Interspecific pollen transfer as a mechanism of competition: Consequences of foreign pollen contamination for seed set in the alpine wildflower,Polemonium viscosum

Summary Earlier studies showed that under natural conditions foreign pollen receipt is correlated with loss of seed set in populations of P. viscosum. Here, we report on experimental pollinations using foreign pollen from two co-flowering species that share pollinators with P. viscosum. Experiments were designed to ascertain whether improper pollen transfer causes reduced seed set under controlled conditions and, if so, to determine the stage at which interference occurs. In flowers pre-treated by pollination with either Mertensia or Castilleja pollen, adherence of subsequently deposited conspecific pollen grains was unaffected. However, conspecific grains had significantly lower germination and ovule fertilization success in flowers receiving foreign pollen than in controls. These results suggest that pollinator infidelity in high alpine plant communities can reduce female reproductive success of P. viscosum by inhibiting the performance of conspecific pollen grains. Negative effects of Mertensia and Castilleja pollen were comparable despite large interspecific differences in pollen grain morphology. Accordingly, susceptibility to foreign pollen interference appears to be an intrinsic property of P. viscosum that is not dependent on the unique structural properties of pollen produced by competitive species.     

How shrub encroachment under climate change could threaten pollination services for alpine wildflowers: A case study using the alpine skypilot,Polemonium viscosum

Under climate change, shrubs encroaching into high altitude plant communities disrupt ecosystem processes. Yet effects of encroachment on pollination mutualisms are poorly understood. Here, we probe potential fitness impacts of interference from encroaching Salix (willows) on pollination quality of the alpine skypilot, Polemonium viscosum. Overlap in flowering time of Salix and Polemonium is a precondition for interference and was surveyed in four extant and 25 historic contact zones. Pollinator sharing was ascertained from observations of willow pollen on bumble bees visiting Polemonium flowers and on Polemonium pistils. We probed fitness effects of pollinator sharing by measuring the correlation between Salix pollen contamination and seed set in naturally pollinated Polemonium. To ascertain whether Salix interference occurred during or after pollination, we compared seed set under natural pollination, conspecific pollen addition, and Salix pollen addition. In current and past contact zones Polemonium and Salix overlapped in flowering time. After accounting for variance in flowering date due to latitude, Salix and Polemonium showed similar advances in flowering under warmer summers. This trend supports the idea that sensitivity to temperature promotes reproductive synchrony in both species. Salix pollen is carried by bumble bees when visiting Polemonium flowers and accounts for up to 25% of the grains on Polemonium pistils. Salix contamination correlates with reduced seed set in nature and when applied experimentally. Postpollination processes likely mediate these deleterious effects as seed set in nature was not limited by pollen delivery. Synthesis: As willows move higher with climate change, we predict that they will drive postpollination interference, reducing the fitness benefits of pollinator visitation for Polemonium and selecting for traits that reduce pollinator sharing.     

Dosage-dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution in the alpine skypilot Polemonium viscosum

All volatile organic compounds (VOCs) vary quantitatively, yet how such variation affects their ecological roles is unknown. Because floral VOCs are cues for both pollinators and floral antagonists, variation in emission may have major consequences for costs and benefits in plant-pollinator interactions. In Polemonium viscosum, the emission rate for the floral VOC 2-phenylethanol (2PE) spans more than two orders of magnitude. We investigated the ecological and evolutionary impacts of this immense phenotypic variation. The emission rate of 2PE varies independently of nectar rewards and thus is uninformative of profitability. Emission is elevated in flowers that are morphologically vulnerable to ant larcenists, suggesting that chemical deterrence may compensate for weak physical barriers. In nature, plants emitting more 2PE than their neighbors escape ant damage. Flower-damaging ants die when exposed to 2PE in the laboratory, and they avoid high 2PE emitters in the field. High 2PE also reduces bumblebee visitation and pollination, suggesting an ecological cost of defense in pollinator service. However, at more moderate emission rates, 2PE enhances the amount of nectar left in flowers, at no pollination cost. In conclusion, repellency of 2PE is highly sensitive to dosage, giving it a key role in shaping ecological interactions between skypilot plants and their floral visitors.     

Bumble bee behavior and selection on flower size in the sky pilot,Polemonium viscosum

Summary In alpine Polemonium viscosum, plants having sweet-scented flowers are primarily pollinated by queens of the bumble bee species, Bombus kirbyellus. In this paper we ask whether two aspects of the pollination effectiveness of bumble bees, visitation rate and pollination efficiency, vary significantly with flower size in sweet-flowered P. viscosum.(i) Bumble bees visited plants with large flowers on 80–90% of encounters, but visited those with smaller flowers on only 49% of encounters. (ii) However, the gain in pollination that large-flowered plants obtained via increased visitation was countered in part because bumble bees deposited fewer outcross pollen grains per visit on stigmas of large flowers than on those of small ones. When both visitation rate and pollination efficiency are taken into account, the predicted value of a single bumble bee encounter declines from 1.06 seeds for flowers larger than 18 mm in diameter to 0.55 seeds for flowers smaller than 12 mm in diameter. Our results suggest that bumble bee pollinators of P. viscosum prefer flower morphologies that are poorly suited for precise pollination. Such behavioral complexities are likely to place constraints on the evolution of optimal floral design.     

Feeding friend and foe: ample pollen mitigates the effects of pollen theft for a gynodioecious plant,Polemonium foliosissimum (Polemoniaceae)

Background and AimsMost angiosperms rely on pollinators to transport pollen and effect fertilization. While some floral visitors are effective pollinators, others act as thieves, consuming pollen but effecting little pollination in return. The importance of pollen theft in male and female reproductive success has received little attention. Here, we examined if pollen consumption by flies altered pollen receipt and exacerbated pollen limitation for a bumblebee-pollinated plant, Polemonium foliosissimum (Polemoniaceae).MethodsTo examine the effect of pollen-thieving flies, we took a three-pronged approach. First, we used single-visit observations to quantify pollen removal and pollen deposition by flies and bumblebees. Second, we manipulated pollen in the neighbourhood around focal plants in two years to test whether pollen reduction reduced pollen receipt. Third, we combined pollen reduction with hand-pollination to test whether pollen thieving exacerbated pollen limitation. Polemonium foliosissimum is gynodioecious in most populations in the Elk Mountains of central Colorado, USA. Thus, we also tested whether pollen theft affected hermaphrodites and females differently.ResultsFlies removed significantly more pollen and deposited less pollen per visit than did bumblebees. Reduction of pollen in the neighbourhood around focal plants reduced pollen receipt in both years but only nearly significantly so in 2015. In 2016, plants were significantly pollen-limited; hand-pollination significantly increased seeds per fruit for both hermaphrodites and females. However, the reduction of pollen around focal plants did not exacerbate pollen limitation for either hermaphrodites or females.ConclusionsOur results suggest that plants tolerate significant consumption of pollen by thieves and pollinators by producing ample pollen to feed both and fertilize available ovules. Our results demonstrate that pollen limitation in P. foliosissimum is driven by lack of effective pollinators rather than lack of pollen. Teasing out these effects elucidates the relative importance of drivers of reproductive success and thus the expected response to selection by different floral visitors.     

High and Dry: Drought Stress, Sex-Allocation Trade-offs, and Selection on Flower Size in the Alpine Wildflower Polemonium viscosum (Polemoniaceae)

Sex-allocation trade-offs may maintain variation in secondary sexual characteristics if such traits vary in their benefits or costs in association with different genders. In Polemonium viscosum, large flowers benefit both male and female aspects of reproduction. In this study, I explore how resource investment in flower size influences the cost of allocation to male and female function. Large flowers exact a water cost in P. viscosum under dry conditions. In an extreme drought in 1997, experimentally watered plants had higher survival and fecundity than controls. By comparing allocation patterns between plants dying from drought and survivors, I tested whether the demographic cost of large flowers increases with allocation to fecundity. Controls that died showed a positive relationship between flower size and fruit production, while survivors showed a negative relationship or trade-off. Watered plants showed no such trade-off. To test whether drought affects the relationship of corolla size to male function, I used leaf-water potential in 1998 to classify plants as stressed or unstressed. Corolla size showed positive correlations to pollen per flower regardless of drought stress. I conclude that under drought the demographic cost of producing large flowers is gender dependent, such that viability selection favors either small-flowered plants with female-biased reproduction or larger-flowered plants with male-biased reproduction.     

Integral assessment of the regrow capacity of alpine plants

A method for the comparative assessment of the regrow capacity (the ability of plants to the after-mowing recovery of above-ground biomass) of herbs in natural plant communities has been proposed. The method is based on the combined use of biomass parameters and the data on the number of shoots for the cases of the single and double removal of the biomass. The regrow capacity of 42 alpine species from four different plant communities has been assessed. The average weighted regrow capacity score decreases in the following series: Geranium-Hedysarum meadows > alpine lichen heaths ≥ alpine snow-bed communities ≥ Festuca varia meadows.     

Cytoplasmic male sterility and restoration of pollen fertility in higher plants

The review deals with cytoplasmic male sterility (CMS) in higher plants: impairment of the pollen formation resulting from interaction of the nuclear and mitochondrial genomes. The information on the known nuclear restorer-of-fertility genes and their effects on the expression of CMS-associated mitochondrial loci are considered. Heteroplasmy of mtDNA in plants and its potential association with CMS inheritance, as well as possible mechanisms of the observed direct and reverse association between altered expression of the CMS-inducing mitochondrial genome, metabolic defects, and pollen sterility are discussed.     

Cytoplasmic male sterility and restoration of pollen fertility in higher plants

The review deals with cytoplasmic male sterility (CMS) in higher plants: impairment of the pollen formation resulting from interaction of the nuclear and mitochondrial genomes. The information on the known nuclear restorer-of-fertility genes and their effects on the expression of CMS-associated mitochondrial loci are considered. Heteroplasmy of mtDNA in plants and its potential association with CMS inheritance, as well as possible mechanisms of the observed direct and reverse association between altered expression of the CMS-inducing mitochondrial genome, metabolic defects, and pollen sterility are discussed.     

Desiccation tolerance,longevity and seed-siring ability of entomophilous pollen from UK native orchid species

Background and Aims

Pollinator-limited seed-set in some terrestrial orchids is compensated for by the presence of long-lived flowers. This study tests the hypothesis that pollen from these insect-pollinated orchids should be desiccation tolerant and relatively long lived using four closely related UK terrestrial species; Anacamptis morio, Dactylorhiza fuchsii, D. maculata and Orchis mascula.

Methods

Pollen from the four species was harvested from inflorescences and germinated in vitro, both immediately and also after drying to simulate interflower transit. Their tolerance to desiccation and short-term survival was additionally assessed after 3 d equilibration at a range of relative humidities (RHs), and related to constructed sorption isotherms (RH vs. moisture content, MC). Ageing of D. fuchsii pollen was further tested over 2 months against temperature and RH, and the resultant survival curves were subjected to probit analysis, and the distribution of pollen death in time (σ) was determined. The viability and siring ability, following artificial pollinations, were determined in D. fuchsii pollen following storage for 6 years at –20 °C.

Key Results

The pollen from all four species exhibited systematic increases in germinability and desiccation tolerance as anthesis approached, and pollen from open flowers generally retained high germinability. Short-term storage revealed sensitivity to low RH, whilst optimum survival occurred at comparable RHs in all species. Similarly, estimated pollen life spans (σ) at differing temperatures were longest under the dry conditions. Despite a reduction in germination and seeds per capsule, long-term storage of D. fuchsii pollen did not impact on subsequent seed germination in vitro.

Conclusions

Substantial pollen desiccation tolerance and life span of the four entomophilous orchids reflects a resilient survival strategy in response to unpredictable pollinator visitation, and presents an alternative approach to germplasm conservation.     

Empirical models of pollen limitation, resource acquisition, and mast seeding by a bee-pollinated wildflower

Synchronous mast seeding is increasingly recognized as common in plant populations. Recent theoretical models show that synchronous mast seeding could be a consequence of resource allocation and storage within individual plants, coupled by pollen limitation in low-flowering years. We used long-term population and weather data to parameterize models of flowering based on stored resources and pollen limitation in Astragalus scaphoides, a bee-pollinated plant that flowers in alternate years. We used these models to test whether internal resource dynamics could explain mast seeding in A. scaphoides and, if so, whether synchrony was caused by pollen limitation and/or fluctuations in precipitation. We compared predictions of models that included all combinations of three factors: constant versus precipitation-dependent resource gain, uniform versus heterogeneous resource gain (among individual plants), and resource-dependent versus resource- and pollen-limited fruit set. Pollen limitation and heterogeneous resource gain were necessary and sufficient to explain alternate-year flowering, but precipitation increased the quantitative match between model predictions and flowering dynamics. Together, our results support the importance of density-dependent pollen limitation as an ultimate and proximate cause of mast seeding in A. scaphoides. Precipitation does not act as a direct cue for synchrony in this species but might affect long-term resource gain and fruiting dynamics.     

Patterns of pollen removal and deposition in Polemonium brandegeei (Polemoniaceae): the role of floral visitors,floral design and sexual interference

The arrangement, colour, shape and size of floral parts (collectively floral design) have evolved primarily to promote mating success via animal‐mediated pollen transfer. Although numerous studies have examined variation in pollinator assemblages, relatively few have examined patterns of pollen removal and deposition in the presence of fluctuating pollinators and ineffective floral visitors; therefore, net pollen removal and deposition by entire visitor assemblages are unclear. We studied the timing (diurnal or nocturnal) and effects of floral traits on pollen removal and deposition under a dynamic visitor assemblage of Polemonium brandegeei. We quantified pollen grains remaining in anthers (pollen removal) and deposited on stigmas (pollen deposition) of plants visited during either the day (07:30–20:00 h) or night (20:30–07:30 h) in natural populations over two flowering seasons. Pollen removal and deposition occurred both diurnally and nocturnally during our study. Increased diurnal removal and deposition coincided with peak floral visitations in 2006. This increase in pollen removal and deposition may reflect increased visits by pollen consumers, effective hawkmoth pollinators and increased self‐pollen deposition due to hot, dry weather. Nonlinear effects of style length significantly affected pollen removal, with less pollen remaining in flowers with intermediate style lengths. Pollen deposition was more complex, with herkogamy and anther height affecting deposition. Further, close proximity of stigmas and anthers increased the potential for sexual interference between pollen removal and deposition. Overall, flower visitations and pollen removal and deposition varied between years and populations, but sex organ placement consistently influenced the removal and deposition of pollen.     

Genetic dissection of embryo sac fertility, pollen fertility, and their contributions to spikelet fertility of intersubspecific hybrids in rice

The partial sterility of hybrids has been a major barrier for utilization of the strong heterosis expressed in hybrids between Oryza sativa ssp. indica and O. sativa ssp. japonica. Wide-compatibility varieties, comprising a special class of germplasm, are able to produce fertile hybrids when crossed to both indica and japonica varieties. However, all the work on wide compatibility and majority of studies on indica/japonica hybrid sterility reported so far were based only on spikelet fertility; thus, it is not known to what extent male and female gamete abortions influence hybrid sterility. In this study, we investigated pollen fertility, embryo sac fertility, and spikelet fertility in an F₁ population of 202 true hybrid plants derived from a three-way cross (02428/Nanjing 11//Balilla). A partial regression analysis showed that the pollen and embryo sac fertility contributed almost equally to spikelet fertility. QTL analysis based on a linkage map of 191 polymorphic marker loci identified two QTLs for pollen fertility, one QTL for embryo sac fertility, and three QTLs for spikelet fertility. The S5 locus, previously identified as a locus for wide compatibility by spikelet fertility analysis, is a major locus for embryo sac fertility, and a QTL on chromosome 5 had a major effect on pollen fertility. These two loci coincided with the two major QTLs for spikelet fertility. The study also detected a QTL on chromosome 8, showing a large effect on spikelet fertility but no effect on either pollen or embryo sac fertility. Very little interaction among the QTLs was detected. The implications of the findings in rice breeding programs are discussed.     

Contrasting the effects of environment,dispersal and biotic interactions to explain the distribution of invasive plants in alpine communities

Despite considerable efforts devoted to investigate the community assembly processes driving plant invasions, few general conclusions have been drawn so far. Three main processes, generally acting as successive filters, are thought to be of prime importance. The invader has to disperse (1st filter) into a suitable environment (2nd filter) and succeed in establishing in recipient communities through competitive interactions (3rd filter) using two strategies: competition avoidance by the use of different resources (resource opportunity), or competitive exclusion of native species. Surprisingly, despite the general consensus on the importance of investigating these three processes and their interplay, they are usually studied independently. Here we aim to analyse these three filters together, by including them all: abiotic environment, dispersal and biotic interactions, into models of invasive species distributions. We first propose a suite of indices (based on species functional dissimilarities) supposed to reflect the two competitive strategies (resource opportunity and competition exclusion). Then, we use a set of generalised linear models to explain the distribution of seven herbaceous invaders in natural communities (using a large vegetation database for the French Alps containing 5,000 community-plots). Finally, we measure the relative importance of competitive interaction indices, identify the type of coexistence mechanism involved and how this varies along environmental gradients. Adding competition indices significantly improved model’s performance, but neither resource opportunity nor competitive exclusion were common strategies among the seven species. Overall, we show that combining environmental, dispersal and biotic information to model invasions has excellent potential for improving our understanding of invader success.     

Some views on plants in polar and alpine regions

Many plants growing in polar and alpine regions clearly solve serious problems of life under extreme climatic conditions, as low temperatures, strong winds, unstable soils and in the North partly 24-h of light.     

Ants on plants: a meta-analysis of the role of ants as plant biotic defenses

We reviewed the evidence on the role of ants as plant biotic defenses, by conducting meta-analyses for the effects of experimental removal of ants on plant herbivory and fitness with data pooled from 81 studies. Effects reviewed were plant herbivory, herbivore abundance, hemipteran abundance, predator abundance, plant biomass and reproduction in studies where ants were experimentally removed (n = 273 independent comparisons). Ant removal exhibited strong effects on herbivory rates, as plants without ants suffered almost twice as much damage and exhibited 50% more herbivores than plants with ants. Ants also influenced several parameters of plant fitness, as plants without ants suffered a reduction in biomass (−23.7%), leaf production (−51.8%), and reproduction (−24.3%). Effects were much stronger in tropical regions compared to temperate ones. Tropical plants suffered almost threefold higher herbivore damage than plants from temperate regions and exhibited three times more herbivores. Ant removal in tropical plants resulted in a decrease in plant fitness of about 59%, whereas in temperate plants this reduction was not statistically significant. Ant removal effects were also more important in obligate ant–plants (=myrmecophytes) compared to plants exhibiting facultative relationships with hemiptera or those plants with extrafloral nectaries and food bodies. When only tropical plants were considered and the strength of the association between ants and plants taken into account, plants with obligate association with ants exhibited almost four times higher herbivory compared to plants with facultative associations with ants, but similar reductions in plant reproduction. The removal of a single ant species increased plant herbivory by almost three times compared to the removal of several ant species. Altogether, these results suggest that ants do act as plant biotic defenses, but the effects of their presence are more pronounced in tropical systems, especially in myrmecophytic plants. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. N. P. de U. Barbosa, L. Diniz, Y. Oki and F. Pezzini contributed equally to this work and are listed in alphabetical order.     

Ants on oaks: effects of forest structure on species composition

The ant fauna of oak forest canopies in Northern Bavaria was studied by canopy fogging on 45 trees in August 2000 and May 2001. The study focused on a comparison of several different forestry management practices resulting in several types of canopy cover. Forests surveyed were: (1) high forest (high canopy cover), (2) coppice with standards (low canopy cover), (3) forest pasture with mostly solitary trees (very low canopy cover) and (4) transitional forest from former coppice with standards to high forest (approaching high canopy cover). This comprised a full gradient of canopy coverage. On the 45 oak trees sampled, a total of 17 ant species were found. Species composition was dependent on the different forestry management practices. The total number of species and the number of species listed in the Red Data Books of both Germany and Bavaria were much higher in the forest pasture and the coppice with standards, as compared to the high forest. The transitional forest was at an intermediate level. The highest number of ant species was found in the forest pasture. This can be explained by the occurrence of species of open habitats and thermophilous species. In the coppice with standards, forest dwelling and arboricolous species dominated, whereas the high forest showed much lower frequencies of arboricolous species like Temnothorax corticalis, Dolichoderus quadripunctatus and Temnothorax affinis. A multivariate analysis revealed that canopy cover (measured as “shade”, in percentage intervals of canopy cover) was the best parameter for explaining species distribution and dataset variation, and to a lesser extent the amount of dead wood, canopy and trunk diameter. Thus ant fauna composition was mostly driven by structural differences associated to the different forestry management practices. Many ant species clearly preferred the more open and light forest stands of the coppice with standards as compared to the dense and shady high forest.