Jennifer C. Geib

Dosage-Dependent Impacts of a Floral Volatile Compound on Pollinators, Larcenists, and the Potential for Floral Evolution in the Alpine Skypilot Polemonium viscosum

All volatile organic compounds (VOCs) vary quantitatively, yet how such variation affects their ecological roles is unknown. Because floral VOCs are cues for both pollinators and floral antagonists, variation in emission may have major consequences for costs and benefits in plant-pollinator interactions. In Polemonium viscosum, the emission rate for the floral VOC 2-phenylethanol (2PE) spans more than two orders of magnitude. We investigated the ecological and evolutionary impacts of this immense phenotypic variation. The emission rate of 2PE varies independently of nectar rewards and thus is uninformative of profitability. Emission is elevated in flowers that are morphologically vulnerable to ant larcenists, suggesting that chemical deterrence may compensate for weak physical barriers. In nature, plants emitting more 2PE than their neighbors escape ant damage. Flower-damaging ants die when exposed to 2PE in the laboratory, and they avoid high 2PE emitters in the field. High 2PE also reduces bumblebee visitation and pollination, suggesting an ecological cost of defense in pollinator service. However, at more moderate emission rates, 2PE enhances the amount of nectar left in flowers, at no pollination cost. In conclusion, repellency of 2PE is highly sensitive to dosage, giving it a key role in shaping ecological interactions between skypilot plants and their floral visitors.

Functional mismatch in a bumble bee pollination mutualism under climate change.

Climate change decoupling mutualism Many coevolved species have precisely matched traits. For example, long-tongued bumblebees are well adapted for obtaining nectar from flowers with long petal tubes. Working at high altitude in Colorado, Miller-Struttmann et al. found that long-tongued bumblebees have decreased in number significantly over the past 40 years. Short-tongued species, which are able to feed on many types of flowers, are replacing them. This shift seems to be a direct result of warming summers reducing flower availability, making generalist bumblebees more successful than specialists and resulting in the disruption of long-held mutualisms. Science, this issue p. 1541 Warming summers shorten bees’ tongues and disrupt well-established mutualisms between bees and plants. Ecological partnerships, or mutualisms, are globally widespread, sustaining agriculture and biodiversity. Mutualisms evolve through the matching of functional traits between partners, such as tongue length of pollinators and flower tube depth of plants. Long-tongued pollinators specialize on flowers with deep corolla tubes, whereas shorter-tongued pollinators generalize across tube lengths. Losses of functional guilds because of shifts in global climate may disrupt mutualisms and threaten partner species. We found that in two alpine bumble bee species, decreases in tongue length have evolved over 40 years. Co-occurring flowers have not become shallower, nor are small-flowered plants more prolific. We argue that declining floral resources because of warmer summers have favored generalist foraging, leading to a mismatch between shorter-tongued bees and the longer-tubed plants they once pollinated.

DENSITY-DEPENDENT EFFECTS OF ANTS ON SELECTION FOR BUMBLE BEE POLLINATION IN POLEMONIUM VISCOSUM

Mutualisms are commonly exploited by cheater species that usurp rewards without providing reciprocal benefits. Yet most studies of selection between mutualist partners ignore interactions with third species and consequently overlook the impact of cheaters on evolution in the mutualism. Here, we explicitly investigate how the abundance of nectar-thieving ants (cheaters) influences selection in a pollination mutualism between bumble bees and the alpine skypilot, Polemonium viscosum. As suggested in past work with this species, bumble bees accounted for most of the seed production (78% +/- 6% [mean +/- SE]) in our high tundra study population and, in the absence of ants, exerted strong selection for large flowers. We tested for indirect effects of ant abundance on seed set through bumble bee pollination services (pollen delivery and pollen export) and a direct effect through flower damage. Ants reduced seed set per flower by 20% via flower damage. As ant density increased within experimental patches, the rate of flower damage rose, but pollen delivery and export did not vary significantly, showing that indirect effects of increased cheater abundance on pollinator service are negligible in this system. To address how ants affect selection for plant participation in the pollination mutualism we tested the impact of ant abundance on selection for bumble bee-mediated pollination. Results show that the impact of ants on fitness (seed set) accruing under bumble bee pollination is density dependent in P. viscosum. Selection for bumble bee pollination declined with increasing ant abundance in experimental patches, as predicted if cheaters constrain fitness returns of mutualist partner services. We also examined how ant abundance influences selection on flower size, a key component of plant investment in bumble bee pollination. We predicted that direct effects of ants would constrain bumble bee selection for large flowers. However, selection on flower size was significantly positive over a wide range of ant abundance (20-80% of plants visited by ants daily). Although high cheater abundance reduces the fitness returns of bumble bee pollination, it does not completely eliminate selection for bumble bee attraction in P. viscosum.

Tracing impacts of partner abundance in facultative pollination mutualisms: from individuals to populations

Partner abundance affects costs and benefits in obligate mutualisms, but its role in facultative partnerships is less clear. We address this gap in a pollination web consisting of two clovers (Trifolium) that differ in specialization on a bumble bee pollinator Bombus balteatus. We examine how pollination niche breadth affects plant responses to pollinator abundance, comparing early-flowering (specialized) and late-flowering (generalized) cohorts of T. parryi and early T. parryi to T. dasyphyllum, a pollination generalist. Co-pollinators disrupt the link between B. halteatus visitation and pollination rate for both clovers. Only for early-flowering T. parryi do visitation, pollination, and seed set increase with density of B. balteatus. Bumble bee density also alters timing of seed germination in T. parryi, with seeds from plants receiving augmented B. balteatus germinating sooner than seeds of open-pollinated counterparts. Benefits saturate at intermediate bumble bee densities. Despite strong effects of B. balteatus density on individual plant fitness components, population models suggest little impact of B. balteatus density on lamda in T. parryi or T. dasyphyllum. Findings show that functional redundancy in a pollinator guild mediates host-plant responses to partner density. Unexpected effects of pollinator density on life history schedule have implications for recruitment under pollinator decline.

Bumble bee nest abundance, foraging distance, and host-plant reproduction: implications for management and conservation

Recent reports of global declines in pollinator species imply an urgent need to assess the abundance of native pollinators and density-dependent benefits for linked plants. In this study, we investigated (1) pollinator nest distributions and estimated colony abundances, (2) the relationship between abundances of foraging workers and the number of nests they represent, (3) pollinator foraging ranges, and (4) the relationship between pollinator abundance and plant reproduction. We examined these questions in an alpine ecosystem in the Colorado Rocky Mountains, focusing on four alpine bumble bee species (Bombus balteatus, B. flavifrons, B. bifarius, and B. sylvicola), and two host plants that differ in their degrees of pollinator specialization (Trifolium dasyphyllum and T. parryi). Using microsatellites, we found that estimated colony abundances among Bombus species ranged from ~18 to 78 colonies/0.01 km2. The long-tongued species B. balteatus was most common, especially high above treeline, but the subalpine species B. bifarius was unexpectedly abundant for this elevation range. Nests detected among sampled foragers of each species were correlated with the number of foragers caught. Foraging ranges were smaller than expected for all Bombus species, ranging from 25 to 110 m. Fruit set for the specialized plant, Trifolium parryi, was positively related to the abundance of its Bombus pollinator. In contrast, fruit set for the generalized plant, T. dasyphyllum, was related to abundance of all Bombus species. Because forager abundance was related to nest abundance of each Bombus species and was an equally effective predictor of plant fecundity, forager inventories are probably suitable for assessing the health of outcrossing plant populations. However, nest abundance, rather than forager abundance, better reflects demographic and genetic health in populations of eusocial pollinators such as bumble bees. Development of models incorporating the parameters we have measured here (nest abundance, forager abundance, and foraging distance) could increase the usefulness of foraging worker inventories in nionitoring, managing, and conserving pollinator populations.

Flight of the bumble bee: Buzzes predict pollination services

Multiple interacting factors drive recent declines in wild and managed bees, threatening their pollination services. Widespread and intensive monitoring could lead to more effective management of wild and managed bees. However, tracking their dynamic populations is costly. We tested the effectiveness of an inexpensive, noninvasive and passive acoustic survey technique for monitoring bumble bee behavior and pollination services. First, we assessed the relationship between the first harmonic of the flight buzz (characteristic frequency) and pollinator functional traits that influence pollination success using flight cage experiments and a literature search. We analyzed passive acoustic survey data from three locations on Pennsylvania Mountain, Colorado to estimate bumble bee activity. We developed an algorithm based on Computational Auditory Scene Analysis that identified and quantified the number of buzzes recorded in each location. We then compared visual and acoustic estimates of bumble bee activity. Using pollinator exclusion experiments, we tested the power of buzz density to predict pollination services at the landscape scale for two bumble bee pollinated alpine forbs (Trifolium dasyphyllum and T. parryi). We found that the characteristic frequency was correlated with traits known to affect pollination efficacy, explaining 30–52% of variation in body size and tongue length. Buzz density was highly correlated with visual estimates of bumble bee density (r = 0.97), indicating that acoustic signals are predictive of bumble bee activity. Buzz density predicted seed set in two alpine forbs when bumble bees were permitted access to the flowers, but not when they were excluded from visiting. Our results indicate that acoustic signatures of flight can be deciphered to monitor bee activity and pollination services to bumble bee pollinated plants. We propose that applications of this technique could assist scientists and farmers in rapidly detecting and responding to bee population declines.

Bumble bee tongue length - Macior 1974

Tongue length measurements from Macior 1974. Used in “Tongue length density function parameter estimation.r” COLUMN DETAILS: BB.SPECIES - bumble bee species name MEAN - mean tongue length (mm) STANDARD.DEVIATION - standard deviation in tongue length (mm)

Bumble bee visits - Front Range

This is the number of individuals of each bumble bee species visiting each plant species as collected by Macior (1974) and Miller-Struttmann in the past (1966-1969) and present (2012-2014). Visitation data from Mt. Evans Wilderness Area and Niwot Ridge Long Term Ecological Research combined as in Macior 1974. Used in “Tube depth density function parameter estimation.r”

Bumble bee community workers present - Front Range

This is the list of bumble bees (Bombus workers) as collected by Nicole Miller-Struttmann and colleagues between 2012 and 2014 at Niwot Ridge Long Term Ecological Research site and Mount Evans Wilderness Area in Colorado. Data from Mt. Evans and Niwot Ridge combined as in Macior 1974. Used in “Tongue length density function parameter estimation.r”

Bumble bee community workers present - Pennsylvania Mountain

This is the list of bumble bees (Bombus workers) as collected by Jenni Geib and colleagues in 2008, 2011 and 2013 at Pennsylvania Mountain, CO. Used in “Tongue length density function parameter estimation.r”