Effects of Cultivation and Proximity to Natural Habitat on Ground-Nesting Native Bees in California Sunﬂower Fields

Home , Eucerini, Melissodes agilis, Xeromelecta californica

JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY 79(4), 2006, pp. 309–320 Effects of Cultivation and Proximity to Natural Habitat on Ground-nesting Native Bees in California Sunﬂower Fields

1 2 3 JOHN KIM, NEAL WILLIAMS, AND CLAIRE KREMEN

ABSTRACT: Agricultural conversion is one of the most prevalent anthropogenic uses on the terrestrial earth. Persistence of organisms in such landscapes is thought to be related to species- specific characteristics such as life history traits and dispersal distance. In an agricultural landscape in California, we examined local (farm-level) and landscape variables associated with nesting preferences of native ground-nesting bees. Compared to the known ground-nesting visitors to crops, bee community nesting on farms was depauperate. Further, more abundant and diverse communities of bees were found nesting at farms with patches of natural habitat near by than farms that were far away from natural habitat. Species responded differently to soil conditions created by farming practices, but the variability in nesting bee abundance was lower in farms near natural habitat than farms far from natural habitat. These findings suggest that most bee species are affected adversely but to varying degrees by agricultural intensification, and that natural habitats may buffer against the bee population variability in agricultural landscape. We present source/sink dynamics and resource limitations as possible explanations for the observed patterns. KEY WORDS: Ground-nesting bees, sunflower, nesting density, source-sink dynamics, agriculture, biodiversity, pollination

Humans have appropriated an estimated 40% of the terrestrial surface for agriculture, greatly modifying the environment and ecosystem processes (Olson et al., 1983; Vitousek et al., 1997; Chapin et al., 2000; DeFries et al., 2004). Consequent loss of habitat and fragmentation are often cited as the greatest threats to biodiversity (Saunders et al., 1991; Wilcove et al., 1996), along with climate change and invasive species (Lodge, 1993; Sala et al., 2000). However, agricultural areas may also act as refuges (Becker et al., 1991; Ricketts et al., 2001; Soto-Pinto et al., 2001) and maintain biodiversity for some taxa (Mander et al., 1999; Noy and Kaplan, 2002; Luck and Daily, 2003). Response to agricultural conversion is thought to be highly species-specific and dependent on life history traits, vagility, and habitat specialization of the organisms (Tucker, 1997; Cane, 2001; Tworek, 2002). Bees represent a group of diverse and understudied organisms whose persistence in the agricultural landscape is poorly understood. In seasonally dry ecosystems, such as the Central Valley in northern California, irrigated agricultural areas may benefit bees by providing more floral resources at certain times of the year than natural habitat has historically offered (Banaszak, 1992; Corbet, 2000). Floral resources are inherently patchy in natural landscapes, and bees may have evolved to find patches of suitable habitats in a matrix of unsuitable areas (Kremen and Ricketts, 2000; Cane, 2001). However, agricultural intensification may deprive bees of other necessary resources, such as appropriate nest sites and nest construction materials. For example, ground-nesting bees may suffer from cultivation practices if tilling alters their preferred nesting conditions or destroys nests during larval development.

1 Nicholas School of the Environment and Earth Sciences, P.O. Box 90328, Duke University, Durham, North Carolina 27708. 2 Bryn Mawr College, Department of Biology, 101 N. Merion Ave. Bryn Mawr, Pennsylvania 19010-2899. 3 University of California, Dept. of Environmental Science, Policy and Management, 137 Mulford Hall #3114, Berkeley, California 94720. Accepted 20 September 2005; Revised 20 June 2006 Ó 2006 Kansas Entomological Society 310 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

Bees exhibit a wide range of nesting requirements. Some species have highly specific preferences for substrate (soil, twig, leaf, etc.), moisture, hardness, and amount of vegetation cover (Potts and Willmer, 1997; Wuellner, 1999) and spend considerable time assessing edaphic conditions at different locations before initiating nests (Brockmann, 1979; Westrich, 1996). Nesting habitats may be limiting for such species partly because sites satisfying all their requirements are relatively rare (Evans, 1966; Michener, 1969; Potts and Willmer, 1998; Wuellner, 1999). Other species have more generalized nesting preferences, and soil and vegetation conditions do not explain the distribution of their nests (Michener et al., 1958; Wcislo, 1984; Mader, 1980). Such diversity among bee nesting requirements implies that those with broader requirements may find farms to be as suitable for nesting as undisturbed areas, while other species suffer from widespread loss of nesting habitats upon agricultural conversion. Bees are of special concern for biodiversity conservation because they are important contributors to agricultural production (McGregor, 1976; Parker et al., 1987; Southwick and Southwick, 1992; Morse and Calderone, 2000). Honeybees, Apis mellifera, form a cornerstone of agricultural pollination. Recent declines in the number of managed honeybee colonies (Watanabe, 1994; Ingram et al., 1996), coupled with a growing recognition that naturally occurring native bees also are important contributors to crop pollination (Kremen et al., 2002a; Klein et al., 2003; Ricketts, 2004; Ricketts et al., 2004), suggest that it is important to understand not only how agricultural landscapes benefit from wild bees but also to what extent they support wild bee populations. Recent studies in an agricultural landscape in California have documented declines in abundance and diversity of native bees with increasing agricultural intensification (Kremen et al., 2002a, b; Kremen et al., 2004; Larsen et al., 2005; Greenleaf, 2005). Some species were relatively insensitive to the amount of natural habitat near the farm, but many were absent on farms with less natural habitat nearby (Kremen, 2004; Greenleaf, 2005). One possible mechanism contributing to this pattern is loss of nesting habitat on farms. Data on nesting patterns within such areas are absent, and the literature on species-specific nesting requirements of these native species is woefully incomplete, although basic nesting guilds of bees are well known. If tilled grounds at farms are unsuitable nesting habitat for ground- nesting bees, nesting sites may be limited in predominantly agricultural landscapes. In such cases, neighboring natural habitat may act as nesting resources for native bees on farms, and farms adjacent to patches of natural habitat could support higher population densities due to surplus bees dispersing from local natural habitat. Some species, however, may persist at low densities on farms if they can accept surrogate nesting habitats such as fallow field borders. Assessing the quality of farms as nesting habitats in a landscape context can reveal how farms and adjacent lands should be managed to maintain a high diversity and density of native bees. We assessed the effect of habitat conversion on bee nesting densities at farm and landscape scales in the same landscape in California studied by Kremen et al. (2002a, 2004). We determined which species of ground-nesting native bees nest on farms, whether proximity to natural habitats affects their nesting densities, and what soil conditions they prefer for nesting.

Materials and Methods Site Description We studied bee nesting densities at 10 conventional sunﬂower farms located in the Capay Valley in the Central Valley of California (35840–539N 122815–509W). Sunﬂowers VOLUME 79, ISSUE 4 311

(Helianthus annuus L. (Asteraceae)) are native to the area and cultivated forms attract more than 30 species of native bees (Kremen et al., 2002b; Greenleaf, 2005). Farms were classified by their proximity to natural or semi-natural chaparral, mixed oak, woodland, and riparian habitats. ‘‘Near’’ farms included .25% of such natural habitat within a 2 km radius of the farms and ‘‘Far’’ farms had ,2% of natural habitat within a 2 km radius. The designations were based on a previous study showing that bee communities responded to spatial scales between 1.2 km and 2.4 km (Kremen et al., 2004). The proportion of natural habitat surrounding each farm (henceforth proximity gradient) was calculated using Arcview GIS, 3.3 by ESRI. Farmers in this region till sunflower fields to 0.3 meter and apply herbicide a few days before the seeds are planted. In a given season, about 1/3 of the field sites are sprayed for the main insect pest, sunflower head-moth, Homoeosoma electellum Hulst (Lepidoptera: Pyralidae) (Carl Hjerpe, Eureka Seeds, pers. comm.). Planting dates vary from farm to farm. Fields are flood irrigated three to four times during the four to five months growing season. Field borders, usually next to dirt roads or irrigation ditches, are left weedy and untilled. Farms were sampled in a random order between July and August of 2003. In our system, number of days between planting and sampling dates and pesticide application did not differ significantly between ‘‘Near’’ and ‘‘Far’’ farm types (number of days between planting and sampling dates: d.f. 5, t-statistics 0.54, P . 0.61; pesticide application: v2 0.62, P . 0.42). All farms had blossoming at the time of the sampling. The surveyed farms were under contract by two different seed companies, but standard method of cultivation was used for all farms (Carl Hjerpe, Eureka Seeds, pers. comm.).

Nesting Density Assessment Number of bees nesting at a given area in a farm was assessed by covering patches of ground with standard sized pieces (6 m 3 1.8 m) of semi-transparent and breathable rowcover fabric (Floating rowcover by Argyl P17) at night after bees had returned to their nests and collecting all bees trapped beneath the cover in the morning. The edges of row cover were sealed to the ground by bags filled with gravel placed along their entire length, and two 60 cm high metal hoops propped up the covers. Preliminary sampling showed that the method trapped bees on bare and vegetated soil, between and over the cultivated rows, as well as sloped banks and irrigation ditches (Williams, unpubl. data; Kim, unpubl. data). It is possible that some species/individuals of ground-nesting bees are unlikely to emerge with the cover in place. Each trap was checked twice to ensure thorough sampling. If the bees are to be collected, we recommend placing collection traps such as pan traps (Kirk, 1984) with the rowcovers. At each farm, we randomly placed seven rowcovers along field borders for one night each. In addition, we sampled the field interior at four of the farms, using seven randomly placed rowcovers at each farm. All farms were flowering at the time of the sampling. All bees were identified to species except for Lasioglossum (Dialictus) spp., which were classified to morphospecies. Lasioglossum (Dialictus) females and males were given separate morphospecies designations because it was difficult to make female-male pairings in this group. Specimens are stored at the Bohart Museum of Entomology, University of California, Davis. Under each rowcover, we also assessed soil hardness and vegetation cover, thought to be important determinants of nesting densities for some species (Evans, 1966; Michener, 1969; Wuellner, 1999). Soil hardness was measured in the field with the Pocket Penetrometer from Forestry Suppliers, Inc. and classified into three categories: soft (0–1.5 kg/cm2), medium 312 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

(1.6–3.0 kg/cm2) or Hard (3.1–4.5 kg/cm2), and the vegetation cover was quantiﬁed by taking digital photographs of the ground under the rowcovers and estimating the green area in the pictures with overlaid grids using Adobe PhotoshopTM, v. 7.0.1. The vegetation cover was categorized as sparse (0–33%), medium (34–66%), and dense (67–100%).

Analysis of Bee Diversity and Density We calculated two diversity estimators, ICE (incidence-based coverage estimator) and Jackknife 2 (incidence-based Jackknife estimator) for bee species at each farm using EstimateS, v. 5.0.1 (Colwell, 2005). ICE is robust to small sample size and to moderate patchiness, and Jackknife is one of the least biased estimators for small sample size and the best for highly patchy distributions (Chazdon et al., 1998). These estimators were thus the most appropriate for use with our data. We used only female bee densities for analyses because females trapped under rowcover placed the previous evening are highly likely to have emerged from a nest, whereas males could be roosting in the vegetation. Females provision the nests as central place foragers while males disperse from natal nests in search of mates and are more likely to be transients (O’Toole and Raw, 1991). Given small sample sizes for individual bee species, we examined the environmental factors associated with densities of nesting bees at the community level. Nesting bee densities, observed species richness, and diversity estimators based on samples from ﬁeld borders were tested for difference between ‘‘Near’’ and ‘‘Far’’ farm types with parametric t-tests. We tested difference in aggregate densities between border and interior habitat categories using a paired t-test. We used the Kruskal-Wallis tests to look for differences in vegetation cover and soil hardness between farms and to assess preferences of different bee species for these characteristics.

Results Effect of the Landscape (Surrounding Natural Habitat) on Bee Diversity and Density We captured a total of 252 female specimens from six (eight including the males) ground-nesting bee species (Appendix I), out of the 15 ground-nesting bee species/groups that are known to visit sunflowers in the area (Greenleaf, 2005). Observed species richness was significantly higher on ‘‘Near’’ farms than on ‘‘Far’’ farms (‘‘Far’’ mean 6 SE: 2.33 6 0.29, ‘‘Near’’ 3.75 6 0.36, d.f. ¼ 8, t ¼3.072, P ¼ 0.015). Similarly, ICE and Jackknife 2 estimated significantly higher diversity on ‘‘Near’’ farms (ICE; ‘‘Far’’ 2.68 6 0.49, ‘‘Near’’ 5.41 6 0.59, d.f. ¼ 8, t ¼3.56, P ¼ 0.007, Jackknife 2; ‘‘Far’’ 2.72 6 0.62, ‘‘Near’’ 5.81 6 0.75, d.f. ¼ 8, t ¼3.17, P ¼ 0.013). Species richness at ‘‘Far’’ farms leveled off with increasing sampling effort, whereas species richness at ‘‘Near’’ farms continued to increase, indicating that ‘‘Near’’ farms were undersampled (Fig. 1). The pooled nesting densities across species at field borders were significantly higher at ‘‘Near’’ farms than at ‘‘Far’’ farms (Fig. 2, ‘‘Far’’ mean: 0.22, SE: 0.04, ‘‘Near’’ mean: 0.41, SE: 0.05, d.f. ¼ 8, t-test: 3.06, P ¼ 0.017). Moreover, the coefficient of variation among densities on ‘‘Near’’ farms was less than a quarter that of ‘‘Far’’ farms (CV: ‘‘Near’’ ¼ 0.120; ‘‘Far’’ ¼ 0.532).

Effect of the Site (Farm) Factors on Density Within farms, nesting densities were higher at ﬁeld borders than at ﬁeld interiors (Fig. 3; interior mean: 0.089 6 0.055, border mean: 0.31 6 0.075, d.f. ¼ 3, Paired t-test: 4.771, VOLUME 79, ISSUE 4 313

Fig. 1. Observed and estimated species richness, ICE (incidence-based coverage estimator), for different farm categories against sample effort. Sampling effort is measured as the number of rowcovers utilized, pooled across sites within the ‘‘Near’’ or ‘‘Far’’ farm categories. Error bars show the standard deviations of the randomized av- erages of estimated species richness for each level of sampling effort. All three richness indices (Jackknife 2 not shown) were signiﬁcantly higher at ‘‘Near’’ farms than at ‘‘Far’’ farms.

P , 0.02). Soil hardness at borders varied widely, but field interiors always had very soft soil (soil hardness; interior mean: 0.1, interior SE: 0.19, border mean: 1.77, border SE: 0.29). At field borders, nesting densities also differed with soil hardness but not with vegetation cover (Kruskal-Wallis; soil hardness, n ¼ 63, k ¼ 3, H ¼ 7.8, P , 0.012; vegetation cover, n ¼ 63, k ¼ 3, H ¼ 0.67, P ¼ 0.71). We looked for soil hardness preferences of the three most common species by comparing their density at different soil hardness from the border samples (Fig. 4). Halictus tripartitus showed a tendency to nest in the firmest soil (Spearman’s Rho; 0.2885, P , 0.022), whereas H. ligatus nested in highest densities in medium soil hardness (Spearman’s Rho; 0.2975, P , 0.018). There was no measurable difference in densities of Lasioglossum (Dialictus) sp. A, the most common species in our sample, between the soil hardness classes (Spearman’s Rho; 0.13, P , 0.31). None of the species showed preference for specific vegetation cover (Spear- man’s Rho; L. (Dialictus) sp. A, P , 0.14, H. tripartitus, P , 0.76, H. ligatus, P , 0.39).

Discussion The landscape in which ‘‘Far’’ farms were located has experienced extensive conversion of natural habitat to agricultural lands. Low bee nesting densities at these sites 314 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

Fig. 2. Comparison of bee densities among farm categories. Histograms represent mean density with standard error, aggregated across species. may have resulted from a combination of factors including changes in the availability of nesting substrates, reliance of bees on floral resources found in natural habitats, and direct mortality on farm sites through soil disturbance and pesticides. Because the two factors vary across the landscape, it is difficult to disentangle whether the nesting or floral resources or both limit the distribution of bee species. Lower densities of ground nesting bees at ‘‘Far’’ farms, compared to ‘‘Near’’ farms, suggests that densities on farms are partially driven by the composition of the landscape surrounding the farm, suggesting a modified type of source-sink dynamics (Pulliam, 1988). The numbers of bees nesting on the farm sites could be enhanced by, but not necessarily depend on, an influx of bees originating from remnants of natural habitat that establish nests on farm sites. Potential mechanisms are discussed below. For example, Lasioglossum sp. and Halictus ligatus were present even at the most heavily disturbed sites, though their densities at ‘‘Far’’ farms were more than a third less

Fig. 3. Histograms represent mean bee densities at ﬁeld borders and ﬁeld interiors on 4 farms with standard errors are shown. VOLUME 79, ISSUE 4 315

Fig. 4. Bee densities partitioned by soil hardness for three common bee species. Histograms represent the interquartile range of the 3 most common species of bees in each soil hardness category from ﬁeld borders are plotted. The line within each bar represents the median, and the error bars represent 1.5 times the midspread. The dots represent outliers. The rowcovers are divided by three soil hardness classes: soft, medium, and hard. The numbers on top of the bars represent number of covers in each soil hardness class. Specimens from these three species accounted for more than 95% of the sample.

than their densities at ‘‘Near’’ farms. We infer that these species are not dependent on emigration from natural habitat for persistence, but that their populations nearer to the natural habitat may be enhanced by dispersal from the natural habitat, resulting in higher densities at ‘‘Near’’ farms. However, some species of Lasioglossum (Dialictus) and Melissodes were only found in ‘‘Near’’ farms, indicating that classic source/sink dynamics may be at work; they cannot persist on farms without frequent inﬂux from natural habitat. For the species that were ubiquitous in both ‘‘Far’’ and ‘‘Near’’ farms, ﬁeld borders may act as stepping-stones, allowing the species to be well distributed across the disturbed landscape. Social or primitively eusocial species such as the two halictid species would be expected to be present more consistently across the season than solitary species such as Melissodes sp. due to their sociality (Chapman and Bourke, 2001). Short sampling period may fail to capture the temporal complexities of the population dynamics of the solitary, shorter-lived species and thus bias the abundance estimates in favor of the social species, though the most abundant nester in the sample were solitary Lasioglossum sp., which indi- cates there are other mechanisms driving the bee distribution across the patchy landscape. Although direct measures of dispersal remain limited for many bee species, studies report short distance movements in mere meters for Lasioglossum (Dialictus) (Kukuk and Decelles, 1986) and more extensive dispersal of three to hundreds of km for other species (Minckley and Reyes, 1996; Viscens and Bosch, 2000). If bees in natural habitat are limited by resources such as nest sites, as has been inferred for a number of species (Potts and Willmer, 1997; Wuellner, 1999), they may indeed disperse into surrounding marginal habitats (Pulliam, 1988).

Floral Resources Reduced nesting densities on ‘‘Far’’ farms may also have resulted from differential floral resource availability at these sites. Offspring number and population densities depend on 316 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY the availability of pollen throughout the flight season during the previous year. Although all of the species in our study utilize sunflower, natural habitats provide complementary floral resources for the bees nesting at farms during times when sunflowers are not flowering (Kremen et al., 2002b). Sunflower fields bloom for one to two weeks compared to the 8 to 21 week range of bee flight seasons. At ‘‘Near’’ farms, bees may be able to switch to native plants or weeds after the crop finishes blooming whereas bees at ‘‘Far’’ farms have only a short window of opportunity to provision their nests with pollen from the crop. In our study system, ‘‘Near’’ farms were consistently adjacent to wild weedy habitats while the ‘‘Far’’ farms had variable floral resource outside the farms (Kremen et al., 2002b). The lower variability of nesting densities at ‘‘Near’’ farms compared to the ‘‘Far’’ farms can be explained by the potential immigration and more consistent availability of floral resources from natural areas.

Onsite Disturbance In addition to landscape level factors, bee densities on the farm may be affected by onsite disturbance. Pesticide (Parker et al., 1987; Kearns et al., 1998) and flood irrigation may cause high mortalities and nest abandonment rates at field interiors. Flooding drowns the larvae, and excessive soil moisture makes broods more susceptible to fungal attacks (Packer and Knerer, 1986). Plowing is another periodic disturbance that may prevent farm populations from building up, and cause long term depressed population densities at ‘‘Far’’ farms isolated from source areas such as natural habitats or fallows. Comparison of the densities at borders and interiors of the fields hints at such small-scale effect on densities for two of three species examined. Nest densities in irrigated and plowed field interiors, were consistently lower than in corresponding border area; providing firm soil on farms could encourage establishment of larger populations for other species that apparently nest successfully in firmer soils; left uncultivated, these areas will also provide alternate floral resources. Although bees have been known to choose nesting sites based on other factors such as soil moisture, substrate, aspect, slope, and light (Potts and Willmer, 1997; Wuellner, 1999), only soil hardness and vegetation cover were measured in this study. Bee species nesting on farms were depauperate compared to the known diversity of ground-nesting sunflower visitors in this region (Greenleaf et al., submitted), which suggests general degradation of bee habitat with agricultural conversion. The sample size may not have been sufficient enough to detect rare species or the missing species may be more sensitive to other nesting factors that are potentially altered by farming (Minckley et al., 2000).

Conclusion Pollination is an important and endangered ecosystem service (Allen-Wardell et al., 1998; Kearns et al., 1998); higher densities and diversities of bees can contribute to better pollination of the crops (Kremen et al., 2002a). Yet the effect of habitat conversion and fragmentation on nesting resources of one of the most important and diverse pollinator groups is poorly understood. Results from our study indicate that bee densities on farms respond to natural habitat in the landscape and to local edaphic characteristics at smaller (within field) spatial scales. Moreover, species differed in their responses to the variables tested. Not all sunflower visitors were found nesting in the farms. Of those that did, some species nested indiscriminately at field borders and interiors, while others nested in higher densities at field borders, presumably because agricultural conversion degraded the quality of the field as their nesting habitat. These differences suggest that VOLUME 79, ISSUE 4 317

numerous optimal nesting habitats spaced evenly across the landscape would serve dispersal of more species than a few large reserves could. Nesting resources may be limited from tilling practices, because two of the three most abundant species do not nest in loose plowed soil; if nesting sites become scarce, increasing border areas or fallow ﬁelds may facilitate dispersal across the landscape and encourage sizable nesting populations on farms. The rare or missing species likely are affected also by soil and other factors; research on biology of these species is important in determining whether these species can recover without costly changes to current practices.

Acknowledgments We would like to thank Dr. Robert Colvin and Mrs. Gay Colvin, the Princeton Environmental Institute, and the Princeton EEB department for their generosity in funding this research. Nikki Nicola and Robbin W. Thorp of UC Davis identiﬁed the bee specimens. We thank two anonymous reviewers for their comments and suggestions.

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Appendix I. Comparison of nesting and sunﬂower visitation abundances by species.

Abundance Observed nesting Family Species Nesting style on ﬂowers abundance on farms Apidae Anthophora urbana Cresson* Groundi Rare None Apis mellifera L. Tree cavityii Common None Bombus californicus Smith Rodent burrow Rare None Bombus crotchii Cresson Rodent burrow Rare None Bombus melanopygus Nylander Rodent burrowiii Rare None Bombus pennsylvanicus sonorous Say Rodent burrowiii Rare None Bombus vosnesenskii Radoszkowski Rodent burrowiv Common None Ceratina dallatoreana Twigii Very rare None Ceratina timberlakei Daly Twigii Very rare None Diadasia bituberculata Cresson* Groundii Common None Diadasia enavata* Cresson Groundii Common None Triepeolus spp. ? Parasite on Rare Males only Eucerini, Melissodes, Peponapis, Svastraii Melissodes agilis Cresson* Ground Common Rare Melissodes lupine Cresson* Groundii Common Males only Melissodes robustior Cockerell* Groundii Common None Melissodes stearnsi Cockerell* Ground Common Rare Peponapis pruinosa Say* Groundv Very rare None Svastra obliqua expurgata Say* Groundvi Common Rare Xeromelecta californica Cresson Parasite on Very rare None Anthophorai Xylocopa tabaniformis orpifex Smith Woodii Very rare None Halictidae Agapostemon texanus* Crawford Groundii Rare None Lasioglossum (Dialictus) spp.* Twig/groundii Common Common Lasioglossum (Evylaeus) spp.* Groundvii Rare None Halictus farinosus Say* Groundviii Very rare None Halictus ligatus Smith* Groundix Common Common Halictus tripartitus Cockerell* Groundix Common Common Megachilidae Megachile apicalis Spinola Twigix Rare None Megachile ﬁdelis Cresson ? Rare None Megachile parallela Smith ? Rare None Osmia atrocyanea ? Very rare None Osmia californica Cresson Wood Very rare None Osmia texana ? Very rare None

The table shows the comparison of nesting abundance and visitation abundance of species on sunflower farms in the region. Visitation abundance was measured by counting bees on set transects through the fields (Greenleaf, submitted). The abundance on flowers data is divided into three categories: common (mean of at least 0.1 visits during a 20 m transect), rare (at least 0.01 visits during a transect), and very rare (at least 0.001 visits during a transect). Where species-specific abundance data was unclear, we consulted an expert (Greenleaf, pers. comm.). The nesting abundance (overall counts from all the rowcovers) is divided into common (.50), rare (.25), and none (0). * denotes the 15 species that are expected to be found with rowcover sampling technique given their nesting biology. None of the species utilizing wood, twigs, tree cavities, or rodent burrows were expected to be found with rowcover sampling technique. Species of Bombus are thought to nest in rodent burrows in undisturbed areas and hence were excluded from the set. Nesting styles without references were bees observed to be ground- nesting in this study. Most ground-nesting species visiting sunflowers in large numbers were also found nesting in the field or along field borders. i Torchio and Trostle, 1986. ii Michener, 2000. iii Thorp, pers. comm. iv Heinrich, 1979. v Hurd et al., 1974. vi Rozen, 1964. vii Packer, 1991. viii Eickwort, 1985. ix Barthell et al., 1998.