AEROBIOLOGY AND POLLEN CAPTURE OF ORCHARD-GROWN PISTACIA VERA (ANACARDIACEAE)

The phenology of pollen release and pollen capture by Pistacia vera was studied in the field and laboratory respectively. Inflorescences of Pistacia vera were examined in a wind tunnel to determine whether the behavior of airborne conspecific pollen around receptive flowers differed as a result of changes in the shape and size of the inflorescence. In addition, the behavior of unclumped (single) and clumped pollen grains was studied to determine differences in the probability of their capture. Wind speeds within a commercial orchard during pollen shedding averaged 0.9–2.2 m/sec and atmospheric pollen concentrations were highest between 0900–1100 hr MST. Each of three stages in inflorescence development (defined on the basis of the number of exserted stigmas) was examined under identical ambient airflow conditions with equal concentrations of airborne pollen (1,000 grains/m³). The general pattern of pollen grain motion involves direct inertial collision by windward surfaces and by sedimentation of pollen onto leeward surfaces; clumped pollen rarely sedimented onto leeward surfaces. Small changes in ambient wind speed (0.5 m/sec to 1.0 m/sec) produced significant changes in the pattern of pollen motion around inflorescences and altered the number of pollen grains captured by leeward surfaces. Thus, wind pollination in P. vera is affected both by windspeed and by the shape or size of flower clusters. Differences in the behavior of clumped and unclumped pollen result from their inertial properties and responsiveness to local changes in the direction and speed of airflow. Unclumped pollen has a higher probability of being captured by leeward surfaces. The apparent insensitivity of pollen motion to differences in inflorescence size may ensure equitable pollination during the acropetal development of flowers.     

WIND POLLINATION OF TAXUS CUSPIDATA

The air disturbance patterns created by and around the ovules of Taxus cuspidata are quantified for various orientations to the direction of ambient airflow, and are shown to largely dictate the motion (vectoral trajectories) and mode of deposition of windborne pollen on ovule surfaces. Perpendicular orientation to the direction of airflow results in two regions characterized by high densities of adhering pollen — one on the windward surface of the ovule, resulting from direct inertial collision, and another on the leeward surface resulting from non-inertial sedimentation. Parallel and inclined orientations of the ovule to the direction of airflow produce quantitative and qualitative variations in the pattern of adhering pollen resulting from inertial and non-inertial deposition. Direct collision of windborne pollen grains with the micropylar ends of ovules occurs for all orientations to wind direction. The aerodynamics of the ovulate shoot complex of Taxus cuspidata is related to that previously described for conifer ovulate cones, cycad megastrobili, and simulated wind tunnel analyses of archaic Paleozoic ovules based on scale models. Water transport of pollen (adhering to integument and bract surfaces) to micropyles quantitatively alters the distribution of adhering pollen grains on ovule surfaces. Although there is no evidence that pollen grains of this species are osmotically ruptured, observations do not preclude the possibility that water transport of pollen may reduce the number of viable pollen grains reaching the micropyle.     

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.     

AERODYNAMICS OF EPHEDRA TRIFURCA: I. POLLEN GRAIN VELOCITY FIELDS AROUND STEMS BEARING OVULES

The behavior of pollen grains within the airspace around Ephedra trifurca is described. Vectoral analyses of pollen grains moving around stems and ovules indicate a complex pattern of directional and magnitudinal changes in trajectories that can be related to the geometries of surfaces that obstruct airflow. Pollen grains, passing around cylindrical stems oriented normal to the direction of ambient airflow, are deflected in circumrotating non-laminar flow-patterns. Stems tilted downwind deflect pollen grains into trajectories along leeward surfaces of stems. These trajectories travel acropetally in a spiraling pattern and may intersect airflow patterns created around and by ovules. Computer analyses of pollen motion in the vicinity of ovules indicate that pollen vector-direction is highly canalized and directed toward micropyles. Within the immediate vicinity of micropyles, which produce pollination droplets, analyses indicate that the magnitudinal variance of pollen grain vectors is high (spanning three orders of magnitude). This variance coincides with dramatic changes in the local Reynolds numbers, resulting in a localized region around the micropyle in which neither viscous nor inertial forces predominate. Based on additional aerodynamics parameters (vector curl, vector-divergence, and vector curl-differential) it is shown that the region around the pollination-droplet is characteristically a “pollen sink” (pollen grains collect in this airspace) in which abrupt changes can occur in the angular momenta of airborne pollen grains. These aerodynamic analyses suggest that the morphology of ovules and the stems to which they are attached facilitates pollen capture by creating an aerodynamic “singularity” (= a unique region) around the pollination-droplet.     

THE MOTION OF WINDBORNE POLLEN GRAINS AROUND CONIFER OVULATE CONES: IMPLICATIONS ON WIND POLLINATION

Comparisons are presented between the three-dimensional airflow patterns created around and by a scale model of a conifer ovulate cone and the trajectories of windborne pollen grains around Picea, Larix, and Pinus ovulate cones. Three general components of the airflow pattern around an ovulate cone model are 1) doldrum-like eddies, rotating over the adaxial surfaces of cone scales and directed toward attached ovules, 2) airflow spiralling around the cone axis along cone scale orthostichies and parastichies, and 3) a complex pattern of vortices (“umbilicus”) directed toward the leeward surface of the ovulate cone. The observed trajectories of pollen grains around cones of Picea, Larix, and Pinus conform to two of these three airflow components: 1) pollen grains are seen to roll along cone scales toward the distal scale margin and to become reentrained in airflow directed backward toward attached ovules, and 2) pollen grains passing around the cone are deflected into the “umbilicus” airflow pattern, where they either settle on or impact with cone scales (approach trajectories), or where they approach the leeward cone surface but are deflected away by airflow passing under the cone (Z-shaped trajectories). Vectoral analyses of pollen grain motion reveal a complex pattern of trajectories influenced by boundary layer conditions defined by ovulate cone geometry and ambient airflow speed. Wind tunnel studies of ovulate cones subtended by leaves and stem indicate that leaves circumscribing the cone act as a snowfence, deflecting windborne pollen toward the cone. Vectoral analyses of airflow patterns and pollen grain trajectories close to ovulate cones indicate that wind pollination in conifers is a non-stochastic aerodynamic process influenced by cone-leaf morphology and the behavior of pollen grains as windborne particles.     

AERODYNAMICS OF WIND POLLINATION IN SIMMONDSIA CHINENSIS (LINK) SCHNEIDER

Wind tunnel analyses of Simmondsia chinensis (Link) Schneider or “jojoba” were conducted to quantify the behavior of airborne pollen grains around individual branches and leaves and near individual carpellate flowers. Field data (wind velocity) were used to ensure a correspondence between wind tunnel and natural conditions. Based upon the visualization of individual pollen grain trajectories, it is concluded that pollen deposition on stigmatic surfaces is influenced by large-scale aerodynamic patterns, generated by foliage leaves, and small-scale airflow patterns, formed around and by floral parts and stigmas. Leaves are seen to deflect airborne pollen grains into trajectories that can intersect ambient airflow at 90° angles, showering decumbent carpellate flowers with pollen. Similarly, flowers can deflect pollen upward and downwind, toward other flowers. The extent of floral bract and sepal recurvature is shown to influence the extent of pollen deposition by determining the characteristic airflow pattern around stigmas. Available evidence concerning the relatively recent evolutionary transition to anemophily in Simmondsia is interpreted within the context of morphological adaptations and exaptations favoring wind pollination.     

AEROBIOLOGY OF SYMPLOCARPUS FOETIDUS: INTERACTIONS BETWEEN THE SPATHE AND SPADIX

The aerobiology of the skunk cabbage, Symplocarpus foetidus (l .) Nutt., is examined as a factor contributing to efficient pollination and temperature regulation around the spadix. Field measurements show that the compass orientation of the asymmetrical opening of the spathe is random, while wind tunnel studies reveal that similar patterns of airflow are generated around the spadix regardless of the orientation of the spathe opening to the direction of airflow. Temperature measurements within a model of the inflorescence reveal that airflow around the spathe effectively maintains heat generated by the spadix, even at airflow speeds of 1.5 m/s. These results are discussed as exaptations of the spathe for pollination and for temperature regulation in sub-freezing weather.     

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     

THE AERODYNAMICS OF POLLEN CAPTURE IN TWO SYMPATRIC EPHEDRA SPECIES

Wind-tunnel analyses of the behavior of airborne pollen around ovules of two Ephedra species (E. trifurca and E. nevadensis) indicate that at certain airflow speeds (0.5 m/sec and 1.0 m/sec) each species is capable of biasing pollination in favor of conspecific pollen. A computer procedure was designed to evaluate the physical basis for this aerodynamic discrimination. This procedure indicates that differences in size and density confer significantly different inertial properties to the two pollen species. Operating within the specific aerodynamic environments generated around ovules from each species, these differences are sufficient to account for the biases observed in the probability of pollination. Within natural populations, there exists significant variation in pollen size (and possibly in density). Accordingly, it is possible that, under certain ambient wind conditions, ovules from each species can select subsets of the entire airborne population of Ephedra pollen.     

REPRODUCTIVE BIOLOGY OF APIACEAE. II. CRYPTIC SPECIALIZATION AND FLORAL EVOLUTION IN THASPIUM AND ZIZIA

The classification of specialized floral syndromes has imposed a bias in the interpretation of pollination systems which may be either more generalized, or more specialized, than we have universally acknowledged. An analysis of floral biology in two umbellifer genera, Thaspium and Zizia, was undertaken in order to determine the extent to which cryptic floral or inflorescence variations determine pollination specialization despite a broad visitor spectrum and open reward system. Separate analyses were made of the primary attractants, nectar and pollen, and the secondary attractants, floral color and floral and inflorescence structure in conjunction with analyses of pollinator movements, stigmatic pollen loads and fruit set. All data support the conclusion that cryptic variation in floral and inflorescence characters enhance specialization for pollination by solitary bees or syrphid flies. In addition, evidence is presented for the importance of the oligolectic relationship between taxa of Thaspium and Zizia and the solitary bee, Andrena ziziae. The need for more experimental work both to further define the oligolectic relationship and to understand how floral and inflorescence color and structure affect insect movements is especially revealed by this study. The degree of pollination specialization in Thaspium and Zizia is not uncommon in Apiaceae and has important implications for floral evolution in this family and other plant groups with pollination systems categorized as “promiscuous.”     

POLLEN INTERFERENCE AND CRYPTIC SELF-FERTILITY IN CAMPSIS RADICANS

The effect of self pollen on the success of cross pollinations was studied in Campsis radicans (L.) Seem., a species previously considered self-sterile. The application of self pollen to stigmas in combination with or preceding the application of cross pollen markedly reduced the likelihood of fruit production. This effect was not due to the dilution of cross pollen nor to physical blocking of the stigmatic surface, since mixtures of talc and cross pollen were as effective as pure cross pollen in causing fruit production. Pollen tubes produced by self pollen grew at rates similar to those from cross pollen, and penetrated the ovary. The interference caused by self pollen appears to take place in the ovary, although it cannot be stated to what degree it is prezygotic or postzygotic. The marked protandry occurring in C. radicans is presumed to be due at least partly to selection for avoidance of these negative effects on female reproductive success. Up to 33% of viable seeds from mixed self + cross pollinations were sired by self pollen. The term “cryptic self-fertility” is coined to describe this phenomenon where pollination with loads of pure self pollen rarely or never yields fruit, but pollination using mixtures of self and cross pollen yields fruit containing considerable numbers of selfed seed. Estimates of selfing frequency that are based on pollination using loads of purely self pollen will be in error for species possessing cryptic self-fertility.     

Population Structure and Reproductive Biology of Saururus cernuus L. (Saururaceae)

Abstract The population structure and reproductive biology of Saururus cernuus (Lizard's Tail; Saururaceae; Piperales), is documented in five sites in southern Louisiana (Mississippi Delta). The species is common throughout the southeastern United States in marshes, along streams, edges of lakes, and in the understory of moist forests. The clonal species exhibits sexual and vegetative reproduction. Wind and insects both play important roles in pollination. Pollen may be borne by insects directly. Alternatively, the pollen may be borne by wind after its release is triggered from pendulous floral spikes (the “Lizard's Tail”) by either wind or insect landings (insect-mediated wind pollination). The plants are self-incompatible and seed set results from a combination of pollination modes with wind pollination being the primary mode (rare in the Magnoliidae). Inflorescence and floral structure exhibit adaptive features that facilitate the various modes of pollen transfer, viz., numerous, small scented, protogynous flowers with no perianth, ultraviolet patterns produced by stamen filaments, small pollen grains, curved inflorescences, and exerted stamens, etc. Fruit production and seed germination are documented and plant growth and densities are compared in sunny versus forest sites.     

AIRFLOW PATTERNS AROUND SOME EARLY SEED PLANT OVULES AND CUPULES: IMPLICATIONS CONCERNING EFFICIENCY IN WIND POLLINATION

Aerodynamic analyses showing characteristic airflow patterns and the potential for wind-mediated pollination are presented for models of Paleozoic (Carboniferous) ovules and ovulate cupules (i.e., Genomosperma kidstoni, G. latens, Salpingostoma dasu, Physostoma elegans, Eurystoma angulare, and Stamnostoma huttonense). Lobes on ovules and cupules are shown to produce localized regions of turbulent flow with a concomitant reduction in airflow velocity. Data based upon models that mimic the characteristics of windborne pollen (= pseudopollen) show that these regions of turbulent flow correspond to those in which suspended pseudopollen impact with ovule and/or cupule surfaces. These data have bearing on a sequence of ovule morphologies purported to show the evolution of the integument by the progressive reduction in length of “preintegumentary” lobes and their acropetal fusion. As the preintegumentary lobes of the models studied consolidate around the megasporangium, regions of turbulent flow and high pseudopollen impact become localized around the pollen chamber or salpinx. The general morphologic trend envisioned for the evolution of the ovule is seen to be associated with an aerodynamic streamlining and an increased potential for wind-mediated pollination. Data for hair-bearing ovules and for ovulate cupules are discussed within the context of possible selective pressures favouring streamlining.     

INCOMPATIBILITY AND THE POLLEN ECONOMY OF JEPSONIA PARRYI

Jepsonia parryi (Saxifragaceae) has heterostylous flowers and is strongly self-incompatible. Pin flowers have long styles, large stigmas, short stamens, and numerous, small pollen grains with finely sculptured walls. Thrum flowers have short styles, small stigmas, long stamens, and fewer, larger pollen grains with coarsely sculptured walls. Pin plants and thrum plants occur in a 1:1 ratio in field populations. Although the insect pollinators of J. parryi transfer ample compatible pollen to pin and thrum stigmas to account for full seed production, much of the pollen deposited on stigmas is incompatible. Analysis of the pollen deposits on stigmas collected from field populations indicates that compatible “legitimate” pollination of pin and thrum flowers is essentially random and is not obviously aided by floral dimorphism. It is suggested that although heterostyly had a positive adaptive value in the past evolutionary history of Jepsonia it is no longer adaptive under the present pollination regime, although it is maintained because of its strong genetic fixity.     

POLLINATION DROP IN RELATION TO CONE MORPHOLOGY IN PODOCARPACEAE: A NOVEL REPRODUCTIVE MECHANISM

Observation of ovulate cones at the time of pollination in the southern coniferous family Podocarpaceae demonstrates a distinctive method of pollen capture, involving an extended pollination drop. Ovules in all genera of the family are orthotropous and single within the axil of each fertile bract. In Microstrobus and Phyllocladus ovules are erect (i.e., the micropyle directed away from the cone axis) and are not associated with an ovule-supporting structure (epimatium). Pollen in these two genera must land directly on the pollination drop in the way usual for gymnosperms, as observed in Phyllocladus. In all other genera, the ovule is inverted (i.e., the micropyle is directed toward the cone axis) and supported by a specialized ovule-supporting structure (epimatium). In Saxegothaea there is no pollination drop and gametes are delivered to the ovule by pollen tube growth. Pollination drops were observed in seven of the remaining genera. In these genera the drop extends over the adjacent bract surface or cone axis and can retain pollen that has arrived prior to drop secretion (“pollen scavenging”). The pollen floats upward into the micropylar cavity. The configuration of the cone in other genera in which a pollination drop has not yet been observed directly suggests that pollen scavenging is general within the family and may increase pollination efficiency by extending pollination in space and time. Increased pollination efficiency may relate to the reduction of ovule number in each cone, often to one in many genera, a derived condition. A biological perspective suggests that animal dispersal of large seeds may be the ultimate adaptive driving force that has generated the need for greater pollination efficiency.     

Gibberellin-like Substances in Developing Barley Grain and Their Relation to Dry Weight Increase

Gibberellin-like activity of two varieties of barley (Hordeum vulgare L.) at different stages of grain development was determined by barley endosperm bioassay (acid phosphatase bioassay). Activity of the acidic ethyl-acetate fraction (“free” GAs) in both varieties displayed two maxima, a first maximum at the 9th day and a second one 20 to 21 days after pollination. Activity of the n-butanol fraction (“bound” GAs) first dropped to a minimum level at the 9th day, then increased to reach a maximum 32 days after pollination, and finally decreased again towards maturity. From the 9th day after pollination, a conversion of “free” GAs to “bound” GAs has probably occurred. From the 12th day after pollination, the curves of rate of dry weight increase and of “free” GAs run nearly parallel, but the latter reached its maximum about 2–4 days earlier than the former. The results indicate that gibberellins may participate in the regulation of the accumulation processes into the barley grain.     

FLORAL PAEDOMORPHY LEADS TO SECONDARY SPECIALIZATION IN POLLINATION OF MADAGASCAR DALECHAMPIA (EUPHORBIACEAE)

The traditional evolutionary interpretation of Von Baer's “laws” of embryology is that retention of early developmental forms into adulthood (paedomorphosis) leads to the evolution of simpler or more generalized morphology and ecology. Here we show that paedomorphosis can also be involved in an increase in ecological specialization, in this case of plant–pollinator relationships. A paedomorphic transition from generalized pollination (by several functional types of pollinators) to specialized pollination (by one or a few species in one functional type) occurred in a clade of endemic Madagascar vines (Dalechampia spp., Euphorbiaceae). This evolutionary transition involved staminate flowers that fail to develop “normally,” instead holding mature pollen inside virtually unopened, bud‐like flowers. This paedomorphic morphology restricts reward access to “buzz‐pollinating” bees, including Xylocopa species (carpenter bees), which can remove pollen by sonication. This is one of very few reports of paedomorphic specialization, and, as far as we are aware, the first documented case of a rapid reversal to specialized pollination in a lineage of plants that had previously switched from specialized to generalized pollination in conjunction with dispersing to a new region.     

Intensified wind pollination mediated by pollen dimorphism after range expansion in an ambophilous biennial Aconitum gymnandrum

Pollination systems and associated floral traits generally differ between core and marginal populations of a species. However, such differences are rarely examined in plants with a mixed wind‐ and bumblebee‐pollination system, and the role of wind pollination during range expansion in ambophilous plants remains unclear. We compared floral traits and the contributions of bumblebee and wind pollination in refugium and marginal populations of the ambophilous plant Aconitum gymnandrum. We found that most floral traits differed between the two populations, and those traits associated with the shift to wind pollination were pronounced in the marginal population. Bumblebee visitation rates varied significantly, but were generally low in the marginal population. Wind pollination occurred in both populations, and the efficiency was lower than that of bumblebee pollination. Two types of pollen grains, namely round and fusiform pollen, were transported to a stigma by bumblebees and wind, but fusiform pollen contributed to wind pollination to a larger degree, especially in the marginal population. Our results suggest that wind pollination was enhanced by pollen dimorphism in the marginal population of A. gymnandrum, and wind pollination may provide reproductive assurance when bumblebee activity is unpredictable during range expansion, indicating that ambophily is stable in this species and shift in pollination system could be common when plants colonize new habitats.     

The evolution of ovule number and flower size in wind-pollinated plants

In angiosperms, ovules are "packaged" within individual flowers, and an optimal strategy should occur depending on pollination and resource conditions. In animal-pollinated species, wide variation in ovule number per flower occurs, and this contrasts with wind-pollinated plants, where most species possess uniovulate flowers. This pattern is usually explained as an adaptive response to low pollen receipt in wind-pollinated species. Here, we develop a phenotypic model for the evolution of ovule number per flower that incorporates the aerodynamics of pollen capture and a fixed resource pool for provisioning of flowers, ovules, and seeds. Our results challenge the prevailing explanation for the association between uniovulate flowers and wind pollination. We demonstrate that when flowers are small and inexpensive, as they are in wind-pollinated species, ovule number should be minimized and lower than the average number of pollen tubes per style, even under stochastic pollination and fertilization regimes. The model predicts that plants benefit from producing many small inexpensive flowers, even though some flowers capture too few pollen grains to fertilize their ovules. Wind-pollinated plants with numerous flowers distributed throughout the inflorescence, each with a single ovule or a few ovules, sample more of the airstream, and this should maximize pollen capture and seed production.     

EXPERIMENTAL ASSESSMENT OF REPRODUCTIVE INTERACTIONS BETWEEN SYMPATRIC ASTER AND ERIGERON (ASTERACEAE) IN INTERIOR ALASKA

Erigeron glabellus and Aster sibiricus have similar flowers, share pollinators, but bloom sequentially in interior Alaska. Both species depend on insect pollination for seed set: the Erigeron is self-incompatible, and the Aster is apparently self-compatible but allogamous. To test the hypothesis that sequential blooming is maintained by natural selection generated by reproductive interference, we manipulated the flowering time of Erigeron, forcing it to bloom simultaneously with Aster, and measured female fecundity in both species. We found no evidence of reduced female fecundity in either species caused by the presence of the sympatric “competitor” or by artificial pollination with the heterospecific pollen prior to conspecific pollination. Two-species mixtures of simultaneously blooming Aster and Erigeron experienced significant interspecific visitation, which may, under natural conditions, cause loss of pollen to alien stigmas and depressed male fecundity, at least in Erigeron. We found no evidence that sequential blooming in Erigeron and Aster is maintained by depressed female fecundity through pollinator sharing. If sequential blooming is maintained by natural selection, it seems more likely to be the result of selection generated by depressed male fitness through pollen loss to alien stigmas.