Ground-nesting Bees Research Articles

Persistent nesting byAnthophoraLatreille, 1803 (Hymenoptera: Apidae) bees in ash adjacent to an active volcano

Ground-nesting bees use a variety of substrates in which to establish cells and complete their reproductive cycles. Here we document the highly aberrant occurrence of a solitary bee species, Anthophora squammulosa Dours, 1870 (Hymenoptera: Apidae: Anthophorini), nesting within meters of an active volcanic crater in Nicaragua, Central America. The nest location is exposed to continuous, strongly acidic gas emissions (>2.7 ppm of SO2), and sporadic vent clearing episodes that blanket the surrounding area with ash and tephra. An assessment of floral resources available within the expected homing distance of the species was cross-referenced with pollen carried by females returning to their nests. At this site, A. squammulosa appears to forage almost exclusively on a single plant, Melanthera nivea (L.) Small, 1903 (Asteraceae), that is adapted to volcanic acidic rain, despite being widely accepted as a generalist bee in the remainder of its range. Notwithstanding the extreme nature of the site, and the co-occurrence of specialist natural enemies and predators, the possibility exists that the site is selected for its beneficial attributes, such as the loose, well-drained substrate and the absence of vegetation. The converse is that the site is sub-optimal with the population constrained by habitat patchiness and limited dispersal options.

Landscape and Local Correlates of Bee Abundance and Species Richness in Urban Gardens.

Urban gardens may preserve biodiversity as urban population densities increase, but this strongly depends on the characteristics of the gardens and the landscapes in which they are embedded. We investigated whether local and landscape characteristics are important correlates of bee (Hymenoptera: Apiformes) abundance and species richness in urban community gardens. We worked in 19 gardens in the California central coast and sampled bees with aerial nets and pan traps. We measured local characteristics (i.e., vegetation and ground cover) and used the USGS National Land Cover Database to classify the landscape surrounding our garden study sites at 2 km scales. We classified bees according to nesting type (i.e., cavity, ground) and body size and determined which local and landscape characteristics correlate with bee community characteristics. We found 55 bee species. One landscape and several local factors correlated with differences in bee abundance and richness for all bees, cavity-nesting bees, ground-nesting bees, and different sized bees. Generally, bees were more abundant and species rich in bigger gardens, in gardens with higher floral abundance, less mulch cover, more bare ground, and with more grass. Medium bees were less abundant in sites surrounded by more medium intensity developed land within 2 km. The fact that local factors were generally more important drivers of bee abundance and richness indicates a potential for gardeners to promote bee conservation by altering local management practices. In particular, increasing floral abundance, decreasing use of mulch, and providing bare ground may promote bees in urban gardens.

Landscape Simplification Constrains Adult Size in a Native Ground-Nesting Bee

Bees provide critical pollination services to 87% of angiosperm plants; however, the reliability of these services may become threatened as bee populations decline. Agricultural intensification, resulting in the simplification of environments at the landscape scale, greatly changes the quality and quantity of resources available for female bees to provision their offspring. These changes may alter or constrain the tradeoffs in maternal investment allocation between offspring size, number and sex required to maximize fitness. Here we investigate the relationship between landscape scale agricultural intensification and the size and number of individuals within a wild ground nesting bee species, Andrena nasonii. We show that agricultural intensification at the landscape scale was associated with a reduction in the average size of field collected A. nasonii adults in highly agricultural landscapes but not with the number of individuals collected. Small females carried significantly smaller (40%) pollen loads than large females, which is likely to have consequences for subsequent offspring production and fitness. Thus, landscape simplification is likely to constrain allocation of resources to offspring through a reduction in the overall quantity, quality and distribution of resources.

Sunflower (Helianthus annuus) pollination in California's Central Valley is limited by native bee nest site location.

The delivery of ecosystem services by mobile organisms depends on the distribution of those organisms, which is, in turn, affected by resources at local and landscape scales. Pollinator-dependent crops rely on mobile animals like bees for crop production, and the spatial relationship between floral resources and nest location for these central-place foragers influences the delivery of pollination services. Current models that map pollination coverage in agricultural regions utilize landscape-level estimates of floral availability and nesting incidence inferred from expert opinion, rather than direct assessments. Foraging distance is often derived from proxies of bee body size, rather than direct measurements of foraging that account for behavioral responses to floral resource type and distribution. The lack of direct measurements of nesting incidence and foraging distances may lead to inaccurate mapping of pollination services. We examined the role of local-scale floral resource presence from hedgerow plantings on nest incidence of ground-nesting bees in field margins and within monoculture, conventionally managed sunflower fields in California's Central Valley. We tracked bee movement into fields using fluorescent powder. We then used these data to simulate the distribution of pollination services within a crop field. Contrary to expert opinion, we found that ground-nesting native bees nested both in fields and edges, though nesting rates declined with distance into field. Further, we detected no effect of field-margin floral enhancements on nesting. We found evidence of an exponential decay rate of bee movement into fields, indicating that foraging predominantly occurred in less than 1% of medium-sized bees' predicted typical foraging range. Although we found native bees nesting within agricultural fields, their restricted foraging movements likely centralize pollination near nest sites. Our data thus predict a heterogeneous distribution of pollination services within sunflower fields, with edges receiving higher coverage than field centers. To generate more accurate maps of services, we advocate directly measuring the autecology of ecosystem service providers, which vary by crop system, pollinator species, and region. Improving estimates of the factors affecting pollinator populations can increase the accuracy of pollination service maps and help clarify the influence of farming practices on wild bees occurring in agricultural landscapes.

Hedgerow presence does not enhance indicators of nest‐site habitat quality or nesting rates of ground‐nesting bees

A major challenge in habitat restoration is targeting the key aspects of a species' niche for enhancement, particularly for species that use a diverse set of habitat features. However, restoration that focuses on limited aspects of a species' niche may neglect other resources that are critical to population persistence. We evaluated the ability of native plant hedgerows, planted to increase pollen and nectar resources for wild bees in agricultural landscapes, to provide suitable nesting habitat and enhance nesting rates of ground‐nesting bees. We found that, when compared to unmanaged field edges (controls), hedgerows did not augment most indicators of nest habitat quality (bare ground, soil surface irregularity, and soil hardness), although coarser soils were associated with higher incidence and richness of nesting bees. Hedgerows did not augment nesting rates when compared to control edges. Although all the bee species we detected nesting were also found foraging on floral resources, the foraging versus nesting assemblages found within a site were highly dissimilar. These results may reflect sampling error; or, species found foraging but not nesting in hedgerows could be utilizing hedgerows as “partial habitats,” nesting outside hedgerow plantings but foraging on the floral resources they provide. We conclude that although hedgerows are known to provide critical floral resources to wild bees especially in resource‐poor intensive agricultural landscapes, simply increasing vegetative diversity and structure may not be simultaneously enhancing nesting habitat for ground‐nesting bees.

Sunflower (Helianthus annuus) pollination in California's Central Valley is limited by native bee nest site location

The delivery of ecosystem services by mobile organisms depends on the distribution of those organisms, which is, in turn, affected by resources at local and landscape scales. Pollinator-dependent crops rely on mobile animals like bees for crop production, and the spatial relationship between floral resources and nest location for these central-place foragers influences the delivery of pollination services. Current models that map pollination coverage in agricultural regions utilize landscape-level estimates of floral availability and nesting incidence inferred from expert opinion, rather than direct assessments. Foraging distance is often derived from proxies of bee body size, rather than direct measurements of foraging that account for behavioral responses to floral resource type and distribution. The lack of direct measurements of nesting incidence and foraging distances may lead to inaccurate mapping of pollination services. We examined the role of local-scale floral resource presence from hedgerow plantings on nest incidence of ground-nesting bees in field margins and within monoculture, conventionally managed sunflower fields in California's Central Valley. We tracked bee movement into fields using fluorescent powder. We then used these data to simulate the distribution of pollination services within a crop field. Contrary to expert opinion, we found that ground-nesting native bees nested both in fields and edges, though nesting rates declined with distance into field. Further, we detected no effect of field-margin floral enhancements on nesting. We found evidence of an exponential decay rate of bee movement into fields, indicating that foraging predominantly occurred in less than 1% of medium-sized bees' predicted typical foraging range. Although we found native bees nesting within agricultural fields, their restricted foraging movements likely centralize pollination near nest sites. Our data thus predict a heterogeneous distribution of pollination services within sunflower fields, with edges receiving higher coverage than field centers. To generate more accurate maps of services, we advocate directly measuring the autecology of ecosystem service providers, which vary by crop system, pollinator species, and region. Improving estimates of the factors affecting pollinator populations can increase the accuracy of pollination service maps and help clarify the influence of farming practices on wild bees occurring in agricultural landscapes.

Nest suitability, fine-scale population structure and male-mediated dispersal of a solitary ground nesting bee in an urban landscape.

Bees are the primary pollinators of flowering plants in almost all ecosystems. Worldwide declines in bee populations have raised awareness about the importance of their ecological role in maintaining ecosystem functioning. The naturally strong philopatric behavior that some bee species show can be detrimental to population viability through increased probability of inbreeding. Furthermore, bee populations found in human-altered landscapes, such as urban areas, can experience lower levels of gene flow and effective population sizes, increasing potential for inbreeding depression in wild bee populations. In this study, we investigated the fine-scale population structure of the solitary bee Colletes inaequalis in an urbanized landscape. First, we developed a predictive spatial model to detect suitable nesting habitat for this ground nesting bee and to inform our field search for nests. We genotyped 18 microsatellites in 548 female individuals collected from nest aggregations throughout the study area. Genetic relatedness estimates revealed that genetic similarity among individuals was slightly greater within nest aggregations than among randomly chosen individuals. However, genetic structure among nest aggregations was low (Nei’s GST = 0.011). Reconstruction of parental genotypes revealed greater genetic relatedness among females than among males within nest aggregations, suggesting male-mediated dispersal as a potentially important mechanism of population connectivity and inbreeding avoidance. Size of nesting patch was positively correlated with effective population size, but not with other estimators of genetic diversity. We detected a positive trend between geographic distance and genetic differentiation between nest aggregations. Our landscape genetic models suggest that increased urbanization is likely associated with higher levels of inbreeding. Overall, these findings emphasize the importance of density and distribution of suitable nesting patches for enhancing bee population abundance and connectivity in human dominated habitats and highlights the critical contribution of landscape genetic studies for enhanced conservation and management of native pollinators.

Evidence of forage distance limitations for small bees (Hymenoptera: Apidae)

The distribution of ground-nesting bees was investigated using transects of water traps in a mosaic of nesting and forage habitats at Shotover Hill in Oxfordshire, UK. The site includes a large area of ground-nesting bee activity and is adjoined on three sides by floristic hay meadows. This study showed that the females of small bee species (< 1.5 mm intertegular span) that were foraging in the hay meadows demonstrated a functional limitation to their homing range. The abundance of small bees declined rapidly with increasing distance from areas of high density nesting; declining more rapidly than might be expected from uniform dispersal into the surrounding landscape. By modelling the occurrence of bees along each transect it was found that the probability of observing a small bee in the hay meadows was reduced to 10% at a distance of 250-370 m from the nesting habitat. The result emphasises the scale on which habitat fragmentation will begin to impact upon bee diversity, and the relative contribution of managed pollen and nectar strips to areas of nesting habitat.

Nesting Biology and Immature Stages of the Panurgine Bee GeneraRhophitulusandCephalurgus(Apoidea: Andrenidae: Protandrenini)

ABSTRACT Herein is presented nesting information on the communal ground-nesting Argentinian bees Rhophitulus xenopalpus Ramos and R. mimus Ramos, which is compared with what is known concerning the closely related Brazilian bee Cephalurgus anomalus Moure and Lucas de Oliveira. The mature larvae of all three taxa are described, illustrated, and compared with one another and with those of other Protandrenini. While larvae of the three species share many similarities, those of R. xenopalpus and R. mimus, though each distinctive, are quite similar, and those of C. anomalus differ from the others in mandibular features and in dorsal body ornamentation. Male and female pupae of R. xenopalpus are also described.

Influence of windbreaks and forest borders on abundance and species richness of native pollinators in lowbush blueberry fields in Québec, Canada

AbstractLowbush blueberry (Vaccinium angustifoliumAiton (Ericaceae)) production is highly dependent on insect pollination to maximise yields. The current losses in honey bee (Apis melliferaLinnaeus (Hymenoptera: Apidae)) colonies pose a serious threat to the blueberry industry, raising interest in alternative pollinators. Abundance and diversity of native pollinators usually decreases with distance from natural habitats. In this study, we evaluated the effects of distance from wooded habitats such as windbreaks and forest borders on the presence of native pollinators in blueberry fields in Lac-St-Jean (Québec, Canada). Four treatments were compared: single-row, double-row, natural windbreaks, and forest borders. Pan-traps were placed at 5, 30, and 60 m from the windbreak or forest border. A total of 3878 native pollinators were collected and 81% were ground-nesting bees. The forest border was the only treatment with higher abundance and species richness on the periphery (5 m) of the field than at further distances, supporting the hypothesis that the presence of pollinators is favoured by habitats potentially offering more abundant and diverse nutritional resources. Our overall results reveal that native pollinators are distributed quite homogeneously in blueberry fields, suggesting that windbreaks are beneficial to native pollinator communities.

Evaluating nesting microhabitat for ground-nesting bees using emergence traps

Nesting resources structure native bee communities and the availability of suitable nests may enhance population abundance and persistence. Nesting rates of ground-nesting bees have proven challenging to assess due to a lack of standardized methods. We quantified the abundance of ground-nesting native bees using emergence traps over a seven-month study period. We then compared specimens captured in emergence traps with pan- and net-collected specimens. We hypothesized that ground-nesting bees would be highly similar to bees found foraging within our study site. However, the species assemblage of ground-nesting bees collected from emergence traps was significantly dissimilar from the assemblages collected with aerial nets and pan traps, indicating different sampling methods target different components of the species assemblage. We then examined the importance of nesting resources found at each emergence trap on the abundance of ground-nesting bees collected from emergence traps. Quantification of potential nesting resources, such as percent bare soil, has been proposed as a proxy of nesting habitat for ground-nesting guilds. Sloped ground and soil compaction were the most predictive nesting resources at the community-level. Further, spatial distribution of nesting resources within the study landscape also affected nesting rates, although this varied by species. Bees occurred in 85% of emergence traps, with sampling date strongly affecting the number of bees collected. Emergence traps provide a useful method of sampling the ground-nesting native bee community and investigating nesting incidence.

Native plants are the bee’s knees: local and landscape predictors of bee richness and abundance in backyard gardens

Urban gardens may support bees by providing resources in otherwise resource-poor environments. However, it is unclear whether urban, backyard gardens with native plants will support more bees than gardens without native plants. We examined backyard gardens in northwestern Ohio to ask: 1) Does bee diversity, abundance, and community composition differ in backyard gardens with and without native plants? 2) What characteristics of backyard gardens and land cover in the surrounding landscape correlate with changes in the bee community? 3) Do bees in backyard gardens respond more strongly to local or landscape factors? We sampled bees with pan trapping, netting, and direct observation. We examined vegetation characteristics and land cover in 500 m, 1 km, and 2 km buffers surrounding each garden. Abundance of all bees, native bees, and cavity-nesting bees (but not ground-nesting bees) was greater in native plant gardens but only richness of cavity-nesting bees differed in gardens with and without native plants. Bee community composition differed in gardens with and without native plants. Overall, bee richness and abundance were positively correlated with local characteristics of backyard gardens, such as increased floral abundance, taller vegetation, more cover by woody plants, less cover by grass, and larger vegetable gardens. Differences in the amount of forest, open space, and wetlands surrounding gardens influenced abundance of cavity- and ground-nesting bees, but at different spatial scales. Thus, presence of native plants, and local and landscape characteristics might play important roles in maintaining bee diversity within urban areas.

Competition between honey bees and wild bees and the role of nesting resources in a nature reserve

The European honey bee exploits floral resources efficiently and may therefore compete with solitary wild bees. Hence, conservationists and bee keepers are debating about the consequences of beekeeping for the conservation of wild bees in nature reserves. We observed flower-visiting bees on flowers of Calluna vulgaris in sites differing in the distance to the next honey-bee hive and in sites with hives present and absent in the Luneburger Heath, Germany. Additionally, we counted wild bee ground nests in sites that differ in their distance to the next hive and wild bee stem nests and stem-nesting bee species in sites with hives present and absent. We did not observe fewer honey bees or higher wild bee flower visits in sites with different distances to the next hive (up to 1,229 m). However, wild bees visited fewer flowers and honey bee visits increased in sites containing honey-bee hives and in sites containing honey-bee hives we found fewer stem-nesting bee species. The reproductive success, measured as number of nests, was not affected by distance to honey-bee hives or their presence but by availability and characteristics of nesting resources. Our results suggest that beekeeping in the Luneburg Heath can affect the conservation of stem-nesting bee species richness but not the overall reproduction either of stem-nesting or of ground-nesting bees. Future experiments need control sites with larger distances than 500 m to hives. Until more information is available, conservation efforts should forgo to enhance honey bee stocking rates but enhance the availability of nesting resources.

Evaluating bee (Hymenoptera: Apoidea) diversity using Malaise traps in coffee landscapes of Costa Rica

AbstractEven though Arabica coffee (Coffea arabica Linnaeus, Rubiaceae) can self-pollinate, bees are important pollinators, without which there is lower fruit quality and yield. We studied bee diversity in coffee agroecosystems in Costa Rica during two coffee flowering seasons (2005 and 2006). Malaise traps were used as a passive sampling method to collect bees during coffee blooms. We collected 1012 bee individuals from three different site types: nonagricultural fields and shaded and unshaded coffee farms. Unshaded coffee farms had significantly higher species richness (S) and number of bee individuals (n) than did the shaded coffee farms and nonagricultural sites. Overall bee diversity did not differ among site types but evenness (J′) was significantly lower in unshaded coffee farms. Using a more detailed community analysis, there was a significant association between functional groups and habitat type with more species and individuals of small-bodied ground-nesting bees (Lasioglossum (Dialictus) Robertson) associated with unshaded coffee farms. A large proportion (49%) of bees collected were of this subgenus, which was never before reported as common in coffee agroecosystems. Further studies should establish whether Dialictus is important in coffee pollination. We propose strategies involving conservation of native bees through simple habitat management for small-scale coffee farms that may improve crop quality and quantity.

Nesting biology and phenology of a population of Halictus farinosus Smith (Hymenoptera, Halictidae) in northern Utah

Nesting biology and phenology in an aggregation of the primitively eusocial ground-nesting bee Halictus farinosus were studied at Green Canyon, Utah from May to August, 2010. Nest architecture was typical of the genus. Nests were small with an average of 3.5 worker and 13.5 reproductive brood per colony. Most workers were mated (77.5%) and had ovarian development (73.4%). The queen-worker size differential was moderate (8.8% for head width and 6.2% for wing length), indicating that sociality in this species is of intermediate strength compared to other social Halictus species. Results from 2010 were compared with those from 1977/1978 and 2002. Varying weather patterns in the years of study led to changes in phenological milestones: in the colder and wetter spring of 2010, nesting behavior was delayed by up to two weeks compared to the other years. While nest productivity was comparable among years, in 2010 the size difference between queens and workers was significantly larger than in 2002, indicating an effect of annual variation in weather conditions on social parameters in this species.

The oligolecty status of a specialist bee of South American Prosopis (Fabaceae) supported by pollen analysis and floral visitation methods

Despite the nest pollen provisions in Western Argentina are composed only of Prosopis, the fact that the ground-nesting bee Eremapis parvula visits several floral hosts suggested that it is a generalist bee species. In the South American Dry Chaco forest, seven nest aggregations of E. parvula were found during three different spring periods. From 34 to 73 species of floral hosts were recorded around each nest aggregation. However, all nest pollen samples were composed of Prosopis pollen alone, as previously found in nests from Western Argentina. Thus, pollen analysis proved that E. parvula is a specialist bee of Prosopis. The “monolecty” and “narrow oligolecty” pollen specialization categories cannot be differentiated using pollen analysis alone. For this reason, a complementary floral visitation method was used. As several Prosopis species have been reported in floral records, the narrow oligolecty category for E. parvula is supported here. Considering that this exomalopsine is a multivoltine bee, and that flowers of some of the more than seven Prosopis species are always available during spring, synchronization between them in rainy periods is highly probable. Thus, it is unlikely that E. parvula has to forage on alternative pollen hosts.

A new phoretic mite species with remarks to the phenomenon “Sporothecae” (Acari, Scutacaridae; Hymenoptera, Aculeata)

We provide the first description of the mite species Imparipes (Imparipes) burgeri n. sp. (Scutacaridae, Heterostigmatina). The species is recorded from localities in Austria, Belgium, Germany, Poland and Slovakia. A total of 759 females have been found phoretic upon 45 host species belonging to ground-nesting or parasitc on ground-nesting hosts apoid bees as well as upon mutillid and pompilid wasps, whereas the latter two groups have not yet been reported as phoretic hosts of scutacarid mites. In contrast to the bee- and wasp associated species Imparipes haeseleri Ebermann & Hall, 2003, I. breganti Ebermann & Hall, 2004 and I. apicola Banks, 1914, I. burgeri has – like the majority of Scutacaridae – no sporotheca. Rearing experiments with I. burgeri carried out on fungal species belonging to the genera Fusarium, Mortierella and some other still unidentified fungi revealed that I. burgeri is a distinct food opportunist. Whereas rearing of I. burgeri was successful, the breeding of the sporotheca possessing Imparipes species failed, presumably due to their high food specificity. These results support our hypothesis that the development of a distinct food specificity in some of the bee associated Imparipes could have led to the evolution of a targeted spore transfer by means of a sporotheca.

Miner Bee, Chimney Bee Anthophora abrupta Say

These gregarious, yet solitary, ground-nesting bees are “…conspicuous as they noisily swing their ponderous bodies to and fro on the wing, arrive home and scramble into their burrows or come tumbling out headlong and dash off into the sunny fields, with all the exuberance of boys just out of school.” This 5-page fact sheet was written by Jason R. Graham, Jamie Ellis, Glenn Hall, and Catherine Zettel Nalen, and published by the UF Department of Entomology and Nematology, December 2011. EENY-512/IN912: Miner Bee, Chimney Bee Anthophora abrupta Say (ufl.edu)

Predicted fates of ground-nesting bees in soil heated by wildfire: Thermal tolerances of life stages and a survey of nesting depths

Periodic wildfire defines plant community composition and dynamics in many of the world’s semi-arid biomes, whose climates and floras also favor wild bee diversity. Invasive flammable grasses, deforestation, historical fire suppression and human ignition are increasing fire frequency and intensifying its severity, as well as introducing fire to previously fireproof biomes. In many of these habitats, bees are key pollinators. Many, often most of the solitary bee species and individuals in these biomes nest underground (so-called “mining” bees). To evaluate their susceptibility to fire, we tested heat tolerances of bees’ four life stages using an experimental design that mimicked heat conduction dynamics of natural soils. All life stages survived heating of up to 45 °C for 27 min, but none survived heating at 54 °C for 9 min; the pupal stage survived best. At near-lethal temperatures, more prolonged heating caused more mortality. These data were related to published studies of heat penetration depths in soil during fire and an exhaustive compilation of published nesting depths reported for mining bees. We conclude that a small fraction (9%) of the shallowest-nesting mining bee species is likely to die from soil heating by wildfire. Among these, ground-nesting megachilids ( Osmia, Megachile) will be most vulnerable, owing to their shallow horizontal nests. Because mining bees prevail in most biomes of the temperate zone, any vegetation rehabilitation efforts should therefore expect that bee communities will largely survive the immediate effects of wildfire, and therefore will need pollen and nectar resources in the year(s) after fire.

Socially peaceful: foragers of the eusocial bee Lasioglossum malachurum are not aggressive against non-nestmates in circle-tube arenas

Due to the universally found nestmate recognition in eusocial insects, it is predictable that non-nestmates interact aggressively. In sweat bees (Hymenoptera: Halictidae), this trend was largely shown for queen–queen interactions, but data on worker–worker interactions are still scarce and somehow controversial. We studied behavioural interactions between foragers of the eusocial and ground-nesting bee Lasioglossum malachurum within circle-tubes. Independently of colony membership, bees exhibited high frequencies of cooperative behaviours, together with lack of aggression and moderate avoidance of social interactions. The cooperative mutual passing was the most frequently recorded behaviour. Size difference between the opponents had no effects on cooperation or avoidance. In a heterospecific experiment, bee foragers were observed to react more aggressively and to pass very rarely towards cuckoo bees, suggesting that our results were not biased by the circle-tube methodology. Our results and comparisons with other bee species suggest that studying worker interactions may be not enough to predict the social organisation in bees. Whatever the evolutionary meaning of this generalised tolerance towards conspecifics, the present findings are somehow in agreement with recent studies showing that L. malachurum colonies may have imperfect nestmate recognition and often include a mixture of related and unrelated workers.