Spatial predictability and resource specialization of bees (Hymenoptera: Apoidea) at a superabundant, widespread resource

Biological Journal of the Linnean Society (1999), 67: 119–147. With 6 figures Article ID: bijl.1998.0295, available online at http://www.idealibrary.com on

Spatial predictability and resource specialization of bees (Hymenoptera: Apoidea) at a superabundant, widespread resource ROBERT L. MINCKLEY1, JAMES H. CANE2, LINDA KERVIN2 AND T. H. ROULSTON Department of Entomology, 301 Funchess Hall, Auburn University, Auburn, AL 36849–5413, U.S.A. Received 10 June 1998; accepted for publication 9 October 1998

For reciprocal specialization (coevolution) to occur among floral visitors and their host plants the interactions must be temporally and spatially persistent. However, studies repeatedly have shown that species composition and relative abundance of floral visitors vary dramatically at all spatial and temporal scales. We test the hypothesis that, on average, pollen specialist bee species occur more predictably at their floral hosts than pollen generalist bee species. Taxonomic floral specialization reaches its extreme among species of solitary, pollen-collecting bees, yet few studies have considered how pollen specialization by floral visitors influences their spatial constancy. We test this hypothesis using an unusually diverse bee guild that visits creosote bush (Larrea tridentata), the most widespread, dominant plant of the warm deserts of North America. Twenty-two strict pollen specialist and 80+ generalist bee species visit Larrea for its floral resources. The sites we sampled were separated by 0.5 to >1450 km, and spanned three distinct deserts and four vegetation zones. We found that species of Larrea pollen specialist bees occurred at more sites and tended to be more abundant than generalists. Surprisingly, spatial turnover was high for both pollen specialist and generalist bee species at all distances, and species composition of samples from sites 1–5 km apart varied as much as repeat samples made at single sites. Nevertheless, the pattern of bee species turnover was not haphazard. As distance among sites increased faunal similarity of sites decreased. Faunal similarities among sites within 250 km of each other were generally greater than if randomly distributed over all sites (the null model). No single ecological category of species (widespread, localized, Larrea pollen specialist, floral generalist) accounted for this spatial predictability. Evidently, concordant local distribution patterns of many ecologically diverse species contribute to the non-random spatial pattern. The ecological dominance of creosote bush does not confer obvious ecological advantages to its specialist floral visitors. Spatial turnover is comparable to that found for bee guilds from other biogeographic regions of the world and is not therefore limited to those bee species that inhabit highly seasonal climates, such as deserts. Philopatry and differences in bloom predictability among sites are probably more important causes for spatial turnover of bee species than are interspecific competition for nest sites or floral resources.  1999 The Linnean Society of London

1

Corresponding author. Email:[email protected] Present address: United States Department of Agriculture-ARS, Bee Biology and Systematics Laboratory, Utah State University, Logan, Utah, U.S.A. 2

0024–4066/99/050119+29 $30.00/0

119

 1999 The Linnean Society of London

120

R. L. MINCKLEY ET AL.

ADDITIONAL KEY WORDS:—deserts – biogeography – species turnover – pollinator assemblage – Zygophyllaceae – Larrea – variation – oligolecty – abundance – species composition. CONTENTS

Introduction . . . . . . . . . . . . . . . . . . . Larrea and its bee guild . . . . . . . . . . . . . . . The plant . . . . . . . . . . . . . . . . . . The Larrea bee guild . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . Study sites . . . . . . . . . . . . . . . . . . Sampling protocol and bee identification . . . . . . . . Resource specialization . . . . . . . . . . . . . . Comparisons of faunal similarity . . . . . . . . . . Decay . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . General characteristics of sites and their Larrea bee faunas . . Sampling reliability . . . . . . . . . . . . . . . Resource specialization, abundance and distribution . . . . Faunal similarity of sites within ecoregions . . . . . . . Faunal similarity among nearby sites and in contiguous habitat Faunal similarity of resampled sites . . . . . . . . . . Faunal similarity across all sites . . . . . . . . . . . Faunal similarity of sites across ecoregions . . . . . . . Decay approach . . . . . . . . . . . . . . . . Differences of plant characteristics among sites . . . . . . Discussion . . . . . . . . . . . . . . . . . . . Sampling reliability and species abundance . . . . . . . Ecological role and spatial predictability . . . . . . . . Spatial structure of the Larrea bee guild . . . . . . . . Why are spatial patterns of floral visitors so unpredictable? . . Acknowledgements . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . Appendix 1 . . . . . . . . . . . . . . . . . . . Appendix 2 . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

120 121 121 121 122 122 123 124 125 125 126 126 126 127 128 129 129 131 131 133 133 133 136 137 138 138 140 140 144 146

INTRODUCTION

Insects that visit flowers for the resources they offer are often cited as examples of mutualists. However, studies of flower-visiting insects have consistently concluded that the spatio-temporal variation in species composition and relative abundance is too great for reciprocal selection to occur between any one insect species and its floral host (Thompson, 1994). Among the most comprehensive studies was that of Herrera (1988) who simultaneously examined the spatial and temporal variation of floral visitors to one perennial shrub species for 6 years at four sites. At one site he found that only one-third of the 70 taxa occurred every year and the relative abundance of most species varied drastically. Studies have reported similar fluctuations that have included one (Guitia´n, Guitia´n & Navarro, 1996; Herrera, 1995) or multiple floral hosts (Petanidou & Ellis, 1993; Steinbach & Gottsberger, 1994), and have spanned a single or multiple years (Fishbein & Venable, 1996). Insect floral visitors to most plant species represent ecologically heterogeneous groups consisting of taxa that range from strict pollen consumers or pollen parasites (Baker & Cruden, 1971; Eguiarte, Martinez del Rio & Arita, 1987), to highly effective pollinators

SPATIAL PREDICTABILITY OF DESERT BEES

121

of plants (e.g. Burquez, Sarukhan & Pedroza, 1987). Floral visitors vary in their degree of taxonomic specificity to floral hosts. Strict floral specialization to one or a closely related set of plant species has evolved solely in taxa that visit flowers for pollen or oils (Gess, 1996; Robertson, 1925; Wcislo & Cane, 1996). To the best of our knowledge there are no nectar specialists who forgo flowers of ‘non-preferred’ plant species when their usual host is scarce or absent. On the other hand, some pollen specialists refuse to visit any plant species for pollen other than their host plant (e.g. Bohart & Youseff, 1976; Strickler, 1979). Bees (superfamily Apoidea) are the most species-rich group of floral-visiting animals that are entirely reliant on pollen for protein. Pollen foraging predilection for bee species varies from broad generalists that use a variety of plant species (polylecty) to those that use one (monolecty) or a few closely related plant species (oligolecty) for pollen (Linsley, 1958). In this study, we test the hypothesis that pollen specialist bee species will occur more reliably at their host plant than pollen generalists that visit flowers of other plant species. Our analysis focuses on spatial variation of the ecologically diverse guild of bee visitors to creosote bush (Larrea tridentata) across a subcontinental area that encompasses three recognized biogeographical zones. This bee assemblage includes 22 species of pollen specialists that visit only Larrea tridentata, and approximately 80+ species of pollen generalists that visit L. tridentata as well as other flowering plant species. The vast majority of floral visitors to this plant are bees. Lepidoptera, beetles, and flies visit this plant’s flowers but rarely in significant numbers (Hurd & Linsley, 1975; pers. obs.). We also examine the relative influence of biogeographic history, distance, and site attributes on faunal turnover in this bee guild. LARREA AND ITS BEE GUILD

The plant The genus Larrea has a classical amphitropical distribution with four species represented in the South American deserts and one species occurring in North America (Raven, 1963). Creosote bush is the “most common and widespread shrub in the North American warm deserts” (Turner, Bowers & Burgess, 1995). Its distribution essentially defines the limits of the Sonoran, Chihuahuan, and Mojave deserts in North America. Individual plants attain 3.5 m in height and may live as clonal rings for several thousand years (McAuliffe, 1988; Vasek, 1980). The yellow, cup-shaped flowers of creosote bush present nectar and pollen simultaneously (Simpson, Neff & Moldenke, 1977) for the 1–2 day period they remain open. Initiation of flowering occurs in response to rainfall events over 12 mm (Bowers & Dimmit, 1994). Plants near Tucson, Arizona remained in flower for about 55 days during the spring (Bowers & Dimmit, 1994). Across most of its range, Larrea blooms in the spring following sufficient winter rain. In areas with summer monsoons, a second, more sporadic bloom also occurs (Abe, 1982; Bowers & Dimmit 1994; Simpson et al., 1977). The Larrea bee guild More than 120 species of native bees visit the flowers of creosote bush (Hurd & Linsley 1975; Simpson et al., 1977; this study), second only to Helianthus annuus

122

R. L. MINCKLEY ET AL.

(sunflower) (Hurd, LaBerge & Linsley, 1980), and all are native except the honey bee (Apis mellifera). Only 6–7 of these Larrea bee species are social and three species are cleptoparasites, or cuckoo bees. Cuckoo bees surreptitiously lay eggs on larval food masses of other bee species. The remaining species nest solitarily in burrows in the ground or in hollowed plant stems, abandoned wasp nests, and beetle burrows. The bees that utilize floral resources offered by Larrea have been well characterized by the previous work done in association with the International Biological Program (IBP) in the early 1970s. Hurd & Linsley (1975) collected bees at flowering creosote bushes at 13 Southwestern sites from 1972 to 1974 and reported that a quarter of these 90 bee species were oligolectic. Another quarter of these species were frequently taken at Larrea flowers, but were not restricted to Larrea for pollen. The remainder were floral generalists less commonly found on Larrea. The foraging predilections of these bee species for creosote bush were confirmed by examination of pollen loads and compilation of host label data from pinned museum material. Pollen specificity of these bee taxa was corroborated by a broad scale IBP project of the bees at perennial desert plants (including creosote bush) done 45 km northwest of Tucson, Arizona (Simpson et al., 1977).

METHODS

Study sites The study was conducted in the Chihuahuan, Sonoran and Mojave deserts of the southwestern United States between mid-March and late May in 1993, 1994 and 1995. Desert designations and vegetation zones were assigned to the collecting sites based on the vegetation map of Brown & Lowe (1980). Four sites (Bonita, Pima, Pomerene, and Pomerene 95) located in the transition zone between the Sonoran and Chihuahuan deserts were difficult to unambiguously assign to a vegetation zone because floral elements were present that are characteristic of both deserts. These four sites were grouped in the same vegetation zone as the nearest site in which designation of the vegetation zone was not ambiguous. Based on this criterion, Bonita and Pima are Chihuahuan desert sites, and Pomerene and Pomerene 95 are Upper Sonoran desert sites. In total, 58 collections were made at 47 localities. Of these localities, 10 were in the Chihuahuan, 7 in the Mojave, and 30 in the Sonoran deserts. In the Sonoran desert we sampled in the Upper (15 sites) and Lower Sonoran (15 sites) vegetation zones (Appendix 1). No sites were resampled in the Mojave desert but five and eight sites were resampled in the Chihuahuan and Sonoran deserts, respectively. Most sites were visited in only one year, although some sites were collected in 2 (n=2) and 3 (n=4) successive years to assess interannual variation, and one site was collected three times in a season to assess seasonal variation (Appendix 1). Temporal patterns are compared in depth in a companion paper (Cane, Minckley, Kervin & Roulston, in prep.), but are used here to distinguish among temporal and fine scale spatial patterns. From now on, we refer to the localities as sites and any systematic collection as a sample. Unless stated otherwise, casual samples taken at these sites are not considered in this study. Sites consisted of one-hectare, relatively flat stands of creosote bush that were more than one third through their flowering season. Most sites had deep sandy soils, judging by the presence of kangaroo rat (Diplodomys spp.) burrows, commonly

SPATIAL PREDICTABILITY OF DESERT BEES

123

associated with these soils (Schmidly, 1974). We also chose sites with intermittent streambeds or washes because some bee species prefer to nest in vertically exposed banks (see Michener et al., 1958). To detail finer scale spatial variation of species composition, we systematically sampled Larrea bees at seven sites at Davis-Monthan Air Force base, Arizona. Sites were distributed at 0, 1, 2, 3, 4 and 11 km along a 12 km east–west transect. Five sites were spaced about 1 km apart; a sixth site was 12 km east of the westernmost site. The sampling protocol was the same as that described in the next section for samples taken on 1-ha plots, except that the samples at 0, 1, 3 and 4 km were taken by single collectors in 0.5 ha plots.

Sampling protocol and bee identification Bees were collected using a stratified random sampling protocol. One-hectare plots were divided into 100, overlapping 2.5 m-wide parallel strip quadrats (= belt transects). For each sampling period, each of two collectors began at a randomly selected x, y coordinate and walked for 20 min along the strip quadrat netting any bee that foraged on Larrea flowers. At the end of the 20 min collection period, bees caught by each collector were placed in separate containers. Sampling periods began every 30 min from the beginning of bee activity in the morning (0630–0800 h) for 6 h. Species accumulation curves from samples taken both in 1993 by us and from data of Hurd & Linsley (1975) showed that a morning to midday census yielded more than 85–95% of all taxa represented in an all day census (unpubl. data). Bees are extremely vagile and occur intermittently at flowers between bouts of nest provisioning or mating activity. By sampling through the period of peak activity, this sampling regime allowed us to obtain reliable, objective estimates of species composition and relative species abundance while not noticeably depleting populations (Cane et al., in prep.). For the analyses presented in this study, all samples represent the combined collections of two collectors during one day’s survey. Most bees were collected and pinned for later identification. Those species that could be identified on the wing (honeybees, Xylocopa californica arizonensis, X. varipuncta and Bombus pensylvanicus sonorus) were tallied from visual counts alone. We identified 94% of the 4803 specimens collected to the level of species. Most of the unnamed specimens were designated as morphospecies. Agapostemon angelicus and A. texanus were pooled into one taxon because females of these species are indistinguishable (Roberts, 1972). Members of the genus Lasioglossum subgenus Dialictus were separated into two morphospecies based on the coloration of their abdomens (red or green). Hurd & Linsley (1975) identified eight spring-active species of L. (Dialictus) during their study of creosote bush but did not specify how many species occurred at one site. Therefore, at sites where two or more L. (Dialictus) species were actually present but tallied as one morphospecies, our data represent an underestimate of the true species richness in our samples. Across all sites, the use of morphospecies results in overestimates of actual abundance and breadth of distribution. Excluded from our analyses were undescribed species (9 species, 15 individuals) and honey bees (Apis mellifera). We were not able to reliably associate sexes of undescribed species. Apis was excluded because: (1) it is not native to North America,

124

R. L. MINCKLEY ET AL.

(2) workers communicate locations and levels of resources to nestmates, whereas females of all other bee species in this study locate floral resources individually, and (3) Apis foragers consume stored pollen and nectar before they leave the nest, which allows them to fly farther than comparably-sized solitary bee species (see Seeley, 1995). These latter two colony attributes are particularly relevant to our crossspecies comparisons because the absence of honeybees may be a consequence of either the presence of other, more productive resources in the area, or the absence of colonies in an area. Native bees typically forage in the vicinity of their nests. In our samples honeybees were >3-fold more abundant (n=3908) than Colletes salicicola, the second most abundant bee species (n=844). We follow the taxonomic classifications of Michener, McGinley & Danforth (1994). Vouchers of all material are deposited at the Auburn University Entomological Museum (Auburn University), Snow Entomological Museum (University of Kansas) and the Bee Biology and Systematics Laboratory (Utah State University).

Resource specialization For our analyses, all bee species were categorized as pollen specialists of Larrea (oligoleges) or generalists (polyleges). Specialist bee species were designated based on: (1) prior information summarized in the IBP studies (Hurd & Linsley, 1975; Simpson et al., 1977); (2) the Catalog of Hymenoptera in America North of Mexico (Krombein et al., 1979); (3) our own field observations; and (4) records from label data on 28 000+ specimens housed in five entomological museums in the United States that have significant holdings of desert bees (see Acknowledgements). We differed from Hurd & Linsley (1975) in three of our designations: Perdita (Perdita) luciae decora and P. (Perditella) marcialis were considered generalists by Hurd & Linsley (1975). In our study we have classified them as Larrea specialists because (1) most female specimens of these species have been collected on Larrea; (2) the large majority of Perdita species are oligolectic (Linsley, 1958), and (3) the few detailed studies of panurgine bee species thought to be ‘putative polyleges’ concluded these taxa were species complexes composed of multiple oligolectic members (Danforth, 1994). In this study, Colletes salicicola is considered a polylege. Hurd & Linsley (1975) list C. salicicola as a Larrea specialist in one table (p. 9) yet state that it is a polylege in their discussion of the species (p. 21). Simpson et al. (1977) also considered it to be a generalist bee species that is commonly associated with Larrea and Cercidium spp. in southern Arizona. All of the oligolectic bee species on Larrea are solitary and nest in the ground, except Hoplitis biscutellae, which builds nests in preformed cavities made by wasps or beetles (Rust, 1980). Among our generalist bee species group, other ecological categories can be distinguished. These include cleptoparasitic bee species, which do not collect pollen but instead co-opt the pollen stores of other species of bees, social species, and pollen specialists of other host plants that collect nectar at various plants, including Larrea. Plant densities were estimated from total counts of the creosote bushes sampled and distances walked along the belt transects summed over all sampling periods. Linear distance walked in a day for each collector was multiplied by 2.5 m to obtain area. The proportion of shrubs in flower was tallied. Data from each collector were then averaged to obtain an estimate of total plant density and flowering plant density

SPATIAL PREDICTABILITY OF DESERT BEES

125

for each site. From these values we were subsequently able to relate features of the plants at a site to bee species richness and abundance. Average Larrea canopy volume at each site was estimated by measuring heights and maximum circumferences of ten randomly chosen plants to calculate spherical volume (Barbour, 1969). We estimated stage of bloom phenology by calculating the ratio of reproductive and post-reproductive flowers (open flowers + withered flowers + fruit) to pre-reproductive buds from the top 30 cm of the tallest branch of the same ten randomly chosen plants.

Comparisons of faunal similarity We compared the similarity of bee faunas across sites using simple presence or absence of bee species and calculating raw similarity values for all pairs of sites [Jaccards index, (n species shared/n species shared + n species unique from site A + n species unique from site B)]. These similarity values were then compared to a distribution of site similarities we generated by randomly drawing species from a species pool that consisted of all taxa in the frequency that we collected across all sites (occurrence incidence, cf. Diamond, 1975). From this species pool, sites were ‘repopulated’ with species until they were filled with the number of species originally collected at each site. The random model therefore assumes that species were equally likely to be found at any site and that the number of sites where they were sampled approximates the number of sites where they occur. Weighting by occurrence incidence was deemed more realistic than assuming all species have equal distributions because occurrence incidence for the species ranged from 1 to 47 sites (Appendix 2) and was strongly right-skewed. This weighting scheme also incorporates information about relative abundance because the likelihood of capturing a species at a given site is also influenced by its local abundance (see Discussion). Thus, widespread and uniformly abundant bee species are most likely to be chosen by the algorithm as it assembles simulated site samples. All simulations were run 1000 times and mean similarities were calculated. This software program is available from the authors. We include collections made in all years of the study. For locations sampled repeatedly, samples in 1995 were chosen because in this year the majority of sites were sampled.

Decay To examine the contribution of the widespread species to observed faunal similarity among sites, species were sequentially removed from the similarity analysis to gauge their effect on the regression line of species similarity on distance. The order in which taxa were removed from the pool was based on the number of sites where they were collected (from most to least). After each species was removed, faunal similarities for all pairs of sites were recalculated and plotted against distance, and the regression value was recalculated. Species were removed until the slope of the regression line became statistically indistinguishable from the slope of the regression line generated in the permutation analysis discussed above. If widespread species were primarily responsible for the observed relationship of faunal similarity on

R. L. MINCKLEY ET AL.

126

6

No. of sites

5 4 3 2 1

0

2

4

6

8 10 12 14 16 18 20 22 24 No. of bee species

Figure 1. Number of bees species collected at 47 1-ha samples. Arrow indicates mean.

distance, then we expected removal of a few of these species would quickly dissolve this faunal similarity-distance relationship.

RESULTS

General characteristics of sites and their Larrea bee faunas Systematic samples from the 1-ha plots yielded from 3 to 23 species (average= 11.2±0.73 SE) with modes at 8 and 16 species (Fig. 1). Pooled for all 47 1-ha samples, 93 species were represented in the 4803 individuals taken. Of these, 89% of the individuals were from only 19 species, whereas 27 species were represented by two specimens or less (Appendix 2). The 93 bee species consisted of three cleptoparasites, 64 generalists, five oligoleges of plants other than Larrea, and 21 oligoleges of Larrea (Appendix 2). Two of the cleptoparasites clandestinely insert their eggs into the nests of Larrea specialists (Hexepeolus rhodogyne into nests of Ancylandrena larreae, and Epeolus mesillae into nests of Colletes clypeonitens) and one (Ericrocis lata) parasitizes several congeneric generalist species [Centris spp. (Rozen & Buchmann, 1990)]. Oligolectic bee species on plants other than Larrea were primarily males that presumably were netted as they stopped for nectar at Larrea flowers.

Sampling reliability To analyse whether the samples taken typified the bee fauna that occurred at a site, we compared the lists of species taken by two collectors at one site. We reasoned that if repeatability among collectors was high, then our samples are adequate representations of the bee species that were present. The overall percentage of taxa caught by both collectors averaged 45±2%, (range 0–75%). However, when we

Cumulative proportion of species

SPATIAL PREDICTABILITY OF DESERT BEES

127

1.0 0.8 0.6 0.4 0.2

0

1

2

3

4

5

6

7

Samples

Figure 2. The cumulative number of bee species from seven samples made at the Sandario Rd. site (Pima Co., Arizona). (D) species accumulation when samples are ordered according to the date the collection was made; (•) estimate of the shape of species accumulation curve calculated by randomizing the order of the actual samples 100 times.

divided taxa at each site into common and rare halves according to their ranked relative abundance, species in the abundant group are represented in the samples of both collectors significantly more frequently than species in the rare group [90 and 20% repeatability for abundant and rare taxa, respectively; (Mann–Whitney U test, T=2265, P<0.001)]. The half-day randomized sampling protocol we used therefore provides a reliable estimate of the more abundant members of the Larrea bee guild but may underrepresent rarer species. Rare bee species may comprise a substantial proportion of the fauna at a site. A species accumulation curve for the Sandario Rd. site (Fig. 2) was calculated from five systematic collections and half-day long casual collection made by us, and one sample made as part of the IBP in 1973 (Hurd & Linsley, 1975). Calculated from first to last date of the samples, as is done traditionally (Coddington, Young & Coyle, 1996; Rand & Meyer, 1990), the species accumulation curve strongly asymptotes largely because the first sample consisted of many species. This analysis indicates that most of the species present at the site were collected. Alternately, when the order samples were taken for these same data is randomized 100 times there is little evidence of an asymptote (Fig. 2). Rare species may include individuals that are residents or transients. Presumably all species in the abundant category were resident.

Resource specialization, abundance and distribution Across all 47 sites the number of specialist bee species averaged 4.5±0.3 SE (range 0–9) and the number of generalist bee species averaged 6.8±0.6 SE (range 0–16). One site (La Jornada) in the Chihuahuan desert consisted exclusively of generalist bee species and one site (Wiley Well) in the Lower Sonoran desert vegetation zone consisted of all Larrea specialists. Compared to generalists, Larrea

R. L. MINCKLEY ET AL.

128

T 1. Comparison of Larrea specialist and generalist bee species for (A) number of sites occupied and (B) mean abundance at sites where species occurred. Values in parentheses are proportions. A

Number of individuals

1.01–1.9

2.0–9.9

10–32

Specialist spp Generalist spp

4 (0.19) 44 (0.61)

9 (0.43) 25 (0.35)

8 (0.38) 3 (0.04)

1–2 8 (0.38) 43 (0.60)

3–22 6 (0.29) 20 (0.28)

23–47 7 (0.33) 9 (0.13)

(v2 =21.69, P<0.001, df=2) B

Number of sites sampled Specialist spp Generalist spp

(v2 = 5.492; P =0.064, df=2)

specialists were proportionally more abundant where they were found (Table 1A) and tended to occur at more sites (Table 1B). Of the 19 most abundant species (those representing 89% of the total individuals collected, see Appendix 1), ten were generalists and nine were specialists. Likewise, when the 21 most widespread species were ranked according to the number of sites where they were collected, 12 were generalists and nine were Larrea specialists (Appendix 1). No species occurred at all sites. The two most widespread taxa were the Larrea oligolege, Trachusa larreae, (36 of 47 sites) and the polylege, Colletes salicicola (34 of 47 sites). Most species occupied few sites and were not abundant. This may indicate high spatial turnover among species of this bee guild, but does not address the question of whether faunal turnover is spatially structured or is simply haphazard, and at what scale spatial structure occurs. High local faunal turnover may occur because bee distributions are very patchy within their ranges, or because our sampling method often missed rare species. This issue is addressed in the following sections. Faunal similarity of sites within ecoregions The numbers of bee species sampled at 1-ha Larrea sites and the ratios of specialist to generalist bee species varied little among vegetation zones. Average species richness was greatest at sites in the Mojave desert and was least at sites in the Upper and Lower Sonoran vegetation zones (Fig. 3). Interestingly, two of the three sites with the greatest number of species were in the transitional area between the Chihuahuan and Sonoran deserts where Larrea is thought to have only recently invaded (Bonita, Pima 95) (Betancourt, Van Devender & Martin, 1990). The third site (Beaver Dam Wash) was at the northern edge of the Mojave desert in southwestern Utah (Appendix 1). The proportion of specialist to generalist bee species over all sites was a weak predictor of species richness (r2=0.08, F=3.94, P=0.05, df=1). The average proportion of generalist bee species was greatest at sites in the Chihuahuan desert and least in the Lower Sonoran desert vegetation zone (Fig. 3). When sites within ecoregions were pooled into four distance categories of 1–5 km, 6–60 km, 61–160 km, and >160 km, average faunal similarity declined with distance with all species combined (Fig. 4A; One-way ANOVA, F=15.925, df=3, P=0.001). The average similarities of sites in the 1–5 km category were greater than those in the 6–60 km category (Tukey’s comparison). Median similarity for these same distances when bee species were divided into generalist (Fig. 4B) and

SPATIAL PREDICTABILITY OF DESERT BEES

129

Average no. of species/site

12 10 8 6 4 2

hi C

n

n

n

ua

ah

hu

ve

a oj M

ra no So L.

a or on .S

U

Figure 3. Mean species richness per site (± 1 SE) in the four desert vegetation zones of generalist (Ε) and specialist (Φ) bee species.

specialist species (Fig. 4C) groups were not statistically distinguishable (for generalists, Kruskal–Wallis one-way ANOVA H=5.182, P=0.159; for specialists, Kruskal– Wallis one-way ANOVA H=3.347, P=0.341). Poor spatial predictability of species composition therefore characterized both the groups of Larrea specialists and generalist bee species at all distances. Faunal similarity among nearby sites and in contiguous habitat To check if discontinuities in Larrea habitat or differences in soil characteristics contributed to the high faunal turnover among sites, we calculated bee species similarities of seven sites collected along a 12 km transect near Davis-Monthan AFB. This area is vegetated by a continuous stand of Larrea on the basin floor, so elevation and soil type are unusually uniform. Faunal similarities for these sites were again low (34±2% SE range 20 to 56%) and did not differ from faunal similarities of sites in the 1–5 km distance category [used above in ‘Faunal similarity of sites within ecoregions’ (t=1.198 P=0.238, df=40)]. Among the Davis-Monthan AFB sites, the correlation coefficient of faunal similarity and distance (r=0.34) did not differ significantly from zero (P=0.94) when tested with an ordinary Mantel permutation test (Manly, 1991). Faunal similarities of resampled sites The taxonomic dissimilarity of neighbouring sites seen in homogeneous desert habitat was unexpected, leading us to examine if differences existed in percent shared species among nearby sites and single sites sampled repeatedly. We first analysed if average faunal similarity of sites separated by 1–5 km (not including Davis-Monthan AFB sites) differed from average faunal similarities of samples made at the same site in succeeding years (n=6 sites). For all species combined, and for

R. L. MINCKLEY ET AL.

130

70

80 A

70

60

B

Percent simlarity

60 50

50

40

40 30

30

20

20

10 0

10

1–5

6–60

61–160 >160

1–5

6–60

61–160 >160

80 70

C

Percent simlarity

60 50 40 30 20 10 0

1–5 6–60 61–160 >160 Distance category (km)

Figure 4. Mean faunal similarities for sites pooled into four categories based on the distance they are separated (1–5, 6–60, 61–160 and >160 km): (A) includes all bee species, error bars indicate ± 1 SE, (B) includes only bee species that are Larrea pollen generalists, and (C) includes only bee species that are pollen specialists. (B) and (C) are Box-Cox representations. Bar extends to 10–90% confidence interval and box extends to 25 and 75% confidence interval. Line in box indicates the median.

specialist and generalist bee species analysed separately, mean similarities were as low for sites 1–5 km apart as they were for sites sampled in successive years (all species, P=0.55; generalists, P=0.16; specialists, P=0.27). A second analysis was done which compared sites separated by 1–5 km to four samples taken at one site in a single season (Sandario Rd. in 1995). The four within-season samples at the Sandario Rd. site were taken ± weekly in 1995 beginning when 40% of the floral buds had opened and ending when only 5% of the floral buds remained. While the first three samples of the season were systematic as described above, the last sample was casually collected because most of the Larrea plants had ceased blooming by this time, making a randomized transect unreasonable. With all species combined, faunal similarities among the four samples ranged from 8 to 26% similarity (average= 17±3%, n=6 comparisons). Faunal similarities averaged 11±5% SE (range 0–29%) for specialists alone and 20±2% SE (range 14–29%) for generalists. Even with the 31 March sample excluded because of the small number of species caught on that

SPATIAL PREDICTABILITY OF DESERT BEES

131

date (n=4), temporal faunal turnover remained high through the season at this site (average similarity for all species=22±4% SD, range=20–26%, average for generalists only=22±7% SD, range 15–29%: average for specialists only=22±6% SD, range=17–29%).

Faunal similarity across all sites With all species pooled, faunal similarities across all sites averaged 21 ± 0.3% SE, and varied widely regardless of the distances they were separated. The range of species shared among sites less than 5 km apart was from 0% to 88% while sites greater than 1000 km apart shared 0–27% of their species. Average faunal similarity for specialist bee species across all sites (22±0.5% SE) was greater than it was for generalist bee species (16±0.3% SE) (Mann–Whitney U test, P<0.001). Despite this variation, faunal similarity decreased moderately and became less variable as distance between sites increased for all species pooled (Fig. 5A), and specialists (Fig. 5C) and generalists (Fig. 5E), and this decline was not an artifact of the fewer sites sampled at the greatest distances. Observed faunal similarities generally remained significantly higher than similarities generated from the null model for distances up to 250–299 km. (Fig. 5B, D, E). If bee activity is strongly influenced by bloom phenology and nearby sites are roughly synchronous in their bloom, high similarity, as we observed here, could be wrongly attributed to distance between sites instead of bloom stage. However, the high faunal similarities of sites within 250–299 km probably were not associated with temporal variability among bees in response to stage of bloom. Nearby sites often differed drastically in bloom phenology because of marked differences in elevation and winter rainfall or because they were sampled either in different years or in the same year but weeks apart (Appendix 1). Average bloom phenology for sites in the four ecoregions was similar, ranging from 47 to 55% through estimated seasonal bloom.

Faunal similarity of sites across ecoregions Average similarities of sites that spanned ecoregion boundaries (e.g. Chihuahuan– Upper Sonoran, Upper Sonoran–Lower Sonoran and Mojave–Lower Sonoran) were grouped into categories of 60–160 km and <160 km and compared to average similarity of comparably spaced sites within ecoregions. Contrary to expectations, in the 60–160 km comparison, faunal similarities were higher for sites that spanned ecoregion boundaries than they were for sites within ecoregions for all species pooled together and for specialist and generalist bee species analyzed separately. However, only in the analysis with all species combined was the difference significant (Table 2). The results of the 160+ km comparison were opposite to those for the 60–160 km category and more closely fit our expectations, i.e. faunal similarities were significantly lower across ecoregion boundaries than within ecoregions for all species combined, and for generalist and specialist bee species analysed separately (Table 2). Because there were fewer sites in the 60–160 km category these results may have been an artifact of undersampling. Alternatively, the ecoregion boundaries may not reflect distributional limits of the bee faunas that characterize them.

R. L. MINCKLEY ET AL. 100 90 80 70 60 50 40 30 20 10 0

60 A

B 50 40 30 20 10 0

100 90 80 70 60 50 40 30 20 10 0

Average percent similarity

Percent similarity of bee fauna at L. tridentata

132

C

100 90 80 70 60 50 40 30 20 10 0

60 D 50 40 30 20 10 0 60

E

F 50 40 30 20 10 0 9

+ 11 0.9 –1 10 49 9. 9– 49 8. 8– 49 7. 7– 49 6. 6– 49 5. 5– 49 4. 4– 49 3. 3– 49 2. 2– 49 1. 1– 9 4.

200 400 600 800 1000 1200 1400 1600

0–

0

Distance (km)

Distance (km x 100)

Figure 5. Faunal similarities for all pairs of sites plotted against distance. (A) and (B) include all bee species, (C) and (D) include only bee species that are Larrea pollen specialists, and (E) and (F) include only bee species that are pollen generalists. (A, C, E) show all site comparisons among 47 sites. (B, D, F) are means and 95% confidence intervals of the observed (Μ) and simulation (Β) data pooled into 50 km bins.

T 2. Comparison of mean similarity values (in percent) for sites within and across vegetation zones. m=Mann–Whitney rank sum test, t=t-test, ∗=P<0.05, ∗∗ =P<0.005

All species Generalists Specialists

Distance

Within veg. zone

Across veg. zone

60–160 160+ 60–160 160+ 60–160 160+

23±1.1 21±0.8 17±1.3 18±0.9 26±2.0 25±1.4

27±1.2 t∗ 18±0.3 m∗∗ 20±1.5 m 15±0.3 m∗∗ 32±2.4 m 20±0.5 m∗∗

SPATIAL PREDICTABILITY OF DESERT BEES

133

Decay approach We hypothesized that the spatial structure in faunal similarity was largely attributable to widespread species. By sequentially removing common species from our computations while preserving the number of site comparisons, some insight was gained into the contribution of a few common species to the spatial structure in faunal similarity. Contrary to our expectations, 24 species were removed from the species composition matrix before the slope of the regression line from the observed data became statistically indistinguishable from the regression line calculated from the permutation data. These 24 species occupied six or more sites. The average number of sites occupied by all 93 species was 6.0 (±0.8 SE). Evidently widespread species also did not account for the non-random patterns in site similarities, as we found for specialist and generalist species.

Differences of plant characteristics among sites Sites varied 53-fold in the estimated canopy volumes of their individual Larrea plants and 45-fold in the total canopy volume of Larrea per hectare. Such variability suggests that the actual or potential amount of pollen and nectar resources available to bees at sites could also account for differences in species richness among sites: resource poor sites may support fewer bee species. The quantities of floral resources at sites were not directly measured, but several measures were taken which may be associated with the actual or potential amount of floral resources available at a site. These were: (1) percent buds in bloom, an estimate of standing crop of floral resource availability on the sample day; (2) stage of bloom, an estimate of floral resource production for the that season up to the sample day; and (3) volume of Larrea bushes/hectare, an estimate of potential floral resource production across years. Fig 6 (A–I) shows that all of these variables were poor predictors of overall species richness for all species, specialists and generalists (r2 for all variables <0.03). Likewise, number of bushes sampled per person per day did not predict the number of total bee species (r2=0.002, P=0.8), or specialists (r2=0.03, P=0.21) or generalists (r2=0.07, P=0.07). This provides some measure of collecting effort because as bee density increases, time spent sampling per bush increases and fewer bushes were sampled in a day.

DISCUSSION

The range in spatial scale presented in this study takes advantage of an unusually widespread, ecologically dominant plant with an exceptionally diverse guild of bee visitors. Sample sites were separated by distances from 0.5 to over 1450 km, ranged in elevation from 30 to 1607 m and spanned four major vegetation zones in three biogeographically distinct deserts. The bee species that visit Larrea are equally varied, including strict Larrea specialists, cleptoparasites and specialists of other desert plants, and generalists that visit Larrea and other flowering plants. This system therefore provides opportunities for many comparisons and, to our knowledge, represents the most extensive spatial survey of floral visitors to date.

0

18 16 14 12 10 8 6 4 2 0

Number of all species

24 B 22 20 18 16 14 12 10 8 6 4 2 0 8000 10 000 12 000 0 2

2000

4000

6000

D

0

25

2

2 r = 0.0001 P = 0.95

2000

4000

6000

18 16 14 12 10 8 6 4 2 0

8000 10 000 12 000

Bush volume/HA

r = 0.09 P = 0.53

20

10 5

4

6

8 10 12 14 16 18 20 22 24

2 r = 0.003 P = 0.24

2

r2 = 0.025 P = 0.3

15

E

0

C

2

r = 0.00003 P = 0.97

4

6

8 10 12 14 16 18 20 22 24

Percent of buds in bloom

0

20

18 16 14 12 10 8 6 4 2 0

40

60

F

0

80

100

R. L. MINCKLEY ET AL.

Number of generalist species

A

134

24 22 20 18 16 14 12 10 8 6 4 2 0

2 r = 0.016 P = 0.41

20

40

60

80

100

Stage of bloom in percent

Figure 6. A–F. Relationship between bush volume, percent of buds in bloom, and seasonal stage of bloom for (A–C) total number of bee species, and (D–F) number of generalist bee species.

Number of specialist species

10

G

2 r = 0.00006 P = 0.96

8

10

H

2 r = 0.014 P = 0.44

8

6

6

6

4

4

4

2

2

2

0

0

0

0

2000

4000

6000

8000 10 000 12 000

Bush volume/HA

0

2

4

6

8 10 12 14 16 18 20 22 24

Percent of buds in bloom

I

2 r = 0.015 P = 0.42

8

0

20

40

60

80

Stage of bloom in percent

Figure 6. G–I. Relationship between bush volume, percent of buds in bloom, and seasonal stage of bloom for number of specialist bee species.

100

SPATIAL PREDICTABILITY OF DESERT BEES

10

135

136

R. L. MINCKLEY ET AL.

Bee species composition at nearby sites was markedly dissimilar, yet in general, sites separated by distances less than 250 km shared more species than expected based on a null model of equiprobable distribution. Neither specificity for Larrea pollen nor the number of sites at which bee species occurred could alone account for the lack of spatial predictability of bees that we observed. Likely, congruent distribution patterns of a diverse set of bee species are responsible for the spatial predictability we found.

Sampling reliability and species abundance Faunal similarity may have been overestimated because our collecting protocol underestimates the true species composition at the 1-ha sites. Underestimates of bee species number can be attributed primarily to (1) our use of a systematic sampling protocol focused on one plant species (instead of all plant species in flower), and (2) the relative abundance of bee species. Roughly one half of the plants in 1-ha plots are sampled during a half-day sampling period (Cane et al., in prep.). Thus, bee species that foraged and nested in a very localized area of the study site, or those that remained in their nests for most of the day could have been missed. Estimates of the number of sampled species at 1-ha sites was also influenced by the presence of other plant species in flower and the predilection of generalist bee species to visit these alternate floral hosts. Few generalist bee species are entirely non-discriminant in the plant species they visit (Ginsberg, 1983), so their presence at creosote bush often reflects the availability (or lack) of other floral hosts. Cleptoparastic bee species and oligolectic species of other plant taxa (Appendix 2) were also included in our generalist groups, even though both typically visit Larrea only for nectar. We made preliminary analyses with both cleptoparasitic and oligolectic bee species of plants other than Larrea removed and these results did not differ from those shown here. Probably the largest factor contributing to underestimates from our half-day samples were locally rare species. The low repeatability among collectors in retrieving rare species and differences in species collected at different times at the same site (Fig. 2) suggests this component of the local bee fauna can be large. Sakagami, Laroca & Moure (1967) and Silviera & Campos (1995) have discussed other biases inherent in systematic samples of bees. Alternatively, temporal variability of the bee fauna could result in overestimates of similarity if bee activity was strongly influenced by bloom phenology and nearby sites had synchronous bloom. Despite the number of poorly represented species in our samples, the randomization test suggests that these samples reliably represent the numerically dominant species at a site. Including only the assumption that species differ in the number of sites where they occur, we were able to show similarity of sites within 300 km were generally high (see ‘Faunal similarity across all sites’, above). Sampling reliability is also high when rank abundance of bee species are incorporated into randomization tests that compare samples made at single sites in different years (Cane et al., in prep.). Although other similarity measures less sensitive to rare species could have been used in this study, we chose Jaccards similarity because our interest was in spatial predictability of bee species and this measure most clearly conveyed presence and absence data. Larrea specialist bee species should also be well represented. They are entirely

SPATIAL PREDICTABILITY OF DESERT BEES

137

reliant on Larrea for their pollen and harvest most of their nectar from this plant. Also, males of most specialist species patrol flowering Larrea in search of receptive females (pers. obs.). Furthermore, our sampling focused solely at Larrea. Therefore, the probability we encountered specialists at Larrea plants was high. Other differences among species in behaviour at the plant (e.g. flight speed, foraging bout duration, etc.), nesting habits (dispersed vs. aggregative nesting), and whether or not foraging is for nectar or pollen also influence capture probability (see also Sakagami et al., 1967). However, these factors would influence estimates of relative abundance more than the presence or absence of species. We predict that further collections at sites would result primarily in an increase in number of generalist or very rare specialist species. For the purposes of broad scale comparisons among specialist and generalist bee groups, the under-representation of highly localized species, generalists, or rare species should not affect the pattern of faunal turnover shown here.

Ecological role and spatial predictability A clear finding from this study is that the ecological dominance of Larrea has not conferred ecological success to all species of its specialist bee fauna, whether or not one defines ecological success in terms of mean abundance, number of sites occupied or geographic distribution. Abundance and distribution of the Larrea specialist species spanned the range we observed for generalist bee species, and spatial turnover of the specialist bee fauna was high and approached that observed for the generalist bee fauna. Of the three bee species that occurred at or near all edges of the range of Larrea, only two are creosote bush specialists, Trachusa larreae and Hesperapis larreae. The 19 other specialist species are considerably less widespread. Evidently, factors other than the presence of the host plant determine distributions and relative abundances of the creosote specialist bee speices. Such factors could include bee dispersal and chance local extinction, interannual flower abundance and predictability and other ecological or evolutionary factors. The low spatial predictability of floral visitors at their hosts has been used to question whether coevolution is as common in plant-pollinator systems as is generally believed (e.g. Herrera, 1988). However, studies of insect-plant mutualisms involving seed predators have shown that even with high spatial turnover of species, coevolution is possible when local populations are sufficiently discrete (Thompson, 1994; Thompson & Pellmyr, 1992; Pellmyr & Thompson, 1996). We found that half of our sites had eleven or fewer bee species present (Fig. 1). In such species-poor settings, the number of pairwise interactions between Larrea and its floral visitors may be sufficiently limited for directional selection to act. We have found that sites resampled 25 years apart have more similar bee species composition and relative abundance than expected when compared to the regional pool of bee species (Cane et al., in prep.). However, Larrea seedling recruitment is so rare and episodic (Bowers, Webb & Rondeau, 1995; Sheps, 1973; Turner, 1990; Valentine & Gerard, 1968) and its generation time so long that it is questionable if the composition of bee pollinators remains sufficiently static for coevolution to occur. In contrast to the plant, bees have convergently specialized on Larrea pollen at least 13–16 times in North America (Minckley & Cane, unpublished data). The attraction of Larrea as a pollen host may be largely associated with its broad geographic range (e.g. Strong, Lawton & Southwood, 1984), although bloom

138

R. L. MINCKLEY ET AL.

predictability and duration may also be involved. All 22 Larrea oligoleges are active during the spring, while only three of these species also emerge during the late summer bloom (Hurd & Linsley, 1975). While Larrea flowers in both seasons in response to rains (Bowers & Dimmitt, 1994), cool winter temperatures delay flower bud formation in the winter and seasonally synchronize bloom to a few week period in the spring as average daily temperatures warm (Abe, 1982). The beginning of summer bloom is more variable and is shorter in overall duration (Abe, 1982): flowering occurs 2–3 weeks after any rainfall event over 12 mm (Bowers & Dimmitt, 1994). Thus, the spring bloom may be easier to track by emerging adult bees and provide more resources over a longer period of time than the summer bloom. In highly variable desert environments, these host plant attributes may be strong selection pressures for specialization once a preference has evolved. Spatial structure of the Larrea bee guild The pattern of high regional diversity and low local diversity of Larrea bee species is similar to that found in warm desert rodent communities of North America and other continents (Kelt et al., 1996). For rodents, one hypothesis forwarded to explain this pattern is that low primary productivity of deserts during the dry season or winter prevents the co-occurrence of many species at one site. This explanation does not fully explain our results for the Larrea bee guild or for bees in general. For one, most bee species are adults for 4–6 weeks and have but one generation per year (Robertson, 1929; Linsley, 1937). Therefore, the timespan of reduced resource levels in a season are minimal for bees compared to rodents. Secondly, high spatial turnover of bee species is not unique to faunas of arid zones. Similar patterns have been reported for bee faunas in the ‘cerrado’, or interior shrub/grassland (Silviera & Campos, 1995; Silviera, pers. comm.) of Brazil, the secondary coastal grassland (Sakagami et al., 1967) of Brazil, the xeric lowlands surrounding the Mediterranean sea (Guitia´n et al., 1996; Herrera, 1988), the high elevation grasslands of Wyoming, U.S.A. (Tepedino & Stanton, 1981), and the eastern deciduous forest, North America (Ginsberg, 1983). Despite differences in the sampling protocols used by the various investigators, all these studies found high spatiotemporal variability among bee faunas. The lack of an asymptote for the species accumulation curve from the Sandario Rd. site (Fig. 2) indicates some of the dynamics of local distributions and abundances of solitary bees. Transient species, resident species that are rare (Coddington et al., 1996), and species with extremely localized populations within their distributions contribute to such a pattern. The warm desert bee fauna of North America is among the most diverse in the world (Michener, 1979), so it is reasonable to expect all of these factors to contribute. Condit et al. (1996) found that species accumulation curves did not asymptote from completely censused 50-ha plots of tropical trees. They attributed this pattern to the high species richness of these areas and because tropical trees occur in extremely localized, widespread patches. Similar dynamics of local distribution and abundance may occur in the bee guild associated with Larrea. Why are spatial patterns of floral visitors so unpredictable? All bee species at Larrea, regardless of whether they were widespread and abundant or highly localized and rare, had patchy local distributions and fluctuated greatly

SPATIAL PREDICTABILITY OF DESERT BEES

139

in abundance. Trachusa larreae and Colletes salicicola represented the most individuals in our collections but were not caught at 29% and 25% of our sites, respectively. Sites where we did not encounter them were within the limits of their known geographic ranges. Furthermore, both species occurred at the edge of the Mojave, Sonoran and Chihuahuan deserts and in the ecotonal region between the Chihuahuan and Sonoran desert where Larrea has become a dominant component of the flora over only the last 150 years (summarized in Cane et al., in prep.). Evidently, these species are readily able to colonize new sites but do not occur in all places where their floral host is found. At the other extreme, Colletes stepheni, a specialist which ranges from southern Nevada to Baja California Sur, was found at only one site in our study (Hopkins Well) where it was the third most abundant species in the sample. However, it was not found three days earlier at Wiley Well, a site 1 km south in the same dune complex. Because this is a large conspicuous species, its absence at Wiley Well was undoubtedly because it was truly absent. Other taxa were equally variable. Why are abundances and local distributions of the bee species associated with Larrea so patchy within the range of this ecologically dominant, widespread host plant? It does not appear that nest sites, pollen and nectar resources, or competition limit bee population size or occurrence where Larrea grows. Friable soils, often used by bees for nesting (Cane, 1991), are exposed and plentiful across much of Larrea’s distribution (MacMahon, 1979). Pollen and nectar production by Larrea can exceed all other perennial plant species at sites (Simpson, 1977) and our results show that floral productivity (bush size, bush density and number of open flowers on the top 30 cm of plants) was a poor predictor of bee species richness (Fig. 6), or bee biomass (unpubl. data). The copious floral resources coupled with low bee abundance found at most sites (Simpson et al., 1977; pers. obs.) suggests that floral resources are superabundant for bees in most years, and if competition for floral resources ever occurs among Larrea bee species it is highly episodic. Instead of a single factor intrinsic to Larrea or the group of bees that visit this plant, the spatial dynamics we observed may best be explained by factors common to most nesting Hymenoptera. For example, many species are strongly philopatric to their natal nest site (Evans, 1974; Yanega, 1990) which can result in the formation of nest aggregations (Linsley, 1958; Michener et al., 1958; Wcislo, 1984). In such cases, abundance and presence or absence of a species depends on proximity to the nesting area. Nest aggregations have been reported for many of the soil-nesting bee species associated with Larrea, including Trachusa larreae (Cane, 1996; Rust, 1988), Centris caesalpinae, C. pallida, C. rhodopus, C. cockerelli (Alcock, Jones & Buchmann, 1976; Rozen & Buchmann, 1990), Hesperapis larreae (pers. obs), Habropoda pallida (Bohart et al., 1972), Colletes stepheni (Hurd & Powell, 1958) and various species of Perdita. Localized occurrence of stem nesting species that visit Larrea occur because, in contrast to ground nesting bee species, nesting substrata can be limited to riparian areas along streams and washes. Megachile (Chelostomoides) spp. utilize exit burrows of beetle larvae and it was our impression that these species were captured at sites with mature mesquite (Prosopis spp.) trees, which are frequently used by beetle larvae. Xylocopa spp. that visit Larrea require dead branches of trees or spent flowering stalks of Agave, Yucca and Dasyliron (Hurd, 1958) for nesting. Interannual reliability of flowering may also influence population size and species diversity at a site. Population size of some specialist bee species tracks yearly changes in resource quantity on their host plant (Minckley et al., 1993). In the Mediterranean

140

R. L. MINCKLEY ET AL.

region, more individuals and species of floral visitors occurred at sites adjacent to water than at more xeric sites (Herrera, 1988; Viejo & Templado, 1986), presumably because the well-watered plants flower more predictably and offer greater amounts of pollen and nectar throughout the season and day. If local bee distributions are primarily determined by philopatry and characteristics of sites, then the spatial dynamics of Larrea bee species may be strongly influenced by local stochastic extinction and colonization events (sensu Hanski, 1982). Presently there is little evidence supporting the ideas that bee guilds are strongly structured by interspecific interactions for food resources (Brown & Kurzius, 1987, 1989). However, more research to test these alternatives would be profitable and the simplicity of the Larrea-bee system would make such a study practical. The single floral resource and seemingly unlimited nesting sites suggests that one or a few factors determine local persistence or extirpation of these bee species across their distribution.

ACKNOWLEDGEMENTS

The following institutions and their curators allowed access to their collections of desert bees: California Academy of Sciences, San Francisco, California (W. Pulawski), Central States Melittological Institute, Austin, Texas ( J. Neff ), Snow Entomological Division of the Natural History Museum, University of Kansas, Lawrence, Kansas (R. R. Brooks, C. D.Michener), USDA-ARS Bee Biology and Systematics laboratory, Logan, Utah (T. Griswold), R. M. Bohart Museum of Entomology, University of California at Davis, Davis, California (L. Kimsey), Essig Museum of Entomology, University of California at Berkeley, Berkeley, California (C. Barr). Patty Ashby, Hugh Cox, Justin Van Zee, and Jacqueline Shinker provided able field assistance in various phases of this project. Special thanks go to Carlos Herrera and John Neff for reviews and ideas. We also thank numerous Federal and State authorities for permission to establish sampling sites on property under their jurisdiction. Support was provided by the United States EPA grant R 820746–01–3, J. Cane P.I. This is contribution no. 17-985971 from the Alabama Experimental Station, Auburn University.

REFERENCES

Abe Y. 1982. Phenology of tetraploid creosotebush, Larrea tridentata (DC) Cov., at the northeastern edge of the Sonoran desert. Unpublished D. Phil. Thesis, University of Arizona, Tucson. Alcock J, Jones CE, Buchmann SL. 1976. The nesting behavior of three species of Centris bees (Hymenoptera: Anthophoridae). Journal of the Kansas Entomological Society 49: 469–474. Baker HG, Cruden RW 1971. Minor parasitism in pollination biology and its community function: the case of Ceiba acuminata. Bioscience 21: 1127–1129. Barbour MG. 1969. Age and space distribution of the desert shrub Larrea divaricata. Ecology 50: 679–685. Betancourt JL, Van Devender TR, Martin PS (eds). 1990. Packrat Middens: the Last 40,000 Years of Biotic Change, Tucson: University of Arizona Press. Bohart GE, Youssef NN. 1976. The biology and behaviour of Evylaeus galpinsiae Cockerell (Hymenoptera: Halictidae). Wasmann Journal of Biology 34: 185–234. Bohart GE, Torchio PF, Maeta Y, Rust RW. 1972. Notes on the biology of Emphoropsis pallida Timberlake. Journal of the Kansas Entomological Society 45: 381–392.

SPATIAL PREDICTABILITY OF DESERT BEES

141

Bowers JE, Dimmitt MA. 1994. Flowering phenology of 6 woody plants in the northern Sonoran desert. Bulletin of the Torrey Botanical Club 121: 215–229. Bowers JE, Webb RW, Rondeau RJ. 1995. Longevity, recruitment and mortality of desert plants in Grand Canyon, Arizona, USA. Journal of Vegetation Science 6: 551–564. Brown DE, Lowe CH. 1980. Biotic communities of the southwest. Rocky Mountain Forest and Range Experiment Station, Fort Collins, Colorado. USDA Forest Service General Technical Report RM-78. Brown JH, Kurzius MA. 1987. Composition of desert rodent faunas: combinations of coexisting species. Annales Zoologici Fennici 24: 227–237. Brown JH, Kurzius MA. 1989. Spatial and temporal variation in guilds of North American granivorous desert rodents. In: Morris DW, Abramsky Z, Fox BJ, Willig MR, eds. Patterns in the Structure of Mammalian Communities. Lubbock, Texas: Texas Tech University Press, 71–90. Burquez A, Sarukhan J, Pedroza AL. 1987. Floral biology of a primary forest palm (Astrocaryum mexicanum) Liebm. Botanical Journal of the Linnean Society 94: 407–419. Cane JH. 1991. Soils of ground-nesting bees (Hymenoptera: Apoidea): texture, moisture, cell depth and climate. Journal of the Kansas Entomological Society 64: 406–413. Cane JH. 1996. Nesting resins obtained from Larrea pollen host by an oligolectic bee, Trachusa larreae (Cockerell) (Hymenoptera: Megachilidae). Journal of the Kansas Entomological Society 69: 99–102. Coddington JA, Young LH, Coyle FA. 1996. Estimating spider species richness in a southern Appalachian cove hardwood forest. Journal of Arachnology 24: 111–128. Condit R, Hubbell SP, Lafrankie JV, Sukumar R, Manokaran N, Foster RB, Ashton PS. 1996. Species-area and species-individual relationships for tropical trees: a comparison of three 50ha plots. Journal of Ecology 84: 549–562. Danforth BN. 1994. Taxonomic review of Calliopsis subgenus Hypomacrotera (Hymenoptera: Andrenidae), with special emphasis on the distributions and host plant associations. Pan-Pacific Entomologist 70: 283–300. Diamond JM. 1975. Assembly of species communities. In: Cody ML, Diamond JM, eds. Ecology and Evolution of Communities. Cambridge, MA: Harvard University Press, 342–444. Eguiarte LE, Martinez del Rio C, Arita H. 1987. Nectar and pollen as resources: the ecological role of visitors to Pseudobombax ellipticum (H.B.K.) Duglan flowers. Biotropica 19: 74–82. Evans HE. 1974. Digger wasps as colonizers of new habitat (Hymenoptera: Aculeata). New York Entomological Society 82: 259–267. Fishbein M, Venable DL. 1996. Diversity and temporal variation in the effective pollinators of Asclepias tuberosa. Ecology 77: 1061–1073. Gess SK. 1996. The Pollen Wasps. Cambridge, MA: Harvard University Press. Ginsberg HS. 1983. Foraging ecology of bees in an old field. Ecology 64: 165–175. Guitia´n J, Guitia´n P, Navarro L. 1996. Spatio-temporal variation in the interactions between Cornus sanguinea and its pollinators. Acta Oecologia 17: 285–295. Hanski AS. 1982. Dynamics of regional distribution: the core and satellite hypothesis. Oikos 38: 210–221. Herrera CM. 1988. Variation in mutualisms: the spatio-temporal mosaic of a pollinator assemblage. Biological Journal of the Linnean Society 35: 95–125. Herrera CM. 1995. Microclimate and individual variation in pollinators: flowering plants are more than their flowers. Ecology 76: 1516–1524. Hurd Jr PD. 1958. Observations on the nesting habits of some New World carpenter bees with remarks on their importance in the problem of species formation (Hymenoptera: Apoidea). Annals of the Entomological Society of America 51: 365–375. Hurd Jr PD, Linsley EG. 1975. Some insects other than bees associated with Larrea tridentata in the southwestern United States. Proceedings of the Entomological Society of Washington 77: 100–120. Hurd Jr PD, Powell JA. 1958. Observations on the nesting habits of Colletes stepheni Timberlake. Pan-Pacific Entomologist 34: 147–153. Hurd Jr PD, Linsley EG. 1975. The principal Larrea bees of the southwestern United States (Hymenoptera: Apoidea). Smithsonian Contributions in Zoology 193: 1–74. Hurd Jr. PD, LaBerge WE, Linsley EG. 1980. Principal sunflower bees of North America with emphasis on the southwestern United States (Hymenoptera: Apoidea). Smithsonian Contributions in Zoology 310: 1–158. Kelt DA, Brown JH, Heske EJ, Marquet PA, Morton SR, Reid JRW, Rogovin KA, Shebrot G. 1996. Community structure of desert small mammals: comparisons across four continents. Ecology 77: 746–761.

142

R. L. MINCKLEY ET AL.

Krombein KV, Hurd Jr. PD, Smith DR, Burks BD. 1979. Catalog of Hymenoptera in America North of Mexico. Washington, D. C: Smithsonian Institution Press. Linsley EG. 1937. The occurrence of double broods in North American andrenid bees (Hymenoptera). Bulletin of the Brooklyn Entomological Society 32: 125–127. Linsley EG. 1958. The ecology of solitary bees. Hilgardia 27: 543–599. MacMahon JA. 1979. North American deserts: Their floral and faunal components. In: Goodall DW, Perry RA, eds. Arid-land Ecosystems: Structure, Functioning and Management. Cambridge: Cambridge University Press. 21–82. Manly BFJ. 1991. Randomization and Monte Carlo methods in biology. London: Chapman & Hall. McAuliffe JR. 1988. Markovian dynamics of simple and complex desert plant communities. American Naturalist 131: 459–490. Michener CD. 1979. Biogeography of the bees. Annals of the Missouri Botanical Garden 66: 277–347. Michener CD, Lange RB, Bigarella JJ, Salamuni R. 1958. Factors influencing the distribution of bees’ nests in earth banks. Ecology 39: 207–217. Michener CD, McGinley RJ, Danforth BN. 1994. The Bee Genera of North and Central America (Hymenoptera: Apoidea). Washington, DC: Smithsonian Institution Press. Minckley RL, Wcislo WT, Yanega DA, Buchmann SL. 1994. Behavior and phenology of a specialist bee (Dieunomia) and sunflower (Helianthus) pollen availability. Ecology 75: 1406–1419. Pellmyr O, Thompson JN. 1996. Sources of variation in pollinator contribution within a guild: the effects of plant and pollinator factors. Oecologia 107: 595–604. Petanidou T, Ellis WN. 1993. Pollinating fauna of a phryganic ecosystem: composition and diversity. Biodiversity Letters 1: 9–22. Rand AS, Myers CW. 1990. The herpetofauna of Barro Colorado Island, Panama: an ecological summary. In: Gentry AH, ed. Four Neotropical Rainforests. New Haven, Connecticut: Yale University Press, 386–409. Raven PH. 1963. Amphitropical relationships in the floras of North and South America. Quarterly Review of Biology 38: 151–177. Roberts RR. 1972. Revision of the bee genus Agapostemon (Hymenoptera: Halictidae). University of Kansas Science Bulletin 49: 437–590. Robertson C. 1925. Hetrotropic bees. Ecology 6: 412–436. Robertson C. 1929. Phenology of oligolectic bees and favorite flowers. Psyche 36: 112–118. Rozen Jr JG, Buchmann SL. 1990. Nesting biology and immature stages of the bees Centris caesalpiniae, C. pallida and the cleptoparasite Ericrocis lata (Hymenoptera: Apoidea: Anthophoridae). American Museum Novitates 2985: 1–30. Rust RW. 1980. Nesting biology of Hoplitis biscutellae, Hymenoptera: Megachilidae. Entomological News 91: 105–109. Rust RW. 1988. Biology of Nomadopsis larreae (Hymenoptera: Andrenidae), with an analysis of yearly appearance. Annals of the Entomological Society of America 81: 99–104. Sakagami SF, Laroca S, Moure JS. 1967. Wild bee biocenotics in Sao Jose dos Pinhais (PR), South Brazil. Preliminary Report. Journal of the Faculty of Sciences Hokkaido University, Series VI, Zoology 16: 253–291. Schmidly DJ. 1974. Factors governing the distribution of mammals in the Chihuahuan desert region. In: Wauer RH, Riskind, DH, eds. Transactions of the Symposium on the Biological Resources of the Chihuahuan Desert Region, United States and Mexico. Washington, D.C. USDI National Park Service Transactions and Proceedings Series 3, 163–192. Seeley TD. 1995. The Wisdom of the Hive. Cambridge, MA: Harvard University Press. Sheps LO. 1973. Survival of Larrea tridentata S. E. M. seedlings in Death Valley National Monument, California. Israel Journal of Botany 22: 8–17. Silviera FA, Campos MJO. 1995. A melissofauna de Corumbatai (Sp) e Paraopeba (MG) e uma analise da biogeografia das albehas do cerrado Brasiliero (Hymenoptera, Apoidea). Revista Brasiliera Entomol. 39: 371–401. Simpson BB. 1977. Breeding systems of dominant perennial plants of two disjunct warm desert ecosystems. Oecologia 27: 203–226. Simpson BB, Neff JL, Moldenke AR. 1977. Reproductive systems of Larrea. In: Mabry TJ, Hunziker JH, Difeo DRJ, eds. Creosote Bush: Biology and Chemistry of Larrea in New World Deserts. Stroudsburg, Pennsylvania: Dowden, Hutchinson and Ross, 92–114. Steinbach K, Gottsberger G. 1994. Phenology and pollination biology of five Ranunculus species in Giessen, Central Germany. Phyton 34: 203–218. Strickler K. 1979. Specialization and foraging efficiency of solitary bees. Ecology 60: 998–1009.

SPATIAL PREDICTABILITY OF DESERT BEES

143

Strong Jr DR, Lawton JH, Southwood JRE. 1984. Insects on Plants: Community Patterns and Mechanisms. Cambridge, MA: Harvard University Press. Stubblefield JW, Seger J, Wenzel JW, Heisler MM. 1993. Temporal, spatial, sex-ratio and bodysize heterogeneity of prey species taken by the beewolf Philanthus sanbornii, Hymenoptera: Sphecidae. Philosophical Transactions of the Royal Society of London B339: 397–423. Tepedino VJ, Stanton NL. 1981. Diversity and competition in bee-plant communities on shortgrass prairie. Oikos 36: 35–44. Thompson JN. 1994. The Coevolutionary Process. Chicago: University of Chicago Press. Thompson JN, Pellmyr O. 1992. Mutualism with pollinating seed parasites amid co-pollinators – constraints on specialization. Ecology 73: 1780–1791. Turner RM. 1990. Long-term vegetation change at a fully protected Sonoran desert site. Ecology 71: 464–477. Turner RM, Bowers JE, Burgess TL. 1995. Sonoran Desert Plants: An Ecological Atlas. Tucson: University of Arizona Press. Valentine DA, Gerard JB. 1968. Life-history characteristics of the creosote bush, Larrea tridentata. New Mexico Agricultural Station Bulletin 526: 3–32. Vasek FC. 1980. Creosote bush: long-lived clones in the Mojave desert. American Journal of Botany 67: 246–255. Viejo JL, Templado J. 1986. Los Pierdos, Satiridos y Ninfalidos (Lep.) de la region de Madrid en relacion con las formaciones vegetales. Graellsia 17: 237–265. Wcislo WT. 1984. Gregarious nesting of a digger wasp as a ‘selfish herd’ response to a parasitic fly (Hymenoptera: Sphecidae; Diptera: Sarcophagidae). Behavioral Ecology and Sociobiology 15: 157–160. Wcislo WT, Cane JH. 1996. Floral resource utilization by solitary bees (Hymenoptera: Apoidea) and exploitation of their stored foods by natural enemies. Annual Review of Entomology 41: 195–224. Yanega DA. 1990. Philopatry and nest founding in a primitively social bee, Halictus rubicundus. Behavioral Ecology and Sociobiology 27: 37–42.

144

APPENDIX 1

Date samples were made, location, vegetation zone, elevation and number of specialist and generalist bee species for all 47 1-ha samples. Arrangement is alphabetical according to site within vegetation zones. Sites followed by an ∗ were resampled in multiple years. The ! indicates three samples were made at this site in one year. Vegetation zone designations for sites followed by an ∗ do not follow the map of Brown and Lowe (1980), as is discussed in the text. Abbreviations for states are AZ= Arizona, CA=California, NM=New Mexico, NV=Nevada, UT=Utah. Abbreviations for vegetation zones are LSON= Lower Sonoran, USON=Upper Sonoran, CHIH=Chihuahuan, and MOJ=Mojave deserts (based on map of Brown and Lowe, ibid.). ND=no data. SITE

State

County

Vegetation zone

Coordinates

Elev (m)

No. specialist species

No. generalist species

No. of species

29-IV-1995 27-IV-1993 28-IV-1995 14-V-1995 8-V-1995 18-V-1995 29-IV-1993 3-VI-1995 09-V-1995 10-V-1995 16-V-1995 18-IV-1994 10-V-1995 9-V-1995 27-V-1994 19-V-1995 21-V-1994 16-V-1994 17-V-1994 28-IV-1995 6-IV-1995 2-V-1995 27-IV-1994 18-IV-1995 24-IV-1995

AZ AZ AZ NM NM NM NM NM NM TX CA CA CA CA NV NV UT AZ AZ AZ AZ AZ AZ AZ AZ

Graham Cochise Graham Dona Ana Hidalgo Socorro Hidalgo Socorro Luna Pecos Inyo San Bern. San Bern. San Bern. Clark Nye Washington Yavapai Yavapai Gila Pima Cochise Cochise Pima Pima

CHIH∗ CHIH CHIH∗ CHIH CHIH CHIH CHIH CHIH CHIH CHIH MOJV MOJV MOJV MOJV MOJV MOJV MOJV USON USON USON USON USON∗ USON∗ USON USON

32°53′ × 109°29′ 31°20′ × 109°30′ 32°54′ × 109°51′ 32°30′ × 106°45′ 32°18′ × 108°43′ 33°34′ × 107°04′ 32°18′ × 108°42 34°20′ × 106°42′ 31°52′ × 107°45′ 31°00′ × 102°55′ 37°09′ × 117°44′ 34°51′ × 115°07′ 35°05′ × 115°33′ 34°54′ × 115°43′ 36°34′ × 114°55′ 36°46′ × 116°24′ 37°09′ × 114°02′ ND 34°41′ × 111°49′ 33°26′ × 110°43′ 32°03′ × 112°01′ 32°05′ × 110°12′ 32°04′ × 110°17′ 32°01′ × 111°22′ 32°07′ × 111°14′

975 1286 910 1219 1371 1365 1298 1610 1300 856 900 730 900 700 810 792 930 1046 1080 1200 520 1280 1138 830 790

4 1 7 0 2 1 3 3 4 3 4 5 5 8 7 5 7 4 4 3 5 4 2 2 4

16 14 16 4 6 2 11 2 10 5 2 11 8 4 9 12 15 4 7 15 9 9 2 3 9

20 15 23 4 8 3 14 5 14 8 6 16 13 12 16 17 22 8 11 18 14 13 4 5 13

R. L. MINCKLEY ET AL.

Bonita n Douglas Pima 95∗ La Jornada 3! Lordsburg 95 s Socorro s Lordsburg Sevilleta 951∗ Tres Hermanas Diamond Y Eureka Goffs Rd. Kelso Cima Kelso Dune ne Las Vegas Nuclear Test Site Beaver Dam Wash Camp Verde McGuireville n Globe Pinckley Peak Pomerene 95 Pomerene Robles Jct I Robles Jct III

Date

Robles Jct II Sandario Rd.∗! s Sandario 95A s Sandario 95B Silverbell 95∗ Silverbell 6e Silverbell 9e e Yuma Organ Pipe, N. M. 1 Organ Pipe, N. M. 2 Organ Pipe, N. M. 3 se Salome 95∗ Tinajas Altas Wenden 95∗ Chemehuevi Hopkins Well Joshua Tree, N.P. Palm Springs n Anza Borrego Palm Springs s Anza Borrego Wiley Well

SITE 21-IV-1995 21-IV-1994 6-IV-1995 11-IV-1995 I-IV-1995 3-IV-1995 5-IV-1995 30-III-1994 6-IV-1994 7-IV-1994 4-IV-1995 14-IV-1995 26-III-1995 13-IV-1995 9-IV-1995 1-IV-1995 9-IV-1995 28-III-1995 31-III-1995 I-IV-1994 30-III-1995 27-III-1995

Date AZ AZ AZ AZ AZ AZ AZ AZ AZ AZ AZ AZ AZ AZ CA CA CA CA CA CA CA CA

State Pima Pima Pima Pima Pima Pima Pima Yuma Pima Pima Pima Maricopa Yuma La Paz San Bem. Riverside Riverside Riverside San Bem. Riverside San Bem. Riverside

County USON USON USON USON USON USON USON LSON LSON LSON LSON LSON LSON LSON LSON LSON LSON LSON LSON LSON LSON LSON

Vegetation zone Elev (m) 823 730 730 730 677 730 707 30 514 548 580 495 354 600 400 120 600 70 450 100 350 120

Coordinates 32°01′ × 111°21′ 32°11′ × 111°13′ ND ND 32°22′ × 111°26′ 32°23′ × 111°26′ 32°23′ × 111°22′ 32°42′ × 114°27′ 32°11′ × 112°48′ 32°11′ × 112°47′ 32°11′ × 112°45′ 33°39′ × 113°18′ 32°18′ × 114°02′ 33°51′ × 113°33′ 34°26′ × 114°39′ 33°36′ × 114°55′ 33°53′ × 115°48′ 33°43′ × 116°23′ 32°08′ × 116°20′ 33°49′ × 116°19′ 32°55′ × 116°16′ 33°35′ × 114°55′

APPENDIX 1—continued

4 2 1 4 3 3 5 7 3 6 6 9 5 8 8 7 3 2 5 5 9 7

No. specialist species

2 6 9 8 7 7 8 2 2 3 3 7 7 9 7 2 2 2 11 3 7 0

No. generalist species

6 8 10 12 10 10 13 9 5 9 9 16 12 17 15 9 5 4 16 8 16 7

No. of species

SPATIAL PREDICTABILITY OF DESERT BEES 145

R. L. MINCKLEY ET AL.

146

APPENDIX 2

Species collected during 1993–6 at 47 1-ha samples, their designation as Larrea specialists or generalists, the number of sites where they were collected, and their abundance calculated for those locations where they occurred. Taxonomy follows Michener et al. (1994). Taxon names followed by 1 are pollen specialists of plant species other than L. tridentata, 2 indicates cleptoparasites. Taxon

Trachusa larreae Colletes salicicola Lasioglossum ‘green’ Hesperapis larreae Colletes clypeonitens Centris cockerelli Perdita covilleae Ancylandrena larreae Megachile fucata Evylaeus amicus Lasioglossum sisymbrii Colletes larreae Hoplitis biscutellae Anthophora cockerelli Colletes louisae Epeolus mesilleae2 Centris rhodopus Centris hoffmannseggiae Megachile discorhina Colletes covilleae Megandrena enceliae Perdita semicaerulea Xylocopa californica Andrena fracta Perdita lateralis Anthophora californica Agapostemon angelicus Colletes perileucus Ashmeadiella breviceps Melissodes tristis Tetralonia angustifrons Nomia tetrazonata Anthophora urbana Ericrocis lata2 Hylaeus episcopalis Tetralonia venusta Megachile newberryi Megachile lippiae Perdita larreae Colletes wootoni Megachile chilopsidis Habropoda pallida Xylocopa tabaniformis Anthophora centriformis Anthidiellum ehrhorni Ashmeadiella foveata Tetralonia albescens Centris pallida1 Bombus sonorus Lasioglossum red Agapostemon melliventris

Specialist (o)/ Generalist (g) Species

Number of sites occupied

Total number of individuals

o g g o o g o o g g g o o g g g g g g o o o g g o g g g g g g g g g g g g g o g g o g g g g g g g g g

37 35 32 27 26 25 20 19 18 16 15 14 14 14 13 13 12 12 11 10 9 8 8 6 6 6 5 5 5 5 5 4 4 4 4 4 3 3 3 3 3 3 2 2 2 2 2 2 2 2 2

810 844 270 315 464 117 269 208 42 44 57 57 23 38 78 88 50 53 51 13 126 209 90 16 133 13 13 8 8 7 17 6 7 6 6 6 5 4 6 3 3 50 3 4 2 2 2 2 3 2 2

Mean abundance 17.6 19.2 6.3 9.8 17.2 4.2 10.3 9.5 2.1 2.6 3 3.8 1.6 2.5 5.6 5.5 3.8 4.1 3.9 29 12.6 17.5 11.3 2.7 16.6 1.9 2.2 1.6 1.6 1.6 2.4 1.5 1.4 1.5 1.5 1.5 1 1.3 2 1 1 16.7 1.5 2 1 1 1 1 1 1 1 continued

SPATIAL PREDICTABILITY OF DESERT BEES

147

APPENDIX 2. continued

Taxon

Ashmeadiella bigeloviae Ashmeadiella paroselae Xylocopa varipuncta Perdita callicerata1 Martinapis occidentalis Perdita luciae Anthophora fulviventris Ashmeadiella cactorum Calliopsis puellae1 Calliopsis larreae Lasioglossum heterorhinum Megachile paroselae Hylaeus wootoni Anthophora petrophila Melissodes paroselae Halictus rubicundus Agapostemon virescens Osmia subfasciata Ashmeadiella femorata Megachile frugalis Andrena piperi Megachile gentilis Lithurge apicalis1 Ashmeadiella gillettei Perdita mimosae1 Osmia marginata Hylaeus coquiletti Perdita punctosignata1 Colletes stepheni Hexepeolus rhodopus2 Hesperapis arida Perdita marcialis Perdita efferta Tetralonia quadricincta Perdita turgiceps Andrena prunorum Centris caesalpinae Megachile coquiletti Perdita eremica Megachile xerophila Megachile productus Megachile odontostoma

Specialist (o)/ Generalist (g) Species

Number of sites occupied

Total number of individuals

g g g g g o g g g o g g g g g g g g g g g g g g g g g g o g o o o g o g g g o g g g

2 2 2 2 2 2 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

5 15 7 5 5 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 32 1 1 10 7 2 2 12 5 3 3 6 3 2

Mean abundance 2.5 7.5 2.3 2.5 2.5 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 32 1 1 10 7 2 2 12 5 3 3 6 3 1