Generalist Bumblebee Research Articles

Learning to handle flowers increases pollen collection for bees but does not affect pollination success for plants

Abstract Cooperation and conflict are common in plant–pollinator interactions. Flowering plants often entice pollinators to visit by offering floral food rewards, thereby facilitating pollination. However, pollinators such as bees can learn to improve their collection of floral rewards (such as pollen), changing how they interact with the flower’s reproductive organs, which together could reduce pollination success. Consequently, complex flowers that slow pollinator learning might benefit the plant. Yet how pollinator learning and flower complexity interact to affect pollination success is unknown. We therefore asked how differences in complexity of 4 flower types (Phacelia campanularia, Exacum affine, Solanum elaeagnifolium, and Erythranthe guttata) affected learning by pollen-foraging generalist bumble bees (Bombus impatiens) and how learning affected pollen collection and pollen deposition on these flowers. We found that bees generally learned how to efficiently handle more complex flower types more slowly. Bees that required more visits to become efficient foragers collected less pollen, with no effect on pollen deposition. Except for the simplest flower type, learning also involved development of motor routines unique to each flower type. Experienced bees overall collected more pollen, but individual differences in motor routines did not affect pollen collection. Conversely, individual differences in motor routines affected pollen deposition, but there was no overall effect of experience. Thus, even though learning overall benefits the bee, it does not alter female (and potentially male) fitness benefits for the plant. We discuss potential reasons for these patterns and consequences for bee behavior and flower evolution.

Intraspecific size shifts in generalist bumblebees and flowers lead to low functional consequences

AbstractBody size is a trait that can affect plant–pollinator interaction efficiency and plant reproductive success. We explored the impact of intraspecific size shifts on the interactions between pollinators and flowering plants under controlled conditions. We considered two development conditions leading to the production of large and small individual flowers of Borago officinalis and Echium plantagineum. We also used the natural variability of worker size within bumblebee colonies to isolate small and large workers. We performed a fully crossed experiment with the two flower sizes of each plant species and the two sizes of bumblebee workers. Our results show that the size of both partners did not affect bee foraging behavior in most of the evaluated parameters and both bee sizes were equally efficient in depositing pollen. Significant differences were found only in pollen deposition across the life of a flower in small flowers of B. officinalis, with the greatest quantity of pollen deposited by small bees. We did not find a relationship between pollinator size and plant fitness. Our results suggest that generalist plant–pollinator interactions may be resilient to future potential mismatches in the size of the partners but remain to be tested if they are still resilient under the new environmental conditions resulting from global changes.

In Which Way Do the Flower Properties of the Specialist Orchid Goodyera repens Meet the Requirements of Its Generalist Pollinators?

This article is the next part of a series of studies documenting the influence of flower traits on the reproductive success (RS) of orchids. Knowledge of factors influencing RS helps to understand the mechanisms and processes crucial for shaping plant-pollinator interactions. The aim of the present study was to determine the role of flower structure and nectar composition in shaping the RS of the specialist orchid Goodyea repens, which is pollinated by generalist bumblebees. We found a high level of pollinaria removal (PR) and female reproductive success (fruiting, FRS) as well as a high level of variation between populations, although in certain populations pollination efficiency was low. Floral display traits, mainly inflorescence length, influenced FRS in certain populations. Among the flower traits, only the height of flowers was correlated with FRS in one population, suggesting that the flower structure of this orchid is well adapted to pollination by bumblebees. The nectar of G. repens is diluted and dominated by hexoses. Sugars were less important in shaping RS than amino acids. At the species level, twenty proteogenic and six non-proteogenic AAs were noted, along with their differentiated amounts and participation in particular populations. We found that distinct AAs or their groups mainly shaped PR, especially when correlations were considered at the species level. Our results suggest that both the individual nectar components and the ratios between them have an impact on G. repens RS. Because different nectar components influence the RS parameters in different ways (i.e., negatively or positively), we suggest that different Bombus species play the role of main pollinators in distinct populations.

Compound-Specific Behavioral and Enzymatic Resistance to Toxic Milkweed Cardenolides in a Generalist Bumblebee Pollinator.

Plant secondary metabolites that defend leaves from herbivores also occur in floral nectar. While specialist herbivores often have adaptations providing resistance to these compounds in leaves, many social insect pollinators are generalists, and therefore are not expected to be as resistant to such compounds. The milkweeds, Asclepias spp., contain toxic cardenolides in all tissues including floral nectar. We compared the concentrations and identities of cardenolides between tissues of the North American common milkweed Asclepias syriaca, and then studied the effect of the predominant cardenolide in nectar, glycosylated aspecioside, on an abundant pollinator. We show that a generalist bumblebee, Bombus impatiens, a common pollinator in eastern North America, consumes less nectar with experimental addition of ouabain (a standard cardenolide derived from Apocynacid plants native to east Africa) but not with addition of glycosylated aspecioside from milkweeds. At a concentration matching that of the maximum in the natural range, both cardenolides reduced activity levels of bees after four days of consumption, demonstrating toxicity despite variation in behavioral deterrence (i.e., consumption). In vitro enzymatic assays of Na+/K+-ATPase, the target site of cardenolides, showed lower toxicity of the milkweed cardenolide than ouabain for B. impatiens, indicating that the lower deterrence may be due to greater tolerance to glycosylated aspecioside. In contrast, there was no difference between the two cardenolides in toxicity to the Na+/K+-ATPase from a control insect, the fruit fly Drosophila melanogaster. Accordingly, this work reveals that even generalist pollinators such as B. impatiens may have adaptations to reduce the toxicity of specific plant secondary metabolites that occur in nectar, despite visiting flowers from a wide variety of plants over the colony's lifespan.

Hold tight or loosen up? Functional consequences of a shift in anther architecture depend substantially on bee body size.

A fundamental question in pollination ecology is how pollinators affect the evolution of different floral forms. Yet functional effects of shifts in floral form for plant and pollinator are frequently unclear. For instance, flowers that conceal pollen within tube-like anthers that are spread apart and move freely (free architecture) or are tightly joined together (joined architecture) have evolved independently across diverse plant families and are geographically widespread. Surprisingly, how their bee pollinators affect the function of both architectures remains unknown. We hypothesised that bee body size would affect foraging success and pollination differently for free and joined anther architectures. Therefore, we modified the anther architecture of a single plant species (Solanum elaeagnifolium) and used a single species of generalist bumble bee (Bombus impatiens), which varies greatly in body size. We found that on free anther architecture, larger bees were better pollinators. More pollen on their bodies was available for pollination and they deposited more pollen on stigmas. Conversely, on joined anther architecture, smaller bees were better pollinators. They collected less pollen into their pollen baskets, had more pollen on their bodies available for pollination, and deposited more pollen on stigmas. While we also found modest evidence that plants benefit more from joined versus free anther architecture, further investigation will likely reveal this also depends on pollinator traits. We discuss potential mechanisms by which pollinator size and anther architecture interact and implications for floral evolution.

Species-Enriched Grass-Clover Mixtures Can Promote Bumblebee Abundance Compared with Intensively Managed Conventional Pastures

(1) Land use intensification has led to serious declines in biodiversity, including in forage production systems for dairy cows. Agri-environmental schemes, such as enriching grasslands in floral species, were shown to be an effective tool to promote biodiversity in higher trophic levels. Here, we studied an innovative pasture-based dairy production system with floral-species-enhanced temporary grasslands, with respect to the effect on wild bee abundance and species richness. (2) We studied three grass-clover mixtures with perennial ryegrass and clover species with different levels of plant diversity for flower cover and wild bees. The grass-clover pastures were rotationally stocked with cattle and parts of the pastures were excluded from grazing. Intensively managed conventional permanent grasslands were studied as the common land use type. Wild bees were caught by sweep netting. Wild bee diversity was analysed with a general linear mixed model. For species richness, an incidence-based coverage estimator was calculated. (3) In total, 541 wild bees from 10 species were found. No wild bees were caught on the conventional grasslands. Wild bee abundance and species richness did not differ among the three grass-clover mixtures, but with increasing flower cover of white clover (Trifolium repens), wild bee abundance increased. Except for one solitary wild bee individual, the recorded community exclusively consisted of bumblebees. While generalist species that are commonly found on farmland dominated, rare long-tongued bumblebees made up 10% on the grazed sites of the multispecies mixture and made up 20% on the ungrazed strips of the binary mixture and multispecies mixture. (4) We conclude that multispecies mixtures can provide resources for generalist bumblebee species, especially when compared with conventional grasslands that offer no resources. Considering that the multispecies mixture has been also shown to reduce greenhouse gas emissions and nitrate leaching, while maintaining high forage yields, our findings add to the potential to promote a wide range of ecosystem services. Yet, should their full potential be enfolded, grazing should partially be excluded, and the mixture should be extended by plant species with more open flowers, suitable for solitary wild bees.

Bumble Bee Foraged Pollen Analyses in Spring Time in Southern Estonia Shows Abundant Food Sources.

Simple SummaryPollinators make a strong contribution to ecosystem stability. However, nowadays, they also need protection and sustainable habitat to live and develop. Not all regions can provide suitable habitats due to agricultural intensification, urbanization, climate changes and corresponding impacts. Our study was conducted in the late spring in south Estonia where arable lands were surrounded by forest patches and rural areas. For better performance, we used both light microscopy and DNA metabarcoding methods for pollen identification. We found that bumble bees foraged on the diverse food sources showing preferences for several main plant families. Additionally, in our case, land-use types did not show important effects on bumble bee food choices and foraging decisions. Various landscape features can provide diverse food sources at the early development stages and support nest longevity. Here, we can say that a better understanding of pollinators’ food preferences can help in the application of more suitable measures for their conservation. Agricultural landscapes usually provide higher quantities of single-source food, which are noticeably lacking in diversity and might thus have low nutrient value for bumble bee colony development. Here, in this study, we analysed the pollen foraging preferences over a large territory of a heterogeneous agricultural landscape: southern Estonia. We aimed to assess the botanical diversity of bumble bee food plants in the spring time there. We looked for preferences for some food plants or signs of food shortage that could be associated with any particular landscape features. For this purpose, we took Bombus terrestris commercial hives to the landscape, performed microscopy analyses and improved the results with the innovative DNA metabarcoding technique to determine the botanical origin of bumble bee-collected pollen. We found high variability of forage plants with no strong relationship with any particular landscape features. Based on the low number of plant species in single flights, we deduce that the availability of main forage plants is sufficient indicating rich forage availabilities. Despite specific limitations, we saw strong correlations between microscopy and DNA metabarcoding data usable for quantification analyses. As a conclusion, we saw that the spring-time vegetation in southern Estonia can support bumble bee colony development regardless of the detailed landscape structure. The absence of clearly dominating food preference by the tested generalist bumble bee species B. terrestris makes us suggest that other bumble bee species, at least food generalists, should also find plenty of forage in their early development phase.

No sex differences in learning in wild bumblebees

Abstract Females and males often face different sources of selection, resulting in dimorphism in morphological, physiological, and even cognitive traits. Sex differences are often studied in respect to spatial cognition, yet the different ecological roles of males and females might shape cognition in multiple ways. For example, in dietary generalist bumblebees (Bombus), the ability to learn associations is critical to female workers, who face informationally rich foraging scenarios as they collect nectar and pollen from thousands of flowers over a period of weeks to months to feed the colony. While male bumblebees likely need to learn associations as well, they only forage for themselves while searching for potential mates. It is thus less clear whether foraging males would benefit from the same associative learning performance as foraging females. In this system, as in others, cognitive performance is typically studied in lab-reared animals under captive conditions, which may not be representative of patterns in the wild. In the first test of sex and species differences in cognition using wild bumblebees, we compared the performance of Bombus vancouverensis nearcticus (formerly bifarius) and Bombus vosnesenskii of both sexes on an associative learning task at Sierra Nevada (CA) field sites. Across both species, we found that males and females did not differ in their ability to learn, although males were slower to respond to the sucrose reward. These results offer the first evidence from natural populations that male bumblebees may be equally as able to learn associations as females, supporting findings from captive colonies of commercial bees. The observed interspecific variation in learning ability opens the door to using the Bombus system to test hypotheses about comparative cognition.

Sensory bias and signal detection trade-offs maintain intersexual floral mimicry

Mimicry is common in interspecies interactions, yet conditions maintaining Batesian mimicry have been primarily tested in predator-prey interactions. In pollination mutualisms, floral mimetic signals thought to dupe animals into pollinating unrewarding flowers are widespread (greater than 32 plant families). Yet whether animals learn to both correctly identify floral models and reject floral mimics and whether these responses are frequency-dependent is not well understood. We tested how learning affected the effectiveness and frequency-dependence of imperfect Batesian mimicry among flowers using the generalist bumblebee, Bombus impatiens, visiting Begonia odorata, a plant species exhibiting intersexual floral mimicry. Unrewarding female flowers are mimics of pollen-rewarding male flowers (models), though mimicry to the human eye is imperfect. Flower-naive bees exhibited a perceptual bias for mimics over models, but rapidly learned to avoid mimics. Surprisingly, altering the frequency of models and mimics only marginally shaped responses by naive bees and by bees experienced with the distribution and frequency of models and mimics. Our results provide evidence both of exploitation by the plant of signal detection trade-offs in bees and of resistance by the bees, via learning, to this exploitation. Critically, we provide experimental evidence that imperfect Batesian mimicry can be adaptive and, in contrast with expectations of signal detection theory, functions largely independently of the model and mimic frequency. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Asteraceae Paradox: Chemical and Mechanical Protection of Taraxacum Pollen.

Excessive pollen harvesting by bees can compromise the reproductive success of plants. Plants have therefore evolved different morphological structures and floral cues to narrow the spectrum of pollen feeding visitors. Among “filtering” mechanisms, the chemical and mechanical protection of pollen might shape bee-flower interactions and restrict pollen exploitation to a specific suite of visitors such as observed in Asteraceae. Asteraceae pollen is indeed only occasionally exploited by generalist bee species but plentifully foraged by specialist ones (i.e., Asteraceae paradox). During our bioassays, we observed that micro-colonies of generalist bumblebee (Bombus terrestris L.) feeding on Taraxacum pollen (Asteraceae) reduced their pollen collection and offspring production. Bees also experienced physiological effects of possible defenses in the form of digestive damage. Overall, our results suggest the existence of an effective chemical defense in Asteraceae pollen, while the hypothesis of a mechanical defense appeared more unlikely. Pre- and post-ingestive effects of such chemical defenses (i.e., nutrient deficit or presence of toxic compounds), as well as their role in the shaping of bee-flower interactions, are discussed. Our results strongly suggest that pollen chemical traits may act as drivers of plant selection by bees and partly explain why Asteraceae pollen is rare in generalist bee diets.

Pollen defenses negatively impact foraging and fitness in a generalist bee (Bombus impatiens: Apidae)

Plants may benefit from limiting the community of generalist floral visitors if the species that remain are more effective pollinators and less effective pollenivores. Plants can reduce access to pollen through altered floral cues or morphological structures, but can also reduce consumption through direct pollen defenses. We observed that Eucera (Peponapis) pruinosa, a specialist bee on Cucurbita plants, collected pure loads of pollen while generalist honey bees and bumble bees collected negligible amounts of cucurbit pollen, even though all groups of bees visited these flowers. Cucurbit flowers have no morphological adaptations to limit pollen collection by bees, thus we assessed their potential for physical, nutritional, and chemical pollen traits that might act as defenses to limit pollen loss to generalist pollinators. Bumble bee (Bombus impatiens) microcolonies experienced reduced pollen consumption, mortality, and reproduction as well as increased stress responses when exposed to nutritional and mechanical pollen defenses. These bees also experienced physiological effects of these defenses in the form of hindgut expansion and gut melanization. Chemical defenses alone increased the area of gut melanization in larger bees and induced possible compensatory feeding. Together, these results suggest that generalist bumble bees avoid collecting cucurbit pollen due to the physiological costs of physical and chemical pollen defenses.

Pollen grain morphology is not exclusively responsible for pollen collectability in bumble bees

Bee-pollinated plants face a dilemma in that bees both passively transport pollen grains among conspecific flowers and actively collect pollen to feed their larvae. Therefore, mechanisms that reduce pollen collection by bees have evolved in melittophilous plants. Malvaceae pollen is uncollectable for corbiculate bees which has previously been ascribed to pollen size, spines, and pollenkitt. We analysed the influence of pollen grain properties (diameter, spine length, spine density) on the collectability of echinate (spiny) pollen by bumble bees (Bombus terrestris). Workers individually foraging on one of eight plant species from six families performed significantly less pollen foraging on plants which have large, echinate pollen grains. Nevertheless, neither pollen grain size, spine length, nor spine density prove to be an absolute disqualifier for collectability. While pollen foragers did not shift to nectar collection but seized visiting flowers with uncollectable pollen, nectar foragers performed regular foraging bouts on these plants. Pollen that is uncollectable for corbiculate bees limits pollen depletion by generalist bumble bees and probably also honey bees while maintaining them as pollinators, which is an effective solution to the pollen dilemma. As previous assumptions about the impact of pollen morphology on its collectability are disproved, potentially determining factors are discussed.

Bumble bees (Hymenoptera: Apidae: Bombus terrestris) collecting honeydew from the giant willow aphid (Hemiptera: Aphididae)

Only rarely have bumble bees (Bombus) been observed collecting honeydew from aphids (Aphididae) feeding on phloem sap. This behavior may be rare because the percentage of sugar in honeydew egested from aphids is generally well below the sugar concentration in floral nectars preferred by bumble bees. Nonetheless, in August 2018, near St. Buryan, Penzance, Cornwall, UK (56.0602N; -5.6034W) we observed large numbers of wildBombusterrestris(Linnaeus) collecting honeydew from a colony of the giant willow aphidTuberolachnussalignusGmelin feeding on the stems of the willowSalixalba. Unlike aphid-tending ants, who glean fresh honeydew directly from the aphid anal opening, the bumble bees were collecting honeydew from leaf litter below the aphid colony. We hypothesized that honeydew collected from exposed ground surfaces was more concentrated due to evaporation under ambient conditions than that released directly from the anus (fresh honeydew). We thus monitored sugar concentrations of fresh honeydew and compared them with the concentrations of the crop contents of worker bumble bees foraging from the leaf litter. Our data show that the concentration of sugar in fresh honeydew was as much as 10% w/w lower than that collected from leaf surfaces, as measured from the crop contents of foragers. The unusually hot, dry weather in Cornwall may have enhanced evaporative concentration of honeydew while restricting floral nectar sources, thus favoring honeydew collection byB.terrestris, a generalist bumble bee forager.

Associative learning of flowers by generalist bumble bees can be mediated by microbes on the petals

Abstract Communication is often vital to the maintenance of mutualisms. In plant-pollinator mutualisms, plants signal pollinators via floral displays, composed of olfactory, visual, and other plant-derived cues. While plants are understood to be associated with microbes, only recently has the role of microbial (yeast and bacteria) inhabitants of flowers as intermediaries of plant-pollinator communication been recognized. Animals frequently use microbial cues to find resources, yet no study has examined whether microbes directly mediate learned and innate pollinator responses. Here, we asked whether microbes on the flower surface, independent of their modification of floral rewards, can mediate these key components of pollinator preference. In the field, we characterized flower and bumble bee microbial abundance, and in laboratory assays we tested whether bumble bees (Bombus impatiens) discriminated flowers on the basis of an experimental floral microbial community on the petals and whether microbe-derived chemicals were effective cues. Learning of microbial community cues was associative and reward context-dependent and mediated by microbial chemicals. Deconstructing the experimental microbial community showed bees innately avoided flowers with bacteria, but were undeterred by yeast. Microbial cues thus potentially facilitate dynamic communication between plants and pollinators such as bumble bees, especially as pollinator visitation can change flower microbiota. We suggest that the study of communication in mutualism generally would benefit by considering not only the multicellular eukaryote partners, but their microbial associates.

Invasive plants as potential food resource for native pollinators: A case study with two invasive species and a generalist bumble bee

It is now well established that invasive plants may induce drifts in the quantity and/or quality of floral resources. They are then often pointed out as a potential driver of bee decline. However, their impact on bee population remains quite unclear and still controversial, as bee responses are highly variable among species. Here, we compared the amino acid composition of pollen from three native and two invasive plant species included in diets of common pollinators in NW Europe. Moreover, the nutritional intake (i.e., pollen and amino acid intakes) of Bombus terrestris colonies and the pollen foraging behaviour of workers (i.e., visiting rate, number of foraging trips, weight of pollen loads) were considered. We found significant differences in pollen nutrients among the studied species according to the plant invasive behaviour. We also found significant differences in pollen foraging behaviour according to the plant species, from few to several foraging trips carrying small or large pollen loads. Such behavioural differences directly impacted the pollen intake but depended more likely on plant morphology rather than on plant invasive behaviour. These results suggest that common generalist bumble bees might not always suffer from plant invasions, depending on their behavioural plasticity and nutritional requirements.

Is non‐host pollen suitable for generalist bumblebees?

Current evidence suggests that pollen is both chemically and structurally protected. Despite increasing interest in studying bee-flower networks, the constraints for bee development related to pollen nutritional content, toxicity and digestibility as well as their role in the shaping of bee-flower interactions have been poorly studied. In this study we combined bioassays of the generalist bee Bombus terrestris on pollen of Cirsium, Trifolium, Salix, and Cistus genera with an assessment of nutritional content, toxicity, and digestibility of pollen. Microcolonies showed significant differences in their development, non-host pollen of Cirsium being the most unfavorable. This pollen was characterized by the presence of quite rare δ7-sterols and a low digestibility. Cirsium consumption seemed increase syrup collection, which is probably related to a detoxification mixing behavior. These results strongly suggest that pollen traits may act as drivers of plant selection by bees and partly explain why Asteraceae pollen is rare in bee generalist diet.

Consequences of toxic secondary compounds in nectar for mutualistbees and antagonist butterflies.

Attraction of mutualists and defense against antagonists are critical challenges for most organisms and can be especially acute for plants with pollinating and non-pollinating flower visitors. Secondary compounds in flowers have been hypothesized to adaptively mediate attraction of mutualists and defense against antagonists, but this hypothesis has rarely been tested. The tissues of milkweeds (Asclepias spp.) contain toxic cardenolides that have long been studied as chemical defenses against herbivores. Milkweed nectar also contains cardenolides, and we have examined the impact of manipulating cardenolides in nectar on the foraging choices of two flower visitors: generalist bumble bees, Bombus impatiens, which are mutualistic pollinators, and specialist monarch butterflies, Danaus plexippus, which are herbivores as larvae and ineffective pollinators as adults. Although individual bumble bees in single foraging bouts showed no avoidance of cardenolides at the highest natural concentrations reported for milkweeds, a pattern of deterrence did arise when entire colonies were allowed to forage for several days. Monarch butterflies were not deterred by the presence of cardenolides in nectar when foraging from flowers, but laid fewer eggs on plants paired with cardenolide-laced flowers compared to controls. Thus, although deterrence of bumble bees by cardenolides may only occur after extensive foraging, a primary effect of nectar cardenolides appears to be reduction of monarch butterfly oviposition.

Impact of pollen resources drift on common bumblebees in NW Europe.

Several bee species are experiencing significant population declines. As bees exclusively rely on pollen for development and survival, such declines could be partly related to changes in their host plant abundance and quality. Here, we investigate whether generalist bumblebee species, with stable population trends over the past years, adapted their diets in response to changes in the distribution and chemical quality of their pollen resources. We selected five common species of bumblebee in NW Europe for which we had a precise description of their pollen diet through two time periods ('prior to 1950' and '2004-2005').For each species, we assessed whether the shift in their pollen diet was related with the changes in the suitable area of their pollen resources. Concurrently, we evaluated whether the chemical composition of pollen resources changed over time and experimentally tested the impact of new major pollen species on the development of B. terrestris microcolonies. Only one species (i.e. B. lapidarius) significantly included more pollen from resources whose suitable area expanded. This opportunist pattern could partly explain the expansion of B. lapidarius in Europe. Regarding the temporal variation in the chemical composition of the pollen diet, total and essential amino acid contents did not differ significantly between the two time periods while we found significant differences among plant species. This result is driven by the great diversity of resources used by bumblebee species in both periods. Our bioassay revealed that the shift to new major pollen resources allowed microcolonies to develop, bringing new evidence on the opportunist feature of bumblebee in their diets. Overall, this study shows that the response to pollen resource drift varies among closely related pollinators, and a species-rich plant community ensures generalist species to select a nutrient-rich pollen diet.

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

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.

Climate change decoupling mutualism

Evolutionary Ecology![Figure][1] Generalist bees replace specialists as climate warmsPHOTO: CANDACE GALEN 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][2] [1]: pending:yes [2]: /lookup/doi/10.1126/science.aab0868