International Journal of
Biodiversity and Conservation

  • Abbreviation: Int. J. Biodivers. Conserv.
  • Language: English
  • ISSN: 2141-243X
  • DOI: 10.5897/IJBC
  • Start Year: 2009
  • Published Articles: 635

Review

Physiological ecology of ferns: Biodiversity and conservation perspectives

O. Roger Anderson
  • O. Roger Anderson
  • Biology and Paleo Environment, Lamont-Doherty Earth Observatory of Columbia University, Palisades, 10964 New York, USA.
  • Google Scholar


  •  Received: 13 March 2021
  •  Accepted: 23 April 2021
  •  Published: 30 April 2021

 ABSTRACT

Ferns have a long geological record extending over millions of years, and they are distributed in diverse environments worldwide; including swamps, coastal locations, open grasslands, mountain terrains, drylands and deserts. Consequently, their physiological ecology is rich with examples of the fern species diversity, and remarkable adaptive variability. This is a review of some major aspects of their physiological ecology (that is, water relations and desiccation tolerance, light and photosynthesis, and temperature and physiological responses), focusing on terrestrial and epiphytic ferns in diverse global geographic locales. Ferns are important economically in horticultural commerce and provide significant ecological services. Climate change and destruction of their natural habitats may lead to extensive loss of fern biodiversity; and some of the current issues related to the protection of their natural habitat and conservation of fern species are addressed.

 

Key words: Biological adaptation, climate change, geographic distribution, human impact, plant evolution.


 INTRODUCTION

Ferns, encompassing approximately 12,000 species (PPG 1, 2016), represent only about 4% of vascular plant diversity (Mehltreter, 2010); nonetheless, they provide important ecological services (Sharpe et al., 2010), and comprise a substantial portion of commercial ornamental plant production as well as horticultural economic development (Hoshizaki and Moran, 2001; Singh and Johari, 2018). Their evolutionary and paleobiological history is extensive beginning in the Middle Devonian, approximately 390 million years ago (mya) with expanded diversity during the Cenozoic (65 mya), when angiosperms were becoming more dominant (Schneider et al., 2004;  Schuettpelz  and  Pryer,  2009). Ferns  were dominant flora in the Carboniferous, later losing space to gymnosperms and angiosperms. Increasing forests provided suitable protective, shady environments where ferns flourished on the forest floor or as epiphytes on tree trunks and limbs (Watkins and Cardelús, 2012). Subsequently, over geological time spans, through adaptation and evolutionary radiation (Sessa, 2018), ferns proliferated to occupy a wide diversity of terrestrial environments; ranging from swamps and coastal locations to more open grasslands, mountain terrains, drylands and deserts. Consequently, their biodiversity and life histories (Figure 1) have commensurately expanded to include a rich panoply of different life forms, physiological adaptive strategies, and wide global habitats.
 
 
A brief comment about terminology: in prior publications, the leafy photosynthetic portion of the fern (including the stipe) was referred to as ‘fronds’ and this is still appropriate; but increasingly the term used is ‘leaves’ as applied to other vascular plants. Therefore hereafter, the term ‘leaves’ will be used largely, except where frond may be more appropriate.
 
In comparison to seed-bearing plants, spore-bearing ferns have a characteristic life cycle with alternating generations of a diploid (2N) spore-bearing sporophyte and a free-living, haploid (1N) gametophyte (prothallus) that produces egg and sperm. After fertilization of the egg producing a zygote, it gives rise to a new sporophyte generation (Figure 1). The dominant phase of the fern life cycle is the sporophyte that produces haploid spores in sporangia, typically occurring on the lower surface of fern leaves (Figure 2a, b), or in separate spikes (sporangiophores) with more specialized, usually reduced and modified fertile sporophylls. The cinnamon fern, Osmundastrum cinnamomeum (L.) C. Presl, observable in the natural environment and commonly grown in gardens, is an example of such a dimorphic fern. A crown of green, pinnate leaves surrounds central sporangiophores with brown, reduced fertile leaves bearing sporangia and spores.
 
The photosynthetic gametophyte (prothallus) that develops from the fern spore is typically thin (one-celled thick) and lacks extensive surface protective covering. Therefore, it is particularly subjected to environmental pressures. Consequently, it can be a precarious link in the alternation of generations in the fern life cycle; because its failure would interdict development of the sporophyte stage, especially if environmental conditions are challenging. Although many species have a chordate (heart-shaped) prothallus as shown in Figure 1, it is important to recognize that in other species the prothallus is strap-shaped, ribbon-like, or even filamentous at maturity, especially varying with the habitat where the species have become adapted.
 
The number of spores released by the sporophyte is usually copious, and most spores are distributed in near vicinity to the mother plant (sporophyte). Consequently, a relatively dense population of gametophytes may develop in surrounding suitable locations, thus increasing the probability of successful completion of the life cycle. However, the density of gametophytes may lead to competition and only a portion of the more vigorous gametophytes survive. Moreover, there is increasing evidence that the powdery spores can be carried by wind to distant locations (including distant oceanic islands); thus, increasing dispersion of the species, assuming the new location is suitable for gametophyte survival (Sharpe et al., 2010). The evolution of very light-weight spores has promoted wide-spread dispersion of some fern species and contributed to their establishment broadly across continents and islands of the oceans in highly diverse geographic locales.  Furthermore, the capacity for some gametophytes to self-fertilize also ensures that even a single gametophyte from a spore carried to distant lands may successfully give rise to a new generation at these distant locations. Depending on the genetic composition of the individual and potential for adaptation in the new locale, a new population may thrive and in some cases through evolution become established as endemics in that geographic locale.
 
 
The biogeography and systematics of ferns have a relatively richer, and historically longer, record of research than physiological ecology that largely expanded in quantity and sophistication during the twentieth and twenty-first centuries. There appears to be few recent reviews of fern physiological ecology addressing the particular topics treated here, although there are other substantial sources on fern ecology, more broadly (Mehltreter et al., 2010). Some representative examples of published research on fern physiological ecology are reviewed here. Ferns have diversified to occupy widely different ecological niches; including, aquatic,  terrestrial,  epiphytic  (growing  on  other  plants) and epilithic (growing near to or upon rocks) species occurring in diverse geographical and climatic locales. Thus, there is a rich source of potential evidence for fern physiological ecology research. A more general treatment of fern research and natural history is provided by Fernández (2018) and Moran (2004). For information on horticultural and cultivation aspects consider Jones (1987). A comprehensive review of gametophyte developmental biology is given by Raghavan (2005). Each of the particular life forms of ferns has evolved specialized morphological and physiological adaptations to better survive in their particular habitat. With increasing concerns about the possible aversive effects of climate change for life on Earth, there is also particular interest in the likely challenges for survival of many fern species that have become adapted to particular environmental niches (Anderson, 2018). Consequently, there are enhanced efforts to better understand the physiological ecology of ferns to more fully document and monitor the distribution and survival of biodiverse fern populations, and the biological communities where they occur. 
 
This review of current research on fern physiological ecology focuses on terrestrial and epiphytic ferns, with particular emphasis on examples of biodiverse groups of ferns that have been published in recent decades. During the literature search, an online survey using the keywords ‘Fern ecophysiology’ was made for each year from present (2021) back to 1900. To delimit the categories of articles reviewed, three main topics were identified: 1) Water relations and desiccation tolerance, 2) Light and photosynthesis, 3) Temperature and physiological responses, and finally 4) Issues of conservation. These were chosen as particularly relevant aspects of physiological ecology for ferns, and consistent with the intent of a review article focusing on diverse groups of ferns in broad global environments. Additionally, articles were selected that were representative of the habitat (terrestrial or epiphytic) and addressed life stages (spores and germination, gametophyte stage, and sporophyte stage). In so far as possible, representative articles were chosen that included varied global locations (geographically and environmentally) that may be of interest to an international audience of readers.


 WATER RELATIONS AND DESICCATION TOLERANCE

In addition to appropriate illumination for photosynthesis, adequate moisture is one of the most important environmental variables controlling the distribution and abundance of terrestrial and epiphytic ferns. Some species (Acrostichum aureum L., known as golden leather fern or swamp fern) are found in freshwater and mangrove swamps or other wet locations. By contrast ‘Cheilanthoid ferns,’ e.g., Cheilanthes spp., Myriopteris spp. (separated from  Cheilanthes, sensu stricto), and Asplenium ceterach L., are adapted to dryland and desert locales. For example, xerophytic Myriopteris lanosa (Michx.) Grusz & Windham (hairy lip fern) has very small leaves, tightly curled (approximating a ball), and is covered with a dense, lanose (wooly) surface coat – particularly adapted to reduce water loss by leaf transpiration. A substantial amount of ecological and laboratory experimental research has focused on water relations and desiccation tolerance of ferns. A useful review of the topic for ‘resurrection plants’ in general is presented by Deeba and Pandey (2017); and more specifically for resurrection ferns by Hietz (2010), Kavitha et al. (2017), and López-Poso et al. (2018). Relevant published research topics are summarized here for terrestrial and epiphytic ferns. Subtopics within each section address environmental and physiological factors or, where relevant, cellular and biochemical adaptations. In general, review of research related to the gametophyte is presented before addressing research with sporophytes.
 
Terrestrial ferns
 
Gametophyte environmental physiological responses  
 
Because of the delicate and potentially fragile state of gametophytes in the fern life cycle, research attention has been given to their tolerance for desiccation stress and adaptive response to water stressful environments, including adaptive variations in tropical species (Watkins et al., 2007) and the role of competition and climate change with particular to the rare fern Asplenium scolopendrium var. americanum (Fernald) Reichst., Rasbach & Viane published by Testo and Watkins (2013). Compared to six other species, gametophytes of A. scolopendrium  var.  americanum had the lowest rates of germination and sporophyte production and exhibited the greatest sensitivity to interspeci?c competition, temperature increases, and desiccation. Given these potentially precarious characteristics, possibly threatening its survival, greater attention to conservation of this species is warranted. Particular attention has been given to gametophyte desiccation tolerance by other rare or endangered species including Camptosorus rhizophyllus (L.) Link, typically growing with mosses and lichens on the shaded surface of dry limestone slabs and on detached limestone slabs in open ravines and torrent beds – particularly challenging environments (Pickett, 1913).
 
The peculiar American species Vittaria appalachiana Farrar and Mickel, growing densely on shaded rock surfaces, exists only in the gametophyte form. It is sometimes known as a ‘gameto-only’ fern, lacking a sporophyte stage in the life cycle and reproducing asexually by photosynthetic propagules (gemmae) produced by the gametophyte. Chambers et al. (2017) report that this unique species, while limited to local sites, shows considerable adaptive variability to desiccation; indicating that it may have greater survival potential than suggested by its limited geographic range. Sato (1992) studied the effects of seasonal variables, especially spring desiccation, on survival and size of gametophytes of Athryium brevifrons Nakai ex Kitag. in a transplant garden of Sapporo Japan. Gametophytes of all sizes decreased with decreasing soil moisture (r = 0.878, p < 0.01). In a similar study in the natural environment, the carbohydrate, lipid content and biomass of the gametophyte stage of the xerophytic hairy lip fern, Myriopteris (Cheilanthes) lanosa, collected from a sandstone bluff in midwestern U.S.A., was reported by Crow and Mack (2011). They found that each gametophyte increased in percent of total biomass (w/w) throughout development; concomitant with ability to better manage water balance during maturation.
 
Moreover, young gametophytes, with high carbohydrate and low lipid content, were located on substrates with a potential for small but continuous water source.        
 
Sporophyte environmental physiological responses.
 
Extensive research has been given to the sporophyte stage of the fern life cycle. Mesophytic ferns, growing in environments with ample precipitation, have been investigated to determine effects of intermittent desiccation events. Liao et al. (2008) examined the effects of variation in soil moisture (80, 60, and 40%) on adaptive characteristics of Adiantum reniforme var. sinensis Y.X. Lin, an endangered species endemic to the Three Gorges Region in China. They found that drought stress decreased leaf growth and photosynthetic capacity, and hence reduced total mass, specific leaf area (SLA) and leaf area ratio (LAR). However, there was an increase in dry matter allocation into the root fraction with decreasing soil moisture. Leaf relative water content (RWC) decreased marginally as soil water was depleted. The authors concluded that these results might be the result of a physiological balance between the demand for water by the leaves and the water uptake from soil by the roots.
 
During the period of 2012 to 2016, California incurred severe seasonal drought. Holmlund et al. (2016) examined tissue-water relations among eight ferns in the Santa Monica Mountains to examine differential mechanisms of drought survival. They reported that five chaparral species had a wider range of tolerance (e.g., water potentials, root depths and leaf phenological traits) than two evergreen species. The evergreen species, nonetheless, were especially diverse, exhibiting wide variations in seasonal tissue water potentials. With respect to conservation perspectives, the authors predict differential survival among fern species as future drought events in California intensify, with desiccation-tolerant resurrection ferns being the most resistant and possibly leading to a reduction in diversity if less tolerant species succumb. Further research by Holmlund et al. (2020) with two species of ‘resurrection ferns’ documented that sufficient moisture is essential during desiccation recovery to ensure sufficient positive root pressure to drive whole-plant desiccation recovery; that is, hydration of the dried leaves alone was insufficient. Changing climate patterns that include only sporadic and limited precipitation may not be adequate to provide sufficient amount and duration of moisture at the roots to fully activate root pressure needed to revive desiccation-tolerant ferns, thus leading to their demise and decreasing biodiversity of the relatively sparse vegetation in these dryland habitats.
 
A rather interesting adaptive response to seasonal desiccation was reported by Farrant et al. (2009) for the unusual   fern,   Mohria    caffrorum   (L.)  Desv., a South African endemic, growing on Table Mountain in Western Cape, South Africa. Samples were collected during the rainy and dry seasons to determine differential responses to the changing seasonal available precipitation. Remarkably, the physiological response varies seasonally; that is, this species is desiccation tolerant during the dry season and becomes desiccation-sensitive in the rainy season, showing a differential physiological adaptive mechanism activated by changing seasonal patterns of precipitation. Its threat status is categorized as ‘Least Concern’ though it is growing in this rather formidable environment, and may be attributed partially to its supple capacity to alter its physiological demands to complement the changing seasonal climate.
 
The desiccation tolerance of ten British fern species was studied by Proctor (2009) who examined the response of excised leaves to drying. Asplenium ruta-muraria Michx., A. septentrionale (L.) Hoffm., A. trichomanes (L.), A. ceterach, Polypodium cambricum (L.), and P. interjectum Shivas withstood drying for periods of a week or more to a RWC of ca. 4-7%, suggesting that they are much more tolerant to drying than most vascular-plant tissue that is irretrievably damaged at an RWC of ca. 30%.  Moreover, small Asplenium species and A. ceterach dried quickly (half-drying times a few hours), suggesting little stomatal control over drying. The much slower drying of the Polypodium species may indicate that their stomata close under water stress. Similarly, Kessler and Siorak (2007) conducted desiccation and rehydration experiments on detached leaves of 37 fern species and six lycophytes obtained from the Botanical Garden at University of Göttingen, Germany, including a range of adaptive life forms (that is, mesomorphic, poikilohydric,  xeromorphic and drought-deciduous). They reported the studied species exhibited wide variation in all measured parameters. Desiccation resistance (percentage of water loss before lethal effect) varied from 30% in the mesophytic species Asplenium nannii Hook. (L) to 99% in  poikilohydric Cheilanthes myriophylla Desv. (L) and intermediate state Adiantum macrophyllum Sw. (L). On the other hand, the desiccation resistance of a clearly mesophytic species, Adiantum trapeziforme  L. (L), was 51%.
 
Further studies by Banupriya et al. (2020) were done on the physiology of a desiccation tolerant species (Adiantum raddianum C. Presl) occurring widely in the Devarayanadurga forest region of Karnataka, India. They reported that during desiccation of detached leaves from healthy plants, the RWC decreased to as low as 16% after four hours with intense inward curling. Upon rehydration, the RWC of the leaves regained 85% of the initial water content within four hours; and approximated the original morphology. Physiological activities of antioxidant enzymes and molecular constituents (superoxide dismutase, peroxidase, catalase, glutathione reductase, lipid peroxidation, and proline) increased during desiccation; however, sucrose and starch content showed differential response. Additional evidence of desiccation-protective organic constituents was reported by de Moraes et al. (2014) who analyzed the sugar content of ferns, with comparison to a lycophyte (club moss), growing in extreme rocky outcrops on the southeastern coast of Brazil. The ferns largely had glucose, fructose, and sucrose as protective osmotic compounds, and the lycophyte had glucose and trehalose. Among the ferns, the total sugar content ranged from 81.31 to 200.92 (mg g-1 DW) and the RWC ranged from 80 to 88.3%.
 
In addition to ferns typically found in mesophytic habitats, xerophytic ferns have been studied extensively to examine their desiccation tolerance and adaptive mechanisms. Hevly (1963) examined adaptations of cheilanthoid ferns in desert environments, largely in Arizona, and summarized the morphological and physiological properties that account for their success in extremely dry environments. These adaptive properties included leaf size in microphyllous species, surface cuticles and indument with wooly coating, osmotic properties, and heat tolerance mechanisms. Harten and Eickmeier (1987) examined the comparative desiccation tolerance of two desert ferns, Cheilanthes tomentosa Link and Notholaena sinuata var. cochisensis (Goodd.) Weath., growing in Big Bend National Park, Texas. The high-elevation species C. tomentosa was most sensitive to extended desiccation and had the slowest photosynthetic recovery and the greatest membrane damage; whereas, the mid-elevation species N. sinuata was consistently intermediate in response. They also compared the results of these two ferns to the low elevation lycophyte, Selaginella lepidophylla (Hooke. & Grev.), that was least sensitive to extended desiccation and had the fastest photosynthetic recovery with least membrane damage.
 
With increasing evidence that some ferns growing at low elevations in coastal regions may be subjected to hypersaline conditions due to ocean flooding, interest has turned to possible effects of salinity on cultivated and naturally occurring ferns. Salanchna and Piechocki (2021) examined the salinity tolerance of four hardy ferns in the genus Dryopteris; namely, D. affinis (Lowe) Fraser-Jenk., D. atrata (Wall. ex Kunze) Ching, D. filix-mas L., and one cultivar D. filix-mas cv. “Linearis-Polydactylon”. All were grown under different light conditions. The species that were treated with 100 mM NaCl (ca. 5.9%) exhibited reduced height, less leaf greenness index and lower fresh weight of the above-ground part. Salinity caused leaf damage in D. affinis and D. atrata, which was not observed in the other two species. The effect of NaCl depended on light treatments and individual species. Among the investigated genotypes, D. filix-mas seemed the most tolerant, and D. affinis and D. atrata the least tolerant to salinity and light stress. Additional aspects of light-related adaptations in terrestrial ferns are presented in a subsequent section on Light and Photosynthesis.
 
Epiphytic ferns
 
Epiphytes, growing on other plants (particularly tree trunks and branches) are vulnerable to desiccation stress because they are particularly exposed to atmospheric and meteorological variables. In regions with rather constant climate (e.g., tropical and some subtropical locales) with sufficient humidity, moderate temperatures and more predictable precipitation, epiphytic species may thrive without specialized adaptations to avoid aversive environmental conditions. In environments with varying climate, especially unpredictable precipitation patterns, epiphytic ferns typically have adaptations to endure periods of desiccation. Consequently, a broad range of adaptive mechanisms have evolved within many taxa of epiphytic ferns to enhance desiccation tolerance. In some cases they are deciduous, shedding leaves, to avoid transpiration and water loss; or in other cases they are desiccation tolerant and endure the dry period in a dormant state (‘resurrection ferns’).
 
A comment about taxonomic nomenclature to be used in the next section: presently the accepted taxonomic name for the common polypody fern is Pleopeltis polypodioides (L.) E.G. Andrews and Windham (previously, Polypodium polypodiodes (L.) Watt.). Therefore, throughout this treatment, the currently accepted name will be used and abbreviated as P. polypodioides.
 
Gametophyte environmental and physiological responses
 
In general, studies of gametophyte physiological ecology are fewer than those of the sporophytes; and for epiphyte species, there appears to be proportionately fewer than for studies of terrestrial species’ gametophytes.
 
However, Watkins et al. (2007) examined the photosynthetic response of laboratory cultured gametophytes of two epiphytic species, Phlebodium pseudoaureum and Microgramma reptans (Cav.) A.R. Sm., in comparison to 10 terrestrial species during desiccation. These tropical species were collected from La Selva Biological Station in the Atlantic lowlands of north-eastern Costa Rica (37-100 m above sea level). The rate of drying varied signi?cantly among species, with the fastest dry down in the terrestrial Thelypteris curta (Christ) C.F. Reed, and slowest rates in two species – the terrestrial Cyclopeltis semicordata (Sw.) J. Sm. and the epiphyte Microgramma reptans (Cav.) A.R. Sm. Depression in photochemical ef?ciency (Fv/Fm), as measured by photosynthetic fluorescence, in desiccated gametophytes was nonlinear and varied among species. During recovery from desiccation, Phlebodium pseudoaureum, compared to the other species, exhibited relatively less depression in Fv/Fm; indicating greater resistance to photoinhibition. Moreover, Microgramma reptans exhibited remarkable Fv/Fm stability – no signi?cant Fv/Fm depression occurred at any of the desiccation intensities.
 
Compared to terrestrial fern species, typically found on the forest floor, the desiccation stress incurred among epiphytes in the canopy may have led to evolutionary adaptations for greater desiccation tolerance. This is further exemplified in a study by Ong and Ng (1998) who found that gametophytes of the epiphytic fern, Pyrrosia piloselloides (L.) M.G. Price, typically found on trunks and branches of wayside trees in Singapore, were able to tolerate 50 days of drought (though with some cell death), and after rehydration were capable of partial recovery forming new offspring gametophytes. However, gametophytes desiccated for only 1–21 days recovered completely upon rehydration, without the death of any cells, and continued growth and maturation.
 
Further studies on the influence of simulated drought on the functioning of the photosynthetic apparatus in gametophytes of Platycerium bifurcatum (Cav.) C. Chr. were published by Rut et al. (2003) who reported the presence of crassulacean acid metabolism (CAM) (that is, non-photosynthetic night fixation of CO2) in this epiphytic fern. CAM was found in the sterile cover leaves, but not in the fertile spore-producing leaves.
 
The photosynthetic efficiency of the gametophyte phase in the fern life cycle may be critical for subsequent sporophyte development. There is evidence that the gametophyte provides photosynthetic nourishment of the young sporophyte during its early stages of development before the one-leaf stage (Sakamaki and Ino, 1999). Consequently, desiccation stress at the gametophyte stage may incur decreases in its photosynthetic efficiency and indirectly lead to less successful development of the young sporophyte.
 
Sporophyte environmental and physiological responses in epiphytic ferns
 
Changes in water content of epiphytic ferns are one of the most significant physiological indicators of the desiccation status of poikilohydric (resurrection) species. Potts and Penfound (1948) measured the water content of P. polypodioides and that of the tree bark where they were growing, and found that there is close correspondence. In the active state, the ferns had mean water content (percentage of oven-dry weight) of 207 ± 32 (bark = 52 ± 16), and when desiccated and dormant the fern water content was 86 ± 13 (bark = 18 ± 4). At varying dates, they measured the water content of the ferns and the relative humidity (RH) and also found a strong correspondence varying from 8% fern water content at RH = 65%, but a much higher 23% water content at RH 94%. They also measured the change in water content of P. polypodioides in laboratory experiments under controlled drying conditions and reported that over 12 hours, the amount of water lost varied from 19% during the first hour to 1% by the twelfth hour, an average change of approximately 1.6% loss per hour.
 
Subsequent studies by Voytena et al. (2015) reported that sporophytes of Pleopeltis pleopeltifolia (Raddi) Alston (commonly found in Brazil) subjected to desiccation for 0, 5, 10 and 15 days showed a sharp decline in water content when non-irrigated, reaching a final value of 9.6% after 15 days. As is typical, the ferns exhibited considerable wilting and frond rolling. A substantial increase was noted in sugar content of the fronds during desiccation – a possible osmotic adjustment and vitrification to protect tissues. During the five initial days of desiccation, the chlorophyll and carotenoid contents decreased abruptly. However, after 1 day of rehydration they partly recovered including resumption of photosynthesis.
 
The pliability of leaf cell walls during desiccation and folding of leaves was documented in P. polypodioides by Layton et al. (2010) who reported that a rise in the content of a putative 31-kDa dehydrin protein, present only during dehydration, may promote the flexibility and folding of the dehydrated leaves. They concluded that the ability to avoid cell wall damage in some desiccation-tolerant species may be partially attributed to cell wall localization of dehydrins enabling a pliable, reversible, large cell-wall deformation. This was further developed by Helseth and Fischer (2005) who derived a mathematical model to explain the physical mechanisms of changes in the pliable structure of the plant tissue during rehydration.
 
Further elucidation of the cellular mechanisms of dehydration and rehydration in P. polypodioides were reported by John (2017) using transcriptomic analysis of gene-activated protein synthesis. She found that Pleopeltis is prepared for desiccation at an early stage of dehydration by: a) accumulating various metabolites, b) reducing energy consuming metabolic activities, and c) subsequently catabolizing some metabolites after resumption of hydration. Additionally, many of the desiccation-induced gene transcripts are constitutively (continuously) expressed under hydrated conditions, which creates a constant supply of some essential molecules that allows the plant to adjust rapidly to desiccation.
 
Relatively less attention has been given to temperate epiphytic ferns. However, Klinghardt and Zotz (2021) analyzed the abundance and seasonal growth of polypod epiphytic ferns at three sites along a rainfall gradient in Western Europe; and reported, surprisingly, that seasonal frond productivity appeared to be unaffected by the amount of annual rainfall and average temperatures. Although it seems likely that these factors do play a role during gametophyte establishment.  However, they reported   that  the  abundance of epiphytic polypod ferns strongly decreased from the wetter end of the rainfall gradient in Ireland towards the drier end in Germany; although, frond turnover was equally high at all study sites during summer months, and equally low during winter.
 
Considerable attention has been given to the so-called ‘filmy ferns’ (Hymenophyllaceae), sometimes with leaves only one-cell thick. Although they are constitutively delicate and typically grow in humid environments, some species of filmy ferns are desiccation tolerant. Other species of ferns growing in moist, shady terrestrial environments also have leaf lamina one to two cells thick; e.g., Adiantum capillus-veneris (L.) Hook. However, many of these are less desiccation tolerant. Ostria-Gallardo et al. (2020) applied molecular genetic analysis of gene networks to analyze desiccation tolerance mechanisms for two Hymenophyllum species (H. caudiculatum Mart. and H. dentatum Cav.) differing in their location within a forest canopy and experimentally studied at three different degrees of dehydration. While there were only a few distinctive genes activated comparatively in the two species, H. caudiculatum had ca. twice the number of activated genes than H. dentatum; and a higher proportion of increased-and-decreased abundance of genes occurred during dehydration. In contrast, the abundance of genes in H. dentatum decreased significantly when transitioning from dehydration to rehydration. Moreover, H. caudiculatum enhanced osmotic responses and phenylpropanoid related pathways; whereas, H. dentatum enhanced its defense system responses and protection against high light stress. Overall, these results provide evidence of the relationship between the species-specific response and the microhabitats that these ferns occupy in nature.
 
The correlation between water relations and within canopy distribution of epiphytic ferns in a Mexican cloud forest was examined by Hietz and Briones (1998). They reported that the filmy fern Trichomanes bucinatum Mickel & Beitel became desiccated completely within hours in moderately dry air and was confined to the stem bases; while Asplenium cuspidatum Lam., with no evident adaptations to cope with drought, grew in the second most shaded zone within the tree crowns. Likewise, Nitta et al. (2020) found a similar functional and habitat-specific diversity of a broad group of epiphytic ferns (including filmy ferns) in community analyses along mountain elevational gradients on the island of Moorea, French Polynesia.
 
Further findings include a variety of experimental and natural environmental studies as follows: a)  Bravo et al. (2016) documented reversible cellular changes during desiccation and recovery of Hymenophyllum collected in the southern temperate rain forest of Chile; b) Flores-Bavestrello et al. (2016) made a comparative analysis of photosynthetic apparatus and responses to dehydration by Hymenophyllum dentatum and Hymenoglossum cruentum (Cav.) C. Presl  isolated  from  different  vertical locations on a host tree in Chile; and c) Proctor (2012)  published evidence of coordinated mechanisms of dehydration and photosynthetic light responses in filmy fern samples collected in New Zealand compared to those collected in Trinidad and Venezuela.


 LIGHT AND PHOTOSYNTHESIS

Although available water is a major factor in fern physiological ecology, the quality and intensity of illumination is particularly important in determining fern distribution and productivity. As in previous sections, a review of research on terrestrial taxa is presented first followed by epiphytes. There is a substantial volume of published research on the topic of light and physiological adaptations of ferns. Examples of research were chosen that particularly highlight diverse geographic locales and climatic regions, globally.
 
Terrestrial ferns
 
Gametophyte environmental physiological responses
 
Spore germination initiates the gametophyte phase of the fern life cycle and substantial research on the effects of light on spore germination has been published, including: a) light induced spore germination (Life, 1907;  Reynolds and Raghavan, 1982); b) spectral quality of light and the role of the light signaling molecule, phytochrome (Raghavan, 1971; Furuya et al., 1982; Zilberstein et al., 1984); and c) the interactions of light and temperature on spore germination (Pareek et al., 2005; Pérez-García et al., 2007). Moreover, Sugai et al. (1987) found that spores of species that normally require light to germinate can be activated by application of gibberellic acid or its methyl esters. Furthermore, complex effects are produced by adding abscisic acid (ABA) in interaction with auxin (indoleacetic acid, IAA) and kinetin (Chia and Raghavan, 1982). ABA can be inhibitory of full germination, leading to incomplete growth of the initial protonema. However, both IAA and kinetin, which alone do not promote full germination, reverse to some extent the inhibitory effect of ABA.
 
The importance of red light induced growth of spores is significant from a physiological ecology perspective, because overlying, shading plants absorb red light and thus may suppress underlying fern spore germination until there is sufficient full illumination to support the photosynthetic requirements of the gametophyte prothallus. It is worthy to note that ABA can take many roles, physiologically, but particularly as reported by Chia and Raghavan (1982) in the prior case, it may accumulate in spores under adverse conditions for germination, and thus delay premature germination in less than desirable environmental circumstances.
 
However, it is important that ABA is under regulatory control by other phytohormones (e.g., IAA and kinetins) to ensure that inhibition is released when environmental conditions are favorable for spore germination and survival of the gametophyte.
 
Sporophyte environmental physiological responses to light
 
There is a substantial literature base on this topic, and only some representative research is reviewed beginning with broad environmental factors and progressing to more detailed physiological response patterns. A rather comprehensive review of the effects of light on fern morphogenesis is presented by Kanegae and Wada (2006).
 
The effects of light intensity, temperature and nutrients on vernal frond emergence and biomass production in the temperate fern Matteuccia struthiopteris (L.) Tod. was reported by Prange (1985) who found that photosynthetic intensity, water availability, and nutrients affect frond productivity, but water availability appeared to be most critical. Maximum net photosynthesis rates of approximately 220 µg CO2 m-2 s-1 were reached at low light intensities of 300 to 600 µmol m-2 s-1. Jordan and Kuehnert (1975), studying Osmundastrum cinnamomea reported that abrupt increases in light (e.g., through local deforestation) increased leaf primordial initiation to some degree, but there was greater primordial development in leaf bud primordia that were set in prior years, suggesting a carry-over effect from one year to the next.
 
In a further study of temperate ferns during the spring season, Tessier (2001) assessed the adaptive value of maintaining photosynthetic (wintergreen) fronds during winter in Dryopteris  intermedia (Muhl.) A. Gray that were found growing in the Catskill Mountains of New York. He studied the photosynthetic productivity during April to May, particularly to explore the potential photosynthetic and retranslocational bene?ts of wintergreen fronds in sustaining the life of the fern. Net photosynthesis occurred throughout the study indicating a potential for movement of ?xed carbon from winter-green fronds to other parts of the plant, though in this study the net photosynthesis was higher in April, immediately after snow melt, compared to May.
 
Saldana et al. (2007) examined the effects of varying light environments on the ecophysiological traits of Blechnum chilense (Kaulf.) Mett. occurring widely in Chilean temperate rainforests. They particularly studied contrasts of plants growing in gaps versus those in forest understories. In gaps with higher light intensity, the survival of B. chilense was positively correlated with water use efficiency (WUE) and negatively correlated with leaf size. In contrast, survival in shaded understories was positively correlated with leaf size. In understories, ferns of lower respiration rate and greater leaf size showed greater fecundity. Thus, whereas control of water loss was optimized in gaps, light capture and net carbon balance were optimized in shaded understories.
 
Similarly, Zhu et al. (2016) examined the response of 16 fern species distributed between open gaps and shaded understories in sub-tropical forests of China. They found that a leaf cost-bene?t analysis contributes to understanding the distribution pattern of ferns in contrasting light habitats. Ferns in the open habitat, employing a quick-return strategy, can pre-empt resources and rapidly grow in the high-resource environment of the open habitats; while a slow-return strategy of ferns in understory locations allows their persistence in the shaded understory of well-established canopies of old-growth forests.
 
Sun flecks, caused by flutter of canopy leaves and swaying branches, produce intermittent and transient peaks in light intensity in the understory habitats. Ferns growing on the forest floor produce concomitant fluctuations in productivity, that can be very rapid, as exemplified by the response of Polypodium virginianum L. ferns growing on cliff edges of the Niagra Escarpment, Canada (Gildner and Larson, 1992a). Further seasonal studies of P. virginianum at the Niagra site (Gildner and Larson, 1992b) showed that carbon gain in the spring greatly exceeded that of any other season. However, there was little change in the photosynthetic response to light on a seasonal basis, even though plants were exposed to highly variable and highly limited light most of the time.
 
Nishida and Hanba (2017) examined the photosynthetic response to drought stress among four temperate fern species from different habitats by withholding irrigation in laboratory experiments.  Among other outcomes, they found that Lepisorus thunbergianus (Kaulf.) Ching (an epiphyte) had low stomatal density and showed high water-use efficiency (WUE) retaining photosynthetic activity with low relative frond water content under drought stress. This indicated they were highly adapted to drought. In contrast, low WUE with low light-saturated photosynthetic rate in Adiantum pedatum L. (growing in terrestrial, shady environments) was associated with much lower photosynthesis than in the other species under drought stress, suggesting lower adaptation to drought-prone habitats.
 
Epiphytic ferns
 
This subsection focuses largely on the sporophyte phase of the life cycle, where a substantial amount of research has been done. Photosynthesis of epiphytic ferns and their within-canopy distribution in a Mexican cloud forest revealed that there was a correlation between distribution of habitats within the canopy, and physiological traits (Hietz and Briones, 2001). Maximum rates of CO­2 uptake (Amax) and photon flux densities at light compensation points (LCP) were  in  the  range  of  shade  plants (Amax =0.6 ± 5.2 mmol CO2 m-2 s-1; LCP = 4 ± 6.5 mmol m-2 s-1), but their saturation light photon intensities (270 ± 550 µmol m-2 s-1) were more typical for sun plants. Amax and nitrogen content per unit dry weight were correlated with the distribution of the species within the canopy; but LCP, apparent quantum yield and dark respiration were not.  
 
Quinnell et al. (2017) examined the photosynthetic rate of Davallia angustata (Wall. ex Hook. & Grev.), an epiphyte on tree trunks and palm trees in south-east Asia. In this case it is not a crassulacean acid metabolic (CAM) plant as are some epiphyte fern species. Under well-watered conditions, D. angustata had a diurnal cycle of photosynthesis with maxima in mid-morning ~0900 hours (solar time). Under optimum irradiance ~45% of full sunlight (qualifying it as a ‘sun plant’), the maximum photosynthetic electron transport rate (ETRmax) was 77.77 ± 3.42 µmol e- m-2 s-1; or, expressed on a Chl a basis = 350 ± 36.0 µmol g-1 (Chl a ) s-1.
 
Given the recurrence of desiccation stress in many epiphytic ferns, some have adapted stress tolerance by evolving CAM photosynthetic capacity, but overall for fewer species compared to many other vascular epiphytes. Winter et al. (1986) studied CAM in a tropical epiphytic fern, Pyrrosia longifolia (Burm. f.), in a fully sun-exposed and in a very shaded site in Northern Queensland, Australia. Maximum rates of net CO­2 uptake and the nocturnal increase in titratable acidity (attributable to dark fixation of the CO2 into organic acids) were lower in shade than in sun leaves.  Based on carbon stable isotopic data, d13C values of sun and shade leaves were not significantly different, and ranged between -14 and -15%o (within the range of CAM plants) suggesting that, in the long term, carbon gain was mainly via CO­­2 dark fixation by crassulacean acid metabolism. Sun leaves had a higher light compensation point of photosynthesis than shade leaves, but the same quantum yield.
 
Additional research on CAM in P. longifolia and Drymoglossum piloselloides (L.) Presl collected in Singapore (Ong et al., 1986), under controlled environmental conditions in laboratory culture chambers, showed that CO­2 exchange under water stress in Pyrrosia was less than in Drymoglossum; showing that Pyrrosia was more susceptible to water stress. During water stress, there was a continuous decrease of CO­2 uptake, both in light and darkness. Moreover, notably, in both plant species a residual diurnal acid rhythm remained, even if the drought stress caused stomatal closure and the nocturnal CO2 uptake from the environment dropped to zero. This indicated ‘CAM idling,’ where CAM depended entirely on recycling of respiratory CO2; that is, from respiration of existing carbon already fixed into organic acids during the night.
 
TEMPERATURE AND PHYSIOLOGICAL RESPONSES
 
Based on a global perspective, a published meta-analysis of the relative effects of temperature versus precipitation on plant traits for a broad range of plant species worldwide has shown that temperature is the better predictor of plant traits than precipitation (Moles et al., 2014). However, as reported in the review of research above; at the local level within a reasonably well-defined climatic regime, the amount and pattern of precipitation is very significant for many fern species, particularly for epiphytes (Zotz and Hietz, 2001). Nonetheless, recognizing that temperature is a major environmental variable, it is remarkable that relatively little research has been done on the role of temperature in fern physiological ecology (Hietz, 2010; Anderson, 2018). Some illustrative studies are reviewed to provide information on the range of topics that have been published.  Given the relatively limited coverage of temperature in the literature, this subsection is not subdivided by subtopics such as ‘Terrestrial ferns’ and ‘Epiphytic ferns’ as was, the case in preceding sections of this paper.
 
Epiphytic ferns have become adapted to dwelling on a relatively wide variety of tree species in subtropical and temperate mountainous regions, adapting to varied temperature and climate regimes, including in the Himalayas (Bhakuni et al., 2021; Joshi et al., 2020). In general, montane regions are likely hotspots for fern diversity (Suissa et al., 2021). Warne and Lloyd (1980) studied the role of temperature in the germination of spores and gametophyte development in some temperate and tropical ferns with the aim of understanding the correlation of temperature responses to the habitat of the ferns. They concluded, based on laboratory-based temperature controlled experiments, that characteristics of spore germination and gametophytic responses to temperature correlate with the natural distributions and life cycles of the studied species. The tropical taxa (Ceratopteris spp.) had optimum development at higher temperatures than observed for the temperate taxa. For example, the pattern of growth response of gametophytes of the temperate fern Matteuccia struthiopteris correlates with the winter and early spring discharge of spores in this species. Moreover, Warne and Lloyd’s data suggest that a limiting factor controlling the southern distribution of this species may be the inability of its gametophytes to complete normal development in warmer climates.
 
Gildner and Larson (1992b) reported that temperature was a significant seasonal covariate in explaining the photosynthetic response of Polypodium virginianum to light intensity when growing in a forest floor location in Canada. Moreover, experiments conducted in the laboratory showed that the response of photosynthesis to temperature was broad. Ong et al. (1986), studying two obligate CAM metabolizing species (Pyrrosia longifolia and Drymoglossum piloselloides), reported that the effects of temperature on CO­­2 exchange were inverse compared to other CAM plants. That is, in both ferns, dark CO­­2 fixation increased when the night temperature was    increased,    and    decreased    with lower night temperatures. Increase in day temperature reduced CO­2 uptake during phase IV (CO2 uptake during the last part of the light period); and during the following night.
 
In Prange’s (1985) studies of the ostrich fern (Matteuccia struthiopteris) a minimum amount of cold exposure was required to break winter dormancy – that is, a base temperature above 5.8°C is required and may be as high as 20°C. After the ostrich fern received its chilling requirement, vegetative emergence did not occur until temperatures were at or above ca. 9.3°C. Stamps et al. (1994), using experimental temperature regimes, examined the effects of temperature on growth of Rumohra adiantiformis (G. Forst.) Ching, also known as the leather leaf fern. When leaves of the leather leaf fern  were produced under a high temperature regime (30°C day/ 25°C night), they grew faster and produced more sori earlier than those in a low-temperature regime (20°C day/ 15°C night). Transpiration and water-use efficiency (mass basis) at light saturation were similar for leaves from both temperature regimes.
 
Seasonal variations in temperature have a marked influence on fern phenology–the timing of leaf emergence and bioactivity. Lee et al. (2018) analyzed a phenological dataset of 225 fern species from around the world to illustrate the distribution of studies during the past half century into leaf and spore production seasonality and the correlation with climate factors. Seasonal patterns were found in most of the phenological phases, especially in temperate regions with cold winters. In tropical to subtropical regions, seasonal patterns vary, and the seasonality of growth and reproduction in ferns may correlate with temperature or precipitation (or both), depending on the habitat locations.
 
Temperate ferns are particularly prone to temperature stress during winter months. Fernández-Marín et al. (2021) assessed frond freezing tolerance and xylem anatomical traits in five wintergreen fern species. They report that only desiccation tolerant species that possessed a greater fraction of narrow tracheids (< 18 µm), compared to sensitive species, tolerated freezing. They concluded that adaptation for freezing tolerance is likely associated with desiccation tolerance through complementary xylem properties (which may prevent risk of irreversible cavitation) and effective photoprotection mechanisms.
 
Rapp and Silman (2014), working in a Peruvian Andean cloud forest, examined the response of Elaphoglossum and other vascular epiphytes growing on trees to changes in temperature after being collected at varying elevations (800 m to over 4000 m), and then after they were transplanted to locations at lower elevations along the eastern slope of the Andes. When vascular epiphytes, with ramet-producing rhizomes, were transplanted down slope from the highest elevation within the cloud forest, they had lower ramet recruitment.
 
Furthermore, the number of ramets declined when transplanted to the lowest elevation, suggesting that warmer temperatures, and lower cloud immersion, could cause community-level changes for species currently above the cloud base.


 CONSERVATION PERSPECTIVES

A general review of current perspectives on fern conservation is given by Mehltreter (2010), including aspects of Risk assessment, Ecological data required for risk assessment and Management strategies for fern conservation. More specific issues of fern conservation related to changing climates are considered by Anderson (2018) and Sharpe (2019). The broad biogeographic distribution and wide habitat diversity of ferns, accompanied by highly diverse taxa adapted to environments ranging from aquatic to dry lands and deserts, exemplifies the remarkable evolutionary radiation of species in this group of vascular plants (Kessler, 2010). Diverse taxa such as those adapted to aquatic, xerophytic, rocky, and dryland environments further exemplify fern exploitation of widely different habitats. The presence of a broad range of epiphytic species living on the branches and trunks of trees, spanning tropical to temperate locales, provides additional witness to their adaptive capacity. Nonetheless, as with other highly evolved vascular plants, many fern species have become specialized to thrive only within particular optimal conditions. Others are endemic to limited geographic regions and in some cases have environmental requirements peculiar to their geographic locale. While all of this diversification and specialized adaptation make ferns a very attractive group of vascular plants for horticultural uses and scientific research, escalating threats by human exploitation, increasing climate change due to anthropogenic sources, and massive destruction of natural habitats (such as burning, agricultural cultivation, logging and commercial development in otherwise pristine natural environments) threaten the survival of many fern species (Arcand and Ranker, 2013; Nowicki and Kowalska, 2018).
 
Desert and dryland species may be considered less threatened due to their robust adaptive response to a hostile environment. However, increasing encroachment of construction for commercial purposes, and land development for human dwelling, puts ferns under additional survival pressure. Furthermore, possible increasing temperatures, and changing precipitation patterns due to climate change, may exceed the resilience of some species. Logging and massive destruction of forested regions pose particular threats to ferns in the understory of trees, where they are adapted to the usually shady, sometimes humid, and typically more constant soil moisture of the forest floor. Epiphytic ferns are particularly threatened by logging that destroys vast swaths of the forests where the epiphytes inhabit the trunks and limbs of trees.  In other cases, tree thinning increases light intensity in remaining trees. This favors invasion of open niches by high-light adapted species that proliferate to the exclusion of other species, and contribute to reduction of epiphyte biodiversity. Moreover, potential major alterations in precipitation patterns due to global climate change may produce protracted dry periods that exceed the epiphytic ferns’ desiccation tolerances.
 
All of these potentially challenging scenarios, and many more documented in the literature, call to our attention how relatively little we know about the physiological ecology of ferns in broad and diverse habitats essential to estimating their risk status. Clearly, a more systematic research agenda is needed to categorize fern taxa into major groups that have particular environmental requirements; and better document their habitats, survival capacity and stress limitations (Anderson, 2018). For example, tree ferns (among other exotic fern species) are impressive plants and important members of plant communities, especially in tropical and sub-tropical environments; but increasing evidence suggests that their survival in some global regions is under threat and additional research and conservation measures are needed (Ramírez-Barahona et al., 2011).
 
It is difficult to judge how effectively ex situ cultivation and preservation in botanical gardens and designated natural preserves can contribute to conservation of threatened or vanishing species. Nonetheless, horticultural and research institutions committed to cultivation and preservation of fern diversity may be one of our best solutions to saving representatives of some threatened fern species, but further efforts to enhance future conservation and biodiversity of ferns within the unique circumstances of botanical garden conservatories are recommended (Mounce et al., 2017). Interestingly, innovative ideas for use of homegardens (especially, in less-developed countries and regions of the world) may be one way to preserve some indigenous fern taxa (Amberber et al., 2014).
 
A variety of ex situ protocols and methods for preservation of fern spores, gametophytes and plants have been proposed (Ballesteros, 2011; Pence, 2013; Ballesteros and Pence, 2018), or through a combination of ex situ and in situ methods (Ibars and Estrelles, 2012). Moreover, some in vitro conservation methods for rare and threatened fern species have been recommended (Barnicoat et al., 2011). Overall, a concentrated and coordinated program of applied research and policy analysis by major plant societies and botanical institutions may be needed to ensure that globally, the remarkable diversity and aesthetic quality of ferns will be preserved for current and subsequent generations.


 CONCLUSIONS AND POSSIBLE DIRECTIONS OF FUTURE RESEARCH

The broad diversity of fern taxa, and the remarkably varied geographic and climatic regions where they have become adapted, provides increasing opportunities to use fern species as model organisms to study ecophysiological research on the dynamics of plant and environmental interactions. With changing climatic regimes, some that threaten the survival of uniquely adapted fern species, further research is warranted on understanding the fundamental morphological and physiological processes that account for the adaptive qualities of different groups of ferns. This is especially true, if we are to better conserve environmentally threatened species.
 
Recent innovative approaches that combine trait analyses, functional types (that is, particular ecologically adapted taxa – some above species level) and modern molecular genetic techniques (such as transcriptomics, proteomics, and molecular phylogenetics) are particularly promising. Given the substantial diversity of ferns at the species level, and the challenges of studying species autecology in greater detail, a research strategy that focuses on broader functional groups and their ecophysiological characteristics may be a more productive approach than species-specific research. With modern experimental, controlled-environment facilities coupled with portable field-based physiological instrumentation, opportunities are open for more sophisticated combined laboratory and field-based research on fern physiological ecology. An endeavor to understand the adaptive mechanisms of ferns, that represent morphotypic and functional groups in varied environments, can be a more efficient and comprehensive approach to understanding fern physiological ecology than focusing on lower taxonomic classes of ferns, per se. Moreover, such comprehensive sources of evidence on the most significant ways ferns have adapted to their environmental niches may provide a moresound basis for conservation policies and practices.


 CONFLICT OF INTERESTS

The author has not declared any conflict of interests.


 ACKNOWLEDGEMENTS

This is to appreciate the important contributions that botanical gardens have made in providing public and professional access to research evidence and education about, major global plant species, including ferns. The botanical gardens’ rich collections, and increasing attention to plant conservation, provide unique opportunities to observe and study fern species gathered from world-wide locales that otherwise may not have been possible. This is Lamont-Doherty Earth Observatory Columbia University Contribution Number 8499.



 REFERENCES

Amberber M, Argaw M, Asfaw Z (2014). The role of homegardens for in situ conservation of plant biodiversity in Holeta Town, Oromia National Regional State, Ethiopia. International Journal of Biodiversity and Conservation 6(1):8-16.
Crossref

 

Anderson OR (2018). Ecophysiology and adaptability of terrestrial ferns: Perspectives in a changing global climate. In. Nowicki L, Kowalska A (eds.), Ferns: Ecology, Importance to Humans and Threats. New York: Nova Scientific Publishers pp. 1-55.

 
 

Arcand NN, Ranker TA (2013). Conservation Biology. In. Ranker TA, Haufler CH (eds.), Biology and Evolution of Ferns and Lycophytes. Cambridge: Cambridge University Press. pp. 257-283.
Crossref

 
 

Ballesteros D (2011). Conservation of fern spores, Chapter 12. In. Fernández H, Kumar A, Revilla MA (eds.), Working with Ferns: Issues and Applications. Springer Science+Business Media LLC. pp. 165-172.
Crossref

 
 

Ballesteros D, Pence VC (2018). Fern conservation: Spore, gametophyte, and sporophyte ex situ storage, in vitro culture, and cryopreservation, Chapter 11. In. Fernández H (ed.), Current Advances in Fern Research. New York, USA: Springer International Publishing AG pp. 227-249.
Crossref

 
 

Banupriya TG, Ramyashree C, Akash D, Yathish NS, Sharthchandra RG (2020). Studies on the mechanism of desiccation tolerance in the resurrection fern Adiantum raddianum. Journal of Applied Biology and Biotechnology 8(01):6-14.
Crossref

 
 

Barnicoat H, Cripps R, Kendon J, Sarasan V (2011). Conservation in vitro of rare and threatened ferns - case studies of biodiversity hotspot and island species. In vitro Cellular and Developmental Biology-Plant 47:37-45.
Crossref

 
 

Bhakuni KK, Joshi SC, Anderson OR, Punetha R (2021). Ferns and lycophytes of Gori Valley, Western Himalaya, Uttarakhand: A case study. American Fern Journal 111(1):6-23.
Crossref

 
 

Bravo S, Parra MJ, Castillo R, Sepúlveda F, Turner A, Bertin A, Osorio G, Tereszczuk, J, Bruna C, Hasbún R (2016). Reversible in vivo cellular changes occur during desiccation and recovery: Desiccation tolerance of the resurrection filmy fern Hymenophyllum dentatum Cav. Gayana. Botanical Journal 73(2):402-413.
Crossref

 
 

Chambers SM, Watkins JE Jr., Sessa EB (2017). Differences in dehydration tolerance among populations of a gametophyte-only fern. American Journal of Botany 104(4): 598-607.
Crossref

 
 

Chia S-GE, Raghavan V (1982). Abscisic acid effects on spore germination and protonemal growth in the fern, Mohria caffrorum. New Phytologist 92:31-37.
Crossref

 
 

Crow WE, Mack MR (2011). Narrow substrate niche of Cheilanthes lanosa, the hairy lip fern, is determined by carbohydrate and lipid contents in gametophytes. American Fern Journal 101(2):57-69.
Crossref

 
 

Deeba F, Pandey V (2017) Adaptive mechanisms of desiccation tolerance in resurrection plants. (Ed. Shulkla V, et al.) Plant Adaptation Strategies in Changing Environment. Springer Nature Singapore Pte Ltd. pp. 29-75. 
Crossref

 
 

Farrant JM, Lehner A, Cooper K, Wiswedel S (2009). Desiccation tolerance in the vegetative tissues of the fern Mohria caffrorum is seasonally regulated. The Plant Journal 57:65-79.
Crossref

 
 

Fernández H (ed.) (2018). Current Advances in Fern Research. New York, USA: Springer International Publishing AG. 544p.
Crossref

 
 

Fernández-Marín B, Arzac MI, López-Pozo M, Laza, JM, Roach T, Stegner M, Neuner G, García-Plazaola JI (2021). Frozen in the dark: Interplay of night-time activity of xanthophyll cycle, xylem attributes, and desiccation tolerance in fern resistance to winter. Journal of Experimental Botany 72(8):3168-3184.
Crossref

 
 

Flores-Bavestrello A, Król M, Ivanov AG, Hüner NPA, García-Plazaola JI, Corcuera LJ, Bravo LA (2016). Two Hymenophyllaceae species from contrasting natural environments exhibit a homiochlorophyllous strategy in response to desiccation stress. Journal of Plant Physiology 191:82-94.
Crossref

 
 

Furuya M, Kadota A, Uematsu-Kaneda H (1982). Percent P¬¬¬¬FR-dependent germination of spores in Pteris vittata. Plant and Cell Physiology 23(7):1213-1217.
Crossref

 
 

Gildner BS, Larson DW (1992a). Photosynthetic response to sunflecks in the desiccation-tolerant fern Polypodium virginianum. Oecologia 89:390-396.
Crossref

 
 

Gildner BS, Larson DW (1992b). Seasonal changes in photosynthesis in the desiccation-tolerant fern Polypodium virginianum. Oecologia 89:383-389.
Crossref

 
 

Harten JB, Eickmeier WG (1987). Comparative desiccation tolerance of three desert pteridophytes: Response to long-term desiccation. The American Midland Naturalist 118(2):337-347.
Crossref

 
 

Helseth LE, Fischer TM (2005). Physical mechanisms of rehydration of Polypodium polypodiodes, a resurrection plant. Physical Review E 71:061903.
Crossref

 
 

Hevly RH (1963). Adaptations of cheilanthoid ferns to desert environments. Journal of the Arizona Academy of Science 2(4):164-175.
Crossref

 
 

Hietz P (2010). Fern adaptations to xeric environments. In. Mehltreter K, Walker LR, Sharpe JM (eds.), Fern Ecology. Cambridge: Cambridge University Press. pp. 140-176.
Crossref

 
 

Hietz P, Briones O (1998). Correlation between water relations and within-canopy distribution of epiphytic ferns in a Mexican cloud forest. Oecologia 114:305-316.
Crossref

 
 

Hietz P, Briones O (2001). Photosynthesis, chlorophyll fluorescence and within-canopy distribution of epiphytic ferns in a Mexican cloud forest. Plant Biology 3:279-287.
Crossref

 
 

Holmlund HI, Lekson VM, Gillespie BM, Nakamatsu NA, Burns AM, Sauer KE, Pittermann J, Davis SD (2016). Seasonal changes in tissue-water relations for eight species of ferns during historic drought in California. American Journal of Botany 103(9):1607-1617.
Crossref

 
 

Holmlund HI, Davis SD, Ewers FW, Aguirre NM, Sapes G, Sala A, Pittermann J (2020). Positive root pressure is critical for whole-plant desiccation recovery in two species of terrestrial resurrection ferns. Journal of Experimental Botany 71(3):1139-1150.
Crossref

 
 

Hoshizaki BJ, Moran RM (2001). Fern Grower's Manual. Portland, OR, USA: Timber Press.

 
 

Ibars AM, Estrelles E (2012). Recent developments in ex situ and in situ conservation of ferns. Fern Gazette 19(3):67-86.

 
 

John SP (2017). Drying without Dying: The resurrection fern Pleopeltis polypodioides. Ph.D. Dissertation: University of Louisiana at Lafayette. 237p.

 
 

Joshi SC, Bhakuni KK, Punetha R, Anderson OR (2020). Observations on epiphytic ferns of Kedarnath Wildlife Sanctuary (West Himalaya). Indian Fern Journal 37:47-58.

 
 

Jones DL (1987). Encyclopedia of Ferns. Portland, OR, USA: Timber Press, 433p.

 
 

Jordan EH, Kuehnert CC (1975). The effect of an increase in light intensity utilization of leaf primordia in Osmunda cinnamomea L. Botanical Gazette 136(3):286-289.
Crossref

 
 

Kanegae T, Wada M (2006). Photomorphogenesis in ferns. In. Schäfer E, Nagy F (eds.), Photomorphogenesis in Plants and Bacteria, 3rd edition. Netherlands, Springer. pp. 515-536.
Crossref

 
 

Kavitha CH, Krishnan M, Murugan K (2017). Resilience of ferns: With reference to desiccation and rehydration stress offer new insights. Kongunadu Research Journal 4(2):89-94.
Crossref

 
 

Kessler M (2010). Biogeography of ferns. In. Mehltreter K, Walker LR, Sharpe JM (eds.), Fern Ecology. Cambridge: Cambridge University Press. pp. 22-60.
Crossref

 
 

Kessler M, Siorak Y (2007). Desiccation and rehydration experiments on leaves of 43 pteridophyte species. American Fern Journal 97(4):175-185.
Crossref

 
 

Klinghardt M, Zotz G (2021). Abundance and seasonal growth of epiphytic ferns at three sites along a rainfall gradient in Western Europe. Flora 274:151749. 
Crossref

 
 

Layton BE, Boyd MB, Tripepi MS, Bitonti BM, Dollahon MNR, Balsamo RA (2010). Dehydration-induced expression of a 31-kDA dehydrin in Polypodium polypodioides (Polypodiaceae) may enable large, reversible deformation of cell walls. American Journal of Botany 97(4):535-544.
Crossref

 
 

Lee P-H, Huang Y-M, Chiou W-L (2018). Fern Phenology. In. Fernández H (ed.), Current Advances in Fern Research. New York, USA: Springer International Publishing AG, pp. 381-399.
Crossref

 
 

Liao XL, Jiang MX, Huang HD (2008). Effects of soil moisture on ecophysiological characteristics of Adiantum reniforme var. sinensis, an endangered fern endemic to the Three Gorges Region in China. American Fern Journal 98(1):26-32.
Crossref

 
 

Life AC (1907). Effect of light upon the germination of spores and gametophyte of ferns. Missouri Botanical Garden Annual Report 1907:109-122.
Crossref

 
 

López-Poso M, Fernández-Marín B, García-Plazaola JI, Ballesteros D (2018). In. Fernández H (ed.), Desiccation tolerance in ferns: From unicellular spore to the multi-tissular sporophyte. Springer Intl. Publishing AG. pp. 401-426. 
Crossref

 
 

Mehltreter K (2010). Fern conservation. In Mehltreter K, Walker LR, Sharpe JM (eds.), Fern Ecology. Cambridge: Cambridge University Press. pp. 323-359.
Crossref

 
 

Mehltreter K, Walker LR, Sharpe JM (eds.) (2010). Fern Ecology. Cambridge: Cambridge University Press, 444p.
Crossref

 
 

Moles AT, Sarah EP, Shawn WL, Habacuc F?M, Monica A, Marianne LT, Lawren S, Andy P, Jens K, Lonnie WA, Madhur A, Michael B, Benjamin B, Jeannine C?B, Hans JCC, Will KC, Sandra D, John BD, Grégoire TF, Joshua GG, Alvaro GG, Frank AH, Thomas H, Timothy DH, Matthew K, Michael K, Hiroko K, Michelle RL, Kenwin L, Ülo N, Vladimir O, Yusuke O, Josep P, Valério DP, Peter BR, Satomi S, Andrew S, Enio ES Jr, Nadejda AS, Emily KS, Nathan GS, Peter MVB, Laura W, Evan W, Ian JW, Hongxiang Z, Martin Z, Stephen PB (2014). Which is a better predictor of plant traits: Temperature or precipitation? Journal of Vegetation Science 25:1167-1180.

 
 

Moraes de MG, Oliveira de AAQ, Santos MG (2014). Sugars in ferns and lycophytes growing on rocky outcrops from southeastern Brazilian coast. Bioscience Journal 30(6):1882-1884.

 
 

Moran RC (2004). A Natural History of Ferns. Portland, OR, USA: Timber Press. 302 pp.

 
 

Mounce R, Smith P, Brockington S (2017). Ex situ conservation of plant diversity in the world's botanic gardens. Nature Plants 3:795-802.
Crossref

 
 

Nishida K, Hanba YT (2017). Photosynthetic response of four fern species from different habitats to drought stress: Relationship between morpho-anatomical and physiological traits. Photosynthetica 55(4):689-697.
Crossref

 
 

Nitta JH, Watkins JEJr, Davis CC (2020). Life in the canopy: Community trait assessments reveal substantial functional diversity among fern epiphytes. New Phytologist 227:1885-1899.
Crossref

 
 

Nowicki L, Kowalska A (eds.) (2018). Ferns: Ecology, Importance to Humans and Threats. New York: Nova Scientific Publishers. 178 pp.

 
 

Ong BL, Ng ML (1998). Regeneration of drought-stressed gametophytes of the epiphytic fern, Pyrrosia piloselloides (L.) Price. Plant Cell Reports 18:225-228.
Crossref

 
 

Ong BL, Kluge M, Friemert V (1986). Crassulacean acid metabolism in the epiphytic ferns Drymoglossum piloselloides and Pyrrosia longifolia: studies on responses to environmental signals. Cell and Environment 9:547-557.
Crossref

 
 

Ostria-Gallardo E, Larama G, Berríos G, Fallard A, Gutiérrez-Morago A, Ensminger I, Bravo LA (2020). A comparative gene co-expression analysis using self-organizing maps on two congener filmy ferns identifies specific desiccation tolerance mechanisms associated to their microhabitat preference. BMC Plant Biology 20:56.
Crossref

 
 

Pareek P, Tripathi MK, Tadav MBL (2005). Germination of fern spores under variable temperature and red light. Bionature 25(1&2):143-146.

 
 

Pence VC (2013). Ex situ conservation of ferns and lycophytes - approaches and techniques. In: Ranker TA, Haufler CH (eds.), Biology and Evolution of Ferns and Lycophytes. Cambridge: Cambridge University Press pp. 284-300.
Crossref

 
 

Pérez-García B, Mendoza-Ruiz A, Sánchez-Coronado ME, Orozco-Segovia A (2007). Effect of light and temperature on germination of spores of four tropical fern species. Acta Oecologia 32:172-179.
Crossref

 
 

Pickett FL (1913). Resistance of the prothallia of Camptosorus rhizophyllus to desiccation. Bulletin of the Torrey Botanical Club 4(11):641-645.
Crossref

 
 

Potts R, Penfound WmT (1948). Water relations of the polypody fern, Polypodium polypodiodes (L.) A. S. Hitchcock. Ecology 29(1):43-53.
Crossref

 
 

PPG 1 (2016). A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54:563-603.
Crossref

 
 

Prange RK (1985). Studies on the physiology and propagation of the ostrich fern Matteuccia struthiopteris. Proceedings of the Royal Society of Edinburgh 86B:153-159.
Crossref

 
 

Proctor MCF (2009). Desiccation tolerance of some British ferns. Fern Gazette 18(5):264-282.

 
 

Proctor MCF (2012). Light and desiccation responses of some Hymenophyllaceae (filmy ferns) from Trinidad, Venezuela and New Zealand: Poikilohydry in a light-limited but low evaporation ecological niche. Annals of Botany 109:1019-1026.
Crossref

 
 

Quinnell R, Howell D, Ritchie RJ (2017). Photosynthesis of an epiphytic resurrection fern Davallia angustata (Wall. ex Hook. & Greve.). Australian Journal of Botany 65:348-356.
Crossref

 
 

Raghavan V (1971). Phytochrome control of germination of the spores of Asplenium nidus. Plant Physiology 48:100-102.
Crossref

 
 

Raghavan V (2005). Developmental Biology of Fern Gametophytes. Cambridge: Cambridge University Press. 361 pp.

 
 

Ramírez-Barahona S, Luna-Vega I, Tejero-Díez D (2011). Species richness, endemism, and conservation of American tree ferns (Cyatheales). Biodiversity and Conservation 20:59-72.
Crossref

 
 

Rapp JM, Silman MR (2014). Epiphyte response to drought and experimental warming in an Andean cloud forest. F1000Research 3:7.
Crossref

 
 

Reynolds TL, Raghavan V (1982). Photoinduction of spore germination in a fern, Mohria caffrorum. Annals of Botany 49:227-233.
Crossref

 
 

Rut G, Krupa J, Rzepka A (2003). The influence of simulated osmotic drought on functioning of the photosynthetic apparatus in gametophytes of the epiphytic fern Platycerium bifurcatum. Polish Journal of Natural Sciences, Supplement 1:144-145.

 
 

Sakamaki Y, Ino Y (1999). Contribution of fern gametophytes to the growth of produced sporophytes on the basis of carbon gain. Ecological Research 14:59-69.
Crossref

 
 

Salanchna P, Piechocki R (2021). Salinity tolerance of four hardy ferns from the genus Dryopteris Adans. Grown under different light conditions. Agronomy 11:49.
Crossref

 
 

Saldana A, Lusk CH, Gonzáles WL, Gianoli E (2007). Natural selection on ecophysiological traits of a fern species in a temperate rainforest. Evolutionary Ecology 21:651-662.
Crossref

 
 

Sato T (1992). Size dependency of gametophytes decay in Athyrium brevifrons Nakai during spring desiccation. Ecological Research 7:1-7.
Crossref

 
 

Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magalion S, Lupia R (2004). Ferns diversified in the shadow of angiosperms. Letters to Nature 428:553-557.
Crossref

 
 

Schuettpelz E, Pryer KM (2009). Evidence for a Cenozoic radiation of ferns in an angiosperm- dominated canopy. Proceedings of the National Academy of Sciences U S A 106:11200-11205.
Crossref

 
 

Sessa EB (2018). Evolution and classification of ferns and lycophytes. In. Fernández H (ed.), Current Advances in Fern Research. New York, USA: Springer International Publishing AG. pp. 179-200.
Crossref

 
 

Sharpe JM (2019). Fern Ecology and Climate Change. Indian Fern Journal 36:179-199.

 
 

Sharpe JM, Mehltreter K, Walker LR (2010). Ecological Importance of Ferns. In. Mehltreter K, Walker LR, Sharpe JM (eds.), Fern Ecology. Cambridge: Cambridge University Press. pp. 1-21.
Crossref

 
 

Singh AP, Johari D (2018). Scope of ferns in horticulture and economic development. In: Current Advances in Fern Research. Fernández H (Ed.). New York, USA: Springer International Publishing AG pp. 153-175. 
Crossref

 
 

Stamps RH, Nell TA, Barrett JE (1994). Production temperatures influence growth and physiology of leatherleaf fern. Horticultural Science 29(2):67-70.
Crossref

 
 

Sugai M, Nakamura K, Yamane H, Sato Y, Takahashi N (1987). Effects of gibberellins and their methyl esters on dark germination and antheridium formation in Lygodium japonicum and Anemia phyllitidis. Plant Cell Physiology 28(1):199-202.

 
 

Suissa JS, Sundue MA, Testo WL (2021). Mountains, climate and niche heterogeneity explain global patterns of fern diversity. Journal of Biogeography 00:1-13.
Crossref

 
 

Tessier JT (2001). Vernal photosynthesis and nutrient retranslocation in Dryopteris intermedia. American Fern Journal 91(4):187-196.
Crossref

 
 

Testo WL, Watkins JE Jr. (2013). Understanding mechanisms of rarity in pteridophytes: Competition and climate change threaten the rare fern Asplenium scolopendrium var. americanum (Aspleniaceae). American Journal of Botany 100(11):2261-2270.
Crossref

 
 

Voytena APL, Minardi BD, Barufi JB, Santos M, Randi ÁM (2015). Pleopeltis pleopeltifolia (Polypodiopsida, Polypodiaceae), a poikilochlorophyllous desiccation-tolerant fern: anatomical and biochemical and physiological responses during water stress. Australian Journal of Botany 62(8):647-656.
Crossref

 
 

Warne TR, Lloyd RM (1980). The role of spore germination and gametophyte development in habitat selection: Temperature responses in certain temperate and tropical ferns. Bulletin of the Torrey Botanical Club 107(1):57-64.
Crossref

 
 

Watkins JE Jr., Cardelús CL (2012). Ferns in an angiosperm world: Cretaceous radiation into the epiphytic niche and diversification on the forest floor. International Journal of Plant Science 173(6):695-710.
Crossref

 
 

Watkins JE Jr., Mack MC, Sinclair TR, Mulkey SS (2007). Ecological and evolutionary consequences of desiccation tolerance in tropical fern gametophytes. New Phytologist 176: 708-717.
Crossref

 
 

Winter K, Osmond CB, Hubick KT (1986). Crassulacean acid metabolism in the shade. Studies on an epiphytic fern, Pyrrosia longifolia, and other rainforest species from Australia. Oecologia (Berlin) 68:224-230.
Crossref

 
 

Zhu S-D, Li R-H, Song J, He P-C, Liu H, Berninger F, Ye Q (2016). Different leaf cost-benefit strategies of ferns distributed in contrasting light habitats of sub-tropical forests. Annals of Botany 117:497-506.
Crossref

 
 

Zilberstein A, Arzee T, Gressel J (1984). Early morphogenetic changes during phytochrome-induced fern spore germination I. The existence of a P¬re-photoinduction phase and the accumulation of chlorophyll. Zeitschrift für Pflanzenphysiologie 114(2):97-107.
Crossref

 
 

Zotz G, Hietz P (2001). The physiological ecology of vascular epiphytes: Current knowledge, open questions. Journal of Experimental Botany 52(364):2067-2078.
Crossref

 

 




          */?>