Landscape genetics of alpine-snowbed plants: comparisons along geographic and snowmelt gradients

The genetic structure of three snowbed-herb species (Peucedanum multivittatum, Veronica stelleri, and Gentiana nipponica) was analyzed using allozymes across nine populations arranged as a matrix of three snowmelt gradients x three geographic locations within 3 km in the Taisetsu Mountains, northern Japan. Phenologically asynchronous populations are packed within a local area in alpine snowbeds, because flowering season of alpine plants depends strongly on the timing of snowmelt. Moderate genetic differentiation was detected among local populations in every species (FST=0.03-0.07). There was a significant correlation between the geographic distance and genetic distance in the P. multivittatum populations, but not in the V. stelleri and G. nipponica populations. On the other hand, a significant correlation between the phenological distance caused by snowmelt timing and genetic distance was detected in the V. stelleri and G. nipponica populations, but not in the P. multivittatum populations. The snowmelt gradient or geographic separation influenced hierarchical genetic structure of these species moderately (FRT <0.04). Restriction of gene flow due to phenological separation and possible differential selection along the snowmelt gradient may produce genetic clines at microgeographic scale in these species.     

Small-scale plant species distribution in snowbeds and its sensitivity to climate change

Alpine snowbeds are characterized by a long-lasting snow cover and low soil temperature during the growing season. Both these key abiotic factors controlling plant life in snowbeds are sensitive to anthropogenic climate change and will alter the environmental conditions in snowbeds to a considerable extent until the end of this century. In order to name winners and losers of climate change among the plant species inhabiting snowbeds, we analyzed the small-scale species distribution along the snowmelt and soil temperature gradients within alpine snowbeds in the Swiss Alps. The results show that the date of snowmelt and soil temperature were relevant abiotic factors for small-scale vegetation patterns within alpine snowbed communities. Species richness in snowbeds was reduced to about 50% along the environmental gradients towards later snowmelt date or lower daily maximum temperature. Furthermore, the occurrence pattern of the species along the snowmelt gradient allowed the establishment of five species categories with different predictions of their distribution in a warmer world. The dominants increased their relative cover with later snowmelt date and will, therefore, lose abundance due to climate change, but resist complete disappearance from the snowbeds. The indifferents and the transients increased in species number and relative cover with higher temperature and will profit from climate warming. The snowbed specialists will be the most suffering species due to the loss of their habitats as a consequence of earlier snowmelt dates in the future and will be replaced by the avoiders of late-snowmelt sites. These forthcoming profiteers will take advantage from an increasing number of suitable habitats due to an earlier start of the growing season and increased temperature. Therefore, the characteristic snowbed vegetation will change to a vegetation unit dominated by alpine grassland species. The study highlights the vulnerability of the established snowbed vegetation to climate change and requires further studies particularly about the role of biotic interactions in the predicted invasion and replacement process.     

Variations in bumble bee preference and pollen limitation among neighboring populations: comparisons between Phyllodoce caerulea and Phyllodoce aleutica (Ericaceae) along snowmelt gradients

Two alpine-snowbed shrubs, Phyllodoce caerulea and P. aleutica (Ericaceae), co-occur in locales in northern Japan with early to late snowmelt, but they have different mating systems. Phyllodoce caerulea is an obligate outcrosser in any population, whereas the selfing ability of P. aleutica is highly variable among neighboring populations along snowmelt gradients: it shows high self-compatibility in early to middle snowmelt populations but low self-compatibility in late snowmelt populations. We investigated the relationships between pollinator availability and mating systems of these species along three snowmelt gradients. Relative abundance of flowers and nectar standing crop of P. caerulea decreased from early to late snowmelt plots. Bumble bees preferred P. caerulea to P. aleutica in early and middle snowmelt plots, while their preference shifted to P. aleutica in late snowmelt plots. Pollen limitation was severe in P. aleutica in early to middle snowmelt plots but it was severe in P. caerulea in late snowmelt plots. Seed-set success under natural conditions of P. aleutica was higher than that of P. caerulea in all plots. Thus, we infer that the selfing ability of P. aleutica under pollinator limitation acts as a reproductive assurance. We conclude that the interaction through pollination between the sympatric species is strong enough to cause a phenotypic change in mating system even within a local area.     

Intrinsic and extrinsic factors acting on the reproductive process in alpine‐snowbed plants: roles of phenology,biological interaction,and breeding system

Pollinator activity and competition for pollinators lead to quantitative and qualitative pollen limitations on seed production and affect the reproductive success of plant species, depending on their breeding system (e.g., self‐compatibility and heterospecific compatibility) and genetic load (e.g., inbreeding depression and hybrid inviability). In alpine ecosystems, snowmelt regimes determine the distribution and phenology of plant communities. Plant species growing widely along a snowmelt gradient often grow with different species among local populations. Their pollinators also vary in their abundance, activity, and behavior during the season. These variations may modify plant–pollinator and plant–plant interactions. We integrated a series of our studies on the alpine dwarf shrub, Phyllodoce aleutica (Ericaceae), to elucidate the full set of intrinsic (species‐specific breeding system) and extrinsic factors (snow condition, pollinator activity, and interspecific competition) acting on their reproductive process. Seasonality of pollinator activity led to quantitative pollen limitation in the early‐blooming populations, whereas in the late‐blooming populations, high pollinator activity ensured pollination service, but interspecific competition for pollinators led to qualitative and quantitative pollen limitation in less competitive species. However, negative effects of illegitimate pollen receipt on seed‐set success might be reduced when cryptic incompatibility systems (i.e., outcross pollen grains took priority over self‐ and heterospecific pollen grains) could effectively prevent ovule and seed discounting. Our studies highlight the importance of species‐specific responses of plant reproduction to changing pollinator availability along environmental gradients to understand the general features of pollination networks in alpine ecosystems.     

Shifts in species richness, herbivore specialization, and plant resistance along elevation gradients

Environmental gradients have been postulated to generate patterns of diversity and diet specialization, in which more stable environments, such as tropical regions, should promote higher diversity and specialization. Using field sampling and phylogenetic analyses of butterfly fauna over an entire alpine region, we show that butterfly specialization (measured as the mean phylogenetic distance between utilized host plants) decreases at higher elevations, alongside a decreasing gradient of plant diversity. Consistent with current hypotheses on the relationship between biodiversity and the strength of species interactions, we experimentally show that a higher level of generalization at high elevations is associated with lower levels of plant resistance: across 16 pairs of plant species, low-elevation plants were more resistant vis-à-vis their congeneric alpine relatives. Thus, the links between diversity, herbivore diet specialization, and plant resistance along an elevation gradient suggest a causal relationship analogous to that hypothesized along latitudinal gradients.     

Drought tolerance and water use by plants along an alpine topographic gradient

Summary In the alpine zones of western North American mountains, topographic-moisture gradients are the results of winter winds blowing snow from the upper windward slopes and ridgetops into snowdrifts on the lee slopes. Wet meadows at the foot of the lee slope are the result of summer snowmelt. Such gradients are repeated many times in a single mountain range. They are useful units for studies of the effects of drought and water use on patterning of alpine vegetation.The research was done through an entire growing season along a topographic gradient at 3,300 m in the Medicine Bow Mountains, Wyoming. Plant water potentials were measured on 29 species (pre-dawn to sunset) at weekly intervals. Simultaneously, leaf conductances were measured on 16 species of these; the remainder had leaves too small for the porometer. Leaf water potentials were generally lowest on the ridgetop and highest in the wet meadow. Highest mean leaf conductances were in the wet meadow plants; the lowest occurred on plants on the upper windward slope. None of the plants on the ridgetop had leaves large enough for the porometer. Plants of most species at all sites but the wet meadow showed sharply reduced leaf conductance or leaf death at plant water potentials below-1.5 MPa. Deep-rooted species such as Trifolium parryi showed maximal conductance at water potentials as low as-1.7 MPa and little reduction in conductance even at lower water potentials. Plant water potentials and leaf conductances showed close relationships with rooting depth, length of dry periods, and position on the gradient.On the occasion of the publication of Volume 50 of OECOLOGIA, the authors respectfully dedicate this paper to Dr. Konrad F. Springer and Dr. M. Evenari for their years of encouragement to the science of physiological ecology. We appreciate their efforts     

Climate change shifts population structure and demographics of an alpine herb,Anemone narcissiflora ssp. sachalinensis (Ranunculaceae), along a snowmelt gradient

Alpine ecosystems, characterized by cold climates and short growing seasons, are thought to be most vulnerable to climate change. Warmer temperatures and earlier snowmelt extend the growing season length and increase drought stress for alpine plants, resulting in changes to their distribution. Anemone narcissiflora ssp. sachalinensis is a perennial herb that grows in the alpine snow-meadows of northern Japan. In the last few decades, its distribution has shifted toward later snowmelt habitat in the Taisetsu Mountains of Hokkaido. We recorded demographic data for this species at early, middle and late snowmelt habitats over four years (2009–2012), and constructed transition matrix models to evaluate how demographic parameters and population growth rate vary between local habitats along a snowmelt gradient. The proportion of reproductive plants was low and seed production was limited in the early snowmelt habitat, with drier soil conditions, in comparison to the middle and late snowmelt habitats, with moist soil conditions. Evidence of the transition from small plants to those in the reproductive stage was limited in the early snowmelt habitat, suggesting that growth was inhibited; the local population in this habitat was estimated to be sustained by seed migration from later snowmelt habitats. These results indicate that advancing snowmelt under climate change may decrease the reproductive activity and population growth rate of snow-meadow plants if seed migration from later snowmelt populations is limited, resulting in the extinction of local populations.     

Morphological and genetic variations of Potentilla matsumurae (Rosaceae) between fellfield and snowbed populations

Identifying ecological factors associated with local differentiation of populations is important for understanding microevolutionary processes. Alpine environments offer a unique opportunity to investigate the effects of habitat-specific selective forces and gene flow limitations among populations at a microscale on local adaptation because the heterogeneous snowmelt patterns in alpine ecosystems provide steep environmental changes. We investigated the variation in morphological traits and enzyme loci between fellfield and snowbed populations of Potentilla matsumurae, a common alpine herb with a wide distribution along snowmelt gradients in northern Japan. We found significant differences in morphological traits between fellfield and snowbed habitats in a northern distribution region. These differences were maintained when plants were grown under uniform conditions in a greenhouse. Allozyme variations among 15 populations from geographically separated regions with different historical backgrounds showed that the populations are more genetically differentiated between the fellfield and snowbed habitats within a region than between populations occupying the same habitat type in different regions. These results suggest that variation in snowmelt regimes could be a driving force creating local adaptation and genetic differentiation of alpine plant populations.     

Patterns and origin of intraspecific functional variability in a tropical alpine species along an altitudinal gradient

Background : Intraspecific functional variability (IFV) along altitudinal gradients is a powerful proxy to infer the responses of plants to abrupt environmental changes. We envisage that IFV shows distinctive patterns in tropical and extratropical alpine regions.

Aims : To characterise the patterns and explore the origin of IFV in a tropical alpine species in a context of upward range extension.

Methods : We examined variations in a series of plant functional traits in Lasiocephalus ovatus, inside and outside a nurse plant along a 600 m altitudinal gradient in the Ecuadorian Andes, and we studied its genetic variability.

Results : More conservative traits were developed at higher elevation, in contrast to extratropical alpine plants, which commonly develop opportunistic traits in response to late snowmelt close to their upper altitudinal limit. The presence of nurse cushions did not alter this trend. Increasing genetic distance along the gradient suggested that IFV might be partly genetically induced.

Conclusions : Our data combined with existing literature in tropical alpine environments lead the way to a stimulating scientific challenge: determining if patterns of plant altitudinal distribution in tropical alpine areas in response to climate change are predictable from patterns described in extratropical alpine areas.     

Timing of snowmelt affects species composition via plant strategy filtering

Plant strategy schemes aim to classify plants according to measurable traits and group species according to their shared evolutionary responses to selective pressures. In this way, it becomes possible to make meaningful comparisons among ecosystems and communities and to predict how plant communities might respond to changes in their environment. Here, we classified common alpine plants which occur in snowpatches (Early and Late snowmelt sites) and in adjacent vegetation (Snow-free sites which melt early in the growing season) using Grime’s CSR plant strategy scheme. Alpine plant communities are largely driven by environmental filters associated with a relatively constant gradient of snowmelt timing. Since snow persistence influences the abiotic environment and plant assemblages alike, we hypothesised that these patterns would be reflected in community CSR scores. Weighted community CSR scores were clustered towards the stress-tolerator (S) corner of the triangular CSR space, and Snow-free communities were significantly more stress-tolerant than Early and Late snowmelt communities. This suggests that snowpatch communities are functionally distinct from surrounding vegetation when considering the major axes of plant variation identified by CSR theory. These results lend further support to the importance of the timing of snowmelt as a key filter, influencing how species and plant strategy types distribute themselves across the alpine landscape.     

Arthropod community composition along snowmelt gradients in snowbeds in the Snowy Mountains of south‐eastern Australia

Environmental gradients drive variation in community composition across a range of spatial scales. In alpine regions, areas of long‐lasting snow (‘snow patches’) create snowmelt gradients that drive considerable change in vegetation structure and composition over small spatial scales. This study examined whether there is parallel variation in arthropod communities using snowmelt gradients in the Australian Alps. Mites (Acarina) were the most common arthropods in snow patches, followed by springtails while, among the insects, the orders Hymenoptera (primarily Formicidae), Diptera, Coleoptera (primarily Carabidae) and Hemiptera (primarily Cicadellidae) dominated. Along the snowmelt gradient, arthropod assemblages changed from having equal proportions of predators and herbivores in early‐melting zones to being predator‐dominated in late‐melting zones, particularly early in the growing season. This followed a transition in vegetation cover and composition and was driven by higher numbers of predacious carabid beetles in later‐melting zones. Overall, however, our results suggest that snowbed arthropod communities in the Australian alpine zone are more sensitive to short‐term effects, such as time since snowmelt, than to differences in vegetation structure and composition or long‐term patterns of snowmelt. Continued advancement of snowmelt timing due to warmer spring temperatures is therefore likely to have more impact on the seasonality of snowbed arthropod communities than on the overall community composition.     

Effect of altitude on the genetic structure of an Alpine grass, Poa hiemata

Background and Aims

The persistence of plants inhabiting restricted alpine areas under climate change will depend upon many factors including levels of genetic variation in adaptive traits, population structure, and breeding system.

Methods

Using microsatellite markers, the genetic structure of populations of a relatively common alpine grass, Poa hiemata, is examined across three altitudinal gradients within the restricted Australian alpine zone where this species has previously been shown to exhibit local adaptation across a narrow altitudinal gradient.

Key Results

Genetic variation across six microsatellite markers revealed genetic structuring along altitudinal transects, and a reduction in genetic variation at high and low altitude extremes relative to sites central within transects. There was less genetic variation among transect sites compared with altitudinal gradients within transects, even though distances among transects were relatively larger. Central sites within transects were less differentiated than those at extremes.

Conclusions

These patterns suggest higher rates of gene flow among sites at similar altitudes than along transects, a process that could assist altitudinal adaptation. Patterns of spatial autocorrelation and isolation by distance changed with altitude and may reflect altered patterns of dispersal via pollen and/or seed. There was evidence for selfing and clonality in neighbouring plants. Levels of gene flow along transects were insufficient to prevent adaptive changes in morphological traits, given previously measured levels of selection.Key words: Poa hiemata, genetic structure, altitudinal gradient, microsatellite, gene flow, climate change     

Divergence among arctic and alpine populations of the annual, Koenigia islandica: morphology, life-history, and phenology

Arctic and alpine habitats occur along complex environmental gradients, and over an extensive geographical range. Despite some selective forces common to these habitats, evolutionary divergence among populations of arctic and alpine plants along this gradient is expected. Of particular significance, both in the context of life-history theory and for implications of climate change, are the few annual species that have adapted to the constraints of an unpredictable, short growing season. In this study, morphological, life-history and phenological characters were found to differ significantly among six widely distributed populations of the arctic-alpine annual Koenigia islandica. On the basis of morphology and life-history traits, populations from high latitudes, with the exception of Svalbard, performed better in simulated arctic conditions, whereas the low latitude alpine plants from Colorado showed enhanced performance under simulated alpine conditions. On the basis of phenology, the six populations can be clearly grouped into arctic, high latitude alpine and alpine populations: arctic plants were found to develop and flower earliest; alpine plants latest. Because these results were obtained using seeds harvested from plants first grown through a complete generation in growth chambers, they indicate strong genetic differentiation. We discuss possible adaptive explanations for observed differences among the six geographically divergent populations.     

Different temperature perception in high‐elevation plants: new insight into phenological development and implications for climate change in the alpine tundra

In alpine habitats, predicted warmer and longer growing seasons will influence plant phenology, with important implications for species adaptation and vegetation dynamics. However, little is known on the temperature sensitivity of different phenophases and on the characteristics allowing phenological variation among and within species. By integrating interannual micro‐climatic variability with experimental warming, we explored how the phenology of three alpine species is influenced by temperature and what mechanisms underlie intra‐ and inter‐specific phenological differences. The present study demonstrated that alpine plants have different temperature responses during their reproductive cycle, do not have constant thermal thresholds and heat‐use efficiencies to achieve the seed dispersal stage and can change their temperature sensitivity to flower along snowmelt gradients. In addition, the length of the reproductive cycle, which proved to be species‐specific under experimental warming, does not seem to be the only life‐history trait under selective pressure due to the short‐length of the snow‐free period. In a warming climate scenario, the phenology of sexual reproduction will be considerably altered, and alpine plants may be subjected to changes in population dynamics driven by altered perception of environmental cues appropriate for coordinating the timing of key life‐history events.     

A hybrid zone dominated by fertile F1s: maintenance of species barriers in Rhododendron

Isolating barriers between interbreeding sympatric or parapatric interfertile species are maintained by processes that occur within their hybrid zones. Although the effects of intrinsic selection on hybrid fitness are well known, less is understood about extrinsic fitness variation. At Tiryal Dag, northeast Turkey, Rhododendron x sochadzeae (R. ponticum x caucasicum) forms large populations in which neither segregation nor backcrossing occur, in habitats intermediate between those of its parents. Using single-copy species-specific random amplified polymorphic DNA and inter simple sequence repeat markers, it was determined that most or all R. x sochadzeae plants are F1s, and that there are many separate genets present. Hand pollination and germination experiments showed that R. x sochadzeae plants can produce viable seed of F2s or backcrosses in either direction. Furthermore, adult backcrosses have been observed in habitats atypical for R. x sochadzeae. From this, all non-F1 hybrid derivatives appear to be eliminated in the hybrid zone at Tiryal Dag as a result of postgermination selection. This absence of post-F1 hybrid derivatives apparently prevents introgression. This type of hybrid population is here termed an F1-dominated hybrid zone (F1DZ), and also occurs in Encelia. The observed dominance of F1s within a narrow habitat range is best explained by habitat-mediated superiority of F1s over all other genotype classes. Therefore, habitat-mediated selection against the second hybrid generation might be preventing interspecific gene flow in R. x sochadzeae. F1DZ formation is postulated to require the formation of F1s in quantity, habitat-mediated superiority in F1s, and highly specific habitat conditions.     

Habitat-specific responses in the flowering phenology and seed set of alpine plants to climate variation: implications for global-change impacts

The timing of the snowmelt is a crucial factor in determining the phenological schedule of alpine plants. A long-term monitoring of snowmelt regimes in a Japanese alpine area revealed that the onset of the snowmelt season has been accelerated during the last 17 years in early snowmelt sites but that such a trend has not been detected in late snowmelt sites. This indicates that the global warming effect on the snowmelt pattern may be site-specific. The flowering phenology of fellfield plants in an exposed wind-blown habitat was consistent between an unusually warm year (1998) and a normal year (2001). In contrast, the flowering occurrence of snowbed plants varied greatly between the years depending on the snowmelt time. There was a large number of flowering species in the fellfield community from mid- to late to late June and from mid- to late July. The flowering peak of an early-melt snowbed plant community was in the middle of the flowering season and that of a late-melt snowbed community was in the early flowering season. These habitat-specific phenological patterns were consistent between 1998 and 2001. The effects of the variation in flowering timing on seed-set success were evaluated for an entomophilous snowbed herb, Peucedanum multivittatum, along the snowmelt gradient during a 5-year period. When flowering occurred prior to early August, mean temperature during the flowering season positively influenced the seed set. When flowering occurred later than early August, however, the plants enjoyed high seed-set success irrespective of temperature conditions if frost damage was absent. These observations are probably explained based on the availability of pollinators, which depends not only on ambient temperature but also on seasonal progress. These results suggest that the effects of climate change on biological interaction may vary depending on the specific habitat in the alpine ecosystem in which diverse snowmelt patterns create complicated seasonality for plants within a very localized area.     

Ants exhibit asymmetric hybridization in a mosaic hybrid zone

Research on hybridization between species provides unparalleled insights into the pre‐ and postzygotic isolating mechanisms that drive speciation. In social organisms, colony‐level incompatibilities may provide additional reproductive barriers not present in solitary species, and hybrid zones offer an opportunity to identify these barriers. Here, we use genotyping‐by‐sequencing to sequence hundreds of markers in a hybrid zone between two socially polymorphic ant species, Formica selysi and Formica cinerea. We characterize the zone, determine the frequency of hybrid workers, infer whether hybrid queens or males are produced and investigate whether hybridization is influenced by colony social organization. We also compare cuticular hydrocarbon profiles and aggression levels between the two species. The hybrid zone exhibits a mosaic structure. The asymmetric distribution of hybrids skewed towards F. cinerea suggests a pattern of unidirectional nuclear gene flow from F. selysi into F. cinerea. The occurrence of backcrossed individuals indicates that hybrid queens and/or males are fertile, and the presence of the F. cinerea mitochondrial haplotype in 97% of hybrids shows that successful F1 hybrids will generally have F. cinerea mothers and F. selysi fathers. We found no evidence that social organization contributes to speciation, because hybrids occur in both single‐queen and multiple‐queen colonies. Strongly differentiated cuticular hydrocarbon profiles and heightened interspecific aggression further reveal that species recognition cues are both present and perceived. The discovery of fertile hybrids and asymmetrical gene flow is unusual in ants, and this hybrid zone will therefore provide an ideal system with which to investigate speciation in social insects.     

Nitrogen economy of alpine plants on the north Tibetan Plateau: Nitrogen conservation by resorption rather than open sources through biological symbiotic fixation

Nitrogen (N) is one of the most important factors limiting plant productivity, and N fixation by legume species is an important source of N input into ecosystems. Meanwhile, N resorption from senescent plant tissues conserves nutrients taken up in the current season, which may alleviate ecosystem N limitation. N fixation was assessed by the ¹⁵N dilution technique in four types of alpine grasslands along the precipitation and soil nutrient gradients. The N resorption efficiency (NRE) was also measured in these alpine grasslands. The aboveground biomass in the alpine meadow was 4–6 times higher than in the alpine meadow steppe, alpine steppe, and alpine desert steppe. However, the proportion of legume species to community biomass in the alpine steppe and the alpine desert steppe was significantly higher than the proportion in the alpine meadow. N fixation by the legume plants in the alpine meadow was 0.236 g N/m², which was significantly higher than N fixation in other alpine grasslands (0.041 to 0.089 g N/m²). The NRE in the alpine meadows was lower than in the other three alpine grasslands. Both the aboveground biomass and N fixation of the legume plants showed decreasing trends with the decline of precipitation and soil N gradients from east to west, while the NRE of alpine plants showed increasing trends along the gradients, which indicates that alpine plants enhance the NRE to adapt to the increasing droughts and nutrient‐poor environments. The opposite trends of N fixation and NRE along the precipitation and soil nutrient gradients indicate that alpine plants adapt to precipitation and soil nutrient limitation by promoting NRE (conservative nutrient use by alpine plants) rather than biological N fixation (open sources by legume plants) on the north Tibetan Plateau.     

Increased spring freezing vulnerability for alpine shrubs under early snowmelt

Alpine dwarf shrub communities are phenologically linked with snowmelt timing, so early spring exposure may increase risk of freezing damage during early development, and consequently reduce seasonal growth. We examined whether environmental factors (duration of snow cover, elevation) influenced size and the vulnerability of shrubs to spring freezing along elevational gradients and snow microhabitats by modelling the past frequency of spring freezing events. We sampled biomass and measured the size of Salix herbacea, Vaccinium myrtillus, Vaccinium uliginosum and Loiseleuria procumbens in late spring. Leaves were exposed to freezing temperatures to determine the temperature at which 50 % of specimens are killed for each species and sampling site. By linking site snowmelt and temperatures to long-term climate measurements, we extrapolated the frequency of spring freezing events at each elevation, snow microhabitat and per species over 37 years. Snowmelt timing was significantly driven by microhabitat effects, but was independent of elevation. Shrub growth was neither enhanced nor reduced by earlier snowmelt, but decreased with elevation. Freezing resistance was strongly species dependent, and did not differ along the elevation or snowmelt gradient. Microclimate extrapolation suggested that potentially lethal freezing events (in May and June) occurred for three of the four species examined. Freezing events never occurred on late snow beds, and increased in frequency with earlier snowmelt and higher elevation. Extrapolated freezing events showed a slight, non-significant increase over the 37-year record. We suggest that earlier snowmelt does not enhance growth in four dominant alpine shrubs, but increases the risk of lethal spring freezing exposure for less freezing-resistant species.     

Seasonal changes in pollen limitation and femaleness along the snowmelt gradient in a distylous alpine herb,Primula modesta

Flowering phenology of alpine plants is strongly determined by the timing of snowmelt, and the conditions of pollination of widely distributed plants vary greatly during their flowering season. We examined the reproductive success of the distylous alpine herb, Primula modesta, along the snowmelt gradient under natural conditions, and compared it with the result of artificial pollination experiments. In addition, the compositions and visit frequencies of pollinators to the flower of P. modesta were examined during the flowering period. The pin and thrum plants of P. modesta growing at the same site have an equal ability to produce seeds if a sufficient amount of legitimate pollen grains are deposited on the stigma surface. However, under natural conditions, their seed‐set success was often (even if not always) restricted by pollen limitation, and the functional gender of the pin and thrum plants biased to the female and male, respectively, associated with their growing sites. These variations were not ascribed to resource limitation nor biased morph ratio but to the seasonal changes in pollination situations, a replacement of pollinator types from long‐ to short‐tongued pollinators resulted in unidirectional pollen transfer from long stamens (thrum plants) to long styles (pin plants). The functional gender specialization may enhance the evolution of dioecy from heterostyly, but the severe pollen limitation may cause the breakdown of heterostyly into homostyly. To consider the evolutionary pathway of heterostylous plants, an accumulation of the empirical data is required demonstrating how phenological synchrony between plants and pollinators is decided and to what degree this relationship is stable over years, along with estimates of selection and gene flow in individual plants.