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Ecology |
2Biology Department, Gustavus Adolphus College, 800 West College Avenue, St. Peter, Minnesota 56082 USA; 33858 Xenia Ave N, Robbinsdale, Minnesota 55422 USA
Received for publication March 5, 2002. Accepted for publication May 16, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Key Words: Botrychium • demography • management • moonwort • phenology • reproductive success • temporal heterogeneity
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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). The belowground rhizome is upright and short with mycorrhizal stem and roots and a single leaf-producing bud at the apex. The bud may contain up to four preformed leaves (Braggins, 1980
). Some species reproduce asexually via belowground gemmae, small (0.5–1 mm) propagules that can independently start a new plant once detached from the parent plant (Farrar and Johnson-Groh, 1990
).
The subgenus Botrychium contains several species that are considered rare or uncommon (Minnesota Department of Natural Resources, 2002
). Whereas many species of Botrychium are truly rare, others only appear to be rare because of their small size, difficulty of finding, difficulty of identifying, and, until recently, the low number of field investigators actively looking for them. In addition Botrychium are able to remain dormant for several years (Montgomery, 1990
; Johnson-Groh and Farrar, 1993
; Muller, 1993
; Kelly, 1994
; Lesica and Ahlenslager, 1996
; Johnson-Groh, 1998
), and in some species they develop, but remain undetected under thick litter and duff (Johnson-Groh, 1998
).
These latter characteristics, along with our lack of understanding of Botrychium ecology, especially belowground aspects, have confounded ecologists and land managers attempting to manage sites for conservation of Botrychium. Managing sites with rare Botrychium may include management practices that are essential to the maintenance of the habitat, such as burning prairies, but which are also potentially harmful to Botrychium. It is not a question of whether to implement such management practices, but rather when to implement management. Documenting the phenology of moonworts is an important step in understanding their ecology and effectively managing for these rare species.
Several annual monitoring studies of Botrychium have been and are being conducted in the United States including western sites (Lesica and Ahlenslager, 1996
; C. L. Johnson-Groh, unpublished data), midwestern sites (Farrar and Johnson-Groh, 1986
; Johnson-Groh and Farrar, 1993
; Johnson-Groh, 1998
), and eastern sites (Montgomery, 1990
). Likewise rare Botrychium have been monitored in France (Muller, 1992
, 1993
) and New Zealand (Kelly, 1994
). In most of these studies a date was chosen for annual monitoring that was presumed to allow detection of the maximum number of plants visible during a single visit. In reality, it is unknown what proportion of plants in the total population may have emerged previously and reached senescence by the monitoring date or how many emerged subsequent to this date.
Permanent plots represent a population sample from which population size estimates are made. If sampling was done at a time before all plants had emerged or after some had senesced, a false estimate of the population size is derived. Understanding how the population changes over the season allows more accurate estimates of population sizes and thus more accurate assessments of the rarity of these species. By understanding their phenology, we can determine "windows" of time during which human impact on these species should be minimized.
Despite abundant data on moonwort population dynamics, little is known about the phenology of Botrychium. Muller (1992)
examined plants of B. matricariifolium (subgenus Botrychium) weekly to determine the effect of drought on plants in France and found that plants affected by spring drought did not sporulate. Montgomery (1990)
monitored B. dissectum twice during the growing season (spring and autumn), studying annual population dynamics, and found population size and herbivory differences between spring and autumn samples. (Botrychium dissectum is in the subgenus Sceptridium, which differs from the subgenus Botrychium in several aspects including morphology and ecology.)
Likewise, relatively few studies have been conducted on the phenology of other pteridophytes. Most of these have been on tropical ferns (Sharpe and Jernstedt, 1990
; Sharpe, 1993
, 1997
) with several studies focusing on tree ferns (Seiler, 1981
, 1995
; Tanner, 1983
; Ash, 1986
, 1987
). Studies conducted on ferns with summer green leaves have largely been restricted to studies conducted by Sato in Japan (Sato, 1982
, 1985a
, b
, 1986
), Wilmot on Dryopteris (1989) and Odland on Thelypteris, Athyrium, and Matteuccia (1995).
This study reports the phenology and demography of two species of moonworts, a prairie species, B. gallicomontanum, and an old-growth maple–basswood species, B. mormo. Five plots were monitored in 1996 and 1997 to determine when the plants emerge, develop, release spores, and senesce.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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). It is endemic to northwestern Minnesota, USA, restricted in its known occurrences to two nearby prairies in Norman County and a third site in Kittson County. Additional populations have not been found despite extensive searches. The second species, B. mormo W. H. Wagner, is a maple–basswood forest species, with a limited distribution that has been found increasingly with recent intensive searches. Botrychium mormo is rare in Wisconsin and Michigan with the highest density of sites and largest populations found in Minnesota. Demographic studies have been conducted since 1987 for B. gallicomontanum and since 1992 for B. mormo by Johnson-Groh. Annual monitoring had been conducted in June for B. gallicomontanum and in August or September for B. mormo. Permanent plots have been established for these long-term ecological studies of which five plots were used for this phenological study. Plots were selected as representatives of different aspects and geographic regions. For phenological analysis three plots containing B. gallicomontanum in Norman County, Minnesota, were monitored from April through June 1996 and 1997. Two plots containing B. mormo, in the Chippewa National Forest, Minnesota, were monitored from June through September 1996 and 1997.
The Norman County prairie plots (B. gallicomontanum) were characterized as a mid-grass prairie on a well-drained, gravelly soil. Associated species included: Botrychium simplex, Schyzachrium scoparium, Stipa comata, Poa pratensis, Artemisia frigida, Andropogon gerardii, Geum trifolium, Amorpha canescens, and Aster sericeus. Three phenology plots (numbers 1, 2, and 3) were located at distant ends within the same preserve (the only known site for this species at the time of the study).
The Chippewa National Forest sites (B. mormo) were characterized as old-growth maple–basswood forests on well-developed organic soils with a dense layer of duff. Associated species included: Tilia americana, Acer saccharum, Betula papyrifera, Carex spp., Aralia racemosa, Botrychium virginianum, Osmorhiza spp., Trillium grandiflorum, Athyrium filix-femina, Arisaema triphyllum, Galium triflorum, Thalictrum dioicum, Uvularia grandifolia, and Sanicula spp. Plots 4 and 5 were located in the Chippewa National Forest approximately 35 km apart.
Plots were oriented north-south and permanently marked with a metal tree anchor. Each plot contained 5.7 m2 in which each individual plant was marked by a numbered aluminum tag attached to an aluminum wire inserted into the ground 2 cm north of the plant. (Potential influences of the tags on plant growth have been tested through comparative studies on "tagless" plots.) Marking each individual plant allowed a high degree of certainty that all plants could be precisely relocated and monitored. Each tag was checked for presence or absence of plants, and plants present were measured and scored as to the stage of development (just emerging, releasing spores, etc.) as well as disturbances such as herbivory. What we refer to henceforth as "plants" are the emergent leaves. Thus, the absence of a "plant" at a tag meant the absence of a visible presence. The status of the belowground stem was undetermined. The heights of the sporophore and trophophore were measured from the base of the plant to the tip of the sporophore or trophophore. During each visit new plants were measured and tagged. This procedure was followed biweekly in 1996 and monthly in 1997. Extreme caution was taken to avoid damaging plants and thereby affecting subsequent measurements. The impact of tags and monitoring on plants has been compared in tagged and untagged plots. No difference was found in size or reappearance between tagged and untagged plots (C. L. Johnson-Groh, unpublished data). A total of 631 plants were observed in this study (219 B. gallicomontanum and 412 B. mormo).
Four stages of development were recognized: emergence, separation, spore release, and senescence (Figs. 1–4). Emergence included the appearance of the plant from the soil and was characterized by the trophophore clasped tightly around the sporophore. As the plants developed, the trophophore separated from the sporophore and spread backward exposing the photosynthetic lamina. This was called the separation stage and included elongation of the sporophore prior to spore release. The spore-release stage included plants that were full size and releasing spores. During this stage the sporangia were characteristically yellow, turning brown, and releasing spores. The final stage, senescence, included plants that had released spores and begun to wither, dry up, or rot. Muller (1992)
recognized four similar stages of development for Botrychium matricariifolium.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Botrychium mormo (the forest species) demonstrated different trends. The population emerged in early June (considerably earlier than previously thought) and increased more rapidly than in B. gallicomontanum, peaking approximately 1 mo later in July (Fig. 8). The population then gradually declined. Botrychium mormo populations spent relatively longer times in the separation, spore release, and senescence stages than did B. gallicomontanum. Plant size increased steadily throughout the season, with the largest plants occurring at the end of the season. It is this occurrence of the largest plants late in the season that previously caused field workers to believe that this was a late-season species. (These plants are small, cryptic, difficult to find, and consequently difficult to quantify through visual surveys.)
The differences in emergence rates noted above are a result of the habitat differences. It is adaptive for spring species in exposed habitats such as a prairie to emerge "cautiously" and not simultaneously given the threat of late-season killing frost. Botrychium gallicomontanum are frequently observed with necrotic tissue due to frost damage. Plants must also emerge early enough to avoid the heat and drought of prairie summers. Conversely, forest species are buffered from temperature and moisture extremes and do not encounter a similar need for, or risk from, early emergence. Botrychium mormo emerges after the threat of late-spring frost has passed and does not exhibit a prolonged period of emergence. Odland (1995)
found similar differences in phenological adaptations in Thelypteris that he attributed to summer temperatures responses.
Opposite trends were found for the separation stage. The mean time between separation and spore release is significantly longer in B. mormo than in B. gallicomontanum (P < 0.0001, N = 170 and 123, respectively). The time between the onset of leaf separation and the release of spores and senescence is very short in B. gallicomontanum, resulting in a relatively short period of photosynthesis. Sunlight is less limited in the prairie and photosynthesis rates may be much higher than for B. mormo in the forest. In an old-growth maple–basswood forest plants may need longer periods to garner adequate carbohydrate reserves.
An added difficulty for B. mormo is emerging through a dense layer of decomposing leaf litter and duff. (Prairie grass litter may accumulate in a deep thatch, but generally it is not densely matted, as is maple–basswood leaf litter.) Botrychium mormo has been observed buried below the litter, never completely emerging. "Albino" forms of B. mormo have also been observed occasionally. Botrychium mormo may receive a significant portion of its carbohydrate from the mycorrhizae and depend less on its own photosynthate than does B. gallicomontanum. To successfully disperse spores, however, the plants must emerge above the leaf litter. The longer period of leaf separation and development prior to spore release observed in B. mormo may allow the plants more time to emerge through the litter so that spores can be released above the litter to maximize dispersal.
Other workers have noted a time lag in frond development. Wagner and Wagner (1977)
found a lag in development for B. lunariodes (subgenus Sceptridium) following emergence, and Sharpe and Jernstedt (1990)
noted a time lag in the development of Danaea, a tropical fern.
The stages of spore release and senescence are similar in both species. Plants emerging later in the season had shorter season spans for both species, completing all stages (emergence, separation, spore release, and senescence) in considerably less time. Any plants appearing before 16 June for B. gallicomontanum and 10 August for B. mormo were capable of advancing through all stages and contributing to the spore bank (Figs. 6 and 9). Following spore release, senescence occurred rapidly in both species. Because of their fleshy nature, plants often wilt and rot quickly, rather than dry out. Only during a drought in 1988 were B. gallicomontanum observed to senesce via drying rather than rotting (C. L. Johnson-Groh, unpublished data).
It is possible for late-emerging plants to develop rapidly enough to produce spores as noted above. These plants have less time for photosynthesis because all the stages are condensed. Late-developing plants must have adequate reserves and probably depend less on photosynthate produced during this period and more on carbohydrate reserves provided by mycorrhizae (Simard et al., 1997
; Smith and Read, 1997
). Late-emerging plants are probably not chronically late annually because of the demand that this would eventually place on carbohydrate resources. There is no evidence either from this study or annual monitoring that individual plants are chronically early or late annually.
Similarly, Sato (1985b)
observed a tendency of ferns occurring on exposed sites to have earlier maturation and spore dispersal than forest ferns. He reasoned that forest ferns needed to acquire a larger size for capture of sufficient radiation. Sato considered the early-maturing species to be R-strategists and the late maturing species to be K-strategists. Many species of Botrychium (B. gallicomontanum, B. campestre, B. ascendens, and B. paradoxum) could be considered R-strategists in that they occur in open habitats more subject to disturbances and/or climate variance than do forest species, develop rapidly as shown in this study for B. gallicomontanum, and have a relatively higher spore set than do similar-sized forest species. (The actual spore set has not been measured, but B. gallicomontanum produces a considerably larger sporophore with more sporangia than B. mormo [Farrar and Johnson-Groh, 1991
; Wagner and Wagner, 1981
].) It is common to find these Botrychium growing in sand dunes or beaches where the flowering plant community is minimally developed. Other species such as B. mormo, B. montanum, B. lunaria, and B. lanceolatum resemble K-selected species; they require a longer period for maturation, grow in well-developed mature communities, and have a lower spore set. While it is tempting to classify Botrychium species as R- and K-strategists, we clearly lack sufficient data on the life history of most species to reach such conclusions.
Reproductive success: spore set
The overall reproductive success of the population may be measured by the annual contribution to the spore bank. Due to herbivory, mechanical damage, disease, or arrested development, not all plants contribute to the spore bank. Of 412 B. mormo plants studied, only 39% completed development (Table 2) moving though the first three stages of emergence, separation, and spore release, and only 55% of B. gallicomontanum plants completed their development.
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), making it difficult to test the viability of these unreleased spores.
Other studies have reported variation in the number of plants that produce spores. Kelly (1994)
demonstrated that only 9–20% of B. australe produce fertile spikes with sporangia in any given year. Kelly attributed this to light levels; plants in heavy shade were unlikely to be fertile. (Botrychium subgenus Botrychium produce sporangia every year they emerge whereas the subgenera Sceptridium and Osmundopteris do not regularly produce sporangia as juvenile aboveground plants.) Muller (1992)
found that some plants wilted prematurely and did not set spores due to a severe spring drought. Sharpe and Jernstedt (1990)
reported that 14% of Danaea sporophytes died prior to maturation.
Plants that did not develop fully were divided into two categories, those that exhibited some visible form of damage and those in which development was arrested for unknown reasons. Plants that were visibly damaged either by herbivores, mechanical abrasion, or diseases may or may not have completed development depending on the extent of the damage. Herbivory is common in moonworts (Montgomery, 1990
; Johnson-Groh and Farrar, 1993
, 1996b
; Kelly, 1994
; Lesica and Ahlenslager, 1996
). Montgomery (1990)
noted herbivory ranged from 12 to 91%. Damage in our study varied from a small amount of trophophore or sporophore tissue removed to the extreme of being totally eaten, leaving only a short stump. Whereas modest herbivory usually left the sporophore or trophophore apparently functional, diseased plants were generally wilted or rotted at the soil surface. A few abnormally developed plants appeared to be the result of mechanical damage. Diseased and abnormal plants generally did not contribute to the spore bank.
Many plants with no visible damage failed to complete development. Arrested development probably occurred due to inadequate resources (light, water, mycorrhizae, time), belowground herbivory, or disease. These plants were similar to those with visible damage, contributing no spores to the spore bank.
In addition to differences in the proportion of damaged to undamaged plants between the two species, there were also differences as to when the damage occurred. Damage to most B. gallicomontanum appeared late in the season at the time of spore release (Fig. 11), whereas damage to B. mormo occurred throughout the season span of the plants (Fig. 12). This may be due to the emergence of B. gallicomontanum concurrently with snowmelt when there are fewer active insect herbivores or disease pathogens, and the increased damage at the end of the season may be due to increased insect and pathogen activity and decreasing soil moisture. Herbivore and disease damage in B. mormo were observed equally throughout all stages. The habitat of B. mormo is relatively homogeneous during the summer season with no obvious limitations for herbivores or pathogens.
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Gehring and Potash (1996)
attempted to correlate spore contribution with plant height. They noted that height was a good estimator of the spore component of fitness and consequently that the overall height of a plant was an easy assessment of the plants' general health. This contradicts findings in this study in which almost half of the plants that did not produce spores were of normal size and had no visible evidence of damage. Height alone is not an adequate predictor of spore set; what appear to be normal healthy plants do not always set spores.
In many flowering plants and ferns, age often correlates with height; the smaller plants are the youngest and the larger plants, the oldest. Applying size–age correlations to Botrychium is problematic. For Botrychium it is clear that comparisons of plant sizes are valid only for plants in the same stage of development. Size comparisons between years may likewise be misleading. During the separation stage B. gallicomontanum and B. mormo increased 12 and 30% (mean of trophophore and sporophore size), respectively, in size during a period of 27 and 22 d.
Population variation and management
Populations observed in this study were compared with annual monitoring results gathered by Johnson-Groh from 1989 to 2001 (Fig. 13). Several conclusions can be drawn regarding annual variation and the timing of monitoring. First, as others have shown, Botrychium population sizes vary greatly from year to year (Montgomery, 1990
; Muller, 1992
, 1993
; Johnson-Groh and Farrar, 1993
; Lesica and Ahlenslager, 1996
). This annual variation is due to many complex environmental and demographic factors. For example, drought has a significant impact on Botrychium as noted by Mueller (1992)
who found that B. matricariifolium is very sensitive to long periods of water deficits in May. Drought and earthworm invasion (Mortensen and Mortensen, 1998
; Groffman et al., 2000
) are the probable factors responsible for the large recent decline in B. mormo populations (Fig. 13).
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Third, and most importantly, all of these Botrychium studies have employed permanent plots to represent a sample of the population from which one can make size estimates. If samples are taken at a time when the population is senescing, a false estimate of the population size may be deduced. This was the case for B. mormo, which had previously been sampled late in the season after the population had declined. This late date had been selected because of the visibility of plants late in the season and literature reports (Wagner and Wagner, 1981
). Indeed, as noted above, the largest plants, which emerge above the litter, are present late in the season. However, the population size at the end of the season is approximately half the peak mid-season population size for B. mormo.
Peak population sizes are sustained for a longer period in B. gallicomontanum than in B. mormo. Consequently there is a longer opportunity to get an accurate population size estimate of B. gallicomontanum. To accurately estimate population sizes for B. mormo, censuses must be done in mid-July and for B. gallicomontanum, in early to mid-June.
Knowledge of phenology can be applied to the management of the habitats in which these ferns are found. Previous studies on the effect of prescribed prairie fires have been conducted in Iowa and Minnesota on a related species, B. campestre (Johnson-Groh and Farrar, 1996a
). Burning generally did not harm the plants, and individual plants that were scorched often returned the following year with increased vigor. However, fire followed by excessive drought or erosion (both natural results of fire) was found to be harmful to B. campestre. Burning B. gallicomontanum early in the season prior to full emergence predictably would have a relatively minor impact on the population. Repeated late-spring burns are more likely to significantly impact the plants through reduced spore set and through increased exposure of the soil to desiccation. Knowing the phenology of B. gallicomontanum helps to ensure that conclusions with regard to fire management are as accurate as possible.
Timber harvest is the greatest anthropogenic threat to forest species. No studies have yet been completed on the impact of timber harvest on forest Botrychium. It seems plausible that similar to fire, timber harvest will affect the microhabitat of B. mormo in many ways, including opening the canopy, changes in soil moisture and mycorrhizae, compaction, etc. Harvest in July would have the greatest impact on B. mormo. Long-term studies are needed on the impact of timber harvest management on rare forest Botrychium.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Ash J. 1987 Demography of Cyathea hornei (Cyatheaceae), a tropical tree-fern in Fiji. Australian Journal of Botany 35: 331-342
Braggins J. E. 1980 Some studies on the New Zealand species of Botrychium SW. (Ophioglossaceae). New Zealand Journal of Botany 18: 353-366
Farrar D. R. C. L. Johnson-Groh 1986 Distribution, systematics and ecology of Botrychium campestre, the prairie moonwort. Missouriensis 7: 51-58
Farrar D. R. C. L. Johnson-Groh 1990 Subterranean sporophytic gemmae in moonwort ferns, Botrychium subgenus Botrychium. American Journal of Botany 77: 1168-1175[CrossRef][ISI]
Farrar D. R. C. L. Johnson-Groh 1991 A new prairie moonwort (Botrychium subgenus Botrychium) from northwestern Minnesota. American Fern Journal 81: 1-6
Gehring J. L. L. Potash 1996 1995 Survey of the Nooksack Botrychium. Report to the Mt. Baker-Snoqualmie National Forest. Mt. Baker-Snoqualmie National Forest, Mountlake Terrac, Washington, USA
Groffman P. M. P. J. Bohlen T. J. Fahey M. C. Fish 2000 Invasion of north temperate forest soils by exotic earthworms. Research Report. Institute of Ecosystem Studies. Millbrook, New York. www.ecostudies.org/research/reports/grofrep2.html
Johnson-Groh C. L. 1998 Population demographics, underground ecology and phenology of Botrychium mormo. In N. Berlin, P. Miller, J. Borovansky, U. S. Seal, and O. Byers, [eds.], Population and habitat viability assessment (PHVA) for the goblin fern (Botrychium mormo), Final Report, 103–108. Conservation Biology Specialist Group, Apple Valley, Minnesota, USA
Johnson-Groh C. L. D. R. Farrar 1993 Population dynamics of prairie moonworts (Botrychium subgenus Botrychium) in Iowa and Minnesota. American Journal of Botany 80: 109 (Abstract)
Johnson-Groh C. L. D. R. Farrar 1996a The effects of fire on prairie moonworts (Botrychium subgenus Botrychium). American Journal of Botany 83: 134 (Abstract)
Johnson-Groh C. L. D. R. Farrar 1996b Effects of leaf loss on moonwort ferns (Botrychium subgenus Botrychium). American Journal of Botany 83: 127 (Abstract)
Kelly D. 1994 Demography and conservation of Botrychium australe, a peculiar, sparse mycorrhizal fem. New Zealand Journal of Botany 32: 393-400
Lesica P. K. Ahlenslager 1996 Demography and life history of three sympatric species of Botrychium subg. Botrychium in Waterton Lakes National Park, Alberta. Canadian Journal of Botany 74: 538-543
Minnesota Department of Natural Resources. 2002 Minnesota's list of endangered, threatened and special concern species. St. Paul, Minnesota. http://www.dnr.state.mn.us/fish_and_wildlife/endangered_species/
Montgomery J. D. 1990 Survivorship and predation changes in five populations of Botrychium dissectum in Eastern Pennsylvania. American Fern Journal 80: 173-182[CrossRef]
Mortensen S. C. Mortensen 1998 A new angle on earthworms. Minnesota Volunteer 61: 20-29
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Muller S. 1993 Population dynamics in Botrychium matricariifolium in Bitcherland (Northern Vosges Mountains, France). Belgian Journal of Botany 126: 13-19
Odland A. 1995 Frond development and phenology of Thelypteris limbosperma, Athyrium distentifolium, and Matteuccia strutuiopteris in western Norway. Nordic Journal of Botany 15: 225-236
Sato T. 1982 Phenology and wintering capacity of sporophytes and gametophytes of ferns native to northern Japan. Oecologia 55: 53-61
Sato T. 1985a Comparative life history of five Hokkaido Polystichum ferns with reference to leaf development in relation to altitudinal distribution. Botanical Magazine of Tokyo 98: 99-111
Sato T. 1985b Comparative life history of Aspidiaceous ferns in northern Japan with reference to fertility during sporophyte development in relation to habitats. Botanical Magazine of Tokyo 98: 371-381
Sato T. 1986 Life history characteristics of Polystichum tripteron with special reference to its leaf venation. Botanical Magazine of Tokyo 99: 361-377
Seiler R. L. 1981 Leaf turnover rates and natural history of the Central American tree fern Alsophilia salvinii. American Fern Journal 71: 75-81[CrossRef]
Seiler R. L. 1995 Verification of estimated growth rates in the tree fern Alsophilia salvinii. American Fern Journal 85: 96-97[CrossRef]
Sharpe J. M. 1993 Plant growth and demography of the neotropical herbaceous fern Danaea wendlandii (Marattiaceae) in a Costa Rican rain forest. Biotropica 25: 85-94[CrossRef][ISI]
Sharpe J. M. 1997 Leaf growth and demography of the rheophytic fern Thelypteris angustifolia (Willdenow) Proctor in a Puerto Rican rainforest. Plant Ecology 130: 203-212
Sharpe J. M. J. Jernstedt 1990 Leaf growth and phenology of the dimorphic herbaceous layer fern Danaea wendlandii (Marattiaceae) in a Costa Rican rain forest. American Journal of Botany 77: 1040-1049[CrossRef][ISI]
Simard S. W. D. A. Perry M. D. Jones D. D. Myrold D. M. Durall R. Molina 1997 Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388: 579-582[CrossRef]
Smith S. E. D. J. Read 1997 Mycorrhizal symbiosis, 2nd ed. Academic Press, New York, New York, USA
Tanner E. V. J. 1983 Leaf demography and growth of the tree-fern Cyathea pubescens Mett. Ex Kuhn in Jamaica. . Botanical Journal of the Linnean Society 87: 213-227
Wagner W. H. F. S. Wagner 1977 Fertile-sterile leaf dimorphy in ferns. Gardens Bulletin Singapore 30: 251-267
Wagner W. H. F. S. Wagner 1981 New species of moonworts, Botrychium subg. Botrychium (Ophioglossaceae), from North America. American Fern Journal 71: 20-30[CrossRef]
Whittier D. 1981 Spore germination and young gametophyte development of Botrychium and Ophioglossum in axenic culture. American Fern Journal 71: 13-19[CrossRef]
Wilmot A. 1989 The phenology of leaf life spans in woodland populations of the fern Dryopteris filix-mas (L.) Schott and D. dilatata (Hoffm.) A. Gray in Derbyshire. Botanical Journal of the Linnean Society 99: 387-395
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