Receptiveness of Foraging Wild Bees to Exotic Landscape Elements

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Receptiveness of Foraging Wild Bees to ExoticLandscape ElementsAuthor(s): Sarah J Hinners and Mervi K Hjelmroos-KoskiSource: The American Midland Naturalist, 162(2):253-265. 2009.Published By: University of Notre DameDOI: http://dx.doi.org/10.1674/0003-0031-162.2.253URL: http://www.bioone.org/doi/full/10.1674/0003-0031-162.2.253

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Receptiveness of Foraging Wild Bees to ExoticLandscape Elements

SARAH J. HINNERS1

Department of Ecology and Evolutionary Biology and Cooperative Institute for Research in Environmental Sciences,

University of Colorado, Boulder 80309

AND

MERVI K. HJELMROOS-KOSKIDepartment of Civil, Environmental and Architectural Engineering, University of Colorado, Boulder 80309

ABSTRACT.—Wild pollinators provide important services in both wild and human-dominatedecosystems, yet this group may be threatened by widespread anthropogenic landscapechange. We explored the responses of wild bees to exotic floral species and novel habitat in afragmented, suburban landscape using pollen grain identification. Pollen loads from beespecimens collected in 13 suburban grassland fragments in Denver, Colorado were sampledand compared with a pollen reference collection. Averaged across two seasonal samplingrounds, 45% of the bee-borne pollen grains were identified to the species level. Wild bees inthis system were very receptive to using alien plants for pollen foraging; at least 45% of pollensampled from bee specimens consisted of non-native pollen grains. During peak flowering inearly summer, bees obtained at least 32% of their pollen resources from within-fragmentsources and at least 7.5% from surrounding suburban residential yards. In midsummer,within-fragment sources represented 58% of pollen sampled while yards dropped to 1.5%.These bees appear to be more accepting of exotic floral species than of exotic habitat types(yards). The advantages and disadvantages of pollen load analysis for movement studies arediscussed.

INTRODUCTION

When a landscape is modified, whether by natural or anthropogenic causes, there isusually a resulting change in landscape structure or pattern. This structural change canaffect the flow of materials and animals through the landscape. Mutualisms such as plant-pollinator relationships may be particularly vulnerable to the effects of landscape change.Each partner in the mutualism depends upon the other, and each one has a unique set ofhabitat requirements that may, or may not, be met in a modified landscape. If a landscape isaltered in such a way that pollinators can no longer move between flower patches, or locatesufficient floral resources, pollination function may be compromised (Steffan-Dewenter andTschartnke, 1999; Lennartsson, 2002; Severns, 2003; Aguilar and Galetto, 2004; Pauw,2007).

Landscape structure has been shown to affect the movement of insects. For example,butterflies inhabiting meadows in the Rocky Mountains in Colorado were more likely tomove between meadows if the intervening matrix consisted of willow than if it consisted ofconifer forest (Ricketts, 2001). Similarly, in Western Europe, when bog fritillary butterflies(Proclossiana eunomia) encountered the edge of a patch of their host plant, they remainedwithin the patch when the surrounding matrix was anthropogenic in nature (plantations

1 Corresponding author: e-mail: [email protected], Campus Box 216, University of Colorado,Boulder, 80309.

Am. Midl. Nat. 162:253–265

253

and pastures), but they were more likely to continue on out of the patch when the matrixwas natural (native peat bog) (Schtickzelle and Baguette, 2003). Both of these examples,one in a natural landscape, the other in a human-modified landscape, address the responsesof insects to habitat heterogeneity. Such responses represent an important area ofecological inquiry because movement of organisms, and the materials they carry, is a keycomponent of ecosystem function (Forman and Godron, 1986; Forman, 1995).

Landscape change commonly results in a pattern of habitat loss and fragmentation, inwhich small areas of the original land cover remain, but these fragments are nowsurrounded by a matrix consisting of a different cover type. The negative effects of thisprocess on biodiversity are thought to derive from two components of this change: theoverall loss of total habitat, and breaking up of formerly continuous habitat intodiscontinuous fragments (Fahrig, 2003). In a recent review, habitat fragmentation wasshown to have overall negative effects on plant reproduction, with the strongest effectsoccurring in self-incompatible plants, implying a reduction in pollination services (Aguilar etal., 2006). There is evidence that pollinators are more sensitive, or quicker to respond, thanplants to habitat loss and fragmentation (Taki and Kevan, 2007). Thus, there is reason forconcern that pollinator populations may be reduced in fragmented landscapes, therebyhaving impacts on pollination function (Buchmann and Nabhan, 1996; Allen-Wardell et al.,1998; Kearns et al., 1998).

Under certain circumstances, habitat loss and fragmentation may not have negativeeffects on biodiversity. Patches of native habitat could be embedded within a heterogeneouslandscape that may provide alternative habitat options for species (Wiens, 1997; Norton etal., 2000; Pawson et al., 2008) or supplemental resources that allow the species to persist in ahabitat fragment (Dunning et al., 1992). One of the critical questions in fragmentationstudies is how different taxa respond to the qualities of the matrix surrounding habitatfragments.

One way to assess a species’ response to a particular element in a modified landscape is bytracking the movements of individuals as they encounter the transition between their nativehabitat and the novel landscape element. For larger animals this is often done using radio orGPS tracking collars, movement-sensitive cameras or visual observation. The movement ofsmaller organisms such as insects is difficult to track, since most are too small to carrytracking devices or to trigger cameras, and their size and mobility make direct observationchallenging. The important ecological role of insects, - as herbivores, predators, food forlarger taxa, and vectors of pathogens, pollination and seed dispersal – makes them aparticularly critical subject for movement studies. Some success has been achieved in usingharmonic radar devices to track bumblebee foraging paths (Osborne et al., 1999), but mostinsects, including other bee species, are too small to carry such equipment. Mark-recapturestudies have also been successful with insects, given sufficient recapture rates (Ricketts,2001). One technique that is occasionally used to track movement in a landscape is theidentification of pollen grains collected from flower-visiting insects (Silberbauer et al., 2004).Many insects visit flowers to consume pollen or nectar or to prey on other insects; pollengrains stick to the insects’ bodies and provide a record of where that individual has been.Pollen load analysis has been used to track the effectiveness of honeybees at cross-pollinating almonds (DeGrandi-Hoffman et al., 1992) and to determine patterns in foragingactivity (Garcia-Garcia et al., 2004). Recently, pollen grains have been used to compare theeffects of different landscape contexts on bee nesting success (Goulson et al., 2002; Williamsand Kremen, 2007) and to relate declines in bumble bee populations to their foragingpreferences in a changing landscape (Kleijn and Raemakers, 2008).

254 THE AMERICAN MIDLAND NATURALIST 162(2)

Humans are primary agents of habitat change; by importing alien species and alteringland cover we alter the biotic and physical environment. This paper addresses the role ofhuman-induced habitat change in mediating an important ecological function - pollination– by exploring the response of wild bees to novel plant species and habitat types in ananthropogenically modified landscape. More specifically, the purpose of this study was touse pollen load analysis to determine the relative importance of matrix- versus fragment-based and native versus exotic, floral resources for wild native bees in a fragmentedlandscape. The habitat fragments consisted of remnant patches of native grasslandsurrounded by a matrix of suburban residential development. The main potential source offloral resources in this matrix consists of cultivated plants growing in residential yards.Because of the ample floral resources available in these yards, the patch-matrix boundary isexpected to be quite permeable to foraging bees and we should, therefore, see a relativelyhigh proportion of matrix-derived pollen carried on bees captured in habitat fragments. Incontrast, a recent study of bee pollen loads in an agricultural landscape showed that most ofthe critical floral resources for bees came from native plants growing in seminatural habitat(Williams and Kremen, 2007). If this pattern applies to this suburban landscape, themajority of pollen species found on bees will be fragment-derived, despite the availability offloral resources in the matrix of yards. The relative proportions of yard- and fragment-derived pollen will give some indication of the role of the suburban matrix for pollinators inthis modified landscape.

Additionally, we wanted to see to what degree these native bees depended on native plantspecies versus alien plant species in their foraging. Although fragments consist of nativegrassland, they are now home to many non-native species. By asking this question, we hopedto gain further insight into the bees’ opportunism: the exotic plants are yet another newelement of this modified landscape and the degree to which native species take advantage ofthese new resources will speak to their adaptability.

METHODS

STUDY SITES

The study sites were located in the greater Denver-Boulder metropolitan area, Colorado(39u449N, 104u599W). The native ecosystem in this area is semi-arid short grass steppe (Simset al., 1978) with trees limited to riparian zones and mesic areas. Annual rainfall averages 35–40 cm, with the greatest precipitation occurring in May, Jun. and Jul. Daily averagetemperatures range from 0 C in Jan. to 23 C in Jul. (National Oceanic and AtmosphericAdministration). All sites occur at elevations between 1554 m and 1890 m above sea level.

Study sites consisted of grassland fragments ranging in size from 3 to 59 ha, embeddedwithin a matrix of suburban residential development. In 2003, 11 grassland fragments weresampled; for the 2004 field season one site was dropped and two were added, so that 12 siteswere sampled in 2004 and a total of 13 sites were sampled over the 2 y. (For site locations,and individual sampling dates, see supplementary materials.) The criteria for choosing siteswere that each fragment should consist primarily of unmowed, ungrazed grassland and thatat least 80% of the circumference consist of suburban residential land use. Theneighborhoods surrounding the fragments were from 10 to 50 y old (median age was20 y) and all consisted of detached, single-family housing. Most yards in theseneighborhoods contained non-native landscaping (turf grass, shade trees, plantings ofornamental flowers and shrubs) and received additional water input during the summermonths from sprinkler systems. The fragments themselves received no additional water

2009 HINNERS & HJELMROOS-KOSKI: WILD BEE FORAGING 255

inputs. With the exception of occasional spot-mowing or spraying to control noxious weeds,fragments were under light management regimes.

BEE AND POLLEN COLLECTIONS

Within each fragment, several circular sampling plots with a diameter of 12 m wereestablished and their center point locations were recorded using a GPS unit (Garmin GPSIII, Garmin International Inc., Olathe, Kansas). The number of sampling plots per siteranged from 2 to 8, depending on the area of the site. Plots were located so as to encompassthe range of slope, aspect and moisture conditions at the site, but they always consisted ofgrassland habitat (wetlands or riparian areas were not sampled). All plots were located atleast 15 m from the edge of the fragment.

Bee specimens were collected during two rounds of sampling, the first during the periodof 8–26 Jul. 2003 and the second during the period of 27 May–12 Jun. 2004. The primarymethod of collection was pan traps, but some specimens were also hand-netted during thesecond round of sampling. Pan traps consisted of Solo brand plastic bowls (Solo CupCompany, Highland Park, Illinois) filled with water and a drop of surfactant. One bowl eachof yellow, white and blue was left out for 24 h at each plot. The three bowls were placed atthe center of the plot in a triangular arrangement approximately 1.5 m apart (insofar asvegetation and rocks allowed). Although isolated weather systems did move through thearea in some of these 24 h periods, all sampling days were primarily sunny and dry. After24 h, any bees caught in the bowl were returned to the lab, rinsed, air dried and pinned. Inaddition, during the second round of sampling, 10 min of hand-netting was conducted ateach plot and the plant species or location from which a bee was collected was noted. Allspecimens were identified to species or morphospecies where possible, otherwise to genus.

In addition to bee specimen collections, we conducted transect surveys of plants in flowerwithin the sampling plot. We walked two pairs of parallel transects across each plot, eachpair perpendicular to the other pair and none passing through the center marker (Fig. 1).Plants in flower were counted and identified to species where possible.

The basis of the pollen grain identification was a pollen reference collection consisting of91 species. To create the collection, pollen samples were collected during the summers of2005 (May–Sept.) and 2007 ( Jun.–Aug.) at the same sites. We collected pollen from allspecies of wildflowers found growing within the sites. In addition, where possible, we

FIG. 1.—Diagram of a circular sampling plot, with central stake marker. Dashed lines representvegetation sampling transects. Edges of the plot were determined by attaching a 6 m string to thecentral stake


collected pollen from cultivated species growing near the study sites. To take a pollensample, we used forceps to pinch off several anthers from each flower and placed them in asmall paper envelope. Whenever possible, we included several individuals of each species,sometimes from several locations. All flower species identifications are based on Weber andWittman (1996). Every flower species in the reference collection was assigned to one ofthree categories: Frag (fragment), Yard (yard, i.e., a cultivated species growing in theresidential matrix), or Either (species that grow in both habitat types such as bindweed -Convolvulus arvensis). If a species could not be identified in the field, it was still assigned acategory and included in the reference collection. (For a list of species included in thepollen reference collection, see supplementary materials.)

Pollen grains from bees and plant field specimens were mounted onto slides. A smallamount of glycerin jelly (Erdtman, 1969) was used to pick up pollen grains from the bee’sbody; this was then placed on the slide, softened using a slide heater and sealed with meltedwax (Kearns and Inouye, 1993). For bee specimens with few pollen grains, all grains thatcould easily and non-destructively be removed from the bee’s body were taken for thesample. For bee specimens with large pollen loads, it was not possible to remove andexamine all of the pollen. Therefore, we took samples primarily from the bee’s scopa, butalso touched the glycerin jelly once to other body surfaces: head and mouth areas, dorsaland ventral surfaces of the thorax and abdomen. It is possible that, due to the fact that thebees shared a pan trap with other bees, some of the pollen sampled from a particular beewas not in fact collected by that particular individual. For this reason, these data areprobably not suitable for matching bee species with flower visitation records. However, all ofthe bees sharing a pan trap were collected in the same location at the same time and we can,therefore, infer that the pollen is representative of the collective foraging efforts of thisparticular group of bees.

Pollen samples were examined for identification using a Nikon Eclipse E400 microscope(400 and 1000 3 magnification). Bee pollen samples that did not match pollen in thereference collection were identified to the nearest taxon possible, usually family butsometimes genus. In these cases, the pollen was usually attributed to the Either category,unless it was clear that any member of that taxon would belong to a particular category. Forexample, pollen identified as the genus Syringa (lilac) was attributed to the Yard categorysince no wild species of this genus are likely to occur in the fragments. Pollen samples foreach bee were scored on the basis of occurrence of a pollen type, not relative abundance.

STATISTICAL ANALYSES

In order to look for seasonal/annual differences in the data, pollen and plant diversitybetween the two sampling rounds were compared using a General Linear Model with a 95%

confidence level. This allowed us to determine whether the data should be treated as twoseparate datasets or as one large dataset.

It is possible that fragment size could have an effect on both plant communitycomposition and bees’ foraging behavior. Therefore, we used simple regression (also with a95% confidence level) to test for relationships between fragment area and the relativeproportions of yard and fragment-derived pollen on bees, native and exotic pollen on bees,and native and exotic plant species in vegetation transects.

We used correlations (Pearson) to look for relationships between plant communitycomposition and pollen load composition at the level of individual sampling plots and at thesite level. All statistical analyses were conducted using SAS statistical software (Version 9.2,SAS Institute Inc., Cary, North Carolina).


RESULTS

Bee sampling resulted in a collection of 699 bee specimens in Jul. 2003 and 1371specimens in May–Jun. 2004. Of those specimens, 19% (131 individuals) of the Jul. 2003bees carried sufficient pollen (at least 15 grains) to collect a sample for analysis; in May–Jun.2004 this number was 14% (199 individuals). In 2003, all of the bee specimens were pan-trapped, while in 2004, 20 of the pollen-bearing bees were captured using a net. There werea total of 338 pollen occurrence records for the 2003 dataset, and 762 for the 2004 dataset.The bees from which pollen samples were taken represented 19 and 21 species ormorphospecies in 2003 and 2004 respectively, all of which were native to the area (seesupplementary materials). Of all the pollen-bearing bees that make up this dataset, onlyeight individuals belonged to oligolectic species. Oligoleges might be expected to responddifferently to exotic landscape elements, since their floral requirements are more specific.However, all of these individuals had more than one type of pollen (presumably fromnectaring visits to other species). We chose to include these individuals in the analysis sincetheir pollen loads did not seem to differentiate them from the rest. Also, oligolectic beesoften specialize on a plant family or genus, which frequently has a cultivated or alien relativeto which the bee species may switch (Tepedino et al., 2008).

The pollen reference collection consisted of 91 angiosperm species: 10 classified asEither, 17 classified as Yard, and the remainder classified as Fragment species. There were46 native species represented in the pollen reference collection, 30 alien species, and 15unknown (identifications not specific enough to determine native versus alien). Averagedover the 2 y, 45% of the pollen from bee samples could be matched with species in thepollen reference collection. This number was strikingly different in the two datasets;however, in the 2003 samples, 68% of the bee pollen matched the reference collection whilein 2004 only 35% could be matched. An additional 7% of the pollen could be identifiedspecifically enough to classify its source despite its absence from the reference collection.The remainder were classified as Either or Unknown (Unknown in this case refers tosamples that could not be identified even to the Family level).

Significant differences were found between the Jul. 2003 and May–Jun. 2004 datasets(Fig. 2), therefore, we treated them separately thereafter. The number of different pollen

FIG. 2.—Diversity of bee-borne pollen and flowering plants during two sampling periods. a) Meannumber of different pollen types per bee in Jul. 2003 (n 5 131) and May–Jun. 2004 (n 5 199), +/2

standard error. The means are significantly different (F 5 41.82, P , 0.0001 with 1 and 328 degrees offreedom). b) Mean flower species richness in sampling plots in Jul. 2003 (62 plots) and May–Jun. 2004(46 plots) +/2 standard error. The means are significantly different (F 5 4.33, P 5 0.04 with 1 and 106degrees of freedom)


types per bee differed significantly between the two datasets (Fig. 2a): bees collected inJul. 2003 carried an average of 2.6 pollen types, while bees collected in May–Jun. 2004carried an average of 3.8 pollen types. An opposite, and also significant, relationship wasobserved in flower species richness based on the transect data, however this relationshipwas weak (R2 5 0.039, P 5 0.04). Flower species richness per sampling plot had a meanspecies richness of 1.29 in the 2003 sampling period and a mean species richness of 0.85in 2004 (Fig. 2b).

Fragment size was found to have no significant relationship with any of the variablestested. The proportions of fragment-derived and native pollen on bees generally showedpositive relationships with fragment size, but these were never close to significance (R2 ,

0.2, P . 0.2). Similarly, the proportions of native and exotic plants in the transect data werenot consistently or significantly related to fragment size. The species richness of nativeplants in our vegetation transects was not correlated with the number of types of pollen inbee pollen loads, nor was there a correlation between the relative percentages of native/exotic plants in vegetation transects and the percentages of these pollen types in bee pollenloads.

The distribution of bee-borne pollen in the four landscape categories (Fragment, Yard,Either, Unknown) varied between the midsummer 2003 and early-summer 2004 samplingdates, partly due to the difference in the proportion of pollen that matched the referencecollection for each date. In Jul. 2003, fragments represented the largest proportion of thetotal pollen collected, comprising 57.9% of the 337 pollen occurrences. Yards wererepresented by 1.5% of pollen records (7 occurrences) and the Either and Unknowncategories made up the rest (37% and 3.1% respectively). In contrast, Either was the largestcategory in the early summer 2004 collection with 58.4% of the total pollen occurrences.Fragments represented 32.4% of the pollen and the Yard percentage grew to 7.6%. Thispattern of distribution of pollen between the four categories is reflected in the meannumber of occurrences of each pollen type per bee (Fig. 3).

The distribution of bee-borne pollen between native and exotic plant species alsoreflected the difference in identification levels between the two datasets. For the 2003 data,52.1% of the pollen carried on bees came from non-native species, 19.2% came from nativespecies and 28.7% was considered to be Either. In 2004, the Either percentage increased to

FIG. 3.—Mean number of occurrences per bee of pollen from four categories of origin (Fragment-derived, Yard-derived, Either fragment or yard, and Unknown) for two sampling dates, +/2 standarderror. a) Jul. 2003; b) May–Jun. 2004


37.3%, Exotic represented 39.3% and Native 23.4%. The data are shown in Figure 4 interms of the mean number of occurrences of each pollen type per bee.

The native plant species most commonly represented and identifiable in the bee pollenloads were Opuntia sp. (Cactaceae), two species of Helianthus, H. annuus and H. pumilus(Asteraceae) and Gaura coccinea (Onagraceae). The most common exotic species in pollenloads were also very widely distributed in fragments, based on field observations: Convolvulusarvensis (Convolvulaceae), Melilotus alba and M. officinalis (Fabaceae); Carduus nutans(Asteraceae); and Elaeagnus angustifolia (Elaeagnaceae).

DISCUSSION

The species composition of the pollen load found on a bee will be determined primarilyby: (a) the floral species composition of the surrounding landscape and (b) the foragingbehavior and preferences of the bee. In this study, bees were captured in fragments of nativegrassland surrounded by suburban residential development. We wanted to know to whatextent these grassland bees made use of exotic floral resources available in residential yards.In this landscape, the yards contain a floral community that is fairly distinct from that of thenative fragments, a community that benefits from resources that fragments lack, such asartificial irrigation, fertilization, etc. Thus, residential yards increase the overall floraldiversity of the landscape. On the other hand, the species in yards are generally exotic and/or bred and domesticated by humans, and they grow in an environment that is very differentecologically from native grassland (in terms of structure, chemistry, etc.). Are native bees inthis landscape attracted to these new and exotic resources and habitats, or do they stick tothe remnant native species and habitats? We have attempted here to shed light on therelative importance of the two components listed above: landscape floral composition andbee foraging behavior, in order to understand how the increasing occupation of naturallandscapes by humans might affect pollinator communities.

Results of the pollen load analyses showed opposite seasonal/annual signals in floralresource diversity and bee foraging behavior. Bees captured in Jul. 2003 carried fewerdistinct pollen types per bee, on average, than bees captured in May–Jun. 2004, howeverdata on floral diversity from plot transects revealed higher average floral diversity in the Jul.2003 sample. In addition to this surprising difference, the percentage of unidentifiablepollen on bees was also much higher in the May–Jun. 2004 dataset. Therefore, it would seem

FIG. 4.—Mean number of occurrences of native and exotic pollen per bee +/2 standard error for twosampling periods. The Either category represents pollen that could not be identified specificallyenough to determine its origin. a) Jul. 2003; b) May–Jun. 2004


that the early-season (2004) bees were finding and using floral resources that we did notdetect within the fragments, either in our vegetation transects or in our pollen referencecollection. It seems probable that the majority of the Unknown and Either pollen from theMay–Jun. 2004 bee samples came from yard sources not fragments. Although it was notquantified in this study, personal observation suggests that the diversity and abundance offloral resources in residential yards did indeed peak in the early summer. Analysis of beepollen loads, in this case, gives a better general picture of the overall floral diversity of thelandscape than our somewhat limited transect data. By using a similar approach, Goulson etal., (2002) were able to detect differences in floral resource diversity between suburban andagricultural landscapes.

While pollen load analysis may be useful for detecting landscape-level floral diversity, thegreater challenge in using this technique is determining exactly which species arerepresented. Success in identification can be improved by using acetolysis on the pollengrains prior to mounting them on slides (Kearns and Inouye, 1993). This process removesresidues and other substances from the surface of the pollen grain, revealing the exinestructure. However, acetolysis is time-consuming and technically challenging for sampleswith only a few pollen grains. In addition, it still does not guarantee that identifications willbe possible – even with an extensive reference collection, some species are difficult todistinguish from their close relatives under the light microscope.

The fragments of native grassland habitat used in this study ranged widely in area. Itmight be expected that the relative proportions of yard- and fragment-derived pollen wouldbe different in a 3 ha fragment than in a 59 ha fragment; one would expect bees in thesmaller fragment to make more use of yard resources than bees in the larger fragment. Inaddition, smaller fragments might be more heavily invaded by exotic plant species thanlarger ones. We found no support for either of these hypotheses in our data, however. Thismay be because all fragments were to some degree irregularly shaped, resulting in a highamount of edge. Thus, yard resources would probably be available within the foragingranges of most bees in most fragments. Also, we found no relationship between fragmentsize and the dominance of native or exotic species in the flowering plant community or inthe pollen samples. The level of invasion by exotics may be more influenced by managementhistory than by fragment area.

Due to the high levels of unidentified pollen in this study, it is difficult to make concretestatements about the relative contributions of fragment and matrix floral species to bees’pollen requirements. In addition, some pollen grains may have been lost when the beeswere rinsed. We do not know the extent of such loss, or to what extent it may be species-specific. The data do, however, provide minimum values that may be a useful starting point.A minimum of 32% of pollen types were fragment-derived in early summer 2004, whilemidsummer values in 2003 were 58%. Thus, at least a third and possibly well over half of thebees’ foraging was conducted within native habitat fragments, depending on the season.The yard component was small in both seasons; however, the yard component of the pollenreference collection was also small, therefore, we can assume that the values obtained hereconsiderably underestimate the true proportion, particularly for the May–Jun. 2004 data.

The question of bee preferences for native or alien species is similarly clouded by thelarge portion of equivocal pollen. In both seasons, the Either component was the second-largest percentage of pollen types. Once again, we can only state minimum percentages.However, in this case the pollen reference collection was less biased. Half of the species inthe reference collection were natives, yet exotic species dominated the bee pollen loads inboth datasets. We found no correlation between the percentage of exotic plants in our


vegetation transects and the percentage of exotic pollen in bee pollen loads. Thus, it isclear that wild bees were not reluctant to visit non-native species and may even seekthem out. This observation is supported by a recent study of wild bee foragers at nativeversus exotic flowers in Capitol Reef National Park, Utah (Tepedino et al., 2008) in whichthree exotic plant species were visited by, on average, twice as many bee species as nativeplants.

These results can provide some insight into how wild native bees respond to landscapechange. The patch-matrix boundary in this study was much less permeable than expected.Clearly, wild bees were able and willing to take advantage of changes that have the potentialto be beneficial, as seen in their intensive use of exotic species. But even considering thebias in the pollen reference collection, the percentage of yard-derived pollen was quite low.The exotics that dominate bee pollen loads were mostly weedy invasives that grewabundantly in fragments (white and yellow sweet clover, musk thistle, Russian olive), butwere rare in yards. In other words, bees appear to be receptive to using non-native floralresources, but in this study, they preferred not to leave the native habitat fragment in orderto do so. There may be other factors preventing bees from foraging extensively in suburbanyards, thus reducing the permeability of the boundary. For example, the increasedstructural complexity in yards may harbor a greater diversity of natural predators. Recentresearch has shown that the effects of spiders and other predators and parasitoids onpollinator populations can be considerable (Dukas, 2005) and that proximity of natural andanthropogenic land uses can be related to increased levels of higher trophic interactionssuch as predation and parasitism (Klein et al., 2006; Albrecht et al., 2007). In addition toinvertebrate predators, the trees and shrubs in yards may provide habitat for increased birdpopulations (Blair, 1996; Bock et al., 2008), which could also increase predation rates onforaging bees.

It should be noted that the bees from which the pollen was obtained were collected innative habitat fragments. The picture provided by these data is therefore incomplete. It ispossible that there exists an entire and mostly separate community of bees that nest andforage primarily in the matrix. If this is the case, competition with yard-dwelling bees couldalso deter fragment-dwelling bees from foraging extensively in yards. An extension of this ora similar study into suburban yards is warranted to provide further understanding of thisquestion.

The effects on native species of novel habitat elements such as non-native species andanthropogenic habitat types can be either positive or negative. For example, non-nativeplants are often visited intensively by native pollinators (Morales and Aizen, 2006). Whilethe pollinators may see the novel plant species as a positive contribution to their habitat,native plants may receive fewer pollinator visits as a result (Chittka and Schurkens, 2001;Larson et al., 2006). On the other hand, non-native plants and habitats may provideadditional resources that allow populations to persist in a highly modified landscape. Forexample, pine plantations provide alternative habitat for native beetles in the absence ofsufficient native forest in the landscape (Pawson et al., 2008). A recent review indicated thatthe presence of exotic plant species may, in many cases, facilitate pollination of native plantsby increasing pollinator abundance overall (Bjerknes et al., 2007) and Tepedino et al. (2008)also found evidence of such facilitation. In the present study, the pattern of high visitationto exotic plant species was observed, yet it is unknown whether the native plants areexperiencing reduced pollination services. The bees used in this analysis were stronglynumerically dominated by generalist species of the family Halictidae, which have beenobserved to be very receptive to exotic plant species (Larson et al., 2006). It may be that


other bee species continue to provide adequate pollination to native flowers. Pollinationfunction in a landscape is effectively the sum of all of the individual pollinator species’ecological responses.

Use of pollen grains to detect bee foraging movements has great appeal because it doesnot involve actively tracking an individual’s movements. The individual is caught and arecord of its recent floral visits is already present on its body. In landscapes where a uniquefloral community characterizes different land uses, this technique has the potential to bevery powerful. The success of pollen load analysis rests on two requirements: (1) acomprehensive pollen reference collection and (2) the ability and equipment to distinguishbetween pollen grains at the genus or species level. The landscape of the present study is aheterogeneous one, with high floral diversity in both habitat fragments and suburban yards,particularly in the early summer. This contributed to the high percentage of pollen thatcould not be attributed to a specific source. In a less floristically complex landscape, such asone dominated by intensive agriculture, pollen load analysis has the potential to beinformative, as some studies have found (DeGrandi-Hoffman et al., 1992; Williams andKremen, 2007).

Acknowledgments.—We would like to thank M. Breed, G. Carey, S. Collinge, C. Kearns, C. Wessman andtwo anonymous reviewers for comments on the manuscript. Excellent field assistants for the projectwere E. Becker and K. Krend, with additional lab assistance from L. Friedman. S. Hinners receivedsupport for this research from Boulder County Open Space, Boulder Open Space and Mountain Parks,the Department of Ecology and Evolutionary Biology at the University of Colorado, Boulder and theNational Science Foundation.

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Receptiveness of Foraging Wild Bees to Exotic Landscape Elements