Insect Visitors and Pollination Ecology of Spalding's Catchfly (Silene spaldingii) in the Zumwalt Prairie of Northeastern Oregon Author(s): Carmen Tubbesing , Christopher Strohm , Sandra J. DeBano , Natalie Gonzalez , Chiho Kimoto and Robert V. Taylor Source: Natural Areas Journal, 34(2):200-211. 2014. Published By: Natural Areas Association DOI: http://dx.doi.org/10.3375/043.034.0209 URL: http://www.bioone.org/doi/full/10.3375/043.034.0209
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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. R E S E A R C H A R T I C L E ABSTRACT: Silene spaldingii S. Watson (Spalding’s catchfly) is a threatened wildflower that relies on insect-mediated pollination. However, its pollination ecology is not well understood, particularly in the Zumwalt Prairie of northeastern Oregon, which contains the largest known S. spaldingii population. Our objectives were to: (1) describe the principal insect visitors to S. spaldingii in the Zumwalt Prairie, (2) quantify the available pool of pollinators in the area, and (3) determine whether the visitation rate to individual plants is associated with the density of S. spaldingii at the patch scale, as predicted by the • resource concentration hypothesis, and/or by the density and composition of non-S. spaldingii bloom- ing plants, as predicted by the facilitation and competition hypotheses. We recorded insect visits to S. spaldingii during peak bloom at 30 patches and characterized the local bee community using blue vane traps. We quantified the patch-scale density of S. spaldingii and the composition and abundance of other blooming species at each patch. Two bumble bee species comprised all observed visits, although they Insect Visitors and constituted only 20% of the total bees sampled on the prairie. Bumble bees showed a high degree of host fidelity even when other blooming plants were present. Per capita visitation rates increased with catchfly density and blooming plant abundance at the patch scale, supporting the resource concentration Pollination Ecology and facilitation hypotheses. Silene spaldingii in the Zumwalt Prairie appears to rely on a narrow pool of pollinators that may preferentially visit it over other blooming plants, and more dense patches of S. of Spalding’s spaldingii may increase pollination efficiency.
Index terms: bumble bees, native bees, pollinators, Silene spaldingii, Spalding’s catchfly, Zumwalt Catchfly (Silene Prairie Preserve spaldingii) in the INTRODUCTION Zumwalt Prairie • Native plants in the Pacific Northwest face a variety of threats related to habitat of Northeastern destruction (e.g., agricultural/urban/sub- 2 Biology Department urban conversion) and degradation (e.g., Oregon Mercyhurst College non-native plant invasions, recreational Erie, PA 16546 activities, improper livestock grazing practices) (Parish et al. 1996; Parks et al. 2005). In Oregon alone, 60 plant species 3Department of Fisheries and Wildlife are listed as threatened or endangered by Oregon State University 1 the state and federal governments (ODA Carmen Tubbesing Hermiston Agricultural Research and 2011). Anthropogenic disturbances not Extension Center only directly impact plants, but can also 1Biology Department Hermiston, OR 97838 affect pollinators on which many flowering Brown University plants depend (Kearns et al. 1998; Aguilar Providence, RI 02912 et al. 2006; Winfree et al. 2009). The risk 4Biology Department of pollination failure is highest in systems Texas State University where plants are pollinated by relatively Christopher Strohm2 San Marcos, TX 78666 few species (Wilcock and Neiland 2002), 3,7 Sandra J. DeBano especially those that require specialized 4 pollinators (e.g., Steiner and Whitehead Natalie Gonzalez 5Department of Fisheries and Wildlife Chiho Kimoto5 Oregon State University 1996). Therefore, an important step for the protection of threatened plant species that 6 Corvallis, OR 97331 Robert V. Taylor rely on pollinators is identifying significant pollinators and understanding factors that 6The Nature Conservancy influence plant-pollinator relationships, including the spatial distribution and den- 7 Corresponding author: sandy.debano@ Enterprise, OR 97828 oregonstate.edu: 541-567-6337 Ext. 116 sity of floral resources (Kearns et al. 1998; Kremen et al. 2007).
In this study, we focused on one such • threatened plant species, Spalding’s Natural Areas Journal 34:200–211 catchfly (Silene spaldingii S. Watson: Caryophyllaceae), a perennial forb na-
200 Natural Areas Journal Volume 34 (2), 2014 tive to the Pacific Northwest Bunchgrass Wardell et al. 1998; Kearns et al. 1998). may act as an attractant for pollinators. Prairie, one of the most threatened and Generalist pollinators may be more likely understudied grasslands in North America Additionally, we know little about how to visit S. spaldingii where it coexists (Tisdale 1982). Historically, this unique spatial variability in floral resources af- with other species that bloom at the same grassland type covered over 8 million fects pollinator visitation of S. spaldingii. time. Alternatively, nearby blooming forbs hectares, but over 90% of it has been con- Plant-pollinator relationships are highly could compete with S. spaldingii, attract- verted to agriculture (Tisdale 1982). This contextual and depend on a number of ing pollinators that would otherwise visit habitat loss has limited S. spaldingii to variables, including the distribution of the S. spaldingii. According to the competi- small, fragmented populations throughout target plant species as well as the identity tion hypothesis (Pleasants 1980; Rathcke its original range in Washington, Oregon, and abundance of proximate plant species 1983; Mitchell et al. 2009), competition Idaho, and Montana. In 2001, the species with overlapping flowering phenologies for pollinators among plants has resulted was listed as “threatened” by the United (Kunin 1997; Ghazoul 2005; Kremen et in plant species evolving spatially and/or States Fish and Wildlife Service (U.S. Fish al. 2007). For S. spaldingii, these factors temporally distinct blooming periods. This and Wildlife Service 2007). have not been studied. hypothesis leads to the prediction that S. spaldingii would have lower pollinator The importance of insect pollination in S. Even in areas with relatively large popu- visitation rates in patches with higher spaldingii reproduction is well established. lations (> 50,000 individuals), such as at densities of heterospecific plants. In fact, This perennial forb is a long-lived, sexually The Nature Conservancy’s Zumwalt Prairie Lesica and Heidel (1996) suggested that reproducing plant with a low reproductive Preserve in northeastern Oregon (U.S. Fish non-native plants may compete with S. rate. Although it can produce seed through and Wildlife Service 2007), the local den- spaldingii for pollinators. geitonogamous self-pollination, fecundity sity of flowering S. spaldingii plants can (i.e., production of viable fruits and seeds) vary widely (e.g., 0.01 to 0.3 individuals The objectives of this study were to: (1) is much greater when insects move pollen m-2 in 2006 – 2008, R.V. Taylor et al. describe the principal insect visitors to the from one plant to another (Lesica 1993). unpubl. data). The resource concentra- threatened plant S. spaldingii within the Lesica (1993) found an overall reduction tion hypothesis (Root 1973) suggests that Zumwalt Prairie Preserve, (2) quantify the in S. spaldingii fitness of more than 95% herbivores are more likely to find and use available pool of pollinators in the area, in the absence of insect pollinators due dense concentrations of host plants. This and (3) determine whether the frequency to decreases in the proportion of fruits work has been extended to pollinators, with which a S. spaldingii plant is visited maturing, the number of seeds per fruit, often in the context of Allee effects in is associated with the patch-level density of rates of germination, and seedling growth plant populations, where low densities S. spaldingii, or the density and composi- and survival. Subsequently, Lesica and can reduce reproductive rates because of tion of non-S. spaldingii blooming forbs Heidel (1996) found that the rate of fruit decreased per capita visitation rates by pol- and shrubs. abortion was negatively correlated with linators (Platt et al. 1974; Silander 1978; METHODS the rate of insect visitation. Thus, there is Thomson 1981; Feinsinger et al. 1986; ample evidence that insect-mediated cross- Sih and Baltus 1987; Klinkhamer et al. pollination is critical to maintaining viable 1989; Kunin 1997; Groom 1998). If this Species Description populations of this species. phenomenon occurs for S. spaldingii, then individual plants in denser patches would Silene spaldingii Wats. (Caryophyllaceae) However, several significant gaps remain garner more visits from pollinators than is an iteroparous, tap-rooted, perennial herb in our understanding of the pollination those in lower density patches, allowing having one to several stems 20 – 50 cm ecology of S. spaldingii, including the more opportunity for pollination. in height (Hitchcock et al. 1969; Lesica identity of its current pollinators. Work by 1999). Plants reproduce only by seed; no Lesica (1993) and Lesica and Heidel (1996) The effect of other blooming plant spe- reproduction via rhizomes or other asexual at five locations in Washington, Oregon, cies on S. spaldingii pollination is also means has ever been observed (Lesica and Idaho between 1988 and 1995 found unknown, although hypothetically, higher 1993; Lesica and Crone 2007). Within a that over 90% of visitors to S. spaldingii densities of blooming heterospecific plants growing season some plants remain dor- were of one bumble bee species, Bombus at the patch scale can either increase pol- mant, some lack reproductive structures, fervidus (Fabricius). Other insects observed linator availability for S. spaldingii via and others bear flowers. Flowers (3 – 20 on flowers included halictid bees, noctuid facilitation (Waser and Real 1979; Schem- per stem) are hermaphroditic, and borne moths, and one vespid wasp (Lesica and ske 1981; Feldman et al. 2004; Moeller in a branched, terminal, cymose inflore- Heidel 1996). Although these data provide 2004) or decrease it through competition secence (Lesica 1999; Lesica and Crone important baseline information about po- (Pleasants 1980; Rathcke 1983; Mitchell 2007). Stems, leaves, and flower bracts are tential pollinators of S. spaldingii over 15 et al. 2009; Morales and Traveset 2009). densely covered with sticky, glandular hairs years ago, more current data are needed to The facilitation hypothesis predicts that, for (Hitchcock et al. 1969). Flowers are tubular, inform recovery planning, especially given generalist pollinators, the total density of bell-shaped, and have a single, one-celled concerns over pollinator declines (Allen- all blooming plants, regardless of species, ovary and 2 – 10 anthers (Hitchcock et al.
Volume 34 (2), 2014 Natural Areas Journal 201 1969). Five, cream-colored, lobed petals barely extend beyond the calyx, each of which has four appendages. Flowers bloom asynchronously, beginning on the Zumwalt Prairie mid-July and continuing into late August (Taylor et al. 2012). Flowers remain open for two to several days (Lesica 1993). Within a flower, anthers mature and shed pollen before styles expand and stigmas become receptive to pollen, reducing the likelihood of self pollination (Lesica 1993). Open flowers may be available for two to several days and more than one flower may be in bloom on the same plant, allowing for geitonogamous pollination (Lesica 1993). Fertilized flowers mature vertically into capsules, each of which holds an average of 61 seeds (R.V. Taylor, unpubl. data). Although S. spaldginii is self-compat- ible, seed production, germination rates, and seedling growth are all substantially lower in fruits resulting from self-pollina- tion (Lesica 1993). Seed dispersal studies have not been conducted; however, seeds from ruptured cup-shaped fruit capsules are probably dispersed by wind, passing wildlife, or when the plant is knocked over Figure 1. (a) Location of the Zumwalt Prairie in eastern Oregon, (b) boundaries of the Zumwalt Prairie (U.S. Fish and Wildlife Service 2007). Preserve, and (c) the location of the 30 S. spaldingii patches and the four blue vane traps. Study Area
The study was conducted at the Zumwalt bumble bee (Bombus occidentalis Greene), es (described above) as well as at one other Prairie Preserve (lat 45º 34’ N, long 116º which has declined in western Oregon and location on the preserve (Grader Pasture), 58’ W) located in Wallowa County in Washington (Rao et al. 2011). where blooming catchfly was also known northeastern Oregon (Figure 1a,b). The to occur. Our 10-day observation period 13,269-ha preserve is owned and managed The preserve has a large population of S. occurred in the middle (and presumably by The Nature Conservancy (TNC) and lies spaldingii (estimated at > 50,000 plants during the peak) of the 29-day blooming in the southwestern portion of the Pacific across 112 ha) with a patchy distribution season in 2010 documented by the annual (Taylor et al. 2009), including a relatively Northwest Bunchgrass Prairie (Tisdale demography and phenology monitoring dense concentration in Harsin Pasture in 1982). At 1060 – 1680 m elevation, the survey of the preserve by TNC (Taylor et the southern portion of the preserve (Figure preserve is dominated by native bunch- al. 2012). The blooming season extended 1c). We attempted to locate all S. spaldingii grasses, including Idaho fescue (Festuca from 22 July to 19 August 2010, with 85% plants that had been documented in Harsin idahoensis Elmer), Sandberg bluegrass of all blooms recorded that year before 13 Pasture in a previous study using GPS (Poa secunda J. Presl), prairie Junegrass August (Taylor et al. 2012). (R.V. Taylor et al. unpubl. data). When (Koeleria macrantha (Ledeb.) Schult.), and a S. spaldingii plant could be found, we bluebunch wheatgrass (Pseudoroegneria We conducted 76.25 person-hours of ob- used the location as the center of a 15-m spicata (Pursh) A. Löve). It has a diverse servations by walking from patch to patch radius sampling patch. We were able to assemblage of over 112 forb species; com- recording all instances of insect visits to S. locate 30 patches in Harsin Pasture that mon species include Aster L. spp., western spaldingii, following visitors to multiple were separated from each other by at yarrow (Achillea millefolium L.), lupines plants, and capturing when possible. We least 30 m. (Lupinus L. spp.), prairie smoke (Geum collected data on species and caste iden- triflorum Pursh), and cinquefoil (Poten- Observations of Insect Visitors tification for captured individuals, genus tilla L. spp.) (Kennedy et al. 2009). The identification for non-captured individuals, Preserve also supports a diverse native bee Observations of insect visits to S. spaldingii and the number and identity of flowering community (Kimoto, DeBano, Thorp, Rao, flowers were conducted between 3 and 12 plants visited. These observations were and Stephen 2012a), including the western August 2010 at the 30 Harsin Pasture patch- supplemented with observations described
202 Natural Areas Journal Volume 34 (2), 2014 in the “Density and Competition Studies” Available Pollinators Bees collected during observations and in section below and seven person-hours after traps were frozen, pinned, labeled, sexed, dusk between 2000 and 2300 using red- We estimated the pool of native bees, a and identified to genus, and for bumble tinted lights (to minimize the likelihood taxon believed to include major pollina- bees, species. We treat B. californicus and of attracting insects). All three activities tors of S. spaldingii (Lesica 1993; Lesica B. fervidus as one species (B. fervidus) resulted in a total of 91.25 person-hours and Heidel 1996), by sampling for 24 although their taxonomic status remains uncertain (Williams 2010). Representative spent by five observers in areas containing hours with four UV-reflective blue vane specimens of all species are vouchered at traps (Stephen and Rao 2005, 2007) in catchfly. Most person-hours were spent at the Oregon State Arthropod Collection at Harsin Pasture, but 17 person-hours were an adjacent area of bunchgrass prairie Oregon State University in Corvallis. spent at Grader Pasture. within the Zumwalt Prairie Preserve on 4 – 5 August 2010. Vegetation in this area Density and Competition Studies Additionally, bees caught on S. spaldingii was similar to that of Harsin and Grader were checked for pollen in the hair cover- Pastures. Blue vane traps were separated To determine whether the frequency of ing their bodies. Pollen was photographed by approximately 200 m, and were more insect visitors to S. spaldingii flowers was S. spaldingii using scanning electron microscopy (SEM) than 2.5 km away from catchfly patches. related to the patch density of or other blooming forbs and shrubs, we at Oregon State University. We collected Blue vane traps consist of a clear plastic monitored each of the 30 patches in Harsin pollen samples from anthers of the only container (15-cm diameter × 15-cm high) Pasture four times, once within each of the other species in Caryophyllaceae (Dianthus with a blue polypropylene screw funnel following time periods: 0800 – 1000, 1000 armeria S. scouleri, S. douglasii) with two 24-cm × 13-cm semitransparent , and that – 1200, 1300 – 1530, and 1530 – 1800. blue polypropylene cross vanes of 3 mm were blooming at that time and examined During each of these time periods, each them with SEM. All pollen was collected at thickness (SpringStar™ LLC, Woodinville, patch was observed for two min by two the preserve except for that of D. armeria; WA, USA; Figure 2a; Stephen and Rao individuals simultaneously, so that two per- insufficient collection at the preserve re- 2005). Traps were suspended approxi- son-hours of observations (30 patches × 2 quired the use of samples from plants in mately 1.2 m from the ground with wire minutes/patch × 2 people) were conducted Corvallis, Oregon. We compared images hangers inserted into aluminum pipes. No in each time period. Although the afternoon of pollen on bees’ bodies with pollen from liquids or other killing agents were used time periods were 0.5 hours longer than the blooming species of Caryophyllaceae. in traps. morning periods, the number of minutes
Figure 2. (a) Blue vane trap in grassland adjacent to S. spaldingii observation patches, and (b) B. fervidus visiting S. spaldingii. Photograph taken by C. Strohm using a Canon Powershot A540.
Volume 34 (2), 2014 Natural Areas Journal 203 of observations in each time period was visits to catchfly plants at each patch, and RESULTS equal. During each two minute observation divided this number by the total number session, the same two people recorded and, of catchfly plants at the patch to calculate Insect Visitors to Catchfly if possible, captured, any visitors to flowers a per capita visitation rate for each patch of S. spaldingii within view of the patch’s throughout the duration of the study. The Throughout the entire study, we observed center (an approximately 15 m radius). resource concentration hypothesis predicts 78 visitation bouts in which a flying insect Collected specimens were identified to that per capita visitation rate will be posi- landed on one or more catchfly flowers species and caste; individuals not collected tively correlated with catchfly density at (the only other insects found on flowers were identified to genus. the patch. The facilitation hypothesis pre- were caterpillars, which were observed dicts that per capita visitation rate will be feeding on all parts of the plant). All flying Silene spaldingii density was recorded by positively correlated with forb and shrub visitors were bumble bees (Bombus). Data counting the stems of catchfly within a blooming abundance and species richness from the density and competition portion 10-m radius of the “focal” catchfly plant while the competition hypothesis predicts of the study allowed us to compare diurnal at the center of the patch following the a negative correlation with these variables. patterns (because of equal observation first observation period at each patch. In addition, the possibility exists that only effort per time period) and showed that The density of all blooming, non-catchfly a subset of blooming plants may be key in bumble bee visitations were more frequent plants was estimated by counting stems of driving facilitation or competition. In this in the afternoon than the morning. Only all non-catchfly blooming forbs or shrubs case, we predict that per capita visitation 4% of visitors were observed in the 0800 within 3 m of the focal plant. A blooming rate will vary with changes in blooming – 1000 period, while 21% were observed stem was defined as containing visible community composition at a patch. To test between 1000 and 1200, 43% between anthers and/or stigmas on at least one this, we used non-metric multidimensional 1300 and 1530, and 32% between 1530 open flower. The total number of bloom- scaling (NMS) ordination to characterize and 1800. Fifty-five individuals visiting catchfly were collected in all portions of ing forb and shrub species within a 3 m the blooming forb and shrub community the study, of which 10% were B. appositus radius was also counted and the identity of at each patch. NMS ordination is a robust Cresson and 90% B. fervidus (Figures 2b, each species recorded; however, counts of technique based on ranked distances and 3a). Percentages of workers, queens, and stem abundance for each species were not performs well with data that are not nor- males are shown in Figure 4 a,c,e. made. When an insect visitor was observed mally distributed and contain numerous at a S. spaldingii plant that was not the zero values (McCune and Grace 2002). We were able to follow 27 visitors to focal individual but that was within the NMS was run on the presence/absence multiple plants, with the average number patch, the non-catchfly blooming density data of plant species using Sorenson’s of plants visited being seven, including and richness was also estimated within distance measure. We excluded all plant both S. spaldingii and non-S. spaldingii. the 3 m radius surrounding that catchfly species that occurred at less than 10% of Fifteen percent of bees visited only one plant. Because surrounding blooming plant patches from the analyses to reduce noise S. spaldingii plant within the bout, 52% composition may have changed at the first (McCune and Grace 2002), resulting in a visited 2 – 5 S. spaldingii plants, 11% patches we monitored between initial data data set reduced from 21 to 13 species. The visited 6 – 10, 19% visited 11 – 15, and collection and completion of all observa- best solution was determined through 250 4% visited more than 15 consecutively. tion periods, we repeated stem-counts and runs of randomized data and dimensionality Fifty-nine percent of the 27 bees visited species tallies of non-catchfly blooming was determined by evaluating the relation- only S. spaldingii flowers. These visita- plants at patches for which observation ship between final stress and the number tion bouts occurred in areas with flowers periods were separated by more than of dimensions. Ordinations were run using of many other species (listed in Table 1), three days. The scale of measurement for PC-ORD, version 5.19, set on “autopilot” and bees often flew over other blooming intra- and inter-specific densities differed mode (McCune and Mefford 2006). forbs as they traveled from one S. spaldingii because S. spaldingii density was much plant to another. lower than all non-target blooming forbs Patch-level variables analyzed included Attempts to take SEM photographs of pol- and shrubs. Thus, meaningful variation in NMS scores, abundance and species rich- S. spaldingii density occurred at a larger len on bees that were caught on S. spaldin- ness of blooming forbs and shrubs, and gii resulted in one photograph with distin- patch size than variation in all non-target density of catchfly. Because most variables guishable pollen. The pollen was located bloom density. were not normally distributed, Spearman on the face of one B. fervidus worker and Statistical Analyses rank correlation was used to test whether its shape and external markings matched each patch-level variable was significantly S. spaldingii pollen and did not match the To test predictions generated by the associated with per capita visitation rate. pollen of the other three Caryophyllaceae resource concentration, facilitation, and All univariate analyses were conducted species that were blooming at the study site competition hypotheses, we summed all with SYSTAT (1997). during the study period (Figure 5). This
204 Natural Areas Journal Volume 34 (2), 2014 provides anecdotal evidence that Bombus resulted in a two axis solution, with axis the Zumwalt Prairie Preserve are bumble carries pollen of S. spaldingii. 1 explaining 45% of the variation in bees, a conclusion consistent with these plant community composition and axis 2 other studies (Lesica 1993; Lesica and Available Pollinators explaining 29%), the number of visits per Heidel 1996). However, although Lesica catchfly plant was not significantly cor- and Heidel (1996) identifiedB. fervidus as Blue vane traps in an adjacent grassland related with axis 1 (r = 0.34, P > 0.05, n the only species of bumble bee associated yielded 444 bees in 10 genera; 47% of s = 30) or axis 2 (r = 0.13, P > 0.05, n = with S. spaldingii throughout its range, we bees collected were Bombus and 53% s 30). The number of visits per catchfly plant found that 10% of bees visiting the plant belonged to other genera. A total of nine did not significantly increase with bloom- in the Zumwalt Prairie were B. appositus species of Bombus were collected. B. fer- ing forb and shrub species richness (r = (Figure 3a). In addition, they found non- vidus made up 19% of Bombus individuals s 0.34, P > 0.05, n = 30). However, patch- bumble bee visitors; at one location, 17% caught in traps and 9% of all bees, while scale density of blooming non-catchfly of S. spaldingii visitors were halictid bees, B. appositus made up 25% of Bombus and forbs/shrubs showed a positive relationship and at two other locations noctuid moths 11% of all bees (Figure 3b). Percentages with per capita pollinator visits (r = 0.42, and vespid wasps were rare visitors (2% of workers, queens, and males are shown s P < 0.05, n = 30). There was a significant and 1%, respectively). In contrast, we did in Figure 4b,d,f. positive correlation between the densities not observe any non-bumble bee flower Density and Competition Studies of catchfly and blooming plants at each visitors. patch (rs = 0.39, P < 0.05). Of the 78 visitations described above, DISCUSSION Several lines of evidence suggest that these 28 occurred during the course of the two species of bumble bees are providing density and competition studies, during Extensive research on Silene has shown that pollination services for S. spaldingii at which 440 S. spaldingii plants in 30 plots most species in this genus are either primar- the Zumwalt Prairie. First, since recruit- were observed, resulting in a visitation ily pollinated by Lepidoptera (especially ment of S. spaldingii is pollinator-limited rate of 0.008 visits per catchfly plant per nocturnal moths) or bumble bees (Kephart (Lesica 1993) and the size of the Zumwalt hour. Patches with higher densities of S. et al. 2006). However, the relative roles of population is relatively large, some plants spaldingii were visited by more potential pollinators are expected to vary spatially can be assumed to be receiving pollination pollinators than patches characterized by and temporally and with a variety of factors, services. The fact that no other invertebrates low catchfly densities, and the number of including patch size and isolation (Kephart were found visiting the plant in over 90 visits per catchfly plant increased with 2006). Our study adds to previous work person-hours of observation during the conducted on smaller populations of S. peak blooming season suggests that these catchfly density (rs = 0.51, P < 0.005, n = 30). Although patches varied in bloom- spaldingii in other areas, and suggests that two species of bumble bees are the most ing plant composition (NMS ordination the principal pollinators of S. spaldingii in significant pollinators. Second, we ob-
Figure 3. Comparison of (a) Bombus species observed visiting S. spaldingii, and (b) Bombus collected in an adjacent grassland using blue vane traps.
Volume 34 (2), 2014 Natural Areas Journal 205 our discovery of S. spaldingii pollen on the face of a Bombus worker caught on a catchfly flower suggests that bumble bees actually transport S. spaldingii pollen.
Males accounted for 49% of Bombus individuals caught on S. spaldingii and 64% of those caught in blue vane traps. These are larger proportions than would be expected for bumble bees in most times of the year, but male bumble bees can reach significant numbers in the late summer (Kearns and Thomson 2001) and some- times even outnumber workers (Ostevik et al. 2010). Though males generally visit fewer flowers than female workers do, they may be more effective pollinators (Ostevik et al. 2010). Ostevik et al. (2010) found that males transfer more pollen between each flower, potentially because they have denser, longer pile (Kearns and Thomson 2001), spend more time handling each flower (Ostevik et al. 2010), and do not remove pollen into corbiculae (i.e., the pollen baskets found on the hind tibiae of most female bumble bees). Male bumble bee pollination may also reduce inbreed- ing depression because males are not tied down to a colony and, therefore, have larger foraging ranges (Kraus et al. 2009), and switch between patches of host plants more frequently than female workers (Ostevik et al. 2010). Therefore, the high propor- tion of male Bombus individuals visiting S. spaldingii may result in more effective pollination than if flowers were pollinated by females only.
Bombus fervidus and B. appositus may visit S. spaldingii more frequently than other bumble bees because they are long- tongued. A bumble bee’s tongue or pro- boscis length often corresponds with the corolla depth of the flower it visits (Pleas- Figure 4. Comparison of percentages of males, workers, and queens collected while visiting S. spaldingii ants 1980), and species with long tongues and in blue vane traps for B. appositus (a, b), B. fervidus (c, d), and both species combined (e, f). may prefer and forage more efficiently on flower species not available to most short-tongued bees (Hobbs 1962). Catchfly served Bombus individuals visit multiple caused by pollinators frequently switching flowers have long narrow corollas that may catchfly plants consecutively. Only 15% between plant species, or interference com- require bumble bees with long tongues to of observed multiple-plant visitation bouts petition, significantly reduces seed set of reach the nectar and pollen (Figure 2b). involved only one catchfly plant, while plants (Waser 1978; Petit 2011). Therefore, The species found visiting catchfly were 34% included six or more. Over half of high pollinator constancy is important for the two most common long-tongued bees the bouts, in which bees visited an aver- providing efficient pollination services. Our present at the Zumwalt Prairie during the age of seven plants, were exclusively to observations suggest that Bombus provides S. spaldingii blooming period, making up S. spaldingii. Interspecific pollen transfer this necessary pollinator constancy. Third, 19% and 25% of all bumble bees captured
206 Natural Areas Journal Volume 34 (2), 2014 Table 1. Blooming plants observed through the course of the study and the number of patches in which the species was present.
Family Name Scientific name # of patches (common name) occurred at:
Apiaceae Perideridia gairdneri (Hook. & Arn.) Mathias 10 (Gardner's yampah)
Asteraceae Erigeron pumilus Nutt. 12 (shaggy fleabane)
Cirsium brevifolium Nutt. 3 (Palouse thistle)
Pyrrocoma carthamoides Hook var. cusickii (A. Gray) 2 Kartesz & Gandhi (largeflower goldenweed)
Grindelia squarrosa (Pursh) Dunal 2 (curlycup gumweed)
Symphyotrichum campestre (Nutt.) G.L. Nesom var. 11 campestre (western meadow aster)
Solidago missouriensis Nutt. var. missouriensis 16 (Missouri goldenrod)
Hieracium cynoglossoides Arv.-Touv. 8 (houndstongue hawkweed)
Achillea millefolium L. var. occidentalis DC. 24 (western yarrow)
Caprifoliaceae Symphoricarpos albus (L.) S.F. Blake 1 (common snowberry)
Caryophyllaceae Silene scouleri Hook. 2 (simple campion)
Dianthus armeria L. 7 (Deptford pink)
Fabaceae Lupinus leucophyllus Douglas ex Lindl. 2 (velvet lupine)
Continued
Volume 34 (2), 2014 Natural Areas Journal 207 Table 1. Blooming plants observed through the course of the study and the number of patches in which the species was present.
Table 1 (Continued ) Family Name Scientific name # of patches (common name) occurred at:
Gentianaceae Gentiana affinis Griseb. 1 (pleated gentian)
Geraniaceae Geranium viscosissimum Fisch. & C.A. Mey. ex C.A. Mey. 1 (sticky purple geranium)
Liliaceae Calochortus macrocarpus Douglas 5 (sagebrush mariposa lily)
Onagraceae Clarkia pulchella Pursh 6 (pinkfairies)
Epilobium brachycarpum C. Presl 9 (tall annual willowherb)
Polygonaceae Eriogonum heracleoides Nutt. var. angustifolium (Nutt.) 3 (parsnipflowerTorr. & A. Gray buckwheat)
Scrophulariacea Orthocarpus tenuifolius (Pursh) Benth. 10 (thinleaved owl's-clover)
Castilleja oresbia Greenm. 1 (pale Wallowa Indian paintbrush)
in blue vane traps, respectively (Figure 1978; Thomson 1981; Feinsinger et al. long proboscises that aid in accessing S. 3). Other bumble bees abundant in blue 1986; Klinkhamer et al. 1989) as well as spaldingii floral resources. They also dis- vane traps, such as B. bifarius Cresson experimental results showing more visitors play pollinator constancy, visiting multiple (19%) and B. rufocinctus Cresson (21%), per plant in patches of plants placed closer catchfly plants consecutively. These factors have intermediate or short tongues. Other together than those placed farther apart imply that these two bumble bee species long-tongued bees, such as B. flavifrons (Kunin 1997). According to the resource may be specializing or “majoring” (sensu, Cresson, B. centralis Cresson, and B. concentration hypothesis, herbivores con- Heinrich 1976) on S. spaldingii in this area nevadensis Cresson, were relatively rare, centrate in dense patches of their host plants during this part of the season, which would making up 5% or less of bumble bees in (Root 1973), with the effect being strongest account for their preference of dense host blue vane traps. for highly specialized herbivores that have patches under the resource concentration adapted tolerance to host-specific herbivore hypothesis. Bees visited individual S. spaldingii plants resistance. Similarly, pollinators that are more frequently when the plants were in specialized to access and benefit from the Although previous work (Lesica and Heidel more dense patches. This is consistent floral resources of a particular plant may 1996) has suggested that other species of with several studies finding higher pol- be more likely to disproportionately occupy blooming plants may act as competitors lination success and reproduction in more dense stands of that plant. The bumble bees of S. spaldingii for pollinators, our results dense patches (Platt et al. 1974; Silander B. fervidus and B. appositus both have do not support this hypothesis. Instead of
208 Natural Areas Journal Volume 34 (2), 2014 al. 2007), conservation strategies should incorporate information about small-scale densities. In portions of the plant’s range that have cattle (Bos) or large populations of other herbivores, fencing particularly dense patches of S. spaldingii may be an ap- propriate conservation tool since ungulate herbivory can be substantial (Taylor et al. Figure 5. SEM photographs of pollen from (a) the face of a B. fervidus worker caught visiting S. spaldingii, 2012). In addition, declines in patch-level (b) S. spaldingii, (c) S. scouleri, (d) S. douglasii, and (e) D. armeria. density of S. spaldingii due to other factors could result in a “positive” feedback spiral if these diminished patches fail to attract decreased per capita visitation rates to S. require pollination by few species with significant numbers of bees, and plants in spaldingii in areas with higher densities of specialized morphologies are more sensi- these patches begin to suffer from pollen other blooming species, we found higher tive to land-use change than plants that limitation. Likewise, land use or manage- per capita visitation rates, and no difference can be pollinated by a wide variety of ment actions that result in decreased na- in visitation rates at patches with varying generalist pollinators (Kremen et al. 2007). tive forb abundance may also negatively richnesses of blooming species or differ- Silene spaldingii appears to have only two impact catchfly populations via decreases ent blooming species compositions. These major pollinators in the Zumwalt Prairie, in pollinator visitation rates. results are consistent with the facilitation of which one (B. fervidus) accounts for ACKNOWDEGMENTS hypothesis; patches with high densities 90% of visits, and those pollinators ap- of flowers may attract B. fervidus and B. pear to preferentially visit catchfly. It is, therefore, vital to prevent B. fervidus and We thank R. Halse and J. Dingeldein for appositus, increasing catchfly visitation in B. appositus populations from declining. help with plant identification, W.P. Stephen those patches. Facilitation is expected to Like most bumble bees, these two species and R.W. Thorp for confirming bumble occur with generalist pollinators, which can nest in underground cavities or above bee species identification, V. Jansen and these species are. B. appositus has been ground in grass tussocks (Hobbs 1966a, H. Schmalz for producing maps and in- found on 9 families and 18 genera of b; Thorp et al. 1983). Understanding how formation on patch characteristics, and A. Moldenke and S. Rao for programmatic flowers and B. fervidus has been found sensitive these habitats are to a variety of support. We also thank W.D. Blankenship, on 15 families and 34 genera of flowers land-use changes, including fire, livestock (Thorp et al. 1983). However, once at the grazing, and pesticide use, is important for S. Bonner, S. Galbraith, C. Peyton, D. patch, B. fervidus and B. appositus may the continued recovery of S. spaldingii. Snodgrass, and S. Thomas for their help in preferentially visit S. spaldingii because In addition, management of grasslands the field and laboratory. Two anonymous their proboscis morphology is particularly should ensure that floral resources for reviewers provided helpful comments on well suited for taking advantage of its pol- these long-lived generalist bumble bees the manuscript. This material is based upon len and nectar sources. Thus, these two are available throughout the season, not work supported by the National Science Foundation under Grant No. 0755511. species may be “facultative specialists,” just when catchfly is in bloom (Menz et Publication of this paper was supported, in the sense that they may be attracted to al. 2011). This may include limiting heavy in part, by the Thomas G. Scott Publica- grazing in early and mid summer, which patches of dense floral resources but are tion Fund. then selective within the patch because can decrease floral resources available to of morphological characteristics that may bumble bees in Pacific Northwest Bunch- impart more efficient handling of certain grass Prairie (Kimoto, DeBano, Thorp, Carmen Tubbesing is a biological techni- flowers (Heinrich 1979). However, more Taylor, et al. 2012b). cian with Nature’s Capital, an Ecological work is needed to examine the relative Assessment Services company based in strength of facilitation and resource con- Additionally, this study showed that dense Boise, Idaho. She recently graduated from centration effects, because, in our study, patches of catchfly plants are disproportion- Brown University with a B.S. in Biology. there was a weak but significant positive ately important for conservation, since they Carmen plans to pursue graduate work are visited more frequently by pollinators correlation between the densities of catch- in forest ecology after exploring a variety and thus probably have greater seed set of field work. fly and blooming plants at each patch. and recruitment. Other work has found that Implications for Conservation dense floral patches tend to have higher Christopher (Chris) Strohm is a graduate pollinator constancy, further improving student in the Department of Entomology at This study supports Lesica (1993) and pollination services (Kunin 1997). Because the University of Kentucky. Chris received Lesica and Heidel’s (1996) conclusions population traits such as patchiness are a B.S. in Biology from Mercyhurst College. concerning the importance of protecting likely to be affected rapidly by land-use His research interests are focused in plant- pollinators of S. spaldingii. Plants that changes and management (Kremen et insect interactions including the impacts
Volume 34 (2), 2014 Natural Areas Journal 209 of invasive species on insect communities C.E. Jones, K. Kennedy, P. Kevan, H. Koo- breeding passerine birds: implications for and the conservation of native plants and powitz, R. Medellin, S. Medellin-Morales, restoration of Northwest bunchgrass prairie. insects. G.P. Nabhan, B. Pavlik, V. Tepedino, and S. Restoration Ecology 17:515-525. Walker. 1998. The potential consequences Kephart, S. 2006. Pollination mutualisms in Sandra (Sandy) DeBano is an Associate of pollinator declines on the conservation of the Caryophyllaceae. New Phytologist biodiversity and stability of food crop yields. Professor in the Department of Fisheries 169:667-680. Conservation Biology 12:8-17. and Wildlife at Oregon State University’s Kephart, S, R. Reynolds, M. Rutter, C. Fenster, Hermiston Agricultural Research and Feinsinger, P., K.G. Murray, S. Kinsman, and and M. Dudash. 2006. Pollination and seed W.H. Busby. 1986. Floral neighborhood Extension Center in northeastern Or- predation by moths on Silene and allied and pollination success in four humming- Caryophyllaceae: evaluating a model system egon. Sandy’s research interests focus on bird-pollinated cloud forest plant species. to study the evolution of mutualisms. New invertebrate-mediated ecosystem services Ecology 67:449-464. Phytologist 169:637-640. including pollination, food web provi- Feldman, T.S., W.F. Morris, and W.G. Wil- Kimoto, C., S.J. DeBano, R.W. Thorp, S. sioning, and decomposition. She works son. 2004. When can two plant species Rao, and W.P. Stephen. 2012a. Temporal primarily in grasslands, riparian areas, facilitate each other’s pollination? Oikos patterns of a native bee community in a and agroecosystems. 105:197-207. North American bunchgrass prairie. Journal Ghazoul, J. 2005. Pollen and seed dispersal of Insect Science 12:108. Available online Natalie Gonzalez received a B.S. in Biol- among dispersed plants. Biological Reviews
210 Natural Areas Journal Volume 34 (2), 2014 Lesica, P., and E. Crone. 2007. Causes and patterns of plant invasions. Perspectives in SYSTAT. 1997. SYSTAT 7.0 for Windows. consequences of prolonged dormancy for Plant Ecology, Evolution and Systematics SPSS Inc., Chicago. an iteroparous geophyte, Silene spaldingii. 7:137-158. Taylor, R.V., J. Dingeldein, and H. Schmalz. Journal of Ecology 95:1360-1369. Petit, S. 2011. Effects of mixed-species pollen 2012. Demography, phenology, and factors Lesica, P., and B. Heidel. 1996. Pollination biol- load on fruits, seeds, and seedlings of two influencing reproduction of the rare wild- ogy of Silene spaldingii. Montana Natural sympatric columnar cactus species. Ecologi- flower (Silene spaldingii) on the Zumwalt Heritage Program, Helena, MT. cal Research 26:461-469. Prairie. The Nature Conservancy, Northeast McCune, B., and J.B. Grace. 2002. Analysis Platt, W.J., G.R. Hill, and S. Clark. 1974. Seed Oregon Field Office, Enterprise, OR. of ecological communities. MjM Software, production in a prairie legume (Astragalus Taylor, R.V., V. Jansen, H. Schmalz, and J. Gleneden Beach, OR. canadensis L.): interactions between pol- Dingeldein. 2009. Mapping and monitoring lination, predispersal seed predation, and Spalding’s catchfly (Silene spaldingii) on McCune, B., and M.J. Mefford. 2006. PC-Ord, plant density. Oecologia 17:55-63. Multivariate analysis of ecological data, the Zumwalt Prairie Preserve, 2006-2008. Version 5.19. MjM Software, Gleneden Pleasants, J.M. 1980. Competition for bumble- The Nature Conservancy, Northeast Oregon bee pollinators in Rocky Mountain plant Beach, OR. Field Office, Enterprise, OR. communities. Ecology 61:1446-1459. Menz, M.H.M., R.D. Phillips, R. Winfree, C. Thomson, J.D. 1981. Spatial and temporal Rao, S., W.P. Stephen, C. Kimoto, and S.J. components of resource assessment by Kremen, M.A. Aizen, S.D. Johnson, and DeBano. 2011. The status of the ‘red-listed’ K.W. Dixon. 2011. Reconnecting plants flower-feeding insects. Journal of Animal Bombus occidentalis (Hymenoptera: Api- Ecology 50:49-59. and pollinators: challenges in the restoration formes) in northeastern Oregon. Northwest of pollination mutualisms. Trends in Plant Science 85: 64-67. Thorp, R.W., D.S. Horning, and L.L. Dunning. Science 16:4-12. 1983. Bumble bees and cuckoo bumble Rathcke, B. 1983. Competition and facilitation Mitchell, R.J., R.J. Flanagan, B.J. Brown, N.M. among plants for pollination. Pp. 305-329 in bees of California. University of California Waser, and J.D. Karron. 2009. New frontiers L. Real, ed., Pollination Biology. Academic Press, Berkeley. in competition for pollination. Annals of Press, New York. Tisdale, E.W. 1982. Grasslands of western North Botany 103:1403-1413. Root, R.B. 1973. Organization of a plant-ar- America: the Pacific Northwest Bunchgrass. Moeller, D.A. 2004. Facilitative interactions thropod association in simple and diverse Pp. 232-245 in A.C. Nicholson, A. McLean, among plants via shared pollinators. Ecol- habitats: the fauna of collards (Brassica and T.E. Baker, eds., Proceedings of the ogy 85:3289-3301. oleracea). Ecological Monographs 43:95- 1982 Grassland Ecology and Classification Symposium. British Columbia Ministry of Morales, C.L., and A. Traveset. 2009. A meta- 124. Forests, Victoria, BC. analysis of impacts of alien vs. native plants Schemske, D.W. 1981. Floral convergence and on pollinator visitation and reproductive suc- pollinator sharing in two bee-pollinated U.S. Fish and Wildlife Service. 2007. Recov- cess of co-flowering native plants. Ecology tropical herbs. Ecology 62:946-954. ery plan for Silene spaldingii (Spalding’s Catchfly). U.S. Fish and Wildlife Service, Letters 12:716-728. Sih, A., and M.-S. Baltus. 1987. Patch size, Portland, OR. [ODA] Oregon Department of Agriculture. pollinator behavior, and pollinator limitation 2011. Oregon Listed Plants. Accessed 14 in catnip. Ecology 68:1679-1690. Waser, N.M. 1978. Competition for humming- bird pollination and sequential flowering August 2011 from
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