Concept: Pollination syndrome
Pollinating insects utilise various sensory cues to identify and learn rewarding flower species. One such cue is floral temperature, created by captured sunlight or plant thermogenesis. Bumblebees, honeybees and stingless bees can distinguish flowers based on differences in overall temperature between flowers. We report here that floral temperature often differs between different parts of the flower creating a temperature structure or pattern. Temperature patterns are common, with 55% of 118 plant species thermographed, showing within-flower temperature differences greater than the 2°C difference that bees are known to be able to detect. Using differential conditioning techniques, we show that bumblebees can distinguish artificial flowers differing in temperature patterns comparable to those seen in real flowers. Thus, bumblebees are able to perceive the shape of these within-flower temperature patterns. Floral temperature patterns may therefore represent a new floral cue that could assist pollinators in the recognition and learning of rewarding flowers.
Many plants defend themselves against herbivores by chemical deterrents in their tissues and the presence of such substances in floral nectar means that pollinators often encounter them when foraging. The effect of such substances on the foraging behaviour of pollinators is poorly understood. Using artificial flowers in tightly-controlled laboratory settings, we examined the effects of the alkaloid nicotine on bumblebee foraging performance. We found that bumblebees confronted simultaneously with two equally rewarded nicotine-containing and nicotine-free flower types are deterred only by unnaturally high nicotine concentrations. This deterrence disappears or even turns into attraction at lower nectar-relevant concentrations. The alkaloid has profound effects on learning in a dose-dependent manner. At a high natural dose, bees learn the colour of a nicotine-containing flower type more swiftly than a flower type with the same caloric value but without nicotine. Furthermore, after experiencing flowers containing nicotine in any tested concentration, increasing numbers of bumblebees stay more faithful to these flowers, even if they become a suboptimal choice in terms of reward. These results demonstrate that alkaloids enhance pollinator flower constancy, opening new perspectives in co-evolutionary process between plants and pollinators.
Pollinators, such as bees, often develop multi-location routes (traplines) to exploit subsets of flower patches within larger plant populations. How individuals establish such foraging areas in the presence of other foragers is poorly explored. Here we investigated the foraging patterns of pairs of bumble bees (Bombus terrestris) released sequentially into an 880m2 outdoor flight cage containing 10 feeding stations (artificial flowers). Using motion-sensitive video cameras mounted on flowers, we mapped the flower visitation networks of both foragers, quantified their interactions and compared their foraging success over an entire day. Overall, bees that were released first (residents) travelled 37% faster and collected 77% more nectar, thereby reaching a net energy intake rate 64% higher than bees released second (newcomers). However, this prior-experience advantage decreased as newcomers became familiar with the spatial configuration of the flower array. When both bees visited the same flower simultaneously, the most frequent outcome was for the resident to evict the newcomer. On the rare occasions when newcomers evicted residents, the two bees increased their frequency of return visits to that flower. These competitive interactions led to a significant (if only partial) spatial overlap between the foraging patterns of pairs of bees. While newcomers may initially use social cues (such as olfactory footprints) to exploit flowers used by residents, either because such cues indicate higher rewards and/or safety from predation, residents may attempt to preserve their monopoly over familiar resources through exploitation and interference. We discuss how these interactions may favour spatial partitioning, thereby maximising the foraging efficiency of individuals and colonies.
Geographically structured phenotypic selection can lead to adaptive divergence. However, in flowering plants, such divergent selection has rarely been shown, and selection on floral signals is generally little understood. In this study, we measured phenotypic selection on display size, floral color, and floral scent in four lowland and four mountain populations of the nectar-rewarding terrestrial orchid Gymnadenia odoratissima in two years. We also quantified population differences in these traits and pollinator community composition. Our results show positive selection on display size and positive, negative, or absence of selection on different scent compounds and floral color. Selection on the main scent compounds was consistently stronger in the lowlands than in the mountains, and lowland plants emitted higher amounts of most of these compounds. Pollinator community composition also differed between regions, suggesting different pollinators select for differences in floral volatiles. Overall, our study is the first to document consistent regional differences in selection on floral scent, suggesting this pattern of selection is one of the evolutionary forces contributing to regional divergence in floral chemical signaling.
Iridescence is a form of structural coloration, produced by a range of structures, in which hue is dependent on viewing angle [1-4]. One of these structures, the diffraction grating, is found both in animals (for example, beetles ) and in plants (on the petals of some animal pollinated flowers ). The behavioral impacts of floral iridescence and its potential ecological significance are unknown [6-9]. Animal-pollinated flowers are described as “sensory billboards” , with many floral features contributing to a conspicuous display that filters prospective pollinators. Yet floral iridescence is more subtle to the human eye than that of many animal displays because the floral diffraction grating is not perfectly regular [5-9]. This presents a puzzle: if the function of petals is to attract pollinators, then flowers might be expected to optimize iridescence to increase showiness. On the other hand, pollinators memorize floral colors as consistent advertisements of reward quality, and iridescence might corrupt flower color identity. Here we tested the trade-off between flower detectability and recognition, requiring bumblebees (Bombus terrestris) to identify artificial flowers that varied in pigmentation and degree of iridescence. We find that iridescence does increase target detectability but that "perfect" iridescence (produced by an artificial diffraction grating) corrupts target identity and bees make many mistakes. However, “imperfect” floral iridescence does not lead to mistaken target identity, while still benefitting flower detectability. We hypothesize that similar trade-offs might be found in the many naturally "imperfect" iridescence-producing structures found in animal-animal, as well as other plant-animal, interactions.
Cost efficient foraging is of especial importance for animals like hawkmoths or hummingbirds that are feeding ‘on the wing’, making their foraging energetically demanding. The economic decisions made by these animals have a strong influence on the plants they pollinate and floral volatiles are often guiding these decisions. Here we show that the hawkmoth Manduca sexta exhibits an innate preference for volatiles of those Nicotiana flowers, which match the length of the moth’s proboscis. This preference becomes apparent already at the initial inflight encounter, with the odour plume. Free-flight respiration analyses combined with nectar calorimetry revealed a significant caloric gain per invested flight energy only for preferred-matching-flowers. Our data therefore support Darwin’s initial hypothesis on the coevolution of flower length and moth proboscis. We demonstrate that this interaction is mediated by an adaptive and hardwired olfactory preference of the moth for flowers offering the highest net-energy reward.
Many plants attract and reward pollinators with floral scents and nectar, respectively, but these traits can also incur fitness costs as they also attract herbivores. This dilemma, common to most flowering plants, could be solved by not producing nectar and/or scent, thereby cheating pollinators. Both nectar and scent are highly variable in native populations of coyote tobacco, Nicotiana attenuata, with some producing no nectar at all, uncorrelated with the tobacco’s main floral attractant, benzylacetone. By silencing benzylacetone biosynthesis and nectar production in all combinations by RNAi, we experimentally uncouple these floral rewards/attractrants and measure their costs/benefits in the plant’s native habitat and experimental tents. Both scent and nectar increase outcrossing rates for three, separately-tested, pollinators and both traits increase oviposition by a hawkmoth herbivore, with nectar being more influential than scent. These results underscore that it makes little sense to study floral traits as if they only mediated pollination services.
Four to six percent of plants, distributed over different angiosperm families, entice pollinators by deception . In these systems, chemical mimicry is often used as an efficient way to exploit the olfactory preferences of animals for the purpose of attracting them as pollinators [2,3]. Here, we report a very specific type of chemical mimicry of a food source. Ceropegia sandersonii (Apocynaceae), a deceptive South African plant with pitfall flowers, mimics attacked honeybees. We identified kleptoparasitic Desmometopa flies (Milichiidae) as the main pollinators of C. sandersonii. These flies are well known to feed on honeybees that are eaten by spiders, which we thus predicted as the model chemically mimicked by the plant. Indeed, we found that the floral scent of C. sandersonii is comparable to volatiles released from honeybees when under simulated attack. Moreover, many of these shared compounds elicited physiological responses in antennae of pollinating Desmometopa flies. A mixture of four compounds-geraniol, 2-heptanone, 2-nonanol, and (E)-2-octen-1-yl acetate-was highly attractive to the flies. We conclude that C. sandersonii is specialized on kleptoparasitic fly pollinators by deploying volatiles linked to the flies' food source, i.e., attacked and/or freshly killed honeybees. The blend of compounds emitted by C. sandersonii is unusual among flowering plants and lures kleptoparasitic flies into the trap flowers. This study describes a new example of how a plant can achieve pollination through chemical mimicry of the food sources of adult carnivorous animals.
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.