Moonworts are monoecious [2].
Overall genetic diversity is low in moonworts compared to other ferns and fern allies. Soil restricts movement of sperm between moonwort gametophytes, so inbreeding is prevalent. There is a high level of intragametophytic selfing ([27,67], review by [2]). In the intragametophytic selfing breeding system of moonworts, sperm released by belowground antheridia swim less than 1 mm to eggs in archegonia on the same gametophyte [17,67]. Except in rare cases, the resulting sporophytes are genetically nearly identical to their parents [67]. Farrar [17] reported that <1% of moonwort plants tested showed genetic evidence of outcrossing. However, he pointed out that although moonworts have likely had low genetic diversity for thousands to millions of years, their low genetic diversity is apparently not a barrier to population viability [17]. Long-distance spore dispersal and clumping of belowground gametophytes [78] allows for limited genetic exchange.
Metapopulation dynamics are likely important in maintaining moonwort populations, but they are poorly understood for Botrychium [2].
Despite barriers to cross-fertilization, hybridization and polyploidy occur in moonworts, sometimes resulting in new species. For example, daisy-leaf moonwort is a tetraploid that probably resulted from hybridization between diploid lanceleaf moonwort and diploid pale botrychium [27,78].
Botanical descriptions:
Descriptions in this review cover characteristics that may be relevant to fire ecology and are not meant for identification.
Moonworts have 2 distinct generations: the gametophyte (n) and sporophyte (2n) [2,48]. The gametophyte spends its life entirely below ground. The gametophyte generation is longest and is little studied. The sporophyte develops and spends most of its life below ground [48]. Its frond emerges above ground at sexual maturity, and the frond is featured in identification keys. Both generations require mycorrhizae for development [34,67]; the gametophyte is entirely dependent on mycorrhizae for water and nutrients [2,34]. Persistence of associated mycorrhizae is likely the most important factor in persistence of moonwort populations (Johnson-Groh 1999 cited in [2]). See Regeneration Processes for further discussion of the moonwort life cycle.
Figure 8. A cutleaf grapefern gametophyte. Ophioglossaceae gametophytes are barely visible without magnification and are rarely microphotographed. Photo © Dr. Steven J. Baskauf, Bioimages.Moonwort gametophytes grow entirely below ground. They are spherical to oblong, ranging from 0.1 [61] to 3.0 mm [10] in diameter. They lack chlorophyll; young gametophytes are nearly colorless but turn brown with age [10]. Rhizoids cover most of their outer surface [67] (pictured in Figure 8 above).
The mature sporophyte consists of the aboveground frond and the belowground caudex, rhizomes, and roots. The frond stalk is usually divided into 2 segments. The sterile segment (the trophophore) supports leaflets or pinnae, while the upper, fertile segment (the sporophore) supports the sporangia (spore cases) [21,67,79]. The common name "moonwort" refers to the half-moon shape of the leaflets [54]. Moonworts are distinguished by the morphology of their leaflets (for example, simple, pinnate, or dissected) [28,63]. The sporangia are arranged in grapelike clusters [21,28,67]. Moonwort spores are just visible without magnification [62]. The sporophyte has a belowground caudex; fleshy, adventitious roots attach to the caudex [31,67,77]. Moonworts are rhizomatous [67]; rhizomes spread horizontally for 1 to 8 inches (3-20 cm) [34]. Roots are few in number (5-30) and lack root hairs ([34], Bower 1926 cited in [67]).
Moonwort population sizes vary greatly, from fewer than 10 to thousands of sporophyte plants (review by [2]). Population size may appear to fluctuate without discernable causes (U.S. Forest Service 1999 in [46]), although population size cannot be determined accurately without intensive sampling (see Other Management Considerations). Moonworts tend to grow in clumps, often within 0.4 inch (1 cm) of one another [78]. Peculiar moonwort, western moonwort, and their hybrid, Waterton moonwort, grow together in Waterton Lakes National Park [39]. Because moonworts are easily overlooked, they may be more common than surveys to date (2014) indicate [49].
Moonworts are short-lived [39]; they are thought to live for 5 to 10 years [62].
Moonworts manufacture trehalose sugar; that ability is also noted in clubmosses but is unusual among higher plants. Trehalose enables plants to withstand desiccation and rehydrate quickly [80].
Mycorrhizae infect moonwort stems, roots, and rhizoids (Campbell 1908, Bower 1926, Rayner 1927, cited in [67]). These fungal associates are largely unidentified, and some species may be undescribed. Vesicular-arbuscular [72,79] and ectomycorrhorizal [21,49] fungi are associated with moonworts. Some mycorrhizae associated with moonworts have been identified as Glomus spp. ([67,79]).
Common moonwort: Common moonwort's fleshy frond arises from a caudex [31] about 5 mm thick [49]. The frond is long (up to 10 inches (25 cm)) and somewhat leathery [12,54]. Frond leaflets are highly variable in form. Environmental conditions during elongation, such as early-season freezing temperatures, affect the morphology of fully extended leaflets [29]. Electron micrographs showed endophytic fungi infecting common moonwort gametophytes but not sporophytes. The gametophytes were 0.1 to 0.3 mm in diameter, with a few rhizoids [61].
Daisy-leaf moonwort: Daisy-leaf moonwort's frond is relatively long (≥4 inches (10 cm)) and membranous to fleshy [12,21]. The sporophyte has short rhizomes and thick roots. In France, daisy-leaf moonwort fronds emerged when plants averaged about 10 years old. Sporophytes lived another 2 (rarely 3) years after reaching sexual maturity. Over 4 years, an average of 50% of sporophytes were not relocated in surveys (and presumed dead) [48].
Figure 9. Daisy-leaf moonwort frond, showing sporangia-bearing, fertile (upper) and sterile (lower) segments. Creative Commons.Mountain moonwort: Mountain moonwort's frond is somewhat succulent. It may reach 5 inches (12 cm) tall, although it is often shorter [49].
Peculiar moonwort: Peculiar moonwort's frond has 2 spore-bearing segments; unlike other moonworts, this species lacks a sterile frond segment. Mature sporophytes usually range from 3 to 5 inches (7-15 cm) tall in open sun but are shorter in shade [21,49]. Vesicular-arbuscular mycorrhizae [79] and/or ectomycorrhizae [21,49] infect peculiar moonwort's roots and rhizoids. In Waterton Lakes National Park, peculiar moonwort sporophytes lived 6 years or less [39].
Raunkiaer [55] life form:The 4 moonworts covered in this review are native to North America [21]. All are rare throughout most of or all of their ranges [35]. Their distributions are as follows:
Common moonwort: Common moonwort occurs in North America, South America, Eurasia, Australia, New Zealand, and the Pacific islands [21,30,77]. In North America, it occurs from arctic Alaska [11] east to the southern tip of Greenland and south to California, New Mexico, the Dakotas, and Pennsylvania [12,21,70,77]. It is rare throughout most of its North American distribution, but it has scattered pockets of abundance in the Rocky Mountains [35].
Figure 3. Common moonwort's distribution in the United States and Canada. Map courtesy of USDA, NRCS. 2014. The PLANTS Database. National Plant Data Team, Greensboro, NC. (2014, February 7).States and provinces [70]:
United States: AK, AZ, CA, CO, ID, ME, MI, MN, MT, ND, NH, NM, NV, NY, OR, PA, SD, UT, VT, WA, WI, WY
Canada: AB, BC, LB, MB, NF, NS, NT, NU, ON, QC, SK, YT
Daisy-leaf moonwort: Daisy-leaf moonwort occurs in eastern North America, Eurasia [21,42,59], Patagonia [22], Australia, and New Zealand [42]. In North America, it occurs from Manitoba east to Labrador and south to the Dakotas, Tennessee, and North Carolina [35,70]. It is the most common moonwort in the Great Lakes and Northeast regions [19], but it is rare on the western edges of its distribution [35].
Figure 4. Daisy-leaf moonwort's distribution in the United States and Canada. Map courtesy of USDA, NRCS. 2014. The PLANTS Database. National Plant Data Team, Greensboro, NC. (2014, February 7).Mountain moonwort: Mountain moonwort has a scattered distribution in the western United States [21,35,70]. It also occurs in British Columbia [35,70] and Alaska. Except in Washington, it is rare throughout its distribution [35].
Figure 5. Mountain moonwort's distribution in the United States and Canada. Map courtesy of USDA, NRCS. 2014. The PLANTS Database. National Plant Data Team, Greensboro, NC. (2014, February 7).Peculiar moonwort: Peculiar moonwort has a scattered distribution in the western United States and southwestern Canada [21,35]. It is rare throughout its distribution [35].
Figure 6. Peculiar moonwort's distribution in the United States and Canada. Map courtesy of USDA, NRCS. 2014. The PLANTS Database. National Plant Data Team, Greensboro, NC. (2014, February 7).Moonworts are apparently adapted to a wide range of successional stages and occur in plant communities with a wide range of FIRE REGIMES, from short-interval surface to very long-interval, stand-replacement fires. In the Northern Rocky Mountains, for example, common, mountain, and peculiar moonwort grow in mountain grasslands. These grasslands historically experienced fire about every 25 to 100 years, with intervals on the short end most common [3]. Common moonwort grows in Rocky Mountain Douglas-fir forests, which historically experienced both surface and mixed-severity fires. Fire-return intervals for these forests ranged from about 25 to 100 years [4,5]. On the Kootenai National Forest, mountain moonwort grows in western redcedar and western hemlock forests that range from 40 to >1,000 years old [72]; this suggests adaptation to a wide range of postfire successional stages. Common, mountain, and peculiar moonwort occur in fir-mountain hemlock forests on the Pacific coast. Historically, these forests had mostly stand-replacement fires, with fire-return intervals ranging from about 125 to 600 years [1].
See the Fire Regime Table for further information on FIRE REGIMES of vegetation communities in which common, daisy-leaf, mountain, and peculiar moonwort may occur. Find further fire regime information for the plant communities in which these species may occur by entering the species' names in the FEIS home page under "Find FIRE REGIMES".
Bare mineral soil favors postfire establishment of clubmoss spores [2]. Because clubmosses are fern allies that, similar to moonworts, have a life cycle that includes belowground gametophyte and aboveground sporophyte stages, Anderson [2] suggested moonworts might also establish from spores after fire prepares a mineral sporebed.
Plant response to fire: To date (2014), only 2 fire studies [9,57] and anecdotal evidence [45] documented postfire responses of the 4 moonworts covered in this review. Moonwort sporophytes growing in mineral soil likely sprout from their caudices and rhizomes after fire. Gametophytes likely establish from spores stored in the soil and dispersed from off site. Postfire reproduction from gemmae may also occur (see Regeneration Processes). A study in Great Smoky Mountain National Park found dormant-season fire had little effect on moonworts [33]. On the Kootenai National Forest, mountain moonworts sprouted after fronds were completely grazed [72], suggesting ability to sprout after top-kill by fire.
Since both gametophytes and sporophytes grow slowly and are always (gametophytes) or mostly (sporophytes) below ground [2], moonworts may not be found in early postfire surveys. Johnson-Groh and others [34] conjectured that after fire, grazing, or logging, "aboveground populations are fairly resilient and rebound following perturbations, although recovery may take several years". However, Anderson [2] speculated that if fire reduces population density, moonwort populations may require ≥80 years to return to prefire levels.
Moonworts occur in fire-adapted ecosystems. In Minnesota, common moonwort grows on sites with a history of fire and logging [46]. Peculiar moonwort is associated with Rocky Mountain lodgepole pine in Montana [74]; Rocky Mountain lodgepole pine forests have a history of mixed-severity fire about every 25 to 75 years and of stand-replacement fire about every 100 to 330 years [4]. See the FIRE REGIMES section and the Fire Regime Table for further information on the FIRE REGIMES of plant communities in which common, daisy-leaf, mountain, and peculiar moonwort may occur.
Favorable conditions for postfire moonwort regeneration include presence of appropriate mycorrhizae, appropriate soil moisture and chemistry, and possibly, mineral soil [17]. Which fungal species and what concentrations of soil water and nutrients are required were unknown as of 2014. Fire severity and effects to litter, duff, and fungal communities are likely important factors in postfire responses of moonworts [72]. Although associated mycorrhizae are critical to survival of moonwort populations, little is known of either the biology of these mycorrhizae or of moonwort-mycorrhizal interactions. The effects of fire on associated mycorrhizae, and mycorrhizal responses to fire, may be critical to postfire survivorship and growth of moonworts [2]. Studies are need on the basic biology and fire ecology of moonwort species and their associated mycorrhizae.
In a pilot study in Great Smoky Mountains National Park, dormant-season (early spring) prescribed fire or raking increased daisy-leaf moonwort density over prefire densities. The Park had 2 known daisy-leaf moonwort populations, 1 with about 42 emerged sporophytes and other with about 114, depending on the year. The populations grew in second-growth yellow-poplar-red maple-eastern hemlock forests, and disturbed leaf litter appeared to favor the daisy-leaf moonwort populations. The larger population was selected for study; it was on a north-facing slope of 5% to 50% at 2,250 feet (686 m) elevation. Daisy-leaf moonwort sporophytes in the larger population were mapped along 2 transects the year prior to treatments (1997). Three 7- × 10-m² plots (1 prescribed fire,1 raked, and 1 control) were established in 1998; treatments were enacted in March 1998. In posttreatment year 1 (1999), daisy-leaf moonwort density increased 35% on the prescribed fire plot and 33% on the raked plot compared to prefire densities (see Figure 11). Total increase on all plots was from 23 emerged daisy-leaf moonworts sporophytes in 1997 to 144 in 1999. The untreated control plot showed no increase during that time. The author concluded that reducing leaf litter favors daisy-leaf moonwort, and that prescribed burning or raking in spring—while daisy-leaf moonwort is still dormant—are effective management tools for maintaining daisy-leaf moonwort populations [57]. Further published studies are needed to confirm trends suggested by this pilot study.
Figure 12. Daisy-leaf moonwort numbers before and after prescribed fire or raking in Great Smoky Mountains National Park [57] Number of daisy-leaved moonworts before the 1998 spring fire. Number of daisy-leaved moonworts after the 1998 spring fire. Number of daisy-leaved moonworts before 1998 spring raking. Number of daisy-leaved moonworts after 1998 spring raking.On the Keweenam Peninsula, Michigan, daisy-leaf moonwort was noted in a 100+-year-old white spruce-balsam fir forest that "showed evidence" of previous fire [45].
Fire apparently had little effect on a peculiar moonwort population in west-central Alberta. Ten years after a wildfire in Willmore Wilderness Park, peculiar moonwort occurred on both burned and unburned plots. The difference in cover was not significant. The plant community was a subalpine fir-Engelmann spruce/kinnikinnick/boreal wildrye forest [9].
Postfire responses of other moonwort species may help understand postfire responses of the 4 moonwort species covered in this review. In Iowa and Minnesota, prescribed spring fires in prairie and maple-beech forests had little effect on Iowa moonwort and Frenchman's Bluff moonwort populations [33]. For most study years, there was no significant difference in either the number or size of Frenchman's Bluff moonwort sporophytes on burned vs. unburned plots in Minnesota. However, the population was slow to recover after fires during or soon following a drought year. The researchers suggested that dormant-season fires do not harm moonwort species [32,33] but the combination of fire and drought may kill "a substantial number" of moonworts (abstract [32]).
Limited postfire surveys in forests have found moonworts in unburned fire refugia or in burns that are several decades old. On the Kootenai National Forest, Mingan moonwort plants were found in old-growth western redcedar stands that the wildfires of 1910 missed. They were also found in a second-growth western redcedar stand, next to a fire-scarred western redcedar stump [72]. Anderson [2] stated that for leathery grapefern, "there is no evidence that it has an affinity for recently burned areas". Five years after the 1988 wildfires in Yellowstone National Park, Wyoming, he found leathery grapeferns in a fire-refuge site along Obsidian Creek but not on adjacent burned sites. The leathery grapeferns were growing beneath mature Engelmann spruces [2].
Pre- and postfire surveys in South Dakota found a leathery grapefern population that might have been declining or going locally extinct, but fire was probably not the cause. On the Black Hills National Forest, a leathery grapefern population was located in Bucher Gulch in 1994, but surveyors found no leathery grapefern plants in Butcher Gulch in annual surveys from 1995 through 2001 (Crook 2003 personal communication in [2]). The site was burned in 2002 by a low-severity fire that left a mosaic of unburned patches. A 2003 survey failed to locate any leathery grapefern plants [2]. Without previous annual surveys, wildfire might have been implicated in this apparent population decline. Since no belowground surveys were conducted (see Other Management Considerations), true population numbers could not be estimated.
Immediate effects of fire on moonworts were undocumented as of 2014. Since moonwort gametophytes are below ground, surface or crown fires may not damage them. Gametophytes residing in litter and duff are likely vulnerable to fire, especially ground fire.
Fire during the growing season likely top-kills emergent moonwort sporophytes. Since their caudices and rhizomes are below ground, fire is probably not lethal to sporophytes growing in mineral soil. Fire may not damage dormant moonwort sporophytes. Most moonwort sporophytes are usually dormant during drought [39], so they are likely dormant in extreme fire years.
Because moonworts are small and ephemeral, herbivores may graze them only incidentally. However, herbivore use of palatable moonwort species may become concentrated in seasons favorable to moonwort emergence and growth. As of 2014, little information was available regarding the relative palatability of moonwort species, and no information was available on their nutritional value.
On the Kootenai National Forest, mountain moonworts showed "considerable levels" of herbivory. Mountain moonworts sprouted after fronds were completely grazed. Cooccurring peculiar moonworts were apparently not grazed [72].
Rocky Mountain bighorn sheep grazed peculiar moonwort in Willmore Wilderness Park. On a scale from 1 (primary forage) to 5 (not grazed), peculiar moonwort utilization was ranked at 2 [9]. In Waterton Lakes National Park, rodents did not graze peculiar moonwort, although they apparently grazed cooccurring Waterton moonwort and western moonwort [39].
Cover value: Moonworts are too small to provide cover for vertebrates.
Moonworts are ephemeral. The single frond of sexually mature sporophytes emerges in spring or early summer [67], and spores disperse in summer. The frond desiccates by midsummer to late fall [67].
Mature moonwort sporophytes may remain dormant for a year or more before re-emerging [31,39]. Drought and lack of nutrients apparently induce dormancy in moonwort species [76,78], although other as yet unidentified factors may also induce dormancy. In Waterton Lakes National Park, 78% of peculiar moonworts sampled were dormant for 1 year, 19% for 2 years, and 3% for >2 years. Approximately 280 peculiar moonwort sporophytes were located in this 4-year study [39]. Annual dormancy rate averaged 13% for a daisy-leaf moonwort population in France. Daisy-leaf moonwort fronds desiccated in spring, prior to spore dispersal, in drought years [47].
Table 1. Phenology of common, daisy-leaf, mountain, and peculiar moonworts Species Region Event Period Common moonwort across range fronds emergefronds emerge
spring
fronds desiccate mid- to late summer [49]POSTFIRE REGENERATION STRATEGY* (adapted from [68]):
Rhizomatous herb, rhizome in soil
Caudex, growing points in soil
Geophyte, growing points in soil
Ground residual colonizer (on site, initial community)
Initial off-site colonizer (off site, initial community)
Secondary colonizer (on- or off-site spore sources)
*These postfire regeneration strategies are possible based on moonwort morphology and methods of regeneration but have not been confirmed in field studies.
Because moonworts are easily overlooked and rare, little is known of their habitat preferences. They tend to grow in open areas including beaches, subalpine and alpine meadows [62], and wood edges [19,77]. They are uncommon in arid environments [62]. In the United States, most moonwort species grow at high elevations [21]. In the Southern Rocky Mountains, they are most common above 9,000 feet (2,700 m) [62]. Soils supporting moonworts are moist [19] to well-drained and often gravelly or rocky [62]. Moonworts generally favor acidic to neutral soil (pH 4.8-7.2) [65]. However, some species, including common moonwort, tolerate or prefer basic soils [9,19,49]. Moonworts are commonly associated with recent (15-30 years) natural and human-caused disturbances, growing on avalanche chutes, talus slopes, and deglaciated areas; along roadsides, airstrips, and ski runs; and in fields, pastures, and areas of mining activity [67]. Farrar [17] reported that in general, moonworts do not have precise habitat requirements. Associated mycorrhizae (see General Botanical Characteristics) apparently mediate many interactions of moonworts species with their environments [17].
The limited information available on habitats of common, daisy-leaf, mountain, and peculiar moonworts (as of 2014) is summarized below. See the Fire Regime Table for a list of plant communities in which these moonworts may occur and information on the FIRE REGIMES associated with those communities. See Appendix B for scientific names of plant species mentioned in this review.
Common moonwort: Common moonwort is cosmopolitan in habitat [19]. It grows on shores, cliff ledges, scree, and open gravelly slopes; in open fields, meadows, and woodlands [19,49]; and occasionally in forests. It tolerates and often grows on dry soils [21] such as sand dunes, but it is most common on moist, well-drained woodland and meadow soils [19]. It prefers neutral [49] to basic [12,49,63] soils.
In Alaska, common moonwort occurs on grassy slopes [29] and shrubfields. In arctic northeastern Alaska, a common moonwort population grew on a south-facing slope in the organic layer of a sandy loam derived from glaciofluvial materials. The plant community was a shrub-grassland dominated by grayleaf willow, shrubby cinquefoil, northern rough fescue, and arctic brome. Common moonworts grew in the middle of the community, appearing as scattered individuals or in pairs. They were growing within grass clumps beneath grayleaf willows [11]. Northeast of Nome, common moonwort was abundant (40% frequency) in an arctic dwarf birch-bog birch dwarf shrubland [25]. In southeastern Alaska, it grew on the face of Yakutat Glacier [67]. Near Palmer in south-central Alaska, it grew in slender wheatgrass, bluejoint reedgrass, and northern rough fescue-mountain cranberry grassland communities [24].
Near the Alaskan Highway in Yukon, Corell [13] observed "numerous" common moonwort plants growing in a limestone sink above timberline. Krummholz subalpine fir, Sitka clubmoss, fir clubmoss, and alpine clubmoss grew on the same site [13].
Common moonwort grows mostly in open communities in the conterminous United States. On the Pacific coast, it grows on grassy slopes and in fields, moist meadows, heathlands, and in open forests. It occurs from low to high elevations [54]. In the Intermountain West, it grows on wet to moist sites at middle to high elevations [14]. In Idaho, it grows in mountain meadows and western redcedar-western hemlock forests. A survey on the Kootenai National Forest, Idaho, found common moonwort grew exclusively in old-growth western redcedar and western hemlock forests [72]. In Glacier National Park, Montana, it grows in mountain meadows, mossy banks, and bogs. In the 1920s, it was noted as "plentiful" on the moraine of Grinnell Glacier [66]. It is reported in grassy meadows and on wood edges in Utah, from 7,700 to 11,500 feet (2,350-3,500 m) elevation [77]. In Colorado, it grows in mountainous regions at elevations up to 12,000 feet (4,000 m) [26]. In the Rocky Mountains of central Colorado, common moonwort was noted in limber pine-Rocky Mountain Douglas-fir-interior ponderosa pine forests [60]. In the San Francisco Peaks of north-central Arizona, it grew in alpine meadows dominated by Ross' avens and sedges. These communities occur at and above 10,100 feet (3,500 m) [52]. Near timberline at 11,600 feet (3,550 m), common moonwort was found in a krummholz Great Basin bristlecone pine-Engelmann spruce/Ross' avens community [56]. In New England, common moonwort occurs on open slopes [64] and in open woodlands [16].
Daisy-leaf moonwort: This species is cosmopolitan in habitat [19]. It grows on roadsides and in meadows, woodlands, forest edges, open to closed forests, and rich swamps [12,19,41,63]. It tolerates moist to dry soils that range from acidic to neutral pH [19]. Across Canada and the United States, it occurs from sea level to 4,000 feet (1,200 m) [21]. In the Intermountain West, it grows in woodlands at low to middle elevations [28]. It occurs above 4,000 feet (1,200 m) in the Black Hills of South Dakota [19]. It is reported in moist woodlands in the Great Plains [23]. In Minnesota, daisy-leaf moonwort gametophytes, collected in the field and identified in the laboratory, were growing with least moonwort in a white oak-bur oak-northern red oak forest [10]. In Michigan, daisy-leaf moonwort grows in conifer and hardwood-conifer forests. In Gogebic and Ontonagon counties, it was found on mesic to dry sites [44]. On the Keweenaw Peninsula, Michigan, daisy-leaf moonwort was noted in a 100+-year-old white spruce-balsam fir forest with eastern white pine and quaking aspen. The site was mesic, and the canopy was opening due to canopy-gap succession [45]. Daisy-leaf moonwort is reported in grassy meadows in Illinois [58]. In Nova Scotia, it grows in hardwood communities on leaf mold or rich alluvial soils [58]. In the Northeast, it occurs in thickets and woodlands in "subacid" soil [22]. In New Jersey, daisy-leaf moonwort occurred in a pin oak woodland and on the border of a pitch pine barren. The pin oak community soil was moist, rich clay, while soil on the pine barren border was dry sand [41]. In Maryland, a daisy-leaf moonwort population was found in "damp woods" along a tributary of the Patapsco River [75]. A population in Montgomery County, Maryland, grew beneath a dense eastern poison-ivy thicket in a yellow-poplar/flowering dogwood stand [20]. In Great Smoky Mountains National Park, North Carolina, daisy-leaf moonwort grew in mesophytic cove forests of yellow-poplar, red maple, and eastern hemlock. A daisy-leaf moonwort population was noted on north-facing slopes of 5% to 50%, at 2,250 feet (686 m) elevation. Daisy-leaf moonworts were most common in areas without leaf litter and duff [57].
Mountain moonwort: Mountain moonwort grows in dark, moist habitats. This, and its gray-green color, earns it the alternate common name "western goblin" [19]. It grows in conifer forests, usually in or near riparian zones [19,21,49,74], and in moist meadows, seeps, and fens [19,74]. Mountain moonwort has been found on calcareous soils [19]. Across its range, it occurs from 3,000 to 6,500 feet (1,000-2,000 m) elevation [21]. In Washington, it prefers old-growth western redcedar riparian forests and is uncommon in other plant communities. Western redcedar forests with mountain moonwort occupy upper terraces near small to moderate-sized streams. Soils are moist, with high concentrations of organic matter and minerals [19]. Surveyors on the Kootenai National Forest found mountain moonwort exclusively in mature second-growth and old-growth western redcedar and western hemlock forests [72]. In California, mountain moonwort occurred in conifer forests at 5,000 to 6,000 feet (1,500-1,800 m), growing mostly in the southern Cascade Range [69]. Specimens were collected near a stream in Butte and Tehama counties, in a mixed-conifer forest of incense-cedar, white fir, sugar pine, and Pacific ponderosa pine [19,76]. Farrar [19] suggested that litter from the Cupressaceae family, which includes western redcedar and incense-cedar, favors mountain moonwort growth. Additionally, mycorrhizae associated with Cupressaceae are also associated with Botrychium [9,19].
Figure 7. Mountain Moonwort growing in incense-cedar debris and litter in an ephemeral drainage on the El Dorado National Forest, California. Photo ©2012 Belinda Lo, courtesy of Creative Commons.Moonworts are common in full sunlight [2,49,62] but tolerate some shade. They grow on open meadows, slopes, and banks [26,49,62]. Limited observations suggest that in open areas, moonworts may grow in shaded microsites. For example, moonworts have been found growing beneath shrubs [11] and near tall bunchgrasses that provide shade [39].
Moonworts are associated with light to moderate disturbances [39] but also occur in late successional stages [19,72]. A review stated that "moderate disturbance may be a critical part of the autecology of Botrychium species" [2]. However, moonworts are generally found on sites disturbed ≥10 years prior (Johnson-Groh 2003 personal communication in [2]).
Common moonwort: Limited studies and observations suggest common moonwort sporophytes are absent or uncommon in the initial stage of postdisturbance succession. In the Intermountain West, common moonwort is more common in partial shade than in either open meadows or closed forests [14]. In arctic Alaska, common moonwort was rooted in deep organic material over glaciofluvial material. The depth of the organic layer in which common moonwort grew suggested that it did not establish in early succession, although the exact depth was not provided. Common moonwort was not found on young glaciofluvial materials [11]. Researchers in Norway suggested that common moonwort is a late-successional species. It was absent from subalpine grasslands ploughed 3 to 5 years prior; it was found exclusively in unploughed subalpine meadows [6].
Daisy-leaf moonwort: Daisy-leaf moonwort occurs in second-growth forests across its range [21]. It grows on open sites as well as in closed-canopy forests. It grew in a roadside barrow pit in Glacier National Park [38], suggesting that it tolerates disturbed sites. In the southern Appalachian Mountains it is restricted to closed, mature hardwood forests [19]. It was noted on shaded trails in the Carolinas [44].
Mountain moonwort: Mountain moonwort grows in shady woodlands and closed forests [21,69] but also in open meadows [19]. In Washington, it is most common in old-growth western redcedar forests but has also been found in mountain meadows on Mt Baker [19]. On the Kootenai National Forest, Vanderhorst [72] found mountain moonwort in second-growth western redcedar forests ranging from 40 to 210 years old and in old-growth western redcedar forests that were probably >1,000 years old. It was often the only groundlayer species growing in the deeply-shaded litter of old-growth western redcedar stands. Vanderhorst did not find it in clearcuts [72].
Peculiar moonwort: Successional preferences of peculiar moonwort had rarely been studied as of this writing (2014). A peculiar moonwort population was found on a south-facing roadside in Glacier National Park [8], suggesting ability to grow on open, disturbed sites. In Waterton Lakes National Park, peculiar moonwort occurred in meadow portions of Rocky Mountain lodgepole pine forest-mountain meadow mosaics. Rocky Mountain lodgepole pine forests are subject to wildfire and pine beetle attacks, which slows Rocky Mountain lodgepole pine invasion into meadows. Sites with peculiar moonwort had a dense litter layer and bare soil was uncommon, suggesting infrequent disturbances [39].Moonworts are classified in the genus Botrychium Sw. (Ophioglossaceae) [21,35,63,70]. Within the genus, moonworts are placed in subgenus Botrychium, while grapeferns are placed in the subgenus Sceptridium [17]. This review provides detailed information on 4 moonwort species. Their scientific names are:
Botrychium lunaria (L.) Sw., common moonwort [12,14,21,29,35,63,70,77]
Botrychium matricariifolium (A. Braun ex Dowell) A. Braun ex Koch, daisy-leaf moonwort [22,35,58,63,70]
Botrychium montanum W.H. Wagner, mountain moonwort [21,35,69,70]
Botrychium paradoxum W.H. Wagner, peculiar moonwort [21,35,70]
This review uses common names for plant species. See Appendix B
for scientific names of plant species mentioned in this review.
In the broad sense, the Botrychium lunaria complex consists of several closely aligned moonwort species [15,19,67]. These taxa are: common moonwort, giant moonwort, Tunux moonwort, and dainty moonwort. Stensvold [67] and Farrar [19] consider dainty moonwort a variety of common moonwort. Their genetic studies found 3 distinct genotypes of common moonwort (proposed names in parentheses) [67]:
1) a genotype endemic to the western United States and Canada (Botrychium lunaria var. crenulatum (W.H. Wagner) Stensvold, dainty moonwort)
2) a genotype endemic to Greenland, Iceland, and Norway (Botrychium lunaria var. melzeri Stensvold, Melzeri's moonwort)
3) a genotype with a circumpolar distribution (Botrychium lunaria var. lunaria, common moonwort)
Hybrids:
Moonworts may hybridize, although resulting plants are usually sterile [27,67]. Common moonwort hybridizes with pointed moonwort [67], spathulate botrychium [67,78], and Mingan moonwort [67]. Mingan moonwort apparently resulted from common moonwort × pale botrychium hybridization [78], and Waterton moonwort from peculiar moonwort × western moonwort hybridization [17,21,78]. Waterton moonwort is known only from western Alberta, in Waterton Lakes National Park [21,39].
Moonworts may reproduce asexually by producing gemmae [18,49]. These spherical propagules grow on rhizomes [34] or aboveground stems [18] and range from 0.5 to 1.0 mm in diameter. They develop below ground after abscission from the stem. Gemmae mature into sporophytes; their development is similar to that of sexually produced embryos. Limited microscopic examinations (n=12 stems/species) found no gemmae on either common moonworts from Colorado or daisy-leaf moonworts from Michigan [18], although NatureServe [49] reported that common moonworts sometimes produce gemmae. Gemmae have been found on mountain moonworts collected in Idaho [72]. Further examinations are needed to determine the importance of gemmae to moonwort regeneration in general and the moonwort species discussed in this review in particular.
Moonworts have caudices and rhizomes [31,67], and they likely sprout from these organs after top-kill. Further research is needed on the ability of moonworts to sprout after disturbances such as fire or grazing.
Botrychium is a genus of ferns, seedless vascular plants in the family Ophioglossaceae.[1] Botrychium species are known as moonworts. They are small, with fleshy roots, and reproduce by spores shed into the air. One part of the leaf, the trophophore, is sterile and fernlike; the other, the sporophore, is fertile and carries the clusters of sporangia or spore cases. Some species only occasionally emerge above ground and gain most of their nourishment from an association with mycorrhizal fungi.
The circumscription of Botrychium is disputed between different authors; some botanists include the genera Botrypus and Sceptridium within Botrychium, while others treat them as distinct. The latter treatment is provisionally followed here.
Moonworts can be found in many environments, including prairies, forests, and mountains. While some Botrychium species are quite rare, conservation efforts can be difficult. Determining the rarity of a species is complicated by the plants’ small leaves, which stand only 2-10 centimeters above the soil.[16] Even more of a challenge in obtaining an accurate population count is the genus’s largely subterranean life cycle. The vast majority of any one population of moonworts actually exists below ground in banks consisting of several types of propagules. One type of propagule is the ungerminated spores, which must percolate through the soil beyond the reach of light in order to germinate. This presumably increases the probability that the spore will be in range of a mycorrhizal symbiont before it produces the tiny, roughly heart-shaped gametophyte, which also exists entirely below ground.[46] Finally, some species produce gemmae, a form of asexual propagation achieved by budding of the root.[16]
Juvenile and dormant sporophytes can also be hidden in the soil for long periods of time. Mature sporophytes do not necessarily produce a leaf annually; they can remain viable underground for up to 10 years without putting up a photosynthetic component. This feat is made possible by their dependence on symbiotic partnership with AM fungi of the genus Glomus, which supply most fixed carbon for growth and reproduction.[47]
This mycorrhizal dependence has also made lab cultivation of moonworts difficult. Thus far, only germination of the gametophyte has been successful.
Botrychium is a genus of ferns, seedless vascular plants in the family Ophioglossaceae. Botrychium species are known as moonworts. They are small, with fleshy roots, and reproduce by spores shed into the air. One part of the leaf, the trophophore, is sterile and fernlike; the other, the sporophore, is fertile and carries the clusters of sporangia or spore cases. Some species only occasionally emerge above ground and gain most of their nourishment from an association with mycorrhizal fungi.
The circumscription of Botrychium is disputed between different authors; some botanists include the genera Botrypus and Sceptridium within Botrychium, while others treat them as distinct. The latter treatment is provisionally followed here.
