Alpine species seed longevity in the soil in relation to seed size and shape – A 5-year burial experiment in the Central Alps

Long-term persistent seeds are generally expected to be small and spherically shaped. In contrast, transient seeds are often large, flattened and elongated. We hypothesized that alpine species follow these trends, and that most species of unstable alpine habitats have the potential to form long-term persistent seed banks. The latter would enable them to delay germination until favourable conditions are present in their environment thereby increasing the likelihood for establishment of seedlings. We selected nine alpine species of more or less unstable habitats (i.e. Achillea moschata, Artemisia genipi, Anthyllis vulneraria ssp. alpicola, Geum reptans, Linaria alpina, Oxyria digyna, Saxifraga aizoides, Saxifraga oppositifolia, and Trifolium pallescens) for this study. Seed longevity was estimated by a 5-year burial experiment in the field with seed excavations after 1 winter, 2 years and 5 years. Germination experiments in the growth chamber and viability tests were performed after each excavation. We detected longevity patterns ranging from transient to long-term persistent. Two species were classified as transient. All other species have the potential to form persistent seed banks, with almost half of the investigated species showing a trend for long-term persistence. Despite contradictory reports, long-term persistent seed banks are an important life history trait of species of unstable alpine habitats. We found that seed shape and hard-seededness are good predictors of seed persistence of alpine species. Seed size seems to be less important. The data from this study support the general hypotheses describing the relationship among seed size, seed shape and seed persistence in the soil.     

Apomixis is not prevalent in subnival to nival plants of the European Alps

Background and Aims

High alpine environments are characterized by short growing seasons, stochastic climatic conditions and fluctuating pollinator visits. These conditions are rather unfavourable for sexual reproduction of flowering plants. Apomixis, asexual reproduction via seed, provides reproductive assurance without the need of pollinators and potentially accelerates seed development. Therefore, apomixis is expected to provide selective advantages in high-alpine biota. Indeed, apomictic species occur frequently in the subalpine to alpine grassland zone of the European Alps, but the mode of reproduction of the subnival to nival flora was largely unknown.

Methods

The mode of reproduction in 14 species belonging to seven families was investigated via flow cytometric seed screen. The sampling comprised 12 species typical for nival to subnival plant communities of the European Alps without any previous information on apomixis (Achillea atrata, Androsace alpina, Arabis caerulea, Erigeron uniflorus, Gnaphalium hoppeanum, Leucanthemopsis alpina, Oxyria digyna, Potentilla frigida, Ranunculus alpestris, R. glacialis, R. pygmaeus and Saxifraga bryoides), and two high-alpine species with apomixis reported from other geographical areas (Leontopodium alpinum and Potentilla crantzii).

Key Results

Flow cytometric data were clearly interpretable for all 46 population samples, confirming the utility of the method for broad screenings on non-model organisms. Formation of endosperm in all species of Asteraceae was documented. Ratios of endosperm : embryo showed pseudogamous apomixis for Potentilla crantzii (ratio approx. 3), but sexual reproduction for all other species (ratios approx. 1·5).

Conclusions

The occurrence of apomixis is not correlated to high altitudes, and cannot be readily explained by selective forces due to environmental conditions. The investigated species have probably other adaptations to high altitudes to maintain reproductive assurance via sexuality. We hypothesize that shifts to apomixis are rather connected to frequencies of polyploidization than to ecological conditions.     

How endangered is sexual reproduction of high-mountain plants by summer frosts? Frost resistance, frequency of frost events and risk assessment

In temperate-zone mountains, summer frosts usually occur during unpredictable cold spells with snow-falls. Earlier studies have shown that vegetative aboveground organs of most high-mountain plants tolerate extracellular ice in the active state. However, little is known about the impact of frost on reproductive development and reproductive success. In common plant species from the European Alps (Cerastium uniflorum, Loiseleuria procumbens, Ranunculus glacialis, Rhododendron ferrugineum, Saxifraga bryoides, S. moschata, S. caesia), differing in growth form, altitudinal distribution and phenology, frost resistance of reproductive and vegetative shoots was assessed in different reproductive stages. Intact plants were exposed to simulated night frosts between ?2 and ?14 °C in temperature-controlled freezers. Nucleation temperatures, freezing damage and subsequent reproductive success (fruit and seed set, seed germination) were determined. During all reproductive stages, reproductive shoots were significantly less frost resistant than vegetative shoots (mean difference for LT₅₀ ?4.2 ± 2.7 K). In most species, reproductive shoots were ice tolerant before bolting and during fruiting (mean LT₅₀ ?7 and ?5.7 °C), but were ice sensitive during bolting and anthesis (mean LT₅₀ around ?4 °C). Only R. glacialis remained ice tolerant during all reproductive stages. Frost injury in reproductive shoots usually led to full fruit loss. Reproductive success of frost-treated but undamaged shoots did not differ significantly from control values. Assessing the frost damage risk on the basis of summer frost frequency and frost resistance shows that, in the alpine zone, low-statured species are rarely endangered as long as they are protected by snow. The situation is different in the subnival and nival zone, where frost-sensitive reproductive shoots may become frost damaged even when covered by snow. Unprotected individuals are at high risk of suffering from frost damage, particularly at higher elevations. It appears that ice tolerance in reproductive structures is an advantage but not an absolute precondition for colonizing high altitudes with frequent frost events.     

Resistance to photoinhibition of photosystem II and catalase and antioxidative protection in high mountain plants

In leaves of three alpine high mountain plants, Homogyne alpina, Ranunculus glacialis and Soldanella alpina, both photosystem II (PSII) and the enzyme catalase appeared to he highly resistant to photoinactivation under natural field conditions. While the Dl protein of PSII and catalase have a rapid turnover in light and require continuous new protein synthesis in non-adapted plants, little apparent photoinactivation of PSII or catalase was induced in the alpine plants by translation inhibitors or at low temperature, suggesting that turnover of the Dl protein and catalase was slow in these leaves. In vitro PSII was rapidly inactivated in light in isolated thylakoids from H. alpina and R. glacialis. In isolated intact chloroplasts from R. glacialis, photoinactivation of PSII was slower than in thylakoids. Partially purified catalase from R. glacialis and S. alpina was as sensitive to photoinactivation in vitro as catalases from other sources. Catalase from H. alpina had, however, a 10-fold higher stability in light. The levels of xanthophyll cycle carotenoids, of the antioxidants ascorbate and glulathione, and of the activities of catalase, superoxide dismutase and glutathione reductase were very high in S. alpina, intermediate in H. alpina, but very low in R. glacialis. However, isolated chloroplasts from all three alpine species contained much higher concentrations of ascorbate and glutathione than chloroplasts from lowland plants.     

Diet selection by European hares (Lepus europaeus) in the alpine zone of the Snowy Mountains, Australia

European hares (Lepus europaeus) are grazers and open grassland specialists that are replaced in mountain areas of their natural range in the northern hemisphere by browsing/intermediate feeding mountain hares (Lepus timidus), but in their introduced range in the southern hemisphere, occupy the alpine zone. We used micro-histological identification of plant fragments and germination of seeds in faecal pellets of L. europaeus from the Snowy Mountains, Australia, to determine diet. We asked whether diet shifted and/or diet breadth expanded in response to seasonally reduced food availability, particularly during winter. If so, did the constraints of food availability in the alpine zone lead to the diet mirroring that of L. timidus in its native alpine habitat. The diet of L. europaeus was dominated by grasses, herbs and shrubs. The main diet items in summer were grasses (70 %) and herbs (28 %). Grasses declined in the diet between summer and autumn when herbs increased to co-dominance, with a further change after establishment of the winter snowpack to a greater preponderance of shrubs (43 % compared with a maximum of 3 % in snow-free months). L. europaeus selected a wider range of plants in winter (59 species compared with 39 in summer) and diet was significantly more variable in winter than in autumn or summer (and in autumn than summer). We concluded that the persistence of L. europaeus in alpine areas of the southern hemisphere is testament to their ability to expand their dietary breadth to occupy mountain climatic zones normally occupied by L. timidus.     

Survival types of high mountain plants under extreme temperatures

Extreme temperatures are a main factor limiting plant growth in high mountain habitats. During winter, the risk of frost damage is highest at windblown and often snow-free sites. During summer, actively growing plants are particularly endangered by episodic cold spells, but also by short-term overheating. The current review gives an overview of extreme temperatures in the European Alps and observations of temperature damage on plants in their natural habitats. Furthermore, seasonal time courses of frost and heat resistance derived from laboratory tests on different plant growth forms are presented. Study species were the cushion plants Silene acaulis, Minuartia sedoides, Saxifraga oppositifolia and Carex firma collected on wind-exposed ridges; the rosette plant Soldanella alpina collected on snow-protected sites, and three Sempervivum species collected in xerothermic habitats.     

Inocybe praetervisa group – A clade of four closely related species with partly different geographical distribution ranges in Europe

Sequence data from a broad geographical region and different habitats show that the Inocybe praetervisa clade is comprised of four closely related species. These species of section Marginatae are characterized by having nodulose spores and a stipe that is abundantly pruinose only in the upper half. Inocybe praetervisa occurs in Southern Europe in mountainous mixed coniferous forests, and is not confirmed from Northern Europe. Inocybe rivularis occurs in northern boreal forests up to the lower alpine zone, associated with Betula in moist habitats, and is not confirmed from Southern Europe. Inocybe taxocystis is confirmed as a later synonym of I. favrei. The species has a wide geographical distribution range in Europe, mainly restricted to the alpine zone and moist soils, associated with Salix herbacea. Inocybe arctica is here described as a new species. It occurs in the arctic and higher alpine zones, associated with Dryas octopetala, Salix polaris, S. reticulata and S. herbacea. All species except I. arctica are shown to have an intercontinental distribution range and are confirmed from North America. Sequence data suggest the occurrence of one additional species in the alpine zone of China. A key to the species in the I. praetervisa group is provided.     

The cytotaxonomy and origin ofRanunculus yaegatakensis,an endemic taxon of Yakushima Island

Ranunculus yaegatakensis, a close relative of the widespreadR. silerifolius, is endemic to the alpine region (ca. 1,600 m alt.) of Yakushima Island. This species differs morphologically fromRanunculus silerifolius mainly due to its dwarfism and leaf shape, but has an identical karyotype with one (Karatsu-type) of the four cytotype ofR. silerifolius. Ranunculus yaegatakensis is highly cross-compatible with the Karatsu-type plants ofR. silerifolius. Their F₁ hybrids show regular meiotic behaviors and set seeds successfully. In addition, the Karatsu-type ofRanunculus silerifolius is found in individuals that are collected not only from the lowland of Yakushima Island but from its neighboring islands. It is supposed to be more specialized than other cytotypes. This evidence suggests thatRanunculus yaegatakensis has been derived from the Karatsu-type plants ofR. silerifolius. We suggest thatRanunculus yaegatakensis be reduced to a variety ofR. silerifolius.     

Do moss samples,pollen traps and modern lake sediments all collect pollen in the same way? A comparison from the forest limit area of northernmost Europe

Moss polsters, pollen traps and lake surface sediment samples are commonly used as climate calibration data or as modern analogues for reconstructing vegetation from fossil profiles, but the differences in pollen content between these media have received little attention. This study aims to analyse how the three media differ in reflecting individual vegetation types and spatial differences in vegetation. 119 modern samples (64 moss polsters, 37 lake surface sediment samples and 18 pollen traps from which a collection was made annually) were taken from northern Fennoscandia and the Kola Peninsula as a broad transect crossing the northernmost forest limits of Betula pubescens ssp. czerepanovii (mountain birch), Pinus sylvestris (Scots pine) and Picea abies (Norway spruce). The pollen assemblages from these samples were compared with the surrounding vegetation visually and via PCA (principle components analysis) and cluster analysis. Both comparisons allow a correct distinction between pollen assemblages of arctic/alpine heath, mountain birch dominated areas, and boreal coniferous forests. The differences between the vegetation zones are stronger than the differences between the sampling media. Nevertheless, lake sediment samples from the mountain birch woodland zone tend to overestimate pine and underestimate birch. Pollen traps are biased towards lower tree pollen percentages and higher values of shrubs, herbs and Cyperaceae. This bias is especially strong in traps that have missing years in the data. Irrespective of the vegetation zone, pollen traps tend to have lower Pinus pollen percentages than in the adjacent moss polsters.     

The effect of alpine ski-slopes on epigeic beetles: does even a nature-friendly management make a change?

Unique alpine ecosystems are threatened by skiing activities all over the world. We studied the effect of alpine ski-slopes on epigeic beetles by pitfall trapping in the Praděd National Nature Reserve (Czech Republic) where the management of ski-slopes has never caused any disturbance to the vegetation cover. Using a mixed modelling approach, we demonstrate a significant effect of ski-slope management on the epigeic beetle community, including its functional diversity. Beetle species responded to the ski-slope individually. We found a noticeable decline in the abundance of most species in the patches with artificially increased accumulation of snow, i.e. close to the interior edges of the ski-slopes. Above all, the ski-slopes were not preferred by relict species such as Neagolius limbolarius, Minota carpathica and Liotrichus affinis but vagile widespread carabids (Amara lunicollis, Poecilus versicolor) and herbivores associated with nitrophilous plants (Gastrophysa viridula) were more abundant on the ski-slopes. A few stenotypic carnivorous and herbivorous species were found on the ski-slopes. A high abundance of mountain herbivores such as leaf beetle Timarcha metallica reflected an increased occurrence of their host plants and carnivores such as Carabus sylvestris and Pterostichus oblongopunctatus could prefer ski-slopes due to the locally increased food supply. With respect to both uniqueness of alpine communities and to the small extent of alpine treeless zone, we recommend considering very cautiously any potential expansion of ski resorts, even those with reasonable ‘nature-friendly’ practices.     

Cytotype stability, facultative apomixis and geographical parthenogenesis in Ranunculus kuepferi (Ranunculaceae)

Background and Aims

Asexual organisms are more widespread in previously glaciated areas than their sexual relatives (‘geographical parthenogenesis’). In plants, this pattern is probably dependent on reproductive isolation and stability of cytotypes within their respective distribution areas. Both partial apomixis and introgressive hybridization potentially destabilize the spatial separation of sexual and apomictic populations. The wide distribution of apomicts may be further enhanced by uniparental reproduction which is advantageous for colonization. These factors are studied in the alpine species Ranunculus kuepferi.

Methods

Geographical distribution, diversity and mode of reproduction of cytotypes were assessed using flow cytometry and flow cytometric seed screening on samples from 59 natural populations of Ranunculus kuepferi. Seed set of cytotypes was compared in the wild.

Key Results

Diploid sexuals are confined to the south-western parts of the Alps, while tetraploid apomicts dominate in previously glaciated and in geographically isolated areas despite a significantly lower fertility. Other cytotypes (3x, 5x and 6x) occur mainly in the sympatric zone, but without establishing populations. The tetraploids are predominantly apomictic, but also show a partial apomixis via an uncoupling of apomeiosis and parthenogenesis in the seed material. Both pseudogamy and autonomous endosperm formation are observed which may enhance uniparental reproduction.

Conclusions

Diploids occupy a glacial relic area and resist introgression of apomixis, probably because of a significantly higher seed set. Among the polyploids, only apomictic tetraploids form stable populations; the other cytotypes arising from partial apomixis fail to establish, probably because of minority cytotype disadvantages. Tetraploid apomicts colonize previously devastated and also distant areas via long-distance dispersal, confirming Baker''s law of an advantage of uniparental reproduction. It is concluded that stability of cytotypes and of modes of reproduction are important factors for establishing a pattern of geographical parthenogenesis.     

The new locally endemic genus Yazdana (Caryophyllaceae) and patterns of endemism highlight the high conservation priority of the poorly studied Shirkuh Mountains (central Iran)

Although mountain ranges are often recognized as global biodiversity hotspots with a high level of endemism, diversity and biogeographic connections of isolated and weakly explored mountains remain poorly understood. This is also the case for Shirkuh Mts. in central Iran. Here, Yazdana shirkuhensis gen. & spec. nov. (Caryophylleae, Caryophyllaceae) is described and illustrated from the high alpine zone of this mountain. Molecular phylogenetic analyses of nuclear and plastid DNA sequence data show that Y. shirkuhensis is related to Cyathophylla and Heterochroa (tribe Caryophylleae). The newly described genus and species accentuate Shirkuh Mts. as a center of endemism, which harbors a high number of narrowly distributed species, mostly in high elevations reaching alpine habitats. As this area is currently not protected, a conservation priority is highlighted for high elevations of Shirkuh Mts.     

Reproductive biology of Ranunculus weyleri (Ranunculaceae), a narrowly endemic plant from the Balearic Islands with disjunct populations

Ranunculus weyleri is a species endemic to Mallorca Island (western Mediterranean basin) that is currently threatened due to its reduced geographical distribution and disjunct, isolated populations. It is a small, perennial herb that inhabits rocky environments, together with other endemic plants with creeping life-forms. In the present study, for the first time the reproductive biology of the species was investigated in terms of its floral phenology (floral stages and times of formation), pollen/ovule (P/O) ratios, and fruit and seed setting under natural and pollen manipulation experiments, assessing the breeding system, pollination vectors and pollen limitations. Cross-pollinations among populations were performed to evaluate the levels of compatibility between populations. In addition, the floral displays and the reproductive outputs of four wild populations were determined. The observed high P/O ratios, results of the hand-pollination experiments, and flower traits indicate that this species is predominantly allogamous. Combinations of both insects (belonging to Coleoptera, Diptera, Lepidoptera and Hymenoptera) and wind (ambophily) constitute the main pollination vectors, and pollen limitation was observed. Interpopulation crossing was effective, and exogamic depression was not present, as evidenced by the fecundity levels. The predation of the floral stems by herbivores (mainly goats) severely limits the reproductive success of this endemic species in wild populations. Finally, several ways of action are proposed for R. weyleri conservation.     

Terrestrial bugs (Heteroptera) in high mountains of the Suntar-Khayata Range (Eastern Yakutia)

Thirty-nine species of bugs, representing meso-and xerophilic inhabitants of open tundra, meadow, and steppe landscapes, were collected within the altitude range of 1260–1850 m above sea level in the upper Kyubyume River basin (63°13′N, 139°36′E, the Indigirka River basin). In the sub-golets sparse forest zone (up to 1550 m), 37 species were recorded, the dominant form being Chlamydatus pullus. The bugs were rare in most of the habitats; their species richness and abundance increased distinctly only on the south-facing slopes, reaching the maximum in the cryophytic steppe. The specific features of these complexes manifested themselves in the prevalence of Capnoda nigroaenea, a xerophilic species of alpine mountain steppes. The rest of the dominants comprised the ecologically flexible Emblethis brachynotus, Chlamydatus pullus, and Galeatus spinifrons. In the goletstundra zone, 8 species were found, half of them being arctic forms (Calacanthia trybomi, Orthotylus artemisiae, Ch. wilkinsoni, and Ch. opacus). Ch. wilkinsoni was the most common species. The species composition of bug groups in the dry lichen-dryad communities within this zone resembled that of similar communities of zonal tundra, whereas the humid habitats remained unpopulated, unlike their plain analogues. Comparison of the heteropteran fauna of mountain tundras in different regions of the Verkhoyansk-Kolyma mountain country attests to significant variations of its species composition. The possible reasons for these differences are discussed.     

Altitudinal variation in Arianta arbustorum (Mollusca,Pulmonata) in the Swiss Alps

Arianta arbustorum is a highly variable helieid snail found in Europe. We have studied biometrically its transition from low altitude where large dark phenotypes are typical, to higher altitudes in the Alps, where small light ones are found. Seven measurements and 10 colour characters were considered. Size varies with altitude while colours rather vary with habitats. Our observations on 5 alpine transects agree with those of previous authors who sampled other alpine areas. It indicates that the species' reaction to alpine conditions is general to large mountain regions. This provides a striking example of consistent variation. Previous authors claim that midland and alpine Arianta stem from different colonizing stocks. However, part of the variation found in the present study appears to be adaptive. Both interpretations can be reconciled.     

Unveiling a wildlife haven: occupancy and activity patterns of mammals at a Tibetan sacred mountain

Here, we present a camera trap survey at a Tibetan sacred mountain to ascertain the status and activity patterns of medium- to large-sized ground-dwelling mammalian fauna. We recorded 15 medium- to large-sized mammal species including 9 carnivores, 4 ungulates, 1 primate, and 1 rodent. Six of the species were categorized by IUCN as globally threatened. The results suggested that the sacred mountain was particularly important for alpine ungulates. The mean occupancy probabilities of blue sheep Pseudois nayaur, Chinese goral Naemorhedus griseus, Chinese serow Capricornis milneedwardsii, and alpine musk deer Moschus chrysogaster were 0.93, 0.91, 0.87, and 0.44 respectively. Domestic dog Canis familiaris also occurs widely across the mountain, with a mean occupancy of 0.60. Temporal activity patterns showed that alpine musk deer were mostly nocturnal, with most captures occurring at night. Chinese serow were active at all periods, with an activity peak at dawn. Blue sheep were strictly diurnal, without any captures at night. Although Chinese goral were predominantly diurnal, captures also frequently occurred at night. Our study not only unveiled a wildlife haven benefiting from religious beliefs about sacred mountains but also pointed to the critical situation of the fauna in the sacred site. The fauna in such sacred sites are diverse but poorly studied, and are subject to threats from domestic dogs, garbage pollution, and population isolation. Future conservation and management efforts in such areas should evaluate the population genetic diversity and assess the impact of non-lethal human disturbance on the wildlife communities.     

The extreme disjunction between Beringia and Europe in Ranunculus glacialis s. l. (Ranunculaceae) does not coincide with the deepest genetic split – a story of the importance of temperate mountain ranges in arctic–alpine phylogeography

The arctic–alpine Ranunculus glacialis s. l. is distributed in high‐mountain ranges of temperate Europe and in the North, where it displays an extreme disjunction between the North Atlantic Arctic and Beringia. Based on comprehensive sampling and employing plastid and nuclear marker systems, we (i) test whether the European/Beringian disjunction correlates with the main evolutionary diversification, (ii) reconstruct the phylogeographic history in the Arctic and in temperate mountains and (iii) assess the susceptibility of arctic and mountain populations to climate change. Both data sets revealed several well‐defined lineages, mostly with a coherent geographic distribution. The deepest evolutionary split did not coincide with the European/Beringian disjunction but occurred within the Alps. The Beringian lineage and North Atlantic Arctic populations, which reached their current distribution via rapid postglacial colonization, show connections to two divergent pools of Central European populations. Thus, immigration into the Arctic probably occurred at least twice. The presence of a rare cpDNA lineage related to Beringia in the Carpathians supports the role of these mountains as a stepping stone between temperate Europe and the non‐European Arctic, and as an important area of high‐mountain biodiversity. The temperate and arctic ranges presented contrasting phylogeographic histories: a largely static distribution in the former and rapid latitudinal spread in the latter. The persistence of ancient lineages with a strictly regional distribution suggests that the ability of R. glacialis to survive repeated climatic changes within southern mountain ranges is greater than what recently was predicted for alpine plants from climatic envelope modelling.     

The role of spontaneous selfing in the pioneer species Saxifraga aizoides

A large variety of reproductive patterns is present among alpine plants to ensure the persistence of populations in such harsh environments. In the present study, the role of spontaneous selfing and its contribution to the actual reproductive success of an alpine pioneer plant was investigated. The results showed that Saxifraga aizoides is clearly self-compatible. Open-pollinated flowers exhibited higher seed numbers per capsules than selfing flowers, albeit the difference was not significant. Although seed weight seemed to be independent from the kind of pollination, open-pollinated flowers had a significantly higher proportion of germinated seeds than selfed ones. Furthermore, the ability of fast germination found in S. aizoides enables the seeds to take advantage of all possible opportunities for germination. In summary, S. aizoides exhibits a successful recruitment strategy for an alpine pioneer species.