In recent decades, there has been a remarkable expansion of pollinator-dependent crops. An increase in the use of commercial pollinator colonies associated with these crops may promote the spillover of managed pollinators into nearby natural habitats. There, these managed pollinators can exploit floral resources similar to those of wild pollinators, and thus increase competition for local resources. Nonetheless, managed pollinator spillover has been poorly studied and research has focused on only one species, the western honeybee (Apis mellifera). In south-western Spain, we investigated the presence, density and exploitation of floral resources by managed (Bombus terrestris) and native bumblebees (B. t. lusitanicus) in 19 Mediterranean pinewood understories across a landscape gradient of strawberry polytunnel greenhouse cover. Sampling was performed over two consecutive years in two seasons: winter, when strawberries begin flowering and farmers frequently use colonies, and spring, when there is greater availability of floral resources and wild pollinators thrive. In winter, the density of managed bumblebees in pinewoods was higher than that of native bumblebees. The presence of managed and native bumblebees in pinewoods showed contrasting patterns in relation to greenhouse cover in the landscape. The presence of managed bumblebees was positively associated with greenhouse cover, whereas that of native bumblebees was negatively associated with greenhouse cover. Overall, the presence and density of bumblebees did not differ between seasons. The two bumblebee subspecies showed similar wild flowering plant preferences, particularly in winter, when flowering plant species are scarce. We conclude that, although managed bumblebees are placed in greenhouse crops, their pollination role extends beyond these crops. Further studies are needed to assess the pollination function of managed pollinators in crops in order to reduce their spillover into natural habitats and thus, the risks posed to native pollinators.

Distance models as a tool for modelling detection probability and density of native bumblebees

AbstractEffective monitoring of native bee populations requires accurate estimates of population size and relative abundance among habitats. Current bee survey methods, such as netting or pan trapping, may be adequate for a variety of study objectives but are limited by a failure to account for imperfect detection. Biases due to imperfect detection could result in inaccurate abundance estimates or erroneous insights about the response of bees to different environments. To gauge the potential biases of currently employed survey methods, we compared abundance estimates of bumblebees (Bombus spp.) derived from hierarchical distance sampling models (HDS) to bumblebee counts collected from fixed‐area net surveys (“net counts”) and fixed‐width transect counts (“transect counts”) at 47 early‐successional forest patches in Pennsylvania. Our HDS models indicated that detection probabilities of Bombus spp. were imperfect and varied with survey‐ and site‐covariates. Despite being conspicuous, Bombus spp. were not reliably detected beyond 5 m. Habitat associations of Bombus spp. density were similar across methods, but the strength of association with shrub cover differed between HDS and net counts. Additionally, net counts suggested sites with more grass hosted higher Bombus spp. densities whereas HDS suggested that grass cover was associated with higher detection probability but not Bombus spp. density. Density estimates generated from net counts and transect counts were 80%–89% lower than estimates generated from distance sampling. Our findings suggest that distance modelling provides a reliable method to assess Bombus spp. density and habitat associations, while accounting for imperfect detection caused by distance from observer, vegetation structure, and survey covariates. However, detection/non‐detection data collected via point‐counts, line‐transects and distance sampling for Bombus spp. are unlikely to yield species‐specific density estimates unless individuals can be identified by sight, without capture. Our results will be useful for informing the design of monitoring programs for Bombus spp. and other pollinators.

Searching for Molecular Markers to Differentiate Bombus terrestris (Linnaeus) Subspecies in the Iberian Peninsula

Bumblebees (genus Bombus Latreille) are pollinator insects of great ecological and economic importance, which commercial use for pollination has increased since the 80s. However, the introduction of foreign Bombus terrestris (Linnaeus) has resulted in a decline of native bumblebee populations in Japan, Chile or Argentina among others. To study the potential introgression of commercial B. terrestris into the Iberian endemic subspecies Bombus terrestris lusitanicus Krüger, it is necessary to find a precise molecular marker that differentiates both subspecies. For this purpose, comparative analyses were carried out between B. t. lusitanicus and B. t. terrestris (Linnaeus) from Spain and from Belgium by sequencing the nuclear genes elongation factor 1-α and arginine kinase and the mitochondrial gene 16S ribosomal RNA, and genotyping with eleven microsatellite loci. No differentiation was observed at the nuclear level, but haplotypes found within the 16S sequence correlated with the morphological characterization of the subspecies. In a case study including individuals sampled before the establishment of bumblebee rearing companies and others from recent samplings, we detected hybrid individuals (those with non-matching morphological subspecies and 16S haplotype) more frequently in the south supporting the naturalization of commercial B. t. terrestris and introgression events between both subspecies. This marker should be used in Iberian populations with the aim to support management and conservation actions in endemic populations of B. t. lusitanicus.

Queen traits and colony size of four bumblebee species of China

Bumblebee pollination efficiency is significantly affected by colony size, which differs among different bumblebee species. Bumblebee colonies are initiated by a single queen; thus queen traits have an important influence on colony development. To make better use of native bumblebee species and select bumblebee species for commercial rearing, queens from four bumblebee species in China, Bombus terrestris, B. lantschouensis, B. patagiatus and B. ignitus, were reared and studied to determine whether differences in queen traits and colony size occur at the interspecific level. In our study, the four bumblebee species differed significantly in colony size, queen body length, spermatheca size and sperm quantity. The queens of the four species mated only once. Among these four bumblebee species, the species with more sperm in the queen’s spermatheca usually exhibited a larger colony size. The quantity of sperm in the queen’s spermatheca might serve as an indicator for selecting bumblebee species with commercial rearing potential. However, our study involved only four bumblebee species; more bumblebee species are needed to confirm the correlation between queen sperm quantity and colony size.

Observations of native bumble bees inside of commercial colonies ofBombus impatiens(Hymenoptera: Apidae) and the potential for pathogen spillover

AbstractMany fruit producers use commercial colonies ofBombus impatiensCresson (Hymenoptera: Apidae) to supplement crop pollination by native bees. A small number of Newfoundland (Newfoundland and Labrador, Canada) farmers forego purchasing new colonies and, instead, purchase previously used colonies from crops in other provinces. This practice has potentially dangerous implications that may adversely affect future native bee diversity in Newfoundland. This study is the first to record the presence of native bumble bee species inside the colonies of new and pre-used commercialB. impatiensand the first to look at diseases in native bumble bees from Newfoundland. Polymerase chain reaction and taxon-specific oligonucleotides were used to screen the commercial and native bumble bee species for pathogens.Crithidia bombi(Lipa and Triggiani), Apicystis bombi(Liu, Macfarlane, and Pengelly),Nosema bombiFantham and Porter, Nosema ceranaeFrieset al., and species ofAscosphaeraOlive and Spiltoir, were detected in native bumble bees that were collected from inside the new and pre-used commercialB. impatiens.Crithidia bombi,A. bombi, andN. bombiwere also detected among native bees that were collected away from the commercial colonies.Nosema apis(Zander) andMelissococcus plutonius(White) were not detected in any of the bees tested. The mixing of native bumble bees inB. impatienscolonies increases the potential for pathogen spillover and spillback that may threaten the small and vulnerable island bee fauna.

Non-native plants affect generalist pollinator diet overlap and foraging behavior indirectly, via impacts on native plant abundance

Flowering invasive plants can have dramatic effects on the resource landscape available to pollinators. Because many pollinators exhibit behavioral plasticity in response to competitor or resource density, this in turn can result in impacts on ecological processes such as pollination and plant reproduction. We examine how interactions between five common generalist eusocial bees change across an invasion gradient by examining how bee abundance and diet overlap changed with variation in both invasive plant abundance and competitor abundance in a temperate oak-savannah ecosystem. Specifically we focus on the bumblebees Bombus bifarius, B. mixtus, B. melanopygus and B. vosnesenskii, as well as the non-native honeybee Apis mellifera, and their interactions with the native flowering plants Camassia quamash, Camassia liechtlinii, and the invasive shrub Cytisus scoparius. We further examine whether changes in pollinator visits to the invasive and two common native plants can explain changes in diet overlap. Abundance of the invasive plant and other common floral resources had strong impacts on focal bee abundance, with certain species more likely to be present at highly invaded sites. This may be because highly invaded sites tended to be embedded in forested landscapes where those bees are common. Diet overlap was most affected by abundance of a common native plant, rather than the invasive plant, with diet overlap increasing non-linearly with abundance of the native plant. Furthermore, Apis mellifera, did not appear to have direct competitive effects on native bumblebees in this habitat. However, visit patterns suggest that bees most abundant at highly invaded sites may compete for access to native resources. Thus the impacts of this invasive plant on our focal bee species may be primarily indirect, via its’ competitive effects on native plants.

Odor Learning and Its Experience-Dependent Modulation in the South American Native Bumblebee Bombus atratus (Hymenoptera: Apidae).

Learning about olfactory stimuli is essential in bumblebees’ life since it is involved in orientation, recognition of nest sites, foraging efficiency and food yield for the colony as a whole. To evaluate associative learning abilities in bees under controlled environmental conditions, the proboscis extension response (PER) assay is a well-established method used in honey bees, stingless bees and successfully adapted to bumblebees of the genus Bombus. However, studies on the learning capacity of Bombus atratus (Hymenoptera: Apidae), one of the most abundant native species in South America, are non-existent. In this study, we examined the cognitive abilities of worker bees of this species, carrying out an olfactory PER conditioning experiment. Bumblebees were able to learn a pure odor when it was presented in paired association with sugared reward, but not when odor and reward were presented in an unpaired manner. Furthermore, if the bees were preexposed to the conditioned odor, the results differed depending on the presence of the scent either as a volatile in the rearing environment or diluted in the food. A decrement in learning performance results from the non-reinforced pre-exposure to the to-be-conditioned odor, showing a latent inhibition phenomenon. However, if the conditioned odor has been previously offered diluted in sugared reward, the food odor acts as a stimulus that improves the learning performance during PER conditioning. The native bumblebee B. atratus is thus a new hymenopteran species capable of being trained under controlled experimental conditions. Since it is an insect increasingly reared for pollination service, this knowledge could be useful in its management in crops.

Genetic structure of the bumble bee Bombus hypocrita sapporoensis, a potential domestic pollinator for crops in Japan

The European bumble bee, Bombus terrestris, is an excellent commercial pollinator. In Japan, B. terrestris is categorized as an invasive alien species, and the use of the bee is restricted. In this study, we identify the native bumble bee Bombus hypocrita sapporoensis as a candidate commercial pollinator in Hokkaido Island. To evaluate the risk of disturbing the natural genetic structure if this bee is used as a commercial pollinator, we sequenced the mitochondrial cytochrome c oxidase subunit I (COI) gene to elucidate the phylogenetic relationship of B. h. sapporoensis in Hokkaido Island and the Asian continent. In addition, we analyzed six microsatellites to further investigate the population genetic structure in Hokkaido Island. The mitochondrial analyses revealed that there is little differentiation within Hokkaido Island; however, there is considerable differentiation between Hokkaido and the Asian continent. Microsatellite analyses using STRUCTURE showed that B. h. sapporoensis in Hokkaido was divided into two genetic groups. Individuals belonging to each group were distributed throughout Hokkaido Island, and no clear geographical differentiation was observed. These results indicate that there would be little risk of genetic disturbance if bees from Hokkaido Island were used. However, it would be advisable to avoid importing continental bees as a pollinating insect in Hokkaido Island.

Empirical, Metagenomic, and Computational Techniques Illuminate the Mechanisms by which Fungicides Compromise Bee Health.

Growers often use fungicide sprays during bloom to protect crops against disease, which exposes bees to fungicide residues. Although considered "bee-safe," there is mounting evidence that fungicide residues in pollen are associated with bee declines (for both honey and bumble bee species). While the mechanisms remain relatively unknown, researchers have speculated that bee-microbe symbioses are involved. Microbes play a pivotal role in the preservation and/or processing of pollen, which serves as nutrition for larval bees. By altering the microbial community, it is likely that fungicides disrupt these microbe-mediated services, and thereby compromise bee health. This manuscript describes the protocols used to investigate the indirect mechanism(s) by which fungicides may be causing colony decline. Cage experiments exposing bees to fungicide-treated flowers have already provided the first evidence that fungicides cause profound colony losses in a native bumble bee (Bombus impatiens). Using field-relevant doses of fungicides, a series of experiments have been developed to provide a finer description of microbial community dynamics of fungicide-exposed pollen. Shifts in the structural composition of fungal and bacterial assemblages within the pollen microbiome are investigated by next-generation sequencing and metagenomic analysis. Experiments developed herein have been designed to provide a mechanistic understanding of how fungicides affect the microbiome of pollen-provisions. Ultimately, these findings should shed light on the indirect pathway through which fungicides may be causing colony declines.

Body Fatty and Amino Acid Composition of a Native Bumblebee, Bombus ignitus Relative to B. terrestris of Foreign Origin in Korea

Bombus terrestris is imported and now commercially produced, while B. ignitus is the native bumblebee species, which is in the process of commercialization in Korea. For the successful rearing, understanding the body composition is important parameter to understand the diet requirement. We measured and compared body fat and amino acid composition of two bumblebee species under mated condition. The results revealed that there was significant difference in the body weight of two tested species. The quantity of body fat (fatty acids) and proteins (amino acids) was found higher in B. ignitus than that was reported for B. terrestris. However, individual fatty acid and amino acid distribution was similar in both species. Dominant fatty acids were oleic acid and palmitoleic acid of among monounsaturated fatty acid, palmitic of saturated fatty acid, and linoleic acid of polyunsaturated fatty acid. Among amino acids, glutamic acid was predominant followed by glycine and leucine. To foster the population of native bumblebee i.e. B. ignitus through rearing, appropriation of feed formulation could be based on this result which could lead the purpose of feed development for indigenous population.

Gyne and Drone Production in Bombus Atratus (Hymenoptera: Apidae)

AbstractFor over a decade, our research group has studied the biology of the native bumblebee, Bombus atratus, to investigate the feasibility of using it to pollinate crops such as tomato, strawberry, blackberry and peppers. Traditionally, captive breeding has depended on the use of captured wild queens to initiate the colonies. The goal of the current work is to investigate conditions required to produce new queens and drones in captivity. In this study, 31 colonies were evaluated under either greenhouse or open field conditions over a 15 month period. A total of 1492 drones (D) and 737 gynes (G, i.e., virgin queens) were produced by all colonies, with 16 colonies producing both drones and gynes (D&G), 11 producing only drones (D) and 4 producing neither. Some of the D&G colonies had more than one sexual phase, but no colonies produced exclusively gynes. More drones and fewer gynes were produced per colony under greenhouse conditions with the highest number of drones produced by D&G colonies. The numbers of immature stages per cell declined in colonies as increasingly more resources were allocated to the production of gynes and the maintenance of increased nest temperature.

Long-term prevalence of the protists Crithidia bombi and Apicystis bombi and detection of the microsporidium Nosema bombi in invasive bumble bees.

An initial survey in 2009 carried out at a site in northwestern Patagonia region, Argentina, revealed for the first time in South America the presence of the flagellate Crithidia bombi and the neogregarine Apicystis bombi, two pathogens associated with the Palaearctic invasive bumble bee Bombus terrestris. In order to determine the long-term persistence and dynamics of this microparasite complex, four additional collections at the same site (San Carlos de Bariloche) were conducted along the following seven years. Both protists were detected in all collections: prevalence was 2%-21.6% for C. bombi and 1.2%-14% for A. bombi. In addition, the microsporidium Nosema bombi was recorded for the first time in the country in the last two collections, at prevalences of 12.4% and 2.4% and unusually high infection intensities (Average = 6.56 × 107 spores per individual). Due to the exceptional dispersal ability of the exotic B. terrestris, these three multihost pathogens should be considered as potential threats to South American native bumble bees.

Native bumble bee (Hymenoptera: Apidae) pollinators vary in floral resource use across an invasion gradient

AbstractIntegration of pollinator-dependent invasive plants into native pollination networks can have direct and indirect effects on local plant and pollinator communities. Impacts on local plants are well documented; however effects on native pollinators have gained less attention. We examine these issues in habitat fragments of the endangered oak-savannah ecosystem in British Columbia, Canada. We measured pollen collection by native bumble bees (Bombus Latreille; Hymenoptera: Apidae) and the introduced honey bee (Apis mellifera Linnaeus; Hymenoptera: Apidae) foraging on two common native plants in habitat fragments with varying invasive (Cytisus scoparius (Linnaeus) Link; Fabaceae) density. The Bombus species with the largest workers had higher proportions of invasive pollen on their bodies and in their corbiculae than smaller workers. Honey bees rarely collected C. scoparius pollen. While some native bumble bees species collect an increasing proportion of C. scoparius pollen with increasing C. scoparius density, this did not translate into an increased potential for pollination. Rather, measures of effective pollination decline with C. scoparius density. Overall, our results suggest that some bee species may be better at finding resources at highly invaded sites. Apis mellifera is likely not playing a major role in facilitating the spread of C. scoparius in our region. Rather C. scoparius is visited by a complement of native bumble bees that are similar to pollinators in the native range of this plant.

Exploring the predation of UK bumblebees (Apidae, Bombus spp.) by the invasive pitcher plant Sarracenia purpurea: examining the effects of annual variation, seasonal variation, plant density and bumblebee gender

Invasive carnivorous plant species can impact the native invertebrate communities on which they prey. This article explores the predation of native UK bumblebees (Bombus spp.) by the invasive pitcher plant species Sarracenia purpurea and discusses the potential effect of S. purpurea on native bumblebees. Specifically, it evaluates whether the extent to which bumblebees are captured varies (i) over successive years, (ii) across June and July, (iii) with density of distribution of pitchers or (iv) with bumblebee gender. Pitcher contents were examined from an established population of Sarracenia purpurea growing in Dorset, UK. Results show that the total extent to which bumblebees were captured differed over the years 2012–2014 inclusive. A 1-year study in 2013 showed that more bumblebees were caught in July than in June and more bumblebees were captured when pitchers grew at high density. Results from 2013 also showed that more pitchers caught more than one bumblebee than would be expected based on a normal probability distribution and that this phenomenon affects female and male bumblebees equally. We discuss possible reasons for these results including that the bumblebees may be using S. purpurea as a resource. Further work is required to establish the exact underpinning mechanisms and the relative roles of plant and bumblebee behaviour within the relationship. Such interaction complexity may have consequences for consideration in invasive carnivorous plant management.

Estimating resource preferences of a native bumblebee: the effects of availability and use–availability models on preference estimates

Identifying resource preference is considered essential for developing targeted conservation plans but, for many species, questions remain about the best way to estimate preference. Resource preferences for bees are particularly difficult to determine as the resources they collect, nectar and pollen, are challenging to estimate availability and collection. Resources are traditionally measured at the flower or inflorescence level, but these measures of availability do not correspond to the resources actually used by bees. Additionally, it is unclear as to whether common models including availability are appropriate for bees which may target resources regardless of available quantities. Here we first compare two common hypotheses of resource use – the ‘random use hypothesis’ and the ‘linear preferences hypothesis’ – using three different measures of availability (pollen, flower and inflorescence) – to determine if one measure of availability was better for understanding bee pollen use. Next, the superior model using availability was compared to a novel model of bee pollen use the ‘target use hypothesis’. This model assumes that bees target some resources regardless of how much of each resource is available (but assuming resources are present at a site), and thus models preference without availability data. Of the models including availability, the linear preference model using inflorescence availability best explained the pollen use data. This suggests that bumblebee pollen use is non‐random and that cues to identify and locate resources (i.e. display size and quantity) may be more important than the quantity of the resource available (i.e. pollen availability). Additionally, in most cases the target use model explained the data equal to or better than the other models suggesting bee resource use may be better modeled without measured availability data compared to linear models. These results could be important for expanding resource use analysis of bees that are difficult to quantify availability.

Effects of alien invasion by Bombus terrestris L. (Apidae) on the visitation patterns of native bumblebees in coastal plants in northern Japan

When alien pollinator species enter a native community of pollinators in which resource partitioning has been established, the pollination network between plants and pollinators may be modified through the interactions between the pollinators over the use of floral resources. We observed the floral-use patterns of native (Bombus hypocrita and B. deuteronymus) and alien (B. terrestris) bumblebee species in a coastal grassland in northern Japan. We analyzed the factors determining resource partitioning patterns. B. hypocrita tended to visit flowers with shallow or wide open corollas, such as Rosa rugosa, whereas B. deuteronymus visited flowers with complex or deeper corollas, such as Lathyrus japonicus. Given the wider floral preference of B. terrestris, floral use by the alien bumblebees consistently overlapped with that of native bumblebees. The visitation of B. terrestris to R. rugosa flowers was positively correlated with that of B. hypocrita. These bumblebee species frequently used similar floral resources, in part because of the large overlap in the seasonality of their foraging activity. The visitation frequency of B. deuteronymus to L. japonicus flowers was independent of the visitation frequency of other bumblebee species. The major visitation periods of the bumblebees to L. japonicus flowers reciprocally differed between B. deuteronymus and B. terrestris, suggesting phenological resource partitioning between these species. Our study suggests that phenological niche partitioning is more common in specialized flowers (L. japonicus) than in generalized flowers (R. rugosa).

High prevalence and infection levels of Nosema ceranae in bumblebees Bombus atratus and Bombus bellicosus from Uruguay

Nosema ceranae is one of the most prevalent pathogens in Apis mellifera and has recently been found in multiple host species including several species of bumblebees. Prevalence and infection intensity of N. ceranae was determined in two species of native bumblebees from Uruguay. Nosema ceranae was the only microsporidia identified and mean prevalence was 72% in Bombus atratus and 63% in Bombus bellicosus, values much higher than those reported elsewhere. The presence of this pathogen in bumblebees may be threatening not only for bumblebee populations, but also to the rest of the native pollinator community and to honeybees.

Exposure Effects on the Productivity of CommercialBombus impatiens(Hymenoptera: Apidae) Quads During Bloom in Watermelon Fields

In light of population declines of honey bees (Apis mellifera L.), research has refocused attention on alternative pollinators and their potential to fulfill pollination services within economically important agricultural crops. Bumble bees are one such alternative, and within the past 20 yr, these pollinators have been reared and sold as commercial pollinators. Investigation into their use has been limited and more research is needed to improve pollinator effectiveness in field settings. Quad pollination units of the commercially reared native bumble bee species, the common eastern bumble bee (Bombus impatiens Cresson), were monitored and evaluated for productivity during peak watermelon [Citrullus lanatus (Thunberg) Matsumura & Nakai] bloom in southern Delaware. Differing colony exposures including various shade structure designs and natural shade were compared to assess the quality of the shade in regards to bumble bee activity during watermelon bloom. Quads receiving different nest treatments were evaluated on the basis of foraging activity and colony weight gain. Results indicated that colonies within quads provided with artificial or natural shade had significantly more foraging activity, weighed more, and produced more cells than colonies in quads placed in the field with no shade. Colonies within quads provided with artificial and natural shade peaked later in terms of foraging and weight gain, suggesting that growers could extend harvest to take advantage of later markets and possible movement into fields that were planted later.