Flower Constancy Research Articles

Insect pollinators show constancy for different flower traits between the most‐ and less‐preferred plants: a case study of the long‐proboscid tangle‐veined fly

The coevolution of insect pollinators and their host plants is a typical example of natural selection; however, how insect pollinators avoid overdependence on one peculiar plant remains unclear. As most insect pollinators exhibit a diet breadth when showing flower constancy, determining the difference and similarity of most and less preferred flowers by insect pollinators may be helpful to understand their trade‐off between flower constancy and overdependence. This was addressed using the long‐proboscid tangle‐veined fly (Nemetrinus spp.). Dietary investigation indicates that the flies show constancy for the morphological characteristic of the Delphinium caeruleum, which is the most preferred plant for this Nemestrinidae fly that has blue, long‐tubed flowers. In a colour selection experiment, focal individuals showed obvious preference for white, which is the colour of less preferred flowers by the fly in the natural environment. In a scent selection experiment, focal individuals showed obvious preference for D. caeruleum and Dracocephalum heterophyllum but avoidance to Dasiphora fruticosa and Dasiphora davurica. This indicates that long‐proboscid tangle‐veined flies can forage on other flowers, despite the existing constancy for D. caeruleum, as long as they do not hate the scent. It seems that long‐proboscid tangle‐veined flies can maximise foraging efficiency by showing constancy for the morphological characteristic of the most preferred plant and for the scent and colour of less‐preferred plants. The trade‐off of long‐proboscid tangle‐veined flies in the selection of nectar sources may be an adaptation to the risk of overdependence on one plant in evolution.

Pollinator effectiveness of a specialist bee exploiting a generalist plant\u2014tracking pollen transfer by Heriades truncorum with quantum dots

Heriades truncorum (Megachilidae) is a specialist bee that forages on Asteraceae and collects pollen by tapping its abdomen on pollen-presenting florets which places the grains directly in the ventral scopa. We tracked pollen transfer by female H. truncorum between conspecific inflorescences of Inula ensifolia and Pulicaria dysenterica by labelling pollen with quantum dots. On average, bees transferred 31.14 (I. ensifolia) and 9.96 (P. dysenterica) pollen grains from the last visited inflorescence, 39% and 45% of which were placed on receptive styles. Pollen germination ratio is significantly lower for inflorescences of P. dysenterica visited by one H. truncorum (0.13%) compared with open control inflorescences (0.51%), which suggests that the bees mainly transfer self-pollen of these self-incompatible plants. Thus, a single visit by H. truncorum does not grant the plant high reproductive success, but the bees’ abundance and flower constancy might reduce this disadvantage.

Flower colour segregation and flower discrimination under the bee vision model in the polymorphic Lysimachia arvensis

Floral colour determines pollinator behaviour, strongly affecting plant-mating systems. Lysimachia arvensis has blue- and red-flowered plants and colour inheritance remains largely unknown. A control of floral colour based on one locus, with the red allele as dominant, has been proposed. This proposal cannot explain the sporadic appearance of other floral colours in wild populations. We studied floral colour segregation in L. arvensis and assessed the possibility that pollinators can visually distinguish colour morphs by using Chittka’s hexagon model, sigmoidal model of bee discrimination and experimental studies on pollinator attendance for two years. Hand crossing between morphs originated a homogeneous F1 with salmon-coloured flowers. In the F2, blue, red, salmon morphs and other plants with intermediate colours appeared, suggesting that more than one single locus are involved in colour segregation. Results from the sigmoidal discrimination model suggest that blue, red and salmon flowers can be discriminated by pollinators. In fact, pollinators showed strong colour constancy and discriminated against the salmon morph. Our study shows that “Flower colour” is a natural marker to assess the rate of crossing between morphs. The extreme rarity of salmon flowers in wild populations and flower constancy of L. arvensis pollinators indicates assortative mating.

Exploiting flower constancy in flower pollination algorithm: improved biotic flower pollination algorithm and its experimental evaluation

Recent growth of metaheuristic search strategies has brought a huge progress in the domain of computational optimization. The breakthrough started since the well-known Particle Swarm Optimization algorithm had been introduced and examined. Optimization technique presented in this contribution mimics the process of flower pollination. It is build on the foundation of the first technique of this kind—known as Flower Pollination Algorithm (FPA). In this paper, its simplified and improved version, obtained after extensive performance testing, is presented. It is based on only one natural phenomena—called flower constancy—the natural mechanism allowing pollen carrying insects to remember the positions of the best pollen sources. Modified FPA, named as Biotic Flower Pollination Algorithm (BFPA) and relying solely on biotic pollinators, outperforms original FPA, which itself proved to be very effective approach. The paper first presents a short description of original FPA and the changes leading to Biotic Flower Pollination Algorithm. It also discusses performance of the modified algorithm on a full set of CEC17 benchmark functions. Furthermore, in that aspect, the comparison between BFPA and other optimization algorithms is also given. Finally, brief exemplary application of modified algorithm in the field of probabilistic modeling, related to physics and engineering, is also presented.

Appetitive reversal learning differences of two honey bee subspecies with different foraging behaviors.

We aimed to examine mechanistically the observed foraging differences across two honey bee, Apis mellifera, subspecies using the proboscis extension response assay. Specifically, we compared differences in appetitive reversal learning ability between honey bee subspecies: Apis mellifera caucasica (Pollman), and Apis mellifera syriaca (Skorikov) in a “common garden” apiary. It was hypothesized that specific learning differences could explain previously observed foraging behavior differences of these subspecies: A.m. caucasica switches between different flower color morphs in response to reward variability, and A.m. syriaca does not switch. We suggest that flower constancy allows reduced exposure by minimizing search and handling time, whereas plasticity is important when maximizing harvest in preparation for long winter is at a premium. In the initial or Acquisition phase of the test we examined specifically discrimination learning, where bees were trained to respond to a paired conditioned stimulus with an unconditioned stimulus and not to respond to a second conditioned stimulus that is not followed by an unconditioned stimulus. We found no significant differences among the subspecies in the Acquisition phase in appetitive learning. During the second, Reversal phase of the experiment, where flexibility in association was tested, the paired and unpaired conditioned stimuli were reversed. During the Reversal phase A.m. syriaca showed a reduced ability to learn the reverse association in the appetitive learning task. This observation is consistent with the hypothesis that A.m. syriaca foragers cannot change the foraging choice because of lack of flexibility in appetitive associations under changing contingencies. Interestingly, both subspecies continued responding to the previously rewarded conditioned stimulus in the reversal phase. We discuss potential ecological correlates and molecular underpinnings of these differences in learning across the two subspecies. In addition, in a supplemental experiment we demonstrated that these differences in appetitive reversal learning do not occur in other learning contexts.

Tasting the unexpected: disconfirmation of expectations leads to lower perceived food value in an invertebrate.

To make sensible decisions, both humans and other animals must compare the available options against a reference point-either other options or previous experience. Options of higher quality than the reference are considered good value. However, many perceptible attributes of options are value-neutral, such as flower scent. Nonetheless, such value-neutral differences may be part of an expectation. Can a mismatch between the expectation and experience of value-neutral attributes affect perceived value? Consumer psychology theory and results suggest it can. To test this in a non-human animal, we manipulated a value-neutral aspect of a food source-its taste-while keeping its absolute value-its sweetness-the same. Individual ants (Lasius niger) were allowed to drink either lemon- or rosemary-flavoured 1 M sucrose. After three successive visits to the food, we switched the taste in the last, fourth, visit to induce a disconfirmation of expectations. In control trials, ants received the same taste on all four visits. Disconfirmed ants showed lower food acceptance and laid less pheromone on the way back to the nest, even though the molarity of the food was unchanged. As ants recruit nest-mates via pheromone depositions, fewer depositions indicate that the ants valued the food less. Thus, an expectation of value-neutral attributes can influence the perceived value of a resource. Such influences of value-neutral variables on value perception may affect how animals interact with and exploit their environment, and may contribute to phenomena such as flower constancy.

Biosynthetic and Functional Color–Scent Associations in Flowers of Papaver nudicaule and Their Impact on Pollinators

Despite increasing evidence for biosynthetic connections between flower pigments and volatile compounds, examples of such relationships in polymorphic plant species remains limited. Herein, color-scent associations in flowers from Papaver nudicaule (Papaveraceae) have been investigated. The spectral reflectance and scent composition of flowers of four color cultivars was determined. We found that pigments and volatiles occur in specific combinations in flowers of P. nudicaule. The presence of indole in the bouquets is strongly associated with the occurrence of yellow pigments called nudicaulins, for which indole is one of the final biosynthetic precursors. Whereas yellow flowers emit an excess of indole, orange flowers consume it during nudicaulin production and lack the substance in their bouquet. By using the honeybee, Apis mellifera, evaluations were made on how color and scent affect the discrimination of these flowers by pollinators. Honeybees were able to discriminate artificial odor mixtures resembling those of the natural flower odors. Bees trained with stimuli combining colors and odors showed an improved discrimination performance. The results indicate that the indole moiety of nudicaulins and emitted indole might be products of the same biochemical pathway. We propose that conserved pathways account for the evolution of color-scent associations in P. nudicaule and that these associations positively affect flower constancy of pollinators.

Floral preferences of hoverflies (Diptera: Syrphidae) in response to the abundance and species richness of flowering plants

For understanding the relationship between floral resources and the abundance of hoverflies, five meadows were selected at different elevations in a forested region. At each site the number of flowering herbaceous plants was assessed along a transect at 10-m intervals. To measure floral density, we counted the number of open flowers per species in each plot. Hoverflies visiting flowering plants were captured in each plot during 10 minutes. Path analysis showed that there was a negative correlation between plant species richness and syrphid abundance. Flower abundance had a strong positive direct effect on syrphid abundance but had indirect effects on the number of syrphid species. Only altitude had a strong positive direct effect on the number of syrphid species and this may be explained by the different climatic conditions. Some plant species attracted more syrphids than others. There were significantly fewer species of hoverfly per plot with increasing numbers of flowers. We interpret this to mean that plant species with a high density of flowers attracted more syrphids of the same species. Analysis of pollen grains extracted from two species of hoverflies showed that flower constancy occurred in three examined sites.

Morphological Complexity as a Floral Signal: From Perception by Insect Pollinators to Co-Evolutionary Implications.

Morphologically complex flowers are characterized by bilateral symmetry, tube-like shapes, deep corolla tubes, fused petals, and/or poricidal anthers, all of which constrain the access of insect visitors to floral nectar and pollen rewards. Only a subset of potential pollinators, mainly large bees, learn to successfully forage on such flowers. Thus, complexity may comprise a morphological filter that restricts the range of visitors and thereby increases food intake for successful foragers. Such pollinator specialization, in turn, promotes flower constancy and reduces cross-species pollen transfer, providing fitness benefits to plants with complex flowers. Since visual signals associated with floral morphological complexity are generally honest (i.e., indicate food rewards), pollinators need to perceive and process them. Physiological studies show that bees detect distant flowers through long-wavelength sensitive photoreceptors. Bees effectively perceive complex shapes and learn the positions of contours based on their spatial frequencies. Complex flowers require long handling times by naive visitors, and become highly profitable only for experienced foragers. To explore possible pathways towards the evolution of floral complexity, we discuss cognitive mechanisms that potentially allow insects to persist on complex flowers despite low initial foraging gains, suggest experiments to test these mechanisms, and speculate on their adaptive value.

Flower Constancy of Bumblebees – The Case of Onobrychis pindicola (Fabaceae) Pollinators

Abstract Pollination in high mountain habitats is an important ecosystem service in climate change conditions. The aim of this study was to use pollen load analysis to assess flower constancy and foraging choices of bumblebees foraging on Onobrychis pindicola, a high-mountain endemic plant. The flower constancy to the foraging source O. pindicola was very high - over half of the bumblebees had pure Onobrychis-type pollen loads. In the mixed pollen loads we found one to seven pollen types other than Onobrychis-type and the functional flower morphology was different from the flag type. Some were gullet while others were dish/bowl functional morphology type. Thus the theory/belief that once discovering the flag blossom as a foraging resource bumblebees tended to visit other plants with such functional morphology was rejected. An abundance of plants did not determine food choice. We could not trace an obvious pattern of the bumblebees’ preference to functional blossom morphology but they were attracted to dish-bowl blossoms.

Bee pollinators of faba bean (Vicia faba L.) differ in their foraging behaviour and pollination efficiency

Insect pollination is essential for crop production by enabling or increasing seed and fruit set in many crops. The grain legume faba bean (Vicia faba L.) is partially allogamous and benefits from bee pollination because bees transfer cross-pollen and improve seed set. Here, we study mechanisms behind bee pollination and address the question whether individual bee species differ in their efficiency to pollinate V. faba. We studied the foraging behaviour of bee pollinators in faba bean fields using transect walks, and the species-specific flower constancy based on pollen analyses. For the first time, we examined the species-specific effects of bee pollinators on seed set and degree of cross-fertilisation. We found that the two locally dominant pollinator species, Apis mellifera (56% of all observed individuals) and Bombus terrestris agg. (37%), did not provide efficient pollination service since they mostly robbed nectar. The less frequent species Bombus hortorum (4%), however, revealed to be the most efficient pollinator. It exhibited only legitimate flower visits, high flower constancy and additionally increased seed set and the degree of cross-fertilisation more than any other species. Our study demonstrates especially that less frequent and more specialised pollinator species with long tongues improve pollination and cross-fertilisation of faba bean, which is of great importance in plant breeding and seed production.

Nicotine in floral nectar pharmacologically influences bumblebee learning of floral features

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.

Pollinator preferences and flower constancy: is it adaptive for plants to manipulate them?

Pollinator preferences and flower constancy: is it adaptive for plants to manipulate them?

Flower pollination algorithm development: a state of art review

The journey of a modern man from a troglodyte is due to human nature to try to unfold the mysteries of nature to improve the lives of human beings. A few years back we even can’t think that school of fish, genes, nature of bat or ant can be used to design optimization algorithms. As nature has the solution of every problem. Researchers working on optimization theory are developing optimization techniques which are inspired by nature and could be utilized as optimization tools for engineering problems. Recently, flower pollination algorithm, which is inspired by the pollination characteristics of flowering plants and associated flower constancy of some pollinating insects, caught the eye of many researchers in the world of optimization. This paper presents a brief review about the algorithm its developments and applications. In the last part of this paper, the authors have listed the limitations and topics within FPA that the authors consider as promising areas of future research.

Sex and breeding behaviour of the Sicilian snail-shell bee (Rhodanthidium siculum Spinola, 1838; Apoidea–Megachilidae): preliminary results

In spring 2014 and 2016, we studied Rhodanthidium siculum in dunes south of Syracuse (Sicily). The females search for one of the frequently empty snail shells (mostly of Theba pisana), checking their size. In a suitable snail shell, a mixture of sand and saliva is deposited in the navel. A severe struggle among several males gets started. At every opportunity, the males try to copulate with the females. Large males occupy the snail shell that is used by the female to bring in pollen and nectar (preferably from Galactites tomentosus, Centaurea sphaerocephala, Glebionis coronaria and Lotus creticus). The procedure of harvesting lasts about 2–3 h, sometimes several hours. During this period, the female is visited for copulation every 2 min (initially even more frequently), preferentially by one large male, but small males occasionally mate as well. After laying one or two eggs, the female closes the snail shell with pieces of seashells or snail shells, aggregated with sand and saliva. The female transports the closed snail shell to a safe site. Depending on weather conditions, this may take several days. The maximum distance of movement observed was about 10 m. Finally, the completed snail shell will be buried, most often beneath a plant. The burial follows a certain pattern of movement. Females ensure higher pollination efficiency than the males due to their higher flower constancy.

Pollen Load and Flower Constancy of Three Species of Stingless Bees (Hymenoptera, Apidae, Meliponinae).

The genera of stingless bees play an important role as pollinators of plants. These bees are actively involved in the pollination of agricultural crops and known to have preferences in selecting flowers to pollinate. The aims of this study were to analyse the pollen load and flower constancy in Tetragonula laeviceps, Lepidotrigona terminata, and Heterotrigona itama. Each individual of species stingless bees collected and was put in a 1.5 mL micro-tube contain 0.5 mL 70% ethanol:glycerol (4:1). Pollen loads on each individual of stingless bees was counted by hemocytometer. Flower constancy of stingless bees was measured based on percentage of pollen type loaded on the body. Results showed that the pollen loads of H. itama was the highest (31392 pollen grains) followed by L. terminata (23017 pollen grains) and T. laeviceps (8015 pollen grains). These species also demonstrated different flower constancy, T. laeviceps on Poaceae flowers (76.49%), L. terminata on Euphorbiaceae flowers (80.46%), and H. itama on Solanaceae flowers (83.33%).

A bird pollinator shows positive frequency dependence and constancy of species choice in natural plant communities.

Animal pollinators mediate reproduction of many plant species. Foraging theory suggests that animal pollinators exhibit preferences for common plant species in natural communities (positive frequency-dependent foraging) and temporary single-species specialization (flower constancy) during foraging bouts. Positive frequency dependence may favor common plant species; flower constancy may enhance conspecific pollen transfer particularly in rare plant species. Previous experimental studies suggest that avian pollinators are unlikely to exhibit these behaviors. We studied foraging behavior of Cape Sugarbirds (Promerops cafer), the main avian pollinator of many Protea species, using focal-plant and focal-bird sampling, assisted by high-resolution maps of the spatiotemporal distribution of Protea individuals and their flowering status. We found that Sugarbird's visitation preference increased with species' relative floral abundance, and that individual Sugarbirds tended to visit single species in sequence. Flower constancy during foraging bouts was significantly higher than expected from random plant-animal encounters at the scale of pollinator movements. Positive frequency dependence may favor the reproduction of abundant plant species while flower constancy may be particularly important for rare plant species. This first simultaneous study of both behaviors in a natural plant-pollinator system shows that bird pollinators exhibit both types of behavior and, in this way, possibly influence plant community structure.

Pre‐ and post‐pollination interaction between six co‐floweringPedicularisspecies via heterospecific pollen transfer

It remains unclear how related co-flowering species with shared pollinators minimize reproductive interference, given that the degree of interspecific pollen flow and its consequences are little known in natural communities. Differences in pollen size in six Pedicularis species with different style lengths permit us to measure heterospecific pollen transfer (HPT) between species pairs in sympatry. The role of pollen-pistil interactions in mitigating the effects of HPT was examined. Field observations over 2yr showed that bumblebee pollinators visiting one species rarely moved to another. Heterospecific pollen (HP) comprised <10% of total stigmatic pollen loads for each species over 2yr, and was not related to conspecific pollen deposition. Species with longer styles generally received more HP per stigma. The pollen tube study showed that pollen from short-styled species could not grow the full length of the style of long-styled species. Pollen from long-styled species could grow through the short style of P.densispica, but P.densispica rarely received HP in nature. Flower constancy is a key pre-pollination barrier to HPT between co-flowering Pedicularis species. Post-pollination pollen-pistil interactions may further mitigate the effects of HPT because HP transferred to long styles could generally be effectively filtered.

Legitimate visitors and nectar robbers on Trifolium pratense showed contrasting flower fidelity versus co-flowering plant species: could motor learning be a major determinant of flower constancy by bumble bees?

Flower visitors often fly among plants of the same species more often than is expected from plant frequency and distribution, a behavior known as flower constancy. Because of its implications for the evolution of floral traits, whether flower constancy is associated with perceptual stimuli, reward value, and/or flower handling skills has been debated by many authors. However, it remains unknown whether flower handling skill has a substantial influence on flower constancy because flowers that require different handling skills generally also differ in their appearance (i.e., shape). We investigated the foraging type constancy of Bombus terrestris workers that foraged flower patches consisting of two (Trifolium pratense and Trifolium repens) or three (T. pratense, T. repens, and Lotus corniculatus) plant species. In these flower patches, individual bees foraged T. pratense flowers by either one of the two foraging modes that require different foraging techniques (legitimate foraging versus nectar robbing). Behavioral and pollen load analysis indicated that bees sometimes switched their foraging types between legitimate visits to T. pratense and visits to T. repens and between nectar robbing on T. pratense and visits to L. corniculatus, though they rarely switched between other combinations of foraging types. These results indicate that factors other than perceptual stimuli and spatial distribution of plants affected foraging type constancy. After considering other factors, such as the rewards and the sizes of individual foragers, we argue that handling skills required to forage flowers affected flower constancy observed in this study.

Determination of Flower Constancy in Bombus atratus Franklin and Bombus bellicosus Smith (Hymenoptera: Apidae) through Palynological Analysis of Nectar and Corbicular Pollen Loads

The flower constancy (the visit to a single plant species during a foraging trip) in pollinator insects is a theme widely discussed in behavioral ecology and has an important implication in the evolution of angiosperms. This behavior was studied in the bumblebees Bombus atratus Franklin and Bombus bellicosus Smith through palynological analysis of the nectar and pollen loads of individuals captured while foraging in a restricted area. In both species, there were more individuals with constant flights than with non-constant ones, although in the nectar loads of B. atratus there were no significant differences between individuals with each flight types. It was verified that the nectar loads of the individuals that made either constant or non-constant flights did not differ in the number of pollen grains they contained. Considering this measurement as an estimate for flight duration, the results would indicate that the probability of changing between plant species during nectar collection is independent of the foraging trip duration. In both species, most individuals who collected nectar and/or pollen from more than one plant species visited just two plant species. In these cases, the pollen of one plant species was predominant. In the bumblebees in which it was possible to analyze nectar and pollen loads, the botanical origin of both resources was the same or they shared the principal species (with the exception of two individuals), showing that bumblebees do not often use a botanical source in an exclusive way to collect nectar and another to collect pollen.