A COMPARISON OF FAUNA IN TWO NORTHERN CALIFORNIA COASTAL

DUNE SYSTEMS

By

Laura Snyder Julian

A Thesis Presented to

The Faculty of Humboldt State University

In Partial Fulfillment of the Requirements for the Degree

Master of Science in Natural Resources: Biology

Committee Membership

Dr. Michael R. Mesler, Committee Chair

Dr. Erik S. Jules, Committee Member

Dr. Frank J. Shaughnessy, Committee Member

Dr. Mahesh Rao, Committee Member

Dr. Michael R. Mesler, Graduate Coordinator

December, 2012

ABSTRACT

COMPARISON OF BEE FAUNA IN TWO NORTHERN CALIFORNIA COASTAL DUNE SYSTEMS

Laura Snyder Julian

Baseline information is needed to protect pollinators in at-risk ecosystems. One such system, Tolowa Dunes (Crescent City, California), in northern California, is undergoing habitat fragmentation caused by an introduced, invasive , . My study had two purposes: 1) to gather baseline data on the bee fauna at

Tolowa, and 2) to explore possible relationships between bee fauna and available floral and nest resources in Northern California coastal dune systems. In particular, I assessed whether the presence of invasive non-native such as A. arenaria affected the bee fauna at Tolowa. Surveys were conducted at Tolowa from March through August 2007 to establish baseline information about the bee community, floral abundance, floral visitation, and bee nest substrate. Vegetation cover, determined from existing data, was used to explore the relationship between bee fauna and landscape at three spatial scales

(100 m, 250 m and 1,050 m). Using existing data from previous studies, I compared the bee fauna I found at Tolowa to that of two other Northern California coastal dune ecosystems: the North Spit of Humboldt Bay (near Eureka, California) and Bodega Head

(Bodega Marine Research Station at Bodega Bay, California). These three areas vary in the composition of their invasive non-native plant communities and bee resources, so comparing these areas can reveal relationships between bee fauna and these

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environmental factors. Bee abundance and species richness at Tolowa were positively correlated with intact, native dune vegetation, especially when the rare plant, argentea was present. A negative correlation was found between cover of A. arenaria , coastal scrub, and total exotic vegetation versus the abundance and/or richness of all . NMS ordination found a scale-dependent relationship between bees and vegetation at 100 m and 250 m, where there was a positive relationship between solitary bees and intact, native dune vegetation. At all scales, solitary bees were negatively associated with

A. arenaria , coastal scrub, and total exotic vegetation. Differences between the bee faunas at Tolowa, the North Spit, and Bodega Head are possibly explained by differences in nest substrate availability. For example, Melissodes pallidisignata is a bee that requires compacted sand for nesting. This bee was absent at the North Spit (where there is little of this nest substrate), but was present at Tolowa and Bodega Head, where compact sand is abundant. Differences in bee faunas at these locations are also possibly explained by differences in floral composition and abundance; while exotic vegetation was positively correlated with abundance of common Bombus spp. at the North Spit, a similar correlation was not found at Tolowa. Possibly, this is because invasive plants at the North

Spit provide some floral resources, whereas at Tolowa the only invasive plant is A. arenaria , which provides no floral resources for bees. My results suggest that the diversity of the coastal bee community at Tolowa is at risk due to habitat fragmentation from A. arenaria invasion.

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ACKNOWLEDGEMENTS

My special gratitude to Dr. Michael Mesler for sharing his enthusiasm for bees and to

Susan Nyoka for sharing her love of coastal dunes. I extend special thanks to the members of my graduate committee, Drs. F. Shaughnessy, E. Jules and M. Rao, for their careful review of my work. Dr. R. Thorp generously shared his time and expertise in bee identification. Thank you to M. Wasbauer for sharing the preliminary results of his bee surveys at Tolowa. I am grateful to Sue Calla and Rick Hiser for their hospitality and for their work, and the work of the Tolowa Dune Stewards, to protect Tolowa. I am especially grateful for the love and sustained support I receive from my husband, Brian

Julian. This is dedicated to my father, Phil Snyder.

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LIST OF TABLES

1. Plant associations and corresponding abbreviations used in vegetation analysis..33

2. Nest and floral resources found at study sites, south to north……....………..….35

3. Site characteristic percent cover for major vegetation types and summary groups at 100 m, 250 m and 1,050 m ...... ……………………………..….36

4. Spearman rank correlation between major vegetation categories...... ……………37

5. Distribution of bee species found at Tolowa during plot surveys...... …40

6. Bee species relative abundance pooled across all sites at Tolowa.....……….…...43

7. Spearman-rank correlation between bee abundance and major vegetation categories. Values in bold indicate significant correlations after Bonferroni correction ( p ≤ .001). Values in bold italics indicate significant correlations after Holm’s correction ( p ≤ .025)...... ….….…...... 44

8. Spearman-rank correlation between bee richness and selected vegetation categories. Values in bold indicate significant correlations after Bonferroni correction ( p ≤ .002). Values in bold italics indicate significant correlations after Holm’s correction (p ≤ .05)...... 47

9. Correlation coeffiecients between the abundance of vegetation and vegetation groups at 100 m, 250 m and 1,050 m and the first two ordination axes, from an NMS ordination of 19 bee species and 36 variables at 12 study sites, Tolowa Dunes. Values in bold are for r values ≥ ± 0.500………………………...……48

10. Correlation coefficients between the abundance of nest substrate at 100 m and the first two ordination axes, from an NMS ordination of 19 bee species and 36 variables at 12 study sites, Tolowa Dunes. Values in bold are for r values ≥ ± 0.500……………………………………………...... 49

11. Correlation coefficients between the abundance of floral resources at 100 m and the first two ordination axes, from an NMS ordination of 19 bee species and 36 variables at 12 study sites, Tolowa Dunes. Values in bold are for r values ≥ ± 0.500.…...... …………………………………………….…………49

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12. Correlation coefficients between the abundance of bee species and bee functional groups at 100 m and the first two ordination axes, from an NMS ordination of 19 bee species and 36 variables at 12 study sites, Tolowa Dunes. Values in bold are r values ≥ ± 0.500……...…………………………………...50

13. Correlation coefficients between the abundance of other categories at 100 m, 250 m and 1,050 m and the first two ordination axes, from an NMS ordination of 19 bee species and 36 variables at 12 study sites, Tolowa Dunes. Values in bold are r values ≥ ± 0.500...... …….……………………………………50

14. Relative abundance of bee species at Tolowa and the North Spit...... 52

15. Summary statistics for NMS ordination axes for combined Tolowa and North Spit ordination. Values over 0.500 are bolded…………………..…….…………53

16. Bees that are common to abundant at one or more sites. Abundance scale; R = < 5; U = 5-10; O = 11-25; C = 26-50; A = > 50 …………………………....57

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LIST OF FIGURES

Figures Page

1. Study site locations: Tolowa, Del Norte County, California; North Spit, Humboldt County, California and Bodega Marine Research Station, Mendocino County, California...... 34

2. Proportional abundance of nest substrate measured in surveys at Tolowa, by plot...... 39

3. Bee species richness at Tolowa, by site...... 41

4. Bee abundance, all species at Tolowa, by site...... 42

5. Bi-plot resulting from nonmetric multidimensional scaling of the bee fauna at Tolowa Dunes...... 51

6. Bi-plot resulting from nonmetric multidimensional scaling of the bee fauna at Tolowa Dunes and the North Spit...... 54

7. Comparison of the bee fauna at Tolowa versus the North Spit: a) number of bees by species, per observation hour, at Tolowa and b) number of bees by species, per observation hour, at the North Spit...... 55

8. Comparison of plot vegetation at Tolowa and the North Spit: a) 1 hectare plot composition by vegetation type, Tolowa and b) 1 hectare plot composition by vegetation type, North Spit...... 56

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LIST OF APPENDICES

Appendix Page

A. Site characterization at 100 m, 250 m and 1,050 m...... 58

B. Floral visitation and floral surveys...... 62

C. Floral visitation by bee species...... 66

D. Bee Species Observed at Tolowa Dunes, March through August, 2007...... 70

E. Indicator Species Analysis Results...... 73

F. Site Number Correspondence with Nyoka’s Study (2004) of the North Spit...... 75

G. Bee Species Collected by Marius Wasbauer at Tolowa Dunes, 2010...... 77

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INTRODUCTION

Conservation of bees is essential for maintaining ecosystem services, as bees are the most important pollinator of wild and cultivated plant species worldwide (Winfree et al. 2009). Bee diversity and abundance is at risk due to habitat loss and agricultural intensification (Aizen and Feinsinger 1994, Cane et al. 2006, Steffan-Dewenter et al.

2005, Williams et al. 2010). As obligate floral visitors, bees are especially vulnerable when habitat fragmentation negatively affects floral abundance and diversity (Biesmeijer et al. 2006). Bee species richness has been shown to be negatively affected by invasive plant species (Dafni and Shmida 1996, Nyoka 2004, Severns and Moldenke 2010), and bee diversity can be limited by a lack of available nest resources (Cane 1991, Potts et al.

2003, Potts et al. 2005). Bee species with small foraging ranges and a high degree of diet specialization may be the most affected by a fragmented landscape (Bommarco et al.

2010).

Coastal dunes are important refugias for terrestrial invertebrates, including bees

(Howe et al. 2010). A number of endemic bee species are found in temperate coastal dunes (Howe et al. 2010). These ecosystems have suffered a disproportionate degree of human-induced degradation due to coastal development, conversion to agriculture, off- highway vehicle recreation, and the introduction of non-native invasive plants (Martinez et al. 2004, Pickart and Barbour 2007). Characterization of existing coastal dune bee communities is an important first step in protecting the native pollinators of these ecosystems.

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My study of the Tolowa Dunes area, in northern California, focused on a poorly

known bee fauna. Existing studies of nearby bee communities in coastal northern

California dunes (Gordon 1984, Thorp and Gordon 1991, Nyoka 2004) may provide only

limited insight into the bee fauna at Tolowa, because bee communities can differ

strongly, even at closely spaced sites in the same type of habitat and in the same general

region (Herrera 1988, Frankie et al. 1998, Williams et al. 2001, Aigner 2004, Wilson et

al. 2009). For example, a study comparing the bee communities at Bodega Marine

Research Station and on the dunes of the north spit of Humboldt Bay found that while the

two sites (289 km apart) harbored a similar number of bee families and genera, they

shared only 22 of 68 species (Thorp and Gordon 1991).

The amount and diversity of floral resources along with the availability of nest

sites can determine composition of bee faunas (Sakagami and Fukuda 1973, Potts et al.

2003, Potts et al. 2005, Bartholomew and Prowell 2006, Carvell et al. 2006, Hisamatsu

and Yamane 2006, Wilson et al. 2009). Both floral and nesting resources can be affected

by disturbance regimes that fragment habitats (Minckley et al. 1999, Potts et al. 2003,

Potts et al. 2005, Williams et al. 2010). Differences between bee communities may also

reflect historic accident and result from stochastic turnover. For example, differing sets of

bee species that require the pollen of Larrea tridentata shrubs as a larval food occur across the range of this plant (Minckley et al. 1999).

Tolowa Dunes is characterized by a landscape mosaic of floral and nest resources of differing quality and abundance. Dune wetlands offer seasonally abundant floral resources but limited nest substrate. Stabilized sand in red fescue dune meadows provides

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nest sites for some bees, while open sand in dune mat is a nest resource for smaller bees

that use the rich floral resources of the dune mat. The presence of a non-native grass,

Ammophila arenaria (European beachgrass), reduces floral abundance. Originally

introduced by ranchers at Tolowa to protect pastures from blowing sand ([Anonymous]

1888), A. arenaria is not uniformly distributed throughout Tolowa’s dunes. The density

and distribution of A. arenaria influences bee foraging: areas long colonized by A.

arenaria have little resource-rich native vegetation and thus little food or nest resources

for bees. The diversity of ecological settings at Tolowa provides an opportunity to

explore the impact of habitat variation on the composition of bee communities at a local

scale.

On a broader scale, I compared the bee fauna of Tolowa to the North Spit (Nyoka

2004) and to Bodega Head (Thorp and Gordon 1991). Although Tolowa and the North

Spit are only 115 km apart and share a common climate and plant community, the two

areas differ in types of disturbance. The best-preserved dune vegetation in California can

be found on the North Spit (Pickart 1998), whereas A. arenaria has fragmented native dune vegetation at Tolowa. Tolowa and Bodega Head are 404 km apart, but have experienced similar types of disturbance. A. arenaria , planted in the 1930s at Bodega to stabilize the dunes and prevent sand from filling the harbor, has significantly degraded native vegetation (Danin et al. 1998). Differences and similarities in the nature of resources in these three coastal dune ecosystems should be reflected in the different bee communities.

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The objectives of my study were 1) to describe the bee fauna found at Tolowa, and 2) to explore possible relationships between bee fauna and habitat quality, looking especially at differences between intact native habitat and habitat fragmented by non- native invasive plants such as A. arenaria . To achieve these objectives, I assessed bee abundance and species richness across a sample of different sites at Tolowa (sites representing the full range of bee habitat quality that exists there), and I compared the bee fauna I found at Tolowa to coastal bee faunas previously described by others at the North

Spit and at Bodega Head.

MATERIALS AND METHODS

Study Area

Tolowa is a barrier dune system of approximately 1,000 ha located between Pt. St.

George and the Smith River (between N 41°56’45”, W 124°12’19” in the north and N

41° 47’21”, W 124°14’52” in the south). Pleistocene sands overlain by Holocene-era sands rest on river terrace sediments, Battery formation, St. George formation, and

Franciscan mélange to form the foredunes and backdunes of Tolowa (Anderson et al.

2001, Cooper 1967 and Davenport 1982). Three lobate moving dunes - reactivations of an older, stabilized system - occur east of Tolowa’s dune forest, immediately north of

Crescent City, California (Cooper 1967).

The dune system is widest in the center at Lake Talawa (1.4 km), narrowing to 0.1 km in the north and to 0.3 km in the south (Figure 1). A large, seasonally-inundated wetland lies between the foredunes and the dune forest just south of where the Smith

River turns northward, and continues to just south of Lake Talawa. To the south, areas of gravel, cobble, and coarse sand interrupt the deflation plain

Rain occurs on the Tolowa coast during winter months. Summers are cool and dry. Average yearly precipitation is 1,524 mm, falling predominately from October to

April. The average high temperature is 15.5° C and the average low is 7.2°C. Snow is rare: the coast experiences over 250 frost-free days a year. Prevailing winds are north- northwesterly (Western Regional Climate Center 2010).

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Dune vegetation at Tolowa is composed of several plant communities (Table 1).

These communities differ in the quality of resources available for bees. For example,

areas dominated by the dune mat alliance, the Festuca rubra herbaceous alliance, or by herbaceous seasonally-inundated swales tend to offer more abundant floral and nest resources. In contrast, coastal scrub and A. arenaria semi-natural stands, dominated by a

single grass species, A. arenaria , have fewer of these essential resources. Other common

dune plant communities, such as dune woodland and shrub-dominated swales, offer

fewer types of nest substrate but do provide seasonally abundant floral resources.

Study Design

To study the impact of variation in habitat quality on bee abundance and diversity at Tolowa, I chose 12 sites along a north-south gradient corresponding to decreasing cover of the invasive exotic, A. arenaria . Each site consisted of a single 1 ha bee census plot in dunes where I had observed bees (Table 2). These plots were located in areas known to have a diversity of nest substrates adjacent to relatively abundant floral resources and thus were often not representative of conditions in the immediately surrounding area. The minimum distance between neighboring plots ranged from 0.4 km to 3.7 km and the average distance between plots was 1.3 km.

Site Characterization. I measured habitat quality at three different scales (100 m, 250 m, and 1,050 m) as a function of the proportional cover of differing vegetation types. I also measured the relative abundance of floral resources and potential bee nest substrates in each of the 100 m² plots. Measuring habitat quality at different scales is important

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because different bee species perceive and respond to variation in habitat quality at

differing spatial scales depending on how far they fly from their nests (Hines and Hendrix

2005, Greenleaf et al. 2007, Williams and Kremen 2007, Zurbuchen et al. 2010). These

three scale categories are useful predictors of bee diversity even though they are

somewhat conservative for large-bodied bees, which can forage widely across the

landscape (Goulson 2003, Hines and Hendrix 2005).

I used ArcMap 9.3 (ESRI 2009) and an existing vegetation map (Nyoka 2003) to

calculate proportional cover of major vegetation types within concentric, nested plots at

the three scales. In order to measure the impact of invasive species on bee fauna, percent

cover for two summary vegetation groups was calculated: “Exotic Vegetation” is the sum

of the cover of Coastal Scrub, European Beachgrass Swards ( A. arenaria semi-natural stands), and Upland Pasture; “Native Vegetation” includes all native plant associations except Coastal Scrub. Coastal Scrub was included in the exotic group because – like

Upland Pasture - it has a significant component of non-native vegetation. An important variable that modifies the habitat quality in any of the vegetation types is the degree of A. arenaria incursion. While A. arenaria is the dominant component of European

Beachgrass Swards, its cover value must exceed 80% to meet the classification rules for inclusion in this type. But even at lower densities, the presence of A. arenaria within native plant associations can affect the quality of nesting and floral resources, thereby weakening the correlation between bees and native habitat. To measure this effect, the cover of A. arenaria (data from Nyoka, 2003) was used as the variable “A. arenaria ” whenever its cover in the underlying vegetation type exceeded 20%.

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To measure floral resources in the 100 m² plots, a survey of flowers known to be visited by bees was conducted during each bee survey visit. A 50 m by 0.5 m belt transect was laid out perpendicular to the plot edge at a randomly chosen starting point, and the total number of open flowers was recorded for each species. For each species, the area occupied by open flowers was calculated by multiplying the number of flowers in the transect by the area of an individual flower. The total area of open flower was the sum of the area of all open flowers for all species present. This approach allowed a between-site comparison of floral abundance for each flower species, and also allowed a comparison of total floral abundance by site. Still, measuring area of open flower provides only a rough approximation of available bee forage, because the size of an individual flower does not necessarily mirror the amount of floral resource offered. In addition, proportional cover of the rare plant Phacelia argentea (CNDDB 2006), a rich source of nectar and pollen for bees, was calculated at the three scales using existing data (Nyoka

2003).

Bees require species-specific nest substrates for successful reproduction (Raw and O’Toole 1991). I measured availability of nest substrates in each 100 m² plot. A 100 m linear transect perpendicular to the plot edge was laid out from a randomly selected starting point on the plot edge. Available nest resources were measured in ten 1 m² quadrats placed randomly along each side of the transect. I counted the number of exposed pithy or hollow plant stems, rodent holes, and pre-existing burrows in the ground or in wood. I also recorded percent cover of open sand, biotic crust, stone, and downed wood.

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In 2007, bees were censused at each site during the main flight season (March

through August). Surveys were conducted between 9:00 am and 5:00 pm, when wind

speed was below 5 mph and temperature above 12°C. The survey protocol followed

Nyoka (2004) where species counts were made by walking transects throughout the plot

and tallying all bees encountered within 1.5 m on either side. If a bee was observed on a

flower, the bee and plant species were noted. Bees that could not be identified in flight

were netted and processed for later identification. Sites were visited in rotation for a total

of three visits of four hours duration at each site. In the event of inclement weather,

surveys were completed within the next seven days. Bees that could not be identified to

species in the field were pooled at the genus level: Andrena , Colletes , Dialictus , Hoplitis ,

Lasioglossum , Nomada, Sphecodes , and Stelis. Not all bumble bees could be identified in

flight; these were recorded as Bombus . Identification to genus was made using The Bee

Genera of North and Central America (: Apoidea, Michner et al. 1994).

Robbin Thorp, U.C. Davis Department of Entomology, identified bees to species.

Identification was possible for 87% of the bees. The remainders were treated as

morphospecies. For purposes of analysis, bee species were either treated individually (for

the seven most abundant species) or pooled as solitary bees or .

Statistical Analyses

I used a variety of tests to examine the impact of a series of environmental factors on bee diversity and abundance across my study sites. All tests were performed with

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NCSS (Hintze 2004), PC-ORD 5.0 (McCune and Mefford 2006), ArcGIS 9.3 (ESRI

2009), or EcoSim (Gotelli and Entsminger 2000) software.

My sites were spatially distinct, but I was concerned that some may have had sets of bee species too similar to represent truly independent samples. To evaluate this, I calculated Moran’s I to test for spatial independence of my study plots in terms of bee species (ArcGIS 9.3).

My data did not have a normal distribution, so I used a nonparametric test

(Spearman-Rank correlation) to examine the relationship between bee species richness and abundance and a variety of environmental variables, including the cover of various vegetation categories, total cover of open flowers (per plot and per individual plant species), and nest substrate abundance. When possible, correlations were performed at three scales (100 m, 250 m, and 1,050 m). Significant alpha levels for correlation analyses were adjusted using a sequential Bonferroni procedure (Holm 1979).

Although simple and direct, my correlation-based approach suffers from potential non-independence of environmental variables and the very limited statistical power associated with a large number of tests. Moreover, it cannot reveal relationships between assemblages of bees and environmental gradients. For these reasons, I used ordination to further examine patterns at Tolowa as well as to compare bee assemblages at Tolowa and the North Spit.

I performed two ordinations: one using data from Tolowa alone, and a second using combined data from Tolowa and the North Spit. I did not use data from Bodega

Head in any of these statistical analyses because they were collected using a different

11 methodology and lacked information about vegetation or other environmental factors necessary to explore possible relationships between bee fauna and environmental factors.

Nevertheless, the Bodega data did include relevant information about bee species richness and abundance in a Northern California coastal dune system, so it was important to consider this data in my study.

For both ordinations, I used non-metric multidimensional scaling (NMS) based on

Sorenson distance measures and the autopilot slow and thorough method (Mather 1976

and Kruskal 1964, in McCune and Grace 2002). Rare species, uncommon vegetation

associations, or nest substrates that occurred at fewer than three sites were not included in

the analyses. Proportional abundance of different bee species was used in ordination. One

plot in the combined ordination had an unusual combination of values for several

variables, and was removed from that ordination as an outlier.

At Tolowa, the primary matrix was comprised of bee fauna data from 12 study

sites. I compared axis scores from this matrix with the percent cover at 100 m, 250 m and

1,050 m of the following: P. argentea , A. arenaria , ten vegetation types, developed areas,

water, beach, open sand, and the two summary groups (Native Vegetation and Exotic

Vegetation). Axis scores were also compared to abundance values for all bee species,

solitary bee and bumble bee summary groups, area of open flower for 26 species of

plants, total area of open flower at each site, and count and percent nest substrate data in

seven categories. Axis scores of the combined ordination of Tolowa and the North Spit

were compared to many variables: percent cover at 100 m of P. argentea , seven

vegetation types, open sand, the two summary groups (Native Vegetation and Exotic

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Vegetation), and the abundance of bumble bees, solitary bees, and 35 individual bee species.

Study sites at Tolowa aligned themselves into two groups based on the degree of

A. arenaria incursion. In the first group (four plots) A. arenaria incursion occurred in

62% or more of the plot area; in the second group (eight plots) A. arenaria was present in

24% or less of the plot. No plots had a “medium” amount cover of A. arenaria (between

24% and 62%). A multi-response permutation procedure (MRPP) was used to test whether differences in the bee fauna of these groups were statistically significant. MRPP was also used to test for differences in bee assemblages for groups of plots based on ordination analyses, and to test the hypothesis that the bee fauna at Tolowa was significantly different from the bee fauna at the North Spit.

As sentinel organisms, indicator species can be used by land managers to evaluate restoration success. To determine diagnostic species at Tolowa, indicator species analysis was performed following the method of Dufrene and Legendre (1997) using a Monte

Carlo test of significance with 4,999 permutations.

Although bee sampling methods at Tolowa were identical to Nyoka’s (2004), observation hours were 55% of Nyoka’s. To compensate, I used rarefaction to compare species richness at the two sites; I calculated Jost’s true diversity (Jost 2007) and estimated evenness using Hurlbert’s probability of specific encounter (PIE, 1971) to compare differences in bee diversity between the two locations. Hutcheson’s t-test was

used to evaluate whether differences in diversity were due to chance. At Tolowa and the

North Spit abundance was calculated as bees per survey hour. Descriptive statistics were

13 used to compare differences in bee presence and abundance at Tolowa and the North Spit and differences between Tolowa, the North Spit, and Bodega Head. For each bee species found at any of the sites, presence at one, two, or at all three sites was reported.

Abundance (as defined in Thorp and Gordon’s 1991 study) was calculated for Tolowa, and abundance at all three sites was then compared.

RESULTS

Tolowa

Variation in Habitat Quality. Habitat quality varied significantly between plots and also varied at different scales within each site (Table 3, Appendix A). At the

100 m scale, cover of native vegetation ranged from 35% to 100%, and cover of native vegetation was positively correlated with dune mat and negatively correlated with exotic vegetation. A. arenaria incursion varied from 4% to 91% at 100 m. There was an inverse relationship between A. arenaria and P. argentea at all three scales, which was most pronounced at 100 m. Most of the significant correlations (P. argentea and A. arenaria , dune mat and exotic vegetation) were similar at both 100 m and at 250 m (Table 4). One association did not fit the patterns typical of the other associations: at 1,050 m, dune mat was negatively associated with herbaceous wetland at 100 m. Dune mat and herbaceous wetland at 1,050 m were both correlated with native vegetation at the same distance (r =

0.811, p = 0.000 and r = 0.881, p = 0.001).

The cover of stone, downed wood, number of pithy stems, rodent holes, and

insect holes varied between sites (Figure 2). The number of pithy stems within a square

meter ranged from zero to 126, the number of rodent holes from zero to eight. Two types

of nest substrate important to coastally-distributed bees were found in all of the bee

survey plots: cryptogamic mat, and open sand. There was no association between nest

substrate abundance and vegetation type (Figure 2, Table 3).

Floral resources differed strongly among sites (Appendix B). Total area of open

flower ranged from 1 to 6,537 cm². I recorded the area of open flower for 28 plant

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15 species, but during bee surveys I observed bees visiting 41 plant species (Appendix B).

No correlation was found between area of open flower and vegetation type. Floral

richness at a given site, based on the number of plant species I observed bees visiting,

varied from 11 to as few as three species. A complete list of floral visits by bee species is

in Appendix C.

Bee Fauna. Twenty species of bees in six families were found at Tolowa study sites during survey hours (Table 5, Appendix D). Three additional species were collected in the dunes while enroute to surveys. Species richness at a given site ranged from four to

14, with an average of seven species per site (S.E.±4.93, Fig. 7). Jost’s true diversity

index for all plots at Tolowa was 3.105. Evenness, as measured by Hurlbert’s PIE, was

0.731. First order Jackknife estimates indicate that 74.8% of the bee fauna present was

sampled.

Bee abundance (all species combined) ranged from six to 322 observations per

site (Appendix C). Bumble bees accounted for 49% of the total observations, solitary

bees for 51% (Table 6). Five solitary bee species and morphospecies ( Anthidium

palliventre , Habropoda miserabilis , Andrena concinnula , Colletes spp., and Mellisodes

pallidisignata ) and two bumble bee species ( and Bombus mixtus )

accounted for 69% of all bee observations. Bombus vosnesenskii , with 517 sightings, was

the most abundant bumble bee species. Anthidium palliventre , at 384 sightings, was the

most abundant solitary bee species. Bee species were not distributed uniformly across

sites. B. vosnesenskii was found at all sites whereas several other species were found at

only a few sites (Table 5). The number of bee visits to flowers recorded at a site ranged

from two to 126 (Appendix B).

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Correlations Analysis. Numerous relationships were found between bee abundance or diversity and cover of P. argentea , A. arenaria , dune mat, or Native

Vegetation (Tables 7 and 8), but these relationships varied or sometimes disappeared depending on the scale. Abundance of solitary bees was negatively correlated with A. arenaria at both 100 m and 250 m, positively correlated with Native Vegetation at 250 m and 1,050 m, and positively associated with P. argentea at all scales. Abundance of

Andrena concinula and Colletes spp. was negatively correlated with A. arenaria at 100 m and 250 m. Abundance of Andrena concinnula was positively associated with P. argentea at 100 m. Abundance of Colletes spp. was also positively associated with P. argentea at 100 m and 250 m, and was positively correlated with Native Vegetation at

250 m and 1,050 m. Abundance of Habropoda miserabilis was positively related to dune mat at 1,050 m. Although just short of statistical significance ( p > 0.025), abundance of

B. vosnesenskii was negatively correlated with both A. arenaria (p = 0.069) and Exotic

Vegetation ( p = 0.039), both at 1,050 m (Table 7).

Richness of solitary bees was negatively associated with A. arenaria at 100 m and

250 m, and positively associated with Native Vegetation at 250 m and 1,050 m. Richness of solitary bees was positively correlated with P. argentea at 100 m, and with cover of either dune mat or P. argentea at 1,050 m. Bumble bee richness was negatively

correlated with dune mat at 100 m (Table 8).

With one exception, neither bee abundance nor bee species richness was related to

the availability of nest substrates in the 100 m² plots. richness increased at

sites where downed wood was more abundant (r = 0.806, p = 0.002). Total flower area

17 was likewise a poor predictor of differences among local bee assemblages. The only significant relationship was a negative correlation between the abundance of solitary bees and cover of Achillea millifolium (yarrow; r = -0.816, p = 0.001).

NMS ordination. Ordination of Tolowa data resulted in a 2-dimensional configuration that described 82% of the variation with a final stress of 7.82 (Tables 9 -

13). Axis 1 accounted for 33% of the variation, and axis 2 accounted for 49% of the variation. The abundance of solitary bees was positively correlated with axis 1, while the abundance of bumble bees was negatively associated with axis 2 (Table 12). Negative values on axis 1 were associated with a greater cover of exotic vegetation, and positive values on axis 1 were associated with P. argentea (Table 11). Groups suggested by ordination were identical to groups based on degree of A. arenaria infestation.

A relatively tight cluster of plots (2, 3, 4, 5, 6, 7, 8) occupies the lower right part

of the ordination diagram (Fig. 5). Solitary bees and bumblebees were relatively abundant

in these plots, especially B. vosnesenskii . These plots were associated with native

vegetation at 100 m and 250 m, with coastal scrub at 1,050 m, exotic vegetation at 250 m,

and with P. argentea at 250 m.

The remaining plots (1, 10, 11, 12) had strongly differing bee assemblages, but in general they supported fewer bee species and bee individuals (Fig. 3, 4). Bombus mixtus was correlated with this group. Correlations between bee fauna and environmental variables varied for these plots, but bee fauna was positively correlated with either exotic vegetation at 100 m, A. arenaria at 100 m, coastal scrub at 100 m and 250 m, native vegetation at 1,050 m or shrub swales at 1,050 m.

18

Multi-response Permutation Procedure. Bee fauna at Tolowa differed based on A. arenaria cover (T = - 4.16, p = 0.002). Ordination analysis suggested visually that plots at Tolowa aligned themselves into two groups based on similarity of bee fauna (Fig. 5);

MRPP confirmed that the bee fauna of these two groups differed (MRPP, T = -4.164, p =

0.002).

Indicator Species Values. Plots that had less than 25% A. arenaria cover were characterized by the presence of Colletes spp. (IV = 87.5, p = 0.0128), all solitary bee species ( IV = 85.8, p = 0.004), B. vosnesenskii (IV = 75.3, p = 0.039), and by Anthidium palliventre, (IV = 68.8, p = 0.0952; Appendix E).

The North Spit and Tolowa Dunes.

I spent 144 hours sampling bees at Tolowa and observed 23 species and 11.1 bees per survey hour (Fig. 7). Nyoka had 208 bee-sampling hours at the North Spit and observed 35 species and 112.7 bees per survey hour (Nyoka 2004). Species diversity at

Tolowa was 52% less than at the North Spit (Jost’s true diversity; t = 2.65, p = 0.01). The

number of effective species at Tolowa was 4.74 compared to 9.04 at the North Spit. At

Tolowa there was a 73% chance that two randomly chosen individual bees would

represent two different species (Hurlbert’s PIE = 0.731), in contrast to an 86% chance at

the North Spit (Hurlbert’s PIE = 0.856).

MRPP confirmed there was a significant difference in faunal composition

between Tolowa and the North Spit (T = -7.90, p = 0.0001). The two locations shared only 13 of 35 species (Table 14); species existing in both areas were present in different

19 proportions (Fig. 7). For example, A. palliventre made up 24% of the bees at Tolowa, but only 17% at the North Spit; Habropoda miserabilis accounted for 11% of total bee abundance at Tolowa but just 6% at the North Spit. Only a single individual of Osmia integra was recorded at Tolowa, while 2.27% of the bees at the North Spit were O. integra . At Tolowa, 48% of all bees were bumble bees, while on the North Spit only 27% were. Species found at one location but absent from the other include wheeleri , present on the North Spit but absent from Tolowa, and Andrena concinnula , found only at Tolowa. There were fewer small-bodied bees (body length ≤ 12mm) at

Tolowa: 8.42% compared to 18.36% on the North Spit. Oligolectic bees were more abundant on the North Spit: 38% in contrast to 26% at Tolowa (Table 14). Bee abundance and diversity was, in general, much greater at the North Spit than at Tolowa.

NMS ordination of combined bee fauna data for Tolowa and the North Spit found a two-dimensional solution after 58 iterations ( p = 0.004). Final stress was 12.72. Axis 1 accounted for 38% of the variation, and axis 2 accounted for 52% of the variation, for a total of 90% of the variation. Axis 1 was positively correlated with abundance of bumble bees, and axis 2 was positively correlated with abundance of solitary bees (Table 15).

Overall, there was little correlation of bee fauna with environmental variables. Three groups of plots weakly aligned themselves in terms of bee fauna (MRPP, T = –1.902, p =

0.053) (Fig. 6). Plots in group 1 (1, 2, 3, 9) were correlated with Bombus vosnesenskii and with the group “bumble bees.” Plots in group 2, especially sites 6, 14, 15, 16, and 18, aligned with Anthidium palliventre and the group “solitary bees.” Plots in group 3 (12,

13, 21, 22, 23) could not be easily characterized. They tended to have fewer bees and

20 fewer bee species (Figures 3, 4; Nyoka 2004), and were correlated with the exotics- dominated vegetation group Coyote Brush (Table 15). Although not reflected in the ordination, these plots had more non-native vegetation than the plots in the other groups

(62%, 95%, 89%, 81%, and 72%, respectively; Nyoka 2004).

Tolowa, the North Spit and Bodega Head

Thorp and Gordon’s study (1991) of the Lanphere-Christiansen Dunes Preserve and Bodega Marine Reserve found 47 bee species at Bodega Marine Reserve and 43 species at the Lanphere-Christiansen Dunes Preserve. I found 23 species at Tolowa.

Wasbauer’s preliminary collection at Tolowa found six additional species (Appendix G).

The three coastal areas shared seven bee species that were common-to-abundant at one or more of the locations: Ceratina acantha , Epeolus minimus , Habropoda miserabilis ,

Bombus caliginosus, Bombus vosnesenskii , Lasioglossum pavonotum ,and Anthidium palliventre (Table 16). Andrena species were present at all three sites. Bodega Marine

Reserve and the Lanphere-Christiansen Dunes Preserve shared an additional seven species: Andrena saccata , Bombus californicus , Bombus caliginosus , Bombus sitkensis ,

Dialictus cabrilli , Dialictus longicornus, and Halictus rubicundus . Colletes hyalinus

oregonensis and Osmia integra were found at Tolowa and Lanphere, but not at Bodega.

Andrena barbilabris , Melissodes pallidisignata, and Colletes fulgides longiplumosus

were found at Tolowa and Bodega, but not at Lanphere. Anthophora bomboides

stanfordiana and Bombus bifarius were found only at Bodega.

DISCUSSION

Previous studies have shown the importance of understanding bee diversity and abundance within a landscape context (Stephen-Dewenter 2002, LeBuhn and Fenter

2008, Persson and Smith 2011). Results of my correlation analyses and ordinations revealed that the presence of invasive plants explained local differences in bee fauna at

Tolowa, and on a broader level, between Tolowa and the North Spit. At Tolowa, bees responded negatively to cover of A. arenaria and to cover of coastal scrub (an exotics- dominated plant association). In contrast, bee species richness and abundance increased in landscapes dominated by cover of native vegetation and, in particular, to cover of the resource-rich plant P. argentea . In addition, the response of individual species to the landscape was scale-dependent. Habropoda miserabilis , a large solitary bee, responded to differences in the landscape only at 1,050 m while Andrena concinnula , a small solitary bee, responded to variation in the landscape at 100 m and 250 m.

The landscape of the dunes at Tolowa resembles the “sky islands” of the

American southwest (Ricketts 2001, Economo 2011). Islands of open dune and native dune vegetation are surrounded by a matrix of A. arenaria . Flowering plants are few in areas of dense A. arenaria , limited to an occasional Anaphalis margaritacea (pearly everlasting) or Achillea millefolium (yarrow). These areas provide few resources for bees, although the cover provides nesting opportunities for rodents, and subsequently for bumble bees, which can nest in abandoned rodent holes (O’Toole and Raw 1991).

In contrast, patches of native vegetation at Tolowa offer both floral rewards and nesting opportunities for bees. Correlation analyses and ordination found a positive

21

22 relationship between solitary bee abundance and cover of native vegetation at all levels.

Bumble bee abundance was associated with dune meadow at 250 m. Abundance of

Habropoda miserabilis was positively correlated with dune mat at 1,050 m. There was a positive correlation between the abundance of nectar-rich P. argentea cover and solitary bees at all scales. Andrena concinnula abundance (at 100 m) and Colletes spp. abundance

(at 100 m and 250 m) was positively correlated with P. argentea cover. Solitary bee species richness was positively correlated with P. argentea at 100 m and 1,050 m.

Greater total area of floral resources was associated with native dune vegetation at

100 m and 250 m, which is not surprising since the only invasive at Tolowa is A. arenaria which lacks bee resources. But what is surprising is that neither correlation analysis nor ordination found total floral abundance to be a significant predictor of bee fauna at Tolowa, contrary to my expectation that bee fauna would be correlated with total available bee food. But possibly my sampling methods were inadequate to capture this expected correlation, because I used a sampling method developed to look at floral abundance in a Mediterranean landscape (Potts et al. 2003), not in a coastal dune ecosystem. Fortunately, like Nyoka (2004), I was able to look at floral abundance indirectly by using data on P. argentea as a surrogate for floral abundance. Nyoka (2004) used data on -phase dunemat in exactly this way. Both Nyoka (2004) and I found that the floral component of these types of vegetation was predictive of bee assemblages.

Bee size and corresponding home range may be determining the differing response to landscape variation at Tolowa. Small bees (such as Andrena concinnula )

23 were responsive to changes at 100 m and 250 m. Colletes fulgides longiplumosus and

Colletes hyalinus oregonensis, medium-sized bees, responded to landscape variation at

250 m. Bumble bees did not respond to variation at any scale. Bumble bees are capable of foraging up to 5 km (Goulson, 2003), so 1,050 m may be too fine a scale to detect bumble bee response to landscape variation. While it is appropriate to separate bee species into guilds such as solitary bees and bumble bees because of differences in life history traits (Steffen-Dewenter et al. 2002), the range in size of bees within these guilds can obscure response to scale. While all bumble bees are large and most solitary bees are small-to-medium-sized, there are large species of solitary bees, such as Habropoda miserabilis . At Tolowa, Habropoda miserabilis was responsive to resource variation only at 1,050 m.

In spring and summer, dunes free of A. arenaria offer abundant forage at Tolowa.

P. argentea blooms in areas of open dune from May through August. Open and moss- covered sand create nesting opportunities for bees such as Andrena concinnula ,

Habropoda miserabilis , and Anthidium palliventre. There are abundant nest resources for bumblebees in red fescue dune meadows. Dune wetlands have retained their native character because A. arenaria growth is inhibited in areas of high water table. Salix spp.

(), Trifolium spp. (), Lotus spp. (lotuses), and ursinus (California blackberry) offer abundant floral rewards. In wetlands, nest substrates are limited to species that can take advantage of wet, clay soils, such as bees in the genus Colletes , which line their nests in a waterproof, cellophane-like substance.

24

The dunes of the North Spit, like Tolowa, are a mosaic of vegetation types. Dune mat provides continued and varied floral resources from April through September (Nyoka

2004). Lathyrus littorali s (silky beach pea), a component of dune mat, blooms in a concentrated burst from late April through May. Invasive arboreus (yellow bush lupine, a component of the Coyote Brush association) and non-native Carpobrotus spp.

(sea fig) provide floral resources in degraded habitat. While A. arenaria has also fragmented native vegetation in these dunes, there are extensive areas of pristine dune vegetation still rich with native dune plants and areas of open sand.

Landscape differences at Tolowa and the North Spit are reflected in the bee fauna. The absence of compacted sand at the North Spit may account for the rarity there of Melissodes pallidisignata , an oligolege of summer composites (Moldenke and Neff

1974) that requires consolidated soil to nest. But this species is found at both Tolowa and at the Bodega Marine Reserve, where such soils are abundant. Oligolectic bees are

dependent on large bursts of single species blooms (Hisamatsu 2006). Osmia integra , an

oligolege of (Moldenke and Neff 1974), is abundant at the North Spit (Gorden

and Thorpe 1991; Nyoka, 2004, was surprised that she found < 3% Osmia integra , but

attributed this to the timing of her surveys). The abundance at the North Spit of Lathyrus

littoralis (Fabaceae) , with its large burst of bloom, may in part explain why Osmia

integra is common there. This species is rare at Tolowa, where there is little Lathyrus

littoralis . Megachile wheeleri, an oligolege of (Moldenke and Neff 1974), is

absent from Tolowa (where there is little Solidago spathulata ), but is the second most

common bee at the North Spit, where this plant is abundant . While present in both dune

25 systems, Anthidium palliventre , an oligolege of Phacelia and legumes (Moldenke and

Neff 1974), is relatively more abundant at Tolowa. Two factors may explain this: P. argentea is present at Tolowa but absent at the North Spit, and the red fescue-beach lupine alliance (dominated by a legume) is extensive at Tolowa but not at the North Spit.

Tolowa has, compared to the North Spit, a greater proportion of large bees and a lesser proportion of small bees. This difference may be due to greater habitat fragmentation at Tolowa. A small bee may not be able to overcome the poverty of floral resources available in small unlinked islands of native vegetation. For example, Andrena concinnula , a small solitary bee found only at Tolowa, was negatively correlated with A. arenaria cover at 100 m. Lasioglossum pavonotum, a small polylectic bee (Moldenke and

Neff 1974), represented 14.84% of all observations at the North Spit, but was a negligible presence at Tolowa. Ceratina acantha , another small polylectic bee, represented 3.52% of the total abundance at the North Spit but only 0.02% at Tolowa.

At Tolowa, A. arenaria invasion has diminished available bee resources, which

helps explain why larger bees such as bumble bees and Habropoda miserabilis comprise

a greater proportion of the total bee population there than at the North Spit. In marginal

environments, forage is scarce and bumble bees (relatively large bees) generally comprise

a greater proportion of bee faunas (Moldenke 1975). The relatively large size of

Habropoda miserabilis enables a greater foraging range (Greenleaf et al. 2007), and

allows them (like bumble bees) to take advantage of floral resources at small, disjunct

patches of intact dune mat such as the landscape at Tolowa.

26

The relative proportion of invasive plants (60% cover at Tolowa compared to

44% at the North Spit, Barbour et al. 2007) may partly explain differences in bee fauna between Tolowa and the North Spit, but differing types of invasives in these two locations may be more important in understanding these differences in bee fauna. Bee abundance and diversity are both much greater at the North Spit than at Tolowa, and I believe this is due to the relative paucity of floral resources at Tolowa compared to the

North Spit. At the North Spit, invaded areas have L. arboreus and Carpobotus spp., both of which are visited by foraging bees (Figure 8). But at Tolowa, invaded areas are dominated by A. arenaria , which provides no floral resources. This is probably why

bumble bees, correlated with exotics at the North Spit, were not correlated with invasive

plants at Tolowa. At Tolowa, flowers are only abundant where there is native dune mat or

dune swale; B. vosnesenskii , the most common bumble bee in both systems, was

negatively associated with invasive vegetation at Tolowa. In the combined ordination,

bee assemblages in the least degraded plots at Tolowa were similar to bee assemblages in

the most degraded plots at the North Spit (4, 5, 6, 7, 8, and 9 at Tolowa; 18, 20, 22, 24,

and 25 at the North Spit). This suggests that changes to bee fauna caused by

fragmentation (with its attendant degratory changes in plant species composition) are

more advanced at Tolowa. Müller et al. (2006) hypothesize that the recent decline of

many bee species is caused by food shortage. At Tolowa, probably a case in point, there

are not sufficient floral resources to support more bees.

Anthropogenic change is causing major declines in bee diversity (Frankie et al.

2009). Habitat loss is much greater for native bees than for other insect groups (Steffen-

27

Dewenter et al. 2005). The bee communities at both Tolowa and the North Spit evidenced changes in species composition and abundance due to habitat loss and fragmentation from invasive plants. In particular, the loss of habitat connectivity negatively affects bee abundance (Steffen-Dewenter 2003). Oligolectic ground nesting bees are especially vulnerable to decreasing habitat size (Cane et al. 2006). I am particularly concerned for

Tolowa: the loss of oligolectic dune bee species, the decreased proportion of solitary dune bees, and the corresponding increase in bumble bee abundance are all signals of bee decline. But a rare plant may preserve some degree of bee species diversity at Tolowa: as an abundant floral resource, P. argentea is able to make up in some measure for the increasing lack of forage as native dune habitat becomes smaller and more disjunct. The large-bodied bee species that have become proportionally more abundant as floral resources are lost (such as Habropoda miserabilis ) may act as bridge species for this rare plant, which is an obligate out-crosser that requires for successful reproduction. Because of its foraging range, Monroe (2010) found that Habropoda miserabilis possibly acts as a bridge between otherwise genetically-isolated patches of dune flora. Fortunately, wild bee communities have been shown to establish rapidly after restoration measures have been carried out (Exler et al. 2009).

Coastal dune restoration projects in Oregon and northern California have focused increasingly on providing habitat for one species, Western Snowy Plover (WSP;

Charadrius alexandrinus nivosus ). While restoration focused on single species may succeed in rescuing endangered species, the downside can be inadvertent damage to other species (Ehrenfeld 2000). Twenty years of coastal dune restoration in Oregon and

28

Washington has had the unintentional effect of reducing richness and abundance of native dune plants in sites managed for WSP, (Zarnetske et al. 2010). Common restoration methods to restore WSP habitat include use of heavy equipment and herbicides. Both methods are highly destructive of bee habitat, destroying nest substrate and reducing available forage. A community-wide restoration approach promises the best hope for recovery of Tolowa’s bees.

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Williams, N. M. and C. Kremen. 2007. Resource distributions among habitats determine solitary bee offspring production in a mosaic landscape. Ecological Applications 17: 910-921.

Williams, N. M., R. L. Minckley, and F. A. Silveira. 2001. Variation in native bee faunas and its implication for community changes. Conservation Ecology 5: 7. < http://www.consecol.org/vol5/iss1/art7/>. Accessed 2006 Oct 21.

Williams, N. M., E. E. Crone, T. H. Roulston, R. L. Minckley, L. Packer and S. G. Potts. 2010. Ecological and life-history traits predict bee species responses to environmental disturbances. Biological Conservation 143: 2280-2291.

Winfree, R., R. Aguilar, D. P. Vázquez, G. LeBuhn and M. A. Aizen. 2009. A Meta-Analysis of Bees' Responses to Anthropogenic Disturbance. Ecology 90: 2068-2076.

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TABLES AND FIGURES

Table 1. Plant associations and corresponding abbreviations used in vegetation analysis (Nyoka 2003).

Plant alliances/associations Dominant species

Native Coastal scrub (CS) Baccharis pilularis, Myrica californica, Gaultheria shallon

Dune mat (DM) Artemesia pycnocephala, , , Calystegia soldanella, Lupinus littoralis, Poa macrantha

Festuca rubra herbaceous alliance* Festuca rubra, Juncus lesueurii, Achillea (DME) millefolium

Dune woodland (DWL) Picea sitchensis, Pinus contorta ssp . contorta, Arctostaphylos uva-ursi

Forest (FOR) Picea sitchensis, Pinus contorta ssp . contorta, Vaccinium ovatum

Herbaceous wetland ( HWL) Juncus falcatus, Trifolium wormskioldii, Carex obnupta , Potentilla anserina ssp. pacifica

Shrub-dominated wetland (SWL) Salix hookerii

Wooded wetland (WWL) Salix sitchensis, Pinus contorta ssp. contorta

Exotic Ammophila arenaria semi-natural Ammophila arenaria herbaceous stands (AMAR)

Upland pasture dominated by non-native Bromus diandrus, Lolium perenne, grasses (XG) Anthoxanthum odoratum, Holcus lanatus, Cynosurus echinatus, Aira spp ., Vulpia spp

*Mapped as dune meadow.

35

36

Figure 1. Study site locations: Tolowa, Del Norte County, California; North Spit, Humboldt County, California and Bodega Marine Research Station, Mendocino County, California. Tolowa sites are numbered from south to north; plot 1 is the southernmost.

37

Table 2. Nest and floral resources found at study sites, south to north.

Site No. Nest Resources Floral Resources (limited, moderate or abundant; type)

1 Abundant open sand, some Limited ; Lupinus littoralis , Fragaria cryptogamic mat chiloensis

2 Cryptogamic mat, freshwater, Abundant; some Phacelia argentea, open sand Lupinus littoralis, abundant dune mat

3 Rodent nesting habitat, pithy Moderate : Salix hookeriana, Rubus stems ursinus, Aster chilensis, Senecio jacobaea

4 Freshwater, some open sand, Abundant; Polygonum paronychia, some cryptogamic mat, Lotus spp. some dune mat abundant wood.

5 Rodent nesting habitat Limited; Grindelia stricta var. compacted soil, pithy stems platyphylla,, Trifolium wormskjoldii

6 Open sand, cryptogamic mat Abundant; Phacelia argentea, abundant dunemat

7 Abundant cryptogamic mat, Abundant; Polygonum paronychia, compacted soil Lupinus littoralis, Phacelia argentea

8 Open sand, cryptogamic mat, Abundant; Phacelia argentea , abundant compacted soil dune mat

9 Open sand, cryptogamic mat Abundant; Phacelia argentea , abundant dune mat

10 Compacted soil, rodent nesting Limited; menziesii ssp. habitat concinnum, Anaphalis margaritacea

11 Abundant wood, rodent Limited; Erysimum menziesii spp. nesting habitat concinnum , some dune mat

12 Freshwater, sand cliffs, rodent Limited; Rubus ursinus, Malus fusca, nesting habitat Achillea millefolium

Table 3. Percent cover of major vegetation types and summary groups at 100m, 250m and 1,050m. Percent cover for all vegetation types and summary groups at 100 m, 250 m and 1,050 m can be found in Appendix A. A. arenaria Phacelia Dune mat Native vegetation Coastal scrub Exotic vegetation Plot argentea no. 100 250 1,05 100 250 1,050 100 250 1,050 100 250 1,050 100 250 1,050 100 250 1,050 m m 0m m m m m m m m m m m m m m m m 1 91 55 8 0 0 0.02 100 60 9 100 72 31 0 3 1 0 3 2 2 11 54 13 8 3 0.24 94 44 8 94 78 49 0 12 2 6 12 5 3 24 52 14 0 0 0.26 0 1 6 90 50 27 1 10 2 11 22 6 4 31 72 16 2 1 0.28 30 11 2 76 40 11 0 10 1 24 37 8 5 21 55 15 0 5 1.08 98 48 11 99 56 31 0 1 1 1 15 7 6 4 27 10 12 4 0.88 99 51 10 100 90 35 0 0 1 0 9 5 7 13 44 16 10 1 0.21 83 46 11 83 67 47 0 1 0 10 27 11 8 15 27 14 26 3 0.46 54 26 16 54 63 53 0 0 0 15 19 6 9 16 61 18 16 3 0.15 85 28 13 88 71 50 0 0 1 12 23 7 10 66 79 23 0 0 0.01 50 21 9 50 34 19 50 42 10 50 54 15 11 62 87 25 0 0 0 88 28 9 88 49 17 6 27 11 12 39 17 12 78 96 18 0 0 0 18 7 4 35 10 7 54 39 8 62 47 13

38

Table 4. Spearman rank correlation between major vegetation categories. Values in bold indicate significant correlation after Bonferroni correction ( p ≤ .0001). Values in bold italics indicate significant correlations after Holm’s correction (p ≤≤≤ .025).

A. Native Exotic P. Dune Herb. A. Native Exotic P. Dune Herb. aren- veg. veg. argen- mat wet-land aren- veg. veg. argen- mat wet-land aria 100 m 100 m tea 100 m 100 m aria 1,050m 1,050m tea 1,050m 1,050m 100 m 100 m 1,050m 1,050m Veg. r r r r r r r r r r r r Level category

A. arenaria 100 m 1 -0.245 0.357 -0.765 -0.252 -0.217 0.217 -0.310 -0.406 0.091 0.105 Native 100 m -0.244 1 -0.951 -0.075 0.783 0.006 0.322 -0.287 -0.193 -0.308 -0.307 vegetation Exotic 100 m 0.357 -0.951 1 -0.030 -0.811 0.070 0.350 0.217 0.000 0.245 0.364 vegetation Phacelia 100 m -0.765 -0.074 -0.030 1 0.123 -0.146 -0.181 0.127 0.501 0.063 0.243 argentea

Dune mat 100 m -0.252 0.783 -0.811 0.123 1 -0.280 -0.049 -0.510 0.151 -0.077 -0.126

H. wetland 100 m 0.093 -0.015 0.132 -0.275 -0.460 0.296 -0.561 0.374 -0.375 -0.706 -0.289

39

Table 4. Spearman rank correlation between major vegetation categories (continued).

A. Native Exotic P. Dune Herb. A. Native Exotic P. Dune Herb. aren- veg. veg. argen- mat wet- aren- veg. veg. argen- mat wet- aria 100 m 100 m tea 100 m land aria 1,050 1,050 tea 1,050 land 100 m 100 m 100 m 1,050 m m 1,050 m 1,050 m m m Veg. r r r r r r r r r r r r Level category A. 250 m 0.762 -0.371 0.524 0.051 0.151 0.047 0.105 0.308 -0.217 -0.427 0.147 0.168 arenaria Native 250 m -0.657 0.721 -0.797 0.560 0.741 -0.343 -0.042 -0.252 -0.119 0.133 -0.112 -0.224 veg. Exotic 250 m 0.427 -0.839 0.860 -0.276 -0.706 0.062 0.174 0.454 0.077 0.052 0.413 0.343 veg. Phacelia 250 m -0.761 0.297 -0.384 0.623 0.428 -0.008 -0.203 -0.181 0.109 0.436 -0.355 0.080 argentea Dune mat 250 m -0.301 0.734 -0.839 0.157 0.958 -0.460 -0.343 -0.077 -0.454 0.304 -0.055 -0.154 H. 250 m -0.434 0.104 -0.126 0.452 -0.154 0.398 -0.035 -0.112 0.489 0.350 -0.245 0.217 wetland

40

100%

90%

80%

70%

60% insect hole rodent hole 50% wood stone pithy stems 40% cryptogamic mat

open sand 30%

Propotion of Nest Substrate Availabilityby Type Availabilityby NestPropotion ofSubstrate 20%

10%

0% Plot 1 Plot 2 Plot 3 Plot 4 Plot 5 Plot 6 Plot 7 Plot 8 Plot 9 Plot 10 Plot 11 Plot 12 Plot Location

Figure 2. Proportional abundance of types of nest substrate at Tolowa by plot.

41

Table 5. Distribution of bee species found at Tolowa during plot surveys.

Plot1 Plot2 Plot3 Plot4 Plot5 Plot6 Plot7 Plot8 Plot9 Plot10 Plot11 Plot12 Andrena concinnula x x x x Anthidium palliventre x x x x x x x x Bombus vosnesenskii x x x x x x x x x x x Bombus mixtus x x x x x x x x x Bombus caliginosus x Bombus rufocinctus x Bombus spp. x x x x x x x Ceratina acantha x Colletes hyalinus oregonensis x x x x x x x Habrapoda miserabilis x x x x x x x x Hoplitis producta gracilis x x Lasioglossum pavanotum x x Megachile perihirta x x x x Mellisodes pallidisignata x x Nomada spp. x Osmia spp. x Osmia integra x Stelis leuchtricha x x x Xylocopa x

.

42

16

14 14

12 12

10 10 9 8 8

6 Number of Bee Species NumberBeeof 6 6

5 5 4 4 4 4

2

0 Plot 1 Plot 2 Plot 3 Plot 4 Plot 5 Plot 6 Plot 7 Plot 8 Plot 9 Plot 10 Plot 11 Plot 12 Site Number

Figure 3. Bee species richness at Tolowa, by site.

43

350

300

250 Bombus spp. Bombus mixtus Bombus voznesenskii

Misc. solitary bees 200 Stelis leucotricha Mellisodes pallidisignata Megachile perihita 150

Number ofbees Number Lasioglossum pavonotum Hoplitis sp. Habrapoda miserabilis 100 Colletes spp.

Anthidium palliventre

Andrena spp. 50

0 Plot1 Plot2 Plot3 Plot4 Plot5 Plot6 Plot7 Plot8 Plot9 Plot10 Plot11 Plot12 Site Number

Figure 4. Bee species abundance at Tolowa, all species by site.

44

45

Table 6. Bee species relative abundance pooled across all sites at Tolowa.

Relative Abundance Bee species All Sites B. vosnesenskii 32.43% Anthidium palliventre 24.09% Habropoda miserabilis 10.79% Bombus spp. 9.28% Andrena concinnula 8.02% B. mixtus 6.81% Colletes spp 3.89% Mellisodes pallidisignata 1.63% Stelis leuchotricha 0.88% Megachile perihirta 0.84% Hoplitis producta gracilis 0.63% Lasioglossum pavonotum 0.38% Osmia trevoris 0.20% Osmia integra 0.02% B. melanopygus 0.02% B. fervidus 0.02% Ceratina acantha 0.02% Nomada sp. 0.02% Xylococo sp. 0.02% All Bombus 49% All solitary bees 51%

Table 7. Spearman-rank correlation between bee abundance and major vegetation categories. Values in bold indicate significant correlations after Bonferroni correction ( p ≤ .001). Values in bold italics indicate significant correlations after Holm’s correction ( p ≤ .025).

Vegetation category Moderate to high Exotic Phacelia Bee group Plot level Native vegetation Dune mat A. arenaria vegetation argentea

r r r r r

100 m -0.895 0.350 -0.504 0.642 0.413

Solitary 250 m -0.161 0.636† -0.161 0.769 0.517 bees

1,050 m -0.373 0.643 -0.252 0.672 0.448

100 m -0.224 0.210 -0.280 0.198 -0.147

Bumble 250 m -0.224 0.357 -0.100 -0.072 -0.056 bees

1,050 m -0.446 0.336 -0.573† 0.130 -0.109

† not significant but of interest.

46

Table 7. Spearman-rank correlation between bee abundance and selected vegetation categories (continued).

Vegetation category Phacelia Bee group Plot level A. arenaria Native vegetation Exotic vegetation Dune mat argentea r r r r r 100 m -0.832 0.200 -0.374 0.644 0.320 Andrena 250 m -0.224 0.666 -0.399 0.526 0.395 concinnula 1,050 m -0.493 0.603† -0.204 0.383 0.271

100 m -0.523 0.043 -0.092 0.557 0.075 Anthidium 250 m -0.523 0.178 0.327 0.531 0.149 palliventre 1,050 m -0.067 0.249 -0.135 0.590 0.330

100 m -0.908 0.374 -0.458 0.671 0.378

Colletes spp. 250 m -0.642 0.759 -0.396 0.719 0.389

1,050 m -0.389 0.788 -0.258 0.509 0.491

100 m -0.231 0.185 -0.320 0.281 0.466 Habropoda 250 m -0242 0.285 0.160 0.399 0.555 miserabilis 1,050 m 0.102 0.580 -0.157 0.197 0.880

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Table 7. Spearman-rank correlation between bee abundance and selected vegetation categories (continued).

Vegetation category Native Exotic Phacelia Bee group Plot level A. arenaria Dune mat vegetation vegetation argentea r r r r r

100 m -0.113 -0.102 0.113 0.123 -0.473

Mellisodes 250 m -0.111 -0.075 0.073 -0.039 -0.473 pallidisignata

1,050 m -0.259 0.220 -0.231 0.312 0.081

100 m -0.324 0.391 -0.440 0.175 0.014 Bombus 250 m -0.322 0.476 -0.455 0.087 0.084 vosnesenskii

1,050 m -0.541† 0.412 -0.601† 0.312 -0.042

100 m 0.098 -0.049 0.014 0.041 -0.336

Bombus 250 m 0.099 0.018 -0.035 -0.282 0.099 mixtus 1,050 m -0.355 -0.081 -0.095 0.011 -0.176

† not significant but of interest.

48

Table 8. Spearman-rank correlation between bee richness and selected vegetation categories. Values in bold indicate significant correlations after Bonferroni correction ( p ≤ .002). Values in bold italics indicate significant correlations after Holm’s correction (p ≤ .05).

Vegetation category Exotic Phacelia Bee group Plot level A. arenaria Native vegetation Dune mat vegetation argentea

r r r r r 100 m -0.895 0.318 -0.480 0.677 0.201

Solitary 250 m -0.705 0.664 -0.208 0.469 0.332 bees

1,050 m -0.551 0.813 -0.498 0.556 0.624

100 m -0.071 -0.563 0.508 0.508 -0.618

Bumble 250 m -0.414 -0.214 0.198 -0.118 -0.508 bees

1,050 m 0.127 0.046 -0.092 0.040 0.019

49

Table 9. Correlation coeffiecients between the abundance of vegetation and vegetation groups at 100 m, 250 m and 1,050 m and the first two ordination axes, from an NMS ordination of 19 bee species and 36 variables at 12 study sites, Tolowa Dunes. Values in bold are for r values ≥ ± 0.500. Correlation coefficients ( r) Variable Axis 1 Axis 2 Spatial scale 100 m 250 m 1,050 m 100 m 250 m 1050 m Vegetation categories A. arenaria (> 20%) - 0.742 - 0.544 0.073 0.455 0.420 - 0.469 Phacelia argentea 0.404 0.651 - - 0.179 - 0.157 - A. arenaria semi-natural - 0.014 0.217 0.287 - 0.257 0.051 - 0.034 stands Coastal scrub - 0.688 - 0.568 - 0.271 0.485 0.532 - 0.630 Dune mat 0.607 0.475 0.196 0.151 0.007 0.543 F. rubra herbaceous alliance - 0.219 - - - 0.576 - Herbaceous swale - 0.344 0.194 0.266 - 0.476 0.366 0.523 Wooded swale - 0.065 0.032 - 0.245 0.257 Forest - - 0.090 - 0.012 - 0.077 - 0.071

Shrub dominate swale - 0.242 0.003 - 0.017 0.658 Exotics-dominate meadow - - 0.307 - - -0.591 Vegetation groups Native 0.616 0.718 0.277 - 0.320 - 0.082 0.695 Exotic - 0.703 - 0.446 - 0.253 0.407 0.560 - 0.655

50

51

Table 10. Correlation coefficients between the abundance of nest substrate at 100 m and the first two ordination axes, from an NMS ordination of 19 bee species and 36 variables at 12 study sites, Tolowa Dunes. Values in bold are for r values ≥ ± 0.500.

Correlation coefficients ( r) Variable Axis 1 Axis 2 Nest substrates Open sand 0.233 0.358 Cryptogamic mat 0.009 - 0.481 Pithy stems 0.293 0.025 Rodent holes 0.200 0.036 Wood 0.293 0.221

Table 11. Correlation coefficients between the abundance of floral resources at 100 m and the first two ordination axes, from an NMS ordination of 19 bee species and 36 variables at 12 study sites, Tolowa Dunes. Values in bold are for r values ≥ ± 0.500.

Correlation coefficients ( r) Variable Axis 1 Axis 2 Floral abundance Total all species 0.074 0.565 Achillea millifolium 0.012 0.431 Erigeron glaucus 0.213 - 0.011 Eriogonum latifolium 0.197 - 0.227 Erysimum menziesii ssp. concinnum 0.172 0.166 Fragaria chiloensis - 0.249 - 0.027 Hypochaeris radicata 0.125 0.498 Lupinus littoralis 0.225 - 0.252 Polygonum paronychia 0.214 - 0.128

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Table 12. Correlation coefficients between the abundance of bee species and bee functional groups at 100 m and the first two ordination axes, from an NMS ordination of 19 bee species and 36 variables at 12 study sites, Tolowa Dunes. Correlation coefficients ( r) Variable Axis 1 Axis 2 Bee species Andrena concinnula 0.474 - 0.379 Anthidium palliventre 0.384 - 0.010 Bombus vosnesenskii 0.198 - 0.707 Bombus mixtus - 0.883 - 0.189 Bombus sitchensis - 0.114 - 0.524 Bombus ssp. - 0.134 - 0.536 Colletes spp. 0.606 - 0.397 Habropoda miserabilis 0.459 - 0.033 Megachile perihirta 0.093 - 0.405 Stelis leucotricha 0.205 - 0.133 Bee groups All solitary 0.729 - 0.356 All bumble bees - 0.065 - 0.690

Values in bold are r values ≥ ± 0.500.

Table 13. Correlation coefficients between the abundance of other categories at 100 m, 250 m and 1,050 m and the first two ordination axes, from an NMS ordination of 19 bee species and 36 variables at 12 study sites, Tolowa Dunes. Values in bold are r values ≥ ± 0.500.

Correlation coefficients ( r) Variable Axis 1 Axis 2 Spatial scale 100 m 250 m 1,050 m 100 m 250 m 1050 m Categories Beach - - 0.142 0.273 - 0.272 - 0.415 Open Sand - - 0.218 - 0.004 - Developed - 0.651 - 0.176 - 0.351 - (roads and trails) Water - - 0.509 - 0.101 - 0.000 - 0.269

53

Plot 10

native vegetation shrub 1,050m swales 1,050m coastal Plot 11 coastal scrub

250m Ammophila scrub arenaria 100m 100m Axis 2 Axis exotic Plot 4 Plot 5 vegetation Plot 8 P.argentea 100m native 250m B. mixtus veg. Plot 1 Plot 9 250m Plot 12 Plot 6 native all veg. solitary bees coastal 100m

scrub 1,050m Plot 7 exotic Plot 2 veg. all B. 250m Bombus voznesenskii

Plot 3

Axis 1

Figure 5. Bi-plot resulting from nonmetric multidimensional scaling of bee fauna at Tolowa Dunes. Bee community is represented by squares (n =12) and environmental variables by vectors (n = 55). Only vectors with an r² value > 0.400 are shown. The color of the square indicates group membership, (MRPP, T = -4.164, p = 0.002).

54

Table 14. Relative abundance of bee species at Tolowa and the North Spit.

Species Tolowa North Spit Oligolectic? B. vosnesenskii 32.43% 19.04% Megachile wheeleri < 0.01% 19.49% yes Anthidium palliventre 24.09% 16.61% yes Habropoda miserabilis 10.79% 6.27% B. spp. 9.28% - Andrena concinnula 8.02% absent B. mixtus 6.81% 5.47% Colletes spp. 3.89% 3.94% Mellisodes pallidisignata 1.63% 0.05% yes Stelis leuchotricha 0.88% 2.02% Megachile perihirta 0.84% 0.17% Hoplitis producta gracilis 0.63% absent Lasioglossum pavonotum 0.38% 14.84% Osmia trevoris 0.20% absent Osmia integra 0.02% 2.27% yes B. melanopygus 0.02% 0.01% B. fervidus 0.02% 0.00% Ceratina acantha 0.02% 3.52% Nomada sp. 0.02% 0.00% Xylococa sp. 0.02% absent B. insularis absent 1.36% Apis mellifera absent 1.22% Hylaeus spp. absent 0.70% Epeolus minimus absent 0.67% B. sitchensis absent 0.60% Coelioxys rufitarsus absent 0.43% B. caliginosus absent 0.38% B. californicus absent 0.31% B. nevadensis absent 0.15% B. rufocinctus absent 0.15% Sphecodes sp. absent 0.14% Halictus sp. absent 0.12% B. huntii absent 0.03% B. edwardsii absent 0.03% B. fernaldii absent 0.01% Agapostemon sp. absent 0.01%

55

Table 15. Summary statistics for NMS ordination axes for combined Tolowa and North Spit ordination. Values over 0.500 are bolded.

Correlation coefficients ( r) Variable Axis 1 Axis 2 Bee species Andrena ssp. 0.393 -0.397 Anthidium palliventre 0.622 -.178 Bombus vosnesenskii 0.151 0.596 Bombus mixtus 0.289 -0.489 Bombus sitchensis 0.001 0.146 Bombus sp. .119 .551 Ceratina acantha 0.169 0.261 Colletes hyalinus oregonensis 0.534 0.145 Habropoda miserabilis 0.162 0.290 Lasioglossum pavonotum 0.109 0.151 Megachile wheeleri -0.049 0.504 Bee groups All solitary 0.439 0.743 All bumble bees 0.683 0.468 Vegetation Phacelia argentea 0.283 0.099 A. arenaria semi-natural stands 0.072 -0.010 Coyote Brush (Coastal scrub) -0.555 -0.490 Dune mat 0.213 -0.358 Herbaceous wetland 0.278 -0.305 Yellow bush lupine -0.131 -0.178 Ice plant -0.228 0.072 Other Developed -0.018 0.138 Open sand -0.170 0.256

Vegetation groups Native 0.376 0.258 Exotic -0.320 -0.019

56

Plot 11 Plot 14 Plot 16 All solitary bees Plot 18 Plot 6 Anthidium palliventre Plot 17 Plot 15 Plot 20 Plot 8 Plot 19 Plot 5

Plot 24 Plot 25 Plot 7

Plot 4 Plot 22

Bombus vosnesenskii Axis 2 Plot 9 Plot 2 coyote brush Plot 23 All Bombus

Plot 21 Plot 13

Plot 3 Plot 1

Plot 12

Axis 1

Figure 6. Bi-plot resulting from nonmetric multidimensional scaling of the bee fauna at Tolowa Dunes and the North Spit. Bee community is represented by square and round icons, (n =24), and environmental variables by vectors (n =41). Only vectors with an r² value > 0.300 are shown. Plots at the North Spit are represented by round icons. Plots at Tolowa are represented by square icons. The color of the plot icon indicates group membership (MRPP, T –1.902, p = 0.053). Green = group 1, blue = group 2 and red = group 3. New site numbers were created for Nyoka’s plots, to avoid duplicates, (Appendix F).

57

Bees per hour 0 1 2 3 4 Agapostemon Andrena concinnula Anthidium palliventre Apis melifera Bombus caliginosus Bombus edwardsii Bombus fervidus Bombus hunteri Bombus insularis Bombus melanopygus Bombus mixtus Bombus nevadensis Bombus rufocintus Bombus sitkensis Bombus spp. Bombus vosnesenskii Ceratina acantha Coelioxys rufitarsus Colletes hyalinus oregonensis Epeolus minimus Habrapoda miserabilis Halictus Hoplitis producta gracilis Hylaeus Lasioglossum pavonotum Megachile perihirta Megachile wheeleri Mellisodes pallidisignata Nomada Osmia integra Sphecodes Stelis leuchotricha Xylocopa a) Tolowa bee observations per hour.

Bees per hour 0 2 4 6 8 10 12 14 16 18 Agapostemon Andrena concinnula Anthidium palliventre Apis melifera Bombus caliginosus Bombus edwardsii Bombus fervidus Bombus hunteri Bombus insularis Bombus melanopygus Bombus mixtus Bombus nevadensis Bombus rufocintus Bombus sitkensis Bombus spp. Bombus vosnesenskii Ceratina acantha Coelioxys rufitarsus Colletes hyalinus oregonensis Epeolus minimus Habrapoda miserabilis Halictus Hoplitis producta gracilis Hylaeus Lasioglossum pavonotum Megachile perihirta Megachile wheeleri Mellisodes pallidisignata Nomada Osmia integra Sphecodes Stelis leuchotricha Xylocopa b) North Spit bee observations per hour.

Figure 7. Comparison of bee fauna at Tolowa versus the North Spit: a) number of bees by species, per observation hour, at Tolowa and b) number of bees by species, per observation hour, at the North Spit.

58

Hectares 0 2 4 6 8 10

developed open sand

dune mat

herbaceous wetland native vegetation

yellow bush lupine sea fig

coyote brush

A. arenaria stands exotic meadows

exotic vegetation Phacelia argentea a) Plot vegetation Tolowa. Hectares 0 2 4 6 8 10 12 14 16 18

developed open sand

dune mat

herbaceous wetland native vegetation

yellow bush lupine sea fig

coyote brush

A. arenaria stands exotic meadows

exotic vegetation Phacelia argentea b) Plot vegetation at Tolowa.

Figure 8. Comparison of plot vegetation at Tolowa and the North Spit: a) 1 hectare plot compositon by vegetation type, Tolowa and b) 1 hectare plot composition by vegetation type, North Spit.

59

Table 16. Bees that are common to abundant at one or more sites. Abundance scale; R = < 5; U = 5-10; O = 11-25; C = 26-50; A = > 50.

Bees Tolowa Bodega Lanphere- Dunes Marine Christensen Reserve Dunes Preserve Andrenidae Andrena saccata - A R Andrena plumiscopa - C - Andrena barbilabris R A - Andrena concinnula A - - Anthophoridae Anthophora bomboides stanfordiana - A - Ceratina acantha R A C Epeolus minimus R C O Habropoda miserabilis A A A Melissodes pallidisignata C A - Apidae Apis mellifera - U A Bombus californicus - R C Bombus bifarius - A - Bombus caliginosus - O C Bombus mixtus C - A Bombus sitkensis - R A Bombus vosnesenskii A A A Colletidae Colletes fulgides longiplumosus C A - Colletes hyalinus oregonensis C - C Halictidae Dialictus cabrilli - C U Dialictus longicornus - A A Halictus rubicundus - A O Lasioglossum pavonotum U A A Anthidium palliventre A O A Coelioxys rufitarsus - - C Megachile wheeleri - - A Osmia integra R - C

APPENDIX A

Site characterization at 100 m, 250 m and 1,050 m.

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Table A1. Site characteristic percent cover at Tolowa at 100 m.

Ammophila Exotic plant Native plant associations Other arenaria Phacelia associations No. Site Name > 20% argentea DM DME HWL OS SWL NATIVE AMAR CS EXOTIC Dev 1 South Dune 91 0 100 0 0 0 0 100 0 0 0 0 2 Airport 11 8 94 0 0 0 0 94 6 0 6 0 3 Pt. St. 24 0 0 22 68 0 0 90 10 1 11 0 George 4 Sweetwater 31 2 30 11 34 0 0 76 24 0 24 0 5 Stone 21 0 98 0 1 0 0 99 1 0 1 0 Barrens 6 Lake Talawa 4 12 99 0 1 0 0 100 0 0 0 0 7 Sage 13 10 83 0 0 0 0 83 10 0 10 6 Barrens 8 Kellogg 15 26 54 0 0 30 0 54 15 0 15 0 9 Superdune 16 16 85 0 0 0 2 88 12 0 12 0 10 Wallflower 66 0 50 0 0 0 0 50 0 50 50 0 Barrens 11 Woodlot 62 0 88 0 0 0 0 88 6 6 12 0 12 Smith River 78 0 18 0 18 2 0 35 8 54 62 0

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Table A2. Site characteristic percent cover at Tolowa at 250 m.

A. Exotic plant Native plant associations Other Plot arenaria Phacelia associations No. > 20% argentea DM DME DWL HWL SWL WWL NATIVE AMAR CS EXOTIC DEV FOR OS WA 1 55 0 60 0 8 4 0 0 72 3 3 3 0 1 21 0 2 54 3 44 .24 8 0 1 0 78 0 12 12 0 0 0 9 3 52 0 1 20 3 26 0 0 50 12 10 22 0 0 1 0 4 72 1 11 1 13 15 0 0 40 27 10 37 0 23 0 0 5 55 5 48 0 0 8 0 0 56 14 1 15 0 0 0 22 6 27 4 51 3 0 36 0 0 90 9 0 9 0 0 0 1 7 44 1 46 0 0 16 5 0 67 26 1 27 0 0 0 0 8 27 3 26 2 0 11 23 0 63 19 0 19 3 0 14 0 9 61 3 28 1 0 17 26 0 71 23 0 23 0 0 0 1 10 79 0 21 0 3 8 2 1 34 12 42 54 0 1 0 4 11 87 0 28 0 19 1 1 0 49 12 27 39 0 0 0 5 12 96 0 7 0 0 3 0 0 10 8 39 47 0 1 0 38

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Table A3. Site characteristic percent cover at 1,050 m.

A. Exotic plant Other Plot Native plant associations arenaria Phacelia associations no. > 20% argentea DM DME DWL HWL SWL WWL NATIVE AMAR CS EXOTIC DEV FOR OS WA BCH 1 8 .02 9 0 0 9 9 4 31 1 1 2 4 53 4 10 0 2 13 .24 8 3 3 25 9 1 49 3 2 5 3 24 0 10 2 3 14 .26 6 3 5 13 0 0 27 4 2 6 1 20 0 33 4 4 16 .28 2 0 6 3 0 0 11 7 1 8 0 38 0 38 4 5 15 1.08 11 0 2 5 13 0 31 6 1 7 0 0 0 44 2

6 10 .88 10 0 0 17 8 0 35 4 1 5 0 6 0 38 3

7 16 .21 11 0 0 28 8 0 47 11 0 11 2 1 0 35 2 8 14 .46 16 0 0 18 19 0 53 6 0 6 2 1 2 33 1 9 18 .15 13 0 0 16 8 12 50 6 1 7 0 7 0 34 2 10 23 .01 9 0 5 3 1 1 19 5 10 15 0 11 0 37 3 11 25 0 9 0 3 3 1 1 17 6 11 17 0 6 0 42 3 12 18 0 4 0 0 2 1 0 7 5 8 13 0 1 0 53 3

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APPENDIX B

Floral Visitation and Floral Surveys

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Flower Visitation

The most visited plant was Polygonum paronychia (beach knotweed, 151 visits total); the next most-visited flower was P. argentea (138 visits). Nine species accounted

for 95% of all flower visitations: P. paronychia , P. argentea , Eriogonum latifolium

(beach buckwheat), Lupinus littoralis (beach lupine), Senecio jacobaea (tansy ragwort),

Aster chilensis (California aster), Erigeron glaucus (seaside daisy), Grindelia stricta var.

platyphylla (gumplant), and Lotus formosissimus (coastal lotus). The most visits recorded

at a site were 126 and the fewest visits at a site were two. A complete list of floral visits

by bee species follows in Appendix C

The number of bee visits to flowers recorded at a site ranged from two to 126. B.

vosnesnskii , the most abundant bumble bee species, visited the greatest number of plant

species (22). Anthidium palliventre , the most abundant solitary bee species, visited 10

species of flowers.

Table B1. Bee floral visits to the 11 most visited species of flowers at Tolowa

Flower species Percent of Total Visits

Polygonum paronychia 20% Phacelia argentea 18% Eriogonum latifolium 12% Lupinus littoralis 12% Senecio jacobaea 9% Aster chilensis 7% Miscellaneous species 5% Grindelia stricta var . platyphylla 5% Erigeron glaucus 5% Lotus formosissimus 3% Hypocharis radicata 2% Lotus corniculatus 1%

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Plant species visited by bees during survey hours. Nomenclature follows Jepson . Eschsch. Achillea millefolium L. Agoseris apargioides (Less.) E. Greene var. eastwoodiae (Fedde) Munz Anaphalis margaritacea (L.) Benth. & Hook. Armeria maritima (Miller) Willd. ssp. californica (Boiss.) Pors. Arctostaphylos uva-ursi (L.) Sprengel f. coactilis (Fern. & Macbr.) P. Wells Aster chilensis Nees Camissonia cheiranthifolia (Sprengel) Raim Castilleja exserta (A.A. Heller) Chuang & Heckard ssp. latifolia (S. Watson) Chuang & Heckard Carex obnupta L. Bailey Calystegia soldanella (L.) R. Br. vulgare (Savi) Ten. Claytonia sibirica L. Conyza bonariensis (L.) Cronq. Erigeron glaucus Ker-Gawler Eriogonum latifolium Smith Erysimum menziesii (Hook.) Wettst. ssp. concinnum (Eastw.) R A. Price Fragaria chiloensis (L.) Duchesne Gnaphalium palustre Nutt. Grindelia stricta DC. var. platyphylla (E. Greene) M.A. Lane Hypochaeris radicata L. Leontodon taraxacoides (Villars) MŽrat Lotus corniculatus L. Lotus formosissimus E. Greene

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Lotus purshianus (Benth.) Clements & E.G. Clements var. purshianus Lupinus bicolor Lindley Lupinus littoralis Douglas Mentha arvensis L. Navarretia squarrosa (Eschsch.) Hook. & Arn. Parentucellia viscosa (L.) Caruel Phacelia argentea Nelson & J.F. Macbr. Polygonum paronychia Cham. & Schldl Ranunculus repens L. Rubus ursinus Cham. & Schldl. Salix hookeriana Hook. Senecio jacobaea L. Senecio sylvaticus L. Stachys ajugoides Benth. var. ajugoides Stellaria media (L.) Villars Trifolium microcephalum Pursh Viola adunca Smith

APPENDIX C

Floral Visitation at Tolowa by Bee Species .

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List of Most Visited Plant Species (95% of Total Visits) by Bee Species Andrena spp. Abronia latifolia Anthidium palliventre Erigeron glaucus Eriogonum latifolium Grindelia stricta var . platyphylla Lotus corniculatus Lupinus littoralis Phacelia argentea Polygonum paronychia Bombus voznesenskii Abronia latifolia Aster chilensis Erigeron glaucus Eriogonum latifolium Erysimum menziesii ssp. concinnum Grindelia stricta var . platyphylla Hypochaeris radicata Lotus formosissimus Lotus corniculatus Lupinus littoralis Phacelia argentea Polygonum paronychia Senecio jacobaea Bombus mixtus

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Phacelia argentea Senecio jacobaea Colletes spp. Erigeron glaucus Eriogonum latifolium Grindelia stricta var . platyphylla Lupinus littoralis Phacelia argentea Polygonum paronychia Habropoda miserabilis Erysimum menziesii ssp. concinnum Hoplitis product gracilis Phacelia argentea Lasioglossum pavanotum Hypochaeris radicata Megachile perihirta Aster chilensis Erigeron glaucus Grindelia stricta var . platyphylla Melissodes pallidisignata Aster chilensis Grindelia stricta var . platyphylla Lotus corniculatus Senecio jacobaea Osmia integra Polygonum paronychia

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Stelis leuchotricha Erigeron glaucus Hypochaeris radicata Phacelia argentea

APPENDIX D Bee Species Observed at Tolowa Dunes, March through August, 2007.

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Species determinations were made by Robbin Thorp. Species marked with an asterisk were collected outside of study plots.

Andrenidae Andrena (Leucandrena) barbilabris Kirby * Andrena (paradrena ) concinnula Robertson Anthophoridae Ceratina (Zadontomerus ) acantha Provancher Epaeolus (Epaeolus ) minimus (Robertson) * Habropoda miserabilis (Cresson) Melissodes (Eumelissodes ) pallidisignata Cockerell Apidae Bombus ( ) melanopygus Nylander * Bombus (Fervidobombus ) fervidus Fabricius Bombus (Pyrobombus ) mixtus Cresson Bombus (Pyrobombus ) vosnesenskii Radoszkowski Nomada sp. * MRM Xylocopa sp. (Latreille) Colletidae Colletes hyalinus oregonensis TimberLake Colletes fulgidus longiplumosus Stephan Halictidae Lasioglossum pavonotum (Cockerell) Lasioglossum (Evyleus ) kincaidii Cockerell Sphecodes sp. Megachilidae

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Anthidium (Anthidium ) palliventre Cresson Hoplitis producta gracilis Cresson Megachile (Xanthosaurus ) perihirta Osmia (Acanthosimoides ) integra Cresson Osmia (Melanosmia ) trevoris Cockerell Stelis (Stelis) leuchotricha (Cockerell )

APPENDIX E

Indicator Species Analysis Results.

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Table E. Indicator species for A. arenaria cover. Values in bold indicate statistically significant results (p ≤ 0.05).

Group Indicator species Indicator value P

Low cover of A. All Bombus 74.3 0.146 arenaria (<25%) All solitary bees 85.8 0.004

Anthidium palliventre 68.8 0.092

Bombus vosnesenskii 75.3 0.039

Colletes spp. 87.5 0.013

High cover of A. Bombus mixtus 42.6 0.888 arenaria (> 60%)

APPENDIX F

Site Number Correspondence With Nyoka’s Study (2004) of the North Spit.

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Table F. Site number correspondence with Nyoka’s study (2004) of the North Spit

Plot number Plot number Plot Name Nyoka (2004) 1 South Dune 2 Airport (Del Norte) 3 Point Saint George 4 Sweetwater 5 Stone Barrens 6 Lake Talawa 7 Sage Barrens 8 Kellogg 9 Superdune 10 Wallflower Barrens 11 Woodlot 12 Smith River 13 1 Clam Beach 14 2 Mad River 15 3 Lanphere 1 16 4 Lanphere 2 17 5 Gun Club 18 6 Lupine Avenue 19 7 Manila community Center 20 8 Powerline 21 9 Pit 22 10 Mill 23 11 Airport (Humboldt) 24 12 Eureka 25 13 Samoa

APPENDIX G Bee Species Collected by Marius Wasbauer at Tolowa Dunes, 2010.

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Bee species collected by netting and pan-traps, September and October, 2010 by Marius

Wasbauer. Species determinations were made by Robbin Thorp, Entomology, UC Davis

(24 November 2010). (w = worker, q = queen, m = male, f = female)

[Families: 3; Genera: 8; species: 15]

APIDAE [Genera: 2; species: 5]

Bombus caliginosus (Frison) 2w

Bombus melanopygus Nylander 3q

Bombus mixtus Cresson 4q, 3w, 1m

Bombus vosnesenskii Radoszkowski 12w, 4m

Ceratina acantha Provancher 30f, 6m

HALICTIDAE [Genera: 4; species: 8]

Agapostemon texanus Cresson 27f, 6m

Halictus tripartitus Cockerell 2f

Lasioglossum olympiae (Cockerell) 19f, 4m

Lasioglossum pacificum (Cockerell) 18f, 3m

Lasioglossum pavonotum (Cockerell) 17f, 13m

Lasioglossum zonulum (Smith)

Lasioglossum (Dialictus ) sp. 6f, 1m

Lasioglossum (Evylaeus ) sp. 1f

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Sphecodes sp. 6f, 1m

MEGACHILIDAE [Genera: 2; species: 2]

Anthidium palliventre Cresson 1f

Megachile perihirta Cockerell 2f