Recent and future declines of a historically widespread pollinator linked to climate, land cover, and pesticides.

The acute decline in global biodiversity includes not only the loss of rare species, but also the rapid collapse of common species across many different taxa. The loss of pollinating insects is of particular concern because of the ecological and economic values these species provide. The western bumble bee (Bombus occidentalis) was once common in western North America, but this species has become increasingly rare through much of its range. To understand potential mechanisms driving these declines, we used Bayesian occupancy models to investigate the effects of climate and land cover from 1998 to 2020, pesticide use from 2008 to 2014, and projected expected occupancy under three future scenarios. Using 14,457 surveys across 2.8 million km2 in the western United States, we found strong negative relationships between increasing temperature and drought on occupancy and identified neonicotinoids as the pesticides of greatest negative influence across our study region. The mean predicted occupancy declined by 57% from 1998 to 2020, ranging from 15 to 83% declines across 16 ecoregions. Even under the most optimistic scenario, we found continued declines in nearly half of the ecoregions by the 2050s and mean declines of 93% under the most severe scenario across all ecoregions. This assessment underscores the tenuous future of B. occidentalis and demonstrates the scale of stressors likely contributing to rapid loss of related pollinator species throughout the globe. Scaled-up, international species-monitoring schemes and improved integration of data from formal surveys and community science will substantively improve the understanding of stressors and bumble bee population trends.

Ecological Drivers and Consequences of Bumble Bee Body Size Variation.

Body size is arguably one of the most important traits influencing the physiology and ecology of animals. Shifts in animal body size have been observed in response to climate change, including in bumble bees (Bombus spp. [Hymenoptera: Apidae]). Bumble bee size shifts have occurred concurrently with the precipitous population declines of several species, which appear to be related, in part, to their size. Body size variation is central to the ecology of bumble bees, from their social organization to the pollination services they provide to plants. If bumble bee size is shifted or constrained, there may be consequences for the pollination services they provide and for our ability to predict their responses to global change. Yet, there are still many aspects of the breadth and role of bumble bee body size variation that require more study. To this end, we review the current evidence of the ecological drivers of size variation in bumble bees and the consequences of that variation on bumble bee fitness, foraging, and species interactions. In total we review: (1) the proximate determinants and physiological consequences of size variation in bumble bees; (2) the environmental drivers and ecological consequences of size variation; and (3) synthesize our understanding of size variation in predicting how bumble bees will respond to future changes in climate and land use. As global change intensifies, a better understanding of the factors influencing the size distributions of bumble bees, and the consequences of those distributions, will allow us to better predict future responses of these pollinators.

The shifting importance of abiotic and biotic factors across the life cycles of wild pollinators.

Organisms living in seasonal environments are exposed to different environmental conditions as they transition from one life stage to the next across their life cycle. How different life stages respond to these varying conditions, and the extent to which different life stages are linked, are fundamental components of the ecology of an organism. Nevertheless, the influence of abiotic and biotic factors on different parts of an organism's life cycle is often not accounted for, which limits our understanding of the ecological consequences of environmental change. We investigated the relative importance of climate conditions, food availability, and previous life-stage abundance in an assemblage of seven wild bumble bee species, asking: how do these three factors directly influence bee abundance at each life stage? To do so, we used a 7-year dataset where we monitored climate conditions, floral resources, and abundances of bees in each life stage across the active colony life cycle in a highly seasonal subalpine ecosystem in the Colorado Rocky Mountains, USA. Bee abundance at different life stages responded to abiotic and biotic conditions in a broadly consistent manner across the seven species: the survival and recruitment stage of the life cycle (overwintered queens) responded negatively to longer winters; the growth stage (workers) responded positively to floral resource availability; and the reproductive stage (males) was positively related to the abundance of the previous life stage (workers). Most species also exhibited some idiosyncratic responses. Our long-term examination of annual bumble bees reveals a general set of responses in the abundance of each life stage to climate conditions, floral resource availability, and previous life stage. Across species, these three factors each directly influenced a distinct life stage, illustrating how their relative importance can shift throughout the life cycle. The life-cycle approach that we have taken highlights that important details about demography can be overlooked without considering life-stage-specific responses. Ultimately, it is these life-stage-specific responses that shape population outcomes, not only for animal pollinators but also for many organisms living in seasonal environments.

Effects of spatial patterning of co-flowering plant species on pollination quantity and purity.

Background and Aims: If two plant species share pollinators, it has been proposed that the interaction between them may range from competitive to facilitative, depending on the way in which they intermingle. In particular, the presence of a rewarding plant species may increase the rate of pollinator visitation to a less rewarding species in its vicinity, but the beneficial increase in visitation may be counteracted by a detrimental increase in heterospecific pollen transfer. We assessed this trade-off using bumble-bees foraging over a gradual spatial transition between two plant species in an indoor cage experiment. Methods: We used two 'species' of artificial flowers - one more rewarding than the other - in arrays that varied in the degree of species intermingling. The flowers dispensed and received powdered food dyes serving as pollen analogues. Captive bumble-bees visited to collect sucrose solution. We quantified dye delivery to the adhesive-tape 'stigmas' in flowers by spectrophotometry. Key Results: Across the spatial transition between species, the less attractive species received more dye (more bee visits) when in proximity to the more attractive species than it did when alone, but the larger dye loads were less pure (more heterospecific pollen transfer). The decline in purity cancelled out the gain in acquisition, so conspecific pollen receipt by the less attractive species was neutrally affected. The more attractive species received fewer visits when surrounded by the less attractive species, so the interaction between the two species was amensalism when considering conspecific pollen reception. Conclusions: Pollinator-mediated interactions between plant species depend on pollination quantity and purity, both of which can depend on spatial intermingling.

Phenological responses to multiple environmental drivers under climate change: insights from a long-term observational study and a manipulative field experiment.

Climate change has induced pronounced shifts in the reproductive phenology of plants, yet we know little about which environmental factors contribute to interspecific variation in responses and their effects on fitness. We integrate data from a 43 yr record of first flowering for six species in subalpine Colorado meadows with a 3 yr snow manipulation experiment on the perennial forb Boechera stricta (Brassicaceae) from the same site. We analyze shifts in the onset of flowering in relation to environmental drivers known to influence phenology: the timing of snowmelt, the accumulation of growing degree days, and photoperiod. Variation in responses to climate change depended on the sequence in which species flowered, with early-flowering species reproducing faster, at a lower heat sum, and under increasingly disparate photoperiods relative to later-flowering species. Early snow-removal treatments confirm that the timing of snowmelt governs observed trends in flowering phenology of B. stricta and that climate change can reduce the probability of flowering, thereby depressing fitness. Our findings suggest that climate change is decoupling historical combinations of photoperiod and temperature and outpacing phenological changes for our focal species. Accurate predictions of biological responses to climate change require a thorough understanding of the factors driving shifts in phenology.

Interannual bumble bee abundance is driven by indirect climate effects on floral resource phenology.

Climate change can influence consumer populations both directly, by affecting survival and reproduction, and indirectly, by altering resources. However, little is known about the relative importance of direct and indirect effects, particularly for species important to ecosystem functioning, like pollinators. We used structural equation modelling to test the importance of direct and indirect (via floral resources) climate effects on the interannual abundance of three subalpine bumble bee species. In addition, we used long-term data to examine how climate and floral resources have changed over time. Over 8 years, bee abundances were driven primarily by the indirect effects of climate on the temporal distribution of floral resources. Over 43 years, aspects of floral phenology changed in ways that indicate species-specific effects on bees. Our study suggests that climate-driven alterations in floral resource phenology can play a critical role in governing bee population responses to global change.

Multitrophic interactions mediate the effects of climate change on herbivore abundance.

Climate change can influence the abundance of insect herbivores through direct and indirect mechanisms. In this study, we evaluated multitrophic drivers of herbivore abundance for an aphid species (Aphis helianthi) in a subalpine food web consisting of a host plant (Ligusticum porteri), mutualist ants and predatory lygus bugs (Lygus spp.). We used a model-selection approach to determine which climate and host plant cues best predict year-to-year variation in insect phenology and abundance observed over 6 years. We complemented this observational study with experiments that determined how elevated temperature interacts with (1) host plant phenology and (2) the ant-aphid mutualism to determine aphid abundance. We found date of snowmelt to be the best predictor of yearly abundance of aphid and lygus bug abundance but the direction of this effect differed. Aphids achieved lower abundances in early snowmelt years likely due to increased abundance of lygus bug predators in these years. Elevating temperature of L. porteri flowering stalks reduced their quality as hosts for aphid populations. However, warming aphid colonies on host plants of similar quality increased population growth rates. Importantly, this effect was apparent even in the absence of ants. While we observed fewer ants tending colonies at elevated temperatures, these colonies also had reduced numbers of lygus bug predators. This suggests that mutualism with ants becomes less significant as temperature increases, which contrasts other ant-hemipteran systems. Our observational and experimental results show the importance of multitrophic species interactions for predicting the effect of climate change on the abundances of herbivores.

Interactions between bee foraging and floral resource phenology shape bee populations and communities.

Flowers are ephemeral, yet bees rely on them for food throughout their lives. Floral resource phenology - which can be altered by changes in climate and land-use - is therefore key to bee fitness and community composition. Here, we discuss the interactions between floral resource phenology, bee foraging behaviour, and traits such as diet breadth, sociality, and body size. Recent research on bumble bees has examined behavioural responses to local floral turnover and effects of landscape-scale floral resource phenology on fitness, abundance, and foraging distances. Comparable studies are needed on non-social, pollen-specialist species. We also encourage greater use of information contained in museum collections on bee phenologies and floral hosts to test how phenology has shaped the evolution of bee-plant associations.

Site fidelity by bees drives pollination facilitation in sequentially blooming plant species.

Plant species can influence the pollination and reproductive success of coflowering neighbors that share pollinators. Because some individual pollinators habitually forage in particular areas, it is also possible that plant species could influence the pollination of neighbors that bloom later. When flowers of a preferred forage plant decline in an area, site-fidelity may cause individual flower feeders to stay in an area and switch plant species rather than search for preferred plants in a new location. A newly blooming plant species may quickly inherit a set of visitors from a prior plant species, and therefore experience higher pollination success than it would in an area where the first species never bloomed. To test this, we manipulated the placement and timing of two plant species, Delphinium barbeyi and later-blooming Gentiana parryi. We recorded the responses of individually marked bumble bee pollinators. About 63% of marked individuals returned repeatedly to the same areas to forage on Delphinium. When Delphinium was experimentally taken out of bloom, most of those site-faithful individuals (78%) stayed and switched to Gentiana. Consequently, Gentiana flowers received more visits in areas where Delphinium had previously flowered, compared to areas where Delphinium was still flowering or never occurred. Gentiana stigmas received more pollen in areas where Delphinium disappeared than where it never bloomed, indicating that Delphinium increases the pollination of Gentiana when they are separated in time. Overall, we show that individual bumble bees are often site-faithful, causing one plant species to increase the pollination of another even when separated in time, which is a novel mechanism of pollination facilitation.

Seasonal change in a pollinator community and the maintenance of style length variation in Mertensia fusiformis (Boraginaceae).

BACKGROUND AND AIMS: In sub-alpine habitats, patchiness in snowpack produces marked, small-scale variation in flowering phenology. Plants in early- and late-melting patches are therefore likely to experience very different conditions during their flowering periods. Mertensia fusiformis is an early-flowering perennial that varies conspicuously in style length within and among populations. The hypothesis that style length represents an adaptation to local flowering time was tested. Specifically, it was hypothesized that lower air temperatures and higher frost risk would favour short-styled plants (with stigmas more shielded by corollas) in early-flowering patches, but that the pollen-collecting behaviour of flower visitors in late-flowering patches would favour long-styled plants. METHODS: Floral morphology was measured, temperatures were monitored and pollinators were observed in several matched pairs of early and late populations. To evaluate effects of cold temperatures on plants of different style lengths, experimental pollinations were conducted during mornings (warm) and evenings (cool), and on flowers that either had or had not experienced a prior frost. The effectiveness of different pollinators was quantified as seed set following single visits to plants with relatively short or long styles. KEY RESULTS: Late-flowering populations experienced warmer temperatures than early-flowering populations and a different suite of pollinators. Nectar-foraging bumble-bee queens and male solitary bees predominated in early populations, whereas pollen-collecting female solitary bees were more numerous in later sites. Pollinators differed significantly in their abilities to transfer pollen to stigmas at different heights, in accordance with our prediction. However, temperature and frost sensitivity did not differ between long- and short-styled plants. Although plants in late-flowering patches tended to have longer styles than those in early patches, this difference was not consistent. CONCLUSIONS: Seasonal change in pollinator-mediated selection on style length may help maintain variation in this trait in M. fusiformis, but adaptation to local flowering time is not apparent. The prevalence of short styles in these populations requires further explanation.