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Variation among four populations of erysimum capitatum in phenotype, pollination and herbivory over an elevational gradient.

INTRODUCTION

Floral morphology, phenology, and floral resources can vary within species over distances as short as lm (reviewed in Linhart and Grant, 1996). Such patterns of geographic variation have frequently been related to physical features of the environment (Linhart and Grant, 1996), but communities of both pollinators and herbivores also may drive the evolutionary divergence of plant characteristics (e.g., Herrera, 1988; Gomez, 1993; Herrera, 1993; Gomez and Zamora, 2000; Haloin and Strauss, 2008; Gomez et al., 2009; Urban, 2011). Interactions between plants, their pollinators, and herbivores can be highly site- and time -specific (Thompson, 1988) resulting in different selection regimes (Rand, 2002; Bradley et al., 2003) and phenotypic divergence among sites. Comparisons among sites of plant phenotype, herbivory and pollinator community composition or behavior allow for investigation of local divergence.

Plants with generalized pollination systems have only rarely been studied in the context of local adaptation to particular communities of pollinators and herbivores (see Aigner, 2005; Gomez et al., 2007; Gomez et al., 2009). Local adaptation may be unlikely if generalized pollination morphology results from selection to maintain relationships with a diverse group of pollinators that are similar among sites (Waser et al., 1996; Dilley et al., 2000; Ellis and Johnson, 2009). Conversely, plants with generalized pollination systems may show population-level phenotypic divergence if pollinator communities are very different among sites. Consistent differences in the most common or effective pollinators could result in local adaptation. Moreover, herbivores, which also vary spatially and temporally, can affect pollinator choices (Adler, 2000) and result in adaptive tradeoffs or overwhelm the strength of selection by pollinators (Irwin and Adler, 2006; Gomez, 2008). Addressing conflicting predictions for local adaptation raised by these issues requires comparative study of multiple populations of plants likely to have different pollinators and herbivores.

Erysimum capitatum is an exceptional plant species in which to examine geographic variation in flower morphology, pollinators, and herbivores. E. capitatum plants are quite variable in morphology and life history characters across their broad geographic range and elevational distribution (Price, 1984). Individuals are visited by a wide array of pollinating insects, and reproductive tissues are attacked by a number of herbivores. Plant species such as E. capitatum that occupy montane regions may be particularly likely to show local differentiation because these areas are very heterogeneous over short distances in both microclimate and cooccurring species (reviewed in Lomolino, 2001). Elevational gradients have been associated with population differentiation in many species (Linhart and Grant, 1996).

We studied four montane populations of Erysimum capitatum for two growing seasons to determine whether a more detailed study of local selection was warranted and to answer the following questions: Is there differentiation in phenotype among populations? What are the common pollinators and herbivores of this relatively unstudied species? Do communities of pollinators and herbivores differ among populations?

METHODS

STUDY SPECIES

Erysimum capitatum (Brassicaceae) occurs throughout the United States (USDA, 2004) and northern Mexico (Turner, 2006). Its life history can differ among individuals and populations, but it is typically a biennial monocarp (Kim and Donohue, 2011). Flower color and other traits vary considerably throughout the species range (Price, 1984; Weber, 1990). Flowers range from yellow and white to red and lavender (Price, 1984). Although we assumed that all populations and individuals studied belonged to a single species, the great phenotypic variation seen E. capitatum may be the result of multiple hybridization events between subspecies and its taxonomy is currently undecided (Turner, 2006). Other plants in the genus Erysimum contain glucosinolates and cardiac glycosides (Renwick et al., 1989; Stadler et al., 1995) and though secondary chemistry has not been studied in E. capitatum, it most likely also contains these compounds.

POPULATIONS

We used four study populations located on the Eastern slope of the Rocky Mountains of Colorado. The Greenbelt Plateau population (GBT) grows at 1980 m (39[degrees]55'N 105[degrees]14'W) in a short grass prairie. The Walker Ranch population (WALK) is at 2209 m (39[degrees]56'N 105[degrees]20'W) in open lower montane Ponderosa pine forest. The population at Nederland (NED) is at 2590 m (39[degrees]58'N 105[degrees]30'W) in open lower montane Ponderosa pine forest. The Elk Meadow population (ELK) grows at 2900 m (40[degrees]01'N, 105[degrees]32'W) in a subalpine dry meadow at the University of Colorado Mountain Research station. Marr (1967) gives complete descriptions of these vegetation types. Flowering begins as early as Mar. and continues through early Jun. in GBT, the lowest elevation population. In the highest elevation population, ELK, flowering begins in late Jun. and continues through mid-Jul., and very few plants have open flowers through the fall. We assessed plant phenotype, herbivory, and pollinator visitation for 50-200 haphazardly selected flowering plants in each of these populations in 2005 and 2006.

PHENOTYPIC CHARACTERS

We measured corolla width at the widest point, corolla tube depth, corolla color, number of open flowers, height of tallest inflorescence, height to first flower on the tallest inflorescence, and stem diameter in 2005 and 2006 in ELK, NED, WAK and GBT.

For all populations, the sampling schemes differed slightly between 2005 and 2006. In 2005 we measured larger plants that were likely to have open flowers throughout the planned period of pollinator observations. In 2006 sample sizes were increased at all sites, necessitating the inclusion of smaller plants. Also, the timing of rainfall and flowering differed between years and may have resulted in differences in plant size. We therefore included height as a covariate in analyses of plant phenotype to control for differences in plant size between years that are unlikely to be meaningful to a description of consistent population-level differences.

We repeated measurements of the number of open flowers, corolla width, and corolla depth on up to 4 d, and/or on multiple flowers per day. We did not obtain equal repetitions of these measurements on all plants because some plants produced flowers for shorter times than others and weather precluded measurements on some days. In 2005 corolla width and depth were measured for three flowers per plant whenever possible. Preliminary analysis suggested that the measurement of corolla width and depth for one flower per plant was sufficient, so in 2006, we measured only one flower per plant at the beginning of the study period or of flowering for an individual plant. Because of differences in the numbers of measurements per plant, measurements for phenotypic characters were collapsed as follows. The average of all measurements was used in analysis of characters for which intraplant differences or measurement error were likely the biggest contributors to variation (corolla width, corolla depth, corolla color). The maximum value was used in the analysis of characters for which measurements were most likely to vary with growth (inflorescence height, height to first flower, number of open flowers, and stem diameter).

Corolla color was quantified in the field by comparing flowers to color chips (Behr paint chips of colors yellow S-G-390 to red S-G-230). The accuracy of this method was confirmed for a subset of plants using digital photographs and standardized RGB color values. Flowers of some plants were old or otherwise deteriorated on days that color was measured, and these plants were not measured. Corolla width and depth of flowers that retained at least three petals were measured with calipers. Corolla width was measured at the widest point of the corolla as seen from the front, and corolla depth was measured from the base of the calyx to the angle between the claw and the limb of a petal. Flowers were considered "open" if they retained at least three or more attached claws of petals. Inflorescence height and the height to the first flower were measured from the ground on the tallest inflorescence. Stem diameter was measured on the tallest inflorescence 30mm above the ground.

Significant phenotypic differences among plants from different sites were evaluated using nested two-way multivariate analysis of covariance (MANCOVA) with height as a covariate for size-related characters (all characters but color). This analysis was followed with univariate two-way analysis of covariance (ANCOVA) for each size-related character. Correlation analysis (proc CORR, SAS 2003) showed that color was not related to size or other characters so it was analyzed separately with a two-way ANOVA. In both analyses, site was nested in year. Inflorescence height of the tallest inflorescence was included as a covariate for characters correlated to it to control for differences between years in plant size that may have been caused by differences in rainfall or sample selection. Including inflorescence height as a covariate rather than as a dependent phenotypic variable also allowed us to test whether the effect of plant size on a given character is the same in all populations. These data were also used in a study of selection by pollinators and herbivores (Lay et al., 2011) but are presented here to provide evidence of differences among populations that precipitated that study.

POLLINATION AND INSECT VISITATION

To observe insect visitation and pollinator community composition, observers watched groups of one to ten plants for 10 min periods during peak visitation times. Each plant was observed for two periods per day on as many days as possible given weather and flowering times of plants. Observers avoided disturbing visitors by minimizing their own shadows on plants, remaining a meter from the closest plant observed. We distinguished between visitors that contacted reproductive parts and those that did not. We grouped likely pollinators (those that contacted reproductive parts) into functional groups based on size and taxonomic order, and observers identified visitors to these functional groups. Preliminary observations showed collections could influence visitation, so we collected samples of insects that were found visiting plants for identification only after observations were completed in each site. Sampling effort differed among sites and years due to differences in flowering times. Data from observation of visitors were also used in a study of selection by pollinators and herbivores (Lay et al., 2011).

In order to determine the level of similarity in pollinator visitation among populations, we calculated Morisita-Horn similarity indices in EstimateS (Colwell, 2005), using pooled pollinator functional group counts from each population. This index is robust to differences in sampling effort but is strongly affected by the most common visitor (Magurran, 2004). Differences in sample size between years were large (with as few as seven observed pollinators in one population in one year). The unequal sample sizes greatly reduced statistical power for analysis of similarity (ANOSIM), a standard nonparametric test for community differences. Therefore, we instead pooled pollinator counts from both years and show only qualitative Morista-Horn similarity indices.

HERBIVORY

Three types of herbivore damage were common on flowers of Erysimum capitatum: petal damage, flower bud galls, and nectar robbing. Multiple herbivores created visually similar petal damage and therefore we could not test for site differences in petal herbivore assemblages.

Damage levels were recorded for each damaged flower on a plant. Damage to broad surfaces of petals (petal limbs) was scored 1 to 4, while 5 indicated complete destruction of anthers and stigma. "1" corresponded to 10% damage or less, "2" to damage between 10% and 25%, "3" to 25-50%, "4" to 50% to damage of all petal limbs. We summed all scores from each plant on each day for a measure of overall damage, and used the maximum value of summed petal damage as the dependent variable in an analysis of covariance (ANCOVA) with site nested in year as main effects and the total number of flowers on the day of maximum petal damage as a covariate. This analysis was performed with aov from the stats package in R (R Development Core Team, 2010).

Gall midge larvae (Cecidomyiidae) form galls from flower buds. Flower bud galls usually fail to open and are identifiable by their swollen calyces. We counted flower bud galls on each plant on each observation day. We then square-root transformed the maximum count for galls found on a single day over the observation period to improve normality. This transformed gall count was the dependent variable in an analysis of covariance (ANCOVA) in which site was nested in year as main effects and height, a good predictor of the total number of available buds, was a covariate. This analysis was performed using the aov function of the stats package in R (R Development Core Team, 2010).

Finally, ants are frequent visitors to flowers. They remove nectar from between the free sepals but rarely contact reproductive parts. We noted ant visitation during pollinator observations and counted ants present on plants directly after pollinator observation periods but performed no statistical analyses of ant visitation.

RESULTS

PLANT SIZE

Size-related characters differed among sites, although there were no consistent patterns related to elevation (Table 1). Inflorescence height varied with site ([F.sub.3,913]) = 49.62, P < 0.0001, Table 1), and plants were significantly shorter in 2006 than in 2005 in all sites ([F.sub.4,913) = 189.20, P < 0.001). When controlling for inflorescence height ([F.sub.(1,799)] = 566.17, P < 0.0001), stem diameter differed among sites ([F.sub.(3,799)] = 6.9, P = 0.003, Table 1), but not between years ([F.sub.(4,799)] = 1.37, P = 0.23). In addition there was a significant interaction between site and inflorescence height, indicating that the relationship between inflorescence height and stem diameter differed among populations ([F.sub.(3,799)] = 15.95, P < 0.0001). Height to first flower differed among sites ([F.sub.(5.799)] = 6.59, P < 0.001) and between years ([F.sub.(4,799)] = 2.92, P < 0.05) even controlling for the large effect of inflorescence height ([F.sub.(1,799)] = 863.65, P < 0.0001). Inflorescences of the same height in different sites had different heights to the first flower ([F.sub.(3,799)] = 16.56, P < 0.0001).

FLOWER CHARACTERS

Flower characters differed among sites and between years (Table 1). Corolla color varied greatly with site with higher sites having redder corollas and lower ones having yellower corollas ([F.sub.3,514]) = 42.01, P < 0.0001, Table 1) but did not differ between years ([F.sub.1,514]) = 0.09, P = 0.75). Both corolla width and depth varied with inflorescence height ([F.sub.FW](1,799) = 151.89, [P.sub.FW] < 0.0001; [F.sub.FD(1,799)] = 132.31, [P.sub.FD] < 0.0001). Corolla width varied among sites (F.sub.3,799) = 10.85, P < 0.0001) and between years ([F.sub.(4,799)] = 5.45, P = 0.04) when controlling for the relationship with inflorescence height. Also, there was a significant interaction between inflorescence height and site meaning that relationship between inflorescence height and corolla width differed among sites ([F.sub.3,799]) = 8.15, P < 0.0001). Corolla depth did not differ among sites ([F.sub.(3,799)] = 0.71 P = 0.55), though there was a significant interaction between site and inflorescence height ([F.sub.3,799]) = 4.17, P < 0.01). Corolla depth also differed between years within sites ([F.sub.(4,799)] = 5.01, P = 0.02). Corolla width and depth were correlated in all sites and years even when the effect of inflorescence height on flower size was removed (r = 0.6, P < 0.001).

Correlations among size-related characters were not constant among sites (Wilk's lambda = 0.90, P < 0.0001) or between years (Wilk's lambda = 0.86, P < 0.001) and varied with plant height (Wilk's lambda = 0.34, P < 0.0001).

POLLINATOR COMMUNITY COMPOSITION

We considered visitors to be pollinators if they came into contact with the reproductive parts of a flower. Pollinators in the studied populations were assigned to functional groups that included large bees, medium bees, small bees, flies, bee-flies, butterflies, and moths (Table 2). "Large bees" include bees over 2 cm in body length (Table 2). "Medium" bees include bees with body lengths between 1 and 2 cm (Table 2). "Small bees" include bees under 1 cm in body length (Table 2). "Flies" included flies that were above 0.25 cm in body length (Table 2). Smaller flies rarely contacted reproductive parts and were nearly impossible to see during observations. Pollen beeries (Meligethes sp., Nitidulidae) interact differently with flowers than other beetles; they enter corolla tubes, are coated in pollen, and spend long periods of time in flowers. Therefore, we treated them as a separate functional group and grouped the small number of other beetle visitors that contacted reproductive parts together (Table 2). These included beetles of the families Coccinellidae and Buprestidae, as well as other unidentified beeries. All bees and pollen beetles were visibly coated in pollen after visiting flowers (Table 2).

Populations had qualitatively different pollinator community compositions, with GBT and ELK being the most different (Table 3). The most similar pollinator communities were at NED and WAK (Table 3). Flies were more common at ELK, and pollen beetles and bees were more common at GBT (Fig. 1).

HERBIVORY

Petal herbivores included grasshoppers, lepidopteran larvae, and nitidulid beetle larvae that lived inside of flowers (most frequently observed). Megachilid bees were never observed, but the rounded edge wounds that are characteristic of these bees occurred frequently. We were unable to rear any of the larvae to maturity, and they are yet to be identified.

On average plants received about 10% damage to their corolla limbs for each flower, though there was a good deal of variation in damage to individual flowers. On any given plant, roughly 30% of flowers were damaged. Levels of petal damage did not differ among sites (Fig. 2A [F.sub.3,780]) = 1.90, P = 0.19). Because there was a significant interaction between the number of flowers and site ([F.sub.1,780]) = 5.38, P = 0.001), there was a difference among sites in the relationship between flowers and petal herbivory. There was no overall difference between years in petal damage ([F.sub.1,780]) = 2.80, P = 0.09). However, there was a significant interaction between year and site [F.sub.3,780] = 3.81, P = 0.01).

Galls were formed by gall midges (Cecidomyiidae). The incidence of galls ranged from 2% of 50 plants at WAK in 2005 to 50% of 197 plants at WAK in 2006. Numbers of galls averaged between 1 and 5 per plant in all sites. Gall number did not vary greatly among sites (Fig. 2B, [F.sub.3,874] = 2.32 P = 0.07) but was greater in 2006 than in 2005 [F.sub.1,874] = 27.66, P < 0.0001) and there was an interaction between site and year [F.sub.3,874] = 17.69, P < 0.0001). The effect of inflorescence height on gall number was large [F.sub.1,874] = 16.06, P < 0.0001), likely because taller plants have more buds to attack. There was no significant interaction between the effect of inflorescence height and site on gall number [F.sub.3,874] = 1.9, P = 0.13), suggesting that plants in different sites of the same height receive similar numbers of galls.

Ants removed nectar from flowers and occasionally attacked bees. Unlike many ant nectarrobbing systems, ants do not damage flower parts of Erysimum capitatum, but remove nectar from openings between sepals. Ants comprised 39% of all insect visitors (192 of 492) at GBT, 50% at WAK (298 of 596), 57% at NED (299 of 525) and 62% (443 of 715) at the ELK.

OTHER ARTHROPODS OBSERVED ON INFLORESCENCES

A number of arthropods that did not contact reproductive parts or visibly remove nectar were observed on inflorescences during observation periods. These included crab spiders, hemipterans, homopterans, and ladybird beetles. In WAKstem boring beetle larvae clipped entire infiorescences. A discussion of this strong effect can be found in Lay et al. (2011).

DISCUSSION

PHENOTYPIC DIFFERENTIATION

Populations of Erysimum capitatum in this study region differed in phenotype and pollinator community composition and levels of herbivory changed from year to year. The traits that varied among the study populations may affect pollinator and herbivore preferences. In particular, corolla color (Table 1), varied from yellow to red among populations, with higher-elevation populations having redder corollas and lower-elevation populations having yellower ones. Corolla color is known to affect pollinator choice, and color variation is associated with variation in pollinator types (reviewed in Willmer, 2011). In addition variation in flower color is linked to variation in secondary metabolites, some of which, like anthocyanins, can deter feeding by insects (Fineblum and Rausher, 1997; Irwin et al., 2003; Strauss et al., 2004). Flower color may be selected upon independently of other traits and has the potential to be selected by both pollinators and herbivores because it is tied to both attractiveness and plant secondary chemistry (Frey, 2004; Strauss et al., 2004). GBT, at the lowest elevation, and ELK, at the highest elevation, were the most different from one another in flower color and also were most divergent in pollinator community composition (Table 1, Fig. 1) and ant visitation. Further work on this dataset (Lay, et al., 2011) showed that color affected visitation in some years.

Height was a good indicator of plant size as taller inflorescences bore more flowers, and flowers on these inflorescences tended to be larger. However, both flower size and number varied among populations in ways that were similar between years (Table 1). The relationship of flower size with height and flower number suggests that flower size is somewhat plastic, as characters related to plant size often are (Frazee and Marquis, 1994; Conner and Sterling, 1996). Corolla width and depth were correlated in all populations and years, which suggests that the shape of flowers may be less variable than their size. Increased flower size and number can increase pollinator visitation, but this effect may differ between types of pollinators (Conner and Rush, 1996).

COMMON POLLINATORS AND POLLINATOR COMMUNITY DIFFERENCES

At the four sites studied, Erysimum capitatum has a generalized pollination system. It is visited by a wide variety of insects that come into contact with reproductive parts, and eight of the nine functional groups identified contain multiple species. Whether most pollination systems are generalized or specialized is still debated (Waser et al., 1996; Johnson and Steiner, 2000; Vazquez et al., 2009) but studies that examine plants in different populations and in the same population over time find that multiple insects act as pollinators to some extent (Herrera, 1988; Brunet, 2009), and other brassicaceous species have been found to have generalized pollination systems (Gomez and Zamora, 1999; Gomez et al., 2009). Generalized pollination has been proposed as a likely outcome of pollinator communities that vary in time and space (Waser et al., 1996; Dilley et al., 2000; Ellis and Johnson, 2009). However, generalized pollination can select for divergent floral morphologies when populations have somewhat different pollinator community compositions, or when pollinator behavior differs among populations (Dilley et al., 2000). Differences in pollinator community composition among populations suggest that divergence as a result of differing pollinator preferences or effectiveness is a possibility in Erysimum capitatum.

Pollinator community composition differed qualitatively among sites (Table 3, Fig. 1). Flies are more common visitors at high-elevation sites, and bees and pollen beetles are more common visitors at low-elevation sites. Although it was not possible to test differences quantitatively because of limited sample size in some sites and some years, the differences in pollinator community are consistent with the results of other studies. For example Kearns (1992) found that in the Rocky Mountains flies are more frequent visitors than bees at higher montane elevations, and flies are frequently found to be common visitors in high elevation sites in other mountain ranges, as well (Arroyo et al., 1982; Elberling and Olesen, 1999; Devoto et al., 2005). The frequency of pollen beetle visits differed greatly among populations (Fig. 1), but this difference may reflect a behavioral difference between high and low elevation beetle populations; beetles are often hidden inside of corolla tubes and hard to observe. Their increased frequency at lower elevations may reflect higher rates of movement from corolla tubes rather than higher abundance. Such differences are possible in other functional groups as well but may be more pronounced in these beetles.

Similarities in communities of pollinating visitors are related to elevation with bees decreasing and flies increasing as a proportion of the total pollinators (Table 3, Fig. 1). However, other than corolla color, trait differences among populations did not appear to be associated with elevation (Table 1). The lack of congruence in variation between plant traits and pollinator types suggests that pollinator communities are not shaping flower size or number in these populations and raises the possibility that other selective agents, possibly herbivores, are more likely to be driving selection for flower number and size than pollinator communities.

HERBIVORY AND OTHER FLOWER VISITORS

Ants were not considered to be part of the pollinator community in analyses of community similarity. Nonetheless, they varied as a proportion of the total number of visitors from site to site, increasing as a proportion of the total visitors in higher elevation sites. They were the most frequent visitors to inflorescences in all populations and removed visible nectar quickly in the morning before other visitors were active. This may not affect pollinator preferences: most bees collect pollen rather than nectar from flowers, and most flies did not appear to be collecting nectar during visits as they neither entered corrolla tubes nor approached flowers from the back. Although nectar removal by ants may not affect attractiveness to other visitors, other ant behavior may. In ELK and NED, aggressive ants were observed attacking approaching bees on several occasions. Bees and ants were only observed on the same plant on a few occassions, so the frequency of this behavior is unknown.

For other taxa where ants constitute the most common or constant visitors, and where plants produce dense flowers low to the ground, ants may be effective pollinators (Gomez, 2000; Ashman and King, 2005). Ants can kill pollen with chemical secretions on their bodies (Beattie et al., 1985), however, viability tests of Erysimum capitatum pollen suggest that it may be less susceptible than pollen of other plants (Claire Lay, pets. obs.). This may be of little importance, as ants only rarely contacted reproductive parts, but they are such frequent visitors that they may perform some pollination service. In addition to possible effects as pollinators, ants may benefit plants by deterring some herbivores, though such interactions were never observed in the field.

The incidence of galls differed among yearsbut was not different among sites. Within each year, height was a significant predictor of the number of galls, perhaps because height is related to the number of flowers produced (i.e., sites for galls). However, the number of galls changed in proportion to plant size between years, as all populations had shorter plants in 2006, but equivalent or greater numbers of galls per plant. Although the effects of nonpollinating gall forming insects that interact with flowers have been studied in fig-fig wasp mutualisms (e.g., Kerdelhue and Rasplus, 1996; Wang et al., 2010), the effects of flower bud galls on pollination in other systems are relatively unstudied. These galls have the potential to both affect fitness directly, through decreased ovules for fertilization, and indirectly, through reduced pollinator attractiveness.

Unlike galls, which are formed by gall midges (Cecidomyiidae), petal damage is caused by a wide variety of insects. Beetle larvae (Nitidulidae), which spend most of their time in flowers, are common sources of damage. However, other insects, including megachilid bees, lepidopteran larvae, and grasshoppers damage petals of Erysimum capitatum. The types of damage caused by all of the herbivores that feed on petals are difficult to distinguish, and petal damage thus reflects the preference and abundance of a number of insects. In general the study populations had relatively equal amounts of petal damage. Because the insects responsible for damaging petals were rarely observed, differences among populations in assemblages of petal-feeding herbivores could not be evaluated.

With the exception of an increase in ant visits as a proportion of total visits, herbivory on flowers differed more between years than among populations. Several types of herbivory are likely to have significant impacts on plant fitness. Galls prevent flowers from opening and setting fruit, so investment in those flowers is lost, and reduced floral display size could have impacts on the attractiveness of plants to pollinators. Petal herbivores and ants may impact fitness directly through loss of resources and indirectly through reduction in pollinators (Burkle et al., 2007; McCall, 2010).

CONCLUSIONS

Populations of Erysimum capitatum in this study region differed in phenotype and pollinator community composition. Populations experienced different incidences of galling insects in different years, and the relative frequency of ant visitors increased with elevation, but otherwise, differences in herbivory were more apparent between years than among populations. Trait differences other than color were patchy, rather than continuous with elevation. It is possible that differences among populations in pollinator visitation and temporal differences in herbivory have acted to cause differentiation in plant traits, although these differences could also be explained by hybridization, genetic drift, or adaptation to abiotic factors.

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SUBMITTED 23 MARCh 2012 ACCEPTED 6 SEPTEMBER 2012

LAY, C. R, (1) LINHART, Y. B. AND DIGGLE, P. K (2)

Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, 80309 USA

(1) Email: Claire.Lay@colorado.edu

(2) Email: Pamela.Diggle@colorado.edu


TABLE 1.--Means [+ or -] SE for phenotypic values in each population.
Means for each year are below  dotted line. Different superscripts
indicate population means (bold) that are different by Tukey's HSD
and traits that differed between years are marked with asterisks.
Sample size (n) for each trait and site  differed for traits due to
availability of flowers. Larger numbers indicate yellower color and
smaller ones  indicate redder color. Populations are ordered from low
to high elevation: GBT (1980 m), WAK  (2209 m), NED (2590 m), and ELK
(2900 m)

            Inflorescence height (mm) *  Height of first flower (mm) *

GBT         185.1 [+ or -] 4.7c n = 141  135.2 [+ or -] 3.0c n = 141
NED         241.2 [+ or -] 5.1a n = 245  197.8 [+ or -] 4.9a n = 235
WAK         163.0 [+ or -] 4.Od n = 244  131.2 [+ or -] 3.7c n = 243
ELK         207.7 [+ or -] 4.7b n = 283  176.3 [+ or -] 4.5b n = 272
GBT2005     242.8 [+ or -] 12.1 n = 43   151.5 [+ or -] 5.4 n = 43
GBT2006     159.8 [+ or -] 4.5 n = 98    128.0 [+ or -] 5.4 n = 98
WAK2005     211.9 [+ or -] 11.1 n = 54   156.9 [+ or -] 9.7 n = 54
WAK2006     149.3 [+ or -] 4.1 n = 192   123.9 [+ or -] 4.0 n = 189
NED2005     322.7 [+ or -] 10.4 n = 98   259.3 [+ or -] 11.7 n = 89
NED2006     186.8 [+ or -] 5.2 n = 147   160.3 [+ or -] 4.6 n = 146
ELK 2005    226.0 [+ or -] 9.1 n = 98    183.2 [+ or -] 7.3 n = 87
ELK 2006    198.1 [+ or -] 5.3 n = 185   173.0 [+ or -] 7.3 n = 185

            Stem diameter (mm)           Corolla color

GBT         2.3 [+ or -] O.1a n = 141    370.0 [+ or -] 4.7a n = 80
NED         2.1 [+ or -] O.1a n = 254    352.1 [+ or -] 1.2b n = 116
WAK         1.8 [+ or -] <O.1c n = 282   350.2 [+ or -] 2.2b n = 135
ELK         1.9 [+ or -] <O.1b n = 273   322.4 [+ or -] 1.8c n = 190
GBT2005     2.9 [+ or -] 0.2 n = 41      368.2 [+ or -] 2.4 n = 41
GBT2006     2.1 [+ or -] 0.1 n = 99      370.0 [+ or -] 4.5 n = 39
WAK2005     2.0 [+ or -] 0.1 n = 91      350.5 [+ or -] 2.6 n = 48
WAK2006     1.7 [+ or -] <0.1 n = 191    350.0 [+ or -] 3.3 n = 87
NED2005     2.7 [+ or -] 0.8 n = 97      354.9 [+ or -] 1.9 n = 81
NED2006     1.8 [+ or -] <0.1 n = 157    345.6 [+ or -] 2.3 n = 35
ELK 2005    2.0 [+ or -] 0.1 n = 87      320.7 [+ or -] 4.0 n = 76
ELK 2006    1.9 [+ or -] 0.1 n = 186     323.6 [+ or -] 2.3 n = 114

            Open flowers *              Corolla width (mm) *

GBT         9.6 [+ or -] 0.6a n = 141   15.1 [+ or -] 0.2b n = 135
NED         6.9 [+ or -] 0.56 n = 238   15.8 [+ or -] 0.2a n = 207
WAK         5.4 [+ or -] 0.3 n = 254    14.2 [+ or -] 0.1 n = 254
ELK         5.3 [+ or -] 0.4c n = 280   15.1 [+ or -] 0.26 n = 263
GBT2005     14.3 [+ or -] 2.2 n = 43    15.6 [+ or -] 0.41 n = 41
GBT2006     7.6 [+ or -] 0.3 n = 99     14.8 [+ or -] 0.2 n = 94
WAK2005     8.1 [+ or -] 0.2 n = 54     16.0 [+ or -] 0.2 n = 93
WAK2006     4.7 [+ or -] 0.3 n = 197    13.2 [+ or -] 0.2 n = 161
NED2005     11.2 [+ or -] 1.4 n = 98    17.9 [+ or -] 0.2 n = 84
NED2006     3.9 [+ or -] 0.6 n = 140    14.5 [+ or -] 2.6 n = 127
ELK 2005    6.3 [+ or -] 0.4 n = 90     14.8 [+ or -] 0.4 n = 80
ELK 2006    4.9 [+ or -] 0.3 n = 190    15.2 [+ or -] 0.4 n = 183

            Corolla depth (mm) *

GBT         10.6 [+ or -] 1.1 n = 135
NED         10.2 [+ or -] 0.1 n = 208
WAK         9.9 [+ or -] 0.1 n = 255
ELK         11.0 [+ or -] 0.1 n = 263
GBT2005     11.2 [+ or -] 0.2 n = 41
GBT2006     10.3i [+ or -] 1.8 n = 94
WAK2005     11.2 [+ or -] 0.2 n = 93
WAK2006     9.1 [+ or -] 0.2 n = 162
NED2005     11.4 [+ or -] 0.1 n = 84
NED2006     9.5 [+ or -] 1.8 n = 128
ELK 2005    10.9 [+ or -] 0.3 n = 80
ELK 2006    11.0 [+ or -] 0.3 n = 183

TABLE 2.--List of adult insects collected after pollinator
observations had concluded at each site.  Some unidentified
samples were lost when a freezer malfunctioned, so this list
is not comprehensive

Site       Order          Family               ID

GBT     Coleoptera     Unidentified   Coleoptera a.
GBT     Diptera        Canopidae      Zodion fulvifrons (Say)
GBT     Hemiptera      Rhopalidae     Rhopalidae sp.
GBT     Hymenoptera    Formicidae     Forelius foetidus
GBT     Hymenoptera    Formicidae     Tapinoma sessile
GBT     Hymenoptera    Halictidae     Andrenidae sp e.
GBT     Hymenoptera    Halictidae     Lasioglossum evylaeus
GBT     Lepidoptera    Unidentified   Lepidoptera a.
GBT     Hymenoptera    Halictidae     Halictus rubicundus
WAK     Coleoptera     Coccinellidae  Coccinellidae sp.
WAK     Coleoptera     Curculionidae  Curculionidae sp.
WAK     Coleoptera     Unidentified   Coleoptera b.
WAK     Diptera        Empididae      Empis sp.
WAK     Diptera        Muscidae       Drymeia sp.
WAK     Hemiptera      Cicadellidae   Cicadellidae sp.
WAK     Hemiptera      Lygaeidae      Lygaeus kalmii
WAK     Hymenoptera    Formicidae     Tapinoma sessile
WAK     Hymenoptera    Andrenidae     Andrenidae sp.
WAK     Hymenoptera    Halictidae     Halictus sp. c.
WAK     Hymenoptera    Halictidae     Lasioglossum sp a
WAK     Hymenoptera    Halictidae     Lasioglossum sp. b.
WAK     Lepidoptera    Unidentified   Lepidoptera b.
NED     Coleoptera     Coccinellidae  Coccinellidae
NED     Coleoptera     Nitidulidae    Meligethes sp.
NED     Coleoptera     Unidentified   Coleoptera c.
NED     Diptera        Chironomidae   Chironomidae
NED     Hemiptera      Cicadellidae   Cicadellidae
NED     Hemiptera      Cicadellidae   Cicadellidae
NED     Hemiptera      Lygaeidae      Lygaeus kalmii
NED     Hymenoptera    Formicidae     Formica argentea
NED     Hymenoptera    Formicidae     Formica obscuriventris elivia
NED     Hymenoptera    Formicidae     Lasius niger
NED     Hymenoptera    Formicidae     Tapinoma sessile
NED     Hymenoptera    Formicidae     Temnothorax rugatulus
NED     Hymenoptera    Formicidae     Temnothorax sessile
NED     Hymenoptera    Halictidae     Lasioglossum sp. c.
NED     Hymenoptera    Unidentified   Unidentified (tiny wasp)
ELK     Coleoptera     Coccinellidae  Coccinellidae sp.
ELK     Coleoptera     Nitidulidae    Meligethes sp.
ELK     Coleoptera     Unidentified   Unidentified a
ELK     Coleoptera     Unidentified   Unidentified b.
ELK     Coleoptera     Unidentified   Unidentified c.
ELK     Diptera        Diptera        Diptera sp.
ELK     Diptera        Muscidae       Muscidae sp. A
ELK     Diptera        Muscidae       Muscidae sp. B
ELK     Diptera        Muscidae       Muscidae sp. C
ELK     Diptera        Muscidae       Muscidae sp. D
ELK     Diptera        Muscidae       Thricops sp.
ELK     Diptera        Syrphidae      Sphaerophoria contigua
                                      (Macquart)
ELK     Hemiptera      Aphididae      Aphididae sp.
ELK     Hemiptera      Cicadellidae   Cicadellidae sp. A
ELK     Hemiptera      Cicadellidae   Cicadellidae sp. B
ELK     Hemiptera      Cicadellidae   Cicadellidae sp. c
ELK     Hemiptera      Lygaeidae      Lygaeus kalmii
ELK     Hemiptera      Miridae        Miridae sp.
ELK     Hemiptera      Rhopalidae     Rhopalidae sp.
ELK     Hymenoptera    Chrysididae    Chrysididae
ELK     Hymenoptera    Formicidae     Formica argentea
ELK     Hymenoptera    Formicidae     Tapinoma sessile
ELK     Hymenoptera    Formicidae     Tetramorium hispidum
ELK     Hymenoptera    Halictidae     Andrenidae sp. a
ELK     Hymenoptera    Halictidae     Andrenidae sp. c
ELK     Hymenoptera    Halictidae     Andrenidae sp. d
ELK     Hymenoptera    Halictidae     Andrenidae sp. f
ELK     Hymenoptera    Halictidae     Bombus favifrons
ELK     Hymenoptera    Halictidae     Bombus mixtus
ELK     Hymenoptera    Megachilidae   Celioxys
ELK     Hymenoptera    Halictidae     Colletes
ELK     Hymenoptera    Halictidae     Duforea maura
ELK     Hymenoptera    Halictidae     Halictus sp. a.
ELK     Hymenoptera    Halictidae     Hoplitus fulgida
ELK     Hymenoptera    Halictidae     Hylaeus basalis
ELK     Hymenoptera    Halictidae     Lasioglossum sp. a.
ELK     Hymenoptera    Halictidae     Lasioglossum sp. e
ELK     Hymenoptera    Halictidae     Osmia sp.
ELK     Hymenoptera    Unidentified   Unidentified (large wasp)
ELK     Hymenoptera    Unidentified   Unidentified (large wasp)
ELK     Hymenoptera    Unidentified   Unidentified (tiny wasp)
ELK     Hymenoptera    Unidentified   Unidentified (tiny wasp)

Site    Count   Functional group

GBT       1            --
GBT       1     Fly
GBT       2            --
GBT       6     Ant
GBT      10     Ant
GBT       1     Ant
GBT       1     Ant
GBT       1     Lepidoptera
GBT       1     Medium Bee
WAK       1     Other Beetles
WAK       1     Other Beetles
WAK       1     Other Beetles
WAK       1     Fly
WAK       1     Fly
WAK       1            --
WAK       2            --
WAK       9     Ant
WAK       1     Medium Bee
WAK       1     Medium Bee
WAK       1     Small Bee
WAK       1     Small Bee
WAK       1     Lepidoptera
NED       1     Other Beetles
NED       7     Nitidulidae
NED       1     Other Beetles
NED       1     Fly
NED       2            --
NED       1            --
NED       3     Ant
NED       4     Ant
NED       5     Ant
NED       3     Ant
NED       4     Ant
NED       1     Ant
NED       1     Ant
NED       1     Small Bee
NED       1            --
ELK       1            --
ELK      11     Nitidulidae
ELK       1     Other Beetles
ELK       1     Other Beetles
ELK       1     Other Beetles
ELK       1     Fly
ELK       1     Fly
ELK       1     Fly
ELK       1     Fly
ELK       1     Fly
ELK       1     Fly
ELK       1     Fly
ELK       1            --
ELK       1            --
ELK       1            --
ELK       2            --
ELK       4            --
ELK       1            --
ELK       1            --
ELK       1     Medium Bee
ELK       3     Ant
ELK       2     Ant
ELK       3     Ant
ELK       1     Small Bee
ELK       1     Small Bee
ELK       1     Small Bee
ELK       1     Small Bee
ELK       1     Large Bee
ELK       1     Large Bee
ELK       1     Medium Bee
ELK       1     Small Bee
ELK       1     Medium Bee
ELK       1     Small Bee
ELK       1     Medium Bee
ELK       1     Medium Bee
ELK       1     Small Bee
ELK       1     Small Bee
ELK       1     Medium Bee
ELK       1            --
ELK       1            --
ELK       1            --
ELK       1            --

TABLE 3.--Morisita-Horn similarity indices for pollinating visitor
functional groups in pairs of  populations. "1" indicates complete
similarity. The least similar populations are GBT and the ELK

Site comparison

GBT and WAK      0.72
GBT and NED      0.75
GBT and ELK      0.52
WAK and NED      0.85
WAK and ELK      0.83
NED and FIX      0.85
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Author:Lay, C.R.; Linhart, Y.B.; Diggle, P.K.
Publication:The American Midland Naturalist
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Geographic Code:1U8CO
Date:Apr 1, 2013
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