Botrychium pallidum - W.H. Wagner
Pale Moonwort
Taxonomic Status: Accepted
Related ITIS Name(s): Botrychium pallidum W.H. Wagner (TSN 506848)
French Common Names: botryche pâle
Unique Identifier: ELEMENT_GLOBAL.2.154737
Element Code: PPOPH01130
Informal Taxonomy: Plants, Vascular - Ferns and relatives
 
Kingdom Phylum Class Order Family Genus
Plantae Filicinophyta Ophioglossopsida Ophioglossales Ophioglossaceae Botrychium
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Concept Reference
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Concept Reference: Kartesz, J.T. 1994. A synonymized checklist of the vascular flora of the United States, Canada, and Greenland. 2nd edition. 2 vols. Timber Press, Portland, OR.
Concept Reference Code: B94KAR01HQUS
Name Used in Concept Reference: Botrychium pallidum
Taxonomic Comments: First described in 1990, from plants formerly identified as B. minganense.
Conservation Status
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NatureServe Status

Global Status: G3
Global Status Last Reviewed: 18Jun2008
Global Status Last Changed: 26Oct2001
Rounded Global Status: G3 - Vulnerable
Reasons: This small, inconspicuous species has a broad but disjunct range including eastern Maine and eastern Quebec, the upper Midwest/Great Lakes region, the Black Hills (SD and WY), the Rocky Mountains, northwestern Montana and adjacent Alberta, central Alberta, and Saskatchewan; also historically known from Manitoba. Nearly 100 occurrences have been documented, but the vast majority of these contain small numbers of aboveground plants; median occurrence size is 5-9 plants and the total population may not be more than about 2500 individuals. Additional occurrences are expected to be found with continued inventory; the species' range may be more continuous than our present knowledge indicates. The primary threat appears to be successional overgrowth of habitat; habitat encroachment due to development, agriculture, and recreation is also a concern.
Nation: United States
National Status: N3
Nation: Canada
National Status: N2 (17Sep2010)

U.S. & Canada State/Province Status
United States Maine (S1), Michigan (S3), Minnesota (S1), Montana (S1S2), South Dakota (S2S3), Wisconsin (S1), Wyoming (S1)
Canada Alberta (S1), Manitoba (SH), Ontario (S1), Quebec (S1S2), Saskatchewan (S1)

Other Statuses

Committee on the Status of Endangered Wildlife in Canada (COSEWIC): Candidate (Medium) (26Jan2015)

NatureServe Global Conservation Status Factors

Range Extent Comments: The range of Botrychium pallidum is broad but highly disjunct. It occurs in eastern Maine (Washington County) and eastern Quebec (e.g. Bic and Forillon Federal Park, Gaspé County), in the upper Midwest/Great Lakes region (from southeastern Michigan around the Lakes to the Upper Peninsula and southern Ontario, through northern Minnesota), in the Black Hills of South Dakota and Wyoming, throughout the Rocky Mountains in Colorado, in northwestern Montana and adjacent montane Alberta, as well as disjunctly in the dry mixedwood boreal forest of central Alberta, and in Saskatchewan. The sole known Manitoba occurrence is now considered historical (C. Foster pers. comm. 2008). A continuous range map was drawn following Johnston (2002) and Farrar (2005), for which the area was calculated to be approximately 1,850,000 km2 using GIS tools.

Area of Occupancy: 126-2,500 4-km2 grid cells
Area of Occupancy Comments: Using a 2 x 2 km grid, Area of Occupancy was calculated to be approximately 388 km2; this is likely a slight underestimate as Michigan and Saskatchewan occurrences are not individually mapped (these were estimated conservatively as one grid cell per county record).

Number of Occurrences: 21 - 300
Number of Occurrences Comments: Approximately 94 occurrences are currently believed extant, using conservative estimates for the number of occurrences in Michigan and Saskatchewan where they are not mapped individually. Of the 94 presumed extant occurrences, 44 are in Minnesota; all other jurisdictions have 6 or fewer. Notably, the 6 South Dakota occurrences were recently (2006) discovered in the Black Hills (identity confirmed by isozyme analysis, D. Farrar). Given the species' disjunct range and small, inconspicuous nature, it is highly likely that additional occurrences will be found with continued inventory effort (Chadde and Kudray 2001, Johnston 2002, Gilman 2004). Nevertheless, there may be fewer undiscovered occurrences for this species compared to some other Botrychium; Williston (2002) noted that "many new moonwort localities were documented during field survey... however, only two new locations were discovered among the rarest of these ferns (B. campestre in South Drywood Creek and B. pallidum in Elk Island National Park)...,which suggests that several species are truly rare and not merely overlooked." An additional 5 historical, 1 failed to find, and 2 unranked occurrences are also known.

Population Size Comments: Wagner is reported to have observed that where it occurred, this species was usually present in only small numbers but that occasional sizeable colonies were found (Mulligan 1999 cited in Chadde and Kudray 2001). This observation seems largely borne out by current occurrence data. A total of approximately 900-1550 aboveground plants have been counted at the various sites; extrapolating up to uncounted sites yields a total population estimate of 1500-2500+ aboveground plants rangewide. Most occurrences are quite small (median size of counted occurrences = 5-9 aboveground plants); the largest known occurrences include one with 100+ plants in Quebec, one with approx. 90 plants in South Dakota, the Maine occurrence with 60 plants, and five Minnesota occurrences with 40-60 plants each (one of these with approx. 400 plants one year). It has been noted that "plants are very small, very inconspicuous, and difficult to inventory at best" (Johnston 2002). For practical reasons, abundance is usually estimated by numbers of aboveground plants rather than by numbers of genetic individuals. However, counts of aboveground plants (mature sporophytes) are known to be an incomplete and inconsistent indicator of population size in Botrychium, because an unknown number of gametophytes, immature sporophytes, and dormant mature sporophytes exist underground. Studies on other Botrychium species have documented large annual fluctuations in the number of aboveground plants at a given site, without any apparent cause (Chadde and Kudray 2001).

Number of Occurrences with Good Viability/Integrity: Few (4-12)
Viability/Integrity Comments: Of 27 extant occurrences that have been ranked, one third (9 occurrences) have been assessed as having excellent or good viability. More than half of these (5) are newly-discovered South Dakota occurrences, with the others in Quebec, Colorado and Minnesota.

Overall Threat Impact: Medium
Overall Threat Impact Comments: The primary threat to B. pallidum appears to be loss of its open, grassy habitat to successional overgrowth, which is likely exacerbated by fire suppression. This species' preference for disturbed, open habitat may lead population viability to be dependent on a shifting mosaic of suitable sites opening for colonization, as occupied sites become overgrown and their generally small populations become vulnerable to local extinction (Chadde and Kudray 2001). Habitat encroachment due to development, agriculture, and recreation are also threats to B. pallidum and its habitat (USDA Forest Service 2000 cited in Chadde and Kudray 2001, Williston 2002). In Quebec, the species is locally threatened by riverine erosion in addition to canopy closure (J. Labrecque pers. comm. 2008). Prolonged drought can be a threat in some areas, as water relations are important to moonworts and their supporting mycorrhizae; moonworts are known not to appear above ground in hot dry years (Chadde and Kudray 2001, Johnston 2002). It is also possible though somewhat unlikely that exotic earthworms are a threat to B. pallidum; this threat is known to impact only B. mormo thus far, which occurs in the habitats most likely to be affected (i.e. those with a thick organic surface layer, in contrast to the open, disturbed habitats apparently preferred by B. pallidum) Chadde and Kudray 2001).

Short-term Trend: Relatively Stable (<=10% change)
Short-term Trend Comments: Appears relatively stable in many parts of the range, e.g. Quebec (J. Labrecque pers. comm. 2008). Johnston (2002) also notes that the disturbed habitats seemingly favored by this species are themselves relatively stable on the landscape, in that sites disturbed by human activities are roughly balancing sites lost through increases in forest cover through protection from fire. However, it is important to note that habitat created by anthropogenic disturbance has not yet been proven to support viable Botrychium populations in the long-term.

Long-term Trend: Unknown
Long-term Trend Comments: Just 5 occurrences are currently believed to be historical (with 1 additional failed to find). However, this species was only described in 1990, and more information is required to understand the total numbers of historical/extirpated vs. still extant occurrences rangewide.

Intrinsic Vulnerability Comments: Vulnerable to increased shade. All Botrychium species are believed to be obligately dependent on mycorrhizal relationships in both the gametophyte and sporophyte generations (Chadde and Kudray 2001). This relationship is important to many aspects of Botrychium ecology; mycorrhizae appear to be a key determinant of Botrychium establishment, distribution, and abundance (Chadde and Kudray 2001). In Botrychium, spores persist in the soil for several years and, along with underground gametophytes and developing sporophytes, form a somewhat buffered population that can rebound from unfavorable years, as long as the sporophytes are not destroyed (Chadde and Kudray 2001).

Environmental Specificity Comments: Habitat moisture balance appears to be important to moonworts and their supporting mycorrhizae (Chadde and Kudray 2001).

Other NatureServe Conservation Status Information

Distribution
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Global Range: The range of Botrychium pallidum is broad but highly disjunct. It occurs in eastern Maine (Washington County) and eastern Quebec (e.g. Bic and Forillon Federal Park, Gaspé County), in the upper Midwest/Great Lakes region (from southeastern Michigan around the Lakes to the Upper Peninsula and southern Ontario, through northern Minnesota), in the Black Hills of South Dakota and Wyoming, throughout the Rocky Mountains in Colorado, in northwestern Montana and adjacent montane Alberta, as well as disjunctly in the dry mixedwood boreal forest of central Alberta, and in Saskatchewan. The sole known Manitoba occurrence is now considered historical (C. Foster pers. comm. 2008). A continuous range map was drawn following Johnston (2002) and Farrar (2005), for which the area was calculated to be approximately 1,850,000 km2 using GIS tools.

U.S. States and Canadian Provinces
Color legend for Distribution Map

U.S. & Canada State/Province Distribution
United States ME, MI, MN, MT, SD, WI, WY
Canada AB, MB, ON, QC, SK

Range Map
No map available.


U.S. Distribution by County Help
State County Name (FIPS Code)
MN Aitkin (27001), Becker (27005), Beltrami (27007), Cass (27021), Cook (27031), Crow Wing (27035), Itasca (27061), Koochiching (27071), Lake (27075), Lake of the Woods (27077), Polk (27119), Roseau (27135), St. Louis (27137)
SD Custer (46033), Lawrence (46081), Pennington (46103)
WI Bayfield (55007)
WY Crook (56011)
* Extirpated/possibly extirpated
U.S. Distribution by Watershed Help
Watershed Region Help Watershed Name (Watershed Code)
04 Baptism-Brule (04010101)+, Beaver-Lester (04010102)+, St. Louis (04010201)+, Beartrap-Nemadji (04010301)+, Lake Superior (04020300)+
07 Mississippi Headwaters (07010101)+, Leech Lake (07010102)+, Prairie-Willow (07010103)+, Elk-Nokasippi (07010104)+, Pine (07010105)+, Snake (07030004)+
09 Otter Tail (09020103)+, Red Lakes (09020302)+, Thief (09020304)+, Clearwater (09020305)+, Roseau (09020314)+, Rainy Headwaters (09030001)+, Vermilion (09030002)+, Little Fork (09030005)+, Big Fork (09030006)+, Rapid (09030007)+, Lower Rainy (09030008)+, Lake of the Woods (09030009)+
10 Middle Cheyenne-Spring (10120109)+, Rapid (10120110)+, Upper Belle Fourche (10120201)+, Redwater (10120203)+
+ Natural heritage record(s) exist for this watershed
* Extirpated/possibly extirpated
Ecology & Life History
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Basic Description: A small (10-15 cm) perennial fern that produces a leaf (trophophore) with a waxy-appearing, pale-green to whitish blade that is dissected, more-or-less folded longitudinally, and up to 4 cm long. A longer, spore-bearing spike (sporophore) arises from the common stalk; this portion is typically 2-4 times the length of the sterile leaf. Leaves appear late spring-early summer. Gametophytes are subterranean and mycorrhizal.
General Description: A small perennial fern with a single aboveground frond less than 15 cm tall, with a waxy, pale whitish green color, and divided into two segments that share a common stalk. The sterile segment is once pinnatifid and has up to 5 pairs of fanshaped pinnae, 2-3 mm long, with concave sides. Each of the pinnae tends to form two lobes, the upper one cleft and larger than the lower. The sterile segment is shaped like a trough along the central axis. The fertile segment is longer than the sterile segment, branched, and bears grape-like sporangia. Leaves appear in late spring to early summer. Spores germinate underground and develop into subterranean gametophytes.
Technical Description: Trophophore stalk 2 - 8 mm, 0 - 1/5 length of trophophore rachis. Trophophore blade more or less longitudinally folded and trough-like when alive, narrowly oblong, 1-pinnate, up to 4 x 1 cm; blade glaucous, pale green to whitish, herbaceous. The pinnae approximate, ascending, up to 5 pairs, small (2-3 mm) flabellate; distance between 1st and 2nd pinnae not or slightly more than between 2nd and 3rd pairs; basal pinna pair approximately equal in size and cutting to adjacent pair, fan-shaped, strongly asymmetric, lobed to divided to tip; basal or both sides of pinnae deeply concave, broadly attached, the larger ones ascending and strongly asymmetrical, often split into 2 unequal lobes, the upper one cleft and larger than the lower, apex rounded, venation like ribs of fan, midrib absent; outer margins entire to irregularly crenulate-denticulate. Sporophores 1-2-pinnate, 1.5-4 times length of trophophore, lower sporophore pinnae with a large or small branch. Spore diameter 23-28 µm; 2n = 90 (Wagner and Wagner 1990, Flora of North America 1993).
Diagnostic Characteristics: Most easily confused with B. minganense, especially small, sun-grown B. minganense plants. Can be distinguished from B. minganense by (1) its pale green to silvery gray-green or whitish color (although this character may not persist in collected plants), (2) its smaller size, including pinnae only 2-3 mm long compared to the 4-6 mm in B. minganense, (3) its pinna sides concave throughout and most strongly so near their juncture with the outer margin, giving the pinna a mushroom shape, compared to of B. minganense pinnae which are concave near the rachis but are more or less straight along the pinna blade, (4) its folded trophophore blade compared to the flat trophophore blade of B. minganense, and (5) its often unevenly divided outer pinna margins and basal sporophore branches, with the upper lobe longer and broader than the lower lobe; outer pinna margins of B. minganense are entire, or if lobed, symmetrically so, and the basal branches of the sporophore are symmetrically branched. Can be distinguished from B. gallicomontanum by its longer trophophore and sporophore stalks; in B. gallicomontanum, the sporophore stalk is typically less than half the length of the trophophore. Also, the pinnae lobes of B. gallicomontanum are more spreading and linear than those of B. pallidum. Can be distinguished from B. ascendens by its distinctive pinnae folding and outer margins as well; pinna of B. ascendens are wedge-shaped with little curvature in the side margins and outer margins are dentate or cleft symmetrically into spreading lobes. Spores of B. pallidum are much smaller than those of B. minganense, B. gallicomontanum, or B. ascendens. B. pallidum is also one of only four moonwort species that commonly produce dense clusters of minute, spheric gemmae at the root bases (Flora of North America 1993, Chadde and Kudray 2001, Farrar 2005).
Palustrine Habitat(s): Riparian, TEMPORARY POOL
Terrestrial Habitat(s): Forest - Conifer, Forest - Hardwood, Forest Edge, Forest/Woodland, Grassland/herbaceous, Old field, Sand/dune, Woodland - Conifer
Habitat Comments: Habitat preferences appear to be somewhat general. Most often found in open habitats of sparse to dense herbaceous vegetation, such as grasslands (e.g. fescue grasslands in valleys). open meadows and fields. sand dunes, sand hills, sandy ridges, oak barrens, open exposed hillsides, and clifftops. Occasionally found in partial shade of open-canopy forests (or in disturbed sites of more closed-canopy forests), including mixed hardwood forest, maple/basswood forest, subalpine fir-Engelmann spruce forest, and red and jack pine communities. Many areas where found have been affected by disturbance; sites kept open due to regular disturbance regimes (e.g. fire, cattle grazing, persistent native ungulate browsing) appear particularly suitable. Disturbed habitats where found include burned or cleared areas, roadsides, grassy ditches, old logging landings and roads, vacant lots, old mining sites, and old fields. Also occasionally known from wetlands, including ephemeral ponds, streamside areas, and high-elevation subalpine forest wetlands. Often associated with other moonworts (Botrychium sp.) such as B. simplex, B. matricariifolium, B. hesperium, B. paradoxum, B. gallicomontanum, B. minganense, B. adnatum, B. pedunculosum, B. ascendens, B. lanceolatum, B. lunaria, B. crenulatum, B. spathulatum, and/or B. michiganense, and/or with Virginia strawberry (Fragaria virginiana). 0 - 3230 m.
Economic Attributes Not yet assessed
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Management Summary
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Stewardship Overview: Given the general preference of the species for open, somewhat disturbed sites, management activities that reduce canopy cover (e.g. prescribed burning, cattle, or removal of woody vegetation) may be desirable, although no specific information regarding this species' response to management is available. Williston (2002) notes observational evidence that it may not be possible to rely upon anthropogenic disturbance for the preservation of all rare moonworts; strategies with the highest chance of success will therefore be those that maintain natural disturbance processes, which requires preserving ecosystem integrity. Given the importance of mycorrhizal relationships for this species, those relationships should be taken into account as well in the development of management plans. However, the ability to do this is currently hampered by lack of knowledge regarding the details of this important relationship.
Population/Occurrence Delineation
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Minimum Criteria for an Occurrence: Any natural occurrence of one or more plants. The number of above ground stems does not necessarily indicate the number of plants in the population, however, because a root base may not send up a stem every year. An Element Occurrence is therefore described by the highest number of aboveground plants in the population over a five-year period. (This number may still not provide an accurate estimate of the total population size.) Because little genetic variability exists within Botrychium species (Farrar pers. comm. 1995), the number of genetic individuals is not a factor in ranking Element Occurrences. Botrychium pallidum, in particular, reproduces both sexually and vegetatively via minute gemmae that are clustered densely at the root bases.
Date: 27Sep2000
Author: Spackman, S. and D. Anderson
Population/Occurrence Viability
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Excellent Viability: Size: The population numbers 100 or more aboveground plants at some point during a 5-year period (based on available EOR data). Condition: The habitat is generally a large, open, grassy field maintained by a disturbance element, such as fire or erosion. Successional plant species have not invaded these open areas. The occurrence should have an excellent likelihood of long-term viability (successful sporophore production is observed indicating that the reproductive mechanisms are intact). This occurrence should be in a high-quality site (i.e. less than 1% cover exotic plant species and/or no significant human disturbances). Landscape Context: the occurrence is surrounded by an area that is unfragmented and includes the ecological processes and natural disturbance regime needed to sustain this species. The presence of an appropriate disturbance regime and the lack of a closed canopy are requirements for this species.
Good Viability: Size: The population numbers 10 to 99 aboveground plants at some point during a 5-year period (based on available EOR data). Condition: The habitat is generally a moderate-to-large, open, grassy field maintained by a disturbance element, such as fire, an eroding slope, or a few cattle. Successional overgrowth may have invaded small portions of the open area. The occurrence should have a good likelihood of long-term viability (successful sporophore production is observed indicating that the reproductive mechanisms are intact) with little human disturbance. If exotic species are present, they comprise less than 10% of the total ground cover. Landscape Context: the surrounding landscape should contain the ecological processes and natural disturbance regime needed to sustain this species but may be fragmented and/or impacted by humans.
Fair Viability: Size: The population consists of a few (generally less than 10) aboveground stems each year (based on available EOR data). Condition: The habitat is a fairly-open, grassy area partially maintained by a disturbance element, such as fire, an eroding slope, or cattle. Successional overgrowth may have shaded significant sections of the open area. The occurrence may be less productive than the above situations, but is still viable (with successful sporophore production observed indicating that the reproductive mechanisms are intact). The occupied habitat is somewhat degraded (exotic plant species make up between 10-50% of the total ground cover and/or there is a moderate level of human disturbance). Landscape Context: there may be significant human disturbance, but the ecological processes and natural disturbance regime needed to sustain the species are still intact.
Poor Viability: Size: Only 1 or 2 above ground plants (based on available EOR data). Condition: The habitat is a previously-open area now succeeding to woody vegetation, which shades out Botrychium pallidum. Or, the habitat may be an open area but over-trampled by more cattle than are necessary to maintain the open field. Little or no evidence of successful reproduction is observed (poor sporophore production or herbivory resulting in sporophore removal). Exotic plant species make up greater than 50% of the total ground cover, and/or there is a significant level of human disturbance. Landscape context: the surrounding area is fragmented with many ecological processes or the necessary natural disturbance regime no longer intact. The occurrence has a low probability of long-term persistence due to inbreeding depression, natural stochastic events, and its intrinsic vulnerability to human impacts.
Justification: A Rank: Very little is known about the population biology of this species (and all other Botrychium species). Large populations in high quality sites are presumed to contain a high degree of genetic variability, have a low susceptibility to the effects of inbreeding depression, and to be relatively resilient. Because Botrychium species do not produce aboveground biomass every year, the EO rank is based on the highest number of individuals observed within a five year period.

C Rank: EOs not meeting "C"-rank criteria are likely to have a very high probability of inbreeding depression and extirpation due to natural stochastic processes and/or occur in degraded habitat with low long-term potential for survival.

Key for Ranking Species Element Occurrences Using the Generic Approach (2008).
Date: 27Sep2000
Author: Spackman, S. and D. Anderson
Notes: COHP
U.S. Invasive Species Impact Rank (I-Rank) Not yet assessed
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Authors/Contributors
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NatureServe Conservation Status Factors Edition Date: 26Oct2001
NatureServe Conservation Status Factors Author: K. Crowley, MRO, rev. Spackman, S. and D. Anderson (2000), rev. L. Morse (2001), rev. K. Gravuer (2008)

Botanical data developed by NatureServe and its network of natural heritage programs (see Local Programs), The North Carolina Botanical Garden, and other contributors and cooperators (see Sources).

References
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Citation for Bird Range Maps of North America:
Ridgely, R.S., T.F. Allnutt, T. Brooks, D.K. McNicol, D.W. Mehlman, B.E. Young, and J.R. Zook. 2003. Digital Distribution Maps of the Birds of the Western Hemisphere, version 1.0. NatureServe, Arlington, Virginia, USA.

Acknowledgement Statement for Bird Range Maps of North America:
"Data provided by NatureServe in collaboration with Robert Ridgely, James Zook, The Nature Conservancy - Migratory Bird Program, Conservation International - CABS, World Wildlife Fund - US, and Environment Canada - WILDSPACE."

Citation for Mammal Range Maps of North America:
Patterson, B.D., G. Ceballos, W. Sechrest, M.F. Tognelli, T. Brooks, L. Luna, P. Ortega, I. Salazar, and B.E. Young. 2003. Digital Distribution Maps of the Mammals of the Western Hemisphere, version 1.0. NatureServe, Arlington, Virginia, USA.

Acknowledgement Statement for Mammal Range Maps of North America:
"Data provided by NatureServe in collaboration with Bruce Patterson, Wes Sechrest, Marcelo Tognelli, Gerardo Ceballos, The Nature Conservancy-Migratory Bird Program, Conservation International-CABS, World Wildlife Fund-US, and Environment Canada-WILDSPACE."

Citation for Amphibian Range Maps of the Western Hemisphere:
IUCN, Conservation International, and NatureServe. 2004. Global Amphibian Assessment. IUCN, Conservation International, and NatureServe, Washington, DC and Arlington, Virginia, USA.

Acknowledgement Statement for Amphibian Range Maps of the Western Hemisphere:
"Data developed as part of the Global Amphibian Assessment and provided by IUCN-World Conservation Union, Conservation International and NatureServe."

NOTE: Full metadata for the Bird Range Maps of North America is available at:
http://www.natureserve.org/library/birdDistributionmapsmetadatav1.pdf.

Full metadata for the Mammal Range Maps of North America is available at:
http://www.natureserve.org/library/mammalsDistributionmetadatav1.pdf.

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