POLLINATION SYSTEMS IN PASPALUM DILATATUM POIR. (POACEAE): AN EXAMPLE OF INSECT POLLINATION IN A TEMPERATE GRASS

The pollination of Paspalum dilatatum was studied in south-central Oklahoma during the summer of 1979. Pollen was liberated between 0700–0900 hr except on humid mornings (RH ≤ 80%), when there was a delay of 2–3 hr and a reduction in the total air-borne pollen concentration. A rapid decrease in air-borne pollen concentration with distance from the source results from: 1) individual pollen grains larger (50–70 μ in diam) than typical wind-pollinated plants, and 2) some pollen dispersed as clusters of grains. Several floral characters of P. dilatatum led to a hypothesis that this perennial grass may be entomophilous as well as anemophilous. Not only were the pollen grains larger than most other wind-pollinated taxa but the species produced fewer than 2,500 pollen grains per ovule. Three additional observations corroborate this view: 1) solitary bees (Halictidae) actively collect pollen during the morning, 2) the number of pollen grains per stigma was significantly (P < 0.001) greater on racemes exposed to both wind and bees than on racemes exposed only to wind, and 3) the combination of bees and wind as pollinators significantly (P < 0.001) increased seed set compared to wind alone.     

Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants

Background

The rich literature that characterizes the field of pollination biology has focused largely on animal-pollinated plants. At least 10 % of angiosperms are wind pollinated, and this mode of pollination has evolved on multiple occasions among unrelated lineages, and hence this discrepancy in research interest is surprising. Here, the evolution and functional ecology of pollination and mating in wind-pollinated plants are discussed, a theoretical framework for modelling the selection of wind pollination is outlined, and pollen capture and the occurrence of pollen limitation in diverse wind-pollinated herbs are investigated experimentally.

Scope and Conclusions

Wind pollination may commonly evolve to provide reproductive assurance when pollinators are scarce. Evidence is presented that pollen limitation in wind-pollinated plants may not be as common as it is in animal-pollinated species. The studies of pollen capture in wind-pollinated herbs demonstrate that pollen transfer efficiency is not substantially lower than in animal-pollinated plants as is often assumed. These findings challenge the explanation that the evolution of few ovules in wind-pollinated flowers is associated with low pollen loads. Floral and inflorescence architecture is crucial to pollination and mating because of the aerodynamics of wind pollination. Evidence is provided for the importance of plant height, floral position, and stamen and stigma characteristics in promoting effective pollen dispersal and capture. Finally, it is proposed that geitonogamous selfing may alleviate pollen limitation in many wind-pollinated plants with unisexual flowers.Key words: Wind pollination, reproductive assurance, pollen limitation, geitonogamy, sex allocation, inflorescence architecture, mating systems     

Leptokurtic pollen-flow,non-leptokurtic gene-flow in a wind-pollinated herb,Plantago lanceolata L.

Summary The purpose of this study was to simultaneously measure pollen dispersal distance and actual pollen-mediated gene-flow distance in a wind-pollinated herb, Plantago lanceolata. The pollen dispersal distribution, measured as pollen deposition in a wind tunnel, is leptokurtic, as expected from previous studies of wind-pollinated plants. Gene-flow, measured as seeds produced on rows of male-sterile inflorescences in the wind tunnel, is non-leptokurtic, peaking at an intermediate distance. The difference between the two distributions results from the tendency of the pollen grains to cluster. These pollen clusters are the units of gene dispersal, with clusters of intermediate and large size contributing disproportionately to gene-flow. Since many wind-pollinated species show pollen clustering (see text), the common assumption for wind-pollinated plants that gene-flow is leptokurtic requires re-examination. Gene-flow was also measured in an artifical outdoor population of male-steriles, containing a single pollen source plant in the center of the array. The gene flow distribution is significantly platykurtic, and has the same general properties outdoors, where wind speed and turbulence are uncontrolled, as it does in the wind tunnel. I estimated genetic neighborhood size based on my measure of gene-flow in the outdoor population. The estimate shows that populations of Plantago lanceolata will vary in effective number from a few tens of plants to more than five hundred plants, depending on the density of the population in question. Thus, the measured pollen-mediated gene-flow distribution and population density will interact to produce effective population sizes ranging from those in which there is no random genetic drift to those in which random genetic drift plays an important role in determining gene frequencies within and among populations. Despite the platykurtosis in the distribution, pollen-mediated gene dispersal distances are still quite limited, and considerable within and among-population genetic differentiation is to be expected in this species.     

The biomechanics of pollen release: new perspectives on the evolution of wind pollination in angiosperms

Evolutionary transitions from animal to wind pollination have occurred repeatedly during the history of the angiosperms, but the selective mechanisms remain elusive. Here, we propose that knowledge of pollen release biomechanics is critical for understanding the ecological and evolutionary processes underpinning this shift in pollination mode. Pollen release is the critical first stage of wind pollination (anemophily) and stamen properties are therefore likely to be under strong selection early in the transition. We describe current understanding of pollen release biomechanics to provide insights on the phenotypic and ecological drivers of wind pollination. Pollen release occurs when detachment forces dominate resistive forces retaining pollen within anthers. Detachment forces can be active or passive depending on whether they require energy input from the environment. Passive release is more widespread in anemophilous species and involves processes driven by steady or unsteady aerodynamic forces or turbulence-induced vibrations that shake pollen from anthers. We review empirical and theoretical studies suggesting that stamen vibration is likely to be a key mechanism of pollen release. The vibration response is governed by morphological and biomechanical properties of stamens, which may undergo divergent selection in the presence or absence of pollinators. Resistive forces have rarely been investigated for pollen within anthers, but are probably sensitive to environmental conditions and depend on flower age, varying systematically between animal- and wind-pollinated species. Animal and wind pollination are traditionally viewed as dichotomous alternatives because they are usually associated with strikingly different pollination syndromes. But this perspective has diverted attention from subtler, continuously varying traits which mediate the fluid dynamic process of pollen release. Reinterpreting the flower as a biomechanical entity that responds to fluctuating environmental forces may provide a promising way forward. We conclude by identifying several profitable areas for future research to obtain deeper insight into the evolution of wind pollination.     

Breeding System and pollination of selected plants endemic to Juan Fernandez Islands

We conducted field studies on the Juan Fernández Islands flora on the breeding system of 25 endemic species from 17 families. We recorded data on flower features, pollen and ovule number, pollen/ovule ratio, pollen size, self-compatibility, floral visitors, and pollination. Flowers are mostly hermaphrodite, inconspicuous, small, and green. Six species are dioecious. Over 80% of the cosexual species are self compatible. However, many species are dichogamous (mostly protandrous); thus, even the self-compatible species may require pollen transfer. Selfing through geitonogamy seems to be the most common system, and several species express mixed breeding systems. Floral visitors are uncommon to rare, except for two hummingbird species (one native and one endemic) that visit five species we studied. In more than 300 h of observation of flowers over three field seasons, we detected only 23 native insect visits representing ten species (Diptera, Lepidoptera, and Coleoptera). One species each of an introduced ant and an introduced bee were also observed on some flowers, all near the single human settlement of San Juan Bautista. Wind directly moving pollen, or indirectly via shaking the flowers, is the most important pollen distribution mechanism. The majority of the wind-pollinated species bear some typical anemophilous features, but also others not characteristic of wind pollination, that presumably represent the condition of their biotically pollinated ancestors. Floral features often reflect ancestral reproductive systems, so floral biology studies of oceanic islands in particular must be done with cognizance of presumed ancestral forms, because the observed characters can be misleading.     

Abiotic pollen and pollination: Ecological, functional, and evolutionary perspectives

The transport and capture of pollen in ~20% of all angiosperm families occurs in air and water. In other words, pollination is abiotic and occurs via the fluid media, not an animal vector. Whereas some early concepts considered abiotic pollination to be largely a stochastic phenomenon, there is sufficient evidence to indicate that wind pollination (i.e. anemophily) and water pollination (i.e. hydrophily) have deterministic features and are sophisticated fluid dynamic solutions to the problem of pollen release, dispersal, and capture.An abiotic pollination syndrome is defined in which there is spatial or temporal separation of carpellate and staminate flowers, which are drab, a reduction in perianth parts, stigmas and anthers are exposed to the fluid, and typically unclumped pollen may be produced in large amounts. Separate pollination syndromes are defined for anemophilous (i.e. wind-pollinated), ephydrophilous (i.e. surface-pollinated), and hydrophilous (i.e. submarine-pollinated) plants. Distinctions are based on habitat and physical conditions for pollination, pollen size, shape, and ultrastructure, morphology and ultrastructure of stigmas, and outcrossing rates. For example, anemophilous pollen are spherical and small, ephydrophilous pollen are spherical or reniform and large, while hydrophilous pollen are filiform (i.e. filamentous) or functionally filiform. The pollination mechanisms and mechanics associated with these syndromes reveals a strong evolutionary relationship between plant morphology and fluid dynamics.     

Allergenicity of Acroptilon repens and Juglans regia pollen in rats

Pollen proteins that are located in the cytoplasm or on the surface of the exine can function as allergens and evoke immune system responses in sensitive patients, leading to allergic rhinitis and asthma. In this research, the pollen allergenicity and ability to induce IgE response of the pollen of two plant species were studied in rats. Acroptilon repens is an herbaceous, invasive plant with entomophilous pollen, while Juglans regia which is a tree crop produces anemophilous pollen. Immunoblot analysis using sera of sensitised rats revealed IgE reactivity to three protein bands including the 70, 41 and 25.12 kDa bands present in the A. repens pollen extract, while only one single immunogenic band of 11 kDa was detected in J. regia pollen extract. Both pollen extracts increased the eosinophil content and caused some clinical signs of allergy in treated rats. The results showed that both entomophilous and anemophilous pollen can be allergenic.     

POLLEN ENERGETICS AND POLLINATION MODES

The caloric content of pollen for several different species was determined by using a semimicro oxygen bomb calorimeter. The species studied were divided into subsets for statistical comparisons. The subsets considered were wind-pollinated dicots, monocots and gymnosperms; insect-pollinated dicots; and taxonomic subclasses of the wind-pollinated angiosperms (Asteridae, Hamamelidae, Caryophyllidae and Commelinidae). The results indicated a statistically significant caloric content difference (0.05 or higher) between wind-pollinated dicots vs. monocots and gymnosperms. There was no statistical difference between wind-pollinated dicots and insect-pollinated dicots. All subclasses were significantly different from one another. A statistically significant difference was found between two tribes in the Asteraceae which have shifted from insect to wind pollination, providing additional evidence for an independent evolution of the two. The need for future research in this area is discussed.     

EQUATIONS FOR THE MOTION OF AIRBORNE POLLEN GRAINS NEAR THE OVULATE ORGANS OF WIND-POLLINATED PLANTS

A technique is presented that is capable of predicting the motion of airborne pollen grains and the probability of pollen capture by wind-pollinated plants. Equations for the motion of rigid-walled particles (= pollen grains, spores, or Sephadex beads) in a supporting, compressible fluid (= air) are derived from the first principles of fluid dynamics. These equations are incorporated into a computer program (MODEL) which can be used with a desktop computer. The operation of MODEL requires empirical data on the pattern of airflow or the motion of a pollen species around the surfaces of the taxonomically relevant ovulate plant organ. With this information, MODEL can predict the behavior of any pollen species for which physical properties (size and density) are specified or empirically known. The significance of this procedure lies in the quantification of physical phenomena that influence the mechanics and fluid dynamics of pollen capture in wind pollination. The technique is illustrated and tested by its application to two grass species (Setaria geniculata and Agrostis hiemalis) for which velocity fields of pollen motion have been previously reported.     

Effect of canopy closure on pollen dispersal in a wind-pollinated species (Fagus sylvatica L.)

The effect of non-reproductive trees and saplings as a physical barrier to pollen dispersal in wind-pollinated species?? forests has not received enough attention in the literature so far. The neighborhood seedling model was used to fit pollen dispersal models for beech at different stages of gap recolonization and to elucidate the effect of saplings as a physical barrier on pollen dispersal at local scale. Phenological overlap of leaf emergence, and pollen release as well as wind directionality patterns were also examined. As a case study, we used a mixed beech-oak forest that was managed as open woodland until 1974. The ban on entry of cattle has led to the recolonization of empty spaces by seedlings and saplings of beech (Fagus sylvatica L.) and two oak species (Quercus petraea (Matts.) Liebl. and Q. pyrenaica Willd.) and, at last, to canopy closure. The average pollen dispersal distance for the first plants that regenerated in the gaps was almost twice those found for recently installed seedlings and seeds collected in traps, supporting the hypothesis that the understory may act as a physical barrier to pollen dispersal. Although a substantial part of effective pollination directionality is at random, horizontal winds and vertical anabatic winds may explain some of this directionality. At the time of beech pollen release, leaves of beech and sessile oak are fully developed, enhancing pollen interception by the saplings. Explicit models of pollen dispersal for wind-pollinated trees should incorporate the effect of canopy closure caused by growth of saplings and account for leaf phenology of co-occurring species in the forest.     

外来入侵植物意大利苍耳的传粉生态学特性

从开花物候、花粉活力、柱头可受性、传粉媒介、花粉散布距离、雄性、雌性功能以及繁育系统等方面系统地研究了意大利苍耳的传粉生态学特性,旨在为揭示该物种成功入侵的机理提供科学依据。研究结果显示:意大利苍耳种群的花期较长,雌花花期可达40d,雄花花期可达30d。其雄性和雌性功能都很强,意大利苍耳单株雄花序和花粉量分别高达3847个/株和37903037粒/株,单株雌花序和单株胚珠数高达3847个/株和7694枚/株,种群平均结实率高达80.59%,即平均每株个体能形成6200枚成熟的果实。花粉活力的日变化呈单峰型曲线,早晨和傍晚的花粉活力最低,14:00时的活力高达99%。雌蕊柱头一经伸出总苞即具有可受性,可受期长达7d,开花后的3—4d柱头的可受性最强。意大利苍耳为风媒传粉植物,在4.5km/h的微风条件下,其花粉的散布距离可达45m,大量的花粉集中分布在距花粉源0—20m的范围内,这对于往往高密度连片分布的意大利苍耳种群来说无疑是一种高效的传粉策略。意大利苍耳的交配系统灵活多样,盛花期自然结实率达到100%,套袋试验结果表明该植物自交亲和,自株自然授粉的结实率高达93%。表明较长的花期、大量的雌雄花序及花粉数量、较高的花粉活力、较长的柱头可授期、较远的花粉风媒散布距离、混合交配系统、以及较高的结实率是意大利苍耳繁殖成功的重要保障,也是其成功入侵的重要原因。     

Transition from wind pollination to insect pollination in sedges: experimental evidence and functional traits

Transitions from wind pollination to insect pollination were pivotal to the radiation of land plants, yet only a handful are known and the trait shifts required are poorly understood. We tested the hypothesis that a transition to insect pollination took place in the ancestrally wind-pollinated sedges (Cyperaceae) and that floral traits modified during this transition have functional significance. We paired putatively insect-pollinated Cyperus obtusiflorus and Cyperus sphaerocephalus with related, co-flowering, co-occurring wind-pollinated species, and compared pairs in terms of pollination mode and functional roles of floral traits. Experimentally excluding insects reduced seed set by 56-89% in putatively insect-pollinated species but not in intermingled wind-pollinated species. The pollen of putatively insect-pollinated species was less motile in a wind tunnel than that of wind-pollinated species. Bees, beetles and flies preferred inflorescences, and color-matched white or yellow models, of putatively insect-pollinated species over inflorescences, or color-matched brown models, of wind-pollinated species. Floral scents of putatively insect-pollinated species were chemically consistent with those of other insect-pollinated plants, and attracted pollinators; wind-pollinated species were unscented. These results show that a transition from wind pollination to insect pollination occurred in sedges and shed new light on the function of traits involved in this important transition.     

EFFICACY OF WIND POLLINATION: POLLEN LOAD SIZE AND NATURAL MICROGAMETOPHYTE POPULATIONS IN WIND-POLLINATED STABEROHA BANKSII (RESTIONACEAE)

A detailed examination was made of the numbers of pollen grains and microgametophytes occurring on stigmas of a dioecious, wind-pollinated species, Staberoha banksii. The number of pollen grains per pistil ranged from 0 to over 100; and the mean pollen load size per pistil per plant varied from 4.4 to 28. Distance to the fourth nearest male plant was used as a measure of local pollen availability and accounted for 63.5% of the between-plant variation in pollen load size. In contrast, the number of microgametophytes did not show a leptokurtic decline with increasing distance from a pollen source. On average there were 5.19 microgametophytes per ovule, which is higher than all comparable data for insect-pollinated taxa, and 66% of the stigmas had two or more microgametophytes. Given that there is a single ovule per flower, there is considerable potential for gametophytic competition. Seedset was very high, averaging 93%, and showed no significant decline in isolated female plants. We suggest that the quantity of pollen is not limiting fertilization in this population and that wind may therefore be highly effective as a pollen vector.     

Estimating anisotropic pollen dispersal: a case study in Quercus lobata

The pollen dispersal distribution is an important element of the neighbourhood size of plant populations. Most methods aimed at estimating the dispersal curve assume that pollen dispersal is isotropic, but evidence indicates that this assumption does not hold for many plant species, particularly wind-pollinated species subject to prevailing winds during the pollination season. We propose here a method of detecting anisotropy of pollen dispersal and of gauging its intensity, based on the estimation of the differentiation of maternal pollen clouds (TWOGENER extraction), assuming that pollen dispersal is bivariate and normally distributed. We applied the new method to a case study in Quercus lobata, detecting only a modest level of anisotropy in pollen dispersal in a direction roughly similar to the prevailing wind direction. Finally, we conducted a simulation to explore the conditions under which anisotropy can be detected with this method, and we show that while anisotropy is detectable, in principle, it requires a large volume of data.     

Anemophilous plants select pollen from their own species from the air

In wind-tunnel experiments, Niklas (1985) has demonstrated the ability of anemophilous plants to select pollen from their own species from the airstream. However, there have been no field experiments to establish whether this operates in nature. We surveyed the pollents on the stigmas of four different, coextensive, dioecious anemophilous species surrounded by a Pinus radiata plantation. The alien pine pollen was overrepresented relative to background levels on only one of the four species. For all three indigenous species with both male and female plants in the area, the highest proportion — in all cases more than 40% — of the pollen found on their stigmas came from their own species. One indigenous species lacked male plants in the area; consequently, the results from this species are difficult to interpret. However, for all four species, there was at least 15% pine pollen, and some pollen of other indigenous species. These results suggest that there is some pollen selection, but that the mechanisms are may be not as effective as Niklas has suggested.     

OPTIMUM POLLEN AND FEMALE RECEPTOR SIZE FOR ANEMOPHILY

A set of mathematical models is developed to describe the relationship between the sizes of pollen grains and female receptors which result in maximum anemophilous pollen transfer. The models predict anemophilous plants should have Stokes numbers in the range of 1.0 to 2.72. The Stokes number is a function of both pollen size and effective receptive surface size. The models were tested with data gathered for 28 assumed anemophilous species and 20 known zoophilous species. The models identify anemophily with an accuracy of approximately 75%. If pollen size alone is used to determine anemophily, then accuracy drops to only 50%. The Stokes number criterion reported here could help in the determination of anemophily of extant and fossil plant taxa.     

Reproductive ecology and pollen representation among neotropical trees

Three years of pollen trapping data from Barro Colorado Island, Panama, are compared with local vegetation inventories. Two hypotheses relating pollen representation to ‘messy’ pollination and flower form are tested. Dioecious taxa were found to be over‐represented in pollen spectra compared with their occurrence in local forests. Similarly, anemophilous and ‘messy’ pollination types were found to be over‐represented. While anemophilous taxa were the best dispersed pollen types, zoophilous taxa were also well‐represented in dispersal classes of 20–40 m and > 40 m. Thus pollen arriving to lake sediments is most likely to be from anemophilous species or those zoophilous species exhibiting ‘messy’ pollination syndromes. Pollination mechanisms will predictably bias the fossil record against certain flower morphologies. These data are of significance to those using the fossil pollen record to reconstruct the timing and sequence of angiosperm evolution. These data help prioritize plants to be included in modern pollen reference collections and to focus the search for ‘unknown’ types on most‐likely candidate families.     

Pollen clumping and wind dispersal in an invasive angiosperm

Pollen dispersal is a fundamental aspect of plant reproductive biology that maintains connectivity between spatially separated populations. Pollen clumping, a characteristic feature of insect-pollinated plants, is generally assumed to be a detriment to wind pollination because clumps disperse shorter distances than do solitary pollen grains. Yet pollen clumps have been observed in dispersion studies of some widely distributed wind-pollinated species. We used Ambrosia artemisiifolia (common ragweed; Asteraceae), a successful invasive angiosperm, to investigate the effect of clumping on wind dispersal of pollen under natural conditions in a large field. Results of simultaneous measurements of clump size both in pollen shedding from male flowers and airborne pollen being dispersed in the atmosphere are combined with a transport model to show that rather than being detrimental, clumps may actually be advantageous for wind pollination. Initial clumps can pollinate the parent population, while smaller clumps that arise from breakup of larger clumps can cross-pollinate distant populations.     

Neither insects nor wind: ambophily in dioecious Chamaedorea palms (Arecaceae)

Pollination of Neotropical dioecious trees is commonly related to generalist insects. Similar data for non‐tree species with separated genders are inconclusive. Recent studies on pollination of dioecious Chamaedorea palms (Arecaceae) suggest that species are either insect‐ or wind‐pollinated. However, the wide variety of inflorescence and floral attributes within the genus suggests mixed pollination mode involving entomophily and anemophily. To evaluate this hypothesis, we studied the pollination of Chamaedorea costaricana, C. macrospadix, C. pinnatifrons and C. tepejilote in two montane forests in Costa Rica. A complementary morphological analysis of floral traits was carried out to distinguish species groups within the genus according to their most probable pollination mechanism. We conducted pollinator exclusion experiments, field observations on visitors to pistillate and staminate inflorescences, and trapped airborne pollen. A cluster analysis using 18 floral traits selected for their association with wind and insect pollination syndromes was carried out using 52 Chamaedorea species. Exclusion experiments showed that both wind and insects, mostly thrips (Thysanoptera), pollinated the studied species. Thrips used staminate inflorescences as brood sites and pollinated pistillate flowers by deception. Insects caught on pistillate inflorescences transported pollen, while traps proved that pollen is wind‐borne. Our empirical findings clearly suggest that pollination of dioecious Chamaedorea palms is likely to involve both insects and wind. A cluster analysis showed that the majority of studied species have a combination of floral traits that allow for both pollination modes. Our pollination experiments and morphological analysis both suggest that while some species may be completely entomophilous or anemophilous, ambophily might be a common condition within Chamaedorea. Our results propose a higher diversity of pollination mechanisms of Neotropical dioecious species than previously suggested.     

Analysis of cedar pollen time series: no evidence of low-dimensional chaotic behavior

Much of the current interest in pollen time series analysis is motivated by the possibility that pollen series arise from low-dimensional chaotic systems. If this is the case, short-range prediction using nonlinear modeling is justified and would produce high-quality forecasts that could be useful in providing pollen alerts to allergy sufferers. To date, contradictory reports about the characterization of the dynamics of pollen series can be found in the literature. Pollen series have been alternatively described as featuring and not featuring deterministic chaotic behavior. We showed that the choice of test for detection of deterministic chaos in pollen series is difficult because pollen series exhibit power spectra. This is a characteristic that is also produced by colored noise series, which mimic deterministic chaos in most tests. We proposed to apply the Ikeguchi–Aihara test to properly detect the presence of deterministic chaos in pollen series. We examined the dynamics of cedar (Cryptomeria japonica) hourly pollen series by means of the Ikeguchi–Aihara test and concluded that these pollen series cannot be described as low-dimensional deterministic chaos. Therefore, the application of low-dimensional chaotic deterministic models to the prediction of short-range pollen concentration will not result in high-accuracy pollen forecasts even though these models may provide useful forecasts for certain applications. We believe that our conclusion can be generalized to pollen series from other wind-pollinated plant species, as wind speed, the forcing parameter of the pollen emission and transport, is best described as a nondeterministic series that originates in the high dimensionality of the atmosphere.