Convergence in leaf phenology traits of two understory ferns in the northwestern Iberian Peninsula

Aims Plants control leaf phenology to maximize annual photosynthetic product. Although ferns play an important ecological role in many habitats, especially forests, their phenology traits have been poorly studied. Here, we investigate the leaf phenology of two ferns of the forest understorey and analyse the relationship between the timing of leaf emergence and spore dispersal and the effect of between-year climatic variation.Methods We compared the leafing and sporing phenologies of two ferns with very large (>2 m), overwintering leaves: Culcita macrocarpa and Woodwardia radicans. We regularly monitored individuals of six populations in the northwestern Iberian Peninsula during a 3-year study. We studied eight phenology variables: leafing start date, leafing end date, leaf expansion time, number of new leaves per individual, between-individual synchrony, within-individual synchrony, percentage of fertile leaves and spore release date. We also determined leaf mass per area (LMA) and gathered data on air temperature and humidity.Important findings Both C. macrocarpa and W. radicans produce few leaves (~2 leaves individual^-1 year^-1), which expand simultaneously for a very long period (from midwinter to early summer), are retained for more than 1 year (37 and 19 months, respectively) and have relatively high LMAs. Such traits, together with large leaf size, have also been found in seed plants from the forest understorey and represent adaptations to this light-limited environment. Spores of both study ferns are simultaneously released in late winter, with little between-year variation caused by differences in air humidity. This remarkable similarity between species suggests that the convergence in timing of leaf emergence favours the convergence in timing of spore dispersal.     

Fern and lycopod spores rain in a cloud forest of Hidalgo,Mexico

The aim of this study was to determine the composition of the “spore rain” of ferns and lycopods in a cloud forest. We tested whether the canopy impedes spore dispersal to surrounding areas and how spore dispersal is affected by rainfall. The spores were captured with a modified Bush–Gosling trap placed at 30 cm above ground level in forested and non-forested sites from March 2009 to February 2010. We collected 2462 fern spores from 158 morphospecies of which 76 were identified to species level. Thirty-seven species were found exclusively in the spore rain, and 39 were found as sporophytes as well (local component). Mean daily spore density (spores m^?2) was calculated to find the sporulation period for each species. Twenty species showed seasonal patterns of sporulation. The highest spore density was found at the forested site (70 morphospecies and 1856 spores), of which 39 morphospecies (1482 spores) corresponded to the local vegetation. Fifty-five taxa were shared between the forested and non-forested site. In the non-forested site, 605 spores were captured belonging to 64 species. The density of spore rain between sites was significantly different. The rainfall amount was the same at both sites, with a dry period in March, April, and July 2009, and February 2010. There was a negative effect of rainfall on spore rain. The main sporulation occurred in the dry season with strong winds. Although the canopy inhibits airborne dispersal of fern spores, a small amount of spores can disperse beyond the canopy and reach surrounding areas. The rainfall might wash spores to ground and favor the colonization and the establishment of new populations.     

蕨类植物不同孢子裂缝类型在中国的分布格局

孢子在蕨类植物分类及有性生殖过程中具有重要地位, 一般都具有裂缝构造, 常见的是单裂缝和三裂缝, 极少数情况下有多裂缝的变异类型。我们统计了中国蕨类2,281种(含种下单位)的孢子裂缝类型, 来探讨两种不同裂缝类型的分布格局。结果表明: (1)具有单裂缝类型的物种数多于三裂缝类型, 单裂缝与三裂缝物种数目的比值(单/三比)与纬度和海拔呈正相关。随着温度下降以及降水量的降低, 具单裂缝孢子的物种比例增加。推测具单裂缝孢子的蕨类分布范围更广, 更适宜生活在干旱及高纬度或高海拔寒冷地区, 而具三裂缝孢子的蕨类更适宜存在于低纬度或低海拔的温暖地区; (2)蕨类植物孢子裂缝类型不是单次起源, 可能存在平行演化。本研究可以为蕨类植物的起源演化与生态适应等研究提供一定的证据。     

Insect–fern interactions: macrolepidopteran utilization and species–area association

Abstract.

• 1 The generalization that ferns are under-utilized by phytophagous insects in comparison to angiosperms may be invalid because of biases involving plant growth form, plant range, and unequal sampling efforts.
• 2 Comparison of nineteen fern species with 652 herb species, the angjosperm growth form most similar to the ferns, indicates no significant difference in the mean number of supported macrolepidopteran species. When the herbs are subdivided into annuals, biennials and perennials, only the annual herbs are significantly different than the ferns.
• 3 Comparisons of the occurrence distributions for ferns and the herb categories also demonstrate that only the annual herbs support more macrolepidopteran species than the ferns. The same results are obtained when random assemblages of herbs are created that are the same size as the fern assemblage.
• 4 Both the occurrence distributions and the species–area relationship for the ferns indicate that host records for insects feeding on ferns may be grossly incomplete.
• 5 The similarity of exploitation of ferns and perennial herbs by the Macro-lepidoptera suggests that other foliage feeding insects may also use ferns at levels equivalent to angiosperms.

     

Water properties in fern spores: sorption characteristics relating to water affinity, glassy states, and storage stability

Ex situ conservation of ferns may be accomplished by maintaining the viability of stored spores for many years. Storage conditions that maximize spore longevity can be inferred from an understanding of the behaviour of water within fern spores. Water sorption properties were measured in spores of five homosporeous species of ferns and compared with properties of pollen, seeds, and fern leaf tissue. Isotherms were constructed at 5, 25, and 45 degrees C and analysed using different physicochemical models in order to quantify chemical affinity and heat (enthalpy) of sorption of water in fern spores. Fern spores hydrate slowly but dry rapidly at ambient relative humidity. Low Brunauer-Emmet-Teller monolayer values, few water-binding sites according to the D'Arcy-Watt model, and limited solute-solvent compatibility according to the Flory-Huggins model suggest that fern spores have low affinity for water. Despite the low water affinity, fern spores demonstrate relatively high values of sorption enthalpy (DeltaH(sorp)). Parameters associated with binding sites and DeltaH(sorp) decrease with increasing temperature, suggesting temperature- and hydration-dependent changes in volume of spore macromolecules. Collectively, these data may relate to the degree to which cellular structures within fern spores are stabilized during drying and cooling. Water sorption properties within fern spores suggest that storage at subfreezing temperatures will give longevities comparable with those achieved with seeds. However, the window of optimum water contents for fern spores is very narrow and much lower than that measured in seeds, making precise manipulation of water content imperative for achieving maximum longevity.     

Lepidopteran Soral Crypsis on Caribbean Ferns1

Insect‐fern interactions are not as well characterized as insect‐angiosperm interactions. For example, the imitation of unique fern structures by insects has not been observed. On a recent trip to Puerto Rico, we collected ferns that bore small Lepidoptera imitating fern sori. Herbarium specimen searches indicate that these Lepidoptera are restricted to the Caribbean on ferns with highly visible sporangia. A possible selective pressure for the evolution of lepidopteran soral crypsis is wasp parasitism, as evidence of parasitoid wasps was found. However, it is more likely that soral crypsis evolved to avoid visually oriented predators such as birds or lizards.     

Macrosiphum on ferns: taxonomy,biology and evolution,including the description of three new species (Hemiptera: Aphididae)

The phytophagous insect fauna of ferns has often been described as depauperate, and some have pointed to the paucity of evidence for adaptive radiation of insect groups feeding specifically on ferns. This paper examines the world's species of fern‐specific Macrosiphum aphids and attempts to determine whether fern‐feeding is a monophyletically derived trait in Macrosiphum. All sixteen species reported to feed on ferns, including three new species, were included in a cladistic analysis, along with fifteen other Macrosiphum species selected to represent the diversity of the genus, Papulaphis sleesmani (Pepper), because of its similarity to fern‐feeding Macrosiphum, and Sitobion avenae (Fabricius), which was used as outgroup. The results gave good support for the monophyly of fifteen of the sixteen fern‐feeders, and also supported a clade consisting of these fifteen fern‐feeders plus Macrosiphum equiseti (Holman), an Equisetum‐specific aphid. One species, Macrosiphum lapponicum Shaposhnikov, from northern Russia, was concluded to be unrelated to other fern‐feeding Macrosiphum. Whether this species truly feeds on a fern requires confirmation. Taxonomic and biological notes are provided for all fern‐feeding Macrosiphum of the world. These include one new combination, Macrosiphum cyatheae (Holman) comb.n., and three new species: Macrosiphum longirostratum sp.n. on Woodsia mollis and Woodsia sp. from Mexico (Michoacán), Macrosiphum miho sp.n. on ‘Aspidium’ sp. from the U.S.A. (Illinois) and Macrosiphum rebecae sp.n. on Adiantum sp. from Mexico (Michoacán). Keys to apterous and alate viviparae of Macrosiphum living on ferns are given.     

Does lack of available suitable habitat explain the patchy distributions of rare calcicole fern species?

In Canada, as in many countries, a relatively large number of fern species occur in specialized habitats and have low numbers of known populations containing few individuals. It has been suggested that the distribution of ferns is mostly determined by factors of climate and habitat due to relatively low limitations in ferns for dispersal and establishment. Here, we attempt to explain whether the local patchy distribution of three calcicole fern species rare in Canada ( Asplenium ruta-muraria , Pellaea atropurpurea and Woodsia obtusa ) is due to a lack of available habitat. Analyses based on micro-scale differences between sites occupied by the ferns and nearby, unoccupied sites did not reveal any significant differences, thereby indicating that the rarity of these species is not entirely driven by the rarity of their microhabitat at a local scale. Our results suggest that the widely accepted premise that ferns are not limited by dispersal or establishment should be reconsidered, as such limitations are the only likely explanation for empty available and suitable habitat.     

A current perspective on apomixis in ferns

This review provides a synopsis of apogamous reproduction in ferns and highlights important progress made in recent studies of fern apomixis. First, a summary of the apomictic fern life cycle is provided, distinguishing between two pathways to diploid spore production that have been documented in apomictic ferns (premeiotic endomitosis and meiotic first division restitution) and briefly discussing the evolutionary implications of each. Next, recent trends in fern apomixis research are discussed, exposing a shift in focus from the observation and characterization of apomixis in ferns to more integrated studies of the evolutionary and ecological implications of this reproductive mode. Peer-reviewed contributions from the past decade are then summarized, spanning the identification of new apomictic lineages through to the developmental, phylogenetic, and population genetic insights that have been made in studies of fern apomixis during that time. Gaps in our understanding are also discussed, including the extent and implications of recombinant apomixis in ferns, the possible reversibility of reproductive mode (from apomictic to sexual) in ferns, and the genomic causes and consequences of apomixis in seed free vascular plants. To conclude, future directions for fern apomixis research are proposed in the context of modern technological advances and recent insights from studies of apomixis in other groups.     

Biological and nutritional aspects involved in fern multiplication

Gametophytes of several species of ferns were mechanically triturated and the resulting homogenates cultured in vitro for propagation purposes. Differences in the time period from spore culture to sporophyte development were perceivable between species. For those species with a fast life cycle and high sporophyte production such as Woodwardia virginica and Dryopteris affinis sp. affinis, homogenization of gametophytes can be considered to be excellent method for propagation, yielding hundreds of sporophytes in a short period of time. Sporophyte formation was inhibited in O. regalis by the succesive application of homogenization to gametophytes regenerated by this technique. The effect of the culture medium composition on fern production was also studied in O. regalis and P. ensiformis gametophytes. In these species, sporophyte formation increased when the gametophytes were cultured in a medium containing water+0.7% agar. Addition of sucrose inhibited gametophyte development and induced their necrosis. The 1/2 dilution of Murashige and Skoog basal medium, without sucrose, favoured leaf expansion in P. ensiformis sporophytes. This revised version was published online in June 2006 with corrections to the Cover Date.     

Fern and bryophyte endozoochory by slugs

Endozoochory plays a prominent role for the dispersal of seed plants, and dispersal vectors are well known. However, for taxa such as ferns and bryophytes, endozoochory has only been suggested anecdotally but never tested in controlled experiments. We fed fertile leaflets of three ferns and capsules of four bryophyte species to three slug species. We found that, overall, spores germinated from slug feces in 57.3 % of all 89 fern and in 51.3 % of all 117 bryophyte samples, showing that the spores survived gut passage of slugs. Moreover, the number of samples within which spores successfully germinated did not differ among plant species but varied strongly among slug species. This opens new ecological perspectives suggesting that fern and bryophyte endozoochory by gastropods is a so-far-overlooked mode of dispersal, which might increase local population sizes of these taxa by spore deposition on suitable substrates.     

A ten year study of the incidence of spores of bracken, (Pteridium aquilinum (L.) Kuhn.) in an urban rooftop airstream in south east Scotland

Field studies of bracken during sporing haveindicated very high numbers of sporesreleased per cubic metre of air. Thecarcinogenic nature of bracken spores poses ahealth hazard to workers and visitors in areasof sporing strands.A retrospective study of bracken spores trappedon slides exposed during Augustand September over the ten year period, 1988–1997, on a rooftop site in Edinburgh,has added an urban dimension to the aerobiologyof bracken.Results have revealed, apart from 1989,consistently low counts. The spore samplerwas situated downwind approximately 1.6 km fromthe nearest sporing stand.A spore calendar, based on the ten years ofcumulative data, has been constructed.     

Phenology and wintering capacity of sporophytes and gametophytes of ferns native to northern Japan

Summary To investigate life history adaptations to cold climates, the leaf development, sporulation period, growing stage of gametophytes, and the frost and drought resistance of sporophytes and gametophytes of 67 fern species native to Kokkaido were studied. Most ferns common in Hokkaido are summer-green with leaves developing during late May to June and decaying during October. Most of the ferns in Hokkaido sporulate during August to early September. Spores dispersed from June to September germinate before winter begins, forming vegetative prothallia. Gametophytes mature only in the following summer. Thus in Hokkaido the gametophytes as well as perennial sporophytes are exposed to severe winter conditions. In order to correlate the life cycles of temperate ferns with winter cold stress, frost resistance of gametophytes, rhizomes, and leaves of sporophytes were determined. Maximal frost resistance of rhizomes reflects the stress conditions of their habitats: rhizomes of forest understory ferns are damaged at-5°to -17.5°C, epiphytic ferns and ferns of habitats exposed to severe frost sustained temperatures of -20° to-40°C. The leaves of winter-green and evergreen ferns resist frost ranging from -25° to -40°C. The leaves of summer-green ferns are killed by late frost below -5°C. With some exceptions, gametophytes of ferns growing on the forest floor resist frost to -40°C and are much hardier than sporophytes. These results suggest the possible restrictive effects of cold climate on the life span of leaves as well as on the sporulation period. If winter cold is one of the decisive factors for seasonality expression and habitat distribution of ferns, the sensitive generation must be the sporophyte rather than the gametophyte. The hardier gametophyte is therefore able to colonize habitats in which the sporophyte is excluded by frost if mechanisms of vegetative propagation are evolved.Contribution No. 2451 from The Institute of Low Temperature Science     

液体培养基条件下乌毛蕨配子体发育的研究

在液体培养基条件下对中国产乌毛蕨(Blechnum orientaleL.)配子体发育进行了观察。结果表明:乌毛蕨的孢子为两面体型,两侧对称,极面观为椭圆形,赤道面观为半圆形或豆形,周壁具脊状褶皱;孢子萌发为书带蕨型;原叶体发育为三叉蕨型,成熟原叶体为对称的心脏形。经比较分析,蕨类植物孢子繁殖时采用混合土培养较适宜;液体培养基和混合土在研究蕨类植物配子体发育时同样具有可行性。孢子形态和配子体发育的观察结果表明,乌毛蕨是蕨类植物中较进化的种类;乌毛蕨科与鳞毛蕨科亲缘关系较近。     

附生蕨类植物的克隆性研究进展

石松类及蕨类植物在高等植物中处于比较特殊的进化与系统发育地位, 同时具有孢子植物(孢子)与种子植物(维管束)的双重特征。附生蕨类植物是蕨类植物中占据独特生境的一个大类群, 其生活史策略及进化历史与其附生生长的森林生态系统紧密相关。大部分附生蕨类植物的克隆生长习性及克隆生活史性状在其生态适应中具有重要作用, 但这方面未引起广泛关注。本文主要综述了中国山地森林中附生蕨类植物的根状茎克隆生长、克隆性与生态适应性、不同克隆生长方式与进化等方面, 并展望了蕨类植物克隆性在森林生态系统过程与功能中的作用, 以及今后如何将蕨类植物生态学研究与气候变化、植被恢复、土地利用变化等全球变化的主流方向进行结合。     

First report of fern (Culcita macrocarpa) spore consumption by a small mammal (Apodemus sylvaticus)

Few vertebrates are known to consume ferns regularly. Several species of mammals consume leaves to some extent but the consumption of fern spores is much rare. In Galicia (Northwest Spain) we studied the seasonal variation in the consumption of Culcita macrocarpa fertile leaves (i.e. with spores) in two populations (Capelada and Eume), assessed whether consumption rate increased with fern population size, and evaluated whether the consumer was a spore predator or a spore disperser. Consumption began in December and finished by mid February, and occurred before spore release, which happened later in Capelada than in Eume, probably influenced by differences in altitude. The consumer was identified as Apodemus sylvaticus by DNA analysis of its droppings and by capture of live animals. Throughout Galicia there was a significant increase in fern consumption rate as the population size of C. macrocarpa increased. Germination tests from droppings were carried out in 14 dishes but only in two dishes 1% and 0.3% of the spores germinated. Our results suggest that woodmouse can disperse spores of C. macrocarpa, although most of the spores were digested.     

Biochemical and evolutionary aspects of arthropod predation on ferns

Summary The widely held assumption that very few arthropods feed on ferns was questioned following field observations of arthropod damage on ferns in the state of Veracruz, Mexico. The extent and type of damage was recorded and it was found that in a measured locality, ferns were no less attacked than the angiospermous flora. As chemistry and arthropod host relationships have been shown to be so closely intertwined, plants collected in the field were analysed for both condensed tannins and cyanogenic glycosides, compounds known to be effective deterrents in temperate climates. Although all ferns tested contained tannins these did not appear to inhibit predation. Cyanogenic glycosides were present in only 3% of the fern species analysed, and it is, therefore, unlikely that they play a significant role as defensive compounds in the ferns examined.A literature search revealed a large number of ferns cited as being arthropod hosts. Approximately 420 named species of arthropods have been recorded, the majority of which are from the orders Coleoptera, Hymenoptera, Lepidoptera, and Hemiptera. Both evolutionary primitive (sawflies) and advanced (moths) arthropods are reported to be present on ferns suggesting possible coevolution of arthropods and ferns both before and after the radiation of angiosperms.     

Invasive feral pigs impact native tree ferns and woody seedlings in Hawaiian forest

Invasive mammals can fundamentally alter native plant communities, especially on isolated islands where plants evolved without them. The globally invasive feral pig (Sus scrofa) can be particularly destructive to native plant communities. Tree ferns are an important understory component in many forests facilitating the establishment of a variety of species. However, the extent and effects of feral pig damage to tree ferns, and associated impacts on plant community regeneration, are largely unknown. We quantified the effect that feral pig damage has on tree fern growth, survival, and epiphytic woody seedling abundance over 1 year on 438 randomly selected tree ferns of three endemic species (Cibotium chamissoi, Cibotium glaucum, and Cibotium menziesii) in a Hawaiian montane wet forest with high tree fern and feral pig densities. Across all tree fern species, feral pigs damaged 13 % of individuals over 1 year. Compared with undamaged tree ferns, moderately- to heavily-damaged individuals had decreases of 4 to 27 % in trunk length increment and lost tenfold more fronds. Tree fern angle (standing, leaning, prone, or semi-prone) and woody seedling abundance co-varied with feral pig damage. Specifically, damaged tree ferns were more often prone or semi-prone and supported more seedlings, but also had annual mortality up to 34 % higher than undamaged tree ferns. Overall, feral pig damage had substantial negative effects on tree ferns by reducing growth and survival. Given the importance of tree ferns as regeneration sites for a variety of native plants, feral pig damage to tree ferns will likely alter future forest composition and structure. Specifically, feral pig damage to tree ferns reduces potential establishment sites for species that either regenerate preferentially as epiphytes or are currently restricted to epiphytic establishment due to ground rooting by feral pigs.     

Functional traits: Adaption of ferns in forest

Ferns that evolved from 400 million years ago show various functional traits and ecological strategies in extant species, over 80% of which belong to the youngest order Polypodiales. How the functional traits and strategies of ferns have changed during their evolutionary history remains unexplored. Here, we measured functional traits that are sensitive to environmental light and water availability in 345 fern species across fern phylogeny, and reconstructed their evolutionary histories. We found that ferns, mainly Polypodiales, have developed diversified functional traits in response to forest environments. Terrestrial species, especially Thelypteridaceae and Athyriaceae in eupolypods II, since the late Jurassic period, have shown decreased leaf mass per area (LMA) and area-based leaf nitrogen (N_area), but increased mass-based leaf nitrogen (N_mass) compared with early-derived polypods. Epiphytic species, mainly those in Polypodiaceae, have shown reductions in N_mass and individual leaf area (Area) since the late Cretaceous period. The adaption of functional traits of Polypodiales to forest environment may have played a crucial role in fern radiation since the late Jurassic period. Integrative analysis of functional traits, especially numerical ones, may shed new light on plant evolution.     

Recurrent genome duplication events likely contributed to both the ancient and recent rise of ferns

Ferns, the second largest group of vascular plants, originated ～400 mil ion years ago(Mya). They became dominant in the ancient Earth landscape before the angiosperms and are stil important in current ecosystems.Many ferns have exceptional y high chromosome numbers,possibly resulting from whole-genome duplications(WGDs).However, WGDs have not been investigated molecularly across fern diversity. Here we detected and dated fern WGDs using a phylogenomic approach and by calculating synonymous substitution rates(Ks). We also investigated a possible correlation between proposed WGDs and shifts in species diversification rates. We identified 19 WGDs: three ancient events along the fern phylogenetic backbone that are shared by 66%–97% of extant ferns, with additional lineage-specific WGDs for eight orders, providing strongevidence for recurring genome duplications across fern evolutionary history. We also observed similar Ks peak values for more than half of these WGDs, with multiple WGDs occurring close to the Cretaceous(～145–66 Mya). Despite the repeated WGD events, the biodiversity of ferns declined during the Cretaceous, implying that other factors probably contributed to the floristic turnover from ferns to angiosperms. This study provides molecular evidence for recurring WGDs in ferns and offers important clues to the genomic evolutionary history of ferns.