skip to main content

Title: Skewness in bee and flower phenological distributions

Phenological distributions are characterized by their central tendency, breadth, and shape, and all three determine the extent to which interacting species overlap in time. Pollination mutualisms rely on temporal co‐occurrence of pollinators and their floral resources, and although much work has been done to characterize the shapes of flower phenological distributions, similar studies that include pollinators are lacking. Here, we provide the first broad assessment of skewness, a component of distribution shape, for a bee community. We compare skewness in bees to that in flowers, relate bee and flower skewness to other properties of their phenology, and quantify the potential consequences of differences in skewness between bees and flowers. Both bee and flower phenologies tend to be right‐skewed, with a more exaggerated asymmetry in bees. Early‐season species tend to be the most skewed, and this relationship is also stronger in bees than in flowers. Based on a simulation experiment, differences in bee and flower skewness could account for up to 14% of pairwise overlap differences. Given the potential for interaction loss, we argue that difference in skewness of interacting species is an underappreciated property of phenological change.

more » « less
Award ID(s):
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Climate change is shifting the environmental cues that determine the phenology of interacting species. Plant–pollinator systems may be susceptible to temporal mismatch if bees and flowering plants differ in their phenological responses to warming temperatures. While the cues that trigger flowering are well‐understood, little is known about what determines bee phenology. Using generalised additive models, we analyzed time‐series data representing 67 bee species collected over 9 years in the Colorado Rocky Mountains to perform the first community‐wide quantification of the drivers of bee phenology. Bee emergence was sensitive to climatic variation, advancing with earlier snowmelt timing, whereas later phenophases were best explained by functional traits including overwintering stage and nest location. Comparison of these findings to a long‐term flower study showed that bee phenology is less sensitive than flower phenology to climatic variation, indicating potential for reduced synchrony of flowers and pollinators under climate change.

    more » « less
  2. Abstract

    Human‐mediated species introductions provide real‐time experiments in how communities respond to interspecific competition. For example, managed honey beesApis mellifera(L.) have been widely introduced outside their native range and may compete with native bees for pollen and nectar. Indeed, multiple studies suggest that honey bees and native bees overlap in their use of floral resources. However, for resource overlap to negatively impact resource collection by native bees, resource availability must also decline, and few studies investigate impacts of honey bee competition on native bee floral visits and floral resource availability simultaneously.

    In this study, we investigate impacts of increasing honey bee abundance on native bee visitation patterns, pollen diets, and nectar and pollen resource availability in two Californian landscapes: wildflower plantings in the Central Valley and montane meadows in the Sierra.

    We collected data on bee visits to flowers, pollen and nectar availability, and pollen carried on bee bodies across multiple sites in the Sierra and Central Valley. We then constructed plant‐pollinator visitation networks to assess how increasing honey bee abundance impacted perceived apparent competition (PAC), a measure of niche overlap, and pollinator specialization (d'). We also compared PAC values against null expectations to address whether observed changes in niche overlap were greater or less than what we would expect given the relative abundances of interacting partners.

    We find clear evidence of exploitative competition in both ecosystems based on the following results: (1) honey bee competition increased niche overlap between honey bees and native bees, (2) increased honey bee abundance led to decreased pollen and nectar availability in flowers, and (3) native bee communities responded to competition by shifting their floral visits, with some becoming more specialized and others becoming more generalized depending on the ecosystem and bee taxon considered.

    Although native bees can adapt to honey bee competition by shifting their floral visits, the coexistence of honey bees and native bees is tenuous and will depend on floral resource availability. Preserving and augmenting floral resources is therefore essential in mitigating negative impacts of honey bee competition. In two California ecosystems, honey bee competition decreases pollen and nectar resource availability in flowers and alters native bee diets with potential implications for bee conservation and wildlands management.

    more » « less
  3. Abstract

    Floral odours play an important role in attracting insect pollinators. Because pollinators visit flowers to obtain pollen and nectar rewards, they should prefer floral odour profiles associated with the highest‐rewarding flowers (honest signals). In previous work, bumblebees exhibited a preference for flowers from outbred over inbredMimulus guttatusplants. Pollen is the only floral reward inM. guttatus, and pollen viability (a reliable indicator of protein content) is reduced in inbred plants. Yet, differences in pollen viability did not explain the observed preferences.

    In this study, we examined the floral volatile profiles of inbred and outbredM. guttatusto identify inbreeding effects and associations between volatile compounds and the number of viable pollen grains per flower, designated “PRQ” (pollen reward quality). We also conducted pairwise choice tests withBombus impatiensto evaluate the ability of bees to discriminate between odours of rewarding and non‐rewarding flowers and to determine whether bumblebee preferences are explained by differences in the floral odours of inbred and outbred plants.

    Inbred plants exhibited reduced emission of β‐trans‐bergamotene, the second‐most abundant compound in the volatile blend of outbred plants. Furthermore, pollen and fertile anthers emitted nonadecane. Six other compounds in the floral blend were positively correlated withPRQ. There was no overlap between compounds affected by inbreeding and compounds associated withPRQ.

    Even when given prior experience foraging onM. guttatus, bumblebees did not distinguish between the floral odours of rewarding and non‐rewarding outbred plants. However, they preferred floral odours from non‐rewarding outbred plants over rewarding inbred plants. Bumblebees without prior experience of flowers preferred volatile blends with higher versus lower amounts of β‐trans‐bergamotene.

    Taken together, these results suggest that the volatile emissions ofM. guttatusprovide reliable indicators of pollen rewards (potential honest signals), but that the preference of bumblebees for outbred plants is not driven by these cues but rather by a sensory bias for β‐trans‐bergamotene. This may represent a subtle form of deceit‐pollination that allows plants to attract pollinators while minimizing investment in costly rewards.

    Aplain language summaryis available for this article.

    more » « less
  4. Abstract

    Vairimorpha (=Nosema) ceranaeis a widespread pollinator parasite that commonly infects honeybees and wild pollinators, including bumblebees. Honeybees are highly competentV. ceranaehosts and previous work in experimental flight cages suggestsV. ceranaecan be transmitted during visitation to shared flowers. However, the relationship between floral visitation in the natural environment and the prevalence ofV. ceranaeamong multiple bee species has not been explored. Here, we analyzed the number and duration of pollinator visits to particular components of squash flowers—including the petals, stamen, and nectary—at six farms in southeastern Michigan, USA. We also determined the prevalence ofV. ceranaein honeybees and bumblebees at each site. Our results showed that more honeybee flower contacts and longer duration of contacts with pollen and nectar were linked with greaterV. ceranaeprevalence in bumblebees. Honeybee visitation patterns appear to have a disproportionately large impact onV. ceranaeprevalence in bumblebees even though honeybees are not the most frequent flower visitors. Floral visitation by squash bees or other pollinators was not linked withV. ceranaeprevalence in bumblebees. Further,V. ceranaeprevalence in honeybees was unaffected by floral visitation behaviors by any pollinator species. These results suggest that honeybee visitation behaviors on shared floral resources may be an important contributor to increasedV. ceranaespillover to bumblebees in the field. Understanding howV. ceranaeprevalence is influenced by pollinator behavior in the shared floral landscape is critical for reducing parasite spillover into declining wild bee populations.

    more » « less
  5. Abstract Aim

    Most of the world's food crops are dependent on pollinators. However, there is a great deal of uncertainty in the strength of this relationship, especially regarding the relative contributions of the honey bee (often a managed species) and wild insects to crop yields on a global scale. Previous data syntheses have likewise reached differing conclusions on whether pollinator species diversity, or only the number of pollinator visits to flowers, is important to crop yield. This study quantifies the current state of these relationships and links to a dynamic version of our analyses that updates automatically as studies become available.



    Time Period


    Taxa studied

    Insect pollinators of global crops.


    Using a newly created database of 93 crop pollination studies across six continents that roughly triples the number of studies previously available, we analysed the relationship between insect visit rates, pollinator diversity, and crop yields in a series of mixed‐effects models.


    We found that honey bees and wild insects contribute roughly equal amounts to crop yields worldwide, having similar average flower visitation rates and producing similar increases in yield per visit. We also found that pollinator species diversity was positively associated with increased crop yields even when total visits from all species are accounted for, though it was less explanatory than the total number of visits itself.

    Main conclusions

    Our analysis suggests a middle ground where honey bees are not responsible for the vast majority of crop pollination as has often been assumed in the agricultural literature, and likewise wild insects are not vastly more important than honey bees, as recent global analyses have reported. We also conclude that while pollinator diversity is less important than the number of pollinator visits, these typically involve many species, underscoring the importance of conserving a diversity of wild pollinators.

    more » « less