ASH MEADOWS NATIONAL WILDLIFE REFUGE The Contributions of to the Reproductive Fitness of 12 Rare on Ash Meadows National Wildlife Refuge Final Report

February 2012

David A. Tanner, Nicole F. Boehme, Catherine M. Clark, and James P. Pitts Department of Biology, State University, Logan, Utah

Submitted to: Ash Meadows National Wildlife Refuge c/o Desert National Wildlife Refuge Complex 4701 N Torrey Pines Las Vegas, NV 89130 Submitted by: BIO-WEST, Inc. 1063 West 1400 North Logan, UT 84321

TABLE OF CONTENTS

1.0 GENERAL INTRODUCTION ...... 1

2.0 RARE PLANTS OF ASH MEADOWS NATIONAL WILDLIFE REFUGE USED IN THE STUDY ...... 2 2.1 Arctomecon merriamii ...... 2 2.1.1 General Information ...... 2 2.1.2 Importance to Pollinators ...... 3 2.2 Astragalus phoenix...... 3 2.2.1 General Information ...... 3 2.2.2 Importance to Pollinators ...... 4 2.3 striatus ...... 4 2.3.1 General Information ...... 4 2.3.2 Importance to Pollinators ...... 4 2.4 Centaurium namophilum ...... 5 2.4.1 General Information ...... 5 2.4.2 Importance to Pollinators ...... 5 2.5 Cordylanthus tecopensis ...... 5 2.5.1 General Information ...... 5 2.5.2 Importance to Pollinators ...... 6 2.6 nudicaulis var. corrugata ...... 6 2.6.1 General Information ...... 6 2.6.2 Importance to Pollinators ...... 6 2.7 Grindelia fraxino-pratensis ...... 7 2.7.1 General Information ...... 7 2.7.2 Importance to Pollinators ...... 7 2.8 Ivesia kingii var. eremica ...... 7 2.8.1 General Information ...... 7 2.8.2 Importance to Pollinators ...... 8 2.9 Mentzelia leucophylla ...... 8 2.9.1 General Information ...... 8 2.9.2 Importance to Pollinators ...... 8 2.10 mohavensis ...... 9 2.10.1 General Information ...... 9 2.10.2 Importance to Pollinators ...... 9 2.11 Sisyrinchium spp...... 9 2.11.1 General Information ...... 9 2.11.2 Importance to Pollinators ...... 9 2.12 Spiranthes infernalis ...... 10 2.12.1 General Information ...... 10 2.12.2 Importance to Pollinators ...... 10

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR i to the Reproductive Fitness of 12 Rare Plants

3.0 TASK 4: IDENTIFY RARE POLLINATORS AT ASH MEADOWS NATIONAL WILDLIFE REFUGE ...... 10 3.1 Methods...... 10 3.1.1 Study Sites ...... 10 3.1.2 Observations and Collections ...... 11 3.1.3 Pollen Reference Library ...... 11 3.1.4 Pollen Quantification ...... 12 3.1.5 Pollinator Classification ...... 12 3.2 Results ...... 13 3.2.1 Arctomecon merriamii ...... 13 3.2.2 Astragalus phoenix...... 14 3.2.3 Calochortus striatus ...... 15 3.2.4 Centaurium namophilum ...... 17 3.2.5 Cordylanthus tecopensis ...... 19 3.2.6 var. corrugata ...... 20 3.2.7 Grindelia fraxino-pratensis ...... 22 3.2.8 Ivesia kingii var. eremica ...... 24 3.2.9 Mentzelia leucophylla ...... 25 3.2.10 Nitrophila mohavensis ...... 27 3.2.11 Sisyrinchium spp...... 28 3.2.12 Spiranthes infernalis ...... 28 3.3 Discussion ...... 29 3.3.1 Is There a Guild of Pollinators Uniquely Important to the Rare Plants of the Refuge? ...... 32

4.0 TASK 5: IDENTIFY THE POLLINATORS OF OTHER CONCURRENTLY BLOOMING FLOWERS ...... 35 4.1 Introduction ...... 35 4.2 Methods...... 35 4.2.1 Plant Identification ...... 35 4.2.2 Insect Collection ...... 36 4.2.3 Insect Preservation and Identification ...... 36 4.3 Results ...... 36 4.3.1 Asclepias ...... 36 4.3.2 Creosote ...... 37 4.3.3 Enceliopsis ...... 37 4.3.4 Grindelia ...... 37 4.3.5 Helianthus ...... 37 4.3.6 Prosopis ...... 37 4.3.7 Salix...... 38 4.3.8 Salvia...... 38 4.3.9 Stanleya ...... 38 4.3.10 Tamarix ...... 38 4.4 Discussion ...... 38 U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR ii to the Reproductive Fitness of 12 Rare Plants

5.0 TASK 6: IDENTIFY THE LOCATION OF NEST SITE AGGREGATIONS AND HABITAT PREFERENCES OF INSECT POLLINATORS ...... 40 5.1 Methods...... 40 5.2 Results ...... 42 5.3 Discussion ...... 46

6.0 GENERAL DISCUSSION AND RECOMMENDATIONS ...... 47

7.0 LITERATURE CITED ...... 49

APPENDIX A: SALIENT LITERATURE NOT CITED IN TEXT

APPENDIX B: LIST OF THE RARE PLANTS AND THEIR POTENTIAL POLLINATORS AT ASH MEADOWS NATIONAL WILDLIFE REFUGE

List of Tables

Table 1. Rare plants of Ash Meadows National Wildlife Refuge (Refuge), with status and approximate bloom times...... 2

Table 2. Data summary for Arctomecon merriamii (ARME)...... 13

Table 3. Data summary for Astragalus phoenix (ASPH)...... 15

Table 4. Data summary for Calochortus striatus (CAST)...... 16

Table 5. Data summary for Centaurium namophilum (CENA)...... 18

Table 6. Data summary for Cordylanthus tecopensis (COTE)...... 19

Table 7. Data summary for Enceliopsis nudicaulis var. corrugata (ENNUC)...... 20

Table 8. Data summary for Grindelia fraxino-pratensis (GRFR)...... 23

Table 9. Data summary for Ivesia kingii var. eremica (IVKI)...... 24

Table 10. Data summary for Mentzelia leucophylla (MELE)...... 26

Table 11. Data summary for Nitrophila mohavensis (NIMO)...... 27

Table 12. Data summary for Sisyrinchium spp. (SISYR)...... 28

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR iii to the Reproductive Fitness of 12 Rare Plants

Table 13. Data summary for Spiranthes infernalis (SPIN)...... 29

Table 14. Pollinator status of the primary pollinators in relation to the 12 rare plants of Ash Meadows National Wildlife Refuge...... 33

Table 15. Coordinates and descriptions of sampling sites used to identify potential nesting habitat on Ash Meadows National Wildlife Refuge...... 40

Table 16. Bee nesting habitat sampling sites grouped by habitat type...... 42

Table 17. Potential nesting habitats for bee pollinators of the 12 rare plants at Ash Meadows National Wildlife Refuge...... 43

Table 18. Preferred habitat for each bee species collected, based on significant difference in bee abundance between habitats...... 45

List of Figures

Figure 1. Sand dune and non-dune sampling sites used to identify potential bee nesting habitat on Ash Meadows National Wildlife Refuge...... 41

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR iv to the Reproductive Fitness of 12 Rare Plants

1.0 GENERAL INTRODUCTION

Ash Meadows National Wildlife Refuge (Refuge) is home to many endangered, threatened, and rare organisms. Among these are 12 plant species that range in special status from species of concern to endangered (rare plants) (Table 1). In the interest of conserving these rare plants amid the planned and current restoration activities at the Refuge, we conducted a study in which we identified the visitors to each of these plants so that their insect pollinators may also be conserved. The success of many plants is enhanced, if not determined by, pollination services offered by insect visitors. Therefore, if the aim of the Refuge is to protect the rare flora within its boundaries, a better understanding of the relationship between these plants and their insect pollinators is required. To this end we 1) conducted a literature review of the pollination ecology of the Refuge’s 12 rare plants and related plants, 2) reviewed museum collections to assist in the field identification of insect pollinators, 3) prepared a taxonomic list of insect pollinators likely to occur on the Refuge, 4) identified the suite of insect pollinators that service the 12 rare plant, 5) identified plant species that support a large portion of the Refuge’s insect pollinator community, and 6) identified habitat preferences and locations of insect pollinator nest sites relative to the 12 rare plants, as well as provided global positioning system (GPS) locations of extant bee aggregations on the Refuge.

Because of the reciprocal relationship between plants and pollinators, we have structured this report to identify which plants are most important to the pollinators and which pollinators are most important to the rare plants of the Refuge. Because tasks 1 through 3 are pedestrian in nature and have little bearing on the results of our study, the list of references used for them and the taxonomic list of potential insect pollinators are located Appendix 1 and 2, respectively.

We accomplished task 4 by making behavioral observations of the as they interacted with the flowers, and by quantifying the pollen located on the body of the insects. Observing the movements of insects on the flowers provided information on whether the insects are transferring pollen between flowers and consequently pollinating the plant, or whether they are only gathering plant rewards. Some insects will visit repeatedly for a nectar reward and never significantly contact plant anthers or stigmas. It is important, therefore, that we determine which insects are only gathering rewards and which could significantly contribute to plant reproduction.

We conclude this report with a list of general recommendations, though we do so with the understanding that they are only recommendations and that the Refuge is under no obligation to accept or adopt them. We understand that the acceptance of our recommendations will be contingent on the perceived obligations of Refuge staff as land managers. We also understand that our recommendations may be in direct opposition to recommendations offered by similar studies conducted on other taxa, though we are currently unaware of incompatible recommendations. We offer these recommendations in full faith that Refuge staff will consider them without bias and with the purpose of conserving the unique biota of the Refuge.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 1 to the Reproductive Fitness of 12 Rare Plants

Table 1. Rare plants of Ash Meadows National Wildlife Refuge (Refuge), with status and approximate bloom times. FEDERAL ENDEMIC TO APPROXIMATE SCIENTIFIC NAME COMMON NAME STATUS/ THE REFUGE BLOOM TIMES a STATUS Arctomecon White bearpoppy No Concern April–June merriamii Ash Meadows Astragalus phoenix Yes Threatened/Endangered March–late May milkvetch Alkali mariposa Calochortus striatus No Concern April–June lily Centaurium Spring-loving Maybe Threatened/Endangered July–September namophilum centaury Cordylanthus Tecopa bird’s beak No Concern July–October tecopensis Enceliopsis Ash Meadows nudicaulis var. Yes Threatened/Endangered April–May sunray corrugata Grindelia fraxino- Ash Meadows Yes Threatened/Endangered June–October pratensis gumplant Ivesia kingii var. Ash Meadows ivesia Yes Threatened August–October eremica Mentzelia Ash Meadows Late May– Yes Threatened/Endangered leucophylla blazingstar September Nitrophila Ash Meadows Yes Endangered Late April–June mohavensis niterwort Sisyrinchium spp. Blue-eyed grasses Unknown Unknown Unknown Ash Meadows lady’s Spiranthes infernalis Yes Concern June–August tresses a Blooming information from a 2006 report by Otis Bay and Stevens Ecological Consulting (additional information about the report is unavailable; citation is unreferenced).

2.0 RARE PLANTS OF ASH MEADOWS NATIONAL WILDLIFE REFUGE USED IN THE STUDY

2.1 Arctomecon merriamii

2.1.1 General Information

Arctomecon merriamii Coville (white bearpoppy) is a caespitose (growing in dense tufts) perennial herb supported by a stout, often long, taproot. The leaves are found toward the base of the plant and form a broad, gray, spherical tuft approximately 10 centimeters (cm) tall. The flowers occur individually on long, naked peduncles (stalks). When open, they range from 2.5 to 4.0 cm in diameter with white, showy that form a wide cup, which insects commonly land in. There are many ; each has a long, slender filament and a bright yellow to orange U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 2 to the Reproductive Fitness of 12 Rare Plants

anther. The stigma lobes are sessile (Jepson 1979). The is an oblong 3.5 to 4.0 cm long, in which the valves split from the apex. The ovary of a single pistol contains approximately 400 ovules, and each mature fruit contains 200 to 300 seeds. The seeds are dark brown to black and approximately 2 millimeters (mm) long with a prominent white elaiosome.

There are 129 occurrences of A. merriamii throughout its range, which includes much of the between 610 to 2,000 meters (m) above sea level. Arctomecon merriamii is considered a regional endemic for Nye and Clark counties, Nevada, and adjacent Inyo and San Bernardino counties, , though it has a sparse distribution across its range. An estimated 20,000 individuals remain across its range in California and Nevada, including approximately 220 plants on the Refuge (approximately 1.1% of the species) (Knight and Clemmer 1987).

Arctomecon merriamii occurs in a wide range of soils, including alkaline clay and sand, gypsum, calcareous alluvial gravels, and carbonate rock outcrops. At the Refuge it is located in sandy soils and occasionally in deep washes, and it seems to prefer areas with some degree of natural disturbance. It is also located on white clay hill and paleospring land types (Jensen 2007, pers. comm.).

2.1.2 Importance to Pollinators

Arctomecon merriamii, a member of the poppy family (Papaveracea), occurs in areas with soils that are suitable, and even desirable, to nesting . Similar to A. merriamii, bees commonly nest in areas with loose sandy soils that are topographically rich. Additionally, A. merriamii is in bloom early in the calendar year, coincidental with some bees. Our data have shown that A. merriamii supports three species of Anthophora (the same that is the primary pollinator of Astragalus phoenix, see below), and four other bee species. These data suggest that A. merriamii likely contributes to the viability of important early pollinators on the Refuge, particularly some important to other rare plants.

2.2 Astragalus phoenix

2.2.1 General Information

Astragalus phoenix Barneby (Ash Meadows milkvetch) is a low, mound-forming shrub. The flowers of this species are large, indeed, larger than many others in the genus; the upper is approximately 2.5 cm long. Individual plants are hemispheric and commonly 10 to 50 cm in diameter, though a few are known to approach 90 cm in diameter. The flower is pink to lavender and is borne on short peduncles that rise only a short distance above the canopy of flowers. One to two flowers occur per florescence. Each flower has ten stamens, nine of which are partially fused while one remains free. There is a single carpel with one unbranched stigma. Each ovary contains 10 to 30 ovules, though this appears to vary significantly (Pavlik 2007, pers. comm.). The fruit has a single chamber that is somewhat inflated and curved with dense, white

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 3 to the Reproductive Fitness of 12 Rare Plants

pubescence. The seeds range in color from green to tan, are approximately 3 mm in diameter, and have a thick coat.

Astragalus phoenix occurs between 670 and 730 m above sea level in saline-alkaline soils adjacent to springs within the Mojave Desert; it can, however, also be found in hard, impacted soils.

2.2.2 Importance to Pollinators

Astragalus phoenix seems to support only a single species of bee, Anthophora porterae. We also collected honey bees from A. phoenix, though we believe they were there incidentally and do not collect much pollen or nectar from the flowers. Astragalus is commonly visited by a variety of bees, and A. phoenix is located in and near habitats that are suitable for bee nesting. It blooms, however, very early in the year when there are very few pollinators available. Our data, therefore, suggest that A. phoenix does not contribute significantly to the community of pollinators on the Refuge.

2.3 Calochortus striatus

2.3.1 General Information

Calochortus striatus Parish (alkali mariposa lily), like many lilies, has a large open flower with exposed stigma and stamens. It is a perennial herb that grows from an erect stem that ranges from 1.0 to 4.5 cm long; the basal leaves, which typically wither soon after the flower has opened, are small. The petals are typically pink to lavender with purple veins, narrow basally, and have dense basal and internal pubescence. This pubescence is coincidental with the nectaries and glands that produce a sticky resin that some bees collect for nest construction. A single ovary may contain 90 ovules; 50 of these commonly develop into seeds (Knight and Clemmer 1987). There are four to five per plant and each is erect and linear. The seeds range in color from green to tan and are approximately 5 millimeters (mm) long (Knight and Clemmer 1987).

Calochortus striatus occurs in open alkali meadows and dry streambeds. It is commonly associated with creosote bush scrub and found between 760 and 1,300 m above sea level (Knight and Clemmer 1987). The range of C. striatus is limited to Clark and Nye counties, Nevada, and adjacent counties in California (Knight and Clemmer 1987).

2.3.2 Importance to Pollinators

Many insects, though mostly bees, use Calochortus striatus as a pollen, nectar, or resin source. We feel that this is largely a product of flower morphology and the location of the floral resources. It has a very open flower that allows insects with a wide variety of body types access to the pollen, nectar, and resin. Additionally, C. striatus is located in loose, sandy soils, which

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 4 to the Reproductive Fitness of 12 Rare Plants

are preferred for nesting by many bees. Calochortus striatus, therefore, seems to be an important plant to many of the pollinating insects of the Refuge.

2.4 Centaurium namophilum

2.4.1 General Information

Centaurium namophilum Reveal et al. (spring-loving centaury) is a glabrous annual that grows up to 45 cm tall (Knight and Clemmer 1987), though we rarely encountered plants exceeding 20 cm tall. The plant is composed of many stems that each bears many flowers (Reveal et al. 1973). The stems originate from a large taproot. The calyx of the flower is cylindrical and surrounds the corolla. The flowers are largely a deep, vibrant pink to magenta, except for a broad whitish band on the lower surface (Reveal et al. 1973). The stamens extend beyond the petals; these twist once pollen has been released. The style extends beyond the stamens and has a bilobed stigma (Reveal et al. 1973). The seeds are rectangular to ovoid and are less than 1 mm across.

Centaurium namophilum is restricted to the mesic to wet alkaline clay soils along the banks of streams and seepages (Reveal et al. 1973). It is also commonly found in and adjacent to thick meadows of salt grass. Its range is restricted between 670 and 730 m above sea level.

2.4.2 Importance to Pollinators

Centaurium namophilum may contribute to the fitness of the Refuge’s insect pollinators, particularly those active later in the season. We collected many insects visiting these flowers, and most were actively collecting pollen, though some may have been there incidentally. Centaurium namophilum occurs in a habitat that is likely not favored by bees. It occurs in wet soils commonly covered by grasses, which inhibit bee nesting. So, it is likely that the species contributes to the more vagile pollinating insects of the Refuge.

2.5 Cordylanthus tecopensis

2.5.1 General Information

Cordylanthus tecopensis Munz and Roos (Tecopa bird’s beak) is a tall (30–40 cm) annual commonly found in wet, saline soils (Knight and Clemmer 1987). The of C. tecopensis is a loose spike 2 to 6 cm long with 12 to 24 flowers (Knight and Clemmer 1987). The flowers are pale lavender and have a closed morphology, preventing entry to all but the most determined visitor. The flowers have two functional stamens and a filiform style (Knight and Clemmer 1987). Cordylanthus tecopensis produces approximately 10 seeds per capsule; the seeds are light brown and approximately 2 mm long (Knight and Clemmer 1987).

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 5 to the Reproductive Fitness of 12 Rare Plants

Cordylanthus tecopensis is restricted to the drainage in California and Nevada at elevations of 650 to 1,400 m above sea level. It is commonly found in the inundated soils of alkaline meadows and flats (Knight and Clemmer 1987).

2.5.2 Importance to Pollinators

Cordylanthus tecopensis is important to pollinators that are active late in the calendar year, despite the soils it is commonly found in. Many of the bees that visit C. tecopensis are either vagile enough to nest far from the plant (e.g., Melissodes) or they may not nest in the soil (e.g., Dialictus).

2.6 Enceliopsis nudicaulis var. corrugata

2.6.1 General Information

Enceliopsis nudicaulis var. corrugata Cronquist (Ash Meadows sunray) is a partially woody perennial 10 to 40 cm tall that grows from a fairly woody root stalk (Mozingo and Williams 1980). The flowers are borne on long stalks that extend well beyond the leaves, which are all basal, of the plant (Mozingo and Williams 1980). There are between 20 and 40 disk flowers, which are strongly compressed, and 10 to 25 ray flowers. The ray flowers have corollas that are approximately 2 cm long (Mozingo and Williams 1980). The fruits are dark brown to black, covered with a silky pubescence, and bear two short awl-shaped awns connected by a whorl of short, fused scales (Mozingo and Williams 1980). The fruits are approximately 10 mm long, and fruit size does not vary between ray and disk flowers (Mozingo and Williams 1980).

Enceliopsis nudicaulis var. corrugata commonly occurs in white alkaline soils along dry washes and in hard, pale limestone outcrops and is associated with desert scrub flora approximately 650 m above sea level. Recent surveys by BIO-WEST, Inc. (BIO-WEST) and Otis Bay and Stevens Ecological Consulting have shown that E. nudicaulis var. corrugata may occupy a broad range of habitats.

2.6.2 Importance to Pollinators

Enceliopsis nudicaulis var. corrugata contributes more to the pollinator communities on the Refuge than any other plant, save perhaps Prosopis glandulosa. We collected more species of bee, wasp, and from E. nudicaulis var. corrugata than from any other of the 12 rare plants. Insects visit this plant for both the copious pollen and nectar it produces, and it is probable that many bees nest close to these plants since they seem to prefer loose, sandy soils.

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2.7 Grindelia fraxino-pratensis

2.7.1 General Information

Grindelia fraxino-pratensis Reveal and Beatley (Ash Meadows gumplant) is a perennial to biennial herb that grows 70 to 100 cm tall (Cochrane 1981). This plant has many stems that all bear many flowers. Each of the peduncles on the stems bears one to four flower heads that consist of 12 to 14 ray flowers and 14 to 16 disk flowers (Cochrane 1981). Both types of flower are largely yellow. The fruits are small, golden brown, and range between 2 and 4 mm long.

Grindelia fraxino-pratensis is restricted to the Ash Meadows area of southern Nevada and is commonly located between 600 to 650 m above sea level. It is commonly found in moist soils supplied by significant seepage from surrounding drainages and is associated with thick meadows of salt grass (Cochrane 1981).

2.7.2 Importance to Pollinators

Because of the morphology of its flowers, G. fraxino-pratensis is visited by many large bees that are active later in the calendar year. As with Cordylanthus, G. fraxino-pratensis is found in inundated soils with associated thick meadows of salt grass. Consequently, the bees visiting G. fraxino-pratensis are either very large, nest in media other than the soil, or both. Grindelia fraxino-pratensis, however, appears to be a very good source of pollen and nectar. Additionally, G. fraxino-pratensis supports a species of the bee genus that is known only from the Refuge.

2.8 Ivesia kingii var. eremica

2.8.1 General Information

Ivesia kingii var. eremica Ertter (Ash Meadows ivesia) is a perennial composed of many shoots that sit atop a thick, woody root. The shoots commonly lay parallel to the ground, or are raised slightly, and are covered with a fine, grayish pubescence. The flower petals are white, ovoid distally, and narrowed basally. There are up to six pistils per flower, each of which may develop into a flask-shaped fruit approximately 2 mm long (pers. obs.).

Ivesia kingii var. eremica, as with Grindelia fraxino-pratensis, is restricted to the Ash Meadows area of Nevada and occurs between 600 and 650 m above sea level. Ivesia kingii var. eremica occurs in flat, saline soils, which are commonly inundated with water, and is commonly associated with thick meadows of salt grass (pers. obs.).

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 7 to the Reproductive Fitness of 12 Rare Plants

2.8.2 Importance to Pollinators

Ivesia kingii var. eremica does not contribute significantly to the Refuge’s bee pollinator community. We collected five bee species from I. kingii var. eremica, and most of these collections were made in 2008. All of the bees that we collected from I. kingii var. eremica were also collected on other plants on the Refuge that likely make greater contributions to the bees’ fitness. While I. kingii var. eremica has an open floral morphology and is a color that is attractive to many bees, it is a relatively small plant, it does not grow in large contiguous mats, and it is located in inundated soils associated with thick meadows of salt grass.

2.9 Mentzelia leucophylla

2.9.1 General Information

Mentzelia leucophylla Brandegee (Ash Meadows blazingstar) is a perennial to biennial plant that can exceed 50 cm in height. It has many erect stems that originate from a single taproot. Each stem supports many flowers; the flowers are bright yellow with corollas on the stalk in an open florescence. The are larger than the petals, triangular, and heavily pubescent. Seeds are produced in a spherical capsule. The seeds are small (2 mm in diameter), flat, circular, and light brownish-yellow.

Mentzelia leucophylla appears to be endemic to the Ash Meadows area of Nevada between 650 and 700 m above sea level (Mozingo and Williams 1980). It is commonly found on west-facing, 20-degree slopes (Mozingo and Williams 1980) in loose, light-colored, fine-textured soils (Reveal 1978) and is commonly associated with shadscale scrub (Nevada Natural Heritage Program 2001).

2.9.2 Importance to Pollinators

Mentzelia leucophylla is located in and adjacent to habitat suitable for bee nesting. Additionally, the color and shape of the flowers make M. leucophylla a highly attractive plant to bees. Mentzelia leucophylla is also interesting because its flowers open near the end of the day, when few other flowers are opening and the floral resources of earlier-blooming plants presumably have been exhausted. We collected 22 species of bee visiting M. leucophylla, including a new species in the genus Perdita that is endemic to Ash Meadows. These data, and those of floral timing, suggest that M. leucophylla is an important plant to the Refuge’s pollinators.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 8 to the Reproductive Fitness of 12 Rare Plants

2.10 Nitrophila mohavensis

2.10.1 General Information

Nitrophila mohavensis Munz and Roos (Amargosa niterwort) is a low-growing perennial of the goosefoot family (Chenopodiaceae) with many erect shoots originating from an extensive system. The flowers are red, very small, and nestled into the upper leak axils. Each flower has five stamens that converge at their base. The pistil has two stigmas. The seeds are also very small, black, or brown.

Nitrophila mohavensis is restricted to alkaline flats with inundated soils at 650 m above sea level (Nevada Natural Heritage Program 2001). It commonly occurs amid a thick salt crust exuded from the inundated soils.

2.10.2 Importance to Pollinators

We did not observe bees using N. mohavensis for forage. Some plants in Chenopodiaceae are pollinated by ants, which N. mohavensis may be, or by wind. We do not feel that N. mohavensis contributes significantly to the Refuge’s pollinator community.

2.11 Sisyrinchium spp.

2.11.1 General Information

Sisyrinchium spp. (blue-eyed grass) is a tall (25 cm) perennial that grows from a rhizome in a variety of soils. On the Refuge Sisyrinchium is commonly found in wet, sandy soils that are frequently inundated. Sisyrinchium produces a small, purple flower composed of six ovate to triangular petals with many exposed stamens that produce bright yellow pollen.

2.11.2 Importance to Pollinators

Sisyrinchium spp. does not contribute significantly to the fitness of the Refuge’s pollinator community. We collected very few bees from these flowers, and the bees we collected were likely there incidentally. In addition to growing in soils commonly inundated with water, Sisyrinchium spp. blooms concurrently with Enceliopsis nudicaulis var. corrugata and competes directly with it for pollinator services.

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2.12 Spiranthes infernalis

2.12.1 General Information

Spiranthes infernalis Sheviak (Ash Meadows lady’s tresses) is a perennial that grows from a tuber. Each stem grows 20 to 40 cm tall (Sheviak 1989). The leaves are located at the base of the plant and rise up the stem in a nearly linear fashion (Sheviak 1989). The flowers exist in a tight spiral that winds up the stem to its terminus. The flowers are pale to yellow when mature (Sheviak 1989). The pollen is encapsulated in sticky packages called pollinia, and the ovary contains many minute ovules.

Spiranthes infernalis is endemic to the Refuge and is found between 670 and 720 m above sea level. It favors wet alkaline meadows and is commonly associated with thick meadows of salt grass (pers. obs.).

2.12.2 Importance to Pollinators

Spiranthes infernalis does not contribute to the fitness of many bee pollinators of the Refuge, though it may represent a significant source of forage for some genera of bees that visit other rare plants. We collected only six bee species from S. infernalis, though this plant appears to support many pollinators relative to others within the genus Spiranthes (Sipes and Tepedino 1994).

3.0 TASK 4: IDENTIFY RARE PLANT POLLINATORS AT ASH MEADOWS NATIONAL WILDLIFE REFUGE

3.1 Methods

To identify the suite of pollinators that service the 12 rare plants of the Refuge, we made field observations of how insects were interacting with the flowers of the plants, collected the insects that were visiting flowers, and identified them in the laboratory. We also removed a sample of the pollen that was on each bee and identified it against a reference collection of pollen, quantified the pollen amount and consistency, and used this as an index for floral fidelity. We then categorized the collected insects according to the quality of their pollination services, which is based on how the insects interacted with the flowers and the pollen analysis.

3.1.1 Study Sites

Because this project was intended to be completed in conjunction with BMP Environmental, we utilized the same populations of plants as they did. The locations of these populations were supplied by BIO-WEST. Before selecting these as study sites we assessed their viability, which was based on the number of plants, estimated plant density, and proximity to other populations U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 10 to the Reproductive Fitness of 12 Rare Plants

of rare plants. Sites were considered unviable if there were fewer than 10 plants in the population, and preference was given to populations that were near other rare plant populations. This maximized the efficiency with which we were able to collect data and allowed us to collect data in areas that ought to be of special interest to Refuge staff.

3.1.2 Pollinator Observations and Collections

Pollinator observations were interspersed with collection periods; we observed pollinator behavior and collected floral visitors in alternating 15-minute sessions. We observed the behavior of insects located within a 1 m2 area. We collected information on the duration of the visit, which parts of the insect’s body contacted the stamens and stigmas, whether pollen or nectar were being collected, how many visits were made to the same plant, and how many flowers were visited by a single insect on the same plant (Beattie 1971; Kearns and Inouye 1993). Many of the rare plants we observed during the 2008 season had very little insect visitation. Consequently, observation periods often exceeded 3 hours. Time was allocated to each plant based on the absolute amount of current insect visitation and the number of other rare plants that were concurrently blooming.

We collected insects in a manner that minimized damage to the plants. If an insect was touching the flower, we gently placed an insect net on the top of the plant and waited for the insect to fly up into the net. If an insect was flying near the plant (i.e., the insect had collected the floral rewards and was leaving the plant), we gently swept our nets through the plants in an attempt to capture the insects. We then transferred the insects into a jar containing cyanide and quickly dispatched them. The insects were then transported to the insect museum at Utah State University, where they were mounted, identified, and prepared for the pollen analysis.

Because there were often many rare plants in bloom simultaneously, we made observations throughout the day at each site and determined the best time of day to observe and collect specimens in an attempt to maximize the efficiency with which we collected data.

We identified bees to the lowest taxonomic level possible; typically this was to species. Some bees, however, were not identified to species because no key to species exists, the specimen was in poor condition, or no specialist could be located to assist with the identification.

3.1.3 Pollen Reference Library

To identify the pollen that we removed from the insects visiting the rare plants, we made a pollen reference library. To make this library, we collected anthers from the 12 target rare plants and other plants blooming in the area. We transported the anthers to the insect museum at Utah State University. Once at the museum, we dried the anthers for 24 hours. We then transferred the pollen to slides and added Calberla’s stain, which is a basic fuchsine stain (Kearns and Inouye 1993). The pollen and stain were held to the slide with a glycerin jelly.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 11 to the Reproductive Fitness of 12 Rare Plants

3.1.4 Pollen Quantification

Once the insects were transported to the insect museum at Utah State University and mounted for examination, they were placed in a relaxing chamber containing paradicholorobenzene or Lysol® Concentrate. We removed the pollen from the body of the insect with a small amount of glycerin jelly infused with Calberla’s stain on a wooden probe. This matrix was applied to the head, thorax, legs, and abdomen of the visiting insect. The pollen on these regions of the insects’ bodies adhered to the glycerin jelly, which was then transferred to a microscope slide (Kearns and Inouye 1993).

We quantified the amount of pollen on the body according to the percentage of body area covered: 0 = none, 1 = up to 10%, 2 = 11–20%, 3 = 21–30%, 4 = 31–40%, 5 = 41–50%, 6 = 51– 60%, 7 = 61–70%, 8 = 71–80%, 9 = 81–90%, 10 = 91–100%, and 11 = more than one layer of pollen. A percentage rating was used for six body sections (ventral and dorsal surfaces of the head, thorax, and abdomen) and the legs.

After the pollen was mounted on the microscope slides, we quantified the amount of pollen removed from each body region of each insect and calculated a ratio of pollen from a target rare plant to that from a non-target plant. We estimate that at least 15 pollen grains are required to successfully pollinate a flower (Cruden 1977).

3.1.5 Pollinator Classification

To determine which insect visitors would most likely be successful pollinators for each target rare plant, we combined the field and laboratory data. We compared the number of observations, total pollen counted, and the ratio of target rare plant pollen to non-target plant pollen (target ratio) for specimens where floral contact was noted. The target ratio is at best an indirect measure of floral constancy. For a large study such as this, however, it is useful to determine the type of pollen insect visitors are collecting during a foraging trip, and to estimate whether the visiting insects have enough pollen present and in the correct places to pollinate the target rare plant. Visitors were ranked by their likelihood of acting as a pollinator. To be considered a candidate of any sort, more than 15 pollen grains must have been counted on the insect’s body, and the grains must have had some probability of being transferred to the stigma of a flower.

A very good pollinator will have been observed at the plant more than five times, have a pollen load that was at least 85% pollen from a target rare plant, or have more than one observation with at least 90% pollen from a target rare plant. Very good pollinators must also move between plants and facilitate cross-pollination. A good pollinator will have a pollen load that was at least 75% from a target rare plant, or it will have been observed more than once with a pollen load consisting of at least 75% pollen from a target rare plant. A pollinator will also be considered good if the pollen load is more than 85% pollen from a target rare plant, but the insect does not move between plants. A likely pollinator will have a pollen load that has between 50% and 75% pollen from a target rare plant, or it will have been observed more than once with a pollen load U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 12 to the Reproductive Fitness of 12 Rare Plants

consisting of between 50% and 75% pollen from a target rare plant. A poor pollinator will have a pollen load that consists of less than 50% pollen from a target rare plant. There are no flower- visitation requirements for the last two classifications.

Please note that the data presented in the Results section include the average proportion of target rare plant pollen on the body of the insects, which may be considerably more or less than individual observations of these proportions.

3.2 Results

3.2.1 Arctomecon merriamii

This plant was frequented by many large bees (Table 2). We found that large bees, such as species of Anthophora, Apis mellifera, Habropoda, and fucata, collected pollen across their bodies, especially ventrally and laterally. We also found that these bees have a greater chance of stigma contact because of their large size. Some of the smaller species of Anthophora, Perdita, and some syrphid rarely contacted the stamens because of their small body sizes. Most pollen that contacted these species was deposited on the dorsal surface of the insects, and consequently it had a very low probability of contacting the stigma.

Table 2. Data summary for Arctomecon merriamii (ARME). AVG. TOTAL TOTAL AVG. AVG. POLLINATOR ARME POLLINATOR OBS. SPECIMENS ARME POLLEN NAME POLLEN STATUS 2008–2009 COLLECTED POLLEN % COVER % COUNT (Bees) Anthophora sp. 2 0 NA NA NA NA Anthophora sp. 4 13 4 4.67 171 3.2 Likely Anthophora sp. 5 13 5 38.49 1,057 4.3 Likely Apis mellifera 16 3 99.76 721 6.8 Very Good Habropoda sp. 1 1 0.03 12 3.4 Poor Megachile fucata 2 2 19.98 9 1.8 Poor Perdita sp. 1 1 88.89 22 1.25 Poor Diptera Eupeodes sp. 1 1 47.92 3 1 Poor

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 13 to the Reproductive Fitness of 12 Rare Plants

Arctomecon merriamii was most commonly visited by two species of Anthophora and Apis mellifera (Table 2). We were unable to identify these Anthophora to species because no key to species exists. We, therefore, have separated these visitors into morphospecies 4 and 5. In addition to collecting pollen from A. merriamii, both morphospecies of Anthophora also visited the concurrently blooming Cryptantha. Anthophora morphospecies 4 had a greater percentage of Cryptantha pollen in its pollen load, suggesting that Cryptantha may be an important component of this species’ nest provision. Morphospecies 5 also had a high percentage of Cryptantha pollen, though the percentage was less than that of morphospecies 4. Apis mellifera also collected large amounts of A. merriamii pollen, but the species did not appear to visit Cryptantha. Based on the relative amount of A. merriamii pollen on the body, we have categorized A. mellifera as a very good pollinator and Anthophora morphospecies 4 and 5 as likely pollinators (Table 2).

Flies also commonly visited A. merriamii, and we observed that instead of interacting with the pistol and stamens, they spent the majority of their time “resting” on the petals. Anther contact was noted, but stigma contact was limited and not much pollen was observed on the flies’ bodies (Table 2).

We also collected a species of Habropoda, a robust bee closely related to Anthophora, from A. merriamii, though it did not noticeably contact the stamens. The pollen load was mostly Cryptantha pollen.

3.2.2 Astragalus phoenix

We noticed the first blooms on this plant in late January, though no bees were visiting the flowers at this time. To effect a pollination event, a bee must depress the keel of the flower, which exposes the stamens and stigma of the flowers. We observed two populations of A. phoenix during the 2008 field season, but noted very little pollinator activity at one of them; we therefore focused much of our effort on collecting data from the other site. We observed A. porterae visiting the flowers of A. phoenix during the 2008 and 2009 seasons. Observations began during the 2008 season in mid-March. We noticed syrphid flies landing on A. phoenix, but we think the flies were there incidentally and were not able to collect floral resources. Early in the bloom season, A. porterae visited A. phoenix to the exclusion of all other plants, though as A. phoenix became senescent, A. porterae began to visit Cryptantha, which bloom coincidentally with A. phoenix. We found this same trend in 2009. We also found large amounts of unidentifiable pollen in the provisions of A. porterae, though this pollen was different between years.

In 2009 we began our observations in late January. The first visitor to A. phoenix was A. mellifera. The pollen analysis shows that A. mellifera was able to collect pollen from A. phoenix, but this was restricted to the corbiculae. Because the pollen was restricted to the corbiculae, and because A. mellifera had difficulty manipulating the flowers to access both stamens and stigma, it is unlikely that A. mellifera was a successful pollinator of A. phoenix (Table 3).

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 14 to the Reproductive Fitness of 12 Rare Plants

Table 3. Data summary for Astragalus phoenix (ASPH). AVG. TOTAL TOTAL TOTAL AVG. AVG. ASPH POLLINATOR POLLINATOR NAME OBS. OBS. SPECIMENS ASPH POLLEN POLLEN STATUS 2009 COLLECTED POLLEN % COVER % 2008 COUNT Hymenoptera (Bees) Anthophora porterae 15 44 16 63.38 872.09 2.18 Very Good Apis mellifera 4 2 93.72 642.1 2.07 Poor Diptera Syrphid, unknown 3 4 0 NA NA NA Poor

The most common visitor during the 2009 season was A. porterae (Table 3). As in 2008, A. porterae was able to successfully manipulate the flowers of A. phoenix and effect multiple pollination events. In late May 2008 we located a nesting population of A. porterae and extracted a pollen provision. This population was in an area with a large Cryptantha population and a diffuse A. phoenix population. An analysis of the pollen provision showed that the pollen was primarily collected from Cryptantha. These data suggest that Cryptantha contributes significantly to the fitness of A. porterae. Further, the data from our behavioral observations and the pollen analysis suggest that A. porterae is the only visitor that can successfully pollinate A. phoenix.

3.2.3 Calochortus striatus

Calochortus striatus is visited by a great many insects, indeed, more than many other rare plants at the Refuge; few of these, however, are likely to successfully pollinate it. Many of the bees and flies that visit C. striatus are relatively small and are able to access the nectaries and resin glands at the base of the petals without touching the exposed stamens or stigma. Consequently, many of the insects that visit C. striatus are considered poor pollinators (Table 4). Larger bees, however, such as angelicus/texanus, Anthidium cockerelli, and a wasp in the genus Chlorion were frequently observed interacting with the stamens and the stigma. The pollen analysis of these species showed a very high percentage of C. striatus pollen. Consequently, we feel that these species will be very good pollinators. Also, we observed vallicola, Halictus ligatus, and a species of Dialictus collecting pollen, and our pollen analysis has identified these as good pollinators.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 15 to the Reproductive Fitness of 12 Rare Plants

Table 4. Data summary for Calochortus striatus (CAST). AVG. AVG. AVG. TOTAL TOTAL TOTAL CAST CAST POLLEN POLLINATOR POLLINATOR NAME OBS. OBS. SPECIMENS POLLEN POLLEN COVER STATUS 2008 2009 COLLECTED % COUNT %

Hymenoptera (Bees) Agapostemon 18 7 10 88.64 833 3.9 Very Good angelicus/texanus Agapostemon melliventris 4 1 0 0 0 Poor Anthidium cockerelli 1 1 93.44 268 2.29 Very Good Anthophora sp. 1 0 NA NA NA NA Anthophora sp. 6 1 1 18.89 94 1.13 Poor Ashmediella aridula 7 7 62.7 69 1.7 Likely Ashmediella gillettei 1 1 NA NA NA NA Ashmediella rufipes 1 1 NA NA NA NA Ashmediella sp. 1 1 1 5.26 1 2.2 Poor Ashmediella sp. 2 1 1 50 0.5 1 Poor Ashmediella sp. 1 or 2 75 NA NA NA Poor Diadasia diminuta 3 3 65.54 176 3.21 Likely Diadasia vallicola 3 3 82.44 232 2.76 Good Dialictus sp. 1 NA NA NA Good Dialictus sp. 1 2 2 80.58 13 1.8 Good Dialictus sp. 4 1 1 86.49 32 1.2 Good Halictus ligatus 6 2 76.2 573 4.4 Good Melissodes sp. 3 1 1 54.66 92 2 Likely Halictid unknown 1 1 97.44 61 3 Poor Hymenoptera (Wasp) Chlorion sp. 2 1 95.99 605 2.5 Very Good Diptera Eupeodes sp. 3 1 0 0 2 Poor Proboscimyia sp. 7 7 43.75 5 1.33 Poor Scaeva sp. 1 1 0 0 0 Poor Tachinidae 9 6 100 2.75 1 Poor Other Coleoptera unknown 1 1 46.14 10 1 Poor Buprestid 8 4 32.78 18 1 Poor

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 16 to the Reproductive Fitness of 12 Rare Plants

3.2.4 Centaurium namophilum

We collected many insects visiting C. namophilum, including ten bee species and five fly species. The most common visitors to C. namophilum were Megachile lippiae, Agapostemon angelicus/texanus, Apis mellifera, a species of Dialictus, and a bee species in the tribe Eucerini (Table 5). We frequently observed M. lippiae and A. mellifera interacting with the flowers of C. namophilum and contacting the stamens and pistols. Our pollen analysis showed that both bees carried a lot of pollen. Megachile lippiae stores pollen on the ventral side of its abdomen, which gives the pollen greater chance of being transferred to another flower than pollen that has been stored on the corbiculae of the legs. Consequently, if pollinator-mediated reproduction is important to C. namophilum, then M. lippiae and A. mellifera are very good pollinators (Table 5). Likewise, the eucerine species makes frequent visits to C. namophilum, contacts the stamens and pistols, and collects a lot of pollen, which may be located on the ventral surface of the body. The relative percentage of C. namophilum pollen on the body of this bee, however, is less than that on the body of either M. lippiae or A. mellifera. Consequently, we have classified this species of bee as a good pollinator (Table 5).

The bee A. angelicus/texanus makes frequent visits to C. namophilum, contacts both the stamens and the stigma, and collects lots of pollen, which may be located on the ventral surface of the body; however, some specimens we collected had a very high proportion of other plant pollen on their bodies. This may inhibit their efficiency as pollinators of C. namophilum. Consequently, we consider A. angelicus/texanus a good pollinator (Table 5).

Finally, the species of Dialictus we collected from C. namophilum, while much smaller than other bees, made frequent visits, contacted both the stamens and the stigma, and had pollen located on the regions of its body that contacted the stigma. Consequently, we consider this species of Dialictus to be a very good pollinator (Table 5).

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 17 to the Reproductive Fitness of 12 Rare Plants

Table 5. Data summary for Centaurium namophilum (CENA). AVG. AVG. TOTAL TOTAL TOTAL AVG. POLLINATOR CENA CENA POLLINATOR OBS. OBS. SPECIMENS POLLEN NAME POLLEN POLLEN STATUS 2008 2009 COLLECTED COVER % % COUNT Hymenoptera (Bees) Agapostemon 10 1 NA NA NA NA melliventris Agapostemon 7 8 3 73.62 2,092 6.29 Good angelicus/texanus Apis mellifera 12 4 4 98.16 1,217 4 Very Good Dialictus sp. 1 9 4 3 100 914 4.87 Very Good Dialictus sp. 3 1 1 NA NA NA NA Eucerini sp. 1 9 6 84.52 1,411 5.05 Good Megachile fortis 1 1 99.38 1,604 6.5 Very Good Megachile lippiae 18 2 10 99.31 1,361 5.49 Very Good Melissodes sp. 1 1 1 35 17 2.2 Poor Hymenoptera (Wasp) Vespid, unknown, 3 1 99.22 111 1 Very Good brown/yellow Diptera Heterostylum sp . 2 2 1 0 0 1.5 Poor Gymnosoma sp. 1 1 2.27 1 1 Poor Poecilanthrax sp. 1 1 0.42 1 1.67 Poor Diptera, unknown 1 1 90 9 1 Poor Syrphid, unknown 1 1 2 20.36 2 1 Poor Coleoptera Coccinellidae 1 1 20 1 1 Poor

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 18 to the Reproductive Fitness of 12 Rare Plants

3.2.5 Cordylanthus tecopensis

As with Astragalus phoenix, the and pistils of Cordylanthus tecopensis are located within a compartment made by the petals. To access the interior of the flower, one of the petals must be depressed; consequently, not all insects that visit this flower will be successful at transferring pollen. Indeed, only insects capable of depressing the appropriate petal while inserting their head into the flower will be successful at pollen transfer.

The most common visitor to C. tecopensis was a species of the bee genus Melissodes (sp. 1; see Table 6). This bee was successful at opening the flower and accessing the pollen. The dorsal side of the head and thorax of this bee had large amounts of C. tecopensis pollen; additionally, the pollen analysis showed many provisions from this bee that were 100% C. tecopensis pollen. Consequently, we consider this bee a very good pollinator (Table 6). Further, C. tecopensis appears to be an important source of pollen for this bee when it is provisioning its nest.

Table 6. Data summary for Cordylanthus tecopensis (COTE). AVG. TOTAL TOTAL TOTAL AVG. AVG. POLLINATOR COTE POLLINATOR OBS. OBS. SPECIMENS COTE POLLEN NAME POLLEN STATUS 2008 2009 COLLECTED POLLEN % COVER % COUNT Hymenoptera (Bees) 0 2 2 100 236 2.5 Very Good clypacthidium Anthophora sp. 1 1 0 1 99.69 1057 2.67 Very Good Melissodes sp. 1 34 16 27 89.54 125 2.37 Very Good Melissodes sp. 2 2 0 2 80.72 78 2.36 Good Dialictus sp. 1 1 98.76 99 1.46 Poor Dialictus sp. 1 1 3 1 0 0 1 Poor Dialictus sp. 4 0 9 1 75 10 1.08 Poor Coleoptera Corimelaena sp. 3 5 24 100 4 1.12 Poor

Anthidiellum clypacthidium and a species of Anthophora are able to manipulate the flower properly, contact the stamens and stigma, and pick up adequate amounts of pollen. Although these bees were not observed in great numbers, they are still listed as very good pollinators (Table 6).

We observed a second species of Melissodes (sp. 2 in Table 6) visiting C. tecopensis, though this species was much less common than Melissodes sp. 1. Melissodes sp. 2 is also capable of correctly manipulating the flower to access the stamens. The pollen analysis for this species U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 19 to the Reproductive Fitness of 12 Rare Plants

revealed a provision with very little C. tecopensis pollen, though in amounts high enough to facilitate pollination. Consequently, we consider this bee to be a good pollinator (Table 6).

Finally, we observed 2 species of Dialictus visiting C. tecopensis. Dialictus, however, is a very small bee and incapable of accessing the interior of the flower. We, therefore, consider the bees from this genus to be poor pollinators of C. tecopensis (Table 6).

3.2.6 Enceliopsis nudicaulis var. corrugata

We collected more insects from E. nudicaulis var. corrugata than from any other species of plant on the Refuge save Prosopis. We consider this to be one of the most important plants for the fitness of the Refuge’s pollinator community. It produces copious amounts of nectar and pollen and attracts a broad array of insects.

Because of the morphology of its flower, most insects that land on E. nudicaulis var. corrugata will successfully contact both the stamens and the stigmas. Most bees that we collected from E. nudicaulis var. corrugata are very good pollinators (Table 7); we consider Anthidium damnersi, Apis mellifera, and Lassioglossum sisyurbrii to be likely pollinators because we were unable to recover much E. nudicaulis var. corrugata pollen in the pollen analysis. The ants and wasps lack the pubescence of bees and are not as good at carrying pollen. With the exception of Pedalonia, we consider all wasps and ants poor pollinators for this plant (Table 7).

We collected 15 species of fly visiting E. nudicaulis var. corrugata. Of these, four species are considered very good pollinators and one is considered a good pollinator (Table 7).

Table 7. Data summary for Enceliopsis nudicaulis var. corrugata (ENNUC). AVG. TOTAL TOTAL TOTAL AVG. AVG. POLLINATOR ENNUC POLLINATOR OBS. OBS. SPECIMENS ENNUC POLLEN NAME POLLEN STATUS 2008 2009 COLLECTED POLLEN % COVER % COUNT Hymenoptera (Bees) Agapostemon 12 37 12 83.62 415 4.52 Good angelicus/texanus Agapostemon 4 5 4 95 57 1 Very Good melliventris Ancylandrena larrea 1 1 99.44 2,289 10.2 Very Good Anthidium cockerelli 2 2 97.23 116 1.71 Very Good Anthidium damnersi 1 1 67.65 62 2 Likely Anthophora sp. 1 1 95.9 91 3.67 Very Good Anthophora sp. 3 3 65 6 92.03 35 3.42 Very Good Apis mellifera 6 2 6 68.89 312 6.15 Likely Ashmediella rufipes 31 1 82.76 24 2 Good

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 20 to the Reproductive Fitness of 12 Rare Plants

Table 7. (Cont.) AVG. TOTAL TOTAL TOTAL AVG. AVG. POLLINATOR ENNUC POLLINATOR OBS. OBS. SPECIMENS ENNUC POLLEN NAME POLLEN STATUS 2008 2009 COLLECTED POLLEN % COVER % COUNT Atoposmia enciliaea 2 2 96.76 524 7 Very Good Colletes sp. 1 3 50 4 98.7 388 6.64 Very Good Diadasia australis 2 2 73.81 847 9.18 Good Diadasia diminuta 1 1 98.76 99 1.17 Very Good Dialictus sp. 15 NA NA NA NA Epeolus mesillae 4 4 99.36 440 5.33 Very Good Epeolus minimus 2 2 91.73 232 1.5 Very Good Halictus ligatus 1 8 2 98.06 255 6.5 Very Good Hoplitis biscutellae 2 3 83.72 291 5.02 Good Lassioglossum 1 1 70.49 207 4.4 Likely sisyurbrii Megachile fucata 4 4 96.92 225 4.75 Very Good Megachile xerophila 3 3 5 77.63 124 4.33 Good Megachilid, 1 1 65 13 2.67 Likely unknown, small Melissodes sp. 1 3 3 87.1 121 3.75 Good Stelis sp. 1 1 100 83 1 Very Good Hymenoptera (Wasps) Pedalonia sp. 5 1 4 81.25 308 2.42 Good Scoliidae 1 0 0 0 Poor Vespid, unknown 1 1 22.26 168 3.17 Poor Wasp, unknown, 1 1 100 7 1.22 Poor small Hymenoptera (Ant) Formicidae 3 0 100 11 1.44 Poor Diptera Eristalis sp. 2 2 85.57 934 6 Good Eupeodes volucris 8 5 9 77.51 146 1.37 Good Syrphid (likely the 1 70 NA NA NA NA Eupeodes) Geron sp. 3 3 0 0 0 Poor Gymnosoma sp. 1 2 1 0 0 0 Poor Lordotus sp. 7 2 7 95.94 82 1.33 Very Good Nimioglossa 3 1 3 92.53 85 1.5 Very Good planicosta Oligodranes sp. 2 4 1 0 0 0 Poor Phthiria sp. 2 2 97.8 56 1 Very Good Scaeva pyrasti 1 1 47.21 71 1.08 Poor

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 21 to the Reproductive Fitness of 12 Rare Plants

Table 7. (Cont.) AVG. TOTAL TOTAL TOTAL AVG. AVG. POLLINATOR ENNUC POLLINATOR OBS. OBS. SPECIMENS ENNUC POLLEN NAME POLLEN STATUS 2008 2009 COLLECTED POLLEN % COVER % COUNT Zodion sp. 1 1 89.99 52 1.33 Very Good Tracusa larreae 1 1 6.014 191 3.17 Poor Bombyliid, unknown 1 12 0 77.78 21 1 Poor Chloropidae 1 2 87.5 7 7 Good Chrysanthrax sp. 1 1 0 0 0 Poor Coleoptera Buprestid 7 3 11 90.61 130 2.39 Good Cleridae 1 1 42.93 41 3 Poor (Coleoptera) Coleoptera, 6 21 8 78.39 18 1.17 Poor unknown Hesperiidae 2 1 2 0 0 0 Poor Hopper 1 0 0 0 Poor Lycaendiae 7 4 8 0 0 0 Poor Pieridae 1 1 1 85.9 9 1 Poor Other Acrididae 1 1 0 0 0 Poor (grasshopper) Arachnid 4 2 3 0 0 0 Poor Lygaediae 2 0 0 0 Poor (immature) Thripidae 2 2 100 23 2.5 Poor

3.2.7 Grindelia fraxino-pratensis

Like Enceliopsis nudicaulis var. corrugata, Grindelia fraxino-pratensis is a member of the family; has an open, compound flower; and most insects that land on the flower head will be capable of transferring pollen. All bees that we collected from G. fraxino-pratensis were either very good or good pollinators (Table 8). Most notable among the pollinators of G. fraxino- pratensis are Apis mellifera and a species of Melissodes. These species carry a very high proportion of G. fraxino-pratensis pollen in their provisions and visit the flowers of G. fraxino- pratensis very frequently. Consequently, we consider both bees to be very good pollinators (Table 8).

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 22 to the Reproductive Fitness of 12 Rare Plants

Table 8. Data summary for Grindelia fraxino-pratensis (GRFR). AVG. TOTAL TOTAL TOTAL AVG. AVG. POLLINATOR GRFR POLLINATOR OBS. OBS. SPECIMENS GRFR POLLEN NAME POLLEN STATUS 2008 2009 COLLECTED POLLEN % COVER % COUNT Hymenoptera (Bees) Anthophora sp. 1 1 1 99.99 1,365 7.67 Very Good Apis mellifera 1 48 6 96.64 1,181 3.18 Very Good Ashmediella 1 2 2 99.97 184 5.86 Very Good melliloti Ashmediella 1 1 92.59 50 3 Very Good rufipes Coelioxis erysimi 1 0 1 83.85 58.5 2.5 Good Diadasia 14 13 88.32 2,251 8.21 Very Good envervata Dialictus sp. 1 1 1 100 2,084 2.2 Good Halictus ligatus 1 1 98.41 129 4 Very Good Megachile 3 2 77.8 1,242 4.56 Good lippiae Megachile 5 4 80.6 1,497 4.71 Good parallela Melissodes sp. 1 7 5 93.74 1,4445 6.48 Very Good Melissodes sp. 2 1 2 98.29 592 3.44 Very Good Melissodes sp. 3 3 3 99.42 1,393 6.53 Very Good Perdita new sp. 8 13 21 81.87 584 3.66 Good Perdita sp.1 3 4 100 126 2.54 Good Hymenoptera (Wasp) Sphex sp. 1 1 50 2 1 Poor Hymenoptera (Ant) Formicidae 1 1 100 135 5 Good Diptera Lygaeidae 1 100 4 1 Poor (Hemiptera) Reduviidae 1 1 100 21 1 Poor (Hemiptera)

Species in the genera Perdita and Dialictus are also frequent visitors to G. fraxino-pratensis. Species from both genera have pollen provisions with a very high percentage of G. fraxino- pratensis pollen. We have classified bees in these genera as good pollinators (Table 8) because small bees may be less likely than large bees to visit flowers from multiple plants and plants in different populations. We will note, however, that we discovered a new species of Perdita that is endemic to the Refuge and visits G. fraxino-pratensis.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 23 to the Reproductive Fitness of 12 Rare Plants

The number of visits and the pollen analysis suggest that ants may also be good pollinators for this plant (Table 8). While there was only a single observation of this insect, it is still considered a good pollinator because of the relative amount of G. fraxino-pratensis pollen recovered from its body, but not a very good pollinator because it did not move between plants.

3.2.8 Ivesia kingii var. eremica

The most frequent visitors to Ivesia kingii var. eremica are flies from the family . We observed species from four genera of bombyliid flies, Villa, Exoprosopa, Crysanthrax, and Lepidanthrax. Some specimens of Villa had enough I. kingii var. eremica pollen to effect a pollination event, though most did not; many specimens were also carrying large amounts of pollen from other plants. We, therefore, consider Villa a poor pollinator (Table 9). Exoprosopa occasionally had very high quantities of I. kingii var. eremica pollen on the ventral surface of its body. We, therefore, consider Exoprosopa to be a likely pollinator (Table 9). We recovered very little pollen from either Crysanthrax or Lepidanthrax, and have classified these as poor pollinators.

We also collected five bee species from I. kingii var. eremica, though they do not visit the plant as frequently as the flies. The pollen analysis showed that these bees have a very high percentage of I. kingii var. eremica pollen in their provision. We have, therefore, classified the bees that visit I. kingii var. eremica as good pollinators (Table 9).

Table 9. Data summary for Ivesia kingii var. eremica (IVKI). AVG. TOTAL TOTAL TOTAL AVG. AVG. POLLINATOR IVKI POLLINATOR OBS. OBS. SPECIMENS IVKI POLLEN NAME POLLEN STATUS 2008 2009 COLLECTED POLLEN % COVER % COUNT Hymenoptera (Bees) Apis mellifera 4 3 2 99.25 1,505 3.15 Good Ashmediella 2 2 99.99 6,970 5.17 Good bigelovia Ashmediella 2 2 100 2,250 2.57 Good leucozona Dialictus sp. 1 8 4 99.84 1,168.8 4.05 Good Dialictus sp. 3 4 4 99.98 3,002.8 5.12 Good Hymenoptera (Wasps) Wasp, tiny 1 1 97.65 83 1.25 Very Good Wasp, unknown 1 1 55.16 145.7 1.33 Likely

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 24 to the Reproductive Fitness of 12 Rare Plants

Table 9. (Cont.) AVG. TOTAL TOTAL TOTAL AVG. AVG. POLLINATOR IVKI POLLINATOR OBS. OBS. SPECIMENS IVKI POLLEN NAME POLLEN STATUS 2008 2009 COLLECTED POLLEN % COVER % COUNT Diptera Crysanthrax mira 4 3 2 100 12 1 Poor Exoprosopa sp. 13 13 4 66.24 159 1 Likely Syrphid, 1 1 100 106 1 Very Good unknown, yellow Lepidanthrax sp. 9 11 5 65.14 10 1 Poor Villa sp. 16 4 6 68.43 108 1.67 Poor Coleoptera Buprestid 3 1 100 6 1 Likely Coleoptera, tiny 2 2 2 83.33 1.5 1 Likely

3.2.9 Mentzelia leucophylla

As mentioned earlier, Mentzelia leucophylla is unique among the rare plants of the Refuge in that its flowers do not open until dusk and they remain open for a only few hours. This occurs when the nectar and pollen reserves for many other flowers have been exhausted. Consequently, M. leucophylla does not compete with many plants for pollination services. The flowers have an open morphology that allows most visiting insects to access the pollen and nectaries. We have found that larger insects interact with the flowers such that pollen is distributed primarily across the ventral side of their bodies. Smaller insects, however, are likely to have pollen distributed on both the ventral and dorsal surfaces of the bee.

The genera Dialictus and Perdita were the most commonly observed visitors on M. leucophylla. The pollen analysis showed that the provisions of these bees contained a high proportion of M. leucophylla pollen, suggesting they visit few other plants while visiting M. leucophylla. This is not overly surprising as they are relatively small bees, are not likely to fly very far, and there is little else blooming at the same time or in the same place as the populations of M. leucophylla that we observed. Consequently, we have categorized all of the species of Dialictus that visit M. leucophylla, and that we were able to recover pollen from, as very good pollinators and the Perdita species as good pollinators (Table 10). We should also note that we discovered a new species of Perdita that visits M. leucophylla and appears to be endemic to the Ash Meadows area.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 25 to the Reproductive Fitness of 12 Rare Plants

Table 10. Data summary for Mentzelia leucophylla (MELE). AVG. TOTAL TOTAL TOTAL AVG. AVG. POLLINATOR MELE POLLINATOR OBS. OBS. SPECIMENS MELE POLLEN NAME POLLEN STATUS 2008 2009 COLLECTED POLLEN % COVER % COUNT Hymenoptera (Bees) Agapostemon 24 28 9 99.81 1,286 3.82 Very Good angelicus/texanus Agapostemon 2 2 99.95 1,761 4.83 Very Good melliventris Anthidium 1 92.76 4,070 3.28 Very Good cockerelli Anthidium sp. 1 1 1 97.68 523 4.22 Very Good Anthophora sp. 4 1 81.63 1,543 3.82 Good Apis mellifera 18 3 6 99.62 1,073 4.12 Very Good Dialictus sp. 1 100 473 3.17 Very Good Dialictus sp. 1 5 5 15 99.52 544 2.58 Very Good Dialictus sp. 3 7 2 99.9 986 4.49 Very Good Dialictus sp. 4 4 2 NA NA NA NA Dialictus 50 235 NA NA NA NA sp./Perdita sp. Dianthidium 1 1 99.9 986 1.06 Very Good implicatum Dianthidium sp.1 1 1 NA NA NA NA Halictid 1 1 100 813 3.24 Very Good Hesperapis 1 1 1 40.81 398 3.33 Poor laticeps Lassioglossom/ 3 1 3 99.9 1,173 4.31 Very Good Dialictus Lassioglossom/ 10 6 98.39 652 4.09 Very Good Dialictus sp. 2 Megachile lippiae 6 4 1 76.7 1,539 6.44 Good Megachile 17 1 5 82.07 720 4.35 Good lobalifrons Perdita new sp. 7 5 99.95 125 1.47 Good Perdita sp. 3 2 3 79.06 451 1.67 Good Hymenoptera (Wasp) Pyilanthus 1 1 98.77 322 1 Very Good gibbussus Diptera Copestylym sp. 1 79.32 192 1.25 Good Eristalis sp. 4 1 70.56 391 5.88 Likely

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The only bee to be categorized as a poor pollinator was Hesperapis laticeps; the remaining bees were either considered very good or good pollinators (Table 10). Most notable among these are Agapostemon angelicus/texanus and Apis mellifera, which are both categorized as very good pollinators. Both of these bees were frequent visitors and the pollen analysis showed high floral constancy. Megachile lobalifrons and a species of Anthophora were also frequent visitors. They frequently moved between flowers and M. leucophylla plants, though the pollen analysis showed a lower proportion of M. leucophylla pollen than we observed in either Agapostemon angelicus/texanus or Apis mellifera. Consequently, we categorize these as good pollinators (Table 10).

3.2.10 Nitrophila mohavensis

Nitrophila mohavensis is a small plant with inconspicuous red flowers that exhibits many characteristics of ant-pollinated plants (Rico-Gray and Oliveira 2007). We observed ants visiting the flowers of N. mohavensis, but we were unable to verify that they were contacting both stamens and stigma. We collected ants visiting N. mohavensis from two genera, Tapinoma and Linepithema. These ants did not vary in how they interacted with the flowers of N. mohavensis. The ants would walk up and down the small plants until finding a flower. They would then go inside the flower for up to 60 seconds. We have categorized Tapinoma and Linepithema as likely pollinators of N. mohavensis (Table 11), though it is unlikely that pollinator-mediated reproduction contributes significantly to the fitness of the species.

We noted other organisms on N. mohavensis, though they were likely there incidentally (Table 11).

Table 11. Data summary for Nitrophila mohavensis (NIMO). TOTAL AVG. NIMO POLLINATOR TOTAL OBS. AVG. NIMO AVG. POLLINATOR SPECIMENS POLLEN NAME 2008–2009 POLLEN % PLACEMENT % STATUS COLLECTED COUNT Hymenoptera (Ants) Linepithema sp. 36 9 100.0 2.0 3.0 Poor Tapinoma sp. 44 18 56.0 1.7 1.7 Poor Hymenoptera (Bee) Dialictus sp. 4 16 1 0.0 0.0 0.0 NA

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3.2.11 Sisyrinchium spp.

We observed very few insects on the flowers of Sisyrinchium; indeed, the most frequent visitor was a small buprestid beetle that was there incidentally. We observed few bees interacting with the flowers, and those that did collected very little pollen with the exception of one specimen of Anthidiellum notatum. The pollen analysis of this bee showed very high floral constancy to Sisyrinchium and over 5000 grains of pollen on its body. The remaining bees either had very little pollen on their bodies or provisions that consisted of less than 25% Sisyrinchium pollen. Consequently, we have categorized all insects that visit Sisyrinchium as poor pollinators (Table 12).

Table 12. Data summary for Sisyrinchium spp. (SISYR). AVG. TOTAL TOTAL TOTAL AVG. AVG. POLLINATOR SISYR POLLINATOR OBS. OBS. SPECIMENS SISYR POLLEN NAME POLLEN STATUS 2008 2009 COLLECTED POLLEN % COVER % COUNT Hymenoptera (Bees) Anthidiellum notatum 2 2 49.38 352 1.88 Poor Anthophora sp. 1 1 1 14.48 2,68.71 5.8 Poor Ashmediella aridula 1 1 26.75 1,536.5 3 Poor Perdita sulphurea, 1 50 1 1 Poor male Diptera Syrphus sp. 1 6 2 63.18 5 1 Poor Other Buprestid 16 13 61.08 13.63 1.13 Poor (Coleoptera)

3.2.12 Spiranthes infernalis

The pollen of S. infernalis is located within a pollinium, and it is unclear how much it contributes to the fitness of the bees collecting it. All of the bees we observed visiting S. infernalis very likely offer the plant some pollination services; they were large bees and all were fitted with a pollinium on the proboscis by the S. infernalis flower. The most frequent visitor to S. infernalis was Apis mellifera, which shows very high floral constancy and spends a considerable amount of time foraging within a patch of S. infernalis flowers. We have classified A. mellifera, therefore, as a very good pollinator (Table 13). Also of note, the species of Melissodes that we collected on S. infernalis was the same species that we collected on Grindelia fraxino-pratensis. This species of Melissodes also exhibited good floral constancy and was observed visiting many flowers on multiple plants. We have also categorized this bee as a very good pollinator (Table 13).

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Table 13. Data summary for Spiranthes infernalis (SPIN). AVG. AVG. AVG. TOTAL TOTAL TOTAL POLLINATOR SPIN SPIN POLLEN POLLINIA POLLINATOR OBS. OBS. SPECIMENS NAME POLLEN POLLEN COVER PRESENT STATUS 2008 2009 COLLECTED % COUNT % Hymenoptera (Bees) Anthophora 1 1 80.67 918.00 1.5 Yes Good sp. 1 Apis mellifera 28 6 94.91 4,484 1.42 Yes Very Good Centris 7 5 78.72 1,974 1.6 Yes Good rhodopus Eucerini sp. 1 3 1 99.33 4,305 4.5 Yes Very Good Megachile 6 3 94.91 3,246 1.42 Yes Very Good lippiae Melissodes 3 3 99.92 5,570 1.5 Yes Very Good sp. 1

3.3 Discussion

As with most large, complex data sets, it is difficult to make general conclusions from our data regarding the importance of the Refuge’s pollinators to its rare plants. Consequently, in this section we will discuss the relative importance of the pollinators to each rare plant, discuss the importance of the rare plants to the pollinator community, and comment on the attention that each deserves. Additionally, we will identify bees that many of the rare plants share for pollination services so that conservation efforts for these critical pollinators may be considered.

Arctomecon merriamii requires pollination services for successful reproduction (Pavlik 2007, pers. comm.), and it is only successfully pollinated by larger bees, as small bees are able to arrive at the nectaries without touching the exposed stamens and stigma. The bees that visit A. merriamii also visit other plants on the Refuge and are consequently not solely dependent on A. merriamii for forage. Most notably, A. merriamii is pollinated by Apis mellifera. Anthophora species construct solitary nests in the ground, and A. mellifera constructs large hives in the cavities of trees and rocks. Therefore, Refuge staff should consider measures to protect A. merriamii and its pollinators. These measures should include, but are not limited to, conserving the integrity of the soils in and around populations of A. merriamii and natural cavities throughout the Refuge.

Astragalus phoenix is also a plant that seems to require pollination services for successful reproduction (Pavlik 2007, pers. comm.). While A. phoenix is visited by a variety of insects, it is only successfully pollinated by Anthophora porterae, which nests communally in loose sandy soils. As this plant is endemic to the Ash Meadows area, and since the Refuge’s population of A. porterae seems to depend heavily on A. phoenix in early spring for forage, we suggest Refuge staff make special considerations for A. phoenix and its pollinator, A. porterae. These

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considerations ought to include, though not be limited to, more extensive surveys for nesting populations of A. porterae. Although we conducted many surveys for this bee, we were unable to survey its entire potential habitat because we were conducting observations on and surveys for other plants blooming concurrently with Astragalus phoenix. In addition to conserving the habitat of A. phoenix, special effort ought to be invested into conserving the habitat of existing nesting populations and potential habitat of A. porterae. Locating nests of A. porterae will require exhaustive surveys. The nests will appear as holes approximately 1.5 cm in diameter in the soil. Potential habitat will include sand dunes and the areas surrounding dunes not seasonally inundated with water; areas that have extant populations of A. phoenix, Cryptantha, or both; and land extending approximately 300 m out from these areas. Anthophora porterae is a large bee capable of flying up to 1 kilometer while foraging, so a 300 m area around extant populations of known forage is a conservative estimate of potential nesting habitat.

Calochortus striatus is visited by many bees, and as with many other lilies it seems to use insect- mediated pollination for reproduction. Larger bees seem to be the most effective at pollinating C. striatus, because many smaller bees are able to access the nectaries and resin glands without touching the stamens or stigma. Because C. striatus is visited by many bees, and because many of its pollinators visit other plants concurrently in bloom with C. striatus, its pollinators do not require additional consideration.

Centaurium namophilum is visited by many bees, but it is unlikely that pollinator-mediated reproduction is important to its reproductive fitness (Pavlik 2007, pers. comm.). The bees that visit C. namophilum also visit other, concurrently blooming plants on the Refuge, including some rare plants. Because C. namophilum may be an important source of forage for important pollinators of other rare plants, we strongly suggest that habitat for C. namophilum be avoided during restoration activities, though no additional considerations need be made for its pollinators.

Cordylanthus tecopensis is visited by many species of bees, though only bees capable of manipulating the flowers successfully access floral resources. It appears unlikely that C. tecopensis requires pollination for successful reproduction, because pollinator-exclusion experiments produced fruit yields that were similar between plants from which pollinators were excluded and those that had access to pollination services (Pavlik 2007, pers. comm.). Melissodes sp.1 also visits other rare plants, namely Enceliopsis nudicaulis var. corrugata, Grindelia fraxino-pratensis, and Spiranthes infernalis. It may be that C. tecopensis is an important source of forage for this species of bee. Unfortunately, very little is known about the natural history of Melissodes, and bees in the genus are notoriously difficult to identify. We suggest, therefore, that fundamental research be conducted on Melissodes sp.1 and the extent to which it depends on C. tecopensis as a source of forage. Finally, while it may be that C. tecopensis does not depend exclusively on insect-mediated pollination services for reproduction, pollination may play an occasional role in maintaining genetic diversity.

Enceliopsis nudicaulis var. corrugata is, perhaps, the most significant rare plant to the Refuge’s pollinator community because it provides floral resources to a great many insects. Indeed, E. U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 30 to the Reproductive Fitness of 12 Rare Plants

nudicaulis var. corrugata appears to be the first of the “cornucopia plants” to bloom each year on the Refuge (see Task 5). While pollination services are important to E. nudicaulis var. corrugata, it is successfully pollinated by so many insects that we do not recommend additional consideration for the insects that visit it, beyond conserving potential nesting habitat such as sand dunes.

Grindelia fraxino-pratensis, like E. nudicaulis var. corrugata, has an open flower morphology and is successfully pollinated by most of the insects that visit its flowers. The most notable of these, however, is the species of Melissodes that also visits C. tecopensis. The two plants occur in similar habitat and bloom at approximately the same time, and while it seems logical that this may lead to transfer of G. fraxino-pratensis pollen to C. tecopensis (or in the opposite direction), our pollen analysis shows that when visiting these plants this Melissodes species visits one to the exclusion of the other within a foraging trip (Tables 6 and 8). This species of Melissodes is a very good pollinator for both plants and an important source of pollination services. We suggest, therefore, that in the interest of conserving both plants additional research should be conducted on the natural history of Melissodes sp.1. The research may include a description of its natural history, ecological requirements, and evolutionary relationships to other species of Melissodes. It may be that both plants also play an important role in maintaining viable populations of the bee. Finally, we discovered a new species of Perdita on G. fraxino-pratensis that appears to be endemic to the Ash Meadows area. Because this species of Perdita is small, it likely nests near extant populations of G. fraxino-pratensis; we suggest, therefore, that areas near extant populations of G. fraxino-pratensis be avoided during restoration activities.

Ivesia kingii var. eremica does not require pollinators for reproduction, and the insects that visit it either visit other plants or none of the other rare plants. We, therefore, do not recommend additional consideration for the insects that visit this plant.

Mentzelia leucophylla is visited by a relatively broad guild of pollinators, many of which visit other rare plants. Because of the unique time of day that the flowers of M. leucophylla open, it does not compete with other concurrently blooming plants and consequently has very high pollinator fidelity. Many of the insects that visit M. leucophylla successfully pollinate it, and we do not feel that any of the insects that visit M. leucophylla require consideration beyond the preservation of bee habitat near extant populations of M. leucophylla. Finally, we also discovered a new species of Perdita on M. leucophylla. As with the new Perdita species found on G. fraxino-pratensis, this new Perdita species is small and likely nests near extant populations of M. leucophylla.

Nitrophila mohavensis is not dependent on insect-mediated pollination services for reproduction (Pavlik 2007, pers. comm.), and the insects that visit it do not require additional consideration.

The breeding system of Sisyrinchium spp. was not investigated by Pavlik et al. Consequently, we do not know if pollination services contribute to this plant’s reproductive fitness. It is unlikely, however, that the bees that visit Sisyrinchium spp. are effective pollinators. Sisyrinchium spp. U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 31 to the Reproductive Fitness of 12 Rare Plants

pollen represents only a small proportion of the total pollen in the provisions of these bees. The insects that visit Sisyrinchium spp., therefore, do not require additional consideration.

Spiranthes infernalis is visited by a narrow guild of bees, all of which can successfully pollinate it. Spiranthes infernalis is unique among the Refuge’s rare plants in that its pollen is contained within a pollinium and conferred to a visiting insect as a package of pollen rather than individual grains. Many orchids, Spiranthes included, place pollinia on the region of the body of visiting insects most likely to contact the pollen receptacle on the female flower; in this case, the pollinium is placed on the proboscis of the bees. Interestingly, and despite this adaptation for pollinator efficiency, Spiranthes infernalis does not appear to require pollination for successful reproduction (Pavlik 2007, pers. comm.). Consequently, we do not recommend conservation measures beyond those discussed below (see General Discussion and Recommendations).

3.3.1 Is There a Guild of Pollinators Uniquely Important to the Rare Plants of the Refuge?

Most of the pollinators that visit the rare plants of the Refuge do not require conservation measures beyond those discussed below (see General Discussion and Recommendations), but our data suggest that there exists a group of genera that visit many of the plants and, generally, are good pollinators. These genera are Anthophora, Apis, Dialictus, Megachile, and Melissodes. Keys to these genera can be found in A Field Guide to Insects: America North of Mexico (Borror and White 1998) or in The Bees of the World (Michener 2007). Each genus visits at least five of the rare plants and is a poor pollinator at no more than two of them (Table 14). We have seen that much of the existing variation in pollination behavior between bees occurs at the generic level, not the species level, so most bees within a genus will behave similarly at flowers and consequently be equally good at pollination. These data are based on the number of visitations we observed during the 2008 and 2009 field seasons and the relative amount of pollen from the rare plants in the provision.

Members of the genus Anthophora are solitary to communally nesting bees that prefer loose, sandy soils (Michener 2007). The nests of bees in this genus are typically 10 to 20 cm deep and terminate in multiple cells that contain an egg and a pollen/nectar provision. We collected six species of Anthophora in non-dune habitats, eight in dune habitats, and four in both dune and non-dune habitats. These bees were either collected from plants with an insect net or in pan traps. Anthophora bees are typically generalist foragers and will therefore utilize a broad range of plants to provision their nests. As a genus, Anthophora is a poor pollinator of Calochortus and Sisyrinchium, a likely pollinator of Arctomecon, a good pollinator of Mentzelia and Spiranthes, and a very good pollinator of Astragalus, Cordylanthus, Enceliopsis, and Grindelia (Table 14). Generally speaking, members of Anthophora are large, clumsy bees that, due to their body size and sometimes erratic behavior, frequently contact the stamens and pistol of a flower. To prevent, then, the loss of Anthophora from the Refuge, restoration activities should avoid areas with extant populations of flowering plants, areas with suitable nesting soils (such as dunes), and most importantly, avoid areas that have extant populations of Astragalus, Arctomecon, or both. U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 32 to the Reproductive Fitness of 12 Rare Plants

Table 14. Pollinator status of the primary pollinators in relation to the 12 rare plants of Ash Meadows National Wildlife Refuge. POLLINATORS a RARE PLANT SPECIES Anthophora Apis Dialictus Melissodes Megachile Arctomecon merriamii Likely Very Good ------Astragalus phoenix Very Good Poor ------Calochortus striatus Poor Very Good Very Good Likely --- Centaurium namophilum --- Likely Good Poor Very Good Cordylanthus tecopensis Very Good Very Good --- Very Good --- Enceliopsis nudicaulis var. Very Good Good Good Good Very Good corrugata Grindelia fraxino-pratensis Very Good Very Good Good Very Good Good Ivesia kingii var. eremica --- Good Good ------Mentzelia leucophylla Good Very Good Very Good --- Good Nitrophila mohavensis ------Sisyrinchium spp. Poor ------Spiranthes infernalis Good Very Good --- Very Good Very Good a Genus names only are given.

Members of the genus Apis are social bees that create colonies that may exceed 30,000 individuals. Apis bees nest in cavities (natural and man-made) and are generalist foragers. We only collected Apis mellifera in non-dune habitats. Unlike the other genera we discuss, Apis is not native to the Americas. It is an unfortunate tendency to assume that all non-native organisms are inherently destructive to local biota. This does not appear to be the case with Apis. While there have been considerable resources invested into studying the effect that the invasive Apis mellifera has on local bee populations, there are at best circumstantial data to suggest a negative effect. This is likely because pollen and nectar are not limiting resources, and Apis mellifera does not compete with native bees for nesting sites. Apis mellifera may impact local biota by assisting the spread of invasive weeds through offering pollination services, but little effort has been invested into this avenue of inquiry. Apis mellifera is a poor pollinator of Astragalus, a likely pollinator of Centaurium, a good pollinator of Enceliopsis and Ivesia, and a very good pollinator of Arctomecon, Grindelia, Mentzelia, and Spiranthes (Table 14). To prevent the loss of Apis mellifera, then, natural and historic cavities ought to be maintained, and Refuge staff should avoid the understandable desire to extirpate extant colonies on the Refuge that are not impacting staff or visitors.

The subgenus Dialictus is composed of many bees that are difficult to identify to species; indeed Dialictus is one of the larger groups of bees on the Refuge. They are very small and usually metallic green to brown. They are also ubiquitous; there are very few areas on the Refuge where we did not collect Dialictus. We collected three species of Dialictus in non-dune habitats, three

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 33 to the Reproductive Fitness of 12 Rare Plants

in dune habitats, and none were collected in both dune and non-dune habitats. Very little, however, is known about the natural history of these bees. They are similar in size to other twig- nesting bees, such as Ceratina and Ashmediella. The twigs Dialictus bees nest in may be as ephemeral as the fibrous stems of herbaceous plants, such as Cryptantha; the bees may also nest in the soil. As a genus, Dialictus is a good pollinator of Centaurium, Enceliopsis, Grindelia, and Ivesia, and a very good pollinator of Calochortus and Mentzelia (Table 14). We also observed Dialictus on Enceliopsis many times (Table 7), though we were unable to successfully recover pollen from the bees. We feel, however, that Dialictus is, at least, a likely pollinator of Enceliopsis. Because members of Dialictus are small bees, they likely nest close to their forage; therefore, we suggest that the areas in and around extant floral hosts of Dialictus be avoided during restoration activities.

Melissodes is a genus that belongs to the tribe Eucerini, which consists of medium-size to large bees, the males of which typically have antennae that exceed the length of the body. The bees in this genus are also notoriously difficult to identify, and the natural history of this group is poorly understood. As a genus, Melissodes is a poor pollinator of Centaurium, a likely pollinator of Calochortus, a good pollinator of Enceliopsis, and a very good pollinator of Cordylanthus, Grindelia, and Spiranthes. Many species of Melissodes nest in sandy and loose soils. We collected six species of Melissodes in non-dune habitats, seven in dune habitats, and three in both dune and non-dune habitats. Therefore, to conserve the populations of Melissodes on the Refuge, we recommend that restoration activities avoid suitable nesting habitat, such as sand dunes, and areas with extant populations of known floral hosts.

Finally, the genus Megachile ought to be a focus of concern for Refuge staff. Megachile belongs to the family , the leaf-cutting bees. Bees in this family nest individually, though many use extant cavities. Megachile bees line extant cavities with small segments of leaves that have been clipped from the surrounding vegetation. Many species of Melissodes nest in sandy, loose soils. We collected four species of Megachile in non-dune habitats, eight in dune habitats, and one in both dune and non-dune habitats. As a genus, Megachile is a good pollinator of Grindelia and Mentzelia, and a very good pollinator of Centaurium, Enceliopsis, and Spiranthes. Unlike most other bees, the pollen basket of Megachile bees is located on the ventral surface of the abdomen. Whereas the pollen in the pollen baskets of most other bees is no longer accessible for pollination (because it is compartmentalized on a portion of the legs that no longer interacts with the pistol), the pollen in the basket of Megachile bees still may contact the pistol. We have observed Megachile bees nesting in the stems of Creosote, and they are known to nest in galleries excavated by a variety of insects in a variety of trees. Additionally, Megachile bees are generalist foragers. To conserve the population of Megachile on the Refuge, therefore, restoration activities ought to avoid extant stands of woody vegetation if the proposed activities will damage the woody vegetation, particularly when these stands are adjacent to populations of flowering plants. Among other areas, woody vegetation around Collins Ranch, Bill Copeland Memorial Highway, and the Creosote dune should be avoided.

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4.0 TASK 5: IDENTIFY THE POLLINATORS OF OTHER CONCURRENTLY BLOOMING FLOWERS

4.1 Introduction

Many angiosperms flower intermittently, which makes the food base for many herbivorous and nectarivorous unreliable through time. While it is true that some nectar- and pollen- feeding insects have evolved close associations with plants, even to the extent that insect emergences are coincidental with the blooming of flowers, most flower-visiting insects lack these close associations. Consequently, relying on a single species of plant may prove to be an ecologically and evolutionary unstable strategy. Indeed, it may be, and often is, more advantageous for insects to have a broad floral host range, that collectively represents a temporally stable food source.

The rarity of a plant may also contribute to uncertainty in a nectarivorous ’s food base. The more spatially localized a plant population becomes the less important it may be to the fitness of its visitors. If a focus of land managers is to conserve rare plants and their pollinators, then we must also account for the affect that concurrently or successively blooming plants are having on the fitness of rare plants and their visitors. While these effects range from the competitive exclusion of one plant through the monopolization of pollinators to mutual benefit between plant species, our study looks only at the potential benefits of concurrently and sequentially blooming plants to rare plants.

Of unique importance are the “cornucopia” plants, or plants that support many animal visitors. These plants may support a majority of the flower-visiting insect species within an area by providing forage when there is little else blooming or supplemental forage when the nectar supply of the current host begins to wane. We wanted to know which, if any, of the potential cornucopia plants supported visitors of the Refuge’s rare plants.

4.2 Methods

4.2.1 Plant Identification

Before the beginning of the 2008 blooming season, we used a list of the Refuge’s plant species to identify plants that would be attractive to insects based on their floral morphology, floral color, floral size, and bloom time. With the exception of Stanleya, we selected plants with the following characteristics: an open flower morphology, such as that seen among the asters; flower color that varied from yellow to white (we excluded plants with flowers that were red or orange because many pollinating insects are incapable of seeing this range of the visual light spectrum); plants that are relatively large and presumably have nectaries and pollen sufficient to attract a large number of visitors; and plants that bloom intermittently and within the reasonable season of

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insect activity. The plants that met these criteria were Asclepias, Creosote, Enceliopsis, Grindelia, Helianthus, Prosopis, Salix, Salvia, Stanleya, and Tamarix.

4.2.2 Insect Collection

We collected insects in and around the cornucopia plants with selective netting and bowl traps. Prior to net collections and the beginning of insect activity on the days we collected insects visiting the cornucopia plants, we set out bowl traps within 10 m of the plots of these plants. We painted the bowl traps fluorescent blue, fluorescent yellow, and white; colors that are all attractive to nectarivorous insects. We filled the bowls with water mixed with a small amount of detergent. We left the bowls accessible to the insects until after insects stopped visiting the plants, which was typically early evening.

We also used an insect net to carefully collect insects from the plants. To the greatest extent possible, we gently laid the net over the plant and allowed the insects to fly up into the net. For insect groups that fly quickly and are easily disturbed from feeding, such as the bees, we swung a net quickly through the plant, which occasionally broke flowers or branches from the plant.

4.2.3 Insect Preservation and Identification

After the insects were collected, we returned with them to Utah State University and pinned and labeled the insects. The collection location, date, host plant, and collector were all noted. We then identified the bees at least to genus; we made species identifications when keys were available and expertise permitted.

4.3 Results

4.3.1 Asclepias

Asclepias is a large plant, typically over 1 m tall, and very attractive to a wide variety of insects. The flowers are small, though they typically produce copious amounts of nectar. The dominant insect we collected from Asclepias was a large spider wasp (family Pompilidae) from the genus Pepsis. As these wasps contribute little to the pollination of other plants, and not at all to the pollination of the Refuge’s rare plants, we will not consider them here. We collected 13 species of bee from Asclepias: one species of , one species of Perdita, two species of Centris, one species of Habropoda, one species of Diadasia, one species of Ericrosis (E. lata), one species of Xeromolecta, one species of Agapostemon (A. melliventris), one species of Ashmediella (A. aridula), and three species of Megachile (including M. lippiae).

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 36 to the Reproductive Fitness of 12 Rare Plants

4.3.2 Creosote

Creosote is a large shrub that commonly exceeds 2 m in height and diameter. The yellow flowers of Creosote are small but have an open architecture. Creosote is known to support a diverse bee assemblage, with many Creosote specialists. We collected 10 species of bee from Creosote: one species of Perdita, one species of Apis (A. mellifera), two species of Centris, three species of Colletes, one species of Hylaeus, one species of Ashmediella, and one species of Atoposmia.

4.3.3 Enceliopsis

Enceliopsis is an herbaceous plant that produces many open, yellow, radial flowers that are very attractive to many insects. We collected 26 bee species from Enceliopsis: two species of Agapostemon (A. melliventris and A. angelicus/texanus), two species of Larrea, two species of Anthidium (A. cockerelli and A. damnersi), two species of Anthophora, Apis mellifera, two species of Ashmediella (including A. rufipes), Atoposmia enciliaea, one species of Colletes, two species of Diadasia (D. australis and D. diminuta), one species of Dialictus, three species of Epeolus (including E. mesillae and E. minimus), three species of Halictus (including Halictus ligatus), Hoplits biscutellae, Lassioglossum sisyurbrii, three species of Megachile (including M. fuctata and M. xerophila), one species of Melissodes, and one species of Stelis.

4.3.4 Grindelia

Grindelia is a small herbaceous plant. It produces many large, yellow, radial, composite flowers. We collected 17 species of bee from Grindelia: one species of Anthophora, three species of Ashmediella (including A. rufipes and A. meliloti), Coelioxis erysimi, Diadasia envervata, Halictus ligatus, two species of Megachile (M. lippiae and M. parallela), two species of Perdita, two species of Dialictus, four species of Melissodes, and Apis mellifera.

4.3.5 Helianthus

Helianthus is a large, abundant plant that is typically attractive to many bees. The flowers are yellow, have an open morphology, and are abundant on the plant. We collected two species of Melissodes from Helianthus.

4.3.6 Prosopis

Prosopis glandulosa is a large tree associated with the dunes of the Refuge. The flowers of Prosopis are large, open, and yellow. They are highly attractive to many insects because they produce copious amounts of nectar. We collected 37 species of bee from Prosopis: one species of Andrena, one species of Calliopsis, six species of Perdita, two species of Anthophora, Apis mellifera, two species of Centris, Diadasia bituberculata, two species of Habropoda, one species of Neolarra, four species of Colletes, two species of Hylaeus, Agapostemon melliventris, two

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species of Halictus, one species of Anthidiellum, one species of Anthidium, five species of Ashmediella (including A. aridula), three species of Megachile, and one species of Stelis.

4.3.7 Salix

Salix is a large tree that produces many open flowers, and though the flowers individually are quite small, they are produced in very high numbers. On the Refuge, Salix seems to be restricted to reliable waterways. We collected five species of bee from Salix: two species of Andrena, one species of Nomada, one species of Colletes, and one species of Lassioglossum.

4.3.8 Salvia

A member of the mint family (Lamiaceae), Salvia commonly has violet to white flowers with bilateral symmetry. The flowers commonly produce a substantial amount of nectar, and advertise the availability of pollen and nectar with floral scents. We collected four species of bee from Salvia: one species of Centris, one species of Anthidium, one species of Ashmediella, and one species of Megachile.

4.3.9 Stanleya

Stanleya is a large herbaceous plant in the mustard family (Brassicaceae). It produces relatively large, yellow, bilateral flowers. We collected 16 species of bee from Stanleya: Apis mellifera, one species of Anthophora, four species of Centris, one species of Habropoda, one species of Xeromolecta, one species of Xylocopa, two species of Colletes, two species of Hylaeus, Agapostemon melliventris, one species of Andrena, and one species of Halictus.

4.3.10 Tamarix

Tamarix is a weedy tree common in the arid southwestern . It produces many small pink flowers that many bees are known to visit. We collected one species of Colletes and one species of Stelis from Tamarix.

4.4 Discussion

Some of these plants supported far fewer flower-visiting insects than we suspected. Specifically, Helianthus, Salix, Salvia, and Tamarix supported very few bee genera. This lack of importance may be a product of the distribution of the plants. Helianthus, for example, is found primarily in marshy areas adjacent to reservoirs, and Tamarix is now very rare on the Refuge, though it is known to support a variety of bees off the Refuge.

The data on the remaining plants can be considered in two ways. First, which of these plants is most significant in supporting insect diversity, and second, which of these plants is most

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significant in supporting the pollinators of rare plants? The plants that support the greatest diversity of insects are Prosopis, Enceliopsis, Asclepias, Creosote, Grindelia, and Stanleya. These plants largely support nectarivorous insects, such as bees and some flies, though they also support many herbivorous insects, such as those in the family Heteroptera. Prosopis and Enceliopsis are, arguably, the most significant of these. Prosopis supports an unparalleled diversity of insects. The data we report here include only the bees, which we noticed to be a small proportion of the insects that utilize Prosopis. Additionally, the abundance and distribution of Prosopis increase its importance to the insects; it is a very common tree on the Refuge. Prosopis is also associated with and appears to stabilize the Refuge’s sand dunes. Dunes are important because many insects use them for nesting, hunting and foraging, and courtship.

Enceliopsis represents the first significant source of pollen and nectar each year, and appears to be the plant that supports the richest assemblage of insects during the early bloom. Interestingly, it is also one of the Refuge’s rare plants. As with Prosopis, Enceliopsis not only supports a rich assemblage of bees, it also supports other insects such as wasps, flies, and butterflies. Also, Enceliopsis has a very broad distribution across the Refuge, making it accessible to many insects.

While Asclepias, Creosote, Grindelia, and Stanleya are important sources of forage for many insects, they are not as numerous nor as broadly distributed as Prosopis or Enceliopsis. Asclepias is found primarily in a few of the dry washes east of Peterson’s Reservoir, Creosote is restricted to the uplands of the refuge, Grindelia is largely restricted to the marshy regions of the Refuge, and Stanleya is restricted to the highly disturbed areas of the Refuge, such as roadsides. The plants’ limited distributions will decrease their importance relative to the other plants, though their regional importance might exceed that of Prosopis or Enceliopsis.

Additionally, we may consider how these plants contribute to the fitness of the pollinators of the rare plants. Many genera of native bees that visit the cornucopia plants also visit and significantly contribute to the pollination of more than one rare plant. These include Agapostemon, Anthophora, Ashmediella, Habropoda, Megachile, Melissodes, and Perdita. Prosopis supports all of these genera, and Enceliopsis supports all but Perdita and Habropoda. The remaining plants support fewer of these genera.

Taken together, these data suggest that Prosopis and Enceliopsis support not only the greatest diversity of nectarivorous insects, but also the greatest number of genera that pollinate the Refuge’s rare plants. It is possible that Prosopis is used as a forage bridge, or a source of pollen and nectar between major plant blooms, and that without it potential pollinators would be greatly reduced later in the season. It is also possible, however, that Prosopis is competing with some plants for insect pollination services, though our study was not designed to test this. Additionally, Enceliopsis is important to many of the Refuge’s pollinating insects. Enceliopsis is the first of the cornucopia plants to bloom on the Refuge, and consequently it represents the first major source of forage. Not surprisingly, therefore, it attracts and supports a great many insects.

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5.0 TASK 6: IDENTIFY THE LOCATION OF NEST SITE AGGREGATIONS AND HABITAT PREFERENCES OF INSECT POLLINATORS

5.1 Methods

Measuring potential nesting habitats for bees on the Refuge was accomplished by selecting 10 sampling sites (Table 15, Figure 1). These sites were selected based on their soil content. The majority of bee species nest in the ground, so soil composition is an important factor in bee nesting. Cane (1991) suggested that many families of desert bees prefer to nest in soils with a high sand ratio; hence the sites selected for this study consisted of habitats with sandy soils. Bees were collected at these sites from February 2009 until October 2009 using two collecting methods, bowl trapping and net trapping. Each site was sampled once every other week throughout the season. Bowl traps consisted of 25 bowls painted fluorescent yellow (8 bowls), fluorescent blue (8 bowls) and white (9 bowls); we set up the bowls in an X formation with each bowl 6 m apart. The location of the trap within a site was determined randomly from week to week. Consistent net sampling between sites was accomplished by limiting the time spent collecting bees to 15 minutes per site.

Table 15. Coordinates and descriptions of sampling sites used to identify potential bee nesting habitat on Ash Meadows National Wildlife Refuge. UTM SITE CODE SITE NAME DESCRIPTION (EASTING NORTHING) Non-dune, grass, and trees. North of the road Site A - 563176 4029978 that passes Devils Hole. Non-dune, Alkali Shrub. South of the road that Site B - 563204 4029801 passes Devils Hole. Non-dune, Alkali Shrub. North of Site D and Site C - 559094 4035101 south of the northern road connecting Longstreet and Peterson Roads. Small, brushy dune; 300 m south of the Site D Isolated Dune 559022 4034728 northern road connecting Longstreet and Peterson Roads. Sand dune with creosote brush. Just south of Site E Creosote Dune 558238 4032743 Peterson Reservoir Dune. Sand dune with short brush. Immediately west Site F Crystal Saltbrush Dune 559098 4028628 of Horseshoe Marsh. Sand dune with Honey Mesquite Brush. West Site G Crystal Mesquite Dune 558927 4028767 of Horseshoe Marsh beyond Site F. Sand dune with Honey Mesquite Brush. South South Spring Site H 558407 4031016 of Spring Meadows Road (the road that runs in Meadows Road Dune front of the Refuge office). Sand dune with short brush. At Peterson Site I Peterson Dune 557875 4033237 Reservoir. Sand dune with Honey Mesquite Brush. South Site J School Springs Dune 561565 4030905 of road to School Springs. U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 40 to the Reproductive Fitness of 12 Rare Plants

Figure 1. Sand dune and non-dune sampling sites used to identify potential bee nesting habitat on Ash Meadows National Wildlife Refuge (Refuge). Letters correspond to site codes given in Table 15. Colors represent habitat type: pink = Honey Mesquite dominated sand dune; yellow = Saltbrush dominated sand dune; green = Creosote dominated sand dune; and orange = Non-dune, Alkali Soil habitat, where eight of the Refuge’s rare plants are found (Astragalus phoenix, Calochortus striatus, Centaurium namophilum, Cordylanthus tecopensis, Enceliopsis nudicaulis var. corrugata, Ivesia kingii var. eremica, Mentzelia leucophylla, and Sisyrinchium spp.).

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Percent cover and dominant vegetation in each of the 10 sampling sites was recorded and compared with the variation of bee species diversity and abundance for each sampling location via analysis of similarities (ANOSIM). This revealed that the 10 sampling sites could be grouped into four habitat types: Non-dune, Alkali Soil habitats typically inhabited by rare plants; Honey Mesquite dominated sand dunes; Saltbrush dominated sand dunes; and Creosote dominated sand dunes (Table 16).

Table 16. Bee nesting habitat sampling sites grouped by habitat type.

HABITAT TYPES SITES a

Non-dune, Alkali Soil habitats typically inhabited by rare Site A, Site B, and Site C plants Saltbrush dominated sand dunes Site D, Site F, and Site I Honey Mesquite dominated sand dunes Site G, Site H, and Site J Creosote dominated sand dunes Site E a Site codes correspond to those used in Table 15.

5.2 Results

Three of the four habitat types were compared using Simpson’s species richness measure. The Creosote dominated sand dune habitat was not considered in these comparisons because there is only a single dune on the Refuge that is dominated by Creosote, and therefore could not be sampled as the other habitats. Comparison of the Non-dune Alkali Soil, Honey Mesquite dominated sand dune, and Saltbrush dominated sand dune habitats using Simpson’s species richness test showed that Saltbrush dominated sand dune habitats support the greatest overall richness of bee species on the Refuge.

Although the Saltbrush dominated sand dune habitat supports the greatest overall bee diversity, it supports the fewest bee species important for pollinating rare plants (Table 17). The greatest numbers of bee species that pollinate the Refuge’s rare plants are found in Non-dune Alkali Soil and Honey Mesquite dominated sand dune habitats. Each habitat supports a unique fauna important for the pollination of different rare plants.

While each habitat supports its own unique assemblage of species, each habitat also has some overlap in bee species, though the abundance of each species per site may vary. A list of bee species most commonly found in each of the four habitats is given in Table 18. If a species was found in more than one habitat, the different abundances were compared between habitats using the chi-square test; this showed which habitat the species could be found in greatest abundance.

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Table 17. Potential nesting habitats for bee pollinators of the 12 rare plants at Ash Meadows National Wildlife Refuge. RARE PLANT BEE SPECIES HABITAT

Non-dune Anthophora sp. 4 Arctomecon merriamii Saltbrush dune Apis mellifera Non-dune Astragalus phoenix Apis mellifera Non-dune Agapostemon angelicus/texanus Non-dune Non-dune Agapostemon melliventris Saltbrush dune Honey Mesquite dune Ashmediella aridula Honey Mesquite dune Calochortus striatus Ashmediella gillettei Honey Mesquite dune Ashmediella rufipes Honey Mesquite dune Diadasia diminuta Non-dune Diadasia vallicola Honey Mesquite dune Dialictus sp. 1 Non-dune Halictus ligatus Non-dune Agapostemon angelicus/texanus Non-dune Non-dune Agapostemon melliventris Saltbrush dune Honey Mesquite dune Apis mellifera Non-dune Centaurium namophilum Dialictus sp. 7 Non-dune Megachile lippiae Non-dune Non-dune Melissodes sp. 4 Honey Mesquite dune Creosote dune Dialictus sp. 7 Non-dune Non-dune Cordylanthus tecopensis Melissodes sp. 4 Honey Mesquite dune Creosote Agapostemon angelicus/texanus Non-dune Non-dune Agapostemon melliventris Saltbrush dune Enceliopsis nudicaulis var. corrugata Honey Mesquite dune Apis mellifera Non-dune Ashmediella rufipes Honey Mesquite dune Colletes sp. 3 Saltbrush dune

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Table 17. (Cont.) RARE PLANT BEE SPECIES HABITAT

Diadasia australis Non-dune Diadasia diminuta Non-dune Halictus ligatus Non-dune Enceliopsis nudicaulis var. corrugata Megachile xerophila Non-dune (cont.) Non-dune Melissodes sp. 4 Honey Mesquite dune Creosote dune Apis mellifera Non-dune Ashmediella rufipes Honey Mesquite dune Dialictus sp. 7 Non-dune Halictus ligatus Non-dune Grindelia fraxino-pratensis Megachile lippiae Non-dune Non-dune Melissodes sp. 4 Honey Mesquite dune Creosote dune Apis mellifera Non-dune Ashmediella bigeloviae Honey Mesquite dune Ivesia kingii var. eremica Ashmediella leucozona Honey Mesquite dune Dialictus sp. 7 Non-dune Agapostemon angelicus/texanus Non-dune Non-dune Agapostemon melliventris Saltbrush dune Honey Mesquite dune Non-dune Mentzelia leucophylla Anthophora sp. 5 Saltbrush dune Apis mellifera Non-dune Dialictus sp. 7 Non-dune Dianthidium implacatum Non-dune Megachile lippiae Non-dune Nitrophila mohavensis - - Agapostemon angelicus/texanus Non-dune Sisyrinchium funereum Anthidiellum notatum Non-dune Ashmediella aridula Honey Mesquite dune Apis mellifera Non-dune Megachile lippiae Non-dune Spiranthes infernalis Non-dune Melissodes sp. 4 Honey Mesquite dune Creosote dune

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Table 18. Preferred habitat for each bee species collected, based on significant difference in bee abundance between habitats. NON-DUNE, ALKALI SALTBRUSH HONEY MESQUITE CREOSOTE DOMINATED SOILS DOMINATED SAND DUNE DOMINATED SAND DUNE SAND DUNE Agapostemon Agapostemon melliventris Agapostemon melliventris Andrena sp. 5 angelicus/texanus Agapostemon melliventris Andrena sp. 4 Andrena sp. 3 Ashmediella nr. Sonora Andrena sp. 1 Anthidiellum sp. 1 Anthophora sp. 2 Calliopsis puellae Andrena sp. 2 Anthophora sp. 2 Anthophora sp. 7 Dioxys sp. 1 Anthidiellum notatum Anthophora sp. 4 Anthophora sp. 8 Hesperapis sp. 3 Anthidiellum sp. 1 Anthophora sp. 9 Anthophora sp. 9 Megachile dentipes Anthophora sp. 2 Anthophora sp. 12 Anthophora sp. 10 Megachile sp. 3 Anthophora sp. 4 Anthophora vaginera Anthophora sp. 12 Melissodes sp. 1 Anthophora sp. 8 Ashmediella breviceps Ashmediella aridula Melissodes sp. 4 Anthophora sp. 11 Ashmediella cubiceps Ashmediella bigeloviae Melissodes sp. 7 Anthophora sp. 13 Calliopsis puellae Ashmediella bucconis Perdita sp. 4 Anthophora vaginera Centris sp. 2 Ashmediella femorata Perdita sp. 20 Apis mellifera Colletes sp. 1 Ashmediella gillettei Ashmediella difugita Diadasia megamorpha Ashmediella leucozona Ashmediella nr. sonora Dialictus sp. 9 Ashmediella opuntiae Ashmediella opuntiae Dioxys sp. 1 Ashmediella prosopidis Calliopsis puellae Hesperapis sp. 1 Ashmediella rufipes Calliopsis sp. 1 Hesperapis sp. 2 Ashmediella rufitarsis Centris sp. 5 Hylaeus sp. 3 Ashmediella xenomaslax Centris sp. 6 Lasioglossum sp. 1 Calliopsis puellae Diadasia australis Megachile nevadensis Colletes sp. 2 Diadasia diminuta Megachile subanograe Diadasia martialis Diadasia vallicola Megachile sp. 1 Diadasia vallicola Dialictus sp. 1 Megachile sp. 2 Dialictus sp. 2 Dialictus sp. 6 Melissodes sp. 4 Dialictus sp. 7 Dialictus sp. 10 Melissodes sp. 5 Dialictus sp. 9 Dianthidium implicatum Melissodes sp. 6 Dufourea sp. 1 Dieunomia xerophila Melissodes sp. 7 Hesperapis sp. 2 Halictus ligatus Melissodes sp. 8 Hesperapis sp. 4 Lasioglossum sp. 1 Neolarra sp. 2 Hylaeus sp. 1 Lasioglossum sp. 3 Perdita sp. 2 Hylaeus sp. 2 Megachile chilopsidis Perdita sp. 12 Hylaeus sp. 3

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Table 18. (Cont.) NON-DUNE, ALKALI SALTBRUSH HONEY MESQUITE CREOSOTE DOMINATED SOILS DOMINATED SAND DUNE DOMINATED SAND DUNE SAND DUNE Megachile lippiae Perdita sp. 13 Lasioglossum sp. 1 Megachile nevadensis Perdita sp. 17 Lasioglossum sp. 2 Megachile xerophila Perdita sp. 18 Lasioglossum sp. 3 Melissodes sp. 1 Perdita sp. 19 Megachile augustina Melissodes sp. 7 Perdita sp. 24 Megachile nevadensis Melissodes sp. 8 Perdita sp. 26 Megachile odontostoma Melissodes sp. 9 Triepiolus sp. 1 Melissodes sp. 1 Perdita sp. 8 Melissodes sp. 4 Perdita sp. 11 Melissodes sp. 8 Perdita sp. 20 Neolarra sp. 1 Perdita sp. 25 Osmia marginata Osmia titusi Perdita sp. 6 Perdita sp. 10 Perdita sp. 15 Perdita sp. 16 Perdita sp. 19 Perdita sp. 22 Perdita sp. 23 Perdita sp.24 Perdita sp. 26 Stelis sp. 1 Stelis sp. 2

5.3 Discussion

Our data suggest that bees that visit the Refuge’s rare plants are collected most commonly in Non-dune, Alkali Soil habitats (Table 18), which is also where many of the rare plants are found. While the Non-dune Alkali Soil and Saltbrush dominated sand dune habitats had the greatest number of species that visit the Refuge’s rare plants, our data show that the Honey Mesquite dominated sand dune habitat also houses many bee species important to the reproduction of these plants. For example, the Honey Mesquite dominated sand dune habitats support every species in the genus Ashmediella collected during this study, and Ashmediella are important pollinators for Calochortus striatus, Enceliopsis nudicaulis var. corrugate, Grindelia fraxino-pratensis, Ivesia kingii var. eremica, and Sisyrinchium funereum.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 46 to the Reproductive Fitness of 12 Rare Plants

It is unlikely that our sampling effort sufficiently represented all areas suitable for bee nesting. When we compared the bee species collected directly from rare plants to bee species collected from the four probable nesting habitats, we found that there were many bee species that visit the rare plants that were unaccounted for in the nesting study. For example, the habitats in which Arctomecon merriamii, Grindelia fraxino-pratensis, and Spiranthes infernalis are commonly found are not indicative of the entire Refuge, nor conducive to bee nesting; consequently, it was not sampled as extensively as other, more-favorable bee nesting habitats. Therefore, some of the bees not collected in the potential nesting areas sampled in this study may in fact be found in and around Arctomecon merriamii, Grindelia fraxino-pratensis, and Spiranthes infernalis.

Based upon the goals of Refuge staff for conserving the Refuge’s 12 rare plants, conserving the habitats where rare plants are found will protect many of the species responsible for pollinating those plants. Also, conservation of Honey Mesquite dominated sand dune habitats will protect several species of Ashmediella, which are important pollinators of multiple rare plants. Although other habitats do not support bees that pollinate any of the rare plants, conservation of these other habitats, including Saltbrush dominated and Creosote dominated sand dune habitats, is important because of the large diversity and uniqueness of bee species found in those areas.

6.0 GENERAL DISCUSSION AND RECOMMENDATIONS

Our data show that pollination services offered by insects are important to many of the Refuge’s 12 rare plants. Indeed, our data suggest that there are viable pollinators for all of the rare plants excepting Nitrophila and Sisyrinchium. This, however, does not mean that all 12 rare plants require pollination services. It is unlikely that Centaurium, Ivesia, Nitrophila, and Sisyrinchium require insect visitation for successful reproduction, though it may play an occasional role in the overall fitness of these plants. That is, while insect-mediated pollination is not always required by these plants, it may be important in maintaining genetic diversity within and between populations when it does occur.

In the interest of maintaining a viable suite of pollinators on the Refuge, restoration plans should include revegetation with Prosopis, Enceliopsis, Asclepias, Creosote, Grindelia, and Stanleya. These plants are known to provide forage for a broad diversity of bees, including many of genera that also visit rare plants.

Finally, our data show that pollinators are found ubiquitously across the Refuge, but the pollinators of rare plants are found coincidentally on the plants and also on sand dunes. Therefore, management of the land in and around the Refuge should include the following strategies:

1. Conservation of important habitat for insect pollinators, including areas in and around extant populations of rare plants and Honey Mesquite dominated sand dunes. Many species of pollinating insects will nest close to reliable sources of pollen and nectar,

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 47 to the Reproductive Fitness of 12 Rare Plants

which many populations of rare plants represent. Also, sand dunes, specifically those stabilized by mesquite, support a diverse assemblage of nectarivorous insects, including many pollinators of the Refuge’s rare plants.

2. Conservation of critical habitat for important pollinators—including Anthophora, Apis, Dialictus, and Megachile—shared among many of the rare plants. Unfortunately, much of the natural history work on these genera has yet to be completed. We therefore suggest that more studies be conducted to illuminate the habitat preferences and ecological needs of these genera on the Refuge.

3. Conservation of plants that support the Refuge’s diverse pollinator community, including Prosopis, Enceliopsis, Asclepias, Creosote, Grindelia, and Stanleya. Prosopis supports a greater diversity of bees than any other plant on the Refuge. It is broadly distributed, numerous, and blooms when many other plants have either ceased or have yet to bloom. Enceliopsis also supports a diverse assemblage of bees, is numerous, and broadly distributed, but it blooms very early in the season.

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7.0 LITERATURE CITED

Beattie, A.J. 1971. Itinerant pollinators in a . Madrono 21:120–124.

Borror, D.J., and R.E. White. 1998. A Field Guide to Insects: America North of Mexico. Boston, MA: Houghton Mifflin.

Cane, J.H. 1991. Soils of ground-nesting bees (Hymenoptera: Apoidea): texture, moisture, cell depth, and climate. Journal of Kansas Entomological Society 64:406–413.

Cochrane, S.A. 1981. Status report Grindelia fraxino-pratensis. Carson City, NV: Nevada Natural Heritage Program.

Cruden, R.W. 1977. Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31:32–46.

Jensen, S. 2007. White Horse Associates. Interview regarding the soils of Ash Meadows. Conducted in February of 2007.

Jepson, W.L. 1979. The Jepson Manual: Higher Plants of California. University of California Press.

Kearns, C.A., and D.A. Inouye. 1993. Techniques for Pollination Biologists. University Press of .

Knight, T.A., and G.H. Clemmer. 1987. Status of populations of the endemic plants of Ash Meadows, Nye County, Nevada. A report to U.S. Fish and Wildlife Service, Great Basin Chapter 6 - References Amargosa Farm Road Solar Energy Project Complex, Reno, Nevada in cooperative agreement with Nevada Division of Forestry, Department of Conservation and Natural Resources, and Nevada Natural Heritage Program, Carson City, NV. Project Agreement No. 86-2-1. 100 pp.

Michener, C.D. 2007. The Bees of the World. Baltimore, MD: Johns Hopkins University Press.

Mozingo, H.N., and M. Williams. 1980. Threatened and Endangered Plants of Nevada. U.S. Department of the Interior, Fish and Wildlife Service, and Bureau of Land Management, Reno, NV.

Nevada Natural Heritage Program. 2001. http://heritage.nv.gov/atlas/atlasndx.htm

Pavlik, B. 2007. Interview regarding the plants of Ash Meadows National Wildlife Refuge. January 2007.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 49 to the Reproductive Fitness of 12 Rare Plants

Reveal, J.L. 1978. Status report on Mentzelia leucophylla. Portland, OR: U.S. Fish and Wildlife Service.

Reveal, J.L., C.R. Broome, and J.C. Beatley. 1973. A new Centaurium (Gentianaceae) from region of Nevada and California. Bulletin of the Torrey Botanical Club 100:353–356.

Rico-Gray, V., and P.S. Oliveira. 2007. The Ecology and Evolution of Ant-Plant Interactions. Chicago: University of Chicago Press.

Sheviak, C.J. 1989. A new Spiranthes (Orchidaceae) from Ash Meadows, NV. Rhodora 91:225– 234.

Sipes, S.D., and V.J. Tepedino. 1994. Reproduction of the rare orchid, Spiranthes diluvialis: breeding system, pollination, and implications for conservation. Conservation Biology 9:929–938.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR 50 to the Reproductive Fitness of 12 Rare Plants

APPENDIX A: SALIENT LITERATURE NOT CITED IN TEXT

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Fleming, T.H., and J.N. Holland. 1998. The evolution of obligate pollination mutualisms: sentia cactus and sentia . Oecologia 114:368–375.

Geer, S.M., V.J. Tepedino, T.L. Griswold, and W.R. Bowlin. 1995. Pollinator sharing by three sympatric milkvetches, including the endangered species Astrasgalus montii. Great Basin Naturalist 55(1):19–28.

Harder, L.D., and S.D. Johnson. 2005. Adaptive plasticity of floral display size in animal- pollinated plants. Proceedings of the Royal Society B 272:2651–2657.

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Hawk, J.L., and V.J. Tepedino. 2007. The effect of staminod removal on female reproductive success in a Wyoming population of endangered blowout penstemon, Penstemon haydenii (Scrophulariaceae). Madrono 54(1):22–26.

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Kindemann, P., and J. Jersakova. 2006. Effect of floral display on reproductive success in terrestrial orchids. Folia Geobotanica 41:47–60.

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Machon, N., P. Bardin, S.J. Mazer, J. Moret, B. Godelle, and F. Austerlitz. 2003. Relationship between genetic structure and seed pollen dispersal in the endangered orchids Spirales spiralis. New Phytologist 157:677–687.

Molau, U. 1993. Relationships between flowering phenology and life history strategies in tundra plants. Arctic and Alpine Research 25(4):391–402.

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Pavlik, B.M., and A.E. Stanton. 2006. Managing populations of rare plants at Ash Meadows National Wildlife Refuge. Report.

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Sipes, S.D., and V.J. Tepedino. 2006. “Perfection” subverted? A contrivance for outcrossing in a rare orchid in influenced by pollinator abundance. Journal of the Torrey Botanical Society 133(3):412–420.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR A-2 to the Reproductive Fitness of 12 Rare Plants

Snelling, R.R., and J.A. Torres. 2004. The spider wasps of Puerto Rico and the British Virgin Islands (Hymenoptera: Pompilidae). Journal of the Kansas Entomological Society 77(4):356–376.

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Tepedino, V.J. 1982. Effects of defoliation on reproduction of a toxic range plant, Zigadenus paniculatus. Great Basin Naturalist 42(4):524–528.

Tepedino, V.J. 1982. Flower visitation and pollen collection records for bees of high altitude shortgrass prairie in Southeaster Wyoming. The Southwestern Entomologist 7(1):16–25.

Tepedino, V.J. 2003. What’s in a name? The confusing case of the death camas bee, Andrena astragali Viereck and Cockerell (Hymenoptera: ). Journal of the Kansas Entomological Society 76(2):194–197.

Tepedino, V.J. 2005.Reproduction and pollination of two rare species of Astragalus from Washington County, Southern Utah: A. holmgreniorum and A. ampullarioides. Final report

Tepedino, V.J., D.G. Alston, B.A. Bradley, T.R. Toler, and T.L. Griswold. 2007. Orchard pollination in Capitol Reef National Park, Utah, USA. Honey bees or native bees? Biodiversity and Conservation 16:3083–3094.

Tepedino, V.J., W.R. Bowlin, T.L. Griswold. 2006. Pollination biology of the endangered blowout penstemon (Penstemon haydenii S. wts.: Scrophulariaceae) in Nebraska. Journal of the Torrey Botanical Society 133(4):548–559.

Tepedino, V.J., B.A. Bradley, and T.L. Griswold. (In press). Might flowers of invasive plants increase native bee carrying capacity? Intimations from Capitol Reef National Park, Utah USA. Natural Areas Journal

Tepedino, V.J., and S.M. Messinger. 2004. beckii, a rare protogynous umbellifer () of Capitol Reef National Park, Central Utah. Madrono 51(3):271–274.

Tepedino, V.J., S.D. Sipes, and T.L. Griswold. 2004. Reproduction and demography of aprica (Asteraceae), a rare endemic of the Southern Utah plateau. Western North American Naturalist 64(4):465–470.

Tepedino, V.J., T.R. Toler, B.A. Bradley, J.L. Hawk, and T.L. Griswold. 2007. Pollination biology of a disjunct population of the endangered sandhills endemic Penstemon haydenii S. Wats. (Scrophulariaceae) in Wyoming, USA. Plant Ecology 193:59–69.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR A-3 to the Reproductive Fitness of 12 Rare Plants

Timmerman-Erskine, M., and R.S. Boyd. 1999. Reproductive biology of the endangered plant socialis (). Journal of the Torrey Botanical Society 126(2):107– 116.

Toler, T.R., E.W. Evans, and V.J. Tepedino. 2005. Pan-trapping for bees (Hymenoptera: Apiformes) in Utah’s west desert: the importance of color diversity. The Pan-Pacific Entomologist 81(3/4):103–113.

Zhang, L., C.H. Barrett, J.Y. Gao, J. Chen, W.W. Cole, Y. Liu, Z.L. Bai, and Q.J. Li. 2005. Predicting mating patterns from pollination syndromes: the case of “sapromyiophily” in Tacca chantrieri. American Journal of Botany 92(3):517–524.

U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR A-4 to the Reproductive Fitness of 12 Rare Plants

APPENDIX B: LIST OF THE RARE PLANTS AND THEIR POTENTIAL POLLINATORS AT ASH MEADOWS NATIONAL WILDLIFE REFUGE. PLANT NAMES ARE FLUSH LEFT AGAINST COLUMN MARGINS. POLLINATOR NAMES (GENUS ONLY) ARE INDENTED WITH LETTERS.

Arctomecon merriamii Grindelia fraxino-pratensis a. Perdita a. Colletes b. Anthophora b. Hylaeus c. Andrena Astragalus phoenix d. Perdita a. Camponotus e. Nomia b. Monomorium f. Augochlorella c. Halictus g. Anthidium d. Andrena h. Dianthidium e. Osmia i. Anthidiellum f. Ceratina j. Protosmia g. Symhalonia k. Chelostomopsis h. Anthophora l. Hoplitis i. Apis m. Ashmediella j. Bombus n. Osmia k. Psithyrus o. Megachile p. Exomalopsis Calochortus striatus q. Synhalonia a. Andrena r. Melissodes b. Calliopsis c. Perdita Ivesia kingii var. eremica d. Duforea a. Hylaeus e. Augochlorella f. Anthidium Mentzelia leucophylla g. Chelostoma a. Andrena h. Osmia b. Perdita i. Synhalonia c. Ceratina d. Anthophora Centaurium namophilum e. Megachile a. Augochlorella f. Hoplitis b. Mellisodes g. Hesperapis c. Apis d. Agapostemon Cordylanthus tecopensis Nitrophila mohavensis a. Anthidium a. None b. Heriades c. Melissodes Sisyrinchium funereum a. Augochlorella Enceliopsis nudicaulis var. corrugata b. Osmia a. Agapostemon c. Ceratina b. Apis c. Anthophora Spiranthese infernalis d. Ceratina a. None e. Perdita U.S. Fish and Wildlife Service Contributions of Insect Pollinators Ash Meadows NWR B-1 to the Reproductive Fitness of 12 Rare Plants