Breeding Biologies, Seed Production and Species-Rich Bee Guilds of Cleome Lutea and Cleome Serrulata (Cleomaceae)

Plant Species Biology (2008) 23, 152–158 doi: 10.1111/j.1442-1984.2008.00224.x

Breeding biologies, seed production and species-rich bee guilds of Cleome lutea and Cleome serrulata (Cleomaceae)

JAMES H. CANE US Department of Agriculture–Agricultural Research Service, Bee Biology and Systematics Laboratory, Utah State University, Logan 84322–5310, United States of America

Abstract

The summer-blooming annual forbs Cleome lutea and Cleome serrulata (Cleomaceae) are native across the US Intermountain West and Rocky Mountains, respectively. Their farmed seed is sought to help rehabilitate western rangelands in those regions. This study of the reproductive biologies and pollinator faunas of C. lutea and C. serrulata is the first for this cosmopolitan family, the sister family to the Brassicaceae. Unlike the S-allele self-incompatibility systems of some Brassicaceae, both species of Cleome were found to be self-fertile and capable of some autogamy. Compared with selfing, outcrossing did not enhance seed set, seed viability or seedling vigor for either species (in fact, selfed progeny were more robust). Large, openly visited plants yielded >20 000 seeds each. Like several species of the sister family Capparaceae, flowers of both species first shed their pollen, secreted nectar and became receptive nocturnally. Although no nocturnal visitors were found, both Cleome species attracted a diverse array of diurnal native bees, wasps and butterflies. Among the many floral generalist bees that work Cleome flowers for pollen and nectar are two managed agricultural pollinators, Apis mellifera and Megachile rotun- data. These observations bode well for pollinating C. lutea and C. serrulata in small commercial seed fields. It appears that diverse wild bees would benefit from the addition of native Cleome to restoration seed mixes, with the objective of sustaining native pollinator faunas during the first few years of postfire plant community rehabilitation. Keywords: Apiformes, Brassicaceae, Capparaceae, pollination, seedling fitness, self-compatibility. Received 3 January 2008; accepted 24 July 2008

Introduction the evolution of self-incompatibility systems in the Bras- sicaceae, and is certainly needed to successfully farm The small cosmopolitan eudicot family Cleomaceae (300 Cleome seed for large-scale rangeland restoration projects. species) is the sister family to the more diverse Brassi- Native species of Cleome might have a unique role to caceae; it also shares characters with the Capparaceae play in plant community restoration in xeric valleys and (= Capparidaceae), with which it has been formerly clas- plains of the US Intermountain West. Rehabilitating sified (Hall et al. 2002). Dominating the family Cleomaceae western USA rangeland plant communities has long are the 180–200 species of the type genus Cleome (called included reseeding, but primarily with grasses and ‘spider-flowers’ or ‘bee-plants’) that occur in many shrubs. Seed of several native forbs are now being grown warmer regions of the world (Iltis 1957; Sanchez-Acebo commercially for this purpose, with more to follow (Cane 2005). Some are annual forbs common in disturbed habi- 2008), but these are all herbaceous perennials that typi- tats; others are woody, but short-lived. Knowledge of the cally do not flower in the year after seeding. In contrast, breeding biologies of Cleome species might be relevant to Cleome are annuals that can provide bloom quickly and, if used by a diverse array of wild bees, might help sustain Correspondence: James H. Cane pollinator communities the year after an autumn restora- Email: [email protected] tion seeding. Larger quantities of affordable seed from

Journal compilation © 2008 The Society for the Study of Species Biology No claim to original US government works POLLINATION NEEDS OF CLEOME 153 native Cleome species, if available from seed farmers, could be added to seed mixes that are used to rehabilitate vast burned rangelands of the Great Basin and neighboring biomes of western USA (Cane 2008). Farming seed crops generally requires pollinator supplementation to realize potential seed yields (Free 1993), but how much can depend on a plant species’ breeding biology. The Brassicaceae, sister group to the Cleomaceae, has a distinctive sporophytic incompatibility (SI) system (Charlesworth et al. 2005) and only pollen flow between plants sets seed. However, species of Cleome are early successional species at disturbed sites; such attributes in other species are often associated with self- fertility and autogamy (Baker & Stebbins 1965). Thus, ecological versus phylogenetic inferences give contrasting predictions for the pollination needs of Cleome. Fig. 1 Flower, fruits and seeds of Cleome lutea. Shown are the To evaluate the pollination needs of a plant, the breed- pistil atop its gynophore and the dehiscing anthers of this hermaphroditic flower, an immature and mature fruit (silique), and ing biology of the plant must be understood. The objec- its dehiscent valves removed to reveal the loop-like replum and tives of the present study were to characterize the floral the content of mature dark seeds. Inset: X-ray positive of C. lutea and breeding biologies of two of the six species in Cleome seeds showing viable (X-ray dense) and non-viable (gray) section Peritoma (Iltis 1957), Cleome lutea (yellow or embryos. Nevada bee-plant) and Cleome serrulata (Rocky Mountain bee-plant). The necessity or benefit of pollinators and cross-pollination was evaluated for producing fruits, magenta for C. serrulata). Hermaphroditic flowers have six fertile seeds and vigorous progeny. Flowering phenology stamens and a large pistil atop a stalked gynophore and the timing of stigma receptivity and anther dehis- (Fig. 1). Staminate flowers have rudimentary pistils that cence were characterized. Data from museum specimens never set pods (Stout 1923). However, Cleome are not and limited field collections of flower visitors to these andromonoecious. A staminate flower begins as a her- plants were also compiled to document pollinator species maphroditic bud; its pistil thereafter fails to develop fully. richness and the attributes of the pollinator guilds. When a raceme is shunting resources to many maturing fruits, most of its flowers become staminate. Over the long Materials and methods flowering season, racemes alternate between the production of staminate and hermaphroditic flowers (Murneek Traits of Cleome lutea and Cleome serrulata 1937); thus, maturing siliques and shedding seed while Both species are robust, tap-rooted annuals native to the continuing to bloom. xeric valleys and plains of western North America. They Daily blooming phenologies were observed on plants are typically found at disturbed sites, such as waste grown in two common gardens in Logan, Utah, USA ′ ′ places, margins of washes or barren sandy desert plains (41°45 N, 111°48 W). To judge stigma receptivity, excised (Iltis 1957). Owing to its beauty, C. serrulata has been cul- pistils were individually inserted into a Pasteur pipette tip tivated in gardens in and beyond its native range in filled with hydrogen peroxide (J. Thomson, pers. comm., western USA. Plants of both species are erect (3–25 dm 1999). Receptivity was indicated by the visible generation tall), glabrous and malodorous. They invariably produce of oxygen bubbles on the bare stigma, the result of per- one or more compact, bracteolate terminal racemes. Indi- oxidase activity (Zeisler 1938). vidual racemes are indeterminate, continually producing new flowers for weeks during the summer. The round Breeding biology seeds (2–4 mm in diameter) are borne in siliques. The seeds lack an endosperm (Sanchez-Acebo 2005) and Seeds were commercially collected and pooled from wild require moist cold stratification for embryo development populations in Utah. The seeds were shallowly planted and germination. outdoors in autumn 2003 at the common garden of the Bee Biology and Systematics Laboratory in Logan, Utah, USA. The following summer, the clay loam soils were infre- Flowering quently irrigated as needed to maintain plant vigor. For Individual plants of both Cleome species produce two each of the four pollination treatments, six well-separated types of like-sized showy flowers (yellow for C. lutea and individuals per species of similar size, vigor and bud

Plant Species Biology 23, 152–158 Journal compilation © 2008 The Society for the Study of Species Biology No claim to original US government works 154 J. H. CANE development were chosen, randomly assigned their medium grain industrial film) (Fig. 1) from lots of 20 treatment, and tagged. These plants were enclosed in seeds per species and color, representing all pollination 7m¥ 7m¥ 2 m walk-in field cages made of Lumite treatments. Persistently pale seeds and pale seeds that had screening (Synthetic Industries, Chicopee, GA, USA) to darkened 1 week after harvest were X-rayed again and exclude flower visitors. Individual pollinator exclusion their germination evaluated. Two lots of 10 dark seeds bags were not used because, in earlier trials, we found that each per species were weighed. flowers on the crowded tall racemes of Cleome transfered Three large, mature, intact plants of C. lutea were taken pollen by passively rubbing or jostling against the at the end of flower production. The life-time silique pro- bag netting. Once the flowers began to shed pollen, each duction per uncaged plant was determined by counting new flower on every tagged raceme was marked and their complements of siliques and replums (a loop of pollinated. tissue that persists after the valves of the siliques have During June and July, two manual pollination treat- dehisced) (Fig. 1). Lifetime seed production was then esti- ments were applied to newly opened flowers of the caged mated by multiplying by the average numbers of seeds plants: geitonogamy (transfer of self pollen) and per silique for that species. xenogamy (outcrossing). As younger crowded plants often produced single racemes, whose flowers proved dif- ficult to tag individually, different plants received single Seedling vigor treatments. Geitonogamous pollination involved rubbing Harvested seeds of C. lutea and C. serrulata from manually the day’s recipient virgin stigmas with fresh anthers from selfed and outcrossed flowers were placed in cold (4°C) an untagged flower from the same plant. Donor anthers storage for 4 months and then planted individually in for xenogamy were taken from untagged plants. Optical ‘conetainers’ in a heated glasshouse. On 19 April 2005, magnifying visors were used as necessary to visually seedlings were measured for size (height, length and confirm pollen transfer. Floral racemes were manually width of largest leaflet). Once the data were transformed pollinated daily until a plant shifted from producing her- (log10), the variances were homogeneous (Levene’s test) maphroditic to staminate flowers. Six other plants per and the data were normally distributed (Kolmogorov– species in the cages served as controls for autonomous Smirnov test). The performance of plants from outcrossed self-pollination (autogamy). Apomixis was impractical to versus selfed seed was compared by general linear model evaluate because the flowers would have needed to be anova followed by REGW a posteriori tests where war- nightly emasculated when they first opened. Adjacent to ranted (Ray & Sall 1985). Statistical significance in all cases the pollination treatment cages, six additional tagged was P Յ 0.05. plants per species were used as positive controls that were freely visited by pollinators. The pollination treatments were compared by species Results using general linear model anova tests for percentage Flowering fruit (silique) set (arcsine or log10 transformed) and for their yields of dark seeds per silique. In general, only the The flowers of Cleome presented an unexpected phenol- dark seeds possessed developed embryos. The data trans- ogy given the diverse diurnal pollinator fauna revealed by formations yielded acceptable normality (Shapiro–Wilk this and other studies (e.g. Messinger 2006). All new statistic, P > 0.01 or better) and homogeneous variances flowers of both species opened nocturnally, starting 1–3 h (Levene’s test, P > 0.04 or better). When differences were after sunset. No new flowers were added during daylight found among treatments (P Յ 0.05), the treatments were hours. For C. lutea, newly opened flowers from 10 plants compared by Ryan–Enot–Gabriel–Welch (REGW) a poste- were checked 150 mins after sunset on 13 July riori tests (Ray & Sall 1985). (23.30 hours mountain daylight savings time [MDST]). New pistils (n = 15) of C. lutea flowers were large, and each stigmatic tip was suffused with red pigment. Their Seed production pollen-free stigmas all produced frequent bubbles when Once siliques were mature, but before they dehisced, they immersed in hydrogen peroxide, indicative of their recep- were individually removed and returned to the labora- tivity. The anthers of half of these flowers had begun to tory. Siliques per raceme and the individual contents of dehisce, each anther first rupturing at its distal tip. For the dark seeds were counted (Fig. 1). To estimate and C. serrulata, the petals had unfurled by approximately compare seed viability, embryo development was com- 90 mins after sunset on 7 August. One or more nectar pared for plump seeds differing in color (dark vs pale) droplets was visible in 90% of these opening flowers, using X-ray imagery (HP 4380 N Faxitron; Hewlitt although at this hour only 2 of 18 flowers had dehiscing Packard, Salt Lake City, UT, USA; 25 KV, 30 s exposure, anthers and none showed stigmatic peroxidase activity.

During the hours after sunset, no flower visitors were The X-ray images of seeds from both Cleome species observed in the large uncaged plots of either species in the revealed the folded embryo within. Images of seeds could northern Utah common gardens, although the nights be visually classed into two groups, those possessing an were warm and calm. By dawn, all new flowers of both X-ray dense embryo (dark in positive image) (Fig. 1 inset) species had opened and possessed fully dehisced anthers, and those whose embryo was less dense (gray). Dark receptive stigmas and large droplets of viscous nectar seeds invariably had an X-ray dense embryo and were all (large enough in C. serrulata to rain out of shaken plants). readily germinable, whether dark at harvest (20 of 20 From an isolated C. lutea plant inspected just before images) or darkening in the week after harvest (20 of 20). sunrise, 11 of 17 stigmas from new flowers lacked pollen, Pale seeds at harvest sometimes lacked the visually dis- and the remaining stigmas had <10 grains. Later that same tinct embryo (5 of 20); those that remained pale 1 week sunny morning (10.30 hours MDST) after several hours of after harvest mostly lacked developed embryos (14 of 20). general bee activity, 14 of 15 stigmas bore pollen (most Mature dark seeds of both species were comparable in had >15 grains) on fresh flowers of the same plant. Thus, weight, averaging 6.7 mg each (for an estimated 150 000 some stigmas of C. lutea receive pollen at night, appar- seeds per kg). ently passively by autogamy; however, more thorough In the common garden, three large openly visited pollination occurred during morning bee activity. C. lutea plants produced an average of 1470 siliques each containing on average eight seeds, those of C. serrulata produced 1229 siliques with 21 seeds each. In a dense Breeding biology and seed production vegetated part of the plot, 22 C. lutea plants grew in 0.1 m2, Ϯ Both C. lutea and C. serrulata are fully self-fertile. Auto- yet even these averaged 6.6 3.6 racemes per plant. One gamy yielded considerable numbers of siliques and seeds big C. lutea raceme set large seeds from 80% of its 336 Ϯ for both species (Table 1). Autogamy is facilitated by the flowers. The C. lutea plants averaged 110 61 racemes per 2 stamens coiling inward later in the day. For C. lutea, m of plot. equivalent proportions of flowers set fruits in the auto- Seedling vigor gamy, geitonogamy and xenogamy treatments; flowers accessible to pollinators were two–threefold more fruitful Progeny of C. lutea grown in the glasshouse from seed (Table 1). The average counts of fertile seeds per silique that was dark at harvest (‘early’) were similar in size to did not differ between treatments. In C. serrulata, auto- those from seed that darkened the week after harvest gamy was inferior to the other treatments, with autoga- (‘late’). Seedling progeny from these two seed maturation mous flowers setting fewer siliques (F3,18 = 3.39, P < 0.04) classes (early or late) were equivalent in leaf and plant each with fewer seeds (F3,228 = 20.49, P < 0.0001) (Table 1). dimensions (6–10 seedlings measured per species; P > 0.1 Neither xenogamy nor pollinator access improved on gei- to P > 0.8). If the seed was viable (dark), then whether it tonogamy for either fruit set or seeds per silique. Com- matured on or off the plant did not affect subsequent paring the two species, siliques of C. serrulata produced seedling vigor. threefold more mature seeds than those of C. lutea in all Progeny from the two manual pollination treatments but the autogamy treatment (Table 1). were not equivalent in vigor in either species. Seedlings

Table 1 Comparison of fruit set, mature dark seeds per silique and progeny vigor for four pollination treatments of Cleome lutea and Cleome serrulata

Pollination treatment (Ϯ SD)† Sum of measured Reproductive Cleome Auto- Geiton- Xeno- Freely Flowers response species gamy ogamy gamy visited Plants or fruits

Flowers setting fruit (%) lutea 23 Ϯ 15 31 Ϯ 15 26 Ϯ 16 76 Ϯ 13* 47 1235 serrulata 34 Ϯ 15* 56 Ϯ 14 63 Ϯ 22 64 Ϯ 32 22 720 Seeds per fruit lutea 6 Ϯ 47Ϯ 47Ϯ 48Ϯ 447263 serrulata 8 Ϯ 6* 19 Ϯ 10 22 Ϯ 11 21 Ϯ 11 22 232 Seedling height (cm) lutea –17Ϯ 3.6* 11 Ϯ 3.6 – 70 – serrulata –13Ϯ 3.7* 10 Ϯ 2.4 – 48 – Seedling longest leaf (cm) lutea –35Ϯ 5.6* 25 Ϯ 3.4 – 70 – serrulata –25Ϯ 3.0 26 Ϯ 3.0 – 48 –

†All statistical comparisons are between treatments within species. *Values are statistically different from other treatments within their row (P Յ 0.05). Only seeds from manual pollinations were sown and compared for progeny vigor. SD, standard deviation.

Plant Species Biology 23, 152–158 Journal compilation © 2008 The Society for the Study of Species Biology No claim to original US government works 156 J. H. CANE resulting from geitonogamy were equal to, or larger than, ful bees, wasps and butterflies during daylight hours, those from xenogamy (Table 1). For C. lutea seedlings of attributes shared with some other desert Cleomaceae (e.g. like age, those from geitonogamy exceeded those from Wislizenia, Cleomella and Oxystylis). With reference to the xenogamy in both height (F1,69 = 43.3, P < 0.001) and Capparaceae, the flowers of Capparis ovata and Capparis length of the longest leaf (F1,69 = 72.7, P < 0.001) (Table 1). spinosa are nocturnal, the former pollinated by sphingid For C. serrulata seedlings of like age, those from geito- moths, while those of C. spinosa (in Israel) are first visited nogamy were 25% taller than outcrossed progeny nocturnally by pollen-foraging Proxylocopa bees, but later

(F1,47 = 6.7, P < 0.015), but seedlings from both treatments the next day by honey bees and other bees as well (Dafni were equivalent in leaf length and leaflet width (Table 1). et al. 1987). Perhaps nocturnal anthesis is a persistent No xenogamy advantage was evident in these measures of ancestral attribute in these Cleome species. For now, no seedling performance. satisfying ecological or phylogenetic explanation is appar- ent for the peculiar flowering schedules of these two species of Cleome. Discussion Beginning in the morning, diverse polylectic (i.e. gen- Both Cleome species possess pollination traits that have eralist) bees, butterflies and wasps opportunistically long been considered favorable for colonists (Baker & sought nectar and sometimes pollen from flowers of both Stebbins 1965). Self-fertility enables the first individual Cleome species in the common gardens (Fig. 2). Bees have that colonizes a site to produce viable seed. The coiling been extensively collected from wild C. lutea in southern stamens of older flowers facilitate autogamy. Further- Utah, both for this study and from 4 years of exhaustive more, progeny from geitonogamous seed grew at least as bee surveys in Grand Staircase-Escalante National Monu- vigorously as progeny from xenogamy. If pollinators are ment (O. Messinger and T. Griswold, pers. comm., 2007). absent, perhaps following some ecological perturbation Polylectic bees were found to be prevalent and wide- such as fire or flood, both Cleome species are capable of spread on C. lutea, accounting for 3/5 of the collected autogamy and facilitated self-pollination. Selection is specimens. Nearly half of the polylectic individuals expected to favor self-fertility of colonizing annuals like sampled belonged to just three genera of small-bodied Cleome when pollinator services might be unreliable (e.g. bees: Halictus, Hylaeus and Lasioglossum sensu lato, plus soon after habitat perturbation) (Lloyd 1992). The rate of diverse Perdita that are likely to be specialists on other expansion and persistence of Cleome populations in nature floral hosts. Bees less frequently collected from C. lutea is not known, but in our common gardens, the parent represent 28 other native bee genera: Agapostemon, plants set massive numbers of readily germinable seeds Andrena, Anthidiellum, Anthidium, Anthophora (Fig. 2), that produced dense stands of seedlings the following Ashmeadiella, Bombus, Ceratina, Colletes, Diadasia, year. If representative of wild populations, even when Dianthidium, Dieunomia, Dufourea, Eucera, Exomalopsis, bees are present, these Cleome species are likely to be Habropoda, Heriades, Macrotera, Megachile, Melecta, under serviced by their pollinators in some years of Melissodes, Nomada, Osmia, Protandrena, Sphecodes, Stelis, massive bloom, circumstances again favoring self-fertility Triepeolus and Xylocopa. Overall, 140 species of native and a degree of autogamy. bees have been taken from C. lutea in southern Utah, Phylogenetic inference from sister families was not pre- dictive of Cleome breeding biologies. These Cleome species did not share the distinct SI system found in their sister family, the Brassicaceae (Charlesworth et al. 2005). Meager evidence from the Capparaceae (sister group to Brassi- caceae and Cleomaceae) was not illuminating either, for while Capparis flexuosa is self-fertile, C. verrucosa is report- edly self-incompatible (Zapata & Arroyo 1978). The nocturnal anthesis of these Cleome flowers is puz- zling. Most species of Brassicaceae flower diurnally. A desert exception, Lyrocarpa coulteri, has drab, somewhat tubular flowers that release a heavy Gardenia-like scent after nightfall (J. Cane, pers. obs., 1994), attributes consis- tent with moth pollination. In contrast, flowers of both C. lutea and C. serrulata are vividly colored and scentless (to humans), attributes atypical for nocturnally pollinated flowers (Faegri & van der Pijl 1979). The flowers attracted Fig. 2 Digger bee (Anthophora californica) hovering to collect no nocturnal visitors in the common gardens, but plenti- pollen from the exserted anthers of a Cleome lutea flower.

Journal compilation © 2008 The Society for the Study of Species Biology Plant Species Biology 23, 152–158 No claim to original US government works POLLINATION NEEDS OF CLEOME 157 collectively representing many of the native bee genera Farmed C. lutea and C. serrulata should produce pro- found in the western USA. digious quantities of seed. Multiplying together seeds per The fauna at C. serrulata has not been so exhaustively silique (Table 1), siliques per raceme and racemes per sampled. Nonetheless, 62 species of native bees were col- plant, each mature, well-pollinated C. lutea plant in the lected in the Grand Staircase-Escalante National Monu- common garden produced an estimated 11 000 viable ment survey, with 95% of those individuals representing seeds (73 g fresh weight). Likewise, large plants of C. 51 bee species shared with C. lutea (Messinger 2006). serrulata each produced an estimated 26 000 seeds Together, the 162 native bee species found on these two (173 g). Conservatively, a farmed hectare of these two Cleome species are a substantial fraction of the species- Cleome species could produce nearly 2000 kg/ha of seed, rich bee community that inhabits the 730 000 hectares of although the species’ indeterminate growth and flowering the National Monument (Messinger 2006). In particular, would prevent harvest of all of that seed at once. one-third of the Monument’s entire fauna of polylectic Adequately abundant pollinators will be necessary to bee species (58% of all 656 species) were collected visit- realize such prodigious seed production by these two ing C. lutea and/or C. serrulata. These two floral hosts Cleome species; plants accessible to pollinators yielded can be expected to attract and feed many additional three–fivefold more viable seed than those limited to polylectic bee species throughout their broad geographic autogamy (Table 1). Fortunately, these Cleome species are ranges in the western USA (23 additional bee species in broadly attractive to a diverse array of generalist bees, the general collections at the Bee Biology and Systemat- including commercially managed species, such as hived ics Laboratory were collected from C. lutea and C. serru- honeybees or alfalfa leaf-cutting bees. General steward- lata). Flowering patches of Cleome attract and feed ship of otherwise unmanageable local ground-nesting diverse floral generalists from local bee communities, bees on farms could also be beneficial. Over several years, underscoring the potential value of these plants for such stewardship practices could foster adequate native bee communities where summer floras are other- numbers of generalist bees to satisfy the pollination needs wise lacking bloom. of fields planted with this crop. In turn, these Cleome Other species-rich floral guilds of bees often include species can feed diverse members of native bee commu- numerous oligolectic species (taxonomic pollen special- nities on a farm, gradually multiplying their numbers to ists) because their hosts (e.g. Helianthus, Larrea, Salix, pollinate additional native summer seed crops. Phacelia) present a ‘predictable plethora’ that oligolectic Ground-nesting bees comprise 90% of the individuals populations can depend on for ample pollen (Wcislo & and 80% of the species taken from C. lutea in the wild. This Cane 1996). In contrast, the two Cleome species examined bodes well for wild bee communities of the Intermountain in the present study appear to be opportunistic colonists West amid postfire restoration seedings because progeny whose annual bloom varies greatly with patchy annual of most of these ground-nesting bees should be deep rainfall. Only a single putative oligolege is associated with enough underground to survive the surface heat of wild- either Cleome species, the tiny bee Perdita zebrata. Perdita fires. Seeded in the autumn during postfire rangeland zebrata is common on C. lutea, accounting for half of the rehabilitation treatments, these Cleome species will germi- 2463 bees sampled from C. lutea in southern Utah. In turn, nate and bloom in the following summer, and their nectar the Cleomaceae account for 90% of all 1100 host labels for and pollen will feed surviving members of mid-summer this bee in the extensive US Department of Agriculture– bee communities at a time when most seeded perennials Agricultural Research Service bee collections at Logan, will often still be in vegetative growth stages. As both suggestive of it being a Cleome specialist. Many of the Cleome species attract a diverse array of bees and set pro- P. zebrata specimens caught from C. lutea were males, sug- digious seed, a land manager’s choice will be guided by gesting that they use Cleome flowers as likely sites to find an individual Cleome species’ geographic range and its mates, a habit common among oligoleges (Eickwort & habitat requirements, particularly soil texture and mois- Ginsberg 1980). A local bee community study found that ture, rather than any difference in value for wild bee P. zebrata dominated C. lutea, rarely if ever visiting the communities. other abundant flowering species used by diverse native floral generalists (Tepedino et al. 2008). Other than P. ze- Acknowledgments brata, the bee faunas found associated with C. lutea and C. serrulata all appear to be floral generalists. This accords Faye Rutishauser, Melissa Weber, Morgan Yost and James well with the relative dearth of floral specialists associated McDonald contributed ably to all facets of the field and with members of the Brassicaceae (Hurd 1979; Gomez & laboratory work. Terry Griswold kindly shared label data Zamora 1999), likely reflecting the fact that their popula- from bee surveys of the Grand Staircase region of south- tions are transient and their floral morphologies and ern Utah and Harold Ikerd assisted with database rewards are unspecialized (Wcislo & Cane 1996). searches. Dr Hugh Iltis enthusiastically shared his

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