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Journal ArticleDOI

A new species of springsnail ( Pyrgulopsis ) from the Owyhee River Basin, Nevada

02 Jul 2012-Western North American Naturalist (Brigham Young University)-Vol. 72, Iss: 1, pp 21-31

TL;DR: A new springsnail species, Pyrgulopsis cybele, from the Owyhee River basin (northwestern Nevada), is described based on morphologic and molecular evidence and suggests that it evolved subsequent to emplacement of the Miocene basalt that carpets the upper South Fork Owyhea basin.

Abstract. We describe a new springsnail species, Pyrgulopsis cybele , from the Owyhee River basin (northwestern Nevada) based on morphologic and molecular (mtCOI) evidence. Pyrgulopsis cybele differs from other members of its genus in its unique pattern of penial ornament, which consists of small glands on the distal edge of the penial lobe, base of the penial filament, and outer edge of the medial section of the penis. It is further differentiated from regional congeners by its thickened inner-shell lip and mtCOI sequences. A Bayesian analysis based on COI data placed P. cybele in a well-supported clade that contained congeners from Snake River, Great Basin, Colorado River, and California Pacific Coastal drainages; the sister taxon of this new species was not resolved. The COI divergence of P. cybele relative to its most genetically similar congener (P. glandulosa) suggests that it evolved subsequent to emplacement of the Miocene basalt that carpets the upper South Fork Owyhee basin. Pyrgulopsis cybele w...

Topics: Pyrgulopsis (59%)

Summary (2 min read)

Introduction

  • Four Pyrgulopsis species have been previously reported from the Owyhee River watershed, a remote and rugged subunit of the Snake River basin that occupies ca. 10,950 mi2 (28,360 km2; Hardy et al. 2004) in Idaho, Nevada, and Oregon (Hershler 1998, Hershler and Liu 2009).
  • They may be threatened by livestock grazing and human disturbance.
  • Se colectó P. cybele de dos manantiales cercanos entre sí a lo largo del Río South Fork Owyhee y por debajo del cruce del gaseoducto de Nevada (Nevada Pipeline Crossing).
  • The authors also evalu - ate the phylogenetic relationships of this species and discuss its conservation status.

METHODS

  • Specimens were relaxed with menthol crystals and fixed in dilute formalin for anatomical study.
  • Sample information and GenBank accession numbers for the se - quenced specimens utilized in this study are in Table 1.
  • Preliminary molecular phylogenetic analyses, which included most of the currently recognized species of Pyrgulopsis, consistently positioned the novelty described herein in a clade with 9 other congeners.
  • Three runs were conducted in MrBayes using the General Time Reversible model (GTR + G) selected by MrModeltest and the default random tree option to determine when the log-likelihood sum reached a stable value (by plotting the log-likelihood scores of sample points against generation time).

SYSTEMATIC DESCRIPTION

  • Family Hydrobiidae Troschel, 1857 Subfamily Nymphophilinae Taylor, 1966 Genus Pyrgulopsis Call and Pilsbry, 1886 Type species: Pyrgula nevadensis Stearns, 1883, by origi - nal designation.
  • Lateral tooth face rectangular, angled; central cusp pointed (Fig. 3C), sometimes bifurcate; lateral cusps 2–3 , 3–5 ; wing medium width, variably flexed, about 200% length of cutting edge; basal tongue variably developed.
  • Bursa copulatrix small, ovate, horizontal, largely overlapped by albumen gland.

HOLOTYPE, USNM 1148155

  • Found in several other springs that were surveyed during the first author’s kayak trip down the South Fork Owyhee River (from the Nevada Pipeline crossing to Three Forks) in June 2009.
  • REMARKS.—This nymphophiline snail is as - signed to Pyrgulopsis based on the superficial position of the bursa copulatrix and bursal duct on the albumen gland, presence of a single seminal receptacle, and diffuse pattern of mantle pigmentation (per Liu and Hershler 2005:296).
  • Pyrgulopsis cybele is distinguished from all other congeners by its unique pattern of penial orna ment consisting of small glandular units on the distal edge of lobe (terminal gland), base of the filament (penial gland), and outer edge of the medial section of the penis (Dg1; see Hershler and Sada 2002 for a discussion of penial variation in this genus).
  • Owyhee basin congeners by its thickened inner shell lip, and mtCOI sequences (see below).
  • The 2 populations of P. cybele differed in shell size (Fig. 2A–2D), but were closely similar in all other morphologic details.

MOLECULAR ANALYSIS

  • The Bayesian analysis (Fig. 6) delineated specimens of P. cybele as a well-supported (100% posterior probability) lineage nested within a (well-supported) clade composed of congeners from the Snake River, Great Basin, Colorado River, and California Pacific Coastal drainages.
  • Pyrgulopsis intermedia and P. robusta formed a well-supported subgroup within this clade; the relationships of P. cybele and the other species were not well resolved.
  • Pyrgulopsis cybele differed from other congeners in - cluded in this analysis by 3.0%–7.4% sequence divergence.
  • Two of the haplotypes (I, II) were shared by both populations of these species.

DISCUSSION

  • The morphologically distinctive novelty de - scribed herein does not appear to be closely related to P. fresti, which is endemic to springs along a lower reach of the Owyhee River (Hershler and Liu 2009), or to the 3 congeners that are distributed in the Owyhee and other drainage basins.
  • This finding is consistent with molecular evidence that regional Pyrgulopsis faunas typically are composites of phylogenetically diverse lineages (Liu and Hershler 2005).
  • The springs inhabited by P. cybele discharge through Miocene basalt, which extensively carpets the South Fork Owyhee River watershed (Coats 1987, Foord et al. 1987: plate 1).
  • The small streams inhabited by this snail appeared to be in good condition when visited by RH, although he did not visit their headspring sources.
  • This reach of the South Fork Owyhee River watershed also may be im - pacted by human recreational activities (e.g., boating).

ACKNOWLEDGMENTS

  • This project was supported (in part) by funds provided by the Center for Biological Diversity, Oregon Natural Desert Association (ONDA), and Western Watersheds Project.
  • Brent Fenty (ONDA) was instrumental in helping to secure this funding.
  • The Bureau of Land Management (Vale District) provided additional logistical support that was facilitated by Shaney Rockefeller.
  • Chris Hansen, Dave Steele, and Dan Thomas provided a large amount of assistance in the field.
  • The authors thank 2 anonymous reviewers and WNAN editor Chris Walser for their constructive comments on a draft of this manuscript.

LITERATURE CITED

  • Use of formalin-preserved samples for molecular analysis.
  • United States Geological Survey Water-Resources Investigations Report 03-4327. 48 pp. HERSHLER, R. 1998.
  • New species and records of Pyrgulopsis (Gastropoda: Hydrobiidae) from the Snake River basin, southeastern Oregon: further delineation of a highly imperiled fauna.

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21
1
Department of Invertebrate Zoology, Smithsonian Institution, Box 37012, Washington, DC 20013-7012.
2
E-mail: hershlerr@si.edu
3
Department of Biology, Metropolitan State College of Denver, Denver, CO 80217.
Pyrgulopsis is a western North American
genus of hydrobiid gastropods that is distributed
from the Snake–Columbia River basin and Mis-
souri River headwaters to the lower Rio Grande
basin (Hershler et al. 2008: fig. 1). The tiny, gill-
breathing species in this genus typically live in
springs and have very small geographic ranges
(Hershler and Sada 2002). Pyrgulopsis contains
133 species (Hershler and Liu 2010, Hershler
et al. 2010), more than half of which (78 of 133,
58%) have been described since 1995. The actual
number of species in this genus is probably
considerably larger than currently recognized,
given that many putative novelties have not
been formally treated taxonomically (e.g., Frest
and Johannes 1995, Liu et al. 2003) and given
that much of the West still has not been sur-
veyed well for these tiny animals.
Four Pyrgulopsis species have been previ-
ously reported from the Owyhee River water-
shed, a remote and rugged subunit of the Snake
River basin that occupies ca. 10,950 mi
2
(28,360
km
2
; Hardy et al. 2004) in Idaho, Nevada, and
Oregon (Hershler 1998, Hershler and Liu 2009).
Three of these species (Pyrgulopsis fresti, Pyr-
gulopsis intermedia, and Pyrgulopsis owyheensis)
are distributed within a reach that extends from
slightly above Three Forks to slightly above
Owyhee Reservoir, Oregon; the fourth (Pyrgu-
lopsis sadai) is found in the East Little Owyhee
River drainage, Nevada (Fig. 1). In 2009 the
first author discovered a population of Pyrgu-
lopsis along the South Fork of the Owyhee
River near the Oregon–Nevada border >100 km
upflow from Three Forks (Fig. 1). A second,
closely proximal population was discovered in
Western North American Naturalist 72(1), © 2012, pp. 21–31
A NEW SPECIES OF SPRINGSNAIL (PYRGULOPSIS)
FROM THE OWYHEE RIVER BASIN, NEVADA
Robert Hershler
1,2
and Hsiu-Ping Liu
3
ABSTRACT.—We describe a new springsnail species, Pyrgulopsis cybele, from the Owyhee River basin (northwestern
Nevada) based on morphologic and molecular (mtCOI) evidence. Pyrgulopsis cybele differs from other members of its genus
in its unique pattern of penial ornament, which consists of small glands on the distal edge of the penial lobe, base of the penial
filament, and outer edge of the medial section of the penis. It is further differentiated from regional congeners by its
thickened inner-shell lip and mtCOI sequences. A Bayesian analysis based on COI data placed P. c y b e l e in a well-supported
clade that contained congeners from Snake River, Great Basin, Colorado River, and California Pacific Coastal drainages; the
sister taxon of this new species was not resolved. The COI divergence of P. c y b e l e relative to its most genetically similar con-
gener (P. g l a n d u l o s a ) suggests that it evolved subsequent to emplacement of the Miocene basalt that carpets the upper
South Fork Owyhee basin. Pyrgulopsis cybele was collected from 2 closely proximal springs along the South Fork Owyhee
River below the Nevada Pipeline Crossing. Although these populations are in a remote wilderness study area, they may be
threatened by livestock grazing and human disturbance.
RESUMEN.—Describimos una nueva especie de caracol de manantial, Pyrgulopsis cybele, de la cuenca del Río Owyhee
(al noroeste de Nevada), con base en evidencias morfológicas y moleculares (mtCOI). Pyrgulopsis cybele difiere de otros
miembros de su género debido a su ornamentación única en el pene, la cual consiste de pequeñas glándulas en el extremo
distal del lóbulo, en la base del filamento y en el extremo exterior de la sección media del pene. Se distingue aún más de
sus congéneres regionales debido a que el labio interno de la concha está engrosado y a las secuencias del gen mtCOI.
Un análisis Bayesiano basado en datos del COI (citocromo c oxidasa subunidad I) colocó a P. c y b e l e en un clado bien apoyado
que incluyó a congéneres del Río Snake, de la Gran Cuenca, del Río Colorado y de algunos ríos de la costa del Pacífico
en California; no se resolvió el taxón hermano de esta nueva especie. La divergencia en el COI de P. c y b e l e con respecto a su
congénere genéticamente más similar (P. g l a n d u l o s a ) sugiere que evolucionó posteriormente al asentamiento de basalto
del Mioceno que cubre la parte alta de la cuenca South Fork Owyhee. Se colectó P. c y b e l e de dos manantiales cercanos
entre sí a lo largo del Río South Fork Owyhee y por debajo del cruce del gaseoducto de Nevada (Nevada Pipeline Crossing).
A pesar de que estas poblaciones se encuentran en un área de estudio silvestre y remota, podrían estar siendo amenazadas
por la ganadería y por perturbaciones humanas.

2010. Here we describe these populations as a
new species of Pyrgulopsis based on morpho-
logical and molecular evidence. We also evalu -
ate the phylogenetic relationships of this species
and discuss its conservation status.
M
ETHODS
Specimens were relaxed with menthol crys-
tals and fixed in dilute formalin for anatomical
study. Snails used for mtDNA sequencing were
preserved in 90% ethanol in the field. Coordi-
nates for the collecting localities were obtained
in the field using a Garmin Oregon 450t GPS
unit (UTM NAD 83). Types for the new species
and other voucher material from this study were
deposited in the Smithsonian Institution’s Na -
tional Museum of Natural History (USNM)
collection.
Five females and 5 males (all adults) from
the type locality of the new species were dis-
sected; large series of males from both locali-
ties were examined to assess variation in penial
glandular ornament. Variation in the number of
cusps on the radular teeth was assessed using
the method of Hershler et al. (2007). Other meth -
ods of morphological study and descriptive
terminology are those used in recent taxonomic
22 WESTERN NORTH AMERICAN NATURALIST [Volume 72
Fig. 1. Map showing the distribution of Pyrgulopsis species in the Owyhee River basin. The arrow points to the area
inhabited by Pyrgulopsis cybele.

investigations of Pyrgulopsis (Hershler 1998,
Hershler et al. 2003a). Basic statistics were com-
piled for the shell data using Systat for Windows
11.00.01 (SSI 2004).
Genomic DNA was extracted from entire
snails using a CTAB protocol (Bucklin 1992). A
658 bp segment of cytochrome c oxidase sub-
unit I (COI) corresponding to “Folmer’s frag-
ment” (Folmer et al. 1994) was amplified and se -
quenced with primers LCO1490 and HCOI2198
following protocols of Liu et al. (2003). Se -
quences were determined for both strands and
then edited and aligned using Sequencherä
version 4.8. We sequenced 3–6 specimens from
the 2 samples of the new species described
herein to assess variation. Sample information
and GenBank accession numbers for the se -
quenced specimens utilized in this study are in
Table 1. The new sequences reported herein
were deposited in GenBank under accession
numbers JN255350–JN255358 (Table 1).
Sequence divergences (uncorrected p dis-
tances) were calculated using MEGA5.05 (Ta -
mura et al. 2011). Preliminary molecular phy-
logenetic analyses, which included most of the
currently recognized species of Pyrgulopsis,
consistently positioned the novelty described
herein in a clade with 9 other congeners. The
final analysis included all of these taxa and 2
congeners that belong to a different clade from
the northern Lahontan basin; one of these con -
geners (Pyrgulopsis gibba) was used as the root.
Phylogenetic relationships were inferred using
Bayesian inference in MrBayes 3.12 (Ronquist
and Huel senbeck 2003). MrModeltest (Nylan-
der 2004) selected the general time reversible
model (GTR + G), which best fit the data under
the Akaike information criterion. In the initial
Baye sian analysis, the burn-in was set at 10%
(10,000 generations) of the chain length (100,000
generations). Three runs were conducted in
MrBayes using the General Time Reversible
model (GTR + G) selected by MrModeltest and
the default random tree option to determine
when the log-likelihood sum reached a stable
value (by plotting the log-likelihood scores of
sample points against generation time). The ln
likelihoods started around –7550 and quickly
converged upon a stable value of about –1700
after 8000 generations. For the final run, Me -
tropolis-coupled Markov chain Monte Carlo
simulations were performed with 4 chains for
1,000,000 generations, and Markov chains were
sampled at intervals of 10 generations to obtain
100,000 sample points. The sampled trees with
branch lengths were used to generate a 50%
majority-rule consensus tree with the first 5000
trees (equal to 50,000 generations) removed to en -
sure that the chain sampled a stationary portion.
S
YSTEMATIC DESCRIPTION
Family Hydrobiidae Troschel, 1857
Subfamily Nymphophilinae Taylor, 1966
Genus Pyrgulopsis Call and Pilsbry, 1886
Type species: Pyrgula nevadensis Stearns, 1883, by origi -
nal designation.
Diagnosis: Liu and Hershler (2005:296).
Pyrgulopsis cybele, new species
T
YPES.—Holotype, USNM 1148155, un -
named spring brook on east side of South Fork
Owyhee River, Elko County, Nevada, N
4648124, E 524954, Zone 11, 1439 m elevation,
coll. RH and Chris Hansen, 1 November 2010.
Paratypes (from same lot), USNM 1157696
(ca. 400 specimens).
E
TYMOLOGY.—This species is named after
Cybele, the Roman goddess of nature.
Referred material: NEVADA. Elko County:
USNM 1128557 (ca. 150 specimens), unnamed
spring brook on east side of South Fork Owyhee
River, ca. 100 m north of the above, N 4645315,
E 525593, Zone 11, 1463 m elevation, coll. RH,
2 June 2009.
D
IAGNOSIS.—A small species of Pyrgulopsis
having a trochoid to ovate-conic shell with
highly convex whorls and a thickened inner
apertural lip. Penis having a medium-sized lobe
and medium-length filament; ornament consist-
ing of penial gland, Dg1, and terminal gland.
D
ESCRIPTION.—Shell trochoid to ovate-conic
(Fig. 2A–D); height 1.6–2.8 mm; whorls 3.25–
4.00. Periostracum tan. Protoconch near plani -
spiral, about 1.4 whorls, diameter about 420 μm,
initial portion weakly wrinkled (Fig. 2E, 2F).
Teleoconch whorls highly convex, shouldered,
sutures impressed, last whorl sometimes slightly
loosened behind aperture; smooth apart from
collabral growth lines. Aperture large, ovate,
angled above. Inner lip complete, usually slightly
disjunct, rarely adnate, thickened internally,
sometimes markedly so; columellar shelf usually
absent, narrow to moderate width when present;
outer lip usually thin, sometimes thickened
adapically, prosocline. Umbilicus usually small,
narrow, rarely absent. Shell measurements and
2012] NEW SPRINGSNAIL FROM NEVADA 23

24 WESTERN NORTH AMERICAN NATURALIST [Volume 72
TABLE 1. Specimen codes, localities, and GenBank accession numbers for Pyrgulopsis species that were included in
the molecular phylogenetic analysis.
Species Specimen code Locality Accession number
cybele P237A-F Spring brook entering north side of South Fork JN255353–JN255358
Owyhee River, Elko Co., NV
P252A-C Spring brook entering north side of South Fork JN255350–JN255352
Owyhee River, Elko Co., NV
gibba P134B, D Springs west of Fee Reservoir, Surprise Valley, AY197603
a
, AY426359
b
Lassen Co., CA
glandulosa Nelson Place spring, Verde River basin, AY627959
a
Yavapai Co., AZ
imperialis P140A, C Spring, Thacker Pass, Kings River Valley, AY379450
c
, AY426350
b
Humboldt Co., NV
intermedia P1B, E Crooked Creek, Highway 95 crossing, Owyhee AY379442
c
, AY426351
b
River basin, Malheur Co., OR
P2B, C Crooked Creek at Crooked Creek State Wayside AY426352
b
, AY426353
b
(19/v/2000), Owyhee River basin, Malheur
Co., OR
P4B, C Skylight Spring, Barren Valley, Malheur Co., OR AY379444
c
, AY379445
c
IP60A-D Crooked Creek at Crooked Creek State Wayside FJ172460
d
, FJ172461
d
,
(16/vii/2006), Owyhee River basin, Malheur FJ172462
d
, FJ172463
d
Co., OR
IP67A, C Spring tributary to Birch Creek, Owyhee River FJ172468
d
, FJ172469
d
basin, Malheur Co., OR
P217A Spring along Owyhee River, above Long Sweet- FJ172488
d
water Rapids, Owyhee River basin, Malheur
Co., OR
P222A, C Spring on hillside, Jackson Hole, Owyhee River FJ172496
d
, FJ172497
d
basin, Malheur Co., OR
P223A, B Mouth of Rinehart Creek, Owyhee River basin, FJ172498
d
, FJ172499
d
Malheur Co., OR
P224C Spring west of Two Mile Spring, Owyhee River FJ172500
d
basin, Malheur Co., OR
militaris P147A, C Spring west of Soldier Meadow Ranch, Black AY197596
a
, AY426362
b
Rock Desert, Humboldt Co., NV
montezumensis Montezuma Well, Verde River basin, Yavapai AY485552
e
Co., AZ
morrisoni Pmor5 Page Springs, Verde River basin, Yavapai Co., AZ AY485551
e
P150A Spring, Bubbling Pond Hatchery, Verde River DQ364007
f
basin, Yavapai Co., AZ
robusta D33C, D XL Spring, Abert Lake basin, Lake Co., OR AY426348
b
, AY426349
b
P3B, D Hughet Spring, Harney basin, Harney Co., OR AY379430
c
, AY379431
c
P5B, C South Fork Malheur Reservoir, Malheur Cave AY379432
c
, AY379433
c
Road crossing, Malheur River basin,
Harney Co., OR
P179A, B Snake River, Glenns Ferry, Snake River basin, AY379426
c
, AY379427
c
Elmore Co., ID
simplex Spring near Strawberry, Verde River basin, AY627949
g
Yavapai Co., AZ
sola Brown Springs, Verde River basin, Yavapai AY627957
g
Co., AZ
stearnsiana Stream in Little Sycamore Canyon, southern GQ275094
h
California coastal drainage, Ventura Co., CA
a
Hershler et al. 2003b
b
Hershler and Liu 2004b
c
Hershler and Liu 2004a
d
Hershler and Liu 2009
e
Hurt 2004
f
Hershler and Liu 2008
g
Liu and Hershler 2005
h
Hershler and Liu 2010

2012] NEW SPRINGSNAIL FROM NEVADA 25
Fig. 2. Scanning electron micrographs of shells and opercula of Pyrgulopsis cybele: A, holotype, USNM 1148155; B,
shell, USNM 1157696; C and D, shells, USNM 1128557; E, shell apex, USNM 1157696; F, close-up showing proto-
conch sculpture, USNM 1157696; G, operculum, outer side, USNM 1157696; H, operculum, inner side, USNM
1157696. Scale bars: A–D = 1.0 mm; E, F = 100 μm; G, H = 200 μm.

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Abstract: We describe "universal" DNA primers for polymerase chain reaction (PCR) amplification of a 710-bp fragment of the mitochondrial cytochrome c oxidase subunit I gene (COI) from 11 invertebrate phyla: Echinodermata, Mollusca, Annelida, Pogonophora, Arthropoda, Nemertinea, Echiura, Sipuncula, Platyhelminthes, Tardigrada, and Coelenterata, as well as the putative phylum Vestimentifera. Preliminary comparisons revealed that these COI primers generate informative sequences for phylogenetic analyses at the species and higher taxonomic levels.

12,098 citations


"A new species of springsnail ( Pyrg..." refers methods in this paper

  • ...A 658 bp segment of cytochrome c oxidase subunit I (COI) corresponding to “Folmer’s fragment” (Folmer et al. 1994) was amplified and se - quenced with primers LCO1490 and HCOI2198 following protocols of Liu et al. (2003)....

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Journal ArticleDOI
TL;DR: The finding that P. micrococcus contains multiple, genetically distinct and geographically restricted lineages suggests that diversification within this highly speciose aquatic genus has been structured in large part by the operation of terrestrial barriers to gene flow.
Abstract: We analysed cytochrome c oxidase subunit I and NADH dehydrogenase subunit I sequence variation among 29 populations of a widely ranging southwestern springsnail (Pyrgulopsis micrococcus) and 18 regional congeners. Cladistic analyses of these sequences depict P. micrococcus as a polyphyletic composite of five well-supported clades. Sequence divergences among these clades and subclades imply the possible occurrence of as many as seven or eight cryptic species in addition to P. micrococcus. Our finding that P. micrococcus contains multiple, genetically distinct and geographically restricted lineages suggests that diversification within this highly speciose aquatic genus has been structured in large part by the operation of terrestrial barriers to gene flow. However, these sequence data also indicate that recent dispersal among hydrographically separated areas has occurred within one of these lineages, which we attribute to passive transport on migratory waterbirds.

101 citations


"A new species of springsnail ( Pyrg..." refers background in this paper

  • ...Pyrgulopsis species are highly vulnerable to extirpation owing to their typically small, fragile habitats and narrow geographic ranges (Melhop and Vaughn 1994, Melhop 1996)....

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Q1. What contributions have the authors mentioned in the paper "A new species of springsnail (pyrgulopsis) from the owyhee river basin, nevada" ?

—We describe a new springsnail species, Pyrgulopsis cybele, from the Owyhee River basin ( northwestern Nevada ) based on morphologic and molecular ( mtCOI ) evidence. Although these populations are in a remote wilderness study area, they may be threatened by livestock grazing and human disturbance. It is further differentiated from regional congeners by its thickened inner-shell lip and mtCOI sequences. The COI divergence of P. cybele relative to its most genetically similar congener ( P. glandulosa ) suggests that it evolved subsequent to emplacement of the Miocene basalt that carpets the upper South Fork Owyhee basin.