Submarine pollination in the marine angiosperm Zostera marina (Zosteraceae). II. Pollen transport in flow fields and capture by stigmas

Flow chamber observations of the filamentous pollen of Zostera marina L. (Potamogetonales) revealed that pollen rotated and moved toward inflorescences where they were captured by stigmas. The mechanics of this abiotic pollination process were examined and found to be related to the flow environment around emergent flowers. The translational movement of pollen was imparted by the advection of the fluid (e.g., pollen kinetic energy, K, ranged from 0.8 x 10-14 to 2.4 x 10-14 J, and the average K of the fluid was _ 0.7 x 10-14 J), while the rotational motion was imparted by the fluid shear stress (tau) within the velocity gradient (e.g., pollen shear stress, sigmat = omegamu where omega is the rotational velocity and mu is the dynamic viscosity, ranged from 3.4 x 10-4 to 26 x 10-4 Pa, and the average fluid shear stress was tau _ 10 x 10-4 Pa; Ackerman, 1997, American Journal of Botany 84: 1099-1109). These results indicate that there is a greater potential for pollination by filamentous pollen relative to spherical pollen. Functionally, while spherical pollen needs to be directly upstream from stigmas to be captured, filamentous pollen need only be in the vicinity of inflorescences and flowers to be captured by stigmas. Thus, in addition to direct interception on stigmas, filamentous pollen can be captured while they rotate past flowers or when they are redirected through the velocity gradient towards flowers. Filamentous pollen is an adaptation to submarine pollination in seagrasses.     

Surface and submarine pollination in the seagrass Zoster a marina L

COX, P. A., LAUSHMAN, R. H. & RUCKLESHAUS, M. H., 1992. Surface and submarine pollination in the seagrass Zostera marina L. Hydrophilous plants can be divided into three ecological categories depending upon whether their pollen is transported above, on, or under the water surface. A mixed mode of submarine and surface hydrophilous pollination occurs in the seagrass Zostera marina L. In the surface mode of pollination, pollen rafts or 'search vehicles' which superficially resemble snowflakes, form at low tide and are transported on the surface of the sea by winds and water currents. Some of the search vehicles collide with the floating female stigmas, effecting pollination. In the submarine mode of pollination, small pollen masses resembling whisk brooms travel beneath the surface of the water. Although we failed to observe a submarine pollination event, SEM analysis of stigmas from subtidal populations confirms that submarine pollination does occur in Z. marina . However, observations of stigmas positioned at and below the surface of the water show surface pollination to be highly efficient. Electrophoretic evaluation of both subtidal and intertidal populations indicates significant genetic variation between populations. Given the high flux rates of surface-borne pollen and pollen viability in excess of 5 h, it is likely that surface-borne pollen is a major source of gene flow in Zostera marina populations.     

TWO-DIMENSIONAL POLLINATION IN HYDROPHILOUS PLANTS: CONVERGENT EVOLUTION IN THE GENERA HALODULE (CYMODOCEACEAE), HALOPHILA (HYDROCHARITACEAE), RUPPIA (RUPPIACEAE), AND LEPILAENA (ZANNICHELLIACEAE)

In most plant species with abiotic pollination systems, pollen is dispersed in three dimensions. Theoretical considerations suggest, however, that there are significant advantages for two-dimensional pollination systems over three-dimensional systems, especially if pollen is dispersed in conveyances or aggregations of large diameter. We report that two-dimensional pollination systems occur in the genera Halodule, Halophila, Lepilaena, and Ruppia, where pollen grains are not transported through the water singly, but in rafts or search vehicles. These genera possess unusual pollen morphologies which facilitate assemblage of pollen grains into search vehicles. These floating search vehicles have large diameters, thus greatly increasing probability of encountering a stigma. The grains have a hydrophobic surface that appears to mediate adhesion by an external coating of proteins and carbohydrates. Similar adaptations to two-dimensional pollination are found in the target organs, the stigmas. The long filamentous stigmas of the marine genera float, as do the indusiate stigmas of the freshwater genera, creating small depressions in the water surface. Pollination occurs through the collision of a moving search vehicle with a floating stigma. The existence of similar pollen search vehicles, stigma morphologies, and flowering phenologies in these unrelated hydrophilous genera evidences convergent evolution towards efficient search strategies in surface-pollinated aquatic plants.     

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.     

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.     

Evolution of pollination system and characters of stigmas in Najadales

Diverse ways of pollination, including aerial, epihydrophilous and hypohydrophilous ones occur in the Najadales. Although the knowledge of pollination biology in this order has been largely accumulated in recent years, most researchers ignored the role of stigmas in the pollination process. Based on the previous works, we supplemented observations on stigmatic characters and pollination mechanism in nine species from four families. The flowers of Aponogeton lakhonensis ( Aponogetonaceae ), Triglochin palustre ( Juncaginaceae), Potamogeton crispus, P. distinctus, P. gramineus, P. pectinatus, P. perfoliatus, P. pusillus (Potamogetonaceae), are all found to open above or on water surface. Stigmas in these species have a large surface area. Correspondingly, the pollen grains are all found to be globular. Of the eight species, except for P. pectinatus and P. pusillus, the remaining six obviously expose their stigmas out of the perianth. Another species , Najas marina (Najadaceae), has filiform stigmas and ellipsoidal pollen grains which can germinate in water before being transferred onto stigmas in natural conditions. Pollination takes place in this species strictly under water. The characters of pollen and stigmas could be divided into two types, and the pollination system is of two kinds of mechanisms of stigmas capturing pollen in the Najadales. The species with globular pollen grains have wide, large stigmas while those producing filiform or precocious pollen grains, which are likely to be captured by stigmas during the pollen dispersal by water currents, normally have filiform stigmas. It is inferred that various water stresses might have resulted in the diversification of pollinationsystem in the Najadales.     

茨藻目植物柱头特征与传粉系统的演化

茨藻目包含有风媒、水表水媒和水下传粉的多种传粉方式。在前人工作的基础上,补充了4科9 种植物的柱头特征和传粉机制的观察。该目花粉和柱头特征可分为两类,传粉系统表现出两种不同的柱头捕获花粉的机制。花粉为球形的种与其宽大的柱头相配;而那些花粉演化为丝状或花粉在水中具先期萌发能力的种,其花粉易被其丝状的柱头所捕获。此外,还推测了导致这个类群传粉系统分化的可能原因。     

Is sexual organ reciprocity related to legitimate pollen deposition in distylous Pulmonaria (Boraginaceae)?

Heterostyly, i.e. the reciprocal positioning of anthers and stigmas, is a floral polymorphism that is thought to promote disassortative (i.e. between‐morph) pollination and to maintain genetic diversity within populations. Recent research, however, has shown several cases of heterostylous plant species in which the reciprocal positioning of the sexual organs varies, which may affect the likelihood of ‘legitimate’ pollination between compatible morphs, and hence morph fitness and ultimately the stability of this floral polymorphism. In this study, we investigated floral morphology and stigmatic pollen deposition patterns in nine Pulmonaria species (Boraginaceae) across Europe to test the hypothesis that sexual organ reciprocity is related to legitimate pollen deposition. We used a recently developed adaptive accuracy concept to assess the level of reciprocity and to relate inaccuracies in positioning of sexual organs to legitimate pollen deposition measured on stigmas in the field. The nine investigated Pulmonaria species showed substantial deviations from perfect reciprocity, with total inaccuracies varying between 2.9 and 20.3% relative to the squared mean of all anther and stigma heights in the population. In almost all cases, most of the inaccuracy was generated by the high‐level organs. Total pollen deposition was always higher on stigmas of long‐styled individuals, but stigmas of short‐styled individuals received significantly more legitimate pollen than stigmas of long‐styled individuals (71.23% and 38.75% respectively). We also found a weak but significant relationship between measures of inaccuracy and the level of disassortative pollination. Under these conditions of pollen flow, the distylous mating system is predicted to persist in only eleven (27%) of all sampled populations. Overall, these results indicate that deviations from perfect reciprocal herkogamy are common in Pulmonaria and have an impact on legitimate pollen deposition.     

Hydrophilous pollination and breeding system evolution in seagrasses: a phylogenetic approach to the evolutionary ecology of the Cymodoceaceae

COX, P. A. & HUMPHRIES, C. J. 1992. Hydrophilous pollination and breeding system evolution in seagrasses: a phylogenetic approach to the evolutionary ecology of the Cymodoceaceae. A phylogenetic analysis of seagrasses of the Cymodoceaceae shows the Cymodoceaceae to be monophyletic and Posidoniaceae to be their sister group. Information on the pollination ecologies and breeding systems of the various genera of the Cymodoceaceae were plotted onto the consensus tree obtained for the group. From this analysis, it is suggested that the clade composed of the Zosteraceae, Posidoniaceae and Cymodoceaceae evolved from a freshwater hydrophilous ancestor that developed submarine pollination and filiform pollen in association with invasion of the marine environment. Dioecism and surface pollination appear to have evolved in the progenitor of the Cymodoceaceae, and hence the seagrasses of the Cymodoceaceae are dioecious due to common descent rather than to convergent evolutionary processes in extant genera.     

Experimental insights on the function of ancillary pollen and stigma polymorphisms in plants with heteromorphic incompatibility

Most heterostylous plants possess a reciprocal arrangement of stigmas and anthers (reciprocal herkogamy), heteromorphic self‐incompatibility, and ancillary polymorphisms of pollen and stigmas. The topographical complementarity hypothesis proposes that ancillary polymorphisms function in the rejection of incompatible pollen thus promoting disassortative pollination. Here, we test this hypothesis by investigating patterns of pollen transfer and capture in populations of dimorphic Armeria maritima and A. pubigera and distylous Limonium vulgare (Plumbaginaceae), and by studying pollen adherence and germination patterns in A. maritima following controlled hand‐pollinations. Armeria lacks reciprocal herkogamy allowing the evaluation of the extent to which ancillary polymorphisms affect the composition of pollen loads. We compared the amounts of compatible and incompatible pollen on stigmas in natural populations and calculated the proficiencies of pollen transfer for each mating type. We detected disassortative pollination in each species, and mating types did not differ in compatible pollen capture, although cob stigmas captured more incompatible pollen. Controlled hand‐pollinations revealed the failure of incompatible pollen to adhere and germinate on stigmas. Our results provided evidence that, while structural in nature, pollen‐stigma dimorphisms are tightly associated with heteromorphic incompatibility and likely function to promote disassortative pollination, especially in the absence of reciprocal herkogamy.     

Ovulate cone,pollination drop,and pollen capture in Sequoiadendron (Taxodiaceae)

In Sequoiadendron ovules are borne inside the ovulate cone, and pollination drops secreted from these ovules collect pollen. We examined: (1) the relation between ovular position and pollen capture; (2) pollen behavior when in contact with a pollination drop; and (3) ultrastructure of ovules during pollination drop secretion. During wet periods a water sheet forms on the surface of the cone due to bract shape and wettability. Pollination drops persist inside the wetted cone, and pollen capture resumes immediately after drying. Pollen landing on a pollination drop is taken inside the drop and carried into the micropyle when the drop contracts. Several notable ultrastructural features appear in the nucellus, integument, chalaza, and bract lamina during pollination-drop secretion. The abaxial surface of the lamina is covered by a membrane that may contribute to the wettable nature of the surface.     

Heterostyly promotes compatible pollination in buckwheats: Comparisons of intraflower,intraplant, and interplant pollen flow in distylous and homostylous Fagopyrum

Premise of the Study

Heterostyly, the reciprocal positioning of stigmas and anthers in different floral morphs, has long been thought to promote intermorph pollination. However, extensive intramorph pollination occurs commonly in heterostylous species, leading to recurrent questions about the functional and evolutionary significance of heterostyly.

Methods

To identify the sources of stigmatic pollen (autogamous [intraflower], geitonogamous [intraplant], vs. interplant), we emasculated either one flower or entire plants in experimental populations of the two closely related buckwheat species, distylous Fagopyrum esculentum and homostylous F. tataricum. Differences in pollen size allowed unambiguous identification of pollen on stigmas.

Results

Only 2.4% of F. tataricum pollen and 1.5% of F. esculentum pollen arrived successfully on compatible stigmas of other plants. In the former (homostylous) species, 71.3% of the pollen load on stigmas was autogamous, 10.8% was geitonogamous, and 17.9% was interplant. In the latter (distylous) species, 37.45% of the pollen on stigmas was autogamous, 13.8% was geitonogamous, 17.0% was intramorph, and 31.75% was intermorph. The amount of incompatible pollen arriving on stigmas was greatly decreased by both one‐flower and whole‐plant emasculations, and thus, the proportion of compatible pollen deposited increased with one‐flower emasculation and increased even more with whole‐plant emasculation.

Conclusions

Our quantification of pollen‐donor sources in these two species indicated that heterostyly in Fagopyrum esculentum provided a nearly 2‐fold fitness advantage (in terms of compatible pollination) over expected (random) pollen transfers between morphs. Because of reduced herkogamy, the homostylous F. tataricum was highly autogamous.     

Submarine pollination in the marine angiosperm Zostera marina (Zosteraceae). I. The influence of floral morphology on fluid flow

An understanding of the process of submarine pollination should provide insight into the evolutionary and reproductive ecology of the marine angiosperms (seagrasses). The flow around the reproductive organs of the seagrass Zostera marina L. (Potamogetonales) was, therefore, examined in a flow chamber. The phenological emergence of flowers during (1) pollen capture and (2) pollen release, and by fruit during (3) seed release, led to a reduction in flow rate toward the inflorescence. This change in flow due to floral emergence was associated with a 50% increase in the fluid shear stress [tau = (2.2 _ 0.3) x 10-3 Pa for an immature flower vs. tau = (3.1 _ 0.5) x 10-3 Pa for a receptive flower]. The Reynolds number (Re) and fluid shear stress around inflorescences and infructescences were comparable, indicating a dynamic similarity in the processes of pollen capture and fruit dehiscence [Re = 47 _ 5, tau = (1.6 _ 0.3) x 10-3 Pa for inflorescences; Re = 38 _ 5, tau = (1.3 _ 0.1) x 10-3 Pa for infructescences]. These results indicate that the emergence of reproductive organs leads to changes in fluid shear stress, which will affect the release, transport, and capture of particles including pollen. Theoretical considerations of these observations using aerosol-filtration theory suggest that pollen capture in Z. marina occurs through direct interception of pollen by stigmas.     

The control of incompatibility in distylous Pulmonaria affinis Jordan (Boraginaceae)

In P. affinis, pin pollen is shorter on average than thrum pollen. Pins have more coronal hooks on stigmatic papillae than thrums, but gaps between papillae are relatively smaller for thrums. Pin stigmas receive more pollen than thrum stigmas. Thrum stigmas receive more (dissortive) pin pollen, but pin stigmas are assortively pollinated. Pollen only germinates when trapped below papilla coronas. On thrum stigmas, most trapped pollen is pin. Pollen germination is better on thrum stigmas than pin stigmas, and thrum stigmas show a close relationship between numbers of legitimate pollen grains, numbers of germinating grains, and numbers of pollen tubes in the style. There is no inhibition of illegitimate pollen germination. Illegitimate pollen tubes are inhibited in the style. Incompatibility operates by a combination of dissortive pollination, dissortive pollen trapping, and stylar pollen tube inhibition. All heteromorphic features differing between pins and thrums are implicated in the inhibition of within-morph fertilization in thrums.     

The pollination of the gynomonoecious Bdallophytum oxylepis (Cytinaceae,Malvales)

Bdallophytum oxylepis is a rare and endemic species belonging to the Cytinaceae family, a root holoparasitic plant in which most resources are allocated to attracting pollinators. This species is gynomonoecious with intraindividual variation in flower size and sex. Moreover, the flowers exhibit sapromyophilous traits, as do other species of Bdallophytum. Firstly, this study aimed to determine whether all floral morphs can form seeds and be pollen donors (in the case of bisexual flowers). Secondly, as this species has floral traits hypothesized to adapt to particular types of pollen vectors (carrion flies), we also studied the pollination of B. oxylepis to confirm whether the syndromes correspond to what occurs in nature. Through pollination treatments, we determined that all floral morphs are functional. By monitoring the inflorescences, we found that pollination is specialized in the studied population. Stingless bees performed pollination, as they have a high visitation rate, frequency, and constancy, and they are unique visitors that deposit pollen on the stigmas. Thus, they appear to be effective pollinators rather than carrion flies, as predicted by the syndrome. As shown here, animal–plant interaction studies can help establish a basis for conserving rare species such as holoparasites. Moreover, knowledge about the reproductive aspects of B. oxylepis reveals essential clues about its life cycle and role in maintaining native pollinators with economic and cultural value, such as stingless bees.     

Demonstration of pollinator‐mediated competition between two native Impatiens species,Impatiens noli‐tangere and I. textori (Balsaminaceae)

Plant–plant interspecific competition via pollinators occurs when the flowering seasons of two or more plant species overlap and the pollinator fauna is shared. Negative sexual interactions between species (reproductive interference) through improper heterospecific pollen transfer have recently been reported between native and invasive species demonstrating pollination‐driven competition. We focused on two native Impatiens species (I. noli‐tangere and I. textori) found in Japan and examined whether pollinator‐mediated plant competition occurs between them. We demonstrate that I. noli‐tangere and I. textori share the same pollination niche (i.e., flowering season, pollinator fauna, and position of pollen on the pollinator's body). In addition, heterospecific pollen grains were deposited on most stigmas of both I. noli‐tangere and I. textori flowers that were situated within 2 m of flowers of the other species resulting in depressed fruit set. Further, by hand‐pollination experiments, we show that when as few as 10% of the pollen grains are heterospecific, fruit set is decreased to less than half in both species. These results show that intensive pollinator‐mediated competition occurs between I. noli‐tangere and I. textori. This study suggests that intensive pollinator‐mediated competition occurs in the wild even when interacting species are both native and not invasive.     

Entwicklungsgeschichte und Ultrastruktur von Pollenkitt und Exine bei nahe verwandten entomophilen und anemophilen Angiospermensippen derAlismataceae,Liliaceae, Juncaceae,Cyperaceae, Poaceae undAraceae

Some closely related members of the monocotyledonous familiesAlismataceae, Liliaceae, Juncaceae, Cyperaceae, Poaceae andAraceae with variable modes of pollination (insect- and wind-pollination) were studied in relation to the ultrastructure of pollenkitt and exine (amount, consistency and distribution of pollenkitt on the surface of pollen grains). The character syndromes of pollen cementing in entomophilous, anemophilous and intermediate (ambophilous or amphiphilous) monocotyledons are the same in principal as in dicotyledons. Comparing present with former results one can summarize: 1) The pollenkitt is always produced in the same manner by the anther tapetum in all angiosperm sub-classes. 2) The variable stickiness of entomophilous and anemophilous pollen always depends on the particular distribution and consistency of the pollenkitt, but not its amount on the pollen surface. 3) The mostly dry and powdery pollen of anemophilous plants always contains a variable amount of inactive pollenkitt in its exine cavities. 4) A step-by step change of the pollen cementing syndrome can be observed from entomophily towards anemophily. 5) From the omnipresence of pollenkitt in all wind-pollinated angiosperms studied one can conclude that the ancestors of anemophilous angiosperms probably have been zoophilous (i.e. entomophilous) throughout.

     

Shortened anther-stigma distance reduces compatible pollination in two distylous Primula species

Aims Distyly has been regarded as an adaptation to improve compatible pollination between two floral morphs with reciprocal herkogamy. The hypothesis that the different positions of anthers and stigmas within flowers as well as their reciprocal position between morphs, reduce the probability of self pollination raised by Darwin has been rarely tested. In this study, we measured stigmatic pollen loads in response to reduced reciprocal herkogamy in two Primula species.Methods To see whether reciprocal herkogamy can increase compatible and/or reduce incompatible pollen deposition, thus promoting compatible pollination, we shortened the distance between anthers and stigmas within the flowers by changing the position of the corolla tube, to which the anthers were fused, i.e. reduced herkogamy in natural populations of Primula secundiflora and P. poissonii and quantified stigmatic pollen loads in the field over 2 years.Important findings In both species, stigmatic pollen loads were significantly higher in the long-styled (L-morph) than in the short-styled morph (S-morph) in both control and manipulated flowers, but percentage of compatible pollen in S-morph were higher. Flowers manipulated to halve the anther–stigma distance showed a similar pattern for 2 years: total pollen grain counts on stigmas did not differ significantly but compatible pollen grains in L- and S-morphs were significantly decreased in both species. The percentage of compatible pollen loads was decreased by 68.7% in P. secundiflora and 65.3% in P. poissonii in L-morphs, while it decreased by 30.6% and 2.9% in S-morphs, respectively. Our manipulation of the relative position of anthers and stigmas in the two distylous species indicated that a lower degree of herkogamy reduced compatible but incompatible pollen transfer was likely to increase. The higher proportion of compatible pollen in the S-morph than in the L-morph in the two Primula species could be attributed to the accessibility of two-level sexual organs, floral orientations and pollinator behaviors. This is a first attempt to manipulate intraflower herkogamy for understanding adaptation of heterostyly, shedding insights into how the reciprocal herkogamy promotes compatible pollination.     

Notes on the floral morphology in Vivianiaceae (Geraniales)

The functional floral morphology of the three genera of Vivianiaceae (= Ledocarpaceae, Geraniales), Rhynchotheca, Viviania and Balbisia, is compared. Likely pollination mechanisms are inferred from morphology and field observations. The flowers of Viviania are nectariferous and apparently zoophilous with nectar as the (primary) pollinator reward. Balbisia has pollen flowers without nectaries, its showy corolla indicates that it is also zoophilous with pollen as sole pollinator reward; bees were observed as flower visitors. One taxon (B. gracilis) may be anemophilous. Rhynchotheca has flowers without petals, with large, pendulous anthers and lacks nectaries. It shows synchronous mass flowering in its natural populations and is evidently anemophilous. A comparison with other Geraniales shows that nectar flowers with small anthers are likely the ancestral condition in Vivianiaceae. This suggests that the pollen flowers with larger anthers of Balbisia and Rhynchotheca may represent an apomorphic condition. The documentation of pollen flowers and anemophily in Vivianiaceae expands the range of known floral and pollination syndromes in Geraniales.