- Proceedings of the National Academy of Sciences of the United States of America
- Published about 3 years ago
With more than 80% of flowering plant species specialized for animal pollination, understanding how wild pollinators utilize resources across environments can encourage efficient planting and maintenance strategies to maximize pollination and establish resilience in the face of environmental change. A fundamental question is how generalist pollinators recognize “flower objects” in vastly different ecologies and environments. On one hand, pollinators could employ a specific set of floral cues regardless of environment. Alternatively, wild pollinators could recognize an exclusive signature of cues unique to each environment or flower species. Hoverflies, which are found across the globe, are one of the most ecologically important alternative pollinators after bees and bumblebees. Here, we have exploited their cosmopolitan status to understand how wild pollinator preferences change across different continents. Without employing any a priori assumptions concerning the floral cues, we measured, predicted, and finally artificially recreated multimodal cues from individual flowers visited by hoverflies in three different environments (hemiboreal, alpine, and tropical) using a field-based methodology. We found that although “flower signatures” were unique for each environment, some multimodal lures were ubiquitously attractive, despite not carrying any reward, or resembling real flowers. While it was unexpected that cue combinations found in real flowers were not necessary, the robustness of our lures across insect species and ecologies could reflect a general strategy of resource identification for generalist pollinators. Our results provide insights into how cosmopolitan pollinators such as hoverflies identify flowers and offer specific ecologically based cues and strategies for attracting pollinators across diverse environments.
Pollination by insects is essential to many ecosystems. Previously, we have shown that floral scent is important to mediate pollen transfer between plants (Kessler et al., 2015). Yet, the mechanisms by which pollinators evaluate volatiles of single flowers remained unclear. Here, Nicotiana attenuata plants, in which floral volatiles have been genetically silenced and its hawkmoth pollinator, Manduca sexta, were used in semi-natural tent and wind-tunnel assays to explore the function of floral scent. We found that floral scent not only functions to increase the fitness of individual flowers by increasing detectability but also by enhancing the pollinator’s foraging efforts. Combining proboscis choice tests with neurophysiological, anatomical and molecular analyses we show that this effect is governed by newly discovered olfactory neurons on the tip of the moth’s proboscis. With the tip of their tongue, pollinators assess the advertisement of individual flowers, an ability essential for maintaining this important ecosystem service.
Pollinator-driven diversification is thought to be a major source of floral variation in plants. Our knowledge of this process is, however, limited to indirect assessments of evolutionary changes. Here, we employ experimental evolution with fast cycling Brassica rapa plants to demonstrate adaptive evolution driven by different pollinators. Our study shows pollinator-driven divergent selection as well as divergent evolution in plant traits. Plants pollinated by bumblebees evolved taller size and more fragrant flowers with increased ultraviolet reflection. Bumblebees preferred bumblebee-pollinated plants over hoverfly-pollinated plants at the end of the experiment, showing that plants had adapted to the bumblebees' preferences. Plants with hoverfly pollination became shorter, had reduced emission of some floral volatiles, but increased fitness through augmented autonomous self-pollination. Our study demonstrates that changes in pollinator communities can have rapid consequences on the evolution of plant traits and mating system.
Flowers use olfactory and visual signals to communicate with pollinators. Disentangling the relative contributions and potential synergies between signals remains a challenge. Understanding the perceptual biases exploited by floral mimicry illuminates the evolution of these signals. Here, we disentangle the olfactory and visual components of Dracula lafleurii, which mimics mushrooms in size, shape, color and scent, and is pollinated by mushroom-associated flies. To decouple signals, we used three-dimensional printing to produce realistic artificial flower molds that were color matched and cast using scent-free surgical silicone, to which we could add scent. We used GC-MS to measure scents in co-occurring mushrooms, and related orchids, and used these scents in field experiments. By combining silicone flower parts with real floral organs, we created chimeras that identified the mushroom-like labellum as a source of volatile attraction. In addition, we showed remarkable overlap in the volatile chemistry between D. lafleurii and co-occurring mushrooms. The characters defining the genus Dracula - a mushroom-like, ‘gilled’ labellum and a showy, patterned calyx - enhance pollinator attraction by exploiting the visual and chemosensory perceptual biases of drosophilid flies. Our techniques for the manipulation of complex traits in a nonmodel system not conducive to gene silencing or selective breeding are useful for other systems.
Pollinators serve critical roles for the functioning of terrestrial ecosystems, and have an estimated annual value of over $150 billion for global agriculture. Mounting evidence from agricultural systems reveals that pollinators are declining in many regions of the world, and with a lack of information on whether pollinator communities in natural systems are following similar trends, identifying factors which support pollinator visitation and services are important for ameliorating the effects of the current global pollinator crisis. We investigated how fire affects resource structure and how that variation influences floral pollinator communities by comparing burn versus control treatments in a southeastern USA old-field system. We hypothesized and found a positive relationship between fire and plant density of a native forb, Verbesina alternifolia, as well as a significant difference in floral visitation of V. alternifolia between burn and control treatments. V. alternifolia density was 44% greater and floral visitation was 54% greater in burned treatments relative to control sites. When the density of V. alternifolia was experimentally reduced in the burn sites to equivalent densities observed in control sites, floral visitation in burned sites declined to rates found in control sites. Our results indicate that plant density is a proximal mechanism by which an imposed fire regime can indirectly impact floral visitation, suggesting its usefulness as a tool for management of pollination services. Although concerns surround the negative impacts of management, indirect positive effects may provide an important direction to explore for managing future ecological and conservation issues. Studies examining the interaction among resource concentration, plant apparency, and how fire affects the evolutionary consequences of altered patterns of floral visitation are overdue.
Most woody plants are animal-pollinated, but the global problem of habitat fragmentation is changing the pollination dynamics. Consequently, the genetic diversity and fitness of the progeny of animal-pollinated woody plants sired in fragmented landscapes tend to decline due to shifts in plant-mating patterns (for example, reduced outcrossing rate, pollen diversity). However, the magnitude of this mating-pattern shift should theoretically be a function of pollinator mobility. We first test this hypothesis by exploring the mating patterns of three ecologically divergent eucalypts sampled across a habitat fragmentation gradient in southern Australia. We demonstrate increased selfing and decreased pollen diversity with increased fragmentation for two small-insect-pollinated eucalypts, but no such relationship for the mobile-bird-pollinated eucalypt. In a meta-analysis, we then show that fragmentation generally does increase selfing rates and decrease pollen diversity, and that more mobile pollinators tended to dampen these mating-pattern shifts. Together, our findings support the premise that variation in pollinator form contributes to the diversity of mating-pattern responses to habitat fragmentation.Heredity advance online publication, 4 September 2013; doi:10.1038/hdy.2013.48.
Floral colour change is visual signals for pollinators to avoid old flowers and increase pollination efficiency. Quisqualis indica flowers change colour from white to pink to red may be associated with a shift from moth to butterfly pollination. To test this hypothesis, we investigated Q. indica populations in Southwest China. Flowers secreted nectar continuously from the evening of anthesis until the following morning, then decreased gradually with floral colour change. The scent compounds in the three floral colour stages were similar; however, the scent composition was different, and the scent emission rate decreased from the white to red stage. Dichogamy in Q. indica prevents self-pollination and interference of male and female functions. Controlled pollinations demonstrated that this species is self-incompatible and needs pollinators for seed production. Different pollinators were attracted in each floral colour stage; mainly moths at night and bees and butterflies during the day. Observations of open-pollinated inflorescences showed that white flowers had a higher fruit set than pink or red flowers, indicating the high contribution of moths to reproductive success. We concluded that the nectar and scent secretion are related to floral colour change in Q. indica, in order to attract different pollinators and promote reproductive fitness.
Several neotropical orchid genera have been proposed as being sexually deceptive; however, this has been carefully tested in only a few cases. The genus Telipogon has long been assumed to be pollinated by male tachinid flies during pseudocopulatory events but no detailed confirmatory reports are available. Here, we have used an array of methods to elucidate the pollination mechanism in Telipogon peruvianus. The species presents flowers that have a mean floral longevity of 33 days and that are self-compatible, although spontaneous self-pollination does not occur. The flowers attract males of four tachinid species but only the males of an undescribed Eudejeania (Eudejeania aff. browni; Tachinidae) species are specific pollinators. Males visit the flowers during the first few hours of the day and the pollination success is very high (42% in one patch) compared with other sexually deceptive species. Female-seeking males are attracted to the flowers but do not attempt copulation with the flowers, as is usually described in sexually deceptive species. Nevertheless, morphological analysis and behavioural tests have shown an imperfect mimicry between flowers and females suggesting that the attractant stimulus is not based only on visual cues, as long thought. Challenging previous conclusions, our chemical analysis has confirmed that flowers of Telipogon release volatile compounds; however, the role of these volatiles in pollinator behaviour remains to be established. Pollinator behaviour and histological analyses indicate that Telipogon flowers possess scent-producing structures throughout the corolla. Our study provides the first confirmed case of (i) a sexually deceptive species in the Onciidinae, (ii) pollination by pre-copulatory behaviour and (iii) pollination by sexual deception involving tachinid flies.
Angiosperms have evolved multiple breeding systems that allow reproductive success under varied conditions. Striking among these are cleistogamous breeding systems, where individuals can produce alternative flower types specialized for distinct mating strategies. Cleistogamy is thought to be environmentally-dependent, but little is known about environmental triggers. If production of alternate flowers is environmentally induced, populations may evolve locally adapted responses. Mimulus douglasii, exhibits a cleistogamous breeding system, and ranges across temperature and day-length gradients, providing an ideal system to investigate environmental parameters that control cleistogamy.
Animal pollination, essential for both ecological services and ecosystem functioning, is threatened by ongoing global changes. New methodologies to decipher their effects on pollinator composition to ecosystem health are urgently required. We compare the main structural parameters of pollination networks based on DNA metabarcoding data with networks based on direct observations of insect visits to plants at three resolution levels. By detecting numerous additional hidden interactions, metabarcoding data largely alters the properties of the pollination networks compared to visit surveys. Molecular data shows that pollinators are much more generalist than expected from visit surveys. However, pollinator species were composed of relatively specialized individuals and formed functional groups highly specialized upon floral morphs. We discuss pros and cons of metabarcoding data relative to data obtained from traditional methods and their potential contribution to both current and future research. This molecular method seems a very promising avenue to address many outstanding scientific issues at a resolution level which remains unattained to date; especially for those studies requiring pollinator and plant community investigations over macro-ecological scales.