DOI: 10.5061/dryad.6q573n61q
title: Climate driven disruption of transitional alpine bumble bee communities

description: Pollinators at high elevations face multiple threats from climate change
 including heat stress, failure to phenological match advancing flower
 resources and competitive pressure from range-expanding species of lower
 elevations. We conducted long-term multi-site surveys of alpine bumble
 bees to determine how phenology of range-stable and range-expanding
 species is responding to climate change. We ask whether bumble bee
 responses generate mismatches with floral resources, and whether these
 mismatches in turn promote community disruption and potential species
 replacement. In alpine environments of the central Rocky Mountains,
 range-stable and range-expanding bumble bees exhibit phenological
 mismatches with flowering host plants due to earlier flowering of
 preferred resources under warmer spring temperatures. However, workers of
 range-stable species are more canalised in their foraging schedules,
 exploiting a relatively narrow portion of the flowering season.
 Specifically, range-stable species show less variance in phenology in
 response to temporally and spatially changing conditions than
 range-expanding ones. Because flowering duration drives the seasonal
 abundance of floral resources at the landscape scale, we hypothesize that
 canalisation of phenology in alpine bumble bees could reduce their access
 to earlier or later season flowers. Warmer conditions are decreasing
 abundances of range-stable alpine bumble bees above the timberline,
 increasing abundance of range-expanding species, and facilitating a novel
 and more species-diverse bumble bee community. However, this trend is not
 explained by greater phenological mismatch of range-stable bees. Results
 suggest that conversion of historic habitats for cold-adapted alpine
 bumble bee species into refugia for more heat-tolerant congeners is
 disrupting bumble bee communities at high elevations, though the precise
 mechanisms accounting for these changes are not yet known. If warming
 continues, we predict that the transient increase in diversity due to
 colonization by historically low-elevation species will likely give way to
 declines of alpine bumble bees in the central Rocky Mountains.
description: <strong>Study system</strong> In
 our alpine (above treeline) study sites (Colorado, USA), we classified
 bumble bees as resident or range-stable if pre-1980 records showed them
 completing their entire life cycle above timberline (<em>B.
 kirbiellus</em> and <em>B. lapponicus</em>
 <em>sylvicola</em>, formerly <em>B.</em>
 <em>balteatus </em>and <em>B. sylvicola</em>,
 respectively; Byron, 1980). Observations of <em>B.
 lapponicus</em> likely included the recently discovered cryptic
 taxon “incognitus” as it overlaps in distribution and is morphologically
 indistinguishable (Christmas et al., 2021). Species were deemed colonizing
 or range-expanding if populations before 1980 were commonly found in lower
 subalpine and montane habitats and nesting was not observed above treeline
 (<em>B. bifarius, B. flavifrons,</em> <em>B. frigidus,
 B. melanopygus, B. mixtus,</em> and <em>B.
 nevadensis</em>; Byron, 1980; Macior, 1974). Flowering phenology and
 floral density were monitored for nine plant species that together
 accounted for ~ 90% of floral resources used historically by alpine bumble
 bees: <em>Trifolium dasyphyllum, T. parryi</em> and
 <em>T. nanum</em>, P<em>enstemon whippleanus,
 Pedicularis groenlandica, Castilleja occidentalis, Mertensia lanceolata,
 Polemonium viscosum</em>, and <em>Rhodiola
 rhodantha</em> (Byron, 1980; Macior, 1974; Miller-Struttmann et al.,
 2015).  Floral resources were surveyed as part of a
 long-term phenological study (13 yrs. between 1977 and 2019; Table 1) on
 Pennsylvania Mountain, Colorado (39°15.803′N, 106°8.564′W; 3600-3970 m).
 Timing and abundances of bumble bee foragers were monitored from 2012-2014
 in elevationally-stratified zones of two Front Range sites [Niwot Ridge
 (low alpine: 40.0567°N, 105.5916°W, 3564m and mid alpine: 40.0585°N,
 105.6119°W, 3700) and Mount Evans (low alpine: 39.6454°N, 105.5925°W,
 3550m; mid alpine: 39.6334°N, 105.6046°W, 3700m; and high alpine:
 39.5964°N, 105.6275°W, 3850m)] where L. W. Macior documented the historic
 ranges (1966-1969) and flowering hosts of species sampled in this study.
 Host plants and bumble bees were sampled weekly throughout the flowering
 season (June-August) in alpine habitats including krummholz vegetation,
 rocky fellfields, exposed ridges, mesic tundra meadows, and swale or marsh
 vegetation. (1) Climate cues affecting flowering time
 in the host plant-community Twenty-three 2 m × 10 m
 plots were established on Pennsylvania Mountain by P.G. Kevan and surveyed
 weekly from the onset to the end of the flowering season in 1977-1981.
 Plots were located nonrandomly to sample prevalent alpine habitat types
 (Byron, 1980). Using aerial photographs and maps in 2012, we found at
 least one edge of each original plot and established a larger survey area
 that included the original plot in its entirety (Miller-Struttman et al.
 2015) . To account for larger sampling scale from 2012-2019, flower
 density was based on the average flower density in all possible
 independent 2 × 10 m subplots within the larger plots. Open flowers or
 inflorescences were counted weekly to provide comparable data to surveys
 from 1977-81. Inflorescence counts at randomly chosen points were used to
 estimate the average number of open flowers per m2. From flower counts we
 extracted day of first flowering, day of peak flowering, and cumulative
 flower density (total flowers produced per m2 over the entire season) for
 each of the nine host-plant species. (2) Cues driving
 foraging phenology of colonizing vs. resident bumble bee species
 In the Front Range (Niwot Ridge and Mount Evans), we collected
 and identified to species and caste all bumble bees observed foraging on
 flowers without regard to plant taxon, during weekly, one-hour walking
 surveys in each elevational zone (median area of 4.22 ha, and range of
 2.13-6.57 ha; Miller-Struttmann et al., 2015). Individuals were
 anesthetized, photographed, marked with non-toxic paint, and released. In
 the rare event that a marked bee was recaptured, it was released without
 additional data collection and was not included in the analyses presented
 here. A small subset of individuals were lethally collected for archival
 purposes and deposited in the Enns Entomology Museum at the University of
 Missouri. Samples were pooled elevationally to
 characterize bumble bee communities within the average flight distance of
 alpine bumble bees (&lt;1km; Geib et al., 2015) for a total of five
 elevational zones in the Front Range (Niwot Ridge and Mount Evans).
 Species abundances were weighted by collection effort in person hours for
 each elevational zone (median = 663; range: 198-840 person hours). For
 queen and worker bumble bees of each species encountered, we estimated the
 timing of emergence and peak foraging activity. Respectively, emergence
 was operationally recognized as the day of year (DOY) of the first
 observation of that species/caste, and peak activity as the DOY when the
 maximum number of foraging individuals were observed in a given
 elevational zone.  Queens of three colonizing species
 (<em>B. flavifrons, B. melanopygus</em>, and <em>B.
 mixtus</em>) were infrequently collected (fewer than five
 populations sampled over three years) and therefore excluded from these
 analyses. To address whether seasonal patterns of
 forager activity are more canalised for resident than colonizing bumble
 bees, we compared curves for temporal variation in forager activity over
 the season. The number of workers of each species on each date was
 calculated at the regional level by pooling samples from all locations and
 elevational bands. The activity curves for each species were tested for
 kurtosis, which quantifies the degree to which the peak of a curve is
 narrower or broader than expected for a normal distribution. We calculated
 the mean elevation at which bumble bees of each species were collected
 along the 2700 m elevational gradient (mean number of individuals per
 species = 1603). (3) Impacts of climate cues on
 synchrony of colonizers and residents with floral resources
 We surveyed flowering weekly in the nine host-plant species using
 12-15, 1m x 2m plots placed within each elevational zone on Niwot Ridge
 and Mount Evans. In 2012, we established an initial set of ten 1m x 2m
 plots before the onset of flowering in each elevational zone. As the
 flowering season progressed, an additional 2-5 plots were established to
 survey areas of later-blooming. Open flowers or inflorescences for each of
 the nine host plants were counted weekly from onset to end of the
 flowering season and converted to number of flowers using the mean flowers
 per inflorescence for a sub-sample (3-30) of inflorescences per plot. For
 two species (<em>T. dasyphyllum </em>and <em>T.
 parryi</em>), we used published flower counts per inflorescence from
 Pennsylvania Mountain (Geib, 2010) and for one (<em>C.
 occidentalis</em>) flower counts from individuals outside of plots
 on Niwot Ridge and Mount Evans (2012-2013). Days of first and peak
 flowering and cumulative flower density were calculated for each
 elevational zone. For workers of each bumble bee
 species, we estimated the yearly phenological mismatch between foraging
 activity and flowering of the host-plant community in each elevational
 zone. To test for mismatch between worker foraging activity and flowering,
 we calculated the difference between day of peak worker foraging and day
 of peak flowering. Negative numbers indicate that worker activity peaked
 before flowering. (4) Relationship of phenological
 mismatch to abundances of resident and colonizing species
 Cumulative abundance of each bumble bee species was estimated as
 the sum of the weekly counts of all workers of that species weighted by
 collection effort over the season within an elevational zone. Relative
 abundance was calculated as the proportional contribution of a species to
 the bumble bee forager community.
 <strong>References</strong> Byron,
 P. A. (1980). On the ecology and systematics of Coloradan bumblebees. In
 Dissertation. University of Colorado, Boulder.
 Christmas, M. J., Jones, J. C., Olsson, A., Wallerman, O.,
 Bunikis, I., Kierczak, M., Peona, V., Whitley, K. M., Larva, T., Suh, A.,
 Miller-Struttmann, N. E., Geib, J. C., & Webster, M. T. (2021).
 Genetic Barriers to Historical Gene Flow between Cryptic Species of Alpine
 Bumblebees Revealed by Comparative Population Genomics. Molecular Biology
 and Evolution, 38(8), 3126–3143. https://doi.org/10.1093/molbev/msab086 Geib, J. C. (2010). The Impacts of Pollinator Abundance on Benefits from Facultative Pollination Mutualism. In Ph. D. Dissertation, University of Missouri (Issue December). University of Missouri. Geib, J. C., Strange, J. P., & Galen, C. (2015). Bumble bee nest abundance, foraging distance, and host-plant reproduction: implications for management and conservation. Ecological Applications, 25(3), 768–778. Macior, L. W. (1974). Pollination ecology of the front range of the Colorado Rocky Mountains. Melanderia, 15, 1–59. Miller-Struttmann, N. E., Geib, J. C., Franklin, J. D., Kevan, P. G., Holdo, R. M., Ebert-may, D., Lynn, A. M., Kettenbach, J. A., Hedrick, E., & Galen, C. (2015). Functional mismatch in a bumble bee pollination mutualism under climate change. Science, 349(6255), 75–78.
description: R markdown, R, and the follow R packages: lme4, AICcmodavg, car,
 r2glmm, nlme, PerformanceAnalytics