Polination Biology: Theory and Primary Practice
Nectar-collecting bumblebees usually move upward while foraging in consecutive flowers on vertical inflorescences. This tendency to successively move upwards has been suggested to be a direct response to available nectar rewards. Therefore, bumblebees starting at bottom flowers will visit the most rewarding flowers first. An alternative explanation is that bumblebees have a better view of the flowers above than those below and they fly to those they can most readily see while maintaining an upright orientation. To evaluate these two hypotheses, we recorded flight patterns of bumblebee (Bombus ignitus) nectar foraging behaviors on upward and downward vertical inflorescences of monkshood (Aconitum kusnezoffii) and measured the difference in the reward for bumblebee from nectar between lower (female phase) and upper (male phase) flowers. We found significant support for the hypothesis explaining bottom-to-up flights while visiting upward vertical inflorescences. Nectar analysis indicated that both nectar volume and sugar content in lower female-phase flowers were significantly higher than those in upper male-phase flowers. Our findings suggest that B. ignitus forage from more to less rewarding flowers and depart when gain of reward is low. We also noted bottom-to-up foraging behaviors for both the downward and upward vertical inflorescences. However, pollinators started from less rewarding male-phase flowers, which was inconsistent with the declining reward hypothesis. Our results suggest that gender-biased nectar production towards the female phase does not directly regulate bumblebee foraging sequences, but rather attract bumblebees starting from the bottom female-phase flowers.
Variable insect behaviors may result in different flower visiting frequencies, which may result in diverse impacts on plant pollination. Although flies, hoverflies, and Italian bees (Apis mellifera ligustica) were the most common visitors of Chimonanthus praecox, these insect groups had disparate visiting behaviors. Flies traveled quickly, and crawled or jumped between flowers. Italian bees also flew quickly or occasionally crawled between flowers. In contrast, hoverflies generally spent a majority of time foraging on a given flower. Based on the average foraging time and inter-floral flight time, one Italian bee could visit 4.57 flowers per minute, whereas individual bees and hoverflies could visit 2.65 and 0.53 flowers on average, respectively. After incorporating the total number of individuals for each insect group, we extrapolated the visiting rates of Italian bees, flies and hoverflies as 498.19, 1,089.74 and 99.78 flowers per minute, respectively. Flies and Italian bees had higher pollination effectiveness (number of pollinated flowers by the same number of visitors in a given time interval under the same condition), with estimates of 93% and 100% (n = 30), respectively, while only 13% (n = 30) for hoverflies. If we consider the pollen load ability and pollination effectiveness for Italian bees and flies, visiting rate may be the main limiting factor for their potential in pollinating flowers. Thus following these conclusions, flies are the major pollinators of C. praecox, followed by Italian bees (pollination role was limited by their low number) and hoverflies (limited by their foraging and hovering behaviors and lower pollination effectiveness).
The relationship between sexual reproduction and resource allocation plays an important role in plant life history and in the evolution of breeding systems. Tulipa sinkiangensis is an early spring perennial ephemeral species endemic to the desert zone of the northern piedmont of the Tianshan Mountains, Xinjiang, China. This species produces offspring only by sexual reproduction, and produces 1-8 flowers per individual in natural populations. The relationships between sexual reproduction allocation and vegetative growth and plant size, respectively, and resource allocation among flowers and fruits at different positions within the inflorescence were studied in T. sinkiangensis. Our aims were to explore the effect of vegetative growth, plant size and flowering order on sexual reproduction allocation in this species. There was a negative correlation between the resources that plants allocate to both vegetative organs (bulb and aboveground vegetative organs) and sexual reproductive organs at flowering stage and fruit maturation stage (P<0.01), suggesting that resource allocation between vegetative growth and sexual reproduction is a trade-off. Production of multiple flowers is a stable character in this species―the total number and biomass of flowers, total fruit biomass, and total number of seeds per individual were positively correlated with plant biomass (P<0.01), indicating that sexual reproduction allocation is size-dependent. In individuals with 2-5 flowers, the biomass of flowers, pollen and ovule production, fruit-set, fruit biomass, seed number, seed-set, and 100-seed weight declined successively with flowering order within the inflorescence, indicating that resource competition for floral allocation was significant and that resource limitation for each flower or fruit is related to flowering order. Plants ensure their reproductive success by reducing resource allocation to late flowers or fruits and increasing the resource allocation to early flowers or fruits in this species.
Classic size-dependent sex allocation models for animal-pollinated plants predict that female allocation increases with plant size. However, some studies have shown a male biased size-dependent sex allocation at flowering stage. We investigated the size-dependent sex allocation strategies within flower and inflorescence in gynomonoecious Aster ageratoides within two naturally-occurring populations in which hermaphroditic and female flowers occur in the same individual. At the flowering stage, male biased size-dependent sex allocation has been observed at both flower and inflorescence level. The pollen/ovule ratio ranged from 750 to 5,250, with a mean of 2,757.14± 206.635, and increased significantly with plant height in one of the populations. At the inflorescence level, the male allocation, which was measured by the proportion of hermaphroditic flowers, increased with plant height in both populations. These results are consistent with the expectation of male biased size-dependent sex allocation at flowering stage, through which A. ageratoides may maximize fitness by enhancing pollen dispersal.
Hermaphroditic plants that simultaneously display multiple flowers may attract more pollinators and create more chances for mating. However, this may also lead to geitonogamy, which may have major impacts on evolution of sex allocation, floral characteristics, and dioecy. To explore adaptive significance of mass-flowering in Hedychium coccineum, we conducted studies on pollination biology of H. coccineum, via hand-pollination and manipulated experiments, pollinator observation, and investigations on population density and natural fruit sets. Overall, inflorescences of H. coccineum were composed of terminal spikes containing 57.33 ± 1.68 (n = 30) cincinnus, and each cincinnus possessed 3.8 ± 0.15 (n = 30) flowers. Flowers in each cincinnus opened in turn, and the same round flowers among each cincinnus within inflorescences opened in successive synchronous cycles. This provided a spike that kept a mass of flowers blooming simultaneously throughout the flowering period. H. coccineum displayed a large floral display at the inflorescence level. Additionally, H. coccineum was self-compatible, and spontaneous self-pollination did not occur. Fruit production of H. coccineum in natural populations was severely pollinator-limited. Meanwhile, H. coccineum was also resource-limited in fruit production. Three butterflies, Papilio memnon, Dercas lycorias, and Appias indra aristoxemus were effective pollinators of H. coccineum. Visiting frequencies of these butterfly species to three inflorescences with different floral display size were obviously different and visitation frequencies increased as the inflorescence increased in floral display size. Pollen grains and ovules of H. coccineum varied significantly among flowers of different rounds in the cincinnus. Ovule production decreased significantly from the first to the fourth round, but pollen grains increased significantly from the first round to the third round. The decrease in ovules and resource limitation in fruit production indicated that mass-flowering in H. coccineum was not for increasing fruit production. The increase in pollen grains from the first round to the third round benefits pollen export and increases male fitness.
Weather patterns in desert environments (e.g., dry heat, strong winds, dust storms, and temperature fluctuations) can be highly unpredictable and can have deleterious effects on sexual reproduction of flowering plants. The herb Limonium otolepis is a dominant species in desert areas of Xinjiang, northwest China; however, reproductive strategies in unfavorable environments remain to be explored. Overall, we addressed flowering pattern and pollination modes, flowering process, floral traits, pollinators, and fruiting characteristics of L. otolepsis in Junggar Basin region. We employed scanning electron microscopy to examine the morphology of pistil stigmas and pollen grains. The flowering period of L. otolepis was from early June to mid-July, with extended flowering due to unsynchronized flowering phenology among individuals in the same population. During a given day, it showed a concentrated flowering and pollen release, with anthesis lasting for about 6-8 h. Petals unfolded at about 8:00 and reached the peak of flowering at about 9:00, with no more flowers opening after 11:00. One flower produced 752 pollen grains with a small amount of nectar. The pollen exine ornamentation was reticulate. Insects, including bees and hoverflies, were primary pollinators. Highest visiting frequencies occurred between 9:00 and 14:00. L. otolepsis was mainly outcrossing given that automatic selfing yielded a few seeds. Overall, fruit sets of open-pollinated flowers were 36.1%. Within inflorescences, fruit sets on basal flowers (45.7%) were significantly higher than those on neighboring flowers (3.3%). Mast flowering in L. otolepis reported here may facilitate pollination in unpredictable weather conditions. The reproductive strategy may also dispense reproductive risk by maintaining flowering asynchrony to prolong overall flowering period.
Scented nectar secreted by flowers is an interesting natural phenomenon in angiosperms that is often overlooked by most researchers. Scented nectar is an evolutionary feature coupling the behavior between flower-visitors and their rewards. The effect of scented nectar on pollinator or nectar-thief is a scientific problem which deserves further exploration. We evaluated Mucuna sempervirens flowering dynamics, floral nectar volatiles, behaviors of Dremomys pernyi and Callosciurus erythraeus to inflorescence opening, nectar’s attraction effect to Apis cerana cerana, and the toxic effect of M. sempervirens nectar to Tapinoma sp. Aliphatic compounds (87.2%) were the main volatiles in nectar of M. sempervirens, whereas ketones accounted for 56.1% of the total volatiles. Lastly, volatile components with sulfur elements were absent from nectar samples. Previous studies of bat pollinated plant species have found that plants in the genus Mucuna always release sulfur compounds. Additionally, we found that the nectar of M. sempervirens was poisonous to Tapinoma sp. ant species, whereas it attracted A. cerana cerana using the Y olfactory bioassay. Squirrel species (D. pernyi and C. erythraeus) were effective pollinators of M. sempervirens, so we suspected that M. sempervirens might not be pollinated by bats only. This study provides data of pollination mechanisms in Mucuna and provides a new perspective of composition and function study of nectar in other plant groups in future.
Thermopsis lanceolata is sand-fixing plant that plays an important role as a spring nectar source in northeastern China; however, little is known about its reproductive characteristics. To ascertain the major pollinators of T. lanceolata, we identified foraging behaviors, pollination process, activity rhythm of floral visitors and the effect of nectar robbers on the seed setting were investigated in Mu Us Sandland, Inner Mongolia. We used photo, video and visual measurement to observe floral visitors in a 10 m × 10 m quadrat. We recorded the species, pollinating behaviors and visiting frequency of all pollinators from 06:00 hours until 19:00 hours in sunny days. Based on visitation frequencies and pollen amounts carried on the body, two bee species, Megachile japonica and Hoplitis princeps were identified as the primary pollinators of T. lanceolata., but visiting frequencies between the two species were significantly different. Daily activity of M. japonica was bimodal with diurnal foraging activities during 9:00-13:00 and 16:00-18:00 hours, whereas daily activity of H. princeps was of unimodal type from 11:30 to 16:30 hours. We also noted nectar robbing behaviors by M. japonica due to the presence of nectar acquisition holes at the base of the flower of T. lanceolata, but found that these behaviors had no effect on seed setting. Pollinator activity peaks indicate a complementary relationship between M. japonica and H. princeps. Our observations of visiting frequencies suggest that M. japonica was a dominant pollinator for T. lanceolata.
Nectar guides are special floral structures that are assumed to attract and/or direct pollinators towards a concealed nectar reward. Nectar guides are commonly found in many angiosperm plants, especially entomophilous flowers, but their functional significance and impacts on the reproductive success of plants are poorly understood. For example, Delphinium caeruleum of the family Ranunculaceae possesses two barbate staminodes, between which is the nectar entrance. To test the effects of these barbs on male and female fitness, we experimentally investigated the effects of barb removal on seed production and pollen exportation of D. caeruleum at the Haibei Station of Qinghai Province. Our results showed that flowers of D. caeruleum were dichogamous and herkogamous, which prevented autonomous selfing in this species. The mating system of D. caeruleum belongs to obligate xenogamy and thus pollinators are necessary for the successful pollination. Compared to control flowers, the number of pollen grains exported was reduced significantly after removing the barbs, but fruit set and seed number was not affected. Our primary results indicate that the barbs on the staminode act as nectar guides, which improve the male fitness of D. caeruleum, but have little effect on female fitness. Our results suggest that selection through male fitness might have played an important role in the floral evolution of D. caeruleum at our study site. These results need to be further investigated at a larger number of sites to evaluate selection mechanisms on floral traits of D. caeruleum.
Heterostyly is a genetically controlled floral polymorphism, which includes both distyly and tristyly. We investigated morph ratio, floral and pollen morphology, and self-incompatibility of Hedyotis pulcherrima. Overall, the natural population of H. pulcherrima was isoplethic, containing long-styled and short-styled morphs with an equilibrium 1:1 ratio. Long-styled and short-styled morph exhibited a precise reciprocal herkogamy, which was significantly correlated with corolla length. Stigma-lobe length, pollen size, and starch content in pollen grains were dimorphic in the two morphs of H. pulcherrima, whereas pollen germination and pollen tube growth in vitro were not significantly different between the two morphs. Artificial pollination revealed that pollen tube shape was normal in both morphs where pollen tubes reached the ovary 24 h after pollination. However, pollen tube growth was arrested in the stigma with the accumulation of callose in the swollen tips in two morphs with self and intramorph pollination, indicating strict heteromorphic self-incompatibility in H. pulcherrima. No fruit was produced in emasculated netted flowers, suggesting the absence of apomixis. Artificial intermorph pollination resulted in 100% of fruit set, significantly higher than those with open pollination. Our results indicate that H. pulcherrima is a typically distylous species with heteromorphic self-incompatibility.
Flowering date along with interactions of other co-flowering species may be factors that determine pollination and reproductive success of a focal plant species. We investigated an alpine bumblebee-pollinated herb Pedicularis gruina to assess the effects of flowering date and co-flowering species on pollination, reproduction, and predation over a three year period (2003-2005). We analyzed pollen load of bumblebees to determine floral constancy, and calculated pollination rates of flowers, fruit set, seed production per capsule and the percentage of seed predation. We found that fruit sets did not differ significantly among years and between different flowering dates when there were no co-flowering species, with 34-38% of flowers producing fruits. However, the presence of co-flowering species could either increase or decrease the pollination and reproduction in P. gruina, which depends on pollinator type and flowering date of the co-flowering species P. densispica. Pedicularis densispica enhanced pollination and reproduction through increased floral resource diversity, whearas P. siphonantha enhanced pollination and reproduction through increased attractiveness with larger displays. Flowering date did not affect fruit set, but significantly affected seed production and seed predation. Seed production decreased significantly at later flowering dates given the same pollination condition(i.e., no co-flowering species, pollinator competition, or facilitative pollination). However, fruits produced in early flowering periods suffered more severe seed predation compared to those in later flowering periods.
The highly specific mutualism between fig trees and their obligate pollinating fig wasps is usually exploited by non-agaonid wasps, and some of these wasps can enter and pollinate the figs just like the obligate pollinating wasps. Therefore, the agaonid and non-agaonid wasps have convergently evolved in their morphological characteristics and phenology. However, there are few data about the convergence of host recognition behaviors among these wasps. In Ficus curtipes, there are three internally ovipositing wasps, i.e. one obligate pollinating wasp, Eupristina sp., and two inquiline wasps (Diaziella yangi and Lipothymus sp.), which can also pollinate the figs if they enter the figs. In this study, we carried out several behavioral experiments with a Y-tube olfactometer to test the hypothesis of convergence of host recognition behaviors among these wasps. We observed and recorded the wasps’ behavior of choice among figs at different developmental phases and among 6-methyl-5-hepten-2-ol, 6-methyl-5-hepten-2-one and the mixture of the two chemicals. Our results showed that all three of the wasps were significantly attracted by the receptive F. curtipes figs when presented with choices between receptive figs and figs at other developmental phases and were significantly repelled by the male phase figs of F. curtipes when presented with choices between male phase figs and figs at other developmental phases. In addition, all of them also preferred to the compound 6-methyl-5-hepten-2-ol at the dose level of 1µL. These results provide evidence for the hypothesis of convergence of host recognition behavior among obligate pollinating fig wasps and non-pollinating fig wasps. The role of behavioral convergence in the evolution of non-obligate pollinating wasps into obligate ones is also discussed.
We measured floral traits of Trollius ranunculoides at different flowering time, observed the taxa of pollinators and pollinator visiting frequencies, and collected the seeds in the end of growing season to estimate pollinator preferences and the overall phenotypic selection gradient. We estimated phenotypic selection on floral traits at different flowering time using female fitness (seed number). We found significant differences of floral traits among different flowering time, with the corresponding preference, taxa, and visiting frequencies of pollinators also different. During early flowering time, visiting frequencies of bees were higher, flower calxy and petal size were wider, and total stalk length was shorter on flowers that bees preferred; however, there was no significant flower preference by different fly species. Furthermore, our estimates of phenotypic selection through female fitness differed at variable flowering time. The results of our study indicate that divergent flowering time and corresponding variation in pollinators might lead to different phenotypes, ultimately resulting in the divergence of floral traits. However, pollinator preference was dissimilar from phenotypic selection estimated by female fitness due to reasons not sufficiently evaluated in this study.
Floral color and scent are two important components of floral design. Although previous studies on floral design have been mostly descriptive. The exploration on their quantitative studies can provide key evidence to learn pollination mechanisms. Our study focuses on recently developed methods for the quantitative measurement of floral color and floral scent. We introduce three floral color measurement and plotting methods, including color chart, colorimeter and spectrometer. Dynamic headspace collection-adsorption, adsorption-solvent desorption and solid phase micro-extraction are the three frequently-used floral scent collection methods and gas chromatography-mass spectrometry and zNose are usually used in floral scent analysis. Lastly, gas chromatography with electroantennographic detector, Y-tube olfactometer and flight cage experiment can help us to evaluate insect behavior.
The interactions between plants and pollinators represent complex pollination networks. Recent improvements in social network analysis provide suitable tools for plant-pollinator interactions within an ecological context. Studies devoted to mutualism in the pollination network at community level have shed important insights into the structure and dynamic of these interactions and also floral evolution. The nested structure of pollination networks suggests that pollination service is redundant, and that relatively generalized species dominate these networks. Although these networks have high species composition turnover, they remain stable in terms of structure and species position, suggesting high interference resistant of pollination networks among seasons or years. Relatively little is known about the mechanisms behind these patterns. It has been suggested that network structure is largely controlled by morphology match between flowers, pollinator traits, and phylogenetic relationships. Meanwhile, community history and biodiversity have been used to link structure and species position of network. Ecologists and evolutionary biologists have become increasingly interested in these networks and recent studies of large-scale dynamics to facilitate the detection of mechanisms between different spatial and biodiverse scales in natural communities. However, there are many challenges of testing these networks. For example, previous visit-centered approaches provide insufficient information about pollen transfer among species, which is essential for plant reproductive success. Also, sample efforts have not been standardized and few studies have focused on zones of high biodiversity. Although debates will continue on the mechanisms behind these patterns, we suggest that factors relating to reproductive success should be considered in future studies, such as the impacts of pollen composition on pollinator condition or pollination efficiency.
Floral symmetry is a classical feature of floral diversity. Actinomorphy and zygomorphy are two main types of floral symmetry in angiosperms. Zygomorphic flowers are thought to have evolved from ancestors whose flowers are actinomorphic. Transition from actinomorphy to zygomorphy has been recognized as a key innovation and is considered crucial in the rapid diversification of angiosperms. In recent years, great progress has been made towards understanding the mechanisms underlying changes in floral symmetry during the evolution of angiosperms in wide-ranging botanical disciplines. Evidence from floral development studies indicates that zygomorphy appears before organ initiation, and persists throughout floral development, or appears later at various stages of development. Reduction, suppression and differential elaboration of floral organs are the major determinants of zygomophy. Floral symmetry is strongly selected by pollinators during the different stages of pollination process. In addition, the tighter flower-pollinator interaction found in zygomorhpic flowers may contribute to increased reproductive success through increased precision in pollen placement on the pollinator’s body. The molecular base of flower symmetry has been explored in core eudicots, and available evidence indicates that CYC-like genes play an important role in the control of zygomorphy. Future prospects in the study of floral symmetry in development biology, pollination biology and molecular genetics are discussed.
Mutualism, or a mutually beneficial interaction between two organisms, are ubiquitous in ecological systems. However, some “empty flowers”, which offer pollinators no any kinds of rewards, design different strategies to attract pollinators without providing rewards to the pollinators. These pollination mechanisms are called deceptive pollination. The family Orchidaceae, representing one of the largest groups in angiosperms, is distinguished by high floral diversity and intricate adaptations to pollinators. Darwin described and identified most of the functional floral morphology and biomechanics in orchid pollination. However, he never recognized that many of the flowers that he examined lacked food rewards for pollinators. Floral evolution in the Orchidaceae appears to be dominated by modes of deceptive pollination, and more than one third of orchid species are thought to be pollinated by deceit. Deceptive pollination is thought to be one of key roles which has lead to relatively high species diversity within the Orchidaceae. Deceptive orchids frequently exploit the food foraging, sexual, oviposition and sleep/warmth behaviors of insects. The most common deception mechanisms include generalized food deception, Batesian floral mimicry, sexual deception, brood-site imitation and shelter imitation. Additionally, floral color, morphology and fragrance play key roles to cheat target pollinators. Relationships between deceptive orchids and their pollinators possibly involve asynchronous evolution; therefore orchids track the diversification of their pollinators. However, deception has negative impacts on the pollinators, which may exert selection on the pollinators. Because duped pollinators tend to avoid rewardless flowers, deceptive orchids suffer low visitation rates and fruit set, various environment factors can affect the reproductive success of these orchids. Deceptive orchids depend largely on insect pollinators for reproduction, and the proclivity of these species to use deceptive pollination strategies puts many of these species at a relatively higher rate of extinction. Therefore, pollination biology studies are needed to provide a scientific basis for proper conservation of orchids. At the community level, co-occurring mimic, non-mimic, and mimic signal providing plant species affect the reproductive fitness of orchids. Therefore, it is necessary to further study the co-evolution webs of deceptive orchids and pollinators along with other related biological and ecological factors.
Interactions among co-evolved species has been assumed to operate in a symmetrical manner, resulting in stable equilibrium or evolutionary stable strategies for the observed species. However, recent observational and experimental data highlight the existence of asymmetrical interactions, which may lead to meta-populations or non-equilibrium states (e.g. chaos) between co-evolved species. Here, we explore the asymmetrical interaction in the classic ‘fig-fig wasp’ co-evolution model system and show how such asymmetric interactions may produce meta-populations. It is well known that there are two different kinds of fig wasps inhabiting fig fruits (i.e. pollinator wasps and non-pollinating exploiter wasps). Exploiter wasps have a fitness advantage over pollinator wasps because they do not pay the cooperative cost. However, figs can effectively restrict exploiter wasps, and reward the pollinator wasps, resulting in complex asymmetric interactions among species. Specifically, the discriminative restriction of paretic wasps by fig trees will cause drastic population decreases or even local extinction of the exploiter species in some fig trees, syconia, or associated habitats. In patches where populations of exploiters are low or extinct, pollinator wasps will immigrate leading to concomitant population size increases due to the high reward of fig trees. The prosperity of pollinator wasps will then attract more exploiters, and population increases of exploiter wasps will lead to the sanction by fig trees again. Over the long term, populations of different wasps will chaotically oscillate either temporally or evolutionary through asymmetric interactions.
One of the main purposes of scientific research is to form questions and collect data to find patterns that best explain a particular process. In plant reproductive ecology, scientists have found important patterns including overwhelming occurrence of co-sexual flowers, separate flowering and fruiting periods, low seed-set ratio, simultaneous mass blooming, high occurrence of outcrossing in harsh habitats, interactions of mating systems and life-history, flower differentiations on the same inflorescence, and heteranthery (stamen differentiations in same flower). The underlying mechanisms of these patterns are in debate and are still in need of further examination. In this paper, we emphasize resource allocation at different levels, i.e. individual, inflorescence, and flower, and try to explain above patterns to reconcile some contradictory results obtained in studies based on different foci. Resource and sexual allocations directly determine the sexual role of a flower and floral traits, and as a consequence, plant mating systems are determined. In the future, studies considering both ecological factors and hierarchical levels will become more important and it is essential to focus more effort to study resource allocation to gain greater understanding and accurate predictions of floral adaptations and evolution.
Biodiversity Committee, CAS
Botanical Society of China
Institute of Botany, CAS
Institute of Zoology, CAS
Institute of Microbiology, CAS
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