skip to main content

Title: The dispersal of microbes among and within flowers by butterflies

Floral microbes, including bacteria and fungi, alter nectar quality, thus changing pollinator visitation. Conversely, pollinator visitation can change the floral microbial community.

Most studies on dispersal of floral microbes have focused on bees, ants or hummingbirds, yet Lepidoptera are important pollinators.

We asked (a) where are microbes present on the butterfly body, (b) do butterflies transfer microbes while foraging, and (c) how does butterfly foraging affect microbial abundance on different floret structures.

The tarsi and proboscis had significantly more microbes than the thorax in wild‐caughtGlaucopsyche lygdamus(Lepidoptera: Lycaenidae) andSpeyeria mormonia(Lepidoptera: Nymphalidae).Glaucopsyche lygdamus, a smaller‐bodied species, had fewer microbes thanS. mormonia.

As a marker for microbes, we used a bacterium (Rhodococcus fascians,near NCBI Y11196) isolated from aS. mormoniathat was foraging for nectar, and examined its dispersal byG. lygdamusandS. mormoniavisiting florets ofPyrrocoma crocea(Asteraceae). Microbial dispersal among florets correlated positively with bacterial abundance in the donor floret. Dispersal also depended on butterfly species, age, and bacterial load carried by the butterfly.

Recipient florets had less bacteria than donor florets. The nectaries had more bacteria than the anthers or the stigmas, while anthers and stigmas did not differ from each other. There was no differential transmission among floral organs.

Lepidoptera thus act as vectors of floral microbes. Including Lepidoptera is thus crucial to an understanding of plant–pollinator–microbe interactions. Future studies should consider the role of vectored microbes in lepidopteran ecology and fitness.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
Ecological Entomology
Page Range / eLocation ID:
p. 458-465
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Floral nectar contains microbes that can influence nectar chemistry and pollinator visitation, and these microbial communities can be affected by pollinators in turn. Some flowers are also visited by nectar robbers, which feed on nectar through holes cut in floral tissue. If nectar robbers alter nectar microbial communities, they might have unexpected impacts on pollinator visitation. We investigated whether robbing could affect nectar microbial communities directly, by introducing microbes, or indirectly, by triggering a plant response to floral damage. We applied four treatments to flowers ofTecoma× “Orange Jubilee” (Bignoniaceae) in an arboretum setting: flowers were (1) covered to exclude all visitors; (2) available to both pollinators and nectar robbers and robbed naturally by carpenter bees; (3) available to pollinators only but cut at the base to simulate nectar robbing damage; or (4) available to pollinators only. We found that nectar in flowers accessible to any visitors was more likely to contain culturable microbes than flowers from which visitors were excluded. Microbial community composition and beta diversity were similar across treatments. Among flowers containing culturable microbes, flowers available to pollinators and nectar robbers had higher microbial abundance than flowers with simulated robbing, but there were no differences between flowers available to pollinators and robbers and unwounded flowers from which robbers were excluded. Overall, our results suggest that floral damage can affect some features of nectar microbial communities, but specific effects of nectar robbing are limited compared with the influence of visitation in general.

    more » « less
  2. Summary

    Epiphytic microbes frequently affect plant phenotype and fitness, but their effects depend on microbe abundance and community composition. Filtering by plant traits and deterministic dispersal‐mediated processes can affect microbiome assembly, yet their relative contribution to predictable variation in microbiome is poorly understood.

    We compared the effects of host‐plant filtering and dispersal on nectar microbiome presence, abundance, and composition. We inoculated representative bacteria and yeast into 30 plants across four phenotypically distinct cultivars ofEpilobium canum. We compared the growth of inoculated communities to openly visited flowers from a subset of the same plants.

    There was clear evidence of host selection when we inoculated flowers with synthetic communities. However, plants with the highest microbial densities when inoculated did not have the highest microbial densities when openly visited. Instead, plants predictably varied in the presence of bacteria, which was correlated with pollen receipt and floral traits, suggesting a role for deterministic dispersal.

    These findings suggest that host filtering could drive plant microbiome assembly in tissues where species pools are large and dispersal is high. However, deterministic differences in microbial dispersal to hosts may be equally or more important when microbes rely on an animal vector, dispersal is low, or arrival order is important.

    more » « less
  3. Abstract

    Nectar scents are thought to function as honest signals of reward used by pollinators, but this hypothesis has rarely been tested.

    UsingPenstemon digitalis, we examined honest signalling of the nectar volatile (S)‐(+)‐linalool and pollinator responses to linalool in both field and laboratory settings. Because our previous work showed that linalool emission was associated with higher female fitness and that nectar is scented with linalool, we hypothesized that linalool was an honest signal of nectar reward. To assess honesty, we measured linalool–nectar associations including nectar volume, sugar amount, concentration and production rate for inflorescences and flowers in several populations. We also assessed whetherBombus impatiens, the main pollinator ofP. digitalisat our sites, can use linalool as a foraging signal. We supplemented real or artificial flowers in the field and laboratory with varying linalool–nectar combinations to measure pollinator behavioural responses.

    We found that an inflorescence's linalool emissions could be used to predict nectar rewards inP. digitalis, but this was driven by indirect associations with display size rather than directly advertising more profitable flowers. For flowers within inflorescences there was also no evidence for an association between signal and reward. Field tests of bumblebee behaviour were inconclusive. However, in laboratory assays, bumblebees generally used variation in linalool emissions to choose more profitable flowers, demonstrating they can detect differences in linalool emitted byP. digitalisand associate them with reward profitability. These results suggest experiments that decouple display size, scent and reward are necessary to assess whether (and when) bees prefer higher linalool emissions. Bees preferred nectars with lower linalool concentrations when linalool flavoured the nectar solution, suggesting the potential for conflicting pressures on scent emission in the field.

    Synthesis. Our results highlight the challenges of assessing function for traits important to fitness and suggest that the perception of floral signalling honesty may depend on whether pollinators use inflorescences or flowers within inflorescences when making foraging decisions. We conclude that future research on honest signalling in flowering plants, as well as its connection to phenotypic selection, should explicitly define honesty, in theoretical and experimental contexts.

    more » « less
  4. 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
  5. Floral nectar is prone to colonization by nectar-adapted yeasts and bacteria via air-, rain-, and animal-mediated dispersal. Upon colonization, microbes can modify nectar chemical constituents that are plant-provisioned or impart their own through secretion of metabolic by-products or antibiotics into the nectar environment. Such modifications can have consequences for pollinator perception of nectar quality, as microbial metabolism can leave a distinct imprint on olfactory and gustatory cues that inform foraging decisions. Furthermore, direct interactions between pollinators and nectar microbes, as well as consumption of modified nectar, have the potential to affect pollinator health both positively and negatively. Here, we discuss and integrate recent findings from research on plant–microbe–pollinator interactions and their consequences for pollinator health. We then explore future avenues of research that could shed light on the myriad ways in which nectar microbes can affect pollinator health, including the taxonomic diversity of vertebrate and invertebrate pollinators that rely on this reward. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’. 
    more » « less