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Morphological Complexity as a Floral Signal: From Perception by Insect Pollinators to Co-Evolutionary Implications
Abstract and Figures
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.
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... Often, complexity is referred to at the level of the genome (genome size, chromosome number, structure of genes; Ren et al., 2018), cells (types, density, interactions, size; Wolkenhauer and Muir, 2011) or tissues (cell types, interactions, layer organisations; López-Martínez et al., 2024). Attempts to study and explain morphological complexity of angiosperms have tried to reduce descriptions of morphology to simple codes (Burleigh et al., 2006), to characterise reproductive structures as modular organs (Leslie and Mander, 2023) and to confine complexity to functional outputs for pollinators (Krishna and Keasar, 2018). These definitions often omit development as an integral part of complexity. ...
Flowering plants – angiosperms – display an astounding diversity of floral features, which have evolved in response to animal pollination and have resulted in the most species-rich plant clade. Combinations of macroscale (e.g. colour, symmetry, organ number) and microscale (e.g. cell type, tissue patterning) features often lead to highly elaborate floral displays. Most studies have focused on model species with simple floral displays to uncover the genetic and evolutionary mechanisms involved in flower evolution, yet few studies have focused on complex floral displays. Here, we review current knowledge on the development and evolution of complex floral displays. We review gene regulatory networks involved in four developmental pathways contributing to overall floral display (inflorescence architecture, organ identity, flower symmetry and flower colour) in classical plant models. We then discuss how evolutionary modification of one or more of these pathways has resulted in the production of a range of complex floral displays. Finally, we explore modular systems in which multiple pathways have been modified simultaneously, generating the most elaborate floral displays.
... In this modified FCI (see Table 2), we substituted this variable for a "reward concealment" variable, which is considered a key characteristic of complex flowers (e.g. Krishna and Keasar 2018;Ornai and Keasar 2020) and accounts for stamen location and form, which are of key relevance for pollen foraging bees and are not considered in the original FCI. ...
Cooperation and conflict are common in plant-pollinator interactions. Flowering plants often entice pollinators to visit by offering floral food rewards, thereby facilitating pollination. However, pollinators such as bees can learn to improve their collection of floral rewards (such as pollen), changing how they interact with the flower’s reproductive organs, which together could reduce pollination success. Consequently, complex flowers that slow pollinator learning might benefit the plant. Yet how pollinator learning and flower complexity interact to affect pollination success is unknown. We therefore asked how differences in complexity of four flower types (Phacelia campanularia, Exacum affine, Solanum elaeagnifolium, and Erythranthe guttata) affected learning by pollen-foraging generalist bumble bees (Bombus impatiens) and how learning affected pollen collection and pollen deposition on these flowers. We found that bees generally learned how to efficiently handle more complex flower types more slowly. Bees that required more visits to become efficient foragers collected less pollen, with no effect on pollen deposition. Except for the simplest flower type, learning also involved development of motor routines unique to each flower type. Experienced bees overall collected more pollen, but individual differences in motor routines did not affect pollen collection. Conversely, individual differences in motor routines affected pollen deposition, but there was no overall effect of experience. Thus, even though learning overall benefits the bee, it does not alter female (and potentially male) fitness benefits for the plant. We discuss potential reasons for these patterns and consequences for bee behavior and flower evolution.
... Raspberry provides abundant nectar sources compared to surrounding vegetation, dominated by leafy vegetables, corn, and trees that produce flowers seasonally. This condition strongly attracts wild pollinators (Krishna and Keasar 2018;Dellinger 2020;Staab et al. 2020;Schmack and Egerer 2023). On the other hand, nectar production of raspberry followed a clear pattern that depended on the cultivar, which may explain the longer flower handling time at 10.00 (Schmidt et al. 2015). ...
Mauritius raspberry (Rubus rosifolius) is an exotic plant cultivated in Indonesia. Studies showed that the productivity of exotic plants is reducing due to a lack of pollination agent for their origin region. Several methods could be applied to overcome this problem. The study aimed to find the most effective method for pollinating this plant among four pollination regimes: Self-pollination, wild insects, stingless bees (Tetragonula laeviceps), and hand-pollination. The observation was conducted on the insect pollinators' activities (visitation rate, flower constancy, and flower handling time), pollination efficiency, and quality of the fruits produced (fruit volume). The results showed a higher visitation rate (10 to 70 per hour), higher flower constancy (visited from 07.00 to 16.00), and longer flower handling time (13.6 s) of T. laeviceps on raspberry flowers than other insects. High activities related to better raspberry pollination success (96%) and bigger fruits produced. Based on this study, applying stingless bees as pollination agents for exotic plants was the best and potentially applicable to other exotic crops.
... The variation in flower color within the same population could be an evolutionary response to attract a diverse range of pollinators, thereby increasing the chances of successful pollination in habitats with variable pollinator availability. These morphological intricacies often suggest evolutionary adaptations to specific ecological niches or pollinator diversification (Krishna and Keasar, 2018;Kriebel et al., 2020). Although flower color is generally seen as an adaptation to pollinator visual perception (Stanton, 1987;Niovi Jones and Reithel, 2001;Sobral et al., 2015), several studies have proposed that mechanisms beyond pollinator preferences might be at play in maintaining intraspecific floral color diversity. ...
Introduction
Salvia L., representing the largest genus within the mint family, is noted for its global distribution of approximately 1000 species, with East Asia, and particularly China, recognized as a critical center of diversity for the genus.
Methods
Our research was conducted through extensive fieldwork in Guidong County, Hunan Province, China, where we identified a previously undescribed species of Salvia. The identification process involved detailed morphological observations, phylogenetic analyses, and plastid genomics.
Results
The newly discovered species, Salvia guidongensis, exhibits unique characteristics not commonly observed in the East Asian lineage of Salvia, including dual floral colors within natural populations—either pale purple or pale yellow. Morphologically, while it shares similarities with members of sect. Glutinaria, S. guidongensis is distinct in its floral morphology, stature, and specific foliar traits. Phylogenetic analysis places S. guidongensis in a unique clade within the East Asian lineage of Salvia, suggesting it may serve as an important evolutionary link. Additionally, we explored the plastome features of S. guidongensis, comparing them with those of closely related species.
Discussion
The discovery of S. guidongensis not only entriches the taxonomic tapestry of Salvia but also provides critical insights into the biogeography and evolutionary pathways of the genus in East Asia. By integrating morphological and molecular data, we validate the novel status of S. guidongensis and highlight its significance in bridging taxonomic and evolutionary gaps within Sect. Glutinaria of Salvia.
... Floral morphology and pollen chemistry have a complex functional interplay: complex morphology such as poricidal anthers and keel petals may restrict reward access to more behaviorally specialized bees (37,40), and broad patterns of protein content correlate with these restrictive mechanisms (13,60). The premise that complex flower morphology, here associated with higher P:L values, would lead to visitation by a less diverse community of bees (37,38,58), was only marginally supported by our data (Fig. 6 and SI Appendix, Fig. S7 and Table S6). ...
As bees’ main source of protein and lipids, pollen is critical for their development, reproduction, and health. Plant species vary considerably in the macronutrient content of their pollen, and research in bee model systems has established that this variation both modulates performance and guides floral choice. Yet, how variation in pollen chemistry shapes interactions between plants and bees in natural communities is an open question, essential for both understanding the nutritional dynamics of plant–pollinator mutualisms and informing their conservation. To fill this gap, we asked how pollen nutrition (relative protein and lipid content) sampled from 109 co-flowering plant species structured visitation patterns observed among 75 subgenera of pollen-collecting bees in the Great Basin/Eastern Sierra region (USA). We found that the degree of similarity in co-flowering plant species’ pollen nutrition predicted similarity among their visitor communities, even after accounting for floral morphology and phylogeny. Consideration of pollen nutrition also shed light on the structure of this interaction network: Bee subgenera and plant genera were arranged into distinct, interconnected groups, delineated by differences in pollen macronutrient values, revealing potential nutritional niches. Importantly, variation in pollen nutrition alone (high in protein, high in lipid, or balanced) did not predict the diversity of bee visitors, indicating that plant species offering complementary pollen nutrition may be equally valuable in supporting bee diversity. Nutritional diversity should thus be a key consideration when selecting plants for habitat restoration, and a nutritionally explicit perspective is needed when considering reward systems involved in the community ecology of pollination.
Bumblebees play a significant role as pollinators for many wild plants and cultivated crops, owing to their elongated proboscis, resilience to diverse weather conditions, robustly furred bodies, and their unique capacity for buzz-pollination. To better understand the effect of greenhouse microclimates on bumblebee foraging behavior and working modes, a long-term record of foraging activity for each Bombus terrestris L. (Hymenoptera: Apidae) forager was monitored by the Radio-frequency identification system. The pattern of task performance, including constant housing, foraging, and day-off rotation, was examined under the microclimate. In addition, the correlation between foraging activity of bumblebees and temperature, relative humidity, illumination in the greenhouse, and pollen viability of tomato plants was further analyzed. Our findings revealed that B. terrestris can respond to microclimatic factors and plant resources while also exhibiting a suitable working pattern within the colony. Day-off rotation was observed as a strategy employed by foragers to prolong their survival time. This division of labor and task rotation may serve as strategies for the survival and development of the colony. Our research may contribute to fully understanding how microclimate and plants influence pollinator behavior within greenhouses, thereby optimizing the pollination management of bumblebees on greenhouse crops.
Syzygium parameswaranii is a mass-blooming endangered tree species endemic to the Western Ghats of India. The reproductive phenoevents of S. parameswaranii were significantly correlated with temperature which indicated that the flowering phenoevents should be accelerated by a specific temperature. Due to its poor floral rewards (nectar) and advertisement, a limited number of floral visitors were drawn to the blossoms of S. parameswaranii . Since there were no attractive or colourful sepals or petals, the large number of stamens served as the major floral attractant and provided pollen grains as a major floral reward because the quantity of nectar was very low. The diversity of floral visitors in S. parameswaranii was relatively limited when compared to other species of Syzygium . The flowers were attracted and visited by only twelve species including ants, bees, beetles, butterflies, moths and wasps. Among these visitors, only seven of them served as efficient pollinators. Scolia dubia was recorded with higher visitation frequency (0.78 ± 0.11) and visitor activity index (0.89) than any other visitor. Due to their frequent visits and effective stigma contact, they were recorded as the most effective pollinators of S. parameswaranii .
The genus Delphinium (Ranunculaceae) with its unique and highly complex floral structure is an ideal system to address some key questions in terms of morphological and evolutionary studies in flowers. In D. anthriscifolium, for example, the original eight petal primordia differentiate into three types at maturity (i.e., two dorsal spurred, two lateral flat, and four ventral reduced petals). The mechanisms underlying their identity determination and morphological differentiation remain unclear. Here, through a comprehensive approach combining digital gene expression (DGE) profiles, in situ hybridization, and virus-induced gene silencing (VIGS), we explore the role of the APETALLATA3-3 (AP3-3) ortholog in D. anthriscifolium. Our findings reveal that the DeanAP3-3 not only functions as a traditionally known petal identity gene but also plays a critical role in petal morphological differentiation. The DeanAP3-3 gene is expressed in all the petal primordia before their morphological differentiation at earlier stages, but shows a gradient expression level difference along the dorsventral floral axis, with higher expression level in the dorsal spurred petals, intermediate level in the lateral flat petals and lower level in the ventral reduced petals. VIGS experiments revealed that flowers with strong phenotypic changes showed a complete transformation of all the three types of petals into non-spurred sepals. However, in the flowers with moderate phenotypic changes, the transformation of spurred petals into flat petals is associated with moderate silencing of the DeanAP3-3 gene, suggesting a significant impact of expression level on petal morphological differentiation. This research also shed some insights into the role of changes in gene expression levels on morphological differentiation in plants.
Bioacoustics is a field of study that examines the production of sound and how it affects living things. Numerous plant species' physiology, behaviour, and eventual survival have all been greatly influenced by sound and its usage in communication. A better framework for future research may be developed along with a greater understanding of how various organisms interact acoustically with plants if the acoustic link between plants and animals is understood. A re-imagination of our knowledge of these organisms is anticipated to result from the systematic investigation of the functional and evolutionary importance of sound in plant life. This will also stimulate the emergence of new ideas and viewpoints regarding the communicative complexity of plants. The primary goal of this study is to examine some information about the bioacoustics interaction between plants and animals their sound, and ecology, including potential techniques of sound production employed by plants. The importance of acoustical research in plant ecology, as well as its potential mechanisms and future applications, are covered in this paper. The first section of this article reviews how plants amplify and transmit sounds produced by insect pests. The second section looks at surprising examples of carnivorous plants that show how plants have evolved to reflect but also enhance animal sounds, potentially revealing new angles in research on the interactions between animals and plants. The discussion then focuses on the mechanisms by which plants produce sound through transpiration stress and photosynthesis, as well as a potential model for these mechanisms.
Plants use visual signals to attract pollinators and direct them to their flowers. Visual capabilities of bees have been extensively studied mostly using artificial paper models. However, there is no empirical determination of the maximal detection distance (MDD) or minimal subtended visual angle (MSVA) of real flowers. Using a six armed radial maze, we tested MDD and MSVA of 12 types of natural and manipulated real flowers by bumble bee (Bombus terrestris) workers. Bees were initially trained to obtain sugar solution at target flowers that were presented at close range on a mobile divider at the back of one of the six arms. Bees were individually marked and tested. For bees that passed the short range test, we gradually increased the distance of the target flower, until the number of successful choices reached chance level, indicating that they could not see the target flowers. The results show that MSVA of flowers is correlated with flower diameter but not with MDD. The variation in MDD to natural flowers by bumble bee workers can be best predicted by: MDD = flower coloured area / (contour line * green contrast). Contour line length determines flower dissectedness. Full circular flowers can be detected from longer distance than dissected flowers with identical diameter. We hypothesize that dissected flower shapes might be compensated by their higher attractiveness for bees. Empirical determination of real flower MDD and MSVA is important for studying bee foraging behaviour, pollinator induced evolution of flower traits and validation of neurophysiological visual models.
Plants use visual signals to attract pollinators and direct them to their flowers. Visual capabilities of bees have been extensively studied mostly using artificial paper models. However, there is no empirical determination of the maximal detection distance (MDD) or minimal subtended visual angle (MSVA) of real flowers. Using a six armed radial maze, we tested MDD and MSVA of 12 types of natural and manipulated real flowers by bumble bee (Bombus terrestris) workers. Bees were initially trained to obtain sugar solution at target flowers that were presented at close range on a mobile divider at the back of one of the six arms. Bees were individually marked and tested. For bees that passed the short range test, we gradually increased the distance of the target flower, until the number of successful choices reached chance level, indicating that they could not see the target flowers. The results show that MSVA of flowers is correlated with flower diameter but not with MDD. The variation in MDD to natural flowers by bumble bee workers can be best predicted by: MDD = flower coloured area / (contour line * green contrast). Contour line length determines flower dissectedness. Full circular flowers can be detected from longer distance than dissected flowers with identical diameter. We hypothesize that dissected flower shapes might be compensated by their higher attractiveness for bees. Empirical determination of real flower MDD and MSVA is important for studying bee foraging behaviour, pollinator induced evolution of flower traits and validation of neurophysiological visual models.
Signals used in communication are frequently complex, being composed of multiple signal components that in combination improve information transfer. A variety of morphological parts are typically used to transmit components of any given complex signal. Our understanding of why a given morphological part is used to transmit a given signal component is poor. We hypothesized that the function of a given signal component is improved by its association with its morphological part and that such parts interact functionally to transmit information. In a laboratory study we characterized the function of different floral signal components transmitted by associated floral parts and the interaction of those signal components. Using Solanum houstonii flowers, we focused on two major floral parts, corolla and anthers, involved in signalling bumble bee (Bombus impatiens) visitors. We further examined how experience affected the relationship between signal component and floral part. Floral visitation involves a stepwise process in which bees approach, land, and acquire pollen. We found the corolla plays the dominant role in eliciting approaches by bees, whether naïve or experienced. Landing is elicited by corolla signals and, to a lesser but additive degree, anther signals. Following experience, anther signals nearly completely dominate corolla signals in eliciting landing. The anthers convey signals mediating pollen acquisition, regardless of the bee’s experience level. Our findings suggest there is selection for specific relationships between signal components and morphological parts, which in turn might drive complex signal evolution.
Visual ecology is the study of how animals use visual systems to meet their ecological needs, how these systems have evolved, and how they are specialized for particular visual tasks. This book provides the first up-to-date synthesis of the field to appear in more than three decades. Featuring some 225 illustrations, including more than 140 in color, spread throughout the text, the book begins by discussing the basic properties of light and the optical environment. It then looks at how photoreceptors intercept light and convert it to usable biological signals, how the pigments and cells of vision vary among animals, and how the properties of these components affect a given receptor's sensitivity to light. The book goes on to examine how eyes and photoreceptors become specialized for an array of visual tasks, such as navigation, evading prey, mate choice, and communication. A timely and much-needed resource for students and researchers alike, the book also includes a glossary and a wealth of examples drawn from the full diversity of visual systems.
Pollination biology at the community level was investigated using quantitative techniques, comparative methodology, measurements of the physical habitat, and consideration of floral characteristics. The frequency of insect visits to flowers was investigated in three contrasting communities: a deciduous woodland-meadow site in eastern Massachusetts, alpine tundra in New Hampshire, and Mediterranean scrub (fynbos) in South Africa. Visits to flowers were most common in woodland-meadow, followed by alpine tundra, and least frequent in fynbos. Bees were the most common visitor in the woodland-meadow and the fynbos, but flies were the most common visitor in the tundra. Flower color often influenced visitation rates and had a weak but significant effect on the type of insect that visited flowers. Preferences for color by different types of insects often changed in different communities, which suggests that floral syndromes may be community-specific. In all communities, tubular flowers were visited less often than open flowers. Less specialized insects were more common on open than tubular flowers, but large variances made few differences statistically significant. Combining measurements of temperature, light, humidity, wind speed, time of day, and season (using cluster analysis) with the shape of a flower, it was predicted that a 10-minute observation would include at least one visit. Flower shape, temperature, light, and season appear to be the most important variables influencing insect visitation rates. Results of this study indicate that relationships between insects and flowers are nonspecific and vary among communities.
A chemical survey of pollen lipids was carried out to examine the composition of pollenkitt in relation to that of whole pollen and to evaluate the possible role of pollenkitt as the principal carrier of chemical cues used by flower visitors. Investigated pollen was collected from 69 angiosperm species (28 families) in California. Lipid extracts of pollenkitt and of the internal portion of pollen were analyzed for each species using thin-layer chromatography. Neutral lipids (energy storage and essential oil constituents) were most diverse in pollenkitt, while polar lipids (mostly membrane constituents) were found almost exclusively in the internal pollen fraction. Patterns in neutral lipid compositions suggest that pollenkitt may provide pollen with species-specific odors. Yellow pigments were observed in pollen of most species, with carotenoids predominating in pollenkitt and flavonoids in the internal fraction. Phenolic and heterocyclic nitrogen compounds were found in the lipid extracts of several species.
The cumulative (season-long) incidence of heterospecific pollen transfer (HPT) was examined using nine sympatric species in a midsuccessional old field. Inflorescences were collected weekly during the flowering season, and the proportion of foreign pollen/stigma was recorded. Flowering phenologies of sympatric species and ovule and seed counts of study species were also recorded. Heterospecific pollen was detected on some stigmas of each species. Medicago sativa (Fabaceae) received the most foreign pollen; in some cases, all of the grains on a stigma were heterospecific. Lotus corniculatus (Fabaceae) received the least amount of foreign pollen; the incidence of heterospecific pollen was near zero in most cases. The mean and range of foreign pollen received varied by as much as an order of magnitude between species. The six species with zygomorphic flowers, all Fabaceae, received more heterospecific pollen than the three species with actinomorphic flowers, Potentilla recta and P. simplex (Rosaceae) and Ranunculus acris (Ranunculaceae). This probably reflects a bias because our data were analyzed on a cumulative basis and the Fabaceae had longer flowering phenologies. HPT was not correlated with the species' relative abundance within the community. Proportion of foreign pollen received varied temporally within species, and this variation generally was not related to phenology of any sympatric taxa or the species' own phenology. Pollen grain diameter was positively related to levels of foreign pollen received by species. This might be caused by poor adhesion of large pollen grains to small stigmatic papillae or if generalist pollinators carrying large amounts of heterospecific pollen visit the large-grained species and specialists with little foreign pollen visit the small-grained species. The large proportions of heterospecific pollen on stigmas of many species indicate that HPT occurs frequently in the community we studied and the implications may include reduced seed set because of occlusion by foreign grains. As yet, however, it is unclear how important a factor HPT is in mediating pollen limitation of reproductive success.
It is now generally accepted for a variety of reasons - morphological as well as physiologica- that the visual systems of arthropods provide a suitable model for the study of information proces sing in neuronal networks. Unlike the neurophysiology of the visual pathway in the frog and the cat which is more than adequately documented, recent work on the compound eye and optical ganglia of spiders, crustaceans, and insects has scarcely been summarized. In order to fill this void so that others, especially vertebrate neurophysiologists may become familiar with the advan tages of these systems, our group at Zurich University organized here in March 1972, a European meeting to discuss the anatomical. ! neurophysiological and behavioral knowledge on the compound eye and the visual. pathway of arthropods. Systems analysis was regarded as the main theme of the conference, but systems analysis of a network of neurons cannot be done as a mere "black-box" maneuver. The conference therefore tried to reconcile neurophysiology and behavioral analysis in order to make predictions about a necessary and sufficient neural structure. The "wiring dia grams" of such a structure might then be confirmed histologically. Hence the aim of the conferen ce was not to deal only with the structure and function of the compound eye - i. e.