Full Issue, Vol. 64 No. 2

Western North American Naturalist

Volume 64 Number 2 Article 18

4-30-2004

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BIOGEOGRAPHIC AND TAXONOMIC RELATIONSHIPS AMONG THE MOUNTAIN SNAILS (GASTROPODA: OREOHELICIDAE) OF THE CENTRAL GREAT BASIN

Mark A. Ports1

ABSTRACT.—Described here are 4 species of mountain snails, Oreohelix, isolated on mountains in the central Great Basin of Nevada and Utah since the end of the Pleistocene. Forty-three mountains were searched during an 18-year period, resulting in 24 mountains found with no oreohelicids present. One population, Oreohelix loisae (19 mm to 23 mm in shell diameter), is described here as a new species related to, but geographically isolated from, the species Oreohelix nevadensis (17 mm to 22 mm diameter). Oreohelix loisae is present only in the Goshute Mountains while O. nevadensis is represented in 3 geographically adjacent ranges in the central Great Basin. These 2 species are possibly related to the Oreohelix haydeni group from the northern Wasatch Range. The subspecies Oreohelix strigosa depressa (15 mm to 21 mm diameter) is present on 11 ranges from western Utah west to east central Nevada. This subspecies is closely related to populations found today in the northern Wasatch Mountains of Utah. The smallest species in diameter (8 mm to 14 mm), Oreohelix hemphilli, is centered in the central Great Basin and found on 16 ranges often in sympatry with 1 or 2 of the larger conspecifics. Both qualitative and quantitative information on shell characters and soft anatomy is provided here for these 4 species. Shell characters, soft anatomy, geographical isolation, and statistical analysis suggest that 4 distinct species inhabit the central Great Basin today. Xeric and calciphilic species include O. hemphilli and O. loisae, while O. strigosa and O. nevadensis typically are associated with permanent water and both metamorphic and limestone mountains.

Key words: mountain snails, Oreohelix, Great Basin biogeography, taxonomy, Oreohelix loisae sp. nov.

The genus Oreohelix (Stylommatophora: philli in the Deep Creek Range. Apparently, Oreohelicidae) is widely distributed but local- Roscoe (1954) misidentified these 2 species ized throughout the Rocky Mountains, Great possibly due to the wide variation in shell Basin, and southwestern regions of North morphology in both species as they occur America (Pilsbry 1939). Recent work (Solem throughout Utah, Colorado, and Idaho (Bran- 1975, Frest and Johannes 1997) has identified dauer 1988, Clarke and Hovingh 1991, Frest 2 centers of diversity in this genus, the 1st from and Johannes 1997). the Salmon River drainage of Idaho and the Fieldwork in the Great Basin, begun in 2nd from the northern Wasatch Mountains of 1982 by Pratt (1985) and continued by Ports Utah and Bear River Range of southern Idaho (1986–2002), has increased knowledge of the (Pilsbry 1939, Clarke and Hovingh 1991). biogeography of the genus Oreohelix in the Pilsbry (1939) described 3 species of Oreo- central Great Basin and suggests that this helix from the central and eastern Great Basin region may be a 3rd center of oreohelicid mountain ranges of Nevada: O. hemphilli New- diversity as predicted by Bequaert and Miller comb, 1869, in the White Pine Range, O. nevad- (1973). Today these populations are fragmented ensis Berry, 1932, in the Schell Creek Range, and isolated on mountain ranges throughout and O. strigosa Gould, 1846 (subspecies de- the region with little opportunity for gene flow pressa Cockerell 1890), from the Snake Range. and dispersal across desert valleys, similar to Roscoe (1954) listed O. subrudis Reeve, 1854, other faunal groups such as high-elevation- and O. eurekensis J. Henderson and Daniels, adapted small mammals in the Great Basin 1916, from the Deep Creek Range in western (Brown 1971). Utah. During visits in 1996 and 1997, how- In this paper I describe the biogeography, ever, the author found a medium-sized shell of shell and soft anatomy, and ecological varia- O. strigosa and smaller-sized shell of O. hem- tion in 3 little-known species of Oreohelix as

1Biology Department, Great Basin College, 1500 College Parkway, Elko, NV 89801.

145 146 WESTERN NORTH AMERICAN NATURALIST [Volume 64 listed for Nevada and present as new to sci- RESULTS ence a previously unknown oreohelicid from Taxonomy and Biogeography the Goshute Mountains on the Nevada–Utah of Oreohelix loisae border in the north central Great Basin. This new species is related to the Oreohelix haydeni The oreohelicid herein is described as a group from the Wasatch Mountains of Utah. new species: Order Stylommatophora; Family Oreohelicidae; Genus Oreohelix Pilsbry, 1904; METHODS AND MATERIALS Oreohelix loisae M.A. Ports, sp. nov. Holotype: ANSP 407556 (Figs. 1, 2, Table 1). Paratypes: From 1986 to 2002, I sought land snails in ANSP 408362, SBMNH 345735. 43 mountains throughout Nevada and eastern DIAGNOSIS.—Description of shell character- Utah. Shells were organized and stored by lots istics: Holotype (Fig. 1, 3 views of the holotype): and stations in a private collection at Great A large shell compared with other Great Basin Basin College. Latitude and longitude of each oreohelicids (holotype, 19.1 mm diameter and station were determined using U.S. Geological 11.4 mm height) with 5.5 whorls. Shell de- Survey topographic maps and confirmed using pressed, broadly conical, spire forming an angle a Garmin GPS II or III. of 100 degrees. Shell convex both on apical At each station empty shells of all age and basal surfaces with a strongly rounded classes were collected by hand and by digging peripheral body whorl. Yellow-brown perio- into rock slides using a rock hammer. Eight to stracum over the apical surface, lighter on the 20 live specimens were collected from each basal surface. Three narrow, yellow-brown station. These specimens were relaxed in men- bands with the peripheral band above the thol for 12 hours and killed by immersing in aperture which descends in front. No banding boiling water for 30 seconds. Bodies were below. An ovate-lunate aperture, 9.4 mm in pulled from their shells, preserved in 75% etha- diameter and 8.5 mm in height (Table 1). Thin nol for 24 hours, fixed in 5% formalin for 24 outer lip not deflected, parietal callus thick hours, and transferred to 50% ethanol for dis- and reflected slightly over the umbilicus. section purposes (Frest and Johannes 1997). Umbilicus deep and moderately wide, 4.6 mm Dissection of soft tissue was carried out in diameter, making up 23% of the shell diam- under a Leicca 40–60X dissection scope. Geni- eter. Four faint to obsolete beaded lirae on the talia were measured in millimeters using ver- basal surface and 4 faint beaded lirae on the nier digital calipers and drawn from preserved apical surface. Fine to moderately coarse, obli- specimens with pen and ink. The radula was que striae on body whorls. Faint periostracal prepared and studied on temporary slides using wreaths associated with the beaded lirae, but a 1% analine blue dye under a compound light no periostracal fringes on the peripheral whorl. microscope. Empty shells were scanned using Whorl sutures moderately impressed between Hewlett Packard Precision ScanPro 1.01 in api- penultimate and body whorls, aperture de- cal, basal, and aperture views, following which scends below the body whorl. images were saved and then printed. The tax- Paratype specimens vary from the holotype onomic description of the new species is accord- in shell size (17.7–21.8 mm shell diameter; ing to recommendations of Winston (1999). The 0.59–0.61 ratio of height/diameter; Table 1), following abbreviations were used for reposi- shell color (a light caulk), lack of bands or the tory institutions: ANSP, Academy of Natural presence of banding, distinct angular whorls Sciences, Philadelphia, for the holotype and to rounded body whorls, and degree of beaded paratypes of O. loisae, topotypes of O. nevad- lirae on the basal and apical surfaces. Juvenile ensis, and O. strigosa; SBMNH, Santa Barbara shells are strongly angular, including aperture Museum of Natural History, paratypes of O. whorl, 4 fine and distinct complete lirae on loisae and topotypes of O. nevadensis, O. stri- both the apical and basal surface; juveniles have gosa depressa, and O. hemphilli; MAP, Mark A. a much more depressed spire than adult shells Ports catalogue numbers. Catalogue numbers, with a large, ovate-lunate aperture. Periostra- localities, species, and dates of collection are cum in juveniles is dark brown, a color that listed in the appendix. A Mann-Whitney U-test accentuates the fine lirae, 3 distinct narrow was used to compare morphometric data be- brown bands, and shallow sutures, umbilicus is tween O. strigosa, O. nevadensis, and O. loisae. narrow, 3.5–whorls. The mean radula formula 2004] CENTRAL GREAT BASIN MOUNTAIN SNAILS 147

Fig. 1. Apical, aperture, and basal view of the holotype specimen of Oreohelix loisae, sp. nov. Shell diameter = 21 mm; shell height = 13 mm.

DESCRIPTION OF GENITALIA OF HOLOTYPE (FIG. 2).—The penis sac is relatively long (9.98 mm) and narrow throughout and is twisted into a tight S shape at the distal end. The distal end of the penis sac is flattened laterally and is the site of attachment for both the rib- bonlike penis retractor muscle and the narrow epiphallus. Internally, 35% of the proximal end of the penis sac is lined with 4–5 regular, longitudinal pilasters, while the remaining internal surface is lined with dense papillae. The epiphallus is relatively long (5.17 mm) and slender, tapering to a thin attachment at both the distal and proximal ends. The distal end of the vas deferens runs along the side of the vagina, coiling around the base of the vagina to enter the apex of the epiphallus in the medial surface between the penis sac and the vagina. The vagina is narrow at the base and broadens at the junction of the free oviduct and the uterus. The spermathecal sac is relatively large Fig. 2. Reproductive system of Oreohelix loisae Ports, sp. and oval in shape and the albumin gland is nov. Holotype from Christmas Tree Canyon, NV (ANSP short and rounded with a sharply recurved 407556). Scale bar = 1 mm. Key: ag = albumin gland, ep black talon. The hermaphroditic duct is highly = epiphallus, fo = free oviduct, prm = penis retractor coiled and compressed and the ovotestes are muscle, ps = penis sack, sp = spermatheca, ut = uterus, va = vagina, vd = vas deferens. Talon is located on relatively short and dense. median side of the albumen gland. The genitalia of 25 dissected paratypes varied in having a penis sac length of 10.1 to 12.9 mm, internal ribbed portion of penis sac of 3.79 mm to 4.39 mm in length, a ratio of penis for the holotype and 15 dissected paratypes is sac length/shell diameter of 0.53 to 0.67, and a 24-1-24 (Table 1). Rows of teeth per radula ratio of internal ribbed portion/total penis sac ranged from 10 to 150, the central tooth is a length of 0.34 to 0.38 (Table 1). rounded unicuspid on a tall broad plate with TYPE MATERIAL.—Holotype: ANSP 407556; no ectocones; lateral teeth 1–15, have a pro- Christmas Tree Canyon, Goshute Mountains, nounced lateral ectocone and a sharp pointed Elko County, NEVADA. 40 25.566′N and –144 cuspid; marginal teeth 16–22, degenerate from 16.233′W. 2784 m. Paratypes: SBMNH 345735; distinctly bicuspid with small, lateral ectocones Felt Wash, Goshute Mountains, Elko County, to very small unicuspid marginal teeth with no NEVADA, 40 27.347′N and –114 16.105′W. ectocones, 23–24. 2477 m (Fig. 5, number 16). 148 WESTERN NORTH AMERICAN NATURALIST [Volume 64

TABLE 1. Measurements of shell characters, soft anatomy, and ratios of 14 populations of Oreohelix from the central Great Basin of North America. Measurements represent mean values in millimeters for shell diameter, umbilicus width, and penis length. Shell Penis Ribbed height/ length/ portion/ Shell shell Umbilicus Radula Penis shell penis Species diameter diameter width formula length diameter length O. nevadensis 19.9 0.64 4.63 28-1-28 13.3 0.77 0.31 Schell Creek Range, n = 16 O. loisae 19 0.59 4.91 24-1-24 10.1 0.53 0.38 Goshute Mountains, n = 10 O. loisae 19 0.61 4.4 24-1-24 12.9 0.67 0.34 Goshute Mountains, n = 6 O. strigosa depressa 15.2 0.66 3.35 30-1-30 10 0.6 0.35 Ruby Mountains, n = 11 O. strigosa depressa 16.3 0.68 3.48 30-1-30 10.8 0.66 0.37 Ruby Mountains, n = 13 O. strigosa depressa 16.5 0.61 3.54 30-1-30 10.3 0.62 0.35 Pequop Mountains, n = 8 O. strigosa depressa 17.6 0.63 4.24 30-1-30 14.1 0.8 0.38 Snake Range, n = 10 O. strigosa depressa 16.9 0.67 3.66 30-1-30 9.9 0.59 0.327 Schell Creek Range, n = 8 O. strigosa depressa 18.2 0.70 3.72 30-1-30 7.7 0.42 0.37 Pilot Range, n = 8 O. strigosa depressa 18.4 0.64 4.46 30-1-30 9.9 0.54 0.38 Deep Creek Range, n = 8 O. strigosa depressa 16.2 0.64 4.56 30-1-30 10.6 0.66 0.37 Egan Range, n = 6 O. hemphilli 11.4 0.6 2.4 22-1-22 4 0.36 0.38 White Pine Range, n = 12 O. hemphilli 12.5 0.64 3.1 24-1-24 4 0.38 0.6 Snake Range, n = 6 O. hemphilli 8.0 0.61 2.6 22-1-22 2.6 0.32 0.36 Ruby Mountains, n = 8

ETYMOLOGY.—This species is named in honor dark brown periostracum. Juvenile specimens of Lois K. Ports, my field companion, friend, have an angular peripheral whorl and flattened and wife. spire. Mean shell diameter is 19.9 mm, the umbilicus is deep and wide at 4.63 mm, shell Taxonomy and Biogeography height/shell diameter ratio is 0.64, and the of Oreohelix nevadensis species possesses a mean radula formula of 28- S.S. Berry, 1932 1-28 (Table 1). The genitalia (Fig. 4) of this snail The Schell Creek mountainsnail (O. nevad- are similar in size (mean 12.9 mm penis sac ensis; SBMNH 345735) is the largest species of length) and shape to that of O. loisae. Although this genus in the Great Basin (mean diameter the penis sac length/shell diameter ratio is of 19.9 mm) and according to Pilsbry (1939) is higher than all other species examined, the most similar to the diverse Oreohelix haydeni ribbed portion/penis sac length is smallest, due (Gabb, 1869) group from north central Utah in to the large shell size and the relatively large the Wasatch Mountains. The shell of O. nevad- ribbed portion length of 4.02 mm (Table 1). ensis (Fig. 3) has weak “spiral striae” or beaded Comparisons of shell diameter (P < 0.001), lirae and broad, distinctive bands against a penis length (P < 0.001), and the ratio of penis 2004] CENTRAL GREAT BASIN MOUNTAIN SNAILS 149

Fig. 3. Apical, aperture, and basal view of Oreohelix nevadensis. Shell diameter = 23 mm; shell height = 15 mm.

This species is limited in its distribution, typically found in small colonies and restricted to the White Pine County and southern Elko County region of Nevada. Taxonomy and Biogeography of Oreohelix strigosa depressa Cockerell, 1890 The Rocky mountainsnail, Oreohelix strigosa (subspecies depressa), in the Great Basin has a smaller shell diameter, 4–5 mm less than the same form found in the Wasatch Range of Utah (Pilsbry 1939), and is intermediate in size between the large-shelled O. nevadensis and the small-shelled O. hemphilli (Table 1). Six of 7 populations examined are intermediate in Fig. 4. Reproductive system of Oreohelix nevadensis penis sac length/shell diameter ratio to the S.S. Berry, 1932. Topotype from Cleve Creek, Schell other 3 species (Table 1). The Baker Creek Creek Range, NV (ANSP 4018885). Scale bar = 1 mm. Key: ag = albumin gland, ep = epiphallus, fo = free ovi- sample (Pilsbry 1939) has a significantly larger duct, prm = penis retractor muscle, ps = penis, sp = penis sac length (P < 0.001) and a larger penis spermatheca, ta = talon, ut = uterus, va = vagina, vd = sac length/shell diameter ratio (P < 0.001 level) vas deferens. when compared with other populations of this species from the Great Basin. The Lutts Creek population from the Ruby sac length/shell diameter were significantly Mountains (Ports 1993; ANSP 401886) had a different (P < 0.001 level) for O. loisae and O. significantly smaller shell diameter (P < 0.001), nevadensis. Mean penis sac length and shell penis sac length (P < 0.001), and penis sac diameter (Table 1) separate this species from length/shell diameter (P < 0.001) compared the others examined, but they are closest to O. with O. loisae (Table 1) from the Goshute Moun- loisae. tains. Eight populations examined had a radula The specimens of O. nevadensis examined formula of 30-1-30, the same radula formula (ANSP 401885, SBMNH 345735; Appendix), found by Jones (1940) in the Wasatch Moun- come from the type locality on Cleve Creek tains. The Lutts Creek snail has 2 to 3 distinct, (Pilsbry 1939) on the east slope of the Schell brown apical bands and a periostracum exhibi- Creek Range and from 2 stations on the west ting a wide range of color variation from caulk slope. I also collected specimens on Goshute white to dark brown (Fig. 6). Creek and McDermid Creek in the Cherry This species was located in 11 of 43 moun- Creek Range and on Smith Creek in the north- tain ranges sampled in the central Great Basin ern Snake Range (Fig. 5). (Appendix). Populations exist today from the 150 WESTERN NORTH AMERICAN NATURALIST [Volume 64

(#)

Fig. 5. Distribution of Oreohelix populations in the central Great Basin of North America: (1) Black Rock Range (16) Pequop Mts. (31) Monitor Range (2) Pine Forest Range (17) East Humbolt Range (32) Hot Creek Range (3) Santa Rosa Range (18) Goshute Mts. (33) Roberts Mts. (4) Tuscarora Mts. (19) Spruce Mts. (34) Diamond Mts. (5) Snowstorm Mts. (20) Cherry Creek Mts. (35) Pancake Range (6) Sheep Creek Mts. (21) Ruby Mts. (36) White Pine Range (7) Independence Mts. (22) Shoshone Range (37) Grant Range (8) Bull Run Mts. (23) Pah Rah Range (38) Egan Range (9) Jarbidge Mts. (24) Pine Nut Mts. (39) Schell Creek Range (10) Good Creek Mts. (25) Sweetwater Mts. (40) Snake Range (11) Raft River Range (26) White Mts. (41) Wilson Creek Range (12) Oquirrh Mts. (27) Stillwater Range (42) Clover Mts. (13) Stansbury Mts. (28) Clan Alpine Mts. (43) Pine Valley Mts. (14) Pilot Range (29) Toiyabe Range (44) Deep Creek Range (15) Toana Range (30) Toquima Range (45) House Range 2004] CENTRAL GREAT BASIN MOUNTAIN SNAILS 151

Fig. 6. Apical, aperture, and basal view of Orehelix strigosa depressa. Shell diameter = 18 mm; shell height = 11 mm.

Fig. 7. Apical, aperture, and basal view of Oreohelix hemphilli. Shell diameter = 12 mm; shell height = 7 mm.

Pilot Range (ANSP 401887) in the north, to This species is located in 16 of 43 moun- the Egan Range in the south, as far west as the tains sampled (Appendix, Fig. 5). The western- Diamond Range, east to the Deep Creek Range most population is found in central Nevada in (ANSP 401888), and farther east to the House the Toiyabe Range, south to the Grant Range, Range (Appendix, Fig. 5). north in the Pilot Range, and east to the Deep Creek Range and House Range of western Taxonomy and Biogeography of Utah (Fig. 5). The last 2 localities represent O. hemphilli (Newcomb, 1869) the 1st records for O. hemphilli from Utah. In The White Pine mountainsnail (SBMNH the Mojave Desert 2 very similar species exist 345737) has the smallest shell diameter (mean (Pilsbry 1939): O. handi Pilsbry and Ferriss, 8–12.5 mm; Table 1) of the Great Basin oreo- 1918, from the Spring Range, and O. califor- helicids. Its shell also has distinct whorled nica S.S. Berry, 1931, from Clark Mountain. lirae on the basal and apical surfaces, and a carinate, keeled, peripheral body whorl (Fig. DISCUSSION 7). The short, swollen penis sac, short epiphallus, and stocky vagina (Fig. 8) are most similar At present 4 species of Oreohelicidae exist to O. carinifera from Montana and O. eureken- in the central Great Basin of North America: sis from the East Tintic Range (Pilsbry 1939). Oreohelix loisae, O. nevadensis, O. strigosa, and The type locality from the White Pine Range is O. hemphilli. Of 19 mountain ranges that sup- intermediate in shell characters and soft ana- port oreohelicids, 2 to 3 species exist in sym- tomy between the 3 populations examined patry in 11 mountain ranges, within which no (Table 1). The radula formula for the type local- species were found to exist below an elevation ity specimens and the Pearl Creek specimens of 2000 m (Appendix, Fig. 5). Roscoe (1954) is 22-1-22, but a radula formula of 24-1-24 was reported both Oreohelix subrudis and Oreohe- discovered for specimens from Murphy Wash lix eurekensis from the Deep Creek Range on (Table 1). the Nevada–Utah border. My collections from 152 WESTERN NORTH AMERICAN NATURALIST [Volume 64

species discussed were not detected in this range. Because of similar shell characters and soft anatomy, I assume that O. nevadensis and O. loisae are related to, and possibly holophyletic with, Oreohelix haydeni from the northern mountains of Utah (Pilsbry 1939). As of this writing, O. nevadensis exists in 3 parallel mountains separated by 2 valleys: the North Snake Range on Smith Creek, the Schell Creek Range on Cleve Creek (the type locality; Pilsbry 1939), and on Goshute Creek in the Cherry Creek Range (Appendix, Fig. 5). In each of these ranges, O. nevadensis is associated with perennial springs or streams lined with narrow-leaf Fig. 8. Reproductive system of Oreohelix hemphilli Newcomb, 1869. Topotype from Cathedral Canyon, cottonwood (Populus angustifolia), willow (Salix White Pine Range, NV (MAP 994). Scale bar = 1 mm. sp.), red-osier dogwood (Cornus stolonifera), Key: ag = albumin gland, ep = epiphallus, fo = free and wild rose (Rosa woodsii). At each locality oviduct, prm = penis retractor muscle, ps = penis, sp = O. nevadensis is sympatric with O. strigosa in spermatheca, ta = talon, ut = uterus, va = vagina, vd = vas deferens. the drainages and O. hemphilli on the drier, brush-covered, rocky slopes above the drainage. It is not unusual to find more than 1 species of oreohelicid on a single, isolated mountain range, this range suggest that these species are actu- as shown by Metcalf and Smartt (1997) in New ally O. strigosa and O. hemphilli, based on Mexico. Adaptation to microhabitats and dis- shell morphology and genitalia. Both species persal biogeography (Pratt 1985) into the Great pairs (O. strigosa–O. subrudis and O. hemphilli– Basin mountains may explain why 2 to 3 species O. eurekensis) are very similar in shell morphol- coexist in the same mountains. In Logan Can- ogy and may be synonymous, as Brandauer yon of the northern Wasatch Range, I found O. (1988) suggested for O. strigosa and O. sub- strigosa and O. haydeni together (Pilsbry 1939), rudis in Colorado. Oreohelix hemphilli and O. while in the Stansbury Range on the east side eurekensis are very much alike in many shell of the Great Basin, I found O. strigosa and O. characters and may be synonymous with O. eurekensis together in the same canyon. Colo- eurekensis in the East Tintic Mountains on the nization from the east into the Great Basin eastern edge of the Great Basin (Pilsbry 1939). also may explain why certain species exist Oreohelix loisae is found in only a few dry where they do today, as suggested for the dis- canyons of the limestone-dominated Goshute tribution of montane mammals in the Great Range in north central Great Basin. A large- to Basin by Brown (1971). Pratt (1985) suggests medium-sized snail, this species is adapted to that several species of land snails that have limestone rockslides with an understory of been isolated on mountains in the Great Basin Symphoricarpus oreophilus, Rhus trilobata, Arte- are at risk of extinction. misia tridentata, and Holodiscus dumosus, be- The most mesic stations in the central Great neath an overstory of white fir (Abies concolor), Basin are occupied primarily by O. strigosa. limber pine (Pinus flexilis), and Great Basin All of the stations listed for this species (Fig. 5, bristlecone pine (Pinus longaeva). Appendix) are on perennial streams in lime- Oreohelix loisae is found from the highest stone or metamorphic ranges in woodlands elevation of the range at 2750 m (bristlecone dominated by quaking aspen (Populus tremu- pine and white fir) to 2450 m in the pinyon loides), limber pine, and white fir with an pine (Pinus edulis) and Utah juniper ( Junipe- understory of wild rose, red-osier dogwood, rus osteosperma) woodlands. Except for spring and common chokecherry (Prunus virginiana). snowmelt and rare summer showers as sources This species of land snail is generally restricted of moisture, there is no open or flowing water to rock slides and boulders but occasionally is in this range. This snail is found in the same found in forest litter. Similar habitat associa- rockslides with O. hemphilli, but the other 2 tions have been described by Henderson (1924) 2004] CENTRAL GREAT BASIN MOUNTAIN SNAILS 153 for oreohelicids at many stations throughout LITERATURE CITED the West. Much less is known about the biogeogra- BEQUAERT, J.C., AND W. B. M ILLER. 1973. The mollusks of the arid Southwest. University of Arizona Press, Tuc- phy, anatomy, and habitat association of Oreo- son. 271 pp. helix hemphilli (Pilsbry 1939). The source of BRANDAUER, N.E. 1988. Family Oreohelicidae (Gastropoda: origin may possibly be the East Tintic Moun- Pulmonata). Colorado University of Colorado Museum, tains, where the similar Oreohelix eurekensis Natural History Inventory of Colorado 9:1–32. exists, or O. hemphilli may be endemic to the BROWN, J.H. 1971. Mammals on mountaintops: non-equi- librium insular biogeography. American Naturalist central Great Basin and has spread east from 105:467–478. the central Great Basin. Stations where O. CLARKE, A.H., AND P. H OVINGH. 1991. Status survey of hemphilli is found in the Great Basin (Fig. 5, selected land and freshwater gastropods in Utah. Appendix) are typically xeric and associated Draft report, USDI, Fish and Wildlife Service. Eco- with limestone rockslides. An understory of search, Inc., Portland, TX. 70 pp. FREST, T.J., AND E.J. JOHANNES. 1997. Land snail survey of shrubs is usually present, including snowberry, the lower Salmon River drainage, Idaho. Technical mountain ninebark (Physocarpus monogynus), Bulletin 97-18, Bureau of Land Management. Deixis and Rocky Mountain maple (Acer glabrum). Consultants, Seattle, WA. 142 pp. Overstory trees consist of mixed conifer wood- HENDERSON, J. 1924. Mollusca of Colorado, Utah, Mon- tana, Idaho, and Wyoming. University of Colorado lands of pinyon pine, Utah juniper, and Rocky Studies 13:65–223. Mountain juniper ( Juniperus scopularum) at JONES, D.T. 1940. A study of the Great Basin land snail, mid-elevations (2250 m). At higher elevations Oreohelix strigosa depressa. University of Utah Bul- (2450 m) the conifers consist of bristlecone letin 31:1–43. METCALF, A.L., AND R.A. SMARTT, EDITORS. 1997. Land snails pine, limber pine, white fir, and Douglas-fir of New Mexico. New Mexico Museum of Natural (Pseudotsuga menziesii). History and Science Bulletin 10. 145 pp. More work, including genetic analysis, is PILSBRY, H.A. 1939. Land Mollusca of North America currently underway in order to understand the (north of Mexico). Volume 1, part 1. Academy of Nat- historical biogeography and taxonomic rela- ural Sciences of Philadelphia Monograph 3(1):1–574. PORTS, M.A. 1996. Habitat affinities and distributions of tionships among these 4 species and their re- land gastropods from the Ruby Mountains and East lationships with the species of oreohelicids Humboldt Range of northeastern Nevada. Veliger from the eastern edge of the Great Basin and 39:335–341. the Wasatch Mountains. PRATT, W.L. 1985. Insular biogeography of central Great Basin land snails: extinction without replacement. Journal of the Arizona-Nevada Academy of Sciences ACKNOWLEDGMENTS 20:14–18. ROSCOE, T.J. 1954. Some terrestrial gastropods from the The artwork, table, and photographs were Deep Creek Mountains, Juab County, Utah. Great provided by Lois K. Ports and Mark E. Ports. Basin Naturalist 14:19. SOLEM, A. 1975. Notes on Salmon River oreohelicid land I acknowledge the support and facilities used snails, with description of Oreohelix waltoni. Veliger at Great Basin College and appreciate the 18:16–30. acceptance and cataloging of snail specimens WINSTON, J.E. 1999. Describing species: practical taxo- by the Academy of Natural Sciences of Phila- nomic procedures for biologists. Columbia Univer- delphia and the Santa Barbara Museum of sity Press, New York. 518 pp. Natural History. I appreciate comments from Received 12 July 2002 Dr. Lawrence E. Stevens and 2 anonymous Accepted 27 August 2003 reviewers. Finally, I thank Lois, Roger, Jacki, and Mark, who endured rough mountain roads and patiently searched through rock slides for snails over many summers. Appendix on the following page. 154 WESTERN NORTH AMERICAN NATURALIST [Volume 64

APPENDIX N, –115°.197 W, 2 June 1989. (12) MAP 818, southwest of Swasey Peak, House Range, Millard County, UTAH. SPECIMENS EXAMINED IV. Oreohelix hemphilli: (1) SBMNH 345737, Cathedral I. Oreohelix nevadensis: (1) ANSP 401855 (topotype); Canyon, Mount Hamilton, White Pine Range, White Pine SBMNH 345735 (topotype), Cleve Creek, east slope of County, NEVADA, 39°.212 N, –115°.465 W, 20 July 2000. the Schell Creek Range, White Pine County, NEVADA, ° ° (2) MAP 761, Murphy Wash, south Snake Range, White 39 .247 N, –114 .925 W, 20 May 1994. (2) MAP 832, Pine County, NEVADA, 38°.788 N, –114°.308 W, 28 May Goshute Creek, Cherry Creek Range, Elko County, ° ° 1997. (3) MAP 669, Pearl Creek, southern Ruby Moun- NEVADA, 40 .058 N, –115 .835 W, 8 August 1988. (3) tains, Elko County, NEVADA, 40°.271 N, –115°.551 W, 11 MAP 807, Smith Creek, North Snake Range, White Pine September 1999. (4) MAP 806, Smith Creek, north Snake County, NEVADA, 39°.243 N, –114°.107 W, 28 March Range, White Pine County, NEVADA, 39°163 N, –114°.164 1994. W, 28 March 1994. (5) MAP 829, Taylor Canyon, Cherry Creek Range, Elko County, NEVADA, 40°.231 N, II. Oreohelix loisae: (1) Holotype, ANSP 407556; –114°.943 W, 21 July 1995. (6) MAP 700, Hooper Canyon, paratypes ANSP 408362, SBMNH 345735, Felt Wash, Quinn Canyon Range, Nye County, NEVADA, 38°.236 N, Goshute Mountains, Elko County, NEVADA, 40°.463 N, –115°.661 W, 8 April 1993. (7) MAP 433, Kingston –114°.269 W, 10 May 1997. (2) Christmas Tree Canyon, Canyon, Toiyabe Mountains, Lander County, NEVADA, Goshute Mountains, Elko County, NEVADA, 40°.444 N, 39°.204 N, –117°.137 W, 10 July 1998. (8) MAP 713, Felt –114°.256 W, 10 October 1986. Wash, Goshute Range, Elko County, NEVADA, 40°.463 N, –114°.269 W, 10 May 1997. (9) MAP 872, Roberts Creek, III. Oreohelix strigosa depressa: (1) ANSP 401886, Roberts Creek Mountains, Eureka County, NEVADA, Lutts Creek, Ruby Mountains, Elko County, NEVADA, ° ° 40°.609 N, –115°.319 W, 19 May 1993. (2) ANSP 401887, 39 .811 N, –116 .312 W, 25 July 1998. (10) MAP 989, canyon on west slope of Highland Range, Lincoln County, Horse Spring, Pilot Range, Elko County, NEVADA, ° ° 41°.024 N, –114°.105 W, 7 August 1992. (3) ANSP 401888, NEVADA, 37 .855 N, –114 .591 W, 26 May 2000. (11) MAP 914, Pine Creek, Toquima Range, Nye County, Birch Creek, Deep Creek Range, Juab County, UTAH, 14 ° ° November 1994. (4) ANSP 401890, Six Mile Creek, NEVADA, 38 .786 N, –116 .883 W, 30 June 1999. (12) ° MAP 743, Six Mile Creek, Pequop Range, Elko County, Pequop Range, Elko County, NEVADA, 41 .003 N, ° ° –114°.562 W, 4 June 1993. (5) MAP 743, Davis Canyon, NEVADA, 40 .319 N, –114 .553 W, 3 August 1993. (13) Diamond Range, Eureka County, NEVADA, 40°.084 N, MAP 74, Hendrys Creek, north Snake Range, White Pine ° ° –115°.869 W, 3 November 1993. (6) MAP 868, Shingle County, NEVADA, 39 .228 N, –114 .136 W, 16 May 1987. Pass, Egan Range, Lincoln County, NEVADA, 38°.522 N, (14) MAP 905, Holt Camp Canyon, Egan Range, White ° ° –114°.916W, 25 May 1999. (7) MAP 721, Berry Creek, Pine County, NEVADA, 39 .704 N, –114 .884 W, 17 Sep- Schell Creek Range, White Pine County, NEVADA, tember 1988. (15) MAP 693, Davis Canyon, Diamond ° ° 39°.361 N, –114°.687 W, 10 July 1993. (8) MAP 990, Range, Eureka County, NEVADA, 41 .084 N, –115 .869 Snake Creek, Snake Range, White Pine County, W, 3 November 1993. (16) MAP 909, Scofield Canyon, ° NEVADA, 38°.994 N, –114°.240 W, 13 May 1989. (9) Grant Range, Nye County, NEVADA, 38 .302 N, ° MAP 820, Hendrys Creek, North Snake Range, White –115 .508 W, 15 June 1999. (17) MAP 857, Hogan’s Pine County, NEVADA, 39°.227 N, –114°.136 W, 14 May Canyon, Pilot Range, Box Elder County, UTAH, (18) 1988. (10) MAP 832, Goshute Creek, Cherry Creek MAP 1002, Birch Creek, Deep Creek Range, Juab Range, White Pine County, NEVADA, 40°.058 N, County, UTAH. (19) MAP 1073 Miller Canyon, House –115°.835 W, 8 August 1988. (11) MAP 747, Ackler Creek, Range, Millard County, UTAH. East Humboldt Range, Elko County, NEVADA, 40°.996 Western North American Naturalist 64(2), ©2004, pp. 155–165

EFFECT OF CRYPTOBIOTIC CRUST TYPE ON MICROARTHROPOD ASSEMBLAGES IN PIÑON-JUNIPER WOODLAND IN CENTRAL NEW MEXICO

S.L. Brantley1 and U.L. Shepherd2

ABSTRACT.—Cryptobiotic crusts make up an important part of the ground cover in arid systems. Along with their roles of retarding soil erosion and enhancing soil fertility, crusts may also be supporting local and regional arthropod biodiversity. We inventoried arthropod species in mossy, lichen, and mixed (lichen and mossy) cryptobiotic crusts at 2 sites in central New Mexico piñon-juniper habitat. We collected 240 crust samples and used a heptane flotation technique to extract the microarthropods. We found 39 species of microarthropods and small macroarthropods, with significantly fewer species on lichen. Species richness was higher in March than in August, but diversity was lower because of dominance by the mite Neonanorchestes sp. Mean area differed significantly for different crust types, but arthropod species richness did not follow the pattern of more species on crusts with larger area. Arthropod species may be influencing such processes as nutrient cycling; therefore, the crust/arthropod interaction may be critical to aridland health.

Key words: microarthropods, cryptobiotic crusts, community structure, biodiversity.

Cryptobiotic crust communities are ecolog- of arthropod species richness and species iden- ically important in arid systems worldwide, tities in 3 crust types (bryophytic, lichen, and particularly in retarding soil erosion; increasing mixed) at 2 sites in central New Mexico. We soil fertility, water infiltration, and nitrogen wished to determine whether arthropods uti- fixation; and interacting with vascular plant lize the less structurally developed lichen crust germination (Evans and Johansen 1999). These and, if so, whether those species represent the crusts are highly threatened in the western same or a different fauna from that found in United States, where they can make up as 1999. In addition, we wondered whether mixed much as 70% of soil cover (Belnap and Lange patches contain species found on either moss 2001). or lichen or whether some other pattern might Crusts may provide important resources to emerge. Based on structure and crust species a large segment of unexplored aridland soil composition, we proposed that different crusts biota. Soils have been described as the “poor might provide different resources, resulting in man’s rainforest” (Giller 1996) due to the large different faunal associations. Quite possibly the range of taxa and their abundance. Soil ani- seasonal preference we reported in 1999 was mals are major regulators of decomposition an anomaly or perhaps arthropods using either and mineralization (Santos et al. 1981). Several lichen or mixed patches are more abundant in studies in the Arctic and Antarctic have shown summer than in winter. a number of species associated with the exten- To investigate these relationships, we ex- sive moss and lichen cover present in those plored 2 questions: (1) Are there differences in cold, arid habitats (Block 1979, Behan and Hill microarthropod richness, abundance, diversity, 1980, Booth and Usher 1986, Block and Convey or species composition on different crust types? 1995). Much less is known about microarthro- and (2) Do these factors differ by season? We pods of crusts in warm, arid environments. predicted that species composition would dif- Shepherd et al. (2002) demonstrated that fer by crust type, with mixed crusts having there is a specific community of arthropods communities composed of species found on associated with bryophytic (mossy) crusts in both mossy and lichen. We also predicted that piñon-juniper habitat. Our present objective is richness, abundance, and diversity would be to expand on that work through an inventory greatest on mixed patches because these were

1Museum of Southwestern Biology, University of New Mexico, Albuquerque, NM 87131. 2University Honors Program, University of New Mexico, Albuquerque, NM 87131.

155 156 WESTERN NORTH AMERICAN NATURALIST [Volume 64 composed of both mossy and lichen crusts. And cm2, three from patches 301–3000 cm2, etc., finally, we predicted, based on results from representing an additional sample for each our previous work (Shepherd et al. 2002), that tenfold increase in area). Where samples came richness, abundance, and diversity would be from on a patch was determined randomly and greatest in March. in the case of very small patches the entire crust was taken. Because individual crust patches STUDY AREA were often quite small, we hoped to reduce damage by avoiding collection of larger sam- We chose 2 study sites in the Cibola National ples. We collected samples from 20 patches of Forest near Placitas, New Mexico, approximately each crust type for each collection period at 30 km north of Albuquerque. Both sites are each site for a total of 240 patches. Sampling located at the base of the Sandia Mountains. for both studies occurred during La Niña They are approximately 3 km apart and are (drought) years. All crust samples were pre- located in different arroyo drainages. Lower served in 70% ethanol until ready for processing. Arroyo (LA; N35°17′13.8″, W106°30′4.3″) is at an elevation of approximately 1775 m and the Extraction Technique dominant tree species is Juniperus monosperma We harvested animals on return to the lab (Engelmann) Sargent. Other vegetation at this using a modified version of the heptane flota- site consists of grasses, several Opuntia species, tion method (Shepherd et al. 2002), originally and numerous shrubs including Fallugia para- described by Walter et al. (1987) and Kethley doxa (D. Don) Endlicher ex Torrey (Apache (1991). We chose this extraction method be- plume) and Ericameria (formerly Chrysotham- cause, unlike funnel methods that depend on nus) nauseosus (Pallas ex Pursh Nessom and animals being alive (MacFadyen 1962, Edwards Baird) (chamisa or rabbitbrush). Piedra Lisa and Fletcher 1971), flotation methods recover ° ′ ″ ° ′ ″ (PL; N35 16 43.0 , W106 28 40.0 ) is at an microarthropods from soil and litter samples elevation of approximately 1950 m. Both Pinus whether they are dead or alive by capturing edulis Engelmann and J. monosperma occur at them in a nonpolar solvent through which the this site. Other vegetation is similar to that of sample has passed. Comparative studies show Lower Arroyo except that there are more shrubs the flotation method is ideally suited to har- and relatively little grass cover. vesting suites of desert-adapted arthropods Each site contained a variety of crust types, that, due to their life history traits, may not including bryophyte-dominant, lichen-domi- respond to moisture gradients set up by fun- nant, and mixed patches. At each site crusts nel techniques (Walter et al. 1987, Andre et al. were most abundant along the arroyo bed on 2002). Results of our earlier work support the rocky or pebbly soil. We chose crust types finding that this method is well suited to work according to their gross morphological traits in highly mineralized soils. Samples were (i.e., differences obvious to the eye). These in- scanned at 90X magnification and slide mounts cluded 1 type of bryophytic crust, 1 lichenized were made for further identification using a crust, and patches that contained the 2 types phase contrast compound microscope. together. Data Analysis METHODS Since we could not standardize crust patch size across types when we sampled, and since Field Collections such differences might account for differences We sampled in March and August 2000. in species richness or abundance, we thought Based on 1999 results, in which almost no it important to determine whether patch size microarthropods were found prior to precipi- differed significantly by crust type. Because tation in either March or August (Shepherd et the data were highly skewed, we used a Krus- al. 2002), we sampled from 36 to 72 hours after kal-Wallis (PROC RANK and PROC ANOVA, a precipitation event and between 0700 and SAS Institute, Inc. 1999) in which the depen- 1200. We used the same protocol reported in dent variable was patch size and the main that earlier paper (i.e., we took one sample of effects were site and crust type. Patch size dif- approximately 8 cm3 from patches with an area fered among crust types, with mixed patches ≤30 cm2, two samples from patches 31–300 significantly larger than either lichen or mossy 2004] MICROARTHROPODS ON CRYPTOBIOTIC CRUSTS 157

(df = 2, P = 0.001), but not among sites (df = 2 seasons, we used the nonparametric Multi- 2, P = 0.96). Response Permutation Procedures (MRPP), To test whether there were differences in which is similar to discriminant analysis used richness across crust types, we first asked for parametric data (McCune and Mefford whether there were differences in richness by 1999). The value of δ (delta, the weighted site. We constructed a 2 × 3 contingency table mean within-group distance) was used to cal- for each crust type for chi square analysis and culate the test statistic T, which described the ran a Bonferroni adjustment (P = 0.02) of separation between groups and was associated these results. Since there were no differences with a corresponding P value. The test also among sites (lichen, n = 79, df = 2, χ2 = 1.6, provided a measure of within-group hetero- P > 0.5; mossy, n = 81, df = 2, χ2 = 0.7, P > geneity (A): A = 0 when within-group hetero- 0.75; mixed n = 80, df = 2, χ2 = 0.2, P > 0.9), geneity equals that expected by chance; A < 0 we pooled site data for further richness com- when within-group heterogeneity is greater parisons. We then used ANOVA in which the than that expected by chance. For our data main effects were season and crust type. A = 0.034 for crust types in March and 0.015 To address differences in abundance among in August. species (and because so many species were rare; see Appendix), we asked whether the 4 RESULTS most abundant varied among site, crust type, and season by means of individual Kruskal- We found arthropods in patches of all crust Wallis tests (PROC RANK and PROC ANOVA, types: 34 species in 3 classes and 7 orders. SAS Institute, Inc. 1999). In each case abun- Mites and collembolans were the dominant dance was the dependent variable, while site, groups with 21 and 5 species, respectively. In crust type, season, and their interactions were addition, we found diplurans, pseudoscorpi- the independent variables. Because these tests ons, thrips, tardigrades, and at least 2 species were based on abundance rather than rich- of nematodes (Appendix). Species richness was ness, site was included as a main effect. significantly greater on mossy and mixed (Fig. 1; For both the richness and abundance analy- F = 7.80, P = 0.02) than on lichen, and in ses, the independent variables were treated as March (32) than in August (20; Fig. 1; F = 10.31, fixed. Significance tests were constructed using P = 0.02). There was no interaction effect for type I sums of squares. crust type by season. We examined the relationship between di- Although we collected few individuals of versity and season and crust type using the most species, the 4 most abundant (the endeo- Shannon index (H) and Simpson’s index of stigmatid mite Neonanorchestes sp., the orib- dominance (D) and the Hill numbers for atid mite Zygoribatula sp., and 2 collembolans species richness (N0), numbers of abundant [Cryptopygus ambus and Tullbergia iowensis]) species (N1), and numbers of very abundant had more than 100 individuals each. Both species (N2; Ludwig and Reynolds 1988). Neonanorchestes sp. (Fig. 2a; F = 21.95, P = To determine whether there were differences 0.0001) and C. ambus (Fig. 2c; F = 2.85, P = in species composition, we used the Jaccard 0.06) preferred mossy crusts. Zygoribatula sp. similarity index (Cj; Magurran 1988) on pooled (Fig. 2b; F = 14.94, P = 0.0001) was more richness data (i.e., with sites combined) to com- abundant at Lower Arroyo (LA) than at Piedra pare crust types in each season. Six macro- Lisa (PL), while both collembolans were more arthropod taxa (Appendix) were omitted from abundant at PL (C. ambus: F = 45.5, P = this analysis because we considered them to 0.0001; T. iowensis: F = 6.83, P = 0.0001; be incidental users of crusts. These included Figs. 2c–d). All 4 species were more abundant lygaeids (seed bugs), mirids (plant bugs), and in March (Fig. 2). cixiids (planthoppers), and a geometrid cater- There were significant interaction effects pillar (all of which are generally found on living among the 3 factors for all 4 species. For Neo- vascular plants), as well as a beetle larva and nanorchestes sp. season × crust type, site × chalcidoid wasp. Most of these species occurred crust type and season × site × crust type were as single individuals in our sampling. significant (P < 0.0001 for all; Fig. 2a). For To test how well species composition and Zygoribatula sp. only site × season × crust abundance separated the 3 crust types and the type was significant (P = 0.04; Fig. 2b). For C. 158 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Fig. 1. Total arthropod species richness by crust type and season. Letters indicate significant differences. For crust type, mossy and lichen differed from each other (P = 0.02), while mixed did not differ from either mossy or lichen. Richness from the 2 seasons differed significantly (P = 0.02). There was no significant interaction effect of crust type and season on richness. ambus season × site, season × crust type, site × thus sp., the acarid, and the pseudoscorpion crust type, and season × site × crust type were occurred only on moss. Speleorchestes sp. (an significant (P = 0.0001, 0.08, 0.02, 0.04, re- endeostigmatid) showed a weak preference for spectively; Fig. 2c). For T. iowensis season × mosses, and the prostigmatid Tydeus sp. also site was significant (P < 0.0001; Fig. 2d). preferred mossy crusts. Eupodes sp. was more Numbers of other arthropods were too low common on mixed crusts. It is unclear whether to show clear patterns, but it is worth noting these species were herbivorous or predaceous. where several species were found. The meso- Although collembolans have been reported stigmatid mite, Hypoaspis (Geolaelaps) sp., the to feed on lichens more than mosses (Lawrey prostigmatids Penthaleus sp. and Raphigna- 1987), at our sites C. ambus, T. iowensis, and 2004] MICROARTHROPODS ON CRYPTOBIOTIC CRUSTS 159

Fig. 1. Continued.

Bourletiella sp. were rather evenly distributed sons were ignored: lichen and mossy = 61%, among crust types (Appendix). The entomo- mossy and mixed = 62%, lichen and mixed = bryid was found only on lichen. 57%. We found the least similarity between Overall abundance (total number of arthro- mossy and mixed patches in August (44%) and pods) was highest on moss, due largely to its between mixed patches in March and August preference by Neonanorchestes sp. mites. Diver- (44%; when richness was high, abundance was sity was lower in March (Table 1), due to the high and there was a strong dominance of Neo- dominance of Neonanorchestes sp. (687 indi- nanorchestes sp.; Table 2). The greatest simi- viduals out of a total of 1402 in March). In larity was found between mossy and mixed in August more species were classified as com- August (74%) followed by mixed and lichen in mon (Hill N1) or very common (Hill N2). August (64%; when richness and abundance Similarities in species composition among were low and no species was dominant). The crust types were moderate when sites and sea- MRPP test showed that differences in species 160 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Fig. 2. Mean number of individuals/sample collected for the 4 most abundant arthropod species by site, season, and crust type: (a) Neonanorchestes sp., (b) Zygoribatula sp., (c) C. ambus, (d) T. iowensis. Note that the mean abundance of Neonanorchestes sp. was greater than for the other 3 species, so that the y-axis is not on the same scale. P-values of the interaction effects are shown on the graphs (significant results marked with *). P-values of main effects are given in the Results section.

composition and abundance were great enough the year. In the present study we collected only to significantly separate the 3 crust types in in March and August, and only after precipita- March (T = –3.865, P = 0.001), but not in tion (the periods of peak activity in 1999), but August (T = –1.585, P = 0.070). we increased crust types to include lichen patches and patches with both moss and DISCUSSION lichen (mixed). In 1999 we found 20 mite and 4 springtail species on mossy crust; in 2000 we We predicted that microarthropod richness collected 17 and 3, respectively. From the lichen and abundance would be greater on mixed crusts we added an entomobryid collembolan, crust than on mossy or lichen because of greater and from mixed crusts we added the nanor- structural and taxonomic heterogeneity, but chestid mite Bimichaelia sp. and a hypogas- we found that richness did not differ signifi- trurid collembolan. Because the numbers of cantly between mixed and mossy, or between individuals collected were low, we do not mixed and lichen. Richness was significantly assume that these added taxa are specialists on lower on lichen than on mossy (Fig. 1). Abun- lichen or mixed crusts. Species that had not dance of 2 of the 4 dominant species was also been collected from mossy crust in 1999 were greater on mossy crusts than on mixed (Fig. 2). Raphignathus sp. and Bryobia sp. (Appendix). Because crust components vary widely (includ- Missing from the collections in 2000 were 5 ing cyanobacteria, fungi, algae, bryophytes), we rare species found in 1999: Dactyloscirus sp., expected microarthropod species composition Erythraeus sp., Passalozetes sp., Pygmephorus to vary by crust type. Similarities among season/ sp., and a galumnid oribatid. crust type combinations were indeed low to In our earlier work we compared our list of moderate (44%–64%), with a high similarity microarthropod species found on crusts with (74%) found only between mossy crust in August species lists for microarthropod communities and mixed crust in August (Table 2). recorded at other locations across our region The current study expanded on work con- (cited in Shepherd et al. 2002). All of those ducted in 1999 (Shepherd et al. 2002), when studies dealt with mites and collembolans found we sampled mossy crusts 7 times throughout in soil and/or on litter; none mentioned the 2004] MICROARTHROPODS ON CRYPTOBIOTIC CRUSTS 161

Table 1. Diversity indices (Shannon H , Simpson’s dominance D, and Hill numbers N0 (species richness), N1 (number of abundant species), N2 (number of very abundant species) for arthropod species by season and crust type (lichen, mossy, mixed).

______Crust type ______Collection month Lichen Mossy Mixed March August H 2.43 1.45 2.20 1.73 2.35 D 0.13 0.64 0.11 0.27 0.14

N0 21 29 26 32 20 N1 11.36 4.20 9.03 5.64 10.49 N2 7.69 1.56 9.09 3.70 7.14

Table 2. Jaccard similarity index (Cj) of arthropod species composition by season and crust type (lichen, mossy, mixed).

______Lichen ______Mossy ______Mixed Mar Aug Mar Aug Mar Aug Lichen – Mar 1.00 0.52 0.61 0.54 0.60 0.62 Lichen – Aug 1.00 0.44 0.63 0.55 0.64 Mossy – Mar 1.00 0.52 0.57 0.52 Mossy – Aug 1.00 0.50 0.74 Mixed – Mar 1.00 0.44 Mixed – Aug 1.00

presence of crusts. We found very low similarity species has been demonstrated to have recovery between our species lists and those recorded rates of 78% of known soil microarthropods in elsewhere in the region (Chihuahuan Desert desert systems from a single flotation cycle 19%, shortgrass prairie 11%). Even with the (Walter et al. 1987). Recovery of specific groups addition of lichen and mixed crusts, and an was shown to be 39% for prostigmatids, 84% added year of sampling, the similarities we for oribatids, 89% for collembolans, 95% for previously reported between our sites and ad- astigmatids, and 69% for mesostigmatids. Based joining biomes did not change substantially. on these recovery values we conclude that We note that there is some difficulty in mesostigmatids and astigmatids occur only comparing our abundance or density results rarely on crusts in our area and that the rich- with others in the literature because our ques- ness and abundance of prostigmatids are prob- tions were about the microarthropods using ably underrepresented. crusts, not the soil habitat in general. We col- For our 4 most abundant species, several lected smaller samples than those customarily interactions among habitat factors were of reported in the literature, which often include interest (Fig. 2). Neonanorchestes sp. was the cores to depths of 10 cm or more, as well as most abundant species we collected (Appen- the soil surface. The small samples may have dix) and yet was the most restricted by site also contributed to the low numbers of indi- (PL), season (March), and crust type (mossy; viduals we collected and may mean there are Fig. 2a, Appendix). All interactions were signif- several rare species still undetected. Because icant at 0.0001, except season × site P = 1.0, of the long recovery time of crusts, we felt this because the mean abundances were equal for technique was warranted (Belnap and Lange PL and LA in August. Numbers were also high 2001). in 1999 (at both PL and LA) in mossy crust, Nonetheless, differences in species identities but were very low in February 1999, which was reflect real differences in community structure a dry period. The sampling in March 1999 was between our habitat and these others in the after snowfall and we collected large numbers region. Overlap was too low to be accounted again after precipitation in 2000. These results for only by sampling differences. In addition, suggest that Neonanorchestes sp. is strongly the extraction method used to harvest these impacted by moisture and cool temperatures, 162 WESTERN NORTH AMERICAN NATURALIST [Volume 64 since PL was generally observed to be the ductivity. We may need to sample more thor- wetter site, with more mossy patches turning oughly following precipitation to discover the green than at LA following the same precipita- response time of the community and the specific tion event (personal observations). Zygoribat- ecological factors that govern use of crusts by ula sp. was the most evenly distributed across these organisms. sites, seasons, and crust types in 1999 and One focus of this study was the influence of 2000, making the species interesting for its habitat heterogeneity on microarthropod rich- overall lack of habitat preferences. This ness and abundance. However, from our field species seems to be less affected by moisture observations and later tests (see Data Analysis and temperature and may be actively in the section) we also discovered that mean area dif- system most of the time. The only significant fered for crust types and could be responsible interaction effect was for site, crust type, and for species richness and abundance patterns season combined (Fig. 2b, Appendix). The dif- we obtained. If area alone accounted for species ferent patterns for these 2 mites may result richness (species-area relationship reviewed from their feeding strategies: Neonanorchestes in Rosenzweig 1995) on a crust type, we would sp. feeds on vegetation or nematodes and has have expected richness to follow the pattern of a body size of approximately 400 µm, while mixed > mossy = lichen, because mean area Zygoribatula sp., with a body size of almost 1 followed that pattern. If habitat heterogeneity mm, can feed on larger particles such as hyphae drove richness, we still would have expected or spores (Behan and Hill 1978). Perhaps Neo- mixed crust to be the richest, because we saw nanorchestes sp. requires wetter crust tissues it offering a mixture of 2 distinct habitat types. than Zygoribatula sp. Both collembolan species In this region lichen crusts are not as well were more abundant in March at PL and developed vertically as the mosses; therefore, occurred on all crust types (Figs. 2c–d), even if habitat heterogeneity were responsible, we though the species vary in body size, colora- would have also expected the lowest richness tion, and mobility. Cryptopygus ambus is the on lichen. larger of the 2 with a body length of 1.5 mm, We found that richness on mixed crust did dark pigmentation, and a well-developed spring- not differ significantly from mossy (Fig. 1, Table ing structure (furcula) used for walking or for 1), so neither area nor habitat heterogeneity jumping. Tullbergia iowensis is <1 mm in alone or in concert explains the patterns seen length, is pale and eyeless, and has no furcula, at our sites. These results, along with amount showing that it spends more time in soil or of species overlap observed and seasonal dif- crust layers than at the surface (Christiansen ferences in richness and abundance, allow us and Bellinger 1980). to propose mechanisms that might account for From results in this paper and in Shepherd these patterns: (1) secondary chemical com- et al. (2002) several consistent patterns emerged: pounds, such as phenolic acids in lichens and (1) we found high numbers of mites during lignin-like compounds in mosses, may influence cool seasons following precipitation, (2) Neo- their palatability (Lawrey 1987) and therefore nanorchestes sp. occurred primarily in mossy presence/abundance of microarthropods; (2) crusts rather than in the other 2 types, (3) Zy- seasonal moisture may be available longer in goribatula sp. occurred in low numbers winter than in summer because of low air tem- throughout the year in all 3 crust types, (4) C. peratures, which may increase production in ambus was collected primarily during the crusts, offering more water and food resources to spring, and (5) T. iowensis occurred in both microarthropods; and (3) species overlap of spring and fall, and so far, C. ambus has not 57%–62% suggests that the fauna is made up been collected from LA. This last point is in- more of generalists than specialists. Neverthe- triguing because the 2 arroyos are separate less, the 4 dominant species revealed significant drainages and yet contain the same kinds of crust type and seasonal preferences (Fig. 2). crusts and are close enough to experience the Crusts may provide resources when vascular same weather conditions. plant growth is slowed or stopped, as in winter. The many rare species and large variance This time of year is less commonly sampled in in abundance in samples within a season or ecological studies but may be important for crust type suggest that this system may respond crust systems, which can function even at tem- very quickly to changes in moisture and pro- peratures near freezing (Lange 2001). 2004] MICROARTHROPODS ON CRYPTOBIOTIC CRUSTS 163

The array of taxa and trophic groups we BLOCK, W. 1979. Nanorchestes antarcticus Strandtmann have found suggests that use of this habitat is (Prostigmata) from Antarctic ice. Acarologia 21: 173–176. not accidental, although it is probably not ex- BLOCK, W., AND P. C ONVEY. 1995. The biology, life cycle clusive. Two of our results suggest that crusts and ecophysiology of the Antarctic mite Alaskozetes do contribute to microarthropod diversity: (1) antarcticus. Journal of Zoology (London) 236:431–449. our species composition in crusts overlapped BOOTH, R.G., AND M.B. USHER. 1986. Arthropod communities in a maritime Antarctic moss-turf habitat: life only slightly (approximately 20%) with that for history strategies of the prostigmatid mites. Pedobi- neighboring regions from studies based on soil ologia 29:209–218. and litter (Shepherd et al. 2002), and (2) sev- CHRISTIANSEN, K., AND P. B ELLINGER. 1980. The Collem- eral of our predominant taxa (Cryptopygus, bola of North America north of the Rio Grande. Grinnell College, Grinnell, IA. 1321 pp. Zygoribatula, and members of the Nanorchest- EDWARDS, C.A., AND K.E. FLETCHER. 1971. A comparison idae) are associated with mosses and lichens in of extraction methods for terrestrial arthropods. IBP other arid systems (Behan and Hill 1978, 1980, Handbook 21:150–185. Block 1979, Block and Convey 1995). EVANS, R.D., AND J.R. JOHANSEN. 1999. Microbiotic crusts and ecosystem processes. Critical Reviews in Plant Microarthropod species may be influencing Sciences 18:183–225. such processes as nutrient cycling and decom- GILLER, P.S. 1996. The diversity of soil communities: the position directly through herbivory on crusts “poor man’s rainforest.” Biodiversity and Conservation or indirectly through predation and detritivory. 5:135–168. KETHLEY, J. 1991. A procedure for extraction of micro- Our current studies help establish a baseline arthropods from bulk soil samples with emphasis on to compare with other habitat types and to track inactive stages. Agriculture, Ecosystems and Envi- species changes that may be due to changing ronment 34:193–200. land use practices or climate change (Wolters LANGE, O.L. 2001. Photosynthesis of soil-crust biota as dependent on environmental factors. Pages 217–240 et al. 2000). The crust/arthropod relationship in J. Belnap and O.L. Lange, editors, Biological soil is found worldwide in arid environments and crusts: structure, function and management. Springer- is probably an ancient association, perhaps 400 Verlag, Berlin. 503 pp. million years old (Walter and Proctor 1999). LAWREY, J.D. 1987. Nutritional ecology of lichen/moss arthropods. Pages 209–233 in F. Slansky, Jr., and J.G. Crusts may act as a conduit between above- Rodriguez, editors, Nutritional ecology of insects, and belowground processes, linking soil fauna mites, spiders and related invertebrates. John Wiley, (micro- to mesoscale) with surface fauna (meso- New York. 1016 pp. to macroscale). LUDWIG, J.A., AND J.F. REYNOLDS. 1988. Statistical ecology: a primer on methods and computing. John Wiley, New York. 337 pp. ACKNOWLEDGMENTS MACFADYEN, A. 1962. Soil arthropod sampling. Advances in Ecological Research 1:1–34. MAGURRAN, A.E. 1988. Ecological diversity and its mea- We would like to thank the USDA Forest surement. Princeton University Press, Princeton, NJ. Service for permission to use sites in the Cibola 179 pp. National Forest, Ed Bedrick for statistical MCCUNE, B., AND M.J. MEFFORD. 1999. PC-ORD: Multi- advice, and Manuel Molles and Diana Northup variate analysis of ecological data, version 4. MjM for laboratory space. Two reviewers also made Software Design, Gleneden Beach, OR. 237 pp. ROSENZWEIG, M.L. 1995. Species diversity in space and valuable comments on the manuscript. time. Cambridge University Press, New York. 436 pp. SANTOS, P.F., J. PHILLIPS, AND W. G. W HITFORD. 1981. The role of mites and nematodes in early stages of buried LITERATURE CITED litter decomposition in a desert. Ecology 62:664–669. SAS INSTITUTE, INC. 1999. SAS/STAT user’s guide, version ANDRE, H.M., X. DUCARME, AND P. L EBRUN. 2002. Soil bio- 8. SAS Institute, Inc., Cary, NC. 1243 pp. diversity: myth, reality or conning? Oikos 96:3–24. SHEPHERD, U.L., S.L. BRANTLEY, AND C.A.TARLETON. 2002. BEHAN, V.M., AND S.B. HILL. 1978. Feeding habits and Microarthropods on cryptobiotic crusts: a call for spore dispersal of oribatid mites in the North Ameri- greater knowledge. Journal of Arid Environments can arctic. Revue d’Ecologie et de Biologie du Sol 52:349–360. 15:497–516. WALTER, D.E., J. KETHLEY, AND J.C. MOORE. 1987. A hep- ______. 1980. Distribution and diversity of North Ameri- tane flotation method for recovering microarthro- can Arctic soil Acari. Pages 717–740 in D.L. Dindal, pods from semiarid soils, with comparison to the editor, Soil biology as related to land use practices. Merchant-Crossley high-gradient extraction method Environmental Protection Agency, Washington, DC. and estimates of microarthropod biomass. Pedobi- 880 pp. ologia 30:221–232. BELNAP, J., AND O.L. LANGE. 2001. Biological soil crusts: WALTER, D.E., AND H.C. PROCTOR. 1999. Mites: ecology, structure, function and management. Springer-Ver- evolution and behaviour. CABI Publishing, Oxon, lag, Berlin. 503 pp. United Kingdom. 322 pp. 164 WESTERN NORTH AMERICAN NATURALIST [Volume 64

WOLTERS, V., W.L. SILVER, D.E. BIGNELL, D.C. COLEMAN, Received 2 December 2002 P. L AVELLE, W.H. VAN DER PUTTEN, P. DE RUITER, ET Accepted 11 June 2003 AL. 2000. Effects of global changes on above- and belowground biodiversity in terrestrial ecosystems: implication for ecosystem functioning. BioScience 50:1089–1098.

APPENDIX. Arthropod species and relative abundance by season and crust type. a = “accidental” species, l = found only on lichen, m = found only on mossy, x = found only on mixed.

______Lichen ______Mossy ______Mixed TAXON Mar Aug Mar Aug Mar Aug

MITES Mesostigmata Family Hypoaspididae Hypoaspis (Geolaelaps) sp.m 1 Endeostigmata Family Nanorchestidae Bimichaelia sp.x 1 Neonanorchestes sp. 7 2 606 4 74 1 Speleorchestes sp. 12 1 27 10 8 4 Prostigmata Family Anystidae Erythracarus sp. 1 2 1 375 Family Bdellidae Spinibdella cronini Baker & Blalock 1 2 3 1 Family Caeculidae Caeculus sp.m 1 Family Eupodidae Eupodes sp. 5 4 1 20 Family Penthaleidae Penthaleus sp.m 1 Family Raphignathidae Raphignathus sp.m 1 Family Teneriffiidae Neoteneriffiola uta (Tibbetts) 2 3 1 Family Tetranychidae Bryobia sp. 1 1 2 Family Tydeidae Tydeus sp. 7 4 45 8 17 6 Oribatei Family Brachychthoniidae Neobrachychthonius sp. 6 10 1 Superfamily Carabodoidea carabodoid sp. 10 14 11 5 19 4 Family Ceratozetidae ceratozetid sp. 3 1 4 Family Cymbaeramaeidae Scapheremaeus sp.x 1 Family Gymnodamaeidae Joshuella striata Wallwork 1 3 1 Family Oribatulidae Zygoribatula sp. 26 15 21 24 19 47 Family Trhypochthoniidae Trhypochthonius sp.x 2 Astigmata Family Acaridae acarid sp.m 1 2004] MICROARTHROPODS ON CRYPTOBIOTIC CRUSTS 165

APPENDIX. Continued.

______Lichen ______Mossy ______Mixed TAXON Mar Aug Mar Aug Mar Aug

COLLEMBOLA Family Entomobryidae entomobryid sp.l 4 Family Hypogastruridae hypogastrurid sp.x 2 Family Isotomidae Cryptopygus ambus Christiansen & Bellinger 51 77 22 Family Onychiuridae Tullbergia iowensis Mills 74 2 37 16 18 6 Family Sminthuridae Bourletiella sp. 18 7 10 5 10 10

NON-MITE ARACHNIDA Pseudoscorpiones Family Opiidae Serianus dolosus Hoff m 1 Araneae Family Gnaphosidae Drassyllus sp.l 1 Family Linyphiidae linyphiid sp.m 1

INSECTA Diplura Family Campodeidae Metriocampa sp.x 1 Family Japygidae japygid sp. 1 2 Heteroptera Family Lygaeidae lygaeid sp.a 11 Family Miridae mirid sp.a 1 Homoptera Family Cixiidae cixiid sp.a 1 Thysanoptera Family Thripidae Arorathrips sp. 4 5 3 Frankliniella sp. 4 2 5 521 Coleoptera undetermined larvaa 1 Lepidoptera Family Geometridae geometrid larvaa 1 Hymenoptera Superfamily Chalcidoidea chalcidoid sp.a 11 Family Formicidae Forelius pruinosus (Roger) 2 4

TARDIGRADA 15 1244

SELECTION OF ANTS BY THE AMERICAN BLACK BEAR (URSUS AMERICANUS)

Janene Auger1, Gary L. Ogborn2, Clyde L. Pritchett3, and Hal L. Black1

ABSTRACT.—We examined selection of ants as food by black bears (Ursus americanus) in Utah by comparing the genera of ants we sampled from study plots in 5 vegetation types with those found in bear scats. In the plots we found 641 ant colonies representing 18 genera. Five genera comprised 85% of all colonies sampled: Formica, Lasius, Camponotus, Tapinoma, and Myrmica. Thirteen genera were found in scats, but 99% were composed of the same 5 listed above. Limited utilization of some ant genera by black bears may reflect body size, colony size, nest type, and presence or absence of a functional sting. Fifty-three percent of all ant colonies in sample plots were found under rocks. Energy values of ants ranged from 4.9 to 6.2 cal ⋅ g–1 dry weight. Pupae of Formica and Camponotus contained slightly more fat than respective workers, but the relationship was reversed for Lasius. Pupal cases were found in 33% of the scats, and bears may prefer ant brood because they are more digestible than adults and lack mechanisms of defense. Ants are a predictable and ubiquitous food source for black bears.

Key words: myrmecophagy, ants, black bears, selective foraging, nutrition, ant colonies.

Although ants (Fomicidae) have been rec- Division of Wildlife Resources (UDWR). This ognized as a component of black bear diets is a hunted population and, as suggested by a throughout North America (Bigelow 1922, Tisch sustained harvest, a stable one as well (Bates 1961, Hatler 1972, Landers et al. 1979, Beeman and Henry 1999). This semi-isolated mountain and Pelton 1980, Graber and White 1983, range lies between latitudes 38°15′ and 38°40′N Maehr and Brady 1984, Rogers 1987, Raine and between longitudes 109°00′ and 109°30′W. and Kansas 1990, Johnson 1996, Noyce et al. Elevation ranges from 1690 m to 3914 m. 1997), few authors have identified ants found Lower canyons and plateaus are rather xeric with in scat below the family level (for exceptions mean annual precipitation <250 mm, while see Johnson 1996, Noyce et al. 1997, Swenson higher elevations may receive annual precipi- et al. 1999, Mattson 2001). Because black bears tation of >3000 mm per year. Precipitation at expend considerable energy and time foraging 2130 m measured over a 45-year period aver- for ants, these insects appear to be an impor- aged 322 mm, with maximum moisture in the tant food item (Rogers 1987, Raine and Kansas form of rain occurring from July through Octo- 1990, Noyce et al. 1997), at least seasonally; ber. May and June are the driest months, aver- yet, little is known about species preferences aging 20 mm and 17 mm, respectively (Rich- or habitats associated with ant consumption by mond 1962). Richmond (1962) characterized bears. In this study we compare the genera of and mapped major vegetation types along the ants eaten by bears with the relative abundance climatic gradient that are easily recognizable of these genera in various vegetation types in and similar to the life zones of Merriam (1898). bear habitat. We also report size diversity and distribution of nest types. METHODS

STUDY AREA We sampled in the 5 most common and extensive vegetation zones throughout the moun- The study was conducted on the LaSal tains, all of which are utilized by black bears Mountains of southeastern Utah where the as foraging habitat (Richmond 1962, Richard- black bear population is managed by the Utah son 1991). These zones include spruce-fir, aspen

1Department of Integrative Biology, Brigham Young University, Provo, UT 84602. 2Utah Division of Wildlife Resources, 1115 N. Main, Springville, UT 84663. 3Monte L. Bean Museum of Life Sciences, Brigham Young University, Provo, UT 84602.

166 2004] ANT SELECTION BY BLACK BEARS 167

TABLE 1. Major vegetation types sampled, number of plots, total area sampled, and total area in each vegetation type on the LaSal Mountains, UT, above 1829 m and below alpine tundra. # of Search Area % total Available % total sample time sampled area habitat available Vegetation types plots (min) (ha) sampled (ha) habitat Aspen 21 368 0.365 14.0 15,750 20.0 Oak–Mountain brush 19 474 0.693 26.5 18,620 23.6 Pinyon-Juniper 23 557 0.536 20.5 24,670 31.3 Ponderosa 16 398 0.492 18.8 10,530 13.3 Spruce-Fir 23 349 0.527 20.2 9,300 11.8 TOTALS 102 2146 2.613 100 78,870 100.0

meadow, oak–mountain brush, ponderosa pine, weighed 100, and most were one-eighth sam- and pinyon-juniper communities (see Richard- pled as follows: each scat was fragmented until son 1991 for a list of common plants in the it would pass through a 1 × 1-cm mesh screen. study area). These 5 vegetation types comprise Fragments were placed on a 46-cm2 cloth on 81.6% of the area above 1829 m. We did not which lines connecting diagonal corners had search for ants in alpine tundra and sagebrush been drawn. Two opposite corners were brought communities, which make up 2.6% and 15.8%, together over the center of the cloth. Holding respectively, of the area above 1829 m (Table 1). the 2 corners together, we lifted the cloth off We searched for ant colonies from May to the table, gently shook it vertically 5–7 times, August 1989 in 102 nonrandomly selected rec- and then laid it flat. The other 2 corners were tangular plots. Plot size averaged 256 m2 and brought together over the center and the cloth the total area sampled was 26,136 m2. The 5 was shaken as before. Three or 4 repetitions of common vegetation types were sampled un- this shaking sequence ultimately centered the evenly for logistical reasons. From a digitized scat on the cloth in an elliptical pile. We bisected vegetation map (Richmond 1962), we derived the scat perpendicular to the length of the pile total available area for each major habitat type with a ruler, using the diagonal lines as a refer- (Table 1). We overturned rocks that were fist- ence. One half was removed and the remain- sized or larger and searched the perimeters of ing half was shaken and bisected as before. We rocks too large to move. We searched under repeated this procedure until a one-eighth sam- litter using a garden rake as necessary, turned ple of the original scat was obtained. Fourteen cow pies, and opened logs and stumps using a of the smallest scats were one-fourth sampled. hatchet. Plots were searched until all substrates Samples that deviated more than 2 g from their thought to contain ants were investigated. expected mass, calculated from dry mass of Colonies were defined as aggregations of adult the entire scat, were recombined with the rest ants accompanied by brood (eggs, larvae, and of the scat and resampled. pupae); however, we counted as colonies aggre- Ant head capsules were removed from the gations where, though brood was not found, samples, identified to genus, and counted with nest entrances were accompanied by active the aid of a dissecting microscope. We assumed workers. When nests were present we recorded that <20 head capsules per genus per scat nest construction type (e.g., under rock, in sample indicated incidental ingestion; thus, wood, or in dirt or thatch mounds) and pre- we did not include those samples in the analy- served ants from each colony in 70% ethanol. sis. Head counts of each sample were multi- Identification to genus was made using keys of plied by the appropriate factor (8 or 4) to esti- Allred (1982) and Wheeler and Wheeler (1986). mate total number of ants per scat. Presence For representative samples of each genus, we or absence of alate head capsules or pupal cases measured body length in natural posture to in each scat was recorded. Acanthomyops speci- the nearest 0.5 mm. mens were combined with Lasius because these During 1988 and 1989 black bear scats genera were impossible to distinguish when were collected as encountered. Scats were air- maxillary palps were broken off during digestion or oven-dried. From the scats containing >1% or scat preparation. Additionally, we collected ants by volume, we randomly selected and vomitus from a snared bear that contained 168 WESTERN NORTH AMERICAN NATURALIST [Volume 64 undigested workers, larvae, and pupae. The sity (ANOVA, P = 0.009, df = 101, F = 3.569), specimen was preserved in 70% ethyl alcohol with aspen habitats having a significantly and individual ants were identified and greater mean colony density (450 colonies ⋅ counted. ha−1) than spruce-fir habitats (170 colonies ⋅ Nutritional composition of the 5 ant genera ha−1) as indicated by Tukey pairwise compar- was assayed according to standard procedures isons. Six genera were found in all vegetation of the Association of Official Analytical Chemists types ranging from low-elevation pinyon- (Williams 1984). Percent water was determined juniper to high-elevation spruce-fir (Table 2). by drying fresh samples to a constant weight Formica and Lasius, the most common genera at 105°C. Crude fiber content was measured found, were more evenly distributed between after digestion of a sample with 1.25% H2SO4 habitats than were Myrmica, Camponotus, and 1.25% NaOH solutions. Total nitrogen con- Leptothorax, and the small Tapinoma (Table 2). tent was determined using the semi-automated High-elevation spruce-fir contained only 12.6% Kjeldahl method. Fat content was measured of the colonies. Nearly half of all colonies sam- directly using anhydrous ether extraction. pled were in either aspen (n = 152) or oak– Finally, ash content was measured after incin- mounain brush (n = 151). eration at 525°C. Sufficient sample material Colonies under rocks were common in all was not available to determine ash content of habitats (Table 3). Colonies under wood (pri- Tapinoma or Myrmica. marily deadfall) and in rotting and live woody Other nutritional parameters were calcu- tissue were most common in aspen and lated as follows. For pupae, we multiplied total spruce-fir. Litter (mainly leaves) provided lit- nitrogen by the constant 6.25 to obtain crude tle suitable habitat for colonies and was even protein (CP). For workers, 0.88 was subtracted less important than cow dung. Mound colonies from %N before calculating CP to adjust for were distributed throughout all habitats but nitrogen bound in the indigestible chitin of constituted only 10.3% of colonies found. the exoskeletons (Wigglesworth 1972, Noyce et Only Pogonomyrmex was not found to al. 1997). We determined percent carbohydrate establish colonies under rocks (Table 4). This by difference (100 minus the sum of crude genus is characterized by elevated rock/soil protein adjusted for chitin, fat, and ash). An mounds that are conspicuous, devoid of vege- estimate of energy content was calculated tation, and important in thermoregulation of using the following conversion factors: 4.8 cal ⋅ the colony and in incubation of brood. Five g−1 crude protein, 9.5 cal ⋅ g−1 fat, and 4.2 cal ⋅ rare genera in our sample were found only g−1 carbohydrate. under rocks. Formica utilized all nest types as did Myrmica. RESULTS We found anecdotal evidence of bears searching for ants and other insects in opened Ant Availability logs, stumps, thatched mounds, and turned We searched 102 plots, a total of 35.8 ha, cow dung and rocks. Of rocks turned by bears, and found 641 ant colonies representing 18 we observed that 1 was estimated to weigh genera. Ninety-two percent of our sample 139 kg, but smaller rocks, some weighing <0.5 plots contained colonies, and 85% of the colonies kg, were the norm. On 1 trail nearly every were Formica, Lasius, Tapinoma, Myrmica,or rock was turned for about 150 m, but we Camponotus. Three genera—Stenamma, Myr- found that most rocks did not have evidence mecocystus, and Crematogaster—were found of ant colonies under them (e.g., no ants, gal- only once. Brood was found in 92.4% of the leries, or chambers). colonies. Ant Utilization Genus richness was greatest in pinyon- juniper where 15 genera were found and least We collected 791 bear scats, 309 of which in aspen where 6 were found (Table 2); how- contained >1% ants by volume. We randomly ever, mean colony density in pinyon-juniper selected 100 of these for analysis. Although 13 was slightly lower than that in aspen, oak– genera were identified in scats, Formica, mountain brush, and ponderosa pine. Six gen- Lasius, Tapinoma, Myrmica, and Camponotus era were unique to pinyon-juniper habitat. comprised 85% of ants utilized by bears. Scats Habitat had a significant effect on colony den- contained a mean of 3.1 ± 1.8 (s) ant genera 2004] ANT SELECTION BY BLACK BEARS 169

TABLE 2. The percent of ant colonies by genus found in 5 habitat types in the LaSal Mountains, UT. Percentages under the habitat heading sum to 100% within rows.

______% of colonies by habitat Pinyon- Oak–Mountain Genus Colonies Juniper Ponderosa brush Aspen Spruce-Fir Acanthomyops 3 33.3 66.7 Aphaenogaster 4 75.0 25.0 Camponotus 51 62.8 7.8 5.9 9.8 13.7 Conomyrma 2 100.0 Crematogaster 1 100.0 Forelius 11 81.8 18.2 Formica 178 11.8 17.4 30.9 25.3 14.6 Lasius 155 7.7 26.5 21.9 23.2 20.7 Leptothorax 30 10.0 10.0 6.7 56.7 16.7 Liometopum 4100.0 Monomorium 11 100.0 Myrmecocystus 1 100.0 Myrmica 84 2.4 28.6 11.9 46.4 10.7 Pheidole 9 100.0 Pogonomyrmex 4 100.0 Solenopsis 16 37.5 12.5 50.0 Stenamma 1 100.0 Tapinoma 76 11.8 26.3 47.4 13.2 1.3 ALL GENERA 641 19.5 20.6 23.6 23.7 12.6 each. The genus Polygerus, though found in rather distinct habitats, only 5 genera were scats, was not identified in the colony sam- important as prey. Colonies of Formica were pling. We identified alate forms from these 5 found in a variety of substrates, but 84.7% of genera in 34% of the scats. Pupal cases were their colonies were located under rocks, in found in 33% of scats, but they were often mounds, or in soft, rotting wood, easily accessi- empty and fragmented, making detection diffi- ble to foraging bears. On the LaSal Mountains cult. Twelve percent of scats had both alate this genus is a widely distributed and rela- and pupal forms. Counting of ant heads was tively vulnerable prey to foraging black bears. straightforward; Formica yielded the highest In a neighboring low-elevation plateau to the median number of individuals per scat as well north (Book Cliffs), a similar broad distribu- as the most individuals recorded in a single tion and abundance of this genus was found scat (Table 5). (Seid 1997). Nutritional Considerations Several factors may contribute to bears’ use or avoidance of certain ant genera. Redford Fat content of ants in our sample ranged (1987) showed that mammals that prey on ants from 20.3% to 46.0% (Table 6). The value for seem to prefer subfamilies Formicinae (e.g., Lasius was the highest and that genus is the Formica, Lasius, and Camponotus) and Doli- most energy rich among those sampled at 6.2 choderinae (e.g., Tapinoma), both of which cal ⋅ g−1. Energy values for workers of Formica lack a functional sting, whereas the subfamily and Camponotus were both 4.9 cal ⋅ g−1 and Myrmicinae (e.g., Myrmica), that possesses a were approximately 20% lower than Lasius. functional sting, appears to be avoided. A sim- Pupae of Formica and Camponotus contained slightly more fat than respective workers, but ilar pattern for neotropical anteaters (Myrme- workers of Lasius contained substantially more cophagidae) was noted by Montgomery and fat than their pupae (Table 6). Lubin (1977). Our data support this pattern with a single exception: Tapinoma does not DISCUSSION have a functional sting, and yet it was seldom eaten by black bears in our study area. Ant Availability and Utilization Tapinoma adults have the smallest body size Although 18 ant genera were distributed and dry weight, which may explain in part across a large elevation gradient and within why they were less attractive to bears. 170 WESTERN NORTH AMERICAN NATURALIST [Volume 64 within rows. Note the importance of rocks

n habitats sum to 100%. Nest type 100.0 ants commonly and infrequently (respectively) consumed by black bears. 50.050.0 50.0 50.0 75.077.8 22.2 25.0 Myrmica ______100.0 100.0 100.0 100.0 and ormica F 2 3 4 1 1 9 4 4 1 51 74.5 2.0 5.9 11.7 5.9 11 36.4 54.5 9.1 1184 81.8 57.1 18.2 1.2 1.2 1.2 28.6 1.2 8.3 1.2 30 20.0 23.3 16.7 40.0 1676 100.0 52.6 1.3 11.9 29.0 2.6 2.6 640 53.1 10.3 1.1 2.5 14.7640 4.7 12.8 53.1 10.3 0.8 1.1 2.5 14.7 4.7 12.8 0.8 177155 32.2 66.5 31.6 0.6 1.9 0.6 1.9 4.5 14.9 7.3 1.9 20.9 12.9 2.3 4. The percent distribution of nest type (location) among 18 genera of ants on the LaSal Mountains, UT. Percentages sum to 100% Percentages 4. The percent distribution of nest type (location) among 18 genera ants on the LaSal Mountains, UT. 3. Percent distribution of nest type throughout major habitat types on the LaSal Mountains, UT. Percentages of nest types withi Percentages distribution of nest type throughout major habitat types on the LaSal Mountains, UT. 3. Percent LL HABITATS LL GENERA ABLE ABLE T A T A asius eptothorax onderosa pine 132 61.4 8.3 3.0 17.4 2.3 6.8 0.8 orelius ormica ogonomyrmex apinoma and the diversity of nest types used by Conomyrma Camponotus Crematogaster HabitatPinyon-JuniperP Oak–Mountain brushAspenSpruce-Fir 125 150 # of nests Rock 70.4 74.0 81 152 MoundGenusAcanthomyops 13.6 16.0Aphaenogaster Litter 32.1 22.4F Dung 16.1 0.7 Sample Under wood 0.8 5.3 2.5 Rock 3.3 In wood Rotting wood Mound 12.8 2.0 2.0 Crevice Litter 0.8 0.7 29.6 89.6 Dung Under wood 0.8 14.5 3.7 In wood Rotting wood 27.6 0.8 37.0 2.0 Crevice F Myrmica Myrmecocystus Pheidole Monomorium P L L Liometopum Solenopsis T Stenamma 2004] ANT SELECTION BY BLACK BEARS 171

TABLE 5. Ant genera found in samples of 100 black bear scats from the LaSal Mountains, UT, during 1987–1989. Only occurrences of ≥20 heads per sample for a given genus were used in computing median number of ant heads per scat. Length Total occurrences Median ant Maximum ant Genus (mm) (≥20 heads per whole scat) heads per scat heads per scat Formica 4.5–7.0 94 704 14,368 Lasiusa 3.0–5.0 52 312 12,160 Tapinoma 2.0–2.5 32 116 2712 Myrmica 4.0–5.0 17 96 736 Camponotus 7.0–12.0 22 60 1568 Monomorium 1.0–1.5 2 200 240 Leptothorax 2.5–3.0 1 32 Pheidole 1.0–1.5 2 56 88 Solenopsis 1.0–1.5 0b 16 Aphaenogaster 4.0–4.5 5 104 400 Liometopum 3.0–4.0 1 160 160 Polygerus 6.0c 0b 8 aAcanthomyops specimens are included with Lasius. bFound in scat, but never ≥20 heads in a whole scat. cGenera not represented in our colony sampling; size from Wheeler and Wheeler (1986).

Although ant nests varied in location and thatch mound search image is guaranteed suc- potential vulnerability, 12 of 18 genera in our cess when investigating Formica mounds, with study area were found in bear scats. This indi- the exception of recently vacated or dead cates that bears were successful in finding colonies. genera that were not abundant in our colony When eating ants, bears ingest brood as sample. Formica routinely build nests that well as adult workers and alates. For example, have an aboveground thatch component used a 41-kg, 2.5-year-old male bear shot in mid- as brooding chambers. Fully 31.2% of the 178 July as a nuisance bear had consumed 2.1 kg Formica colonies were the thatch variety. These (wet weight) of Formica, approximately 7840 clearly visible nests of Formica may increase workers and 54,700 brood (Seid 1997). The vulnerability of the species to foraging bears, value of this meal was about 695 calories, which could account in part for their frequent which would have provided about 37% of this consumption. Additionally, Formica and Myr- bear’s daily maintenance requirement (McNab mica were the only genera with colonies in all 1988, Robbins 1993). His intestines were empty, 8 substrate types. While both use the same suggesting that he had obtained this meal a diverse nest locations, Formica is frequently short time before death. The brood-to-adult eaten and Myrmica with its defensive sting is ratio of the stomach contents was 7:1, far greater not. Pogonomyrmex is a semiarid genus occur- than the average of 2.0 ± 0.79 (s) obtained ring at lower elevations in our study area. from sampling 379 colonies representing 8 ant Stings of these ants produce intense pain in genera in the same habitat (Seid 1997). Sam- humans and probably in bears as well. We ples taken by Seid (1997) were from beneath have never observed Pogonomyrmex in the rocks only. The vomitus of the bear we exam- examination of >1700 black bear scats from ined contained ants in a ratio of 3.8:1. Others Utah (Black unpublished data). have also reported that brood found in stomachs Given that 53% of all nests were found under significantly outnumber adult ants (Bigelow rocks and 94% of ant genera on the LaSal 1922, Hatler 1972; but see Noyce et al. 1997 Mountains use rocks as nest sites, rock-turn- for an exception for the genus Acanthomyops). ing by black bears would seem to be the forag- In light of this, if a single scat represents ing strategy of choice. Odor, ant activity, and only a portion of a meal and because several perhaps geometry of the rock (Seid 1997) are scats are produced in a 24-hour period (per- clues a bear might use to select rocks bearing sonal observation), then daily ant intake is ants; however, rocks are often turned and the greater than the analysis of an isolated scat soil beneath gives no indication that an ant would indicate. For comparison, the daily ant colony was there. In contrast, thatch mounds intake for the giant anteater (Myrmecophaga are visually distinctive, and a bear with a tridactyla) is 14,253 individuals (Montgomery 172 WESTERN NORTH AMERICAN NATURALIST [Volume 64

and Lubin 1977); for the northern tamandua 1 e −

g (Tamandua mexicana), 9000; and for the silky ⋅ anteater (Cyclopes didacylus), 700–4700 (Mont- cal gomery 1985). Brood constituted <10% of the individuals ingested by the latter 2 specialists d (Montgomery 1985). Thus, black bears would appear to rival many ant specialists as ant predators (Table 5). Seasonally, the amount of brood varies, but apparently brood is usually available regardless of season and is rather ubiquitous (Noyce Ash hydrate et al. 1997, Swenson et al. 1999, this study). We suspect that brood extraction is a primary

ains, UT. motivation for foraging at colonies and might t

Fa explain cropping behavior common in bears and other myrmecophagous species (Noyce et al. 1997, Swenson et al. 1999). Our observations at thatch mound nests of Formica revealed c intense nest reconstruction following bear attacks, with hundreds, if not thousands, of

for chitin workers teeming over the disturbed nest. If consumption of workers is most important, bears should simply disturb a colony and wait

b for immediate worker recruitment to the dam- aged site (Hölldobler and Wilson 1990). Bears may leave nests because little or no brood was found or because available brood was consumed. In the cropping scenario many workers would be consumed incidental to the ingestion of brood. Given that some Formacine ants have low formic acid content (Swenson et al. 1999), are devoid of stings, have little armor, and exhibit little aggression when nests are disturbed, black bears should be able to feed on them with relative impunity. High brood-to- fiber (N) tein (CP) adult ratios in the stomachs of bears strongly suggest that at least on some occasions adults are not the prey being harvested. O 2 Nutritional Considerations Several reasons have been proposed for the inclusion of ants in diets of omnivores. They may represent a spicy snack or condiment (Nishida and Hiraiwa 1982, Dufour 1987) or 0.41.0 67.8 73.9 8.7 10.6 6.8 9.4 42.5 58.8 32.9 24.9 supply a food high in fat and protein (McGrew Dry mass Crude Nitrogen Crude pro- CP adjusted1974, Landers et al. Carbo- 1979, Beeman and Pelton 1980, Nishida and Hiraiwa 1982, Maehr and Brady 1984, Dufour 1987, Redford 1987). There was no clear pattern in our data to indicate larvae 2.2 69.0 2.8 6.2 38.8 38.8 9.2 pupae 8.9 76.9 6.7 6.8 42.5 42.5 24.6 5.9 14.2 5.0 pupaepupae 1.9 0.5 76.8 72.6 9.2 9.1 9.0 8.0 56.3 50.0 56.3 50.0 24.1 31.7 3.6 5.3 3.2 0.2 5.1 5.4 worker 10.9 65.3 35.7 8.0 50.0 44.5 22.0 4.4 16.3 4.9 workerworker 4.3 0.9 78.6 59.6 21.5 12.6 9.5that 6.7 pupae 59.4 contain 41.9 higher 53.9 36.4 amounts 20.3 46.0of 3.4 fat than 4.0 9.6 0.8 4.9 6.2

a workers. It has been shown, however, that ant 6. Nutritional values (% dry mass) of the 5 ant genera most frequently found in black bear scats collected from LaSal Mount a and termite alates have relatively more fat 0.88) 6.25 (Noyce et al. 1997, Wigglesworth 1972), except for pupae and larvae in which chitin content is negligible. 1972), except 0.88) 6.25 (Noyce et al. 1997, Wigglesworth 6.25. ABLE

− than workers of the same species (Griffiths × T orkers and pupae combined. asius ormica apinoma 100 – (% adj. CP + % chitin fat ash), equals 12.8%. N 4.8 (% adj. CP) + 9.5 fat) 4.2 carbohydrate). (N W Myrmica Camponotus Genus Caste (mg) H L T F a b c d e 1968, Redford and Dorea 1984, Dufour 1987, 2004] ANT SELECTION BY BLACK BEARS 173

Noyce et al. 1997). We have no nutritional ACKNOWLEDGMENTS data for alates, but higher digestibility and lack of defense mechanisms of the pupae may We thank D.M. Black, K.T. Harper, S.H. make them more preferable to bears. Jenkins, D.B. Ogborn, and 2 anonymous re- Nutritionally, Formica, Lasius, and Cam- viewers, all of whom made valuable comments. ponotus workers consistently had higher crude Funding was provided by the Utah Division of fiber than their respective pupae (Table 6). Wildlife Resources, USDA Forest Service, Higher crude fiber content in adults was prob- Department of Zoology at Brigham Young ably due to chitin, because adult exoskeletons University, D Elden Beck Scholarship Fund, were not digested during fiber analysis but and private donations. remained as readily identifiable pieces in the residue measured as crude fiber. Thus, eggs, LITERATURE CITED pupae, and larvae, all of which lack thick chitin- ALLRED, D.M. 1982. Ants of Utah. Great Basin Naturalist containing exoskeletons, may be more digest- 42:415–511. ible to bears. In some areas in North America, BATES, J.W., AND A. HENRY. 1999. 1998 Utah black bear from spring emergence until the ripening of harvest Publication 99-25. Utah Department of Nat- summer mast crops, bears gain weight slowly ural Resources, Division of Wildlife Resources. Salt (Noyce and Garshelis 1998). During this time Lake City. 21 pp. BEEMAN, L.E., AND M.R. PELTON. 1980. Seasonal foods and ant utilization is higher than in other seasons feeding ecology of black bears in the Smoky Moun- (Tisch 1961, Hatler 1972, Landers et al. 1979, tains. International Conference on Bear Research Beeman and Pelton 1980, Maehr and Brady and Management 4:141–147. 1984, Rogers 1987, Raine and Kansas 1990, BIGELOW, N.K. 1922. Insect food of the black bear (Ursus americanus). Canadian Entomologist 43:49–50. Noyce et al. 1997) and may be critical to growth BRODY, A.J., AND M.R. PELTON. 1988. Seasonal changes in and maintenance. The percentages of fat, carbo- digestion in black bears. Canadian Journal of Zool- hydrate, and protein actually available to bears ogy 66:1482–1484. from ants are not known. Brody and Pelton CORNELIUS, C., G. DANDRIFOSSE, AND C. JEUNIAUX.1976. Chitinolytic enzymes of the gastric mucosa of Perod- (1988) showed that the digestibility of gross ictus potto (Primate Prosimian): purification and energy and crude protein for black bears enzyme specificity. International Journal of Bio- changes from summer to fall. Additionally, chemistry 7:445–448. bears may produce elevated production of DUFOUR, D.L. 1987. Insects as food: a case study from the northwest Amazon. American Anthropologist 89: chitinolytic enzymes when consuming quanti- 383–397. ties of ants. This has been shown for some GRABER, D.M., AND M. WHITE. 1983. Black bear food other vertebrates (Jeuniaux 1961, Cornelius et habits in Yosemite National Park. International Con- al. 1976). ference on Bear Research and Management 5:1–10. GRIFFITHS, M. 1968. Echidnas. Pergamon Press Ltd., Conclusions Oxford, UK. 282 pp. HATLER, D.F. 1972. Food habits of black bears in interior Black bears consume a variety of ant taxa Alaska. Canadian Field-Naturalist 86:17–31. but may select those that occur at high colony HÖLLDOBLER, B., AND E.O. WILSON. 1990. The ants. Belk- densities; lack a functional sting; have low nap Press of Harvard University Press, Cambridge, MA. 732 pp. formic acid content, large body size, and large JEUNIAUX, C. 1961. Chitinase: an addition to the list of colonies; and build conspicuous nests. They hydrolases in the digestive tract of vertebrates. may prefer ant brood over adults because Nature 192:135–136. brood have a lower crude fiber content and JOHNSON, L.A. 1996. Black bear myrmecophagy in the Central Upper Peninsula of Michigan. Master’s thesis, have no apparent chemical, anatomical, or Northern Michigan University, Marquette. 67 pp. behavioral defenses. Energy values of ants LANDERS, J.L., R.J. HAMILTON, A.S. JOHNSON, AND R.L. coupled with high-volume consumption sug- MARCHINTON. 1979. Foods and habitat of black bears gest that ants provide black bears with an in southeastern North Carolina. Journal of Wildlife important source of food. This study gives Management 43:143–153. MAEHR, D.S., AND J.R. BRADY. 1984. Food habits of Florida additional support to the speculation of Stir- black bears. Journal of Wildlife Management 48: ling and Derocher (1990) that black bears may 230–235. be facultatively, if not obligately, myrme- MATTSON, D.J. 2001. Myrmecophagy by Yellowstone griz- cophagous, at least seasonally. The density, zly bears. Canadian Journal of Zoology 79:779–793. MCGREW, W.C. 1974. Tool use by wild chimpanzees in diversity, and geographic distribution of ants feeding upon drive ants. Journal of Human Evolution accommodate this trophic adaptation. 3:501–508. 174 WESTERN NORTH AMERICAN NATURALIST [Volume 64

MCNAB, B.K. 1988. Complications inherent in scaling the RICHARDSON, W.S. 1991. Habitat selection and feeding basal rate of metabolism in mammals. Quarterly ecology of black bears in southeastern Utah. Mas- Review of Biology 63:25–54. ter’s thesis, Brigham Young University, Provo, UT. MERRIAM, C.H. 1898. Life zones and crop zones of the 75 pp. United States. USDA, Bureau of Biological Survey RICHMOND, G.M. 1962. Quaternary stratigraphy of the Bulletin 10:1–79, 1 map. LaSal Mountains. Geological Survey Professional MONTGOMERY, G.G. 1985. Impact of vermilinguas (Cyclopes, Paper 324. United States Department of the Interior, Tamandua: Xenarthra = Edentata) on arboreal ant Geological Survey. 135 pp. populations. Pages 351–363 in G.G. Montgomery, ROBBINS, C.T. 1993. Wildlife feeding and nutrition. Acade- editor, The evolution and ecology of armadillos, sloths, mic Press, San Diego, CA. 352 pp. and vermilinguas. Smithsonian Institute Press, Wash- ROGERS, L.L. 1987. Effects of food supply and kinship on ington, DC. social behavior, movements, and population growth MONTGOMERY, G.G., AND Y.D. Lubin. 1977. Prey influ- of black bears in northeastern Minnesota. Wildlife ences on movements of neotropical anteaters. Pages Monographs 97:1–72. 103–131 in R.L. Phillips and C. Jonkel, editors, Pro- SEID, M.A. 1997. Ant colonies under rocks as a food ceedings of the 1975 Predator Symposium. Montana source for black bears (Ursus americanus). Master’s Forest and Conservation Experiment Station, Uni- thesis, Brigham Young University, Provo, UT. 47 pp. versity of Montana, Missoula. STIRLING, I., AND A.E. DEROCHER. 1990. Factors affecting NISHIDA, T., AND M. HIRAIWA. 1982. Natural history of a the evolution and behavioral ecology of the modern tool-using behavior by wild chimpanzees in feeding bears. International Conference on Bear Research upon wood-boring ants. Journal of Human Evolu- and Management 8:189–204. tion 11:73–99. SWENSON, J.E., A. JANSSON, R. RIIG, AND F. S ANDEGREN. NOYCE, K.V., AND D.L. GARSHELIS. 1998. Spring weight 1999. Bears and ants: myrmecophagy by brown bears changes in black bears in northcentral Minnesota: in central Scandinavia. Canadian Journal of Zoology the negative foraging period revisited. Ursus 10: 77:551–561. 521–531. TISCH, E.L. 1961. Seasonal food habits of the black bear NOYCE, K.V., P.B. KANNOWSKI, AND M.R. RIGGS. 1997. Black in the Whitefish Range of northwestern Montana. bears as anteaters: seasonal associations between Master’s thesis, Montana State University, Bozeman. bear myrmecophagy and ant ecology in north-central 108 pp. Minnesota. Canadian Journal of Zoology 75: WHEELER, G.C., AND J.N. WHEELER. 1986. The ants of 1671–1686. Nevada. Allen Press, Inc., Lawrence, KS. 138 pp. RAINE, R.M., AND J.L. KANSAS. 1990. Black bear seasonal WIGGLESWORTH, V.B. 1972. The principles of insect physi- food habits and distribution by elevation in Banff ology. 7th edition. Chapman and Hall, London. 827 National Park, Alberta. International Conference of pp. Bear Research and Management 8:297–304. WILLIAMS, S., EDITOR. 1984. Official methods of analysis. REDFORD, K.H. 1987. Ants and termites as food: patterns 14th edition. Association of Official Analytical of mammalian myrmecophagy. Pages 349–399 in Chemists, Inc., Arlington, VA. 1141 pp. H.H. Genoways, editor, Current mammalogy. Plenum Press, New York. Received 18 September 2001 REDFORD, K.H., AND J.G. DOREA. 1984. The nutritional Accepted 10 May 2003 value of invertebrates with emphasis on ants and termites as food for mammals. Journal of Zoology 203: 385–395. Western North American Naturalist 64(2), ©2004, pp. 175–183

COMPARATIVE LIFE HISTORY FOR POPULATIONS OF THE SCELOPORUS GRAMMICUS COMPLEX (SQUAMATA: PHRYNOSOMATIDAE)

Aurelio Ramírez-Bautista1,3, Elsa Jiménez-Cruz1, and Jonathon C. Marshall2

ABSTRACT.—A Teotihuacán population of the Sceloporus grammicus complex was compared with other previously studied populations (Parque Nacional Zoquiapan [PNZ], Monte Alegre Ajusco [MAA], Pedregal San Angel [PSA], Cantimplora [CA], Capulín, Laguna, Paredon, Michilia, and south Texas) for variations in several life history characteristics (SVL at sexual maturity, reproductive period, ovulation and gestation time, and litter size). Mean body size at sexual maturity of females from Teotihuacán was larger than PNZ, MAA, CA, and Capulín. Reproductive period (vitellogenesis, ovulation, gestation, and birth) for the Teotihuacán population was the shortest of all populations. In the Teotihuacán population, gestation time was similar to the Capulín and MAA populations but was shorter than all other populations except the Michilia population. Embryonic development at ovulation varied among populations, with Teotihuacán and Capulín showing earlier stages (stages 1) at ovulation than all other populations. Teotihuacán, PSA, PNZ, and Texas all showed similar litter size, which were larger than Laguna, Paredon, MAA, Capulín, and CA populations. Differences in reproductive characteristics of these populations could indicate phylogenetically constrained, reproductively isolated populations, or they may be explained as merely responses to different environments.

Key words: Reptilia, Squamata, Phrynosomatidae, Sceloporus grammicus, reproduction, México, chromosome races, polytypy.

In the last 3 decades, following contributions and Congdon 1978, Dunham 1982), but this by Tinkle (1969), Tinkle et al. (1970), and Fer- approach is limited by the paucity of intra- guson et al. (1980), several studies have docu- specific studies. mented variation in life histories, population Intraspecific studies on reproductive pat- dynamics, and demography both among lizard terns have revealed geographic variation in species (Ballinger 1973, Dunham 1980) and life history characteristics such as clutch size, among populations of a single species (Ballinger egg size, fecundity, and age at maturity among 1979, Ferguson et al. 1980, Dunham 1982, Bena- populations. Among congeners variation also bib 1994, Lemos-Espinal et al. 1998). Geogra- exists in components of reproductive cycles, phic variation of life history characteristics for such as length of the reproductive season, lit- some species has been studied extensively. ter size, gestation time (viviparous species), Examples of such species include Sceloporus and snout-vent length (SVL) at sexual maturity undulatus (Ferguson et al. 1980), S. variabilis (e.g., S. variabilis [Benabib 1994]; S. grammicus (Benabib 1994), S. grammicus (Lemos-Espinal [Martínez 1985, Lemos-Espinal et. al. 1998]; et al. 1998), Urosaurus bicarinatus (Ramírez- S. jarrovi [Goldberg 1971]). Variation in these Bautista et al. 1995), and U. ornatus (Dunham reproductive characteristics might be related 1982). Variations in the life histories found in to environmental factors such as food availabil- these studies are possibly adaptations to dif- ity (Ballinger 1977, Dunham 1982), duration of ferent environmental pressures (local environ- appropriate environmental conditions (Benabib ments), but data about roles played by resource 1994), or phylogenetic history (Dunham and availability, predators, and climate on the reg- Miles 1985). ulation of populations at that time were nonex- Chromosome races of the Sceloporus gram- istent (Ferguson et al. 1980). Many studies of micus complex inhabit a range of habitats across lizard life histories have attempted to obtain the Mexican Plateau (Fig. 1), from deserts to empirical data to test current hypotheses of high-elevation mountain environments (Aré- life history evolution (Tinkle et. al. 1970, Vitt valo et al. 1991). The few populations that have

1Centro de Investigaciones Biológicas (CIB), Universidad Autónoma del estado de Hidalgo, A.P. 1-69 Plaza Juárez, C.P. 42001, Pachuca, Hidalgo, México. 2Department of Zoology, Brigham Young University, Provo, UT 84602, USA. 3Corresponding author.

175 176 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Fig. 1. Map of distribution range of 7 chromosomal races of the S. grammicus complex in central México (taken from Arévalo et al. 1991). Sample site used in our study (Teotihuacán) is indicated by the solid black arrow. In Arévalo et al. (1991), solid triangles = standard race, open triangles = high standard, solid circles = F6, open circles = F5, solid squares = F5+6, open squares = FM3, square with star embedded = FM1, and thatched square = FM2. Sites of questionable race status = open circle and locality number. Capital letters enclosed in circles show hybrid zones between certain races. Dark shading delimits México City; 2000-, 3000-, and 4000-m contours are identified by extensive gray shading, limited fine-grained gray, and white “island” volcanic peaks, respectively.

been studied all exhibit reproductive activity MATERIALS AND METHODS in which gametogenesis, courtship, and mating occur in the fall, and pregnancy proceeds over Data from the Teotihuacán population were winter with parturition during the following obtained between October 1984 and Septem- early spring (Guillette and Casas-Andreu 1980, ber 1985 at Santiago Tolman, Teotihuacán Lemos-Espinal et al. 1998). The objective of (19°41′N, 98°52′W), state of México, at an ele- this study is to compare the reproductive char- vation of 2294 m. The climate of the area is acteristics of a new population, Teotihuacán, seasonally temperate, with highest temperatures with other previously studied populations of and rainfall occurring in summer. Mean annual the Sceloporus grammicus complex. precipitation is 559.6 mm, and vegetation type 2004] SCELOPORUS GRAMMICUS: COMPARATIVE LIFE HISTORY 177 is mesquite grassland and pine forest (Rze- 3300 m and an annual precipitation of 790.5 dowski 1978). Climatic and meteorological mm. Méndez-De la Cruz (1988) studied 2 pop- data for a 15-year period (1969–1984) were ulations: Monte Alegre Ajusco (MAA; 19°13′N, recorded at the Estación Metereológica at San 99°17′W), at an elevation of 3200 m, and El Martín de las Pirámides and at García (1981). Capulín (19°11′N, 99°19′W), at an elevation of Monthly sample sizes from Teotihuacán were 3400 m. Annual precipitation for both loca- 6 to 10 females, although in some months tions was 1340 mm, and habitat was pine for- (November and December) up to 14 adult est. Lemos-Espinal et al. (1998) studied 2 pop- females were collected. All adult lizards col- ulations: Laguna (3700 m) and El Paredón lected had an SVL large enough to indicate (4400 m), located in the Campo Experimental they were sexually mature (Ramírez-Bautista Forestal San Juan Tetla (19°10′N, 98°36′W), and Vitt 1997, 1998). We sampled 118 females, state of México; the pine forest habitat had measuring snout-vent length to the nearest 0.1 1187.5 mm of annual precipitation. Table 1 mm. The smallest female (44.1 mm) showing summarizes habitat data for each location. vitellogenic follicles or embryos in the uterus Where possible, populations (Table 2) were was used as an estimation of the minimum size assigned to a chromosomal race according to (in SVL) at sexual maturity (Ramírez-Bautista criteria established by Sites and Davis (1989), et al. 1995, 1996, 1998). Gonads and fat bodies Sites (1993), and Arévalo et al. (1991, 1993). The of females were removed and weighed to the species Sceloporus anahuacus and S. palaciosi nearest 0.0001 g. are based on the Lara-Góngora (1983) descrip- Clutch size was determined by counting em- tion, although further study is needed to firmly bryos in the oviducts of adult females during establish species rank for each. the reproductive season. We calculated relative RESULTS clutch mass (RCM; Vitt and Congdon 1978) as mass of embryos (embryonic stages from 34 to Variation in Climate 40) / (females mass – clutch weight). We calcu- Teotihuacán and localities of 9 populations lated a Pearson’s product-moment correlation compared in this study differ dramatically in coefficient to test for a relationship between amount and variability of annual precipitation clutch size and SVL of females. (Table 1). Over 82% of mean annual precipita- We compare these reproductive character- tion falls in the 6 months (May–October) dur- istics with other populations from the S. gram- ing which 5 populations of S. grammicus (Teo- micus complex (sensu lato Sites 1993). Guil- tihuacán, Michilia, Texas, PSA, and CA) are in lette and Casas-Andreu (1980) studied some reproductive activity. However, other popula- reproductive characteristics of a population tions (PNZ, MAA, Capulín, Laguna, and Pare- ° ′ ° ′ from PNZ (19 41 N, 98 42 W), state of México, don) receive greater average annual precipita- in 1978–79. The pine woodland habitat at an tion as their seasonal distribution of rainfall is elevation of 3200 m had an annual precipita- more extended (April–October; García 1981). tion of 1169.3 mm. Ortega and Barbault (1984) performed a similar study from December Snout-Vent Length 1980 to December 1981 for a population from at Sexual Maturity Michilia (24°1′N, 104°40′W), Durango. This Mean body sizes of sexually mature females oak-pine forest habitat at 2480 m received an differed greatly between populations (ANOVA; average of 576 mm of annual precipitation. F5,295 = 45.08, P < 0.005; Table 2). Female Guillette and Bearce (1986) studied popula- body size from the Teotihuacán population was tions from southern Texas and the lowlands of larger than that from PNZ, MAA, CA, Capulín, Tamaulipas (26°4′N, 98°17′W) at an elevation and PSA, but the PSA populations showed of 38 m in an oak forest that received 423.8 similar size (P > 0.05). Snout-vent length at mm of annual precipitation. Martínez (1985) sexual maturity was larger at PSA than at studied 2 populations: Pedregal San Angel (PSA; Laguna, Paredon, Michilia, PNZ, MAA, Cap- 19°26′N, 99°81′W), Distrito Federal, where ulín, and CA (Table 2). the habitat, an oak-pine forest at an elevation of 2400 m, had 840 mm of precipitation annu- Reproductive Traits ally, and La Cantimplora (CA; 19°15′N, Reproductive activity (vitellogenesis, ovula- 99°11′W), in pine woodland at an elevation of tion, gestation time, and birth) varied among 178 WESTERN NORTH AMERICAN NATURALIST [Volume 64 N 7 0.24 0.45 ± ± eotihaucán complex. PNZ complex. T grassland/Pine 0.32 55.2 ), F5+6 (fixed fissions in ), F5+6 (fixed 6 0.17 5.09 ± ± CA S. grammicus , S. palaciosi 0.55 45.01 6 0.19 3.7 ± ± e studies of the PSA rcía (1981; data for a 15-year period). Sites (1993), and Arévalo et al (1991, 1993), HS 5 0.6 53.04 0.14 5.3 ± ± Capulín 5 0.16 3.72 0.61 44.5 ± ± MAA complex; SVL MMS = snout-vent length minimum and maximum at sexual maturity; SVL MMS = snout-vent length minimum and maximum at sexual complex; 4 0.07 48.8 0.25 3.51 ± ± PNZ ), F6 (fixed fission of metacentric chromosome 6, 2n = 34 ), F6 (fixed S. grammicus 3 0.06 5.2 xas . S. grammicus ± Te – x s S. 1 ± 2 1.7 5.4 ± Michilia ), S (standard, 2n = 32, ). Mean is followed by 1 0.13 6.2 ± aredon P S. anahuacas S. g. disparilis Laguna Paredon Michilia Texas S. PNZ MAA Capulín PSA CA Teotihuacán 1 0.09 3.31 ± 67 54 46 21 48 54 60 24 26 62 ————48.5 ————48.5 Laguna C) 13.1 13.1 17.4 23.3 11.1 12.0 12.0 15.1 12.0 14.8 ° 1. General habitat description including average annual precipitation and temperature for 10 localities sampled reproductiv 2. Reproductive characteristics from different female populations of the ABLE ABLE T T itellogenesis Aug–Sept Aug–Sept Aug–Dec Jul–Sept Jul–Sept Jul–Sept Jul–Sept May–Aug May–Jul Oct–Nov opulation (HS) (HS) (S) (F5+6) (F6) (HS) (HS) (S) (S) (S) emperature ( Lemos-Espinal et. al. 1998 Ortega and Barbault 1984 Guillette and Bearce 1986 1980 Guillette and Casas-Andreu Méndez-De la Cruz 1988 Martínez 1985 This study = sample size. Chromosomal races are given with each population and based on ranges established by Sites Davis (1989), (high-elevation standard, 2n = 32, chromosome 5 and 6, 2n = 36, Altitude (m)Plant communityPrecipitation (mm)T Pine 3700 1187.5 Pine 4400 1187.5 Oak/Pine 576 2480 OakP 423.8 —V Ovulation PineGestation timeLitter size 1169.3 2000–3200 Oct–MayRangeSVL (mm) Oct Pine 3200SVL MMS 3.64 Oct–May 1340N 1 Jan–May2 Pine 3400 2–5 Oct 39–523 13404 Nov–May5 6 Oak/Pine 39.2–507 Sept–May 2400 2–4 840 Jan Pine Nov–April 44–60 3300 790.5 Nov–April Oct–Nov Mesquite 3–9 Sept–April 2200 — 559.6 Sept Oct–May 3–7 42.3–61.2 Oct–Nov Nov–April 37.9–54 Oct–Nov 3–7 38.6–50 Sept 2–6 40–62 Sept 2–6 34–55 Nov 44.1–72.3 2–11 2–6 2–9 (Parque Nacional Zoquiapan), MAA (Monte Alegre, Ajusco), PSA (Pedregal San Angel), and CA (Cantimplora) data were taken from Ga Nacional Zoquiapan), MAA (Monte Alegre, Ajusco), PSA (Pedregal (Parque 2004] SCELOPORUS GRAMMICUS: COMPARATIVE LIFE HISTORY 179 these 10 populations of the S. grammicus com- = 0.76, P < 0.05; Méndez-De la Cruz 1988), plex. The Teotihuacán population showed a Laguna (r = 0.85, P < 0.0001; Lemos-Espinal shorter reproductive period (7 months, Octo- et al. 1998), and Paredon (r = 0.89, P < 0.001; ber–April; Table 2) than Laguna, Paredon, and Lemos-Espinal et al. 1998). This pattern indi- Michilia (10 months, August–May), MAA (10 cates that litter size is proportional to maternal months, July–April), Texas and PNZ (11 months, body size in all populations. July–April), PSA (12 months, May–April), and Fat Body Cycle CA (13 months, May–May). Gestation times from Teotihuacán (6 months), Capulín (6 The Teotihuacán and Texas populations were months), Michilia (5 months), and MAA (6 the only studies used to analyze reproductive months) populations were all shorter than activity with fat body cycle in females. Repro- Texas (7 months), Laguna, Paredon, PSA, and ductive cycle of females from the Teotihuacán CA (all 8 months), and PNZ (9 months) popu- population did not show any relationship be- lations. tween log10 gonadal mass and log10 fat body 2 mass (R = 0.016, F1,117 = 1.83, P > 0.05), Embryonic Development and a similar pattern is shown in the Texas at Ovulation population (Guillette and Bearce 1986). Developmental stages of eggs at ovulation Relative clutch mass was measured only varied among populations. At Teotihuacán egg from the Teotihuacán population, and it was ± development varied from stage 1 to stage 8 0.338 0.024 (0.015 – 0.80; N = 57). Relative (ovulation occurred in November), at Michilia clutch mass was correlated with female SVL (r all eggs were at stage 4 (ovulation in January), = 0.449, F1,55 = 13.88, P < 0.0005), and there at Texas, stage 12 (November), at PZN, stage 2 was significant variation in RCM among months (ANOVA; F = 17.28, P < 0.0001). Females (September), at MAA eggs were either in stage 5,55 – 2 or 3 (November), at El Capulín eggs varied exhibited an RCM during November (x = 0.162 ± 0.021, N = 13) and December (x– = from stage 1 to 4 (November), and at PSA and ± CA eggs showed stage 5 development (Sep- 0.233 0.025, N = 11) lower than following tember). Snout-vent length at birth was mea- months, which increased significantly from January (x– = 0.360 ± 0.037, N = 10) to April sured in only 3 populations; for the Teotihua- – ± cán population it ranged from 18.0 mm to 22.0 (x = 0.555 0.061, N = 4; P < 0.0001). mm, and for both Paredon and Laguna popu- DISCUSSION lations SVL at birth ranged from 19.0 mm to 20.0 mm. Reproduction in the S. grammicus complex Litter Size females (sensu Sites 1993) is characterized by viviparous fall reproductive activity (Guillette Litter size differed significantly among pop- and Casas-Andreu 1980, Ortega and Barbault ulations (ANOVA; F9,295 = 54.8, P < 0.001). 1984). This type of reproductive cycle is simi- Multiple comparisons revealed that mean lit- lar to other viviparous temperate zone species ter size for Teotihuacán, PSA, PZN, and Texas at high elevations, such as S. bicanthalis (Guil- populations did not vary significantly (F1,155 lette 1982), Barisia imbricata (Guillette and = 2.32, P > 0.05; Table 2), but these popula- Casas-Andreu 1987), B. monticola (Vial and tions showed larger litter size than Laguna, Stuart 1985), Eumeces copei (Guillette 1983, Paredon, MAA, Capulín, and CA (F8,249 = Ramírez-Bautista et al. 1996), and E. lynxe 23.5, P < 0.001). Largest litter size was from (Ramírez-Bautista et al. 1998). However, fall the Michilia population (6.2 ± 1.7; P < 0.05). reproduction is also known to occur in lowland However, litter size was significantly corre- species, such as Gerrhonotus liocephalus (Flury lated with SVL in some populations such as 1949), Eumeces egregius (Mount 1963), Scelo- Teotihuacán (r = 0.78, P < 0.001), PNZ (r = porus cyanogenys (Crisp 1964), S. poinsetti (Ball- 0.68, P < 0.001; Guillette and Casas-Andreu inger 1973), S. grammicus (Ortega and Barbault 1980), Michilia (r = 0.88, P < 0.01; Ortega 1984), S. grammicus disparilis (Guillette and and Barbault 1984), Texas (r = 0.78, P < 0.001; Bearce 1986), and S. jarrovii (Ramírez-Bautista Guillette and Bearce 1986), MAA (r = 0.62, P et al. 2002). These data suggest that fall repro- < 0.05; Méndez-De la Cruz 1988), Capulín (r duction could be an adaptation to factors other 180 WESTERN NORTH AMERICAN NATURALIST [Volume 64 than high elevation (Guillette and Casas-Andreu altitude populations (Smith et al. 1994). This 1980, 1987, Guillette 1982, Guillette and Bearce pattern could correspond to the Teotihuacán 1986). population, because it is the lower-altitude Fall reproduction occurs at both low and locality (Table 1). Larger females from the Teo- high elevation in several species within differ- tihuacán population might be the result of ent generic lineages, such as Sceloporus (Phry- greater food availability and/or a greater amount nosomatidae), Barisia (Anguidae), and Eumeces of time spent in feeding (reproductive activity (Scincidae). Within each of these species, groups [vitellogenesis] is later in Teotihuacán than in inhabiting mountain habitats of México have other populations). However, growth rates of independently evolved a similar set of repro- S. grammicus from different environments ductive characteristics (Guillette and Casas- (Laguna and Paredon) were similar regardless Andreu 1980, Guillette and Bearce 1986, of food availability and environmental temper- Ramírez-Bautista et al. 1998). The advantage ature (Lemos-Espinal and Ballinger 1995). of a fall reproductive strategy is the produc- Although growth rates in lizard species have tion of young at a time when resources are been correlated with food, precipitation, and abundant (spring), which is particularly advan- temperature of the environment, for the Teoti- tageous in environments (temperate and tropi- huacán and other populations additional fac- cal zones where this type of reproduction tors appear to influence SVL at sexual matu- occurs) with short growing seasons (Guillette rity. Although precipitation (559.6 mm) and 1983). temperature (14.8°C) from Teotihuacán are low, the area nevertheless has resources (insects) as Snout-Vent Length abundant as or more abundant than in all at Sexual Maturity other areas (Table 1). Life history characteristics of S. grammicus Reproductive Traits from Teotihuacán vary from those of populations previously studied from different environments This study indicates a marked difference in (Table 2). Mean SVL at sexual maturity for reproductive activity between the Teotihuacán females from Teotihuacán was larger than for and other populations. For example, reproduc- other populations (Table 2). These data could tive period was shorter at Teotihuacán than at be related to time available for growth before any other population. While gestation time reaching sexual maturity or different growth was similar to that of other populations such as rates and food availability or both (Ballinger El Capulín, Michilia, and MAA, it was shorter 1977, 1979, Ramírez-Bautista and Vitt 1997). than Texas, Laguna, Paredon, PSA, CA, and Gestation times for Teotihuacán and Michilia PZN. Developmental stages of eggs at ovulation populations (November–April and January–May, also varied among populations; for example, in respectively) were as short as or shorter than Teotihuacán and Capulín females ovulation gestation in all other populations (Table 2). occurs at an earlier stage (stage 1) than in the Parturition occurs in April and reproduction other populations. Variation in these charac- begins in October for Teotihuacán. These data teristics among populations might be explained indicate that females reach sexual maturity at by the major influence of the environment, as age 7 months for Teotihuacán and 8 months occurs in other lizard species (Ballinger 1979, for Michilia. These data also suggest that females Dunham 1980, Ferguson et al. 1980, Ramírez- from these populations have more time to grow, Bautista et al. 1995). Shorter reproductive per- reaching sexual maturity at a larger size than iod (vitellogenesis, ovulation, and gestation time) populations in other species (Smith et al. 1994). for the Teotihuacán population could be ex- However, even though the Teotihuacán popu- plained by the following: (1) length of the veg- lation has the largest SVL at maturity and long etative growing season may be shorter since growth period before maturity, this trend in precipitation is lower than in other populations not supported by comparisons with other pop- with longer reproductive period (Table 1), and/ ulations in our study. For instance, PSA has or (2) late reproduction (vitellogenesis: October– the 2nd largest SVL but has nearly the short- November) would allow lizards more time for est growth period. growing, and they could have larger body size Females of S. jarrovi from low-altitude pop- at sexual maturity (as occurs in this population). ulations grow faster than females from high- Cost of a shortened reproductive period may 2004] SCELOPORUS GRAMMICUS: COMPARATIVE LIFE HISTORY 181 be small compared with the advantage gained do prove valid, they might be explained by the by a longer growth period and larger SVL at HS race showing similar life history character- maturity in the Teotihuacán environment. istics due to the evolutionary history of that Litter size varied among populations and race, and the smaller differences (vitellogene- increased with female body size at all locali- sis and gestation time) could be a local adapta- ties (Guillette and Casas-Andreu 1980, Ortega tion. The other populations (chromosomes races and Barbault 1984, Guillette and Bearce 1986, S, F6, F6+6) vary in life history characteristics; Lemos-Espinal et al. 1998). This phenomenon these differences could be a complex of local is characteristic of many phrynosomatids such adaptation tending toward evolutionary diver- as Urosaurus bicarinatus (Ramírez-Bautista et gence (i.e., genetic differences between popu- al. 1995), U. (Dunham 1982), S. spinosus and lations). Again, more in-depth analysis is needed S. horridus (Valdéz-Gonzalez and Ramírez- to determine whether life history traits among Bautista 2002), S. jarrovi (Ballinger 1973), and populations are due to phylogenetic constraint S. variabilis (Benabib 1994). Variation in litter or local adaptation and which environmental size among localities could be explained by factor(s) are exerting the greatest influence. among-sites variation in densities and survi- Such an analysis was not possible for the above vorship; for example, litter size from Michilia study, because data for each individual were was higher (6.2 ± 1.7) than that of Laguna available only for the Teotihuacán population. (3.64 ± 0.09) and Paredon (3.31 ± 0.13), where- This study provides a very general comparison as densities of these populations were 42 adult of life history traits between populations and individuals ⋅ ha–1, 74 individuals ⋅ ha–1, and 146 at the same time gives an in-depth description individuals ⋅ ha–1, respectively (Lemos-Espinal of life history traits for a new population. et. al. 1998, Ortega et al. 1999). We could not compare the RCM for the ACKNOWLEDGMENTS Teotihuacán population because no previous study has been carried out in other popula- We thank A. Nieto-Montes de Oca for his tions. This study showed that values of RCM help in the field; J.W. Sites, Jr., and M. Belks increased with an increase in embryonic de- for reading the manuscript; J. Barba-Torres for velopment. Vitt and Price (1982) tested differ- his help in statistics analysis; A. Borgonio and ences in RCM between phrynosomatid and R. León-Rico for their logistic help. teiid lizards and found that in Sceloporus, RCM is higher (x– = 0.256 ± 0.009) than in LITERATURE CITED Cnemidophorus (x– = 0.148 ± 0.006) species. RCM for S. grammicus prior to birth ranged ARÉVALO, E., C.A. PORTER, A. GONZÁLEZ, F. MENDOZA, J.L. CAMARILLO, AND J.W. SITES, JR. 1991. Population from 0.360 (January) to 0.555 (April); this pat- cytogenetics of the Sceloporus grammicus complex tern is similar to that of other species such as (Iguanidae) in central México. Herpetological Mono- S. jarrovi (0.150–0.388 [Parker 1973]; 0.138– graphs 5:79–115. 0.468 [Ramírez-Bautista et al. 2002]). ARÉVALO, E., G. CASAS, S.K. DAVIS, G. LARA, AND J.W. SITES, JR. 1993. Parapatric hybridization between chromo- In comparing life history traits with chro- some races of the Sceloporus grammicus complex mosome races, we note some general trends. (Phrynosomatidae): structure of the Ajusco transect. First, some populations that belong to the Copeia 1993:352–372. same chromosome race (Laguna, Paredon, and BALLINGER, R.E. 1973. Comparative demography of two viviparous lizards (Sceloporus jarrovi and Sceloporus El Capulín in the HS race) show similar life poinsetti). Ecology 54:269–283. history characteristics; however, PSA (also an ______. 1977. Reproductive strategies: food availability as HS) does not (Table 2). In other populations of a source of proximal variation in lizard. Ecology the chromosomes races S, F6, F5+6 (Michilia, 58:628–635. Cantimplora, Teotihuacán, Parque Nacional ______. 1979. Intraspecific variation in demography and life history of the lizard Sceloporus jarrovi along an Zoquiapan, Monte Alegre Ajusco, and south altitudinal gradient in southeastern in Arizona. Ecol- Texas), life history trait similarity did not seem ogy 60:901–909. to group according to chromosome race (Table BENABIB, M. 1994. Reproduction and lipid utilization of 2). The small sampling of populations and the tropical population of Sceloporus variabilis. Herpe- absence of a rigorous testing (i.e., principal tological Monographs 8:160–180. CRISP, T. 1964. Studies of reproduction in the female ovo- components analysis) are cause for care in in- viviparous iguanid lizard Sceloporus cyanogenys terpretation of the above data. If these trends (Cope). Texas Journal of Sciences 16:481. 182 WESTERN NORTH AMERICAN NATURALIST [Volume 64

DUNHAM, A.E. 1980. An experimental study of interspe- Doctoral, Facultad de Ciencias, Universidad Nacional cific competition between the iguanid lizards Scelo- Autónoma de México. porus merriami and Urosaurus ornatus. Ecological MOUNT, R.H. 1963. The natural history of the red-tailed Monographs 50:304–330. skink, Eumeces egregus Baird. American Midland ______. 1982. Demographic and life-history variation Naturalist 70:356–385. among populations of the iguanid Urosaurus ornatus: ORTEGA, A., AND R. BARBAULT. 1984. Reproductive cycles implications for the study of life-history phenomena in the mezquite lizard Sceloporus grammicus. Jour- in lizards. Herpetologica 38:208–221. nal of Herpetology 18:168–175. DUNHAM, A.E., AND D.B. MILES. 1985. Patterns of covari- ORTEGA-RUBIO, A., R. BARBAULT, AND G. HALFFTER. 1999. ations in life history traits of squamate reptiles: the Population dynamics of Sceloporus grammicus effects of size and phylogeny considered. 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VITT, L.J., AND J.D. CONGDON. 1978. Body shape, repro- VITT, L.J., AND H.J. PRICE. 1982. Ecological and evolution- duction effort, and relative clutch mass in lizards: ary determinants of relative clutch mass in lizards. resolution of a paradox. American Naturalist 112: Herpetologica 38:237–255. 595–608. Received 1 October 2002 Accepted 7 May 2003 Western North American Naturalist 64(2), ©2004, pp. 184–192

INFLUENCE OF BLACK-TAILED PRAIRIE DOG TOWNS (CYNOMYS LUDOVICIANUS) ON CARNIVORE DISTRIBUTIONS IN THE OKLAHOMA PANHANDLE

Michael J. Shaughnessy, Jr.,1,3 and Richard L. Cifelli2

ABSTRACT.—Carnivores were recorded at prairie dog towns and non-prairie dog town paired sites in the Oklahoma Panhandle over 4 sampling sessions from October 1995 to February 1997. We established carnivore presence through the use of baited tracking plates dusted with chalk and matched with infrared-triggered cameras. Five carnivore species were recorded at both prairie dog towns and paired sites across the Oklahoma Panhandle. Of these, 4 were recorded with sufficient regularity to permit analyses. Carnivores were analyzed at prairie dog towns across the entire Panhandle and in the Panhandle’s westernmost county (Cimarron County) only. Canids showed no significant preference for prairie dog towns or other areas. In the Oklahoma Panhandle and Cimarron County only, occurrence of swift fox (Vulpes velox) between prairie dog towns and control sites was insignificant. Badgers (Taxidea taxus) and spotted skunks (Spilogale putorius) occurred significantly more often at prairie dog towns in Cimarron County but not in the Panhandle. No single mustelid species showed a significant association with either prairie dog towns or non-prairie dog town habitats. Our results indicate that whereas prairie dog towns do attract some carnivore species, the presumption that prairie dogs are “keystone species” for so many organisms (especially threatened or endangered species) in the current plains ecosystem may not be as clear as previously thought.

Key words: prairie dog town, keystone species, carnivore, swift fox, coyote, badger, skunk.

The ability of black-tailed prairie dogs (Cyno- Hoogland 1995, Barko 1997). In Oklahoma, 48 mys ludovicianus) to broadly alter biotic and species of vertebrates have been reported to abiotic characteristics of their environment be associates of black-tailed prairie dog towns; has been the focus of intense scientific investi- 22 of these species are considered rare and/or gation over the last 20 years (Bonham and Ler- protected by federal or state legislation (Shack- wick 1976, Clark et al. 1982, Garrett et al. 1982, ford and Tyler 1991). O’Meila et al. 1982, Coppcock et al. 1983, Since the turn of the century, black-tailed Agnew et al. 1986). More recently, research prairie dog populations have experienced peri- has been directed to questions regarding the ods of decline and recovery due to numerous specific effects black-tailed prairie dog activi- factors ranging from disease to federal and pri- ties have on other prairie organisms (Clark et vate control practices (Miller et al. 1994). The al. 1982, Knowles et al. 1982, Agnew et al. area presently covered by black-tailed prairie 1986, Whicker and Detling 1988, Sharps and dog towns in the central plains may have been Uresk 1990, Miller et al. 1994, Barko 1997). reduced by as much as 99% since the turn of Their ability to alter their environment has led the century (Miller et al. 1994). Structure and to the suggestion that black-tailed prairie dogs arrangement of black-tailed prairie dog towns may function as “keystone species” (a species in the environment have changed as well. In having a dominating influence on the compo- the past black-tailed prairie dog towns were sition of a community [Ricklefs 1997]) in the typically large and continuous (Marsh 1984). prairie ecosystem, creating patches of more With the reduction in black-tailed prairie dog suitable or even preferred habitat for other populations, towns in some areas have become prairie organisms (Clark et al. 1982, Forrest et increasingly fragmented, smaller, and isolated al. 1988, Seal et al. 1989, Sharps and Uresk 1990, (Marsh 1984). As a keystone species, the black- Knowles and Knowles 1994, Miller et al. 1994, tailed prairie dog would be expected to have a

1Department of Zoology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019. 2Oklahoma Museum of Natural History, University of Oklahoma, 2401 Chautauqua Avenue, Norman, OK 73072. 3Present address: Department of Biology, College of Mathematics and Science, University of Central Oklahoma, 100 North University Drive, Edmond, OK 73034.

184 2004] PRAIRIE DOG INFLUENCES ON CARNIVORES IN OKLAHOMA 185 disproportionate effect on species assemblages towns more often than they occur in surround- wherever they occur. This change in landscape ing habitats. These questions were intended to dynamics could be expected to significantly provide a better understanding of the role of affect those species associated with black-tailed black-tailed prairie dogs in structuring local prairie dog towns. and regional carnivore assemblages. Populations of black-tailed prairie dogs have declined in Oklahoma, particularly in the region STUDY AREA known as the Panhandle (Osborn and Allan 1949, Shaw et al. 1991). Populations in the Pan- We conducted research on prairie dog towns handle also are unstable, as illustrated by the and carnivores in the Oklahoma Panhandle, fact that only 39% of black-tailed prairie dog which is adjacent to the northwesternmost part towns mapped in 1967 survived to 1989 (Shaw of the body of the state and is approximately et al. 1991). During 1991 some of the largest 267 km long (east–west) and 55 km wide (north– black-tailed prairie dog towns in the Panhandle south). Three counties (Cimarron, Texas, Beaver) were decimated by sylvatic plague (Yersinia of approximately equal size comprise the Pan- pestis; Shaw et al. 1991). This reduction of handle. populations and town sizes has provided an Historically, the Panhandle was a shortgrass increased incentive to study the relationships prairie dominated by blue grama (Bouteloua between black-tailed prairie dogs and their gracilis), buffalograss (Buchloe dactyloides), vertebrate associates. and prairie three-awn (Aristida oligantha; Among the associates reported for black- Shaughnessy 2003). Prairie dog towns occurred tailed prairie dog towns, mammalian carnivores in all habitat types throughout the Panhandle have the potential to be some of the most (Shackford and Tyler 1991). Panhandle prairie severely affected by decreases in population dog towns also were reported to be continu- size and town area. As upper trophic-level con- ous, spreading unbroken for miles (Shackford and Tyler 1991). Historically and currently, sumers, mammalian carnivores may depend several major riparian areas cut through the upon prairie dog towns to provide food sources, landscape. These are dominated by large east- both prairie dogs themselves and small mam- ern cottonwoods (Populus deltoides) and taller mals and birds they may attract (Koford 1958, grasses (Shaughnessy 2003). A mesa habitat, Forrest et al. 1988, Sharps and Uresk 1990, characterized by sand sagebrush (Artemisia fil- Hoogland 1995). Mammalian carnivores also ifolia), juniper (Juniperus scopulorum), prickly may exploit prairie dog burrows as potential pear and/or cholla (Opuntia spp.), and two- denning sites, particularly on the edges of needle pinyon (Pinus edulis; Shaughnessy 2003), prairie dog towns. Smaller carnivores also may dominates the northwest corner of the Pan- depend upon the burrows of prairie dogs as handle. escape routes when pursued by larger carni- Over time the Panhandle environment has vores. The black-footed ferret (Mustela nigripes), been altered by human activities (Shaughnessy a mammalian carnivore known to be highly 2003). Agricultural, livestock, and fossil fuel associated with prairie dogs, suffered high interests have come to dominate the landscape losses when prairie dogs in Wyoming died (Shaughnessy 2003). Although historical hab- from sylvatic plague (Forrest et al. 1988, Seal itat types still persist, the quality and quantity et al. 1989). In Oklahoma, the 3-county Pan- of habitats have changed. Grassland, mesa, and handle region supports 17 mammalian carni- riparian areas are now almost entirely grazed vore species (14 extant, 3 historically) in 5 by domestic cattle or converted to other agri- families (Caire et al. 1989). Four of these mam- cultural uses, and little remains of the original, malian carnivores are reported to be associated extensive shortgrass prairie (Shaughnessy 2003). with black-tailed prairie dog towns (Shackford Prairie dog towns also have been reduced in and Tyler 1991). numbers and sizes due to periodic episodes of The purpose of this research was to exam- plague (Yersinia pestis) and eradication efforts ine carnivore occurrence and activity at black- of landowners (Marsh 1984, Shaw et al. 1991). tailed prairie dog towns in the Oklahoma Pan- Presently, the total area covered by prairie dog handle. We also investigated whether these towns in the Oklahoma Panhandle is approxi- carnivores occur at black-tailed prairie dog mately 562 ha (Shaughnessy 2003). 186 WESTERN NORTH AMERICAN NATURALIST [Volume 64

MATERIALS AND METHODS County reported the most consistent and highest numbers of carnivore detections at both We determined the presence and distribu- prairie dog towns and non-town sites. As a tion of carnivores by using baited tracking result, we analyzed separately data from plates at preestablished tracking stations apply- Cimarron County where we recorded for 53 ing the method described in Shaughnessy functional plate nights (5 plates total) at prairie (2003). Stainless steel tracking plates (approxi- dog towns and 51 functional plate nights (5 mately 1 m × 1 m) were placed at tracking sta- plates total) at paired sites. A functional plate tions and sprayed with a mixture of isopropyl night is defined as 1 tracking plate operated alcohol and carpenter’s chalk. A 1-inch hole for 1 night without rain. was drilled through the center of each plate, allowing it to be placed directly over a stake Statistical Methods that permanently marked the tracking station Due to the ordinal nature of the data (2- (Shaughnessy 2003). Bait, consisting of canned sample ranked test), we used nonparametric mackerel and/or beef scraps, was placed in the statistics. All data for carnivore counts at middle of the plate or on the stake. We exam- prairie dog towns and paired sites were ana- ined the plates for tracks and moved them lyzed with a Wilcoxon paired-sample test. This at the end of the 3-night sampling period test was chosen because the sampling and sta- (Egoscue 1956, Orloff et al. 1986). tistical design had paired prairie dog towns Ninety permanent tracking stations were with adjacent non-prairie dog town control established previously throughout the Pan- sites before we initiated data collection. We handle in a stratified random design as part of felt that these a priori pairings appropriately a broader project examining Panhandle carni- linked the 2 sampling designations. As a result, vore distributions (Shaughnessy 2003). Stations the Wilcoxon paired-sample test was deter- were established based first on county area mined to be the most rigorous and appropriate and then on area covered by major habitats for these analyses. (Shaughnessy in press). Habitats were identified The westernmost county in the Oklahoma by vegetation, physiographic features, and/or Panhandle (Cimarron) accounted for most car- land use (Shaughnessy 2003). Of 90 stations, nivore detections during all phases of this 16 were established at prairie dog towns and study. Two separate analyses were conducted, 16 at control sites located in habitats adjacent 1 analyzing data for the entire Panhandle and to the prairie dog town stations. In almost all a 2nd analyzing data only for Cimarron County. instances control sites were located within The 2 analyses would help determine what about 15 km of tracking stations at prairie dog effect, if any, the skewed detection frequen- towns. Because of this, we could reasonably cies had on data analyses and interpretation. expect that any carnivores detected at one site All statistical tests were computed according to could potentially be detected at that site’s pair protocol described in Zar (1984). (Zoellick and Smith 1992). In all instances con- The nature of the data generated by track- trol sites were placed in habitats similar to or ing plates was such that individual carnivores nearly identical to those in which the prairie of the same species could not be distinguished. dog town sites occurred, and control sites were As a result, it was impossible to determine if paired with prairie dog town sites as part of multiple detections of the same species of car- the statistical design. nivore at the same site resulted from visits by We conducted 4 tracking plate surveys in different carnivores or a single carnivore that the Panhandle from October 1995 to February visited the site many times. Analyses did not 1997, one survey during each season to mini- require this type of differentiation though, as mize within-season variation in carnivore de- data were not used to estimate carnivore num- tections. Panhandle counties were surveyed in bers. Rather, data were used to measure carni- staggered succession, offset by 1 day per county. vore activity between 2 habitat types (prairie We completed all surveys within 7 days of dog towns and non-prairie dog town areas). their initiation. Tracking plates at prairie dog Carnivore-preferred habitats would necessar- towns were operated for 163 functional plate ily generate more detections, either by attract- nights across the Panhandle and for 155 func- ing many carnivores or by retaining just a few tional plate nights at paired sites. Cimarron carnivores over time. 2004] PRAIRIE DOG INFLUENCES ON CARNIVORES IN OKLAHOMA 187

RESULTS

Five carnivore species were identified at black-tailed prairie dog towns (Vulpes velox, Canis latrans, Spilogale putorius, Taxidea taxus, and Lynx rufus). We detected 4 of these carnivores often enough to permit individual analyses: Vulpes velox (6 detections at prairie dog towns, 15 detections at paired sites), Canis latrans (9, 3), Spilogale putorius (7, 4), and Taxidea taxus (3, 0). The bobcat, Lynx rufus, was not detected often enough to permit individual analysis (0, 1), but data on bobcats were included in analyses of all carnivores at prairie dog towns. A single striped skunk, Mephitis mephitis, was detected at 1 paired site in the Panhandle during this study, but no striped skunks were detected at prairie dog towns. Fig. 1. Comparison of canid, mustelid, and all carnivore At prairie dog towns we recorded 25 carni- detection frequencies at prairie dog towns and control vore detections over the course of the study. sites in the Oklahoma Panhandle, 1995–1997. Twenty-five detections were also recorded at paired sites during this same period. Analysis using a Wilcoxon paired-sample test revealed ≥ no significant differences between carnivore paired sites (n = 5; T+ = 6, T– = 9; P 0.05; detections at prairie dog towns and non- Fig. 2). Ten canids were recorded at prairie prairie dog town paired sites (n = 11; T+ = dog towns whereas 11 were recorded at paired 32.5, T– = 30.5; P ≥ 0.05; Fig. 1). Data in fig- sites. ures are presented as indices of activity ex- Individual species also were analyzed for pressed as the number of detections divided differences in occurrence between prairie dog by functional plate nights. towns and non-prairie dog town sites. In our Seventeen carnivore track detections (in 4 analysis of coyote (Canis latrans) detections at species) were recorded at prairie dog town prairie dog towns and paired sites across the sites in Cimarron County and 14 (in 5 species) Panhandle, we found no significant differ- at paired sites: Vulpes velox (6 detections at ences between coyote occurrences at prairie prairie dog towns, 10 detections at paired sites), dog towns and at paired sites (n = 5; T+ = Canis latrans (4, 1), Taxidea taxus (3, 0), Spilo- 13.52, T– = 1.5; P ≥ 0.05; Fig. 2). However, 9 gale putorius (4, 2), Lynx rufus (0, 1). Again, coyotes detections were recorded at prairie the analysis using Wilcoxon paired-sample dog towns in contrast to only 3 at paired sites. tests revealed no significant differences in car- Coyote occurrences at prairie dog towns and nivore detections between prairie dog towns paired sites in Cimarron County only were not and their paired sites in Cimarron County (n analyzed because the data set was too small ≥ = 5; T+ = 9, T– = 5; P 0.05; Fig. 1). and the distribution of the data across the Pan- We analyzed canids as a group with respect handle was not as skewed. to their occurrence at prairie dog towns and Across the Panhandle, 6 swift foxes were paired sites. Of 2 canid species detected (Canis recorded at prairie dog towns whereas 15 were latrans and Vulpes velox), we recorded 15 track recorded at paired sites. The Wilcoxon paired- detections at prairie dog towns and 18 at paired sample analysis of these data was insignificant sites. Wilcoxon paired-sample analysis revealed (n = 7; T = 5; P ≥ 0.05). When we analyzed no significant differences in detections of canids data for swift foxes detected in Cimarron County between prairie dog towns and paired sites (n only, results were also insignificant (n = 5; T = ≥ ≥ = 10; T+ = 24, T– = 31; P 0.05; Fig. 2). 4; P 0.05; Fig. 2). In Cimarron County, 6 swift Analysis of canid data for Cimarron County foxes were recorded at prairie dog towns com- also resulted in no significant differences in pared with 10 at non-prairie dog town paired canid detections at prairie dog towns and sites. 188 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Fig. 3. Comparison of mustelid species at prairie dog towns and control sites in the Oklahoma Panhandle, 1995–1997.

Fig. 2. Comparison of Vulpes velox and Canis latrans detection frequencies at prairie dog towns and control sites in the Oklahoma Panhandle, 1995–1997. were they detected outside Cimarron County. However, we recorded 3 badgers at prairie dog town sites in Cimarron County (Fig. 3). Due to the small sample size, we performed Mustelids were analyzed as a group as well. no statistical tests on these data. The data are Across the Oklahoma Panhandle, we recorded presented here merely to illustrate a trend of 10 mustelids in 2 species at prairie dog towns badgers toward prairie dog towns. and 6 mustelids in 3 species at non-prairie dog town paired sites. Mustelids did not occur sig- DISCUSSION nificantly more often at prairie dog towns across the Panhandle than at the non-prairie dog Sample sizes and visitation rates at perma- town paired sites (n = 8; T+ = 25, T– = 11; P nent tracking stations were low, which is not ≥ 0.05; Fig. 3). In Cimarron County mustelids uncommon for tracking studies (Humphrey were significantly associated with prairie dog and Zinn 1982, Conner et al. 1983). However, ≤ towns (n = 4; T = 0; P 0.05; Fig. 3). Seven the low numbers of data could have had an mustelids were recorded at prairie dog towns effect on the power of the tests to detect sig- in Cimarron County whereas only 2 were re- nificant differences. The paired-sample design corded at paired sites. and the use of nonparametric procedures for The spotted skunk (Spilogale putorius) was analyzing the data addressed some of these the mustelid we most often recorded at prairie deficiencies, but the small nature of the data set dog towns and paired sites. Spotted skunks must be kept in mind for any interpretations. were recorded 7 times at the former sites and In general, carnivore species detected dur- 5 times at the latter sites across the Panhandle. ing this study did not show a significant affilia- Spotted skunks, however, were not significantly tion with black-tailed prairie dog towns in the associated with either prairie dog towns or Oklahoma Panhandle. Total numbers of carni- paired sites (n = 8; T = 7; P ≥ 0.05; Fig. 3). In vore detections at prairie dog towns and paired Cimarron County spotted skunks again were sites were very similar for the entire Panhandle not significantly associated with either prairie (Fig. 1) and for Cimarron County as well, which dog towns or paired sites (n = 4; T+ = 3, T– was, in terms of total detections and frequency = 0; P ≥ 0.05; Fig. 3). Four spotted skunks of detections, the county in which carnivores were recorded at prairie dog towns in Cimar- were most abundant (Fig. 1). ron County and only 2 at paired sites. There were variations among canids with The badger (Taxidea taxus) was the only respect to affiliation with prairie dog towns. other mustelid we detected at prairie dog towns. The 2 canids detected during the study (coyote No badgers were recorded at paired sites, nor and swift fox) showed divergent patterns in 2004] PRAIRIE DOG INFLUENCES ON CARNIVORES IN OKLAHOMA 189 association with prairie dog towns. When com- may be important areas for coyotes, in this in- bined, canids were not significantly associated stance, interspecific interactions, which affect with prairie dog towns either in Cimarron canid distributions in the broader prairie eco- County alone or across the entire Panhandle. system, may be operating at prairie dog towns. Individually, however, certain trends were Mustelids also exhibited interesting occur- apparent. Coyotes, while not statistically sig- rence patterns between prairie dog towns and nificantly associated with prairie dog towns, paired sites. Although mustelids were signifi- trended toward higher numbers of detections cantly associated with prairie dog towns in at prairie dog towns (Fig. 2). Cimarron County, they were not significantly Swift foxes trended away from prairie dog associated with prairie dog towns across the towns in Cimarron County and across the entire Panhandle (Fig. 3). Three mustelids were de- Panhandle (Fig. 2). These results do not seem tected during this study, but only 2 (badger to support the long-held assumption that prairie and spotted skunk) were detected at prairie dog towns are important resource areas for dog towns. Striped skunks were not detected sensitive species like the swift fox. at the prairie dog town stations during any Interference competition, aggression, and part of the study and were detected only once even predation have been documented between at a control site. Even with poor representa- canids in many different ecosystems (Carbyn tion of striped skunks, mustelids still exhibited 1982, Rudzinski et al. 1982, Sargeant et al. 1987, a significant association with prairie dog towns Harrison et al. 1989, Bailey 1992, Peterson in Cimarron County and a preference for prairie 1995, Dayan and Simberloff 1996, Johnson dog towns across the Panhandle. No single et al. 1996). Because larger canids harass and mustelid species exhibited a significant associ- threaten smaller canids, some resources or ation with either prairie dog towns or paired areas become unavailable to the smaller canids. sites across the Oklahoma Panhandle or in Cim- Small canids persist in the environment by arron County alone. behaviorally avoiding those areas that are most We detected badgers only at prairie dog likely to contain larger canids (Carbyn 1982, towns and never at paired sites during the Sargeant et al. 1987, Harrison et al. 1989, White course of this study. The occurrence of bad- and Ralls 1993, White et al. 1994, Ralls and gers exclusively at prairie dog towns appears White 1995, Gese et al. 1996). to be the reason mustelids, in general, were It is possible that this dynamic is at work determined to be significantly associated with between swift foxes and coyotes in the Okla- these areas. The total absence of badgers at homa Panhandle at black-tailed prairie dog paired sites suggests that badgers have a strong towns. Coyotes and swift foxes trended in association with prairie dog towns. Badgers opposite directions at prairie dog towns and have long been known to be associated with paired sites. Prairie dog towns may be areas prairie dog towns and are, in fact, major pred- rich in resources that canids recognize and ators of prairie dogs and ground squirrels attempt to exploit. However, smaller canids, (Spermophilus tridecilineatus) in Oklahoma such as swift foxes, may perceive an increased (Caire et al. 1989). risk of predation at prairie dog towns due to Spotted skunks also were detected at prairie increased coyote presence. Thus, they avoid dog towns in slightly disproportionate (although prairie dog towns, confining their activity away not significant) numbers (7 detections at towns, from towns to areas of lower coyote densities. 5 at paired sites). However, these trends are Across broader Panhandle habitats, swift foxes not sufficiently large enough to permit inter- were detected more frequently in range and pretation. mesa habitats, away from prairie dog towns Prairie dog towns appear to be important (Shaughnessy 2003). Coyotes were detected in- resource areas for carnivores (particularly frequently in the broader range and mesa non- mustelids in general) in the Oklahoma Pan- prairie dog town areas (Shaughnessy 2003). handle. Nonetheless, their overall importance Swift foxes in the Oklahoma Panhandle may and the strength of carnivore associations with be forgoing prairie dog towns as resource areas prairie dog towns (particularly for some rarer in favor of the more “coyote depauperate” range carnivores) may not be as clear as previously and mesa habitats. While prairie dog towns thought for specific species. Swift foxes persist 190 WESTERN NORTH AMERICAN NATURALIST [Volume 64 in other parts of the Oklahoma Panhandle environment should be reexamined as it relates (Shaughnessy 2003) despite their lower fre- to carnivores. quency of detection at prairie dog towns (possibly due to the heightened coyote presence in ACKNOWLEDGMENTS these areas). This is not to say that prairie dog towns are We express our most sincere thanks to the not vital habitats of the plains ecosystem. following people who were influential in the Prairie dog towns in the plains ecosystem are completion of this manuscript: J. Thompson, undeniably unique areas. Their role in struc- L. Toothaker, K. Pandora, N. Czaplewski, and turing and influencing prairie communities M. Jakubauskas, as well as C. Vaughn and M. has been well documented for many species Kaspari for their assistance, guidance, and (Clark et al. 1982, Whicker and Detling 1988, advice over the course of this study. Sincere Sharps and Uresk 1990, Miller et al. 1994, thanks are extended to all landowners and Hoogland 1995). They increase species rich- ranchers in the Oklahoma Panhandle who per- ness, mix topsoil and subsoil, and have large mitted us access to their land to perform field- overall effects on ecosystems and biodiversity work. We also thank graduate students of the in the plains (O’Meila et al. 1982, Coppcock et Zoology Department at the University of Okla- al. 1983, Hoogland 1995). Other carnivores homa. We express our gratitude to D. Legates are also known to be highly associated with who helped design the statistical analyses. prairie dog towns (e.g., black-footed ferret and These studies were supported, in part, by fund- badger). However, it is equally important not ing through Section 6 of the Endangered to overlook or underestimate other species Species Act to M. 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Journal of Wildlife Manage- homa. Report submitted to the Oklahoma Depart- ment 53:181–185. ment of Wildlife Conservation. 24 pp. HOOGLAND, J.L. 1995. The black-tailed prairie dog: social SHARPS, J., AND D.W. URESK. 1990. Ecological review of life of a burrowing mammal. University of Chicago black-tailed prairie dogs and associated species in Press. 557 pp. western South Dakota. Great Basin Naturalist 50: HUMPHREY, S.R., AND T.L. Z INN. 1982. Seasonal habitat 339–345. use by river otters and Everglades mink in Florida. Journal of Wildlife Management 46:375–381. SHAUGHNESSY, M.J., JR. 2003. Swift fox detection methods and distribution in the Oklahoma Panhandle. In: L. JOHNSON, W.E., T.K. FULLER, AND W.L. FRANKLIN. 1996. Sympatry in canids: a review and assessment. In: Carbyn and M. Sovada, editors, Ecology and conser- J.L. Gittleman, editor, Carnivore ecology, behavior vation of swift foxes in a changing world. Canadian and evolution. Volume 2. Cornell University Press, Circumpolar Institute, University of Alberta, Edmon- Ithaca, NY. 644 pp. ton, Alberta, Canada. HAW ARTER AND ESLIE R KNOWLES, C.J., AND P.R. KNOWLES. 1994. Additional records S , J.H., T.S. C , D.M. L , J . 1991. Black- of Mountain Plovers using prairie dog towns in footed ferret reintroduction assessment in Oklahoma. Montana. Prairie Naturalist 16:183–186. Final report to the Oklahoma Department of Wildlife KNOWLES, C.J., C.J. STONER, AND S.D. GEIB. 1982. Selec- Conservation. 14 pp. tive use of black-tailed prairie dog towns by Moun- STAPP, P. 1998. A reevaluation of the role of prairie dogs in tain Plovers. Condor 84:71–74. Great Plains grasslands. Conservation Biology 12: KOFORD, C.B. 1958. Prairie dogs, whitefaces and blue 1253–1259. grama. Wildlife Monographs 3:1–78. WHICKER, A.K., AND J.K. DETLING. 1988. Ecological con- MARSH, R.E. 1984. Ground squirrels, prairie dogs and sequences of prairie dog disturbances. BioScience marmots as pests on rangeland. Pages 195–208 in 38:778–785. Proceedings of the conference for organization and WHITE, P.J., AND K. RALLS. 1993. Reproduction and spac- practice of vertebrate pest control, Hampshire, Eng- ing patterns of kit foxes relative to changing prey land, 30 August–3 September 1982. Plant Protection availability. Journal of Wildlife Management 57: Division, Fernherst, England. 861–867. MILLER, R.E., G. CEBALLOS, AND R. READING. 1994. The WHITE, P.J., K. RALLS, AND R.A. GARROTT. 1994. Coyote– prairie dog and biotic diversity. Conservation Biol- kit fox interactions as revealed by telemetry. Cana- ogy 8:677–681. dian Journal of Zoology 72:1831–1836. O’MEILA, M.E., F.L. KNOPF, AND J.C. LEWIS. 1982. Some WHITE, P.J., K. RALLS, AND C.A. VANDERBILT WHITE. 1995. consequences of competition between prairie dogs Overlap in habitat and food use between coyotes and beef cattle. Journal of Range Management 35: and San Joaquin kit foxes. 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ZAR, J.H. 1984. Biostatistical analysis. 2nd edition. Pren- ZOELLICK, B.W., AND N.S. SMITH. 1992. Size and spatial tice-Hall, Englewood Cliffs, NJ. 718 pp. organization of home ranges of kit foxes in Arizona. Journal of Mammalogy 73:83–88.

TEMPERATURE AND HIGH SALINITY EFFECTS IN GERMINATING DIMORPHIC SEEDS OF ATRIPLEX ROSEA

M. Ajmal Khan1,2, Bilquees Gul1,2, and Darrell J. Weber1,3

ABSTRACT.—Atriplex rosea L. (Chenopodiaceae; tumbling orach), an annual herb, is a widely established weedy species of disturbed sites in all counties of Utah. Seeds of Atriplex rosea were collected from a salt marsh in Faust, Utah, and are dimorphic, light brown, and 2–2.5 mm wide, or black and 1–2 mm wide. Seed germination responses of the black and brown seeds were studied over a range of salinity and temperature. Both brown and black seeds germinated at 1000 mM NaCl, and the optimal temperature for germination of both types was 20°–30°C. Variation in temperature, however, affected germination of black seeds more than brown seeds. At lower thermoperiod only 40%–50% black seeds germinated in nonsaline control, and germination was almost completely inhibited with the inclusion of salinity. How- ever, all brown seeds germinated in control at temperatures above 5°–15°C, and inhibition caused by salinity was com- paratively lower. Brown seeds had a higher germination rate than black seeds at all temperature and salinity treatments. The highest rate of germination of both seeds occurred at the temperature regime of 5°–15°C. Recovery of germination for black seeds when transferred to distilled water after being in various salinity treatments for 20 days was quite variable. Recovery decreased with increase in salinity at lower temperature regimes, increased with salinity at optimal thermoperiod, and had no effect at 20°–30°C. Brown seeds recovered poorly from salinity at all thermoperiods except 5°–15°C, where recovery decreased with an increase in salinity. Brown seeds are adapted to germination in the early part of the growing season, whereas black seeds are capable of surviving harsher conditions and can germinate in later time periods. Characteristics of the dimorphic seeds increase chances for survival in the harsh saline desert environment.

Key words: Atriplex rosea, halophyte, salinity, seed germination, temperature, dimorphic seeds.

Natural habitats where halophytes can grow perianth but no bracteoles (Ungar 1987). In A. are often subject to sudden changes in tem- triangularis both large and small seeds have perature and salinity regimes that could result bracteoles surrounding them when the fruit is in high mortality of seedlings (Ungar 1991). mature (Ungar 1984). Germination polymor- Severe environmental pressure may lead to phism is extremely important to species growing the development of seed dimorphism in halo- in variable environments because it provides phytes, which could provide different spatial alternate temporal and spatial germination and temporal dispersal potential by allocating opportunities, preventing a single local hazard their resources between smaller, more dormant, from eliminating an entire plant population readily dispersed r-type units and larger, more (Khan et al. 2001a, 2001b). Seed dimorphism readily germinable K-type units (Harper 1977, and polymorphism have also been reported for Khan and Ungar 1984a, 1984b, Khan et al. a number of halophytic taxa including Arthroc- 2001a). Seed dimorphism and polymorphism nemum, Chenopodium, Cakile, Salicornia, Sal- have been reported in the genus Atriplex (Hall sola, Spergularia, Suaeda, and Trianthema and Clements 1923, Beadle 1952, Frankton and (Ungar 1977, Khan and Ungar 1984a, 1984b, Bassett 1968, Taschereau 1972, Drysdale 1973, Galinato and van der Valk 1986, Mohammad Khan and Ungar 1984a, 1984b, Ungar 1984). and Sen 1988, Ungar 1988, Morgan and Myers However, the mechanism for production of 1989, Khan and Gul 1998) and may have re- large and small seeds is not clear for most sulted in plasticity in their germination re- species of Atriplex (Khan and Ungar 1984b). sponses to varying environments. In A. hortensis large seeds are produced within Atriplex species have been reported to vary bracteoles in earlier flowers that do not contain considerably in their salinity tolerance at ger- a perianth, while small seeds are produced later mination (Ungar 1995). Atriplex patula can in the growing season by flowers containing a germinate at 60 mM NaCl (Galinato and van

1Botany and Range Science (now Department of Integrative Biology), Brigham Young University, Provo, UT 84602-5181, USA. 2Present address: Department of Botany, University of Karachi, Karachi-75270, Pakistan. 3Corresponding author.

193 194 WESTERN NORTH AMERICAN NATURALIST [Volume 64 der Valk 1986), A. triangularis at 280 mM Utah, USA, 48 km south of the Great Salt Lake. NaCl (Khan and Ungar 1984a, 1984b), A. Conductivity of the soils was determined using rhagodoides at 309 mM NaCl (Mahmood and a Beckman RC16C meter. Seeds were sepa- Malik 1996), A. griffithii at 345 mM NaCl rated from their inflorescence, air-dried, and (Khan and Rizvi 1994), A. nummularia at 309 then separated into groups of brown and black mM NaCl (Uchiyama 1981), A. prostrata at seeds. Seeds were stored at 4°C and were sur- 600 mM NaCl (Bakker et al. 1985), and A. hal- face treated using the fungicide Phygon (2,3- imus at 856 mM NaCl (Zid and Boukhris 1977). dichloro-1,4-naphthoquinone). Germination was Atriplex seeds can maintain viability after an carried out in 50 × 9-mm tight-fitting plastic extended exposure to salinity (Zid and Bouk- petri dishes (Gelman #7232) with 5 mL of test haris 1977, Uchiyama 1981, Keiffer and Ungar solution as described below. Each of these 1995), and the seeds recover completely when dishes was placed in a 10-cm-diameter plastic transferred to distilled water. This recovery of petri dish to further reduce the loss of water seed germination varies with species and by evaporation. We used 4 replicates of 25 changes in thermoperiod (Khan and Ungar seeds for each treatment and considered seeds 1997). germinated with emergence of the radicle. Atriplex rosea L. (Chenopodiaceae; tum- Effects of temperature on germination were bling orach), an annual herb, is a widely estab- determined using 12-hour alternating temper- lished weedy species of disturbed sites, often ature regimes of 5°–15°C, 10°–20°C, 15°–25°C, in riparian habitats, barnyards or annual bed- 20°–30°C, and 25°–35°C. Both black and brown ding grounds, at elevations of 850–2560 m in seeds were germinated in distilled water and all counties of Utah (Welsh et al. 1987). Native 200, 400, 600, 800, and 1000 mM NaCl at to Eurasia, it is widespread in North America. each of the above-mentioned temperature The species grows in the bottom of internally regimes. Percentage germination was recorded drained basins at the margins of the Great every 2nd day for 20 days. After 20 days we Basin salt playas (Billings 1945) where the transferred ungerminated seeds from the majority of the salt in the soil is NaCl with NaCl treatments to distilled water to study the concentrations up to 1027 mM (Hansen and recovery of germination, which was also re- Weber 1975). It is commonly found with Tri- corded at 2-day intervals for 20 days. Recovery glochin maritime, forbs A. prostrata and Kochia percentages were determined by the following scopari, and the grass Distichlis spicata. formula: (a – b) / (c – b)*100, where a is total Atriplex rosea produces seeds by autumn and number of seeds germinated after being trans- most of the seeds are dispersed onto the saline ferred to distilled water, b is total number of soil around the parent plant. However, water seeds germinated in saline solution, and c is upon which they readily float sometimes total number of seeds. The rate of germination causes long-range dispersal of seeds. Seeds of was estimated using a modified Timson index A. rosea are dimorphic, light brown, and 2–2.5 of germination velocity = ∑G/t, where G is mm wide, or black and 1–2 mm wide (Hall the percentage of seed germination at 2-day and Clements 1923, Welsh et al. 1987). The intervals and t is the total germination period germination of halophyte seeds in temperate (Khan and Ungar 1984a). The maximum value salt playas and salt marshes usually occurs in possible using this index with our data was 50 the spring when the temperatures are moder- (i.e., 1000/20). The higher the percentage ate (8°–18°C) and soil salinity is reduced by value, the more rapid the rate of germination. precipitation (Khan and Weber 1986, Gul and Germination data (20 days and rate of germi- Weber 1999). The goal of this study was to nation) were arcsine transformed before statis- examine effects of high salinity and thermo- tical analysis. Data were analyzed using a 3- period on the germination and recovery of way analysis of variance (SPSS, Inc. 2001) to brown and black seeds of A. rosea. determine the significance of main effects (salinity, thermoperiod, and seed type) and MATERIALS AND METHODS their interactions in affecting the rate and percentage of germination. If significant differ- Seeds of A. rosea were collected during the ences occurred, a Bonferroni analysis (multi- autumn of 1996 from a salt marsh at Faust, ple range test = modified LSD, P < 0.05) was 2004] GERMINATION OF DIMORPHIC SEEDS OF ATRIPLEX ROSEA 195

TABLE 1. Results of 3-way ANOVA of characteristics by seed color, salinity, and thermoperiod treatments. Numbers represent F-values. Independent Seed color Salinity Thermoperiod variable (SC) (S) (T) SC × S SC × TT × S SC × T × S Final germination 84*** 346*** 62*** 5*** 12*** 7*** 2** Rate of germination 106*** 417*** 93*** 10*** 7*** 10*** 3** Recovery rate of germination 100*** 5*** 12*** 1.4n.s. 31*** 6*** 2.6*** Percent recovery 20*** 137*** 21*** 50*** 6*** 47*** 10***

*P < 0.05 **P < 0.01 ***P < 0.001

carried out to determine if significant differ- rate of black seeds was obtained at 20°–30°C. ences occurred between individual treatments Rates decreased with increase or decrease in (SPSS, Inc. 2001). temperature. Black seeds showed varied response with RESULTS change in temperature regime when transferred to distilled water after 20 days of salin- A 3-way ANOVA indicated significant (P < ity treatment (Fig. 4). At suboptimal tempera- 0.001) effects of salinity, temperature, and ture regimes, recovery decreased with an seed color on percent seed germination, rate increase in salinity, while there was no change of germination, recovery, and rate of recovery in recovery response with increase in salinity of A. rosea (Table 1). at 15°–25°C (Table 3). At optimal temperature Germination of both black and brown seeds regime (20°–30°C), however, recovery increased was inhibited with the increase in salinity; few with salinity concentrations. In contrast, brown seeds of both germinated in 1000 mM NaCl seeds showed a poor recovery at all tempera- (Figs. 1, 2). Both seed types germinated well at tures except at lowest salinity treatment at the optimal temperature regime of 20°–30°C, 5°–15°C (Fig. 4). A linear regression explains a and any further increase or decrease in tem- high proportion of the germination response peratures significantly decreased germination with R2 (coefficient of regression) values rang- (Figs. 1, 2). However, the effect of temperature ing from 0.04 to 0.73 for black seeds and from on seed germination was more pronounced in 0.09 to 0.27 for brown seeds in various tem- black seeds, which showed only 40% germina- perature treatments (Fig. 4). tion in nonsaline control at 5°–15°C and ger- Rates of recovery of black seed germination mination of only a few seeds at the lowest were greatest at the warmest thermoperiod salinity treatment (100 mM; Fig. 1). Germina- (25°–35°C) and progressively decreased with tion of brown seeds reached approximately decreased temperature (Table 3). Recovery rate 90% within about 2 days at the optimal tem- of germination was poor for brown seeds but perature regime (20°–30°C) compared with 8 remained unchanged with changes in thermo- days in black seeds under similar conditions; period (Table 3). however, about 18% of the seeds germinated with the 1000 mM NaCl treatment in both DISCUSSION types of seeds (Figs. 1, 2). A linear regression of final germination ver- Seed dimorphism and polymorphism are sus NaCl concentration explains a high pro- reported in many Atriplex species growing portion of the germination response, with R2 under saline conditions (Koller 1957, Frankton values ranging from 0.54 to 0.86 for black and Bassett 1968, Drysdale 1973, Baker 1974, seeds and from 0.58 to 0.89 for brown seeds in Khan and Ungar 1984a, 1984b, Ungar 1991). various temperature treatments (Fig. 3). Gustafsson (1973) reported that the rate and Rate of germination of both black and brown percentage of germination of black and brown seeds progressively decreased with increases seeds of A. triangularis and A. longipes were in salinity (Table 2). The fastest germination scarcely different. Khan and Ungar (1984a, 196 WESTERN NORTH AMERICAN NATURALIST [Volume 64 Germination (%)

± Fig. 1. Percentage germination (mean sx–) of black seeds of Atriplex rosea in 0, 200, 400, 600, 800, and 1000 mM NaCl at thermoperiods of 5°–15°C, 10°–20°C, 15°–25°C, 20°–30°C, and 25°–35°C. Germination (%)

± Fig. 2. Percentage germination (mean sx–) of brown seeds of Atriplex rosea in 0, 200, 400, 600, 800, and 1000 mM NaCl at thermoperiods of 5°–15°C, 10°–20°C, 15°–25°C, 20°–30°C, and 25°–35°C.

1984b) reported that black seeds of A. triangu- salt tolerance while large brown seeds have laris were both morphologically and physio- soft seed coat, lower ionic and phenolic acid logically different from brown seeds. Small black contents, higher salt tolerance, and ready ger- seeds have hard seed coats, more ions and minability (Khan and Ungar 1984a, 1984b, phenolic contents, and dormancy with lower 1986a, 1986b). 2004] GERMINATION OF DIMORPHIC SEEDS OF ATRIPLEX ROSEA 197 Germination (%)

Fig. 3. Regression lines of germination (%) of black and brown seeds of Atriplex rosea after being in 0, 200, 400, 600, 800, and 1000 mM NaCl at thermoperiods of 5°–15°C, 10°–20°C, 15°–25°C, 20°–30°C, and 25°–35°C for a 20-day period.

Atriplex rosea seeds have distinct morphol- higher than seawater (Bakker et al. 1985, Zid ogy and are physiologically different to some and Boukharis 1977). Atriplex rosea seeds extent. Great Basin desert halophytes are a were collected from a population found in the group of plants that are more salt tolerant than salt marshes of Faust, Utah, along with other any other group of plants that have been re- halophytes such as A. patula, Distichlis spi- ported. These halophytes, Kochia americana cata, Scirpus maritimus, Suaeda moquinii, and (Clarke and West 1969), Salicornia pacifica Triglochin maritima, with soil electroconduc- var. utahensis (Khan and Weber 1986), Allen- tivity (EC) ranging from 850 mM to 1031 mM rolfea occidentalis (Gul and Weber 1999), Sali- NaCl in the A. rosea zone. Plants surviving in cornia rubra (Khan et al. 2000), Suaeda mo- such a high saline environment require a quinii (Khan et al. 2001a), Kochia scoparia higher degree of salt tolerance during seed (Khan et al. 2001b), Sarcobatus vermiculatus germination. (Khan et al. 2002a), and Salsola iberica (Khan Variations in temperature regime under both et al. 2002b), germinate at salinity concentra- saline and nonsaline conditions have different tions higher than 800 mM NaCl. All of them effects on brown and black seeds of A. rosea. except Allenrolfea occidentalis have some ger- Black seed germination was more sensitive to mination at 1000 mM NaCl. Both brown and changes in temperature regimes. Both types of black seeds of A. rosea showed 15% germina- seeds have optimal germination at 20°–30°C, tion at 1000 mM NaCl. This pattern is consis- but black seed germination was inhibited sub- tent with the other Great Basin species. How- stantially with a decrease in temperature. ever, when comparison of seed germination Temperature and salinity interact to affect ger- responses with salinity was made among Atriplex mination of halophytes (Khan and Ungar 1984a, species, A. rosea appeared to be more salt tol- 1984b, Khan and Weber 1986, Khan and Rizvi erant during germination. Species like A. num- 1994, Khan and Ungar 1996, 1997, Khan and mularia, A. patula, A. triangularis, and A. rhago- Gul 1998, Khan and Ungar 1998, 1999). Some doides could germinate in up to 300 mM NaCl species are more sensitive to change in tem- (Uchiyama 1981, Galinato and van der Valk perature (Cressa cretica, Triglochin maritime, 1986, Khan and Ungar 1984a, 1984b, 1986a, Polygonum aviculare, and Zygophyllum sim- 1986b, Mahmood and Malik 1996), A. griffithii plex) than others (Arthrocnemum indicum, at 345 mM NaCl (Khan and Rizvi 1994), and Haloxylon recurvum, and Suaeda fruticosa; A. prostrata and A. halimus at concentrations Sheikh and Mahmood 1986, Khan 1991, Khan 198 WESTERN NORTH AMERICAN NATURALIST [Volume 64 c b c d < a b c c c d c 0.9 P 2 4 1 2 3.3 1 1 1 0 4.4 0.6 ± ± ± ± ± ± ± ± ± ± ± ± 9 8 3 0 8 9 7 13 42 29 12 10 C C ° ° –35 –35 ° ° b d f 1 a a b c d e f c e 9 5 2 2 2 3.7 5 4.8 1 2 1 4.9 ± ± ± ± ± ± ± ± ± ± ± ± 5 7 2 33 19 11 17 27 24 15 31 26 b c d a b c c c d c 2 1 2 1 1 4.2 4 1 0 1.8 3.1 0 ± ± ± ± ± ± ± ± ± ± ± ± 6 0 5 8 48 33 18 13 10 22 10 C25 C25 ° ° –30 –30 ° ° b a b b b c d a b b c 5 2 2 3 2 6 2 2 2 1 00 4 ± ± ± ± ± ± ± ± ± ± ± ± 8 6 44 36 18 13 28 31 32 36 c c c d a b c d d e 3 3 3 1 1 1 00 09 2.2 4.5 2.4 0.3 ± ± ± ± ± ± ± ± ± ± ± ± 9 6 3 0 0 4 7 7 1 44 28 17 C20 C20 ° ° –25 –25 ° ° c c a d a b b d b b c c 1 4 8 2 5 3 2.0 1 0.6 0.6 0 1.2 ± ± ± ± ± ± ± ± ± ± ± ± 9 8 6 0 32 12 27 27 27 22 16 c c d c c d a b c b c 1 2 2 3.5 3 2 1.7 1.0 0.5 04 2.5 0.5 ± ± ± ± ± ± ± ± ± ± ± ± 8 7 5 3 0 7 6 black and brown seeds in various salinities thermoperiods. Different letters superscript represent sig- 40 20 18 11 10 C15 C15 ° ° –20 –20 ° ° c d e c c d e a b c a b black and brown seeds in various salinities thermoperiods. Different letters superscript represent significant ( 3 1 7 3 1 1.1 1.5 0.8 1.7 1.1 2.5 0.8 ± ± ± ± ± ± ± ± ± ± ± ± Atriplex rosea 5 7 4 2 8 3 5 7 53 13 16 18 ) of – x s ± Atriplex rosea c c d a b a c c d a b b 6 1 1 3.0 2.5 0.7 0.3 0.8 0.6 0.7 0.8 1.0 ) of – x ± ± ± ± ± ± ± ± ± ± ± ± s 9 6 4 9 7 9 ± 26 10 10 10 31 17 C10 C10 ° ° –15 –15 ° ° 5 5 c c a b a c a b c d c d 3 1 1 0.7 0.4 0 2.2 0.9 1 0.4 0 2.1 ± ± ± ± ± ± ± ± ± ± ± ± 15 10 ______< 0.05) differences between salinity treatments at each temperature regime. ANOVA, Bonferroni test. < 0.05) differences between salinity treatments at each temperature regime. ANOVA, P 3. Rate of recovery germination (mean 2. Rate of germination (mean ABLE ABLE T T NaCl (mM) Black Brown Black Brown BlackNaCl (mM) Brown Black Black Brown Brown Black Black Brown Brown Black Brown Black Brown Black Brown nificant ( 0 2004006008001000 3 1 2 1 0 0 4006008001000 9 10 2 0 0.05) differences between salinity treatments at each temperature regime. ANOVA, Bonferroni test. 0.05) differences between salinity treatments at each temperature regime. ANOVA, 200 2 2004] GERMINATION OF DIMORPHIC SEEDS OF ATRIPLEX ROSEA 199 Recovery of germination (%)

Fig. 4. Regression lines of the recovery of germination (%) of black and brown seeds of Atriplex rosea after being in 0, 200, 400, 600, 800, and 1000 mM NaCl at thermoperiods of 5°–15°C, 10°–20°C, 15°–25°C, 20°–30°C, and 25°–35°C for a 20-day period.

and Rizvi 1994, Khan and Ungar 1996, Khan ered completely after they were transferred to and Gul 1998). Germination percentage of distilled water. Similar recovery responses have several Atriplex species was greater in the been reported from a number of halophytic range of 12°–25°C at various salinity concen- species (Khan and Ungar 1996, 1997, 1998), trations but declined beyond this range; i.e., while species like Z. simplex had little recov- the tolerance of salinity stress was greater at ery at any NaCl concentration in all thermo- the optimum temperature (Beadle 1952, Spring- periods. Nondormant seeds of glycophytes field 1966, Ignaciuk and Lee 1980, Khan and normally die when exposed to salinity (Par- Ungar 1984a, 1984b, Khan and Rizvi 1994). tridge and Wilson 1987). Khan and Ungar (1984a) found that alternating Atriplex rosea produces brown and black temperatures of 25°C and 5°C enhanced seed seeds on the same plant. It has been demon- germination of A. triangularis and that increases strated that seed dimorphism provides an in salinity (86–285 mM) decreased both the adaptive advantage in saline habitats through rate of and total seed germination. Khan and production of multiple germination periods Rizvi (1994), reporting the effect of tempera- that increase chances of survival for at least ture regimes on seed germination of A. grif- some seedling cohorts (Ungar 1995). Atriplex fithii var. stocksii (Atriplex stocksii), found that rosea usually grows as one of the salt marsh a relatively cooler temperature regime (10°– species of Great Basin playas where soil salin- 20°C) promoted seed germination in both saline ity is extremely high (100 dS m–1). These and nonsaline conditions. plants recruit through seeds, leaving no evi- Brown seeds of A. rosea, when exposed to dence of vegetative propagation (personal salinity for 20 days and then returned to dis- observation), and grow in areas characterized tilled water, showed a substantial recovery at by great fluctuations in soil salinity and ambi- lower temperature regimes, which decreased ent temperature. The present study has deter- with increase in salinity. However, at optimal mined that dimorphic seeds produced by this temperature regimes, recovery percentages plant also differ physiologically in their response increased with increase in salinity. Brown seeds to temperature and salinity during germina- showed a poor recovery response. Zid and tion. Black seeds are more sensitive to change Boukharis (1977) found that a high percentage in temperature, and lower temperature regimes of ungerminated seeds of A. halimus recov- decreased seed germination in both saline and 200 WESTERN NORTH AMERICAN NATURALIST [Volume 64 nonsaline conditions. However, brown seeds GUSTAFSSON, M. 1973. Evolutionary trends in Atriplex tri- are more tolerant of both temperature and angularis group in Scandinavia. I. Hybrid sterility and chromosomal differentiation. Botanical Notisser salinity at cooler conditions. It appears that 126:345–392. brown seeds could germinate early in the grow- HALL, H.M., AND F.E. CLEMENTS. 1923. The phylogenetic ing season to preempt the site and have an method in taxonomy. The North American species of early start. This could result in a plant with Artemisia, Chrysothamnus and Atriplex. Carnegie In- more vigor and a higher reproductive effort stitute of Washington, Publication 326, Washington, later in the growing season as reported for A. DC. HANSEN, D.J., AND D.J. WEBER. 1975. Environmental fac- triangularis (Khan and Ungar 1996). Saline tors in relation to the salt content of Salicornia paci- desert habitats are subjected to rapid change fica var. utahensis. Great Basin Naturalist 35:86–96. in environmental conditions. Delay in rainfall HARPER, J. 1977. Population biology of plants. Academic could cause salinity concentration of the soil Press, London. solution to increase manyfold, which could IGNACIUK, R., AND J.A. LEE. 1980. The germination of four annual strand-line species. New Phytologist 84: result in high mortality of young plants. Under 581–591. these conditions new plants could be recruited KEIFFER, C.W., AND I.A. UNGAR. 1995. The effect of through black seeds, thereby ensuring conti- extended exposure to hypersaline conditions on the nuity of the species. So both seed morphs have germination of five inland halophyte species. Ameri- the potential for complementary establishment can Journal of Botany 84:104–111. KHAN, M.A. 1991. Studies on germination of Cressa cretica syndromes. L. seeds. Pakistan Journal of Weed Science Research 4:89–98. ACKNOWLEDGMENTS KHAN, M.A., AND B. GUL. 1998. High salt tolerance in germinating dimorphic seeds of Arthrocnemum indicum. M.A. Khan thanks the Department of Inte- International Journal of Plant Sciences 159:826–832. grative Biology at Brigham Young University KHAN, M.A., B. GUL, AND D.J. WEBER. 2000. Germination responses to Salicornia rubra to temperature and for the award of adjunct professorship and for salinity. Journal of Arid Environments 45:207–214. the use of university facilities, and thanks the ______. 2001a. 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INFLUENCE OF YELLOW STARTHISTLE (CENTAUREA SOLSTITIALIS) ON SMALL MAMMALS IN CENTRAL CALIFORNIA

Kirsten Christopherson1 and Michael L. Morrison2

ABSTRACT.—Yellow starthistle (Centaurea solstitialis) is native to Europe and Asia and has quickly invaded disturbed grasslands and rangelands in the western United States. The purpose of our study was to determine the effects of starthistle on rodents at Beale Air Force Base, Yuba County, California, by examining rodent species diversity, species abundance, age structure, and reproductive condition among locations with low, medium, and high percent cover and height of starthistle. Listed in decreasing order of abundance, the rodents were house mouse (Mus musculus), California vole (Microtus californicus), deer mouse (Peromyscus maniculatus), western harvest mouse (Reithrodontomys megalotis), and roof rat (Rattus rattus). Indices of diversity did not differ among starthistle cover categories. Regression analyses showed that Reithrodontomys megalotis was more abundant in high-cover starthistle plots, with 90.5% of captures occurring in at least 40% starthistle cover. Significant differences were found in capture rates, reproduction, and age between season only. To manage for all rodent species, an area with medium percent cover and height of starthistle will likely provide adequate protective cover.

Key words: small mammals, rodents, yellow starthistle, Centaurea solstitialis, Beale Air Force Base, Yuba County, California.

Yellow starthistle (Centaurea solstitialis; grasses could not use. Starthistle has become Asteraceae) is an aggressive, invasive annual an economic hardship on agriculture by inhibit- plant from the Mediterranean region of Europe ing the growth of other plants in orchards, and Asia. The first introductions in California vineyards, and rangelands (DiTomaso 1998). may have occurred as early as 1824 and were Exotic plant species also are recognized as followed by subsequent introductions through- a potential threat to the existence of many out the century (Roche et al. 1997). Starthistle wildlife species. Several studies have docu- has rapidly occupied grasslands and rangelands mented the negative effects of invasive plant that have previously undergone disturbance as species on Burrowing Owls (Athene cunicu- a result of agriculture, construction, military laria; Coulombe 1971, Zarn 1974) and Swain- activities, or other means. It is currently con- son’s Hawks (Buteo swainsoni; Estep 1989). sidered California’s most invasive weed, occu- The effects of nonnative plants on rodents have pying up to 6 million hectares in California also been documented. In New Mexico the (DiTomaso 1998, DiTomaso et al. 1999). The use of exotic vegetation by rodents correlated main feature that gives this plant an advantage only with short-term weather fluctuations, over annual and perennial competitors is the while native vegetation was used consistently difference in the timing of its life cycle. In late (Ellis et al. 1997). spring, when most grasses are flowering, yellow Our goal was to determine, by examining starthistle plants are just beginning to emerge differences in rodent assemblages between from the ground as small rosettes. By the time locations of starthistle and those with mainly the grasses have matured and the annuals have annual grasses, whether the introduction of become dormant, starthistle is just beginning yellow starthistle has been detrimental to noc- its reproductive stage (Roche et al. 1994). Roche turnal rodents. We determined whether differ- et al. (1994) showed that the starthistle plant ences existed in rodent (1) species diversity, concentrates its early growth on developing a (2) species abundance, (3) age, and (4) repro- deep taproot and later develops its leaves. ductive condition among locations with low, This strategy may allow it to survive summer medium, and high percentages of cover and drought conditions by reaching water that the height of starthistle. Although most grasses at

1Beale AFB Environmental Flight, 9 CES/CEV, 6601 B Street, Beale AFB, CA 95904. 2Great Basin Institute, University of Nevada, Reno, NV 89557-0031.

202 2004] SMALL MAMMALS AND STARTHISTLE 203 the site also are nonnative, these species are are medusahead (Taeniatherum caput-medusae), more closely related to the natural vegetation ripgut brome (Bromus diandrus), Italian rye- of the region than is starthistle, which differs grass (Lolium muliflorum), soft chess (Bromus substantially from most native and nonnative hordeaceus), and wild oat (Avena fatua). Forbs grasses in its height, canopy cover, and life and native perennial grasses also occur, but cycle. they are relatively rare compared with domi- Van Horne (1983) and Pulliam (1988) recog- nant introduced grasses. The base also supports nized that the presence of animals in an area relatively smaller areas of riparian oak (Quercus does not necessarily imply that the area is of spp.) woodlands and oak savannah (U.S. Army high quality. A high-quality habitat, or source, Corps of Engineers 1999), but it is mainly the is one in which reproductive success outweighs grassland areas that have widespread, heavy mortality (Van Horne 1983). If the highest- infestation of yellow starthistle. quality habitat is saturated, the young or less fit animals may be forced into areas of lesser METHODS quality. In such sinks, little or no reproduction takes place and mortality is relatively high (Van We established 21 sampling plots that con- Horne 1983, Pulliam 1988, Meffe and Carroll sisted of varying amounts of starthistle cover. 1994). Therefore, we collected data on age and Sampling plots were chosen by visually esti- reproductive condition in an attempt to deter- mating the percentage of starthistle within the mine the quality of the habitat. proposed trapping area. We conducted our study from April 1998 through March 1999 for a STUDY SITE total of 6745 trap-nights. Trapping was divided into 4 seasons: spring, April–June 1998 (1889 Beale Air Force Base (AFB; 39°8′N, trap-nights); summer, July–September 1998 121°26′W) is in Yuba County, California, on (1890 trap-nights); autumn, October 1998–early the eastern edge of the Central Valley be- January 1999 (1529 trap-nights); and winter, tween the agricultural lands of the valley and late January–March 1999 (1437 trap-nights). the foothills of the western Sierra Nevada. We sampled all 21 plots each season. Trap- The base is 9285 ha in size, of which approxi- nights varied between seasons because high mately 80% is undeveloped. Elevation varies capture rates in some seasons required the re- from 26 m to 213 m above mean sea level, duction in number of traps set in the interest generally with the higher elevation on the east of animal safety (i.e., because of wet or cold side of the base in the Sierra Nevada foothills weather); most plots were sampled for 3 nights. (U.S. Army Corps of Engineers 1999). Because of unequal trapping efforts, we ex- The site has cool, moist winters and hot, dry press relative rodent abundance as a capture summers. Average annual precipitation is index, calculated by multiplying the number approximately 52 cm, most of which occurs be- of new animals caught per trap night by 100 tween November and March. Average monthly trap-nights (Nichols and Conroy 1996, Morri- temperatures range from 4°C in December son and Hall 1998). and January to 36°C in July (Beale AFB Com- Because many plot sizes were limited by bat Climatology Center unpublished data). boundaries such as fences, grazed pastures, The rainy season of 1997–98 was under the firing ranges, and buildings, standard plot con- effects of the El Niño ocean currents. Rainfall figurations were not possible. Instead, each plot at the study site from July 1997 to June 1998 consisted of 3 lines spaced 15 m apart, and was 103.48 cm, approximately double the aver- each line contained 10 trap stations with each age. The rainy season that usually ends in March trap spaced 10 m away from the next; thus, continued into June 1998 with localized flood- each plot covered approximately 2700 m2. ing. Abnormal freezing temperatures occurred Large Sherman live-traps (7.6 × 8.9 × 22.9 in mid-December (Beale AFB Combat Clima- cm) were baited with a rolled oats and peanut tology Center unpublished data). butter mixture. They were furnished with poly- The land comprises mostly exotic annual ester batting material and covered on the tops grassland, about 50% of which supports cattle and sides with soil and plant material to grazing from November through May of each decrease the chance of hypothermia. When year. Common nonnative grasses at the site necessary, we also protected traps from rain 204 WESTERN NORTH AMERICAN NATURALIST [Volume 64 and excessive heat by placing cedar shingles (Zar 1996:39) for each starthistle cover cate- on top. Traps were set out in late afternoon gory within each season and performed a 2- and checked each morning. All mammals cap- way ANOVA of season versus cover category. tured were identified to species and marked Starthistle cover categories, starthistle height with a permanent marking pen and toenail categories, and the 4 seasons were used as in- clipping to determine whether animals were dependent variables in 3-way factorial ANOVA recaptured within the same session. tests (Zar 1996:179) on the dependent vari- Age, mass (weight in grams), and reproduc- ables of abundance capture index, reproductive-condition data were used to compare the tive-condition index, and age-structure index quality of plots. Age was categorized as adult, for all captures combined as well as each species subadult, or juvenile depending on established individually. In reporting ANOVA test results, weights and pelage color for each species. we will discuss only the main effects unless we Reproductive condition was scored as nonre- specifically state that an interaction occurred productive, scrotal testes, perforated vagina, between independent variables. When the null enlarged nipples, and/or pregnant. All animals hypothesis was rejected in any ANOVA, the were released at the capture site. To correct Tukey test (Zar 1996:212) was used to deter- for closed but empty traps, we adjusted trap- mine where differences existed. nights prior to analysis following Jackson (1952) Additionally, we performed separate simple and Nelson and Clark (1973). A reproductive- linear regression analyses (Zar 1996:319) on condition index was determined by dividing the percentage of starthistle cover versus rodent the number of reproductive animals by the abundance for each species and total animal total number of different individuals captured, abundance within each season. This set of tests while an age-structure index was calculated as was performed to assess whether the level of total number of different adults captured divided starthistle in an area can be a predictor of by total number of individuals captured. abundance of each species caught or of total We quantified vegetation cover using the animal abundance. point-intercept method (Higgins et al. 1996, Elzinga et al. 1998) once per season in each of RESULTS the 21 trapping plots. Additionally, in each trapping plot we assessed vegetation at 19 points Listed in decreasing order of abundance, spaced 5 m apart along each of the 3 transects the 5 rodent species captured were house for a total of 57 points per trapping plot. mouse (Mus musculus), California vole (Micro- Starthistle cover was calculated as a percent- tus californicus), deer mouse (Peromyscus manage in each plot by dividing total number of iculatus), western harvest mouse (Reithrodon- points scoring positive for starthistle by total tomys megalotis), and roof rat (Rattus rattus; number of points measured. This process Table 1). Only a single R. rattus was captured allowed the placement of each plot into a star- during the study, and while it was used in cal- thistle category: low (0%–33%), medium (34%– culating diversity indices, the species was not 67%), or high (68%–100%) starthistle cover. used in all statistical tests. Average yellow starthistle height at each plot All 4 predominant species were captured in was calculated, and 3 average height categories all categories of starthistle cover. Indices of were established: low (≤25 cm), medium (26– diversity did not differ among seasons (F = 49 cm), or high (≥50 cm). 2.34, df = 3, P = 0.15) or starthistle cover cat- We initially tested all data for normality us- egories (F = 0.89, df = 2, P = 0.44). ing the Kolmogorov-Smirnov goodness-of-fit For overall species abundance, no signifi- test (Zar 1996:471). Data that were not normal cant differences were detected among the low, were transformed via logarithmic or arcsine medium, and high categories of starthistle transformations and tested again for normality. cover (F = 1.38, df = 2, 81, P = 0.26) or Because the data did not deviate severely from starthistle height (F = 2.63, df = 2, 81, P = the assumptions of the tests, we used parame- 0.08), but significant differences in abundance tric tests for their increased power (Zar 1996: existed between seasons (F = 23.53, df = 3, 187). All statistics were performed with alpha 81, P < 0.001). The spring capture rate was ≤ 0.05. Using the species abundance indices, significantly lower than all other seasons in we calculated a Shannon-Wiener diversity index that it represented only 4.3% of total captures 2004] SMALL MAMMALS AND STARTHISTLE 205

TABLE 1. Abundance indices by season and species at Beale Air Force Base, Yuba Co., CA, during yellow starthistle study from April 1998 to March 1999. Abundance index = (number of different individuals / number of trap-nights) × 100. Mus Microtus Peromyscus Reithrodontomys Rattus Season Total musculus californicus maniculatus megalotis rattus Spring 3.5 0.6 1.8 1.2 0.0 0.0 Summer 17.1 7.3 8.2 1.2 0.4 0.0 Autumn 35.7 16.3 16.9 1.2 1.4 0.0 Winter 25.0 10.9 5.4 5.8 2.9 0.1

in our study. Summer had a significantly lower of all captures) in comparison with all other capture rate (21.0% of total captures) than seasons when the reproductive rate ranged autumn (43.9% of total captures; Table 1). from 3.2% to 27.3% (F = 22.43, df = 3, P < The abundance of Mus was significantly (F 0.001). Reithrodontomys megalotis was more = 11.62, df = 3, 81, P < 0.001) lower in spring reproductively active in the summer season than in all other seasons. When rodent abun- (50% of all captures) compared with the other dance versus starthistle cover, height, and sea- seasons in which the reproductive rate ranged son was analyzed for each species individually, from 0% to 4.9% (F = 10.58, df = 2, P = 0.004). significant differences were detected for R. The overall reproductive index for summer was megalotis and M. californicus. An interaction at least 24% lower than all other seasons. between starthistle cover and season was iden- In testing individual species for age-related tified for R. megalotis abundance (F = 4.42, df effects of starthistle cover, starthistle height, = 6, P = 0.001). The winter season accounted and season, significant differences were found for 61.7% of all R. megalotis captures, and only for R. megalotis by season. More adult 90.5% of all individuals of this species were in animals were captured in autumn (85.7% of plots with at least 40% starthistle cover. An captures) and winter (95.1% of captures) as interaction was detected between starthistle opposed to only 50% in the summer (F = 6.79, cover and height (F = 4.59, df = 4, P = 0.003) df = 2, P = 0.016). No R. megalotis individu- and starthistle height and season (F = 2.43, df als were captured in the spring. = 5, P = 0.046) for M. californicus abundance. The autumn season accounted for 52.3% of all DISCUSSION individuals of M. californicus captured, with the highest percentage (48.2%) caught in low All 4 main rodent species captured were starthistle. Only 5.6% of M. californicus were found in all 3 categories of starthistle cover. captured in spring, with most (96.7%) of these However, capture rate was lowest in spring. in medium and tall starthistle. This low capture rate was likely related to the There was a significant relationship between heavy rain during the spring season and is starthistle cover and abundance of R. megalo- probably not typical of all years. Localized tis over all seasons (r2 = 0.08, n = 84, P = flooding conditions may have forced rodents to 0.01) and specifically in winter (r2 = 0.37, n = abandon their burrows or other nesting sites, at 21, P <0.01). Sixty-two percent of the cap- which time they became more exposed to pre- tures of this species occurred in winter. dation (Getz 1985). When reproductive condition was assessed Vegetative cover is thought to be the most in relation to starthistle cover and height and important factor in supporting healthy Micro- season, only the effect of season was signifi- tus populations, and in most studies popula- cant. Microtus californicus had lower repro- tion size tends to correlate positively with ductive activity (3.5% of all captures) in autumn cover (Rose and Birney 1985). Increased cover than in spring and winter seasons, when 25.3% provides protection from predators and perhaps and 31.2% of individuals, respectively, were regulates humidity and temperature. Predation reproductively active (F = 5.13, df = 3, P = is one of the most significant pressures on 0.004). Mus musculus was more reproduc- Microtus as this species is a frequent prey item tively active during the summer season (65.2% in most grasslands (Pearson 1985). Because 206 WESTERN NORTH AMERICAN NATURALIST [Volume 64 our results did not indicate a positive relation- native bunchgrasses can be successfully estab- ship between Microtus abundance and star- lished, they would provide a situation in which thistle cover, we think that areas with high an investigation could be conducted to com- starthistle cover and areas with the other plant pare starthistle and nonnative grassland areas species (primarily nonnative grasses) present with restored sites composed of native grasses. at our study site provide adequate cover for this species to survive and reproduce. ACKNOWLEDGMENTS Reithrodontomys megalotis and M. californicus are cover-dependent species that avoid We thank the United States Air Force for areas that lack plant cover (Kaufman and supporting this project and allowing access to Kaufman 1989, Poopatanapong and Kelt 1999). their land; B. Reinhardt for providing supplies, In our study R. megalotis was the only species equipment, and other logistical support; S. to significantly increase in abundance in re- Abafo, C. Bailey, S. Hoover, M. Hulst, J. Love- sponse to increased yellow starthistle cover. lady, J. Orr, W. Swift, and N. Tuato’o-Bartley The low r2 (0.08) for R. megalotis over all sea- for field support; L. Hall-Stiernelof, G. Trapp, sons was likely the result of the few captures and M. West for input on the study design and analysis; and 2 anonymous reviewers for proof this species over the entire study. Because viding constructive comments. 62% of all R. megalotis captures occurred in the winter, this higher number of captures LITERATURE CITED within fewer trapping sessions may account 2 for the relatively higher r value of 0.37. We COULOMBE, H.N. 1971. Behavior and population ecology think the higher capture rate of Reithrodonto- of the burrowing owl, Speotyto cunicularia, in the mys in high starthistle cover particularly sup- Imperial Valley of California. Condor 73:162–176. DITOMASO, J.M. 1998. Biology and impact of yellow star- ports the idea of cover dependence. thistle. Pages 82–84 in M.S. Hoddle, editor, Califor- Mus, the most abundant species captured nia conference on biological control. University of during our study, was ubiquitous across the California Press, Berkeley. study plots regardless of starthistle height and DITOMASO, J.M., W.T. LANINI, C.D. THOMSEN, T.S. PRATHER, C.E. TURNER, M.J. SMITH, C.L. ELMORE, ET AL. 1999. cover. It is unlikely, therefore, that this species Pest notes: yellow starthistle. University of Califor- can be managed through changes in starthistle nia Agricultural and Natural Resources Publication structure. 7402, University of California, Davis. Although some differences in abundance ELLIS, L.M., C.S. CRAWFORD, AND M.C. MOLLES, JR. 1997. Rodent communities in native and exotic riparian were found, we ascertained no significant rela- vegetation in the middle Rio Grande Valley of cen- tionships between reproductive-condition index tral New Mexico. Southwestern Naturalist 42:13–19. and starthistle development (cover or height). ELZINGA, C.L., D.W. SALZER, AND J.W. WILLOUGHBY. 1998. It appears, therefore, that individuals were Measuring and monitoring plant populations. BLM Technical Reference 1730-1, Bureau of Land Man- able to reproduce in all categories of starthis- agement, Denver, CO. tle even though abundances might be rela- ESTEP, J.A. 1989. Biology, movements, and habitat relation- tively low in certain categories. Thus, no dif- ships of the Swainson’s Hawk in the Central Valley ferences in habitat quality as measured by of California, 1986–1987. California Department of Fish and Game, Nongame Bird and Mammal Sec- reproductive condition were evident. tion Report, Sacramento. At Beale AFB and other locations in the GETZ, L.L. 1985. Habitats. Pages 286–309 in R.H. Tamarin, region, attempts are being made to restore editor, Biology of new world Microtus. American native plant communities. We do not know the Society of Mammalogists. HIGGINS, K.F., J.L. OLDEMEYER, K.J. JENKINS, G.K. CLAM- impact that such restoration activities might BEY, AND R.F. HARLOW. 1996. Vegetation sampling have on rodent communities, including the and measurement. Pages 567–591 in T.A. Bookhout, influence on abundance of the exotic Mus. We editor, Research and management techniques for wild- have, however, shown that even a noxious weed life and habitats. Allen Press, Inc., Lawrence, KS. JACKSON, W.B. 1952. Populations of the wood mouse (Per- such as yellow starthistle can provide high- omyscus leucopus) subjected to the applications of quality habitat for rodents. Planting bunch- DDT and Parathion. Ecological Mongraphs 22: grasses such as purple needlegrass (Nassella 259–281. pulchra) might provide the necessary habitat KAUFMAN, D.W., AND G.A. KAUFMAN. 1989. Population biology. Pages 233–270 in G.L. Kirkland, Jr., and J.N. components, including protective cover, with Layne, editors, Advances in the study of Peromyscus which these animals evolved. If large areas of (Rodentia). Texas Tech University Press, Lubbock. 2004] SMALL MAMMALS AND STARTHISTLE 207

MEFFE, G.K., AND C.R. CARROLL. 1994. Principles of con- taurea solstitialis L.) invasion. Northwest Science servation biology. Sinauer Associates, Inc., Sunder- 68:86–96. land, MA. 600 pp. ROCHE, C.T., D.C. THILL, AND B. SHAFII. 1997. Reproduc- MORRISON, M.L., AND L.S. HALL. 1998. Responses of mice tive phenology in yellow starthistle (Centaurea sol- to fluctuating habitat quality. I. Patterns from a long- stitialis). Weed Science 45:763–770. term observational study. Southwestern Naturalist ROSE, R.K., AND E.C. BIRNEY. 1985. Community ecology. 43:123–136. Pages 310–339 in R.H. Tamarin, editor, Biology of NELSON, L., JR., AND F. W. C LARK. 1973. Correction for new world Microtus. American Society of Mammalo- sprung traps in catch effort calculations of trapping gists. results. Journal of Mammalogy 54:295–298. U.S. ARMY CORPS OF ENGINEERS. 1999. Integrated natural NICHOLS, J.D., AND M.J. CONROY. 1996. Techniques for resources management plan—Beale Air Force Base, estimating abundance and species richness. Pages California. Volume I. Sacramento, CA. Prepared 177–234 in D.E. Wilson et al., editors, Measuring with technical assistance from Jones & Stokes Asso- and monitoring biological diversity: standard methods ciates (JSA 96-219), Sacramento, CA. Prepared for for mammals. Smithsonian Institution Press, Wash- Beale Air Force Base, CA. ington, DC. VAN HORNE, B. 1983. Density as a misleading indicator of PEARSON, O.P. 1985. Predation. Pages 535–566 in R.H. habitat quality. Journal of Wildlife Management 47: Tamarin, editor, Biology of new world Microtus. 893–901. American Society of Mammalogists. ZAR, J.H. 1996. Biostatistical analysis. Prentice Hall, Upper POOPATANAPONG, A., AND D.A. KELT. 1999. Management Saddle River, NJ. 662 pp. of small mammals in a relict grassland in California’s ZARN, M. 1974. Burrowing owl (Speotyto cunicularia hy- Central Valley. Transactions of the Western Section pugaea). Habitat management series for unique or of the Wildlife Society 35:15–21. endangered species. Report 11, T-N-250, Bureau of PULLIAM, H.R. 1988. Sources, sinks, and population regu- Land Management, Denver, CO. 25 pp. lation. American Naturalist 132:652–661. ROCHE, B.F., C.T. ROCHE, AND R.C. CHAPMAN. 1994. Im- Received 13 August 2001 pacts of grassland habitat on yellow starthistle (Cen- Accepted 9 June 2003 Western North American Naturalist 64(2), ©2004, pp. 208–218

CONE AND SEED PRODUCTION IN PINUS PONDEROSA: A REVIEW

Pamela G. Krannitz1 and Thomas E. Duralia1

ABSTRACT.—Factors associated with seed cone production in Pinus ponderosa were reviewed to identify broad patterns and potential effectiveness of restoration activities. Cone and seed production are quite variable, with differences between (1) years, (2) sites, and (3) individual trees. Between-year, population-wide crop failures suggest large-scale triggers for cone and seed production, perhaps high temperatures and dry weather. Stem diameter is the most important determinant for cone production at the tree level, with other factors such as genetic disposition, moisture, soil nutrients, and insect pests and disease playing a smaller role. Some extrinsic factors affect growth rate, indirectly affecting cone production. For example, less competition and lower stand densities result in P. ponderosa trees that increase in diameter more quickly, possibly because of more light, and produce seeds earlier. This literature suggests that restoration activities, especially thinning, will result in trees better able to produce larger seed crops. The effect of prescribed fire is less clear, with contradictory effects depending on site conditions, burn severity, and nutrient status of the site.

Key words: Ponderosa pine, cone production, seed production, restoration activities, stand thinning.

Historical reconstruction of ponderosa pine, Picoides albolarvatus than newer and managed Pinus ponderosa Dougl. ex P.&C. Lawson, for- stands (Dixon 1995). Restoration activities in ests over the last 100 years has shown range- Washington state have focused on reintroduc- wide significant increases in densities and a ing fire to Pinus ponderosa ecosystems which, concomitant reduction in fire frequency (Cov- in Methow Valley Ranger District, has resulted ington and Moore 1994, Mast et al. 1997, 1999, in anecdotal reports of increased abundance of Brown and Sieg 1999, Moore et al. 1999, Picoides albolarvatus (Dale Swedberg personal Everett et al. 2000, Veblen et al. 2000, Turner communication). Picoides albolarvatus is the and Krannitz 2001). This has resulted in an umbrella species of restoration activities in the emphasis toward restoration of Pinus ponder- northern part of the range for Pinus ponderosa forests to reduce tree densities to earlier osa, and yet there are very little data on the levels to prevent wildfires, to rejuvenate stands, effect of tree thinning and prescribed burning and to benefit associated wildlife (Covington on the ecosystem or the bird. In the South- et al. 1994, Harrod et al. 1999, Mast et al. 1999, west, Picoides albolarvatus does not occur, but Kolb et al. 2001). One wildlife species of inter- general effects of tree ingrowth on diversity of est in the northernmost part of the P. pon- native flora and fauna are of concern (Coving- derosa range is the uncommon and in some ton and Moore 1994). Here, a research team at places endangered White-headed Woodpecker, Northern Arizona University at Flagstaff has Picoides albolarvatus. The White-headed wood- promoted and initiated restoration of Pinus pecker is most abundant in California, where ponderosa (Covington et al. 1997) and has be- it relies on seeds from a variety of tree species gun documenting some of the effects on the (Garrett et al. 1996). Picoides albolarvatus ecosystem (i.e., Crawford et al. 2001). albolarvatus is a species of concern in Oregon, Because of the lack of direct evidence on Washington, and Idaho, while in British Colum- the benefits of current restoration activities for bia it is nationally endangered. Here, P. pon- seed-eating species of interest such as Picoides derosa cones provide the only suitable food albolarvatus, this review gathers what is known source in the nonbreeding months (Garrett et about cone production in P. ponderosa in gen- al. 1996). In Oregon it is clear that old-growth eral and assesses whether restoration activities Pinus ponderosa stands, with many snags and are likely to benefit Picoides albolarvatus large-diameter trees, are more productive for through enhanced cone production.

1Environment Canada, Canadian Wildlife Service, 5421 Robertson Road, RR 1 Delta, British Columbia, Canada, V4K 3N2.

208 2004] SEED PRODUCTION IN PINUS PONDEROSA 209

STUDY SPECIES resumes the next spring, fertilization takes place, and seeds mature by fall. This lengthy (26- to Taxonomy and Range 27-month) reproductive cycle of initiation, dif- Three varieties of Pinus ponderosa Dougl. ferentiation, pollination, fertilization, and em- ex P.&C. Lawson are recognized though the bryo and seed development provides a large taxonomy is not yet resolved: P. ponderosa var. window for a complex variety of potentially ponderosa Dougl. (Pacific ponderosa pine), P. interacting factors to play a role in the fre- ponderosa var. scopulorum Engelm. (Rocky quency of P. ponderosa cone production and Mountain ponderosa pine), and P. ponderosa the quantity of seeds produced (Roeser 1941, var. arizonica (Engelm.) Shaw (Arizona pine; Puritch and Vyse 1972, Eis et al. 1983, Owens Kral 2000). The distribution of P. ponderosa and Blake 1985, Eremko et al. 1989). ranges from near 52°N in south central and southeastern British Columbia (both ponder- Variability in Productivity osa and scopulorum subspecies) east to Nebra- Seed cone production in Pinus ponderosa is ska, south to northern Mexico (the arizonica variable, with 3 broad categories of contribut- subspecies), and west to the Pacific Coast (Kral ing factors: differences between (1) years, (2) 2000). Within the Pacific variety 3 races (South- sites, and (3) individual trees (Table 1). Many ern California, Pacific, and North Plateau) have years result in no cone production at all, and been differentiated (Conkle and Critchfield other years result in heavy production, with 1988). There are also 3 races within P. pon- many cones on more than half the population derosa var. scopulorum: Southern, Central, (McDonald 1992). Throughout its range, these and Northern Interior (Wells 1964). abundant crops occur about every 3 to 8 years The P. ponderosa environment is broadly (Roeser 1941, Fowells and Schubert 1956, Lar- characterized by cool to cold winters and warm, son and Schubert 1970, Boldt and van Deusen dry summers with periods of prolonged drought. 1974, Dahms and Barrett 1975, Eis et al. 1983). Because P. ponderosa is the widest ranging Differences in cone production between pine in North America, the droughts that sites within an area are not as variable, with occur during different seasons in its areas of some site differences being marginally signifi- distribution depend on location. In the Pacific cant (Table 1; data from Dale and Schenk 1978) Northwest and California, summers are typi- and others not being significant at all (Table 1; cally dry, while summer rains are usual for the data from Linhart 1988). Within sites, differ- eastern slope of the Rockies, the Black Hills of ences in cone production between trees can South Dakota, and the Southwest (Curtis and be striking, with some trees consistently being Lynch 1957, Hope et al. 1991, Agee 1998). big producers (Linhart and Mitton 1985). Annual precipitation in the ponderosa pine zone of British Columbia is 280–500 mm REGULATION OF SEED (Hope et al. 1991). AND CONE PRODUCTION The range of P. ponderosa encompasses elevations from near sea level at Tacoma, Washing- The 27-month development of a seed-bear- ton, to between 250 m and 1200 m in British ing cone provides many opportunities for ma- Columbia (Eremko et al. 1989), and to more ternal regulation of seed and cone production than 2740 m in California, Colorado, and Ari- via cone, ovule, or embryo abortion. Though P. zona (Curtis and Lynch 1957). ponderosa cone crops can be decimated by a combination of physiological dysfunction and Reproductive Cycle insect damage, unexplained conelet abortions and Seed Production can prevent as much as 66% of the ovules from For 12- to 16-year-old P. ponderosa trees in becoming seed (Pasek and Dix 1988). Good the northern part of the range, seed cones are years for producing cones are also good years initiated in mid- to late summer and differen- for producing seed: over a 24-year period, tiate in September to October (Eis et al. 1983, more filled seeds than unfilled seeds were pro- Owens and Blake 1985). Pollination occurs duced in years with heavy cone production between April and June the following year, and (McDonald 1992). pollen tube and ovule development begins There has been one study on factors associ- and proceeds until midsummer. Development ated with ovule abortion, though it was done 210 WESTERN NORTH AMERICAN NATURALIST [Volume 64

TABLE 1. Variability in seed or cone production for Pinus ponderosa (PP). K = 1000. Variation in seed Time Location or cone production period Comments Source California 0–18K seeds ⋅ ha−1 to 400K 1200K seeds ⋅ ha−1 (yearly) 24 years r2 = 0.76, P < 0.01 McDonald 1992 1958–1981 filled seeds and cone crop, 613 trees ⋅ ha−1 Washington 0–384 cones ⋅ tree−1, 48% variation 7 years 8 different PP trees Daubenmire 1960 attributed to year (P < 0.0001) 1951–1957 followed and 9% to tree (P > 0.2)a Idaho and 0–9.4K cones ⋅ 100 PP trees−1,3 years 12 widely dispersed Dale and Schenk eastern 32% variation attributed to site 1967–1969 sites, 42–770 1978 Washington (P = 0.07), 28% to year PP ⋅ ha−1 (P = 0.002)a Colorado 4–12.3K cones ⋅ 100 PP trees−1,4 years 4 sites Linhart 1987 1.3% variation attributed to site 1984–1987 (P > 0.2), 42% to year (P = 0.10)a Arizona 1.2–29.7 cones ⋅ 100 PP trees−1 10 years 62.5 PP ⋅ ha−1 Larson and 1956–1965 Shubert 1970 Colorado 0–7.7K cones ⋅ 100 PP trees−1 10 years 78 PP ⋅ ha−1 Roeser 1941 1926–1935 California 0–338 cones ⋅ 100 PP trees−1 21 years 5 PP ⋅ ha−1, 9 P.Fowells and 1933–1953 lambertiana ⋅ ha−1, Shubert 1956 48 Abies concolor ⋅ ha−1 aANOVA, SAS 1990

on a congener of Pinus ponderosa (Karkkainen Washington, larger cone crops of 8 trees over et al. 1999). Seventy-six percent of experimen- 7 years were correlated with higher-than-aver- tally self-pollinated ovules in P. sylvestris age June through September temperatures 2 aborted, compared with 26.5% for cross-polli- years earlier (Daubenmire 1960). Temperature nated and 30% for naturally pollinated ovules. effects have also been demonstrated in other For naturally pollinated seeds, maternal genetic Pinus species: differences between 1995 and differences accounted for 29% of the variation 1996 in cone production in P. sylvestris were in ovule abortions (Karkkainen et al. 1999). associated with differences in temperatures at Unfortunately, no measurements of the effect time of bud initiation in 1993 and 1994 (Karls- of environmental variables were made. Ovule son 2000). abortions have been thought to be associated There is scattered evidence that cold tem- with self-pollination, temperature, competition, peratures negatively affect seed cone crops in and disease or insect infestation (Owens and P. ponderosa (Maguire 1956, Schubert 1974, Blake 1985, Karlsson 2000). Barrett 1979, Owens and Blake 1985), with below-freezing, late spring temperatures killing FACTORS AFFECTING FREQUENCY 2nd-year conelets (Maguire 1956, Sorensen AND QUANTITY OF CONE CROPS and Miles 1974). Pollen cones of P. ponderosa are less susceptible to freezing (Roeser 1941), Factors Contributing as are cones of other pine species such as P. to Annual Variation contorta (Sorensen and Miles 1974). Negative TEMPERATURE.—Higher-than-average tem- effects of cold temperatures underscore how peratures during seed cone initiation in P. weather at any time during the 27-month P. ponderosa have been associated with above- ponderosa reproductive cycle might negate or average cone production. Over a 23-year period enhance weather effects at another time (Dau- in California, whenever total average tempera- benmire 1960). tures for April and May were above or below MOISTURE.—Little information exists on the average, the cone crop 27 months later was effects of moisture specific to seed cone pro- also above or below average, respectively duction in P. ponderosa, and results from other (Maguire 1956). Similarly, in Whitman County, species are conflicting and often confounded 2004] SEED PRODUCTION IN PINUS PONDEROSA 211 by other factors (Owens and Blake 1985). For When P. ponderosa stands are thinned, pho- example, there is a positive correlation between tosynthetically active radiation increases (Riegel low rainfall in the spring and summer months et al. 1992), and subsequent increases in seed when cones are initiated and subsequent cone production are often attributed to increased production, but low moisture is often accom- light (Sprague et al. 1979). Evidence from panied by high temperatures and high insolation Pinus species other than ponderosa suggests (Owens and Blake 1985). Anecdotal evidence that an increase in light results in an increase suggests that reproductive bud initiation in P. in cone production, either for whole trees (P. ponderosa benefits from dry summers (Eis et al. sylvestris; Sarvas 1962) or individual branches 1983, Eremko et al. 1989). Irrigation in the (P. banksiana; Despland and Houle 1997). spring combined with removal of moisture in Anecdotal evidence suggests that P. ponderosa the summer produced larger cone crops in P. is similarly dependent on light (Pearson 1912). taeda than in controls (Dewers and Moehring In addition, changes in the crown location of 1970). cone production upon stand thinning showed a localized dependence on light; P. sylvestris Site-related Factors trees in a closed stand produced 40% of cones STAND DENSITY.—In general, there is an in the upper 2 m of crown, and 7 years post- increase in productivity, including seed cone thinning that figure dropped to 15%, with a production, with a decrease in stand density. greater proportion of cones being produced on In a comparison of 12 sites in Idaho, seed pro- lower branches that were now exposed to light duction was negatively associated with density (Karlsson 2000). These kinds of localized of both P. ponderosa (rs = –0.80, P = 0.0034) changes in cone production attributable to and all trees (rs = –0.67, P = 0.017; data from light are better indicators of the importance of Dale and Schenk 1978; Spearman rank corre- light than whole-tree responses because stand lation [SAS 1990]). Similarly, 4 blocks of vary- thinning will also affect midday temperatures ing P. ponderosa stem densities in Arizona (Riegel et al. 1992). showed concomitant variation in cone and seed NUTRIENT AVAILABILITY AND FERTILIZERS.— production (rs = –1.0, P < 0.0001; data from Effects of increased nutrients, either added or Heidmann 1983). Cone yield differences in as a result of thinning, are not as clear as the response to stand density have been observed effect of increased light. Often there is im- for many decades, with individual P. ponderosa proved flowering and seed production in Pinus trees yielding on average 24.7 L of cones in when fertilization is combined with thinning, “dense” stands, 38.8 in “medium,” and 63.4 in irrigation, or girdling treatments (Puritch and “open” stands (Pearson 1912). Vyse 1972, Owens and Blake 1985). For exam- When P. ponderosa stands are thinned, stem ple, P. taeda clones increased seed cone pro- diameter of released trees consistently increases duction much more in a combined irrigation (Schubert 1974, Martin 1988, Feeney et al. and fertilization treatment than in either treat- 1998); this also holds true for older individuals ment alone (Sprague et al. 1979, Gregory et al. 150+ years of age (Latham and Tappeiner 1982). 2002). The responses of stem diameter to re- When N alone was added to thinned stands ductions in stem density are consistent, and in of P. sylvestris, an increase in stemwood pro- Pinus resinosa they have been predictably mod- duction occurred, but cone production was eled (Laroque 2002). Stem diameter is consis- lower than that of the controls (Valinger 1993). tently associated with cone production (see Adding P along with N at 3 levels of concen- section below on tree size, age, and domi- tration to a thinned, even-aged, 55-year-old P. nance), and the growth response to thinning ponderosa stand near Flagstaff, Arizona, resulted can be large: P. ponderosa stands in the South- in a linear increase of seed cone production west thinned from 48.21 m2 to 6.89 m2 basal (Heidmann 1984). The number of trees bear- area ⋅ ha−1 grew 5 times faster in diameter ing cones was always highest in the high fertil- than those in unthinned stands (Schubert 1974). izer treatments, and significantly higher in year Since trees of larger diameter produce the 4 (P < 0.025) and marginally higher in year 5 majority of cones, increased cone production (P < 0.1) of a 6-year study. The period of the may be a longer-term benefit of thinning. experiment encompassed 3 reasonably good 212 WESTERN NORTH AMERICAN NATURALIST [Volume 64 cone crops, with production in these years lin- poor P. ponderosa sites do not have extra total early related to fertilizer levels (P < 0.05). Dur- N to transform, however, and even light sur- ing this time period 4 times more cones were face fires can be detrimental to trees over time produced on trees fertilized at the high rate in this case (Monleon et al. 1997). than in the unfertilized controls (Heidmann Tree Differences 1984). FIRE EFFECTS.—Pinus ponderosa evolved TREE SIZE, AGE, AND DOMINANCE.—For Pinus with relatively frequent, but low-intensity, fires in general and Pinus ponderosa in particular, (Agee 1988, Arno 1988), and fire suppression the largest seed and cone crops are borne by over the last 100 years has resulted in dramatic the largest-diameter trees (Fowells and Schu- increases in stem density (Harrod et al. 1999, bert 1956, Larson and Schubert 1970, Sundahl Mast et al. 1999, Turner and Krannitz 2001). 1971, Linhart and Mitton 1985, Latta and Lin- From the literature already reviewed, it is hart 1997, Karlsson 2000). In a 6-year study fol- clear that thinning results in greater cone pro- lowing more than 200 Colorado P. ponderosa duction, but there is little direct data on whether trees, diameter was a better predictor of cone or not fire improves production over and above production (r2 = 0.43, P < 0.001) than age that of thinning. The effect of fire on P. pon- (P > 0.05), although diameter and age were derosa ecosystems is complex and may be correlated (P < 0.001; Linhart and Mitton 1985, beneficial or detrimental, depending on the Latta and Linhart 1997). In California, P. pon- nutrient status of the site, initial conditions of derosa trees over 66 cm dbh produced at least the stand, and timing and severity of the burn. some cones over a 16-year period, while only The effect of fire on cone and seed produc- 13% of the smallest class (between 9.1 and tion can be indirectly assessed by its effect on 19.1 cm dbh) bore cones (Fowells and Schu- growth because larger trees generally produce bert 1956). Only P. ponderosa trees ≥49.5 cm more cones (see next section). In unthinned P. in diameter produced 500 cones or more at ponderosa stands, fire was detrimental to least once in the 16-year period (Fowells and growth of surviving trees (Sutherland et al. Schubert 1956). 1991, Swezy and Agee 1991) largely because Larger-diameter trees also produce cones of high burn severity attributable to accumu- more frequently. Over a 16-year period in Cal- lated fuels due to fire suppression. When fire ifornia, frequency of cone production ranged occurred in a thinned stand in Arizona, with from once for the 19.3–29.2 cm dbh class up to the woody debris having been removed prior 10 times for all trees larger than 61 cm (rs = to the fire, fire improved resin production 0.65, P = 0.02, n = 12, for number of crops in compared with the thinned treatment and the 16 years and diameter; data from Fowells and control (Feeney et al. 1998). This has been Schubert 1956; Fig. 1). Similarly, in Arizona associated with increased resistance to insect the frequency of cone crops was highly corre- pests such as the bark beetle (Feeney et al. lated with tree diameter (Larson and Schubert 1998), which may in turn affect growth and or 1970; Fig. 1). Cone production of 100 cones or cone production. more per tree was not as frequent as crops The effect of fire on nutrient availability for with more than 5 cones, but both classes in- Pinus ponderosa will be noticeable in cone creased in frequency with diameter (Larson production (see previous section on nutrient and Schubert 1970; Fig. 1). Frequency of cone availability). Fire did not affect the rate of N production increased linearly with diameter cycling over and above that of thinning in both up to approximately 80 cm in diameter, after Arizona (Kaye and Hart 1998) and a nutrient- which it plateaued (Fig. 1). Similarly, cone pro- poor site in Oregon (Monleon et al. 1997), but duction in P. ponderosa increased with age but it decreased total N and organic-matter con- the rate of increase was smaller among older tent (Covington and Sackett 1984, Kaye and trees (Latta and Linhart 1997). Hart 1998). This, however, did not reduce avail- Smaller-diameter Pinus edulis produce male ability of N to the trees because, as also shown cones and larger-diameter trees produce female by other studies, more of the total N was trans- cones (Floyd 1983). Normally, Pinus is consid- formed and made more readily available for up- ered to be monoecious with both male and fe- take (Schoch and Binkley 1986, Knoepp and male stroboli on the same tree, but size segre- Swank 1995, Kaye and Hart 1998). Nutrient- gation of the sexes has led to the suggestion 2004] SEED PRODUCTION IN PINUS PONDEROSA 213

Fig. 1. Relationship between frequency of seed cone crop production and stem diameter of P. ponderosa. Data taken from citations listed; 5+ or 100+ refers to cone crops >5 or >100 cones, respectively. that Pinus edulis is functionally dioecious (Floyd Pinus ponderosa) and angiosperms is directly 1983). In P. ponderosa sex segregation does not associated with leaf mass (Greene and Johnson occur to this extent, and older trees that produce 1994). female cones also produce some male strobili. COMPETITION.—The largest P. ponderosa Younger trees do tend to produce mostly male cone crops are produced by isolated trees that strobili, with the greatest production occur- are free from competition. Over 10 years in ring from large-diameter young trees (Linhart central Arizona, isolated trees free to grow on and Mitton 1985). all sides not only produced cone crops more Dominant trees, those with crowns extend- frequently but also averaged 274 cones per ing above the general crown level in a stand, year versus 158 cones for open stands, 90 also tend to be more productive than trees cones for trees on the margin of stands, and 42 whose crowns are in the canopy (co-dominants) cones for interior trees (Larson and Schubert or lower (Fowells and Schubert 1956, Larson 1970). Some benefits of reductions in stand and Schubert 1970). Tree height alone had a density mentioned earlier can be attributed to much smaller effect on seed production than reduced competition for resources such as did stem diameter; small-diameter but domi- light. The only caveat is while low stand den- nant P. ponderosa trees in California did not sities are beneficial for cone production, iso- produce seed cones with the same frequency lated P. ponderosa trees self-pollinate at a or in the same number as trees of greater higher frequency than stand-grown trees, and diameter (Fowells and Schubert 1956). How- self-pollinated cones bear lower percentages ever, almost all counted cones were borne on of filled seed (Sorensen and Miles 1974). Pinus dominants (99%), with only 0.92% of total cones ponderosa seedlings from seeds of lower-den- produced on co-dominant trees. Intermediate sity stands are also more inbred and have or suppressed crown classes produced only lower heterozygosity and survival ability (Far- 0.05% of total cones (Fowells and Schubert ris and Mitton 1984). 1956). Closer inspection of these data shows Competition with the understory shrub layer that the effect of dominance on seed produc- for resources other than light also plays a role tion relates to greater leaf production: seed in P. ponderosa growth (Oliver 1984, McDon- production in both gymnosperms (including ald and Abbott 1997). In a northern California 214 WESTERN NORTH AMERICAN NATURALIST [Volume 64 plantation, P. ponderosa grew to 20 cm in seed and cone production (see review within diameter in 31 years without competition from Eriksson et al. 1998). In P. ponderosa only gird- shrubs, whereas with a heavy shrub cover ling has been applied, with varying success. diameters averaged 5.4 cm (McDonald and Wide (2.5 cm to 5 cm, with small bridge) and Abbott 1997). Similarly in Oregon, P. ponderosa narrow girdling (cut around entire circumfer- trees 13 cm to 51 cm in diameter (19 to 36 ence) were applied during bud initiation in years old) added an average of 7.6 cm in diam- May in western Montana, and both methods eter over 10 years when surrounded by under- increased cone production of the 1st crop to story vegetation, but they averaged 16.5 cm be formed post-treatment, although some without surrounding ground cover (Dahms and treated trees showed no response (Shearer Silen 1956, cited in Barrett 1979). Reduced and Schmidt 1970). On average, treated trees growth was associated with greater suscepti- produced about 20 cones versus 1 cone pro- bility to damage by insects (Oliver 1984, duced by the paired controls (Shearer and McDonald and Abbott 1997). Schmidt 1970). The treatment had no lasting GENETICS.—Genetic differences were sus- effect in subsequent years. pected a number of years ago when Linhart et al. (1979) observed that only a few Pinus trees FACTORS AFFECTING SEED produced the majority of cones. Pinus ponderosa AND CONE LOSS trees that produce abundant cone crops were Insects shown to be genetically distinct from those that did not (Linhart et al. 1979). Pinus pon- The native pines of North America host at derosa and P. sylvestris trees of the same least 1111 insect species, and Pinus ponderosa diameter produce either abundant cone crops hosts 367 of them, the highest for any pine (de or many male strobili, but not both in abun- Groot and Turgeon 1998). Nine species are dance (P. ponderosa: Linhart and Mitton 1985; associated with pollen cones and 35 species P. sylvestris: Savolainen et al. 1993). Trees that are associated with seed cones (de Groot and produce both produce fewer of each (Linhart Turgeon 1998). Other insects, not specialized and Mitton 1985, Savolainen et al. 1993). In on cones, may also affect production by weak- addition, individual trees that are genetically ening or killing trees outright (e.g., pine bee- predisposed for high female cone production tles, Dendroctonus spp.; Curtis and Lynch bear a cost in vegetative growth: they have 1957, Oliver and Ryker 1990, de Groot and smaller stem diameters than P. ponderosa trees Turgeon 1998). with low cone production of the same age While pollen cone insects may be relatively (Linhart et al. 1979). benign (Hedlin et al. 1980), seed cone insects Recently, plantations of genetic clones of a can destroy high proportions of cone crops in variety of Pinus species showed that seed cone some years (Larson and Schubert 1970, de Groot production has a strong genetic component (P. and Turgeon 1998). The coneworm, Dioryctria banksiana: Todhunter and Polk 1981; P. nigra: auranticella (Grote), for example, killed 80% of Matziris 1993; P. sylvestris: Burczyk and Cha- P. ponderosa cones in interior British Colum- lupka 1997). For P. sylvestris, variation in cone bia (Ross and Evans 1957) and northern Ari- production attributable to different clones ex- zona (Blake et al. 1989), and up to 57% in ceeded that for differences between years, but Idaho (Dale and Schenk 1978). At 10 sites in in both cases data were collected for only 2 northern Arizona, seed damage by all insect years (Savolainen et al. 1993, Burczyk and pests, including the coneworm, ranged from a Chalupka 1997). Byram et al. (1986), monitor- low of 1% to a high of 91% per cone (Schmid ing clonal plantations over many years, noted et al. 1984). Survival of 1st season conelets can that clones of P. taeda would change rank from be especially difficult: survival averaged only year to year in cone production. 19.5%, and 76.8% of those survived a 2nd year (Pasek and Dix 1988). SILVICULTURAL INDUCEMENTS Diseases FOR CONE PRODUCTION As with insects, diseases of Pinus ponderosa A variety of silvicultural treatments have are many and may reduce cone production been used in Pinus seed orchards to increase directly or indirectly by undermining tree 2004] SEED PRODUCTION IN PINUS PONDEROSA 215 health. Dwarf mistletoe, Arceuthobium spp., is ents and water, increased temperature, and P. ponderosa’s most widespread disease and reduced disease and insect pests. These in turn causes the most damage (Oliver and Ryker have been shown to promote growth in stem 1990). In the Southwest it has been particu- diameter, which is strongly linked to cone pro- larly devastating and is sometimes responsible duction. The only negative issue with respect for significant mortality (Schubert 1974). Among to thinning is the possibility of self-pollination trees that survive, the parasite impairs tree that leads to greater ovule abortion. The effect growth and reduces seed production and seed of fire is less clear, but limited evidence sug- viability (Schubert 1974, Hawksworth and gests that combining fire with thinning is the Shaw 1988, Harrington and Wingfield 1998). best way to improve health, growth, and cone Elytroderma deformans is P. ponderosa’s most production in P. ponderosa stands. serious foliage disease and may slow the growth Factors that influence cone production, but of mature trees, occasionally killing them. Bark that are not normally controlled in natural P. beetles may also be quick to attack affected ponderosa stands, include climate, which may trees, which, like trees parasitized by Arceutho- affect annual variation and crop failures; genet- bium, develop characteristic witches’ brooms ics, with only some trees being genetically (Curtis and Lynch 1957, Oliver and Ryker 1990, predisposed to produce large cone crops; and Harrington and Wingfield 1998). seed predators, which in some areas can be Other pathogens that significantly affect P. responsible for substantial seed loss. ponderosa include species of Armillaria and a What does this all mean for the White- diverse assemblage of parasites, cankers, root headed Woodpecker? Thinning treatments diseases, heart rots, foliage diseases, blights, being carried out in the northern part of the P. and rusts (Oliver and Ryker 1990), many of ponderosa range will certainly increase seed which have benefited from fire suppression as and cone production unless the trees that are well as from leftover stumps from thinning removed are the ones that are genetically pre- and harvest operations (Harrington and Wing- disposed for greater seed and cone production. field 1998). Diseases might be more prevalent However, given the benefits of outcrossing, a at higher stand densities; in P. sylvestris higher few younger trees that predominantly produce stand densities increased susceptibility to a pollen should also be left in the stand. canker (Niemela et al. 1992). Other Animals ACKNOWLEDGMENTS Squirrels (Tamiasciurus hudsonicus, Sciurus We thank Rene McKnight and Saskia Arne- aberti, and S. kaibabensis) destroy potential cone sen for editorial assistance. The research of crops by vigorously clipping conelet-bearing PGK is supported by operational funds from twigs and directly clipping cones and consum- Environment Canada. ing seeds (Keith 1965, Larson and Schubert 1970, Snyder 1993). In the southern part of LITERATURE CITED the P. ponderosa range, Sciurus aberti reduced cone production of target trees to 10% that of AGEE, J.K. 1998. Fire and pine ecosystems. Pages 193–218 nontarget trees (Snyder 1993). White-headed in D.M. Richardson, editor, Ecology and biogeography Woodpeckers and other woodpeckers are also of Pinus. Cambridge University Press, New York. ARNO, S.F. 1988. Fire ecology and its management impli- P. ponderosa seed predators (Garrett et al. cations in ponderosa pine forests. Pages 133–139 in 1996), but their effect on overall seed and D.M. Baumgartner and J.E. Lotan, editors, Ponderosa cone production has not been quantified. pine: the species and its management. Symposium proceedings, Spokane, WA, 29 September–1 Octo- ber 1987. Washington State University Publications, CONCLUSION Pullman. BARRETT, J.W. 1979. Silviculture of ponderosa pine in the Restoration activities in natural stands of P. Pacific Northwest: the state of our knowledge. U.S. ponderosa include thinning and fire, in combi- Department of Agriculture, Forest Service General nation and alone. Research on P. ponderosa Technical Report PNW-97, Portland, OR. BLAKE, E.A., M.R. WAGNER, AND T.W. K OERBER. 1989. Rel- and other Pinus species suggests that thinning ative effect of seed and cone insects on ponderosa increases cone production through greater pine in northern Arizona. Journal of Economic Ento- light availability, reduced competition for nutri- mology 82:1691–1694. 216 WESTERN NORTH AMERICAN NATURALIST [Volume 64

BOLDT, C.E., AND J.L. VAN DEUSEN. 1974. Silviculture of iana Lamb. trees at the limit of the species distribu- ponderosa pine in the Black Hills: the status of our tion in northern Quebec (Canada). Ecoscience 4: knowledge. U.S. Department of Agriculture, Forest 521–252. Service Report RM-124, Fort Collins, CO. DEWERS, R.S., AND D.M. MOEHRING. 1970. Effect of soil BROWN, P.M., AND C.H. SIEG. 1999. Historical variability water stress on initiation of ovulate primordia in in fire at the ponderosa pine–Northern Great Plains loblolly pine. Forest Science 16:219–221. prairie ecotone, southeastern Black Hills, South DIXON, R.D. 1995. Ecology of White-headed Woodpeckers Dakota. Ecoscience 6:539–547. in the central Oregon Cascades. Master’s thesis, Uni- BURCZYK, J., AND W. C HALUPKA. 1997. Flowering and cone versity of Idaho, Moscow. production variability and its effect on parental bal- EIS, S., D. CRAIGDALLIE, AND G.R. POWELL. 1983. Repro- ance in a Scots pine clonal seed orchard. 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Responses of exotic plant species to fires in Pinus ponderosa forests in northern Arizona. Department of Agriculture, Technical Bulletin 1150, Journal of Vegetation Science 12:261–268. Government Print Office, Washington, DC. ARRETT APHAEL AND IXON CURTIS, J.D., AND D.W. LYNCH. 1957. Silvics of ponderosa G , L.K., M.G. R , R.D. D . 1996. pine. U.S. Department of Agriculture, Forest Service White-headed Woodpecker (Picoides albolarvatus). Miscellaneous Publication 12, Intermountain Forest No. 252 in A. Poole and F. Gill, editors, The birds of and Range Experiment Station, Ogden, UT. North America. The Academy of Natural Sciences, DAHMS, W.G., AND J.W. BARRETT. 1975. Seed production Philadelphia, PA, and the American Ornithologists’ of central Oregon ponderosa and lodgepole pines. Union, Washington, DC. 23 pp. U.S. Department of Agriculture, Forest Service Report GREENE, D.F., AND E.A. JOHNSON. 1994. Estimating the PNW-191, Portland, OR. mean annual seed production of trees. Ecology 75: DALE, J.W., AND J.A. SCHENK. 1978. Cone production and 642–647. insect-caused seed losses of ponderosa pine in Idaho GREGORY, J.D., W.M. GUINNESS, AND C.B. DAVEY. 1982. and adjacent Washington and Montana. Bulletin 24, Fertilization and irrigation stimulate flowering and University of Idaho, Forest, Wildlife and Range cone production in a loblolly pine Pinus taeda seed Experiment Station, Moscow. orchard. Southern Journal of Applied Forestry 6: DAUBENMIRE, R.F. 1960. A seven-year study of cone pro- 44–48. duction as related to xylem layers and temperature HARRINGTON, T.C., AND M.J. WINGFIELD. 1998. Diseases in Pinus ponderosa. American Midland Naturalist and the ecology of indigenous and exotic pines. Pages 64:189–193. 381–404 in D.M. Richardson, editor, Ecology and DE GROOT, P., AND J.J. TURGEON. 1998. Insect-pine inter- biogeography of Pinus. Cambridge University Press, actions. Pages 354–380 in D.M. Richardson, editor, New York. Ecology and biogeography of Pinus. 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HAWKWORTH, F.G., AND C.G. SHAW III. 1988. Damage and culture, Forest Service Report RM-58, Rocky Moun- control of major diseases of ponderosa pine. Pages tain Forest and Range Experiment Station, Fort 99–108 in D.M. Baumgartner and J.E. Lotan, editors, Collins, CO. Ponderosa pine: the species and its management. LATHAM, P., AND J. TAPPEINER. 2002. Response of old-growth Symposium proceedings, Spokane, WA, 29 Septem- conifers to reduction in stand density in western ber–1 October 1987. Washington State University Oregon forests. Tree Physiology 22:137–146. Publications, Pullman. LATTA, R.G., AND Y.B. L INHART. 1997. Path analysis of nat- HEDLIN, A.F., H.O. YATES III, D.C. TOYAR, B.H. EBEL, T.W. ural selection on plant chemistry: the xylem resin of KOERBER, AND E.P. MERKEL. 1980. Cone and seed ponderosa pine. Oecologia 109:251–258. insects of North American conifers. Environment LINHART, Y.B., 1988. Ecological and evolutionary studies Canada, Canadian Forest Service, Ottawa, Canada; of ponderosa pine in the Rocky Mountains. Pages USDA Forest Service, Washington, DC; Universi- 77–89 in D.M. Baumgartner and J.E. Lotan, editors, dad Autonoma Chapingo, Chapingo, Mexico. Ponderosa pine: the species and its management. HEIDMANN, L.J. 1983. Seed production in southwestern Symposium proceedings, Spokane, WA, 29 Septem- ponderosa pine on a sedimentary soil. U.S. Depart- ber–1 October 1987. Washington State University ment of Agriculture, Forest Service Research Note Publications, Pullman. RM-434, Fort Collins, CO. LINHART, Y.B., AND J.B. MITTON. 1985. Relationships among ______. 1984. Fertilization increases cone production in a reproduction, growth rates, and protein heterozy- 55-year-old ponderosa pine stand in central Arizona. gosity in ponderosa pine. American Journal of Botany Forest Science 30:1079–1083. 72:181–184. HOPE, G.D., D.A. LLOYD, W.R. MITCHELL, W.R. 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Seed production of Pinus sylvestris after Symposium proceedings, Spokane, WA, 29 Septem- release cutting. Canadian Journal of Forest Research ber–1 October 1987. Washington State University 30:982–989. Publications, Pullman. KAYE, J.P., AND S.C. HART. 1998. Ecological restoration MAST, J.N., T.T. VEBLEN, AND M.E. HODGSON. 1997. Tree alters nitrogen transformations in a ponderosa pine– invasion within a pine/grassland ecotone: an approach bunchgrass ecosystem. Ecological Applications 8: with historic aerial photography and GIS modeling. 1052–1060. Forest Ecology and Management 93:181–194. KEITH,J.O. 1965. The Abert squirrel and its dependence on ponderosa pine. Ecology 46:150–163. MAST, J.N., P.Z. FULE, M.M. MOORE, W.W. C OVINGTON, AND A.E.M. WALTZ. 1999. Restoration of presettle- KNOEPP, J.D., AND W. T. S WANK. 1995. Comparison of available soil nitrogen assays in control and burned forest ment age structure of an Arizona ponderosa pine for- sites. 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U.S. Department of Agri- culture, Forest Service Report PSW-RP-231, Pacific culture, Forest Service Report RMRS-P-22, Rocky Southwest Forest and Range Experiment Station, Mountain Research Station, Ogden, UT. Albany, CA. KRAL, R. 2000. Pinus Linnaeus in Flora of North America MONLEON, V.J., K. CROMACK JR., AND J.D. LANDSBERG. 1997. north of Mexico. Volume 2: Pteridophytes and gym- Short- and long-term effects of prescribed under- nosperms [on-line]. Flora of North America Associa- burning on nitrogen availability in ponderosa pine tion. Available from http://hua.huh.harvard.edu/ stands in central Oregon. Canadian Journal of Forest FNA/ [cited 5 April 2002]. Research 27:369–378. LAROQUE, G.R. 2002. Examining different concepts for MOORE, M.M., W.W. COVINGTON, AND P. Z . F ULE. 1999. the development of a distance-dependent competi- Reference conditions and ecological restoration: a tion model for red pine diameter growth using long- southwestern ponderosa pine perspective. 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Forest Ecology and Management 14:13–22. Western North American Naturalist 64(2), ©2004, pp. 219–230

PLANT SPECIES DIVERSITY IN A GRASSLAND PLANT COMMUNITY: EVIDENCE FOR FORBS AS A CRITICAL MANAGEMENT CONSIDERATION

Monica L. Pokorny1, Roger L. Sheley1, Tony J. Svejcar2, and Richard E. Engel1

ABSTRACT.—This study quantified species and functional group diversity in a grassland plant community in southwestern Montana. Specific objectives were to measure the richness and density of functional groups within the grassland community, measure the biomass of each functional group, and calculate diversity indices for each functional group. We hypothesized that diversity would be greater than previous descriptions for the Festuca idahoensis/Agropyron spicatum habitat type because our multiple-season method would recognize seasonal and environmental variations in community composition. Of the species present, we hypothesized that forb functional groups account for the majority of richness and biomass of this grassland plant community. Species richness and density were measured during spring, summer, and fall of 2000, and biomass was collected during spring, summer, and fall of 2001. Species richness was measured by counting all species present on 4-m2 plots. We measured forb density per 4-m2 plot and determined grass density by counting tillers per species within a 0.2 × 0.5-m frame. Diversity indices were calculated for each functional group. Biomass by functional group was clipped from three 0.2 × 0.5-m frames per 4-m2 plot. Data support the hypothesis that multiple-season sampling recognizes greater species diversity at one location because both sites were more diverse plant communities than previously described for this habitat type. We documented 14 graminoids and 69 forbs from just 2 sites. Total diversity of a 4-m2 plot averaged 42 species, consisting of 5 grasses, 12 deep-rooted forbs, and 25 shallow- rooted forbs. Our data also support the hypothesis that forb functional groups represent the majority of the richness and biomass of the grassland community. Forbs account for 83% of species richness in this research. In addition, forbs represent a greater proportion of plant biomass than grasses on our sites. Functional group diversity and forb diversity should be a larger consideration in Festuca idahoensis/Agropyron spicatum grassland management decisions. We recommend that land managers recognize forb species and forb functional group diversity in grassland classifications. Maintaining diversity should be a primary objective of land managers because increased diversity has been found to increase community stability and productivity, and decrease the risk of invasion by undesired species. To encourage land managers to put more resources into monitoring diversity, a simple and repeatable sampling procedure applicable to both community and landscape scales needs to be developed.

Key words: grasslands, community composition, species richness, species diversity, functional group diversity, forbs.

Grasslands are the largest biome on earth, ence and abundance of characteristic plant comprising 24% of the world’s vegetation and species. More recent classifications of grass- about 125 M ha in the United States (Sims and land habitat types in the northwestern United Risser 2000). Near the start of the 20th century, States identify major grassland vegetation types, descriptions of grasslands focused on under- seral stages of each type, and response to graz- standing the value of species for livestock grazing management practices (Daubenmire 1970, ing, and few quantitative data were used to de- Mueggler and Stewart 1980). A common trend scribe plant community productivity or species of these classification systems is the vegetative composition and function in the system (Kear- type’s grass species nomenclature and empha- ney et al. 1914, Shantz and Piemeisel 1924). sis on managing grass for livestock production Grasslands soon began to be described by their (Stoddart and Smith 1943, Daubenmire 1970, particular climax plant community. Clements Mueggler and Stewart 1980, Willoughby et al. (1920) classified and described grasslands of 1998). the western United States as 1 of 5 grassland While forb species are listed as diverse com- formations. Since Clements, ecologists have ponents of grassland communities (Dauben- recognized and described finer level classifica- mire 1970, Sims et al. 1978, Mueggler and tions of the grasslands. Stoddart and Smith Stewart 1980, Jensen et al. 1988b, Hogg et al. (1943) described 18 range types, based on pres- 2001), they have not been a primary focus in

1Department of Land Resources and Environmental Sciences, Montana State University, Box 173120, Bozeman, MT 59717-3120. 2USDA-ARS, 67826-A, Highway 205, Burns, OR 97720.

219 220 WESTERN NORTH AMERICAN NATURALIST [Volume 64 classification and land management practices majority of richness and biomass of a grass- (Willoughby et al. 1998, Fuhlendorf and Engle land plant community. 2001), perhaps because forb species composition varies with environmental and biological METHODS factors (MacCracken et al.1983), or because Study Areas forbs have the greatest production variability within habitat types (Jensen et al. 1988a). This study was conducted on 2 sites within Conversely, year-to-year and site-to-site varia- the Festuca idahoensis/Agropyron spicatum tion of forbs may be a function of methodology habitat type (Mueggler and Stewart 1980). This limitations in these classifications. Vegetative habitat type lies at the cool-wet end of grass- classifications have historically documented land habitat types and can be found at elevations species composition only once during the grow- ranging from 1400 m to 2300 m. Predominant ing season (Stoddart and Smith 1943, Dauben- indigenous perennial grasses include Idaho mire 1970, Mueggler and Stewart 1980, Jensen fescue (Festuca idahoensis Elmer) and blue- et al. 1988b). Depending on annual variation bunch wheatgrass (Agropyron spicatum Pursh). in climate, early- or late-developing forbs may The proportion of forbs to graminoids varies have been missed in data collection for classi- with location and increases with precipitation fication descriptions. Measuring diversity once for this habitat type (Mueggler and Stewart at peak standing crop does not account for di- 1980). Some predominant indigenous forbs in- versity of spring or fall forbs. To estimate actual clude prairie sage (Artemisia ludoviciana L.), community diversity and diversity of forbs arrowleaf balsamroot (Balsamorhiza sagittata within a site, we believe periodic field sam- [Pursh] Nutt), and lupine (Lupinus spp.). pling must occur. Medium shrubs are absent from this habitat Ecologists and land managers have recog- type unless it has been severely disturbed. We nized the importance of diverse plant commu- chose the Festuca idahoensis/Agropyron spica- nities in maintaining healthy ecosystems (Dar- tum habitat type because it is widely distributed win 1859, Elton 1958, MacArthur and Wilson throughout the mountain grasslands in south- 1967, Goodman 1975, Pimm 1991). It is possi- western Montana and the western United States ble that forbs, or groups of forbs with similar and provides a model system for applied eco- characteristics, are important management logical research. groups and play a vital role in ecosystem func- Sites were located on the Flying D Ranch tions such as invasion resistance and nutrient approximately 70 km west (45°34′N, 111°34′W) cycling (Symstad 2000, Dukes 2001, Tilman et of Bozeman, Montana. Sites lie on an east– al. 2001, Pokorny 2002). Despite the potential northeast aspect of a 20° slope at 1624 m ele- role of forbs in plant community processes, only vation. Our specific sites were chosen because limited attention is given to their composition they were near enough to one another to be in grasslands during management practices. considered similar and appeared to represent The purpose of this research was to quan- the late seral stage within the Festuca idahoen- tify species and functional group diversity in a sis/Agropyron spicatum habitat type. Annual grassland plant community in southwestern average precipitation is 41 cm and annual Montana. Specific objectives included identi- average temperature is 6.5°C (Fig. 1). fying plant species richness, density, and bio- Prior to plot establishment, we tested soils mass within a Festuca idahoensis/Agropyron for presence of picloram (4-amino-3,5,6-trichlor- spicatum grassland habitat type using a multi- opicolinic acid, potassium salt) and nutrient ple-season sampling method, identifying vari- availability to minimize the risk that site char- ous functional groups based on their morphol- acteristics and plant community composition ogy, and comparing richness with previously were influenced by herbicide applications or described diversities of this habitat type. We differing resource availability. Picloram was not hypothesized that species richness would be detected at the 0.01 mg ⋅ kg–1 level. At depths greater than previous descriptions of habitat of 0–15 cm, mass water content, total N, NH4-H, type of a given location because of our multi- K, total soil C, and C:N did not differ between ple-season method of quantifying the commu- sites 1 and 2. Site 1 had higher NO3-H and S nity. Of the species present we hypothesized levels and lower P levels in the shallow soils that forb functional groups account for the than site 2. The only difference between sites 2004] FORBS AS A MANAGEMENT CONSIDERATION 221

Fig. 1. Average monthly precipitation and temperature gathered from the Red Bluff Experimental Station, approximately 4 km from the study sites.

in nutrient concentration at depths of 15–40 size has increased during the past 20 years. In cm was NO3-N, which was higher on site 1 general, site disturbances have been low and than site 2. the plant communities are in a late seral stage. Soil classifications indicated site 1 soils are Plot Design, Treatments, loamy-skeletal, mixed, frigid, active Typic Haplo- and Measurements cryolls (Haplo Cryic Mollisol), and site 2 soils are coarse-loamy, mixed, frigid, active Typic This study was part of a larger research pro- Haplocryolls (Haplo Cryic Mollisol). Soil project aiming to achieve multiple objectives. file descriptions for each site showed small Describing the treatments for the larger ex- variations in the structure, material, and pH of periment is essential for understanding why the A and Bw horizons. Main differences in soil sample sizes differ in the data collected for profiles were depth of the A horizon (22 cm this portion of the research. Species of grass, verses 12 cm, site 1 and 2, respectively) and forbs, and spikemoss were combined into presence of a Bw horizon at site 2. The Bw functional groups based on morphological simi- horizon structure, which contributed substan- larities. Forbs were further divided into 2 func- tially to total profile depth, had larger, blockier tional groups based on average rooting depth soil aggregates than the A or Bk horizons of of each species, determined by careful excava- each site. tion of each species to determine root structure The area has been grazed for decades, and and rooting depth. The distinction between a in some years of its recent history (50–60 years) shallow and a deep depth was based on a nat- it has been heavily grazed by either cattle (Bos ural break within the roots sampled, which taurus) or bison (Bison bison). Bison grazing occurred at about 15 cm. In cases where the during the past 10 years has been sporadic. average root depth was close to 15 cm, species Windblown slopes are prime winter habitat with primarily fibrous roots were considered for wildlife. In the study area winter use by elk shallow-rooted, while taproots were grouped (Cervus elaphus) has steadily increased as herd with deep-rooted forbs. 222 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Treatments were arranged in a randomized, mine species distribution between sites. Fre- complete-block design with 4 replications on quency of occurrence was calculated as num- each of 2 sites. Treatments were applied by ber of plots a species occurred in divided by removing a functional group or groups in com- total number of plots. Species richness per bination from the 2 × 2-m plots. This study seasonal sample period was calculated as a consisted of 7 removal treatments: (1) shallow- percentage of total species richness. Richness, rooted forbs, (2) deep-rooted forbs, (3) all forbs, biomass, and density were summarized for (4) grasses, (5) all plant material, (6) nothing shallow-rooted forb, deep-rooted forb, and (control), and (7) moss, lichens, and spikemoss grass functional groups individually and for (collectively referred to as spikemoss through- the plot as a whole (hereafter referred to as out the paper). While removing functional “overall plot”). Biomass was averaged over the groups in spring, summer, and fall of 2000, we 3 seasons for this comparison. For the spikemoss recorded species richness and density for all functional group, mean percent cover, rich- species removed as well as for all species on ness, and biomass were summarized. Richness the control plots (nothing removed). Spring was always summarized per plot (4 m2) while sampling occurred when the majority of spring density, biomass, and percent cover were ephemeral forbs were in bloom, summer sam- averaged per m2. Both the Simpson and Shan- pling coincided with peak standing crop, and non-Weaver diversity indices were calculated fall sampling occurred after 95% of the vegeta- for each functional group. The Simpson diver- tion was senescent. To measure species richness sity index is defined as D = 1/(sum[Pi2]) where we counted all species present on the plot, Pi is the proportion of the ith species (Begon and for forb density we counted the number of et al. 1990). The Shannon-Weaver index is plants per species in the plot. Grass density defined as H = –sum(Pi[lnPi]) (Begon et al. was determined by counting the number of 1990). To further describe the habitat type and tillers per species within a 0.2 × 0.5-m frame. variation in plant species richness, density, and A single frame was placed randomly in each plot. biomass within this habitat type, data compar- For the spikemoss functional group, percent isons between the 2 sites were conducted using foliar cover was estimated within a 0.2 × 0.5-m the Student’s t test in SPSS software (SPSS frame for each species representing ≥1% of the plot area. Forbs and Selaginella species version 10.0 1999). We used ANOVA to inves- were identified using Dorn (1984) while grasses tigate the degree of seasonal variability of follow the nomenclature in Cronquist et al. functional group biomass. In this case, functional group, season, and block were all main (1977). We used Flowers (1973) and McCune × (1995) to identify mosses and lichens. effects and functional group season was the Aboveground biomass of shallow-rooted interaction term. Tukey’s multiple compar- forbs, deep-rooted forbs, and grasses was col- isons were calculated in SAS when P-values ≤ lected during spring, summer, and fall of 2001 were 0.05 (SAS 1990). from all plots where their biomass was not removed as a treatment. Thus, there are different RESULTS sample sizes for each group. Plots were divided Frequency, Density, Biomass, into 3 subplots that were randomly assigned to and Cover each of the 3 sample periods to prevent sampling the same area twice. Plants were clipped Twenty-four plant families were represented to ground level within three 0.2 × 0.5-m frames in 4 functional groups on the study sites. Plant randomly placed in each subplot. Plant above- families most often encountered were Aster- ground biomass was separated by functional aceae (16 taxa), Fabaceae (7 taxa), and Poaceae group as it was clipped. As part of the treat- (14 taxa). In total, 84 vascular plants, 2 nonvas- ments, we removed spikemoss from 2 plots in cular plants, and 4 lichens were identified in each block. All plant tissues were oven-dried this grassland system (Table 1). Of those species, (40°C, 160 hours) to a constant weight. We then 47 were shallow-rooted forbs, 22 were deep- weighed them and recorded their biomass. rooted forbs, 14 were grasses, 4 were lichens, 1 was a spikemoss, and 2 were mosses. Shal- Data Analysis low-rooted forbs (0–15 cm roots) consisted of Species frequency of occurrence in the 4- annual, short-lived perennials, and perennial m2 plots was calculated for each site to deter- species with bulbs, rhizomes, fibrous roots and/ 2004] FORBS AS A MANAGEMENT CONSIDERATION 223 or shallow taproots. Deep-rooted forbs (15–40 site 1. Site 2 had a greater biomass of grasses cm roots) were primarily perennial taprooted than site 1. Site 2 also had twice as much bio- plants with varying lateral root lengths and mass of the spikemoss functional group as site depths. Idaho fescue and bluebunch wheatgrass 1 did (Table 3). Selaginella densa formed an were the most commonly occurring grasses. almost continuous layer on the soil at site 2 Arrowleaf balsamroot, lupine, prairie milkvetch (66% cover), surrounding the base of bunch- (Astragalus adsurgens Pallas), and blazing star grasses, and had vascular vegetation growing (Liatris punctata Hook) are deep-rooted forbs through and within its foliage. In comparison, that occurred on nearly every plot. Shallow- site 1 had more bare ground. rooted forbs were dominated by both spring We were interested in natural variability ephemeral forbs, including death camas (Ziga- and distribution of functional group biomass denus venenosus Wats.) and yellowbell (Fritil- over the 3 seasons in diverse grassland com- laria pudica Pursh), and midsummer bloomers, munities and found that biomass at site 1 var- including penstemon (Penstemon eriantherus ied among functional groups and with season Pursh) and blanketflower (Gaillardia aristata (Table 4). Deep-rooted forbs had a greater bio- Pursh). A single species of spikemoss, resurrec- mass (48 g ⋅ m–2) than shallow-rooted forbs (24 tion plant (Selaginella densa), accounted for g ⋅ m–2) and grass (27 g ⋅ m–2) at site 1 (Table 5). 99% of the cover and biomass of the spikemoss The highest functional group biomass occurred group, while mosses and lichens were rarer in in the fall while biomass of functional groups occurrence and distribution. was lowest during spring (Table 5). On site 2 Twenty-four species had ≥75% frequency of the amount of biomass depended on func- occurrence on both sites (Table 1). While most tional group, season, and a functional group × species were evenly distributed over both sites, season interaction (Table 4). All 3 functional there were some exceptions. Iris missouriensis groups yielded similar biomass in spring (Fig. had a frequency of occurrence of 90% at site 1 2). In summer, grasses (30 g ⋅ m–2) and deep- and was absent from site 2. Eight species had rooted forbs (36 g ⋅ m–2) had a greater biomass at least 3 times the frequency of occurrence on than shallow-rooted forbs (16 g ⋅ m–2). Deep- site 1 than site 2. Sixteen species were present rooted forbs produced more biomass (65 g ⋅ on site 1 in low frequencies while absent from m–2) than either of the other 2 functional site 2. Carex filifolia and Cladonia pyxidata groups in the fall. Fall biomass for grass and occurred on site 2 with at least 3 times the fre- shallow-rooted forbs was 36 g ⋅ m–2 and 23 g ⋅ quency of site 1. Five species were present on m–2, respectively. Deep-rooted forbs was the site 2 in low frequencies while absent from only group whose biomass varied seasonally site 1. The percent of plant species that could with an increase in biomass from spring (20 g ⋅ be identified varied by season. Of the total num- m–2) to summer (60 g ⋅ m–2). Biomass of spike- ber of species present on the sites, 52%, 76%, moss on plots was not used for the analysis of and 44% were able to be identified in spring, variance because it does not represent the summer, and fall samplings, respectively. group’s seasonal biomass (Mueggler and Stew- Mean overall plot species density was 22.9 art 1980, van Tooren et al. 1990). plants ⋅ m–2 and 45.3 plants ⋅ m–2 on sites 1 and Species Diversity 2, respectively (Table 2). Grass tillers were about twice as dense on site 2 (434.6 tillers ⋅ Overall plot mean species richness within a m–2) as on site 1 (187.6 tillers ⋅ m–2). This 4-m2 plot was 43.6 and 39.4 for sites 1 and 2, probably accounted for greater overall density respectively (Table 2). Site 1 had greater species on site 2. While shallow-rooted forbs generally richness of shallow-rooted forbs (26.9), grasses had a lower frequency of occurrence on site 2 (5.5), and spikemoss (2.6) than what was re- than on site 1, their density was about one- corded for site 2. Site 2 (12.3) had a greater third greater on site 2 (3.3 plants ⋅ m–2) than richness of deep-rooted forbs than site 1 (10.8). on site 1 (2.6 plant ⋅ m–2). Two diversity indices were calculated for Site 1 had a greater overall plot biomass each site because the indices have different (89.1 g ⋅ m–2) than site 2 (74.8 g ⋅ m–2; Table 2). meanings of equitability (Table 2). For both Shallow-rooted forbs accounted for 23.5 g ⋅ indices, equitability increases with an increase m–2 (26%) and deep-rooted forbs for 47.5 g ⋅ in the index. According to the Simpson index, m–2 (53%) of the plant community biomass at the equitability of shallow- and deep-rooted 224 WESTERN NORTH AMERICAN NATURALIST [Volume 64

TABLE 1. Species functional group assignment, average root depth, and frequency in 4-m2 plots on site 1 and site 2, respectively. The shallow-rooted forb, deep-rooted forb, grass, and the spikemoss functional groups are represented by S, D, G, and M, respectively. Species Common nameFunctional Average rootFrequency of group depth (cm) occurrence Achillea millefolium L. Yarrow S 10 0.28 / 0.21 Allium cernuum Roth. Nodding onion S 5 0.97 / 1.00 Alyssum alyssoides L. Alyssum S 3 0.06 / 0.00 Antennaria parvifolia Nutt. Small leaf pussytoes S 11 0.65 / 0.66 Arabis nuttallii Robinson Nuttall rockcress S 5 1.00 / 0.34 Arenaria congesta Nutt. Ballhead sandwort S 4 0.97 / 1.00 Arnica sororia Greene Arnica S 10 0.28 / 0.25 Artemisia campestris L. Common sagewort S 12 0.09 / 0.00 Artemisia dracunculus L. Green sagewort S 3 0.06 / 0.00 Artemisia frigida Willd. Fringed sage S 14 1.00 / 0.40 Artemisia ludoviciana L. Man sage S 3 0.31 / 0.28 Astragalus agrestis Dougl. ex Hook Field milkvetch S 10 0.00 / 0.09 Besseya wyomingensis (A. Nels.) Rydb. Kittentail S 12 0.97 / 0.91 Castilleja pallescens (Gray) Greene Pale Indian paintbrush S 7 1.00 / 1.00 Cerastium arvense L. Chickweed S 8 1.00 / 0.94 Chenopodium leptophyllum Nutt. Lambsquarter S 7 0.09 / 0.03 Comandra umbellata (L.) Nutt. Bastard toadflax S 4 1.00 / 0.90 Dodecatheon conjugens Greene Shooting star S 6 0.97 / 0.90 Douglasia montana Gray Mountain douglasia S 9 1.00 / 0.88 Erigeron caespitosus Nutt. Tufted fleabane S 13 0.90 / 0.90 Erysimum asperum Nutt DC. Plains wallflower S 5 0.16 / 0.00 Erysimum inconspicuum (Wats.) MacM. Wallflower S 6 0.09 / 0.00 Fritillaria pudica Pursh Yellow bell S 6 0.97 / 1.00 Gaillardia aristata Pursh Blanketflower S 6 1.00 / 1.00 Galium boreale L. Bedstraw S 3 0.22 / 0.00 Gaura coccinea Nutt. ex Pursh Gaura S 3 0.09 / 0.03 Gutierrezia sarothrae Britt. & Rusby Broom snakeweed S 6 0.63 / 0.72 Haplopappus acaulis Nutt. Goldenweed S 7 0.00 / 0.03 Heterotheca villosa Pursh Golden aster S 6 0.59 / 0.75 Iris missouriensis Nutt. Bearded iris S 11 0.90 / 0.00 Linum lewisii Pursh Flax S 8 0.97 / 1.00 Lesquerella alpina (Nutt.) Wats. Alkaline bladderpod S 7 0.19 / 0.00 Lomatium cous Coult. & Rose Mountain lomatium S 12 0.94 / 0.75 Musineon divaricatum Pursh Musineon S 10 0.13 / 0.06 Nothocalais cuspidata (Pursh) Greene Cuspidate nothocalais S 14 1.00 / 1.00 Nothocalais troximoides (Gray) Greene Nothocalais S 8 0.56 / 0.97 Penstemon eriantherus Pursh Penstemon S 4 1.00 / 1.00 Sedum borschii Clausen Stone crop S 3 0.03 / 0.00 Senecio canus Hook Woolly groundsel S 8 0.94 / 0.66 Sisyrinchium montanum Greene Blue eye grass S 5 0.97 / 0.72 Vicia americana Mahl. ex Willd. American vetch S 10 0.97 / 0.88 Viola nuttallii Pursh Yellow violet S 4 0.72 / 0.84 Viola nuttallii var. vallicola A. Nels. Yellow violet S 4 0.03 / 0.03 Zigadenus venenosus Wats. Death camas S 6 1.00 / 1.00 Unknown forb 1 Unknown forb S 5 0.03 / 0.00

forbs did not differ statistically between sites. the overall plot differed between sites. At site Site 1 (D = 3.11) had a greater Simpson index 1, grasses, shallow-rooted forbs, and overall for grass than site 2 (D = 1.66); therefore, grass species per plot were more evenly distributed species were more evenly distributed at site 1 than at site 2. Evenness values ranged from H than at site 2. Overall plot species diversity for = 1.27 for grass, to H = 2.81 for shallow- site 1 (D = 4.28) was >2 times greater than rooted forbs, and to H = 1.86 for the overall diversity at site 2 (D = 1.78). The Shannon- plot total. As with the Simpson index, site 2 (H Weaver diversity index indicated that equi- = 1.99) had greater evenness of deep-rooted tability of species within functional groups and forbs than site 1 (H = 1.85). 2004] FORBS AS A MANAGEMENT CONSIDERATION 225

TABLE 1. Continued. Species Common nameFunctional Average rootFrequency of group depth (cm) occurrence Unknown forb 2 Unknown forb S 6 0.03 / 0.00 Unknown forb 3 Unknown forb S 3 0.03 / 0.00 Anemone multifida Poir. Ball anemone D 19 0.06 / 0.00 Anemone patens L. Pasque flower D 26 0.50 / 0.97 Astragalus adsurgens Pallas Prairie milkvetch D 30 1.00 / 0.94 Astragalus crassicarpus Nutt. Plum milkvetch D 20 0.41 / 0.84 Balsamorhiza sagittata (Pursh) Nutt Arrowleaf balsamroot D 35 1.00 / 0.78 Clematis hirsutissima Pursh Vase flower D 24 0.25 / 0.03 Crepis acuminata Nutt. Hawksbeard D 16 0.19 / 0.06 Crepis occidentalis Nutt. Hawksbeard D 20 0.59 / 0.66 Frasera speciosa Dougl. ex Griseb Green gentian D 30 0.56 / 0.84 Geum triflorum Pursh Prairie smoke D 19 0.13 / 0.06 Geranium viscosissimum Fisch Sticky geranium D 20 0.00 / 0.03 Heuchera parviflora Nutt. Littleleaf allumroot D 20 0.44 / 0.00 Ipomopsis spicata Nutt. (Grant) Spike ipomopsis D 27 0.56 / 0.88 Liatris punctata Hook Blazing star D 19 1.00 / 0.97 Lithospermum ruderale Dougl. ex. Lehm Puccoon D 35 0.63 / 0.84 Lupinus sericeus Pursh Lupine D 35 0.97 / 0.97 Mertensia oblongifolia (Nutt.) G. Don Bluebell D 20 0.09 / 0.00 Phlox albomarginata Jones Phlox D 16 0.41 / 0.66 Oxytropis lagopus Nutt. Haresfoot loco D 20 0.06 / 0.13 Oxytropis sericea Nutt. White pointloco D 20 0.50 / 0.81 Taraxacum officinale Weber Common dandelion D 18 0.97 / 1.00 Tragopogon dubius Scop. Goatsbeard D 18 0.41 / 0.69 Agropyron spicatum Pursh Bluebunch wheatgrass G 15 1.00 / 0.96 Aristida longiseta L. Red three-awn G 15 0.25 / 0.04 Bouteloua gracilis H.B.K. Lag Blue grama G 5 0.79 / 0.38 Carex filifolia Nutt. Threadleaf sedge G 10 0.08 / 0.29 Carex rossii Boott Ross sedge G 11 0.00 / 0.17 Festuca idahoensis Elmer Idaho fescue G 10 1.00 / 1.00 Festuca ovina L. Sheep fescue G 10 0.00 / 0.08 Helictotrichon hookeri (Scribn.) Henr. Spike oat G 11 0.75 / 0.25 Koeleria nitida Nutt. Junegrass G 9 0.38 / 0.21 Poa cusickii Vasey Cusick bluegrass G 7 0.50 / 0.33 Poa pratensis L. Kentucky bluegrass G 7 0.21 / 0.00 Poa secunda Presl. Sandbergs bluegrass G 10 0.46 / 0.08 Stipa comata Trin. & Rupr. Needle and thread G 12 0.08 / 0.17 Agropyron spp. Wheatgrass G 8 0.04 / 0.04 Selaginella densa Rydb. Compact spikemoss M n/a 0.84 / 1.00 Xanthoparmelia wyomingica Rockfrog M n/a 0.36 / 0.02 Peltigera rufescens Felt pelts M n/a 0.20 / 0.07 Cladonia chlorophaea Peppered pixie-cup M n/a 0.75 / 0.61 Cladonia pyxidata Pixie-cup M n/a 0.09 / 0.27 Tortula ruralis Hairy screw moss M n/a 0.07 / 0.09 Bryum caespiticum Moss M n/a 0.25 / 0.04

DISCUSSION mented a total of 27 species of graminoids and 69 forb species from 45 sites. In comparison, Species diversity of both sites was high we documented 14 graminoids and 69 forbs (Daubenmire 1970, Mueggler and Stewart from just 2 sites. It is hard to quantify the rich- 1980). Sampling over time allowed us to docu- ness per site from Mueggler and Stewart; how- ment greater species richness than previously ever, based on the average constancy of each suggested for this habitat type (Daubenmire life-form, 25% of the 27 grass species (7) and 1970, Mueggler and Stewart 1980). In their 24% of the 69 forb species (17) occurred on classification description of the Festuca ida- each of their 45 sites. Similarly, Daubenmire hoensis/Agropyron spicatum habitat type in (1970) documented an average of 3 grasses, 9 Montana, Mueggler and Stewart (1980) docu- annual forbs, and 8 perennial forbs per 4 m2 in 226 WESTERN NORTH AMERICAN NATURALIST [Volume 64

TABLE 2. Means and P-values generated from independent t tests for species richness, density, Simpson diversity index, and Shannon-Weaver index at both sites. Functional group Site n Density Biomass Richness Simpson Shannon-Weaver (m2) (g ⋅ m–2) (4 m2) diversity index diversity index Grass 1 24 187.6 27.3 5.5 3.11 1.27 224434.6 29.7 4.0 1.66 0.65 df 46 40 46 46 46 P-value <0.0001 0.303 <0.0001 <0.0001 <0.0001 Deep-rooted forbs 1 32 1.9 47.5 10.8 4.95 1.85 2321.9 40.3 12.3 5.35 1.99 df 62 32 62 62 62 P-value 0.813 0.266 0.001 0.236 0.008 Shallow-rooted forbs 1 32 2.6 23.5 26.9 12.56 2.81 2323.3 17.2 23.2 11.69 2.59 df 62 32 62 62 62 P-value <0.0001 0.017 <0.0001 0.536 <0.0001 Overall plot 1 16 22.9 89.1 43.6 4.28 1.86 21645.3 74.8 39.4 1.78 0.99 df 30 30 30 30 30 P-value <0.0001 0.053 0.017 <0.0001 <0.0001

TABLE 3. Mean richness, biomass, and percent cover of moss, lichen, and spikemoss on both sites. Sample size per site was 56 for richness and percent cover and 8 for biomass. Functional group Site Richness (4 m2) Biomass (g ⋅ m–2)Percent cover (m2) Moss / Lichen / Spikemoss 1 2.6 168 46 2 2.1 366 66 df 110 14 110 P-value 0.009 0.002 <0.0001

the Agropyron spicatum/Festuca idahoensis hab- on our sites. This was consistent with Mueggler itat type of Washington. Our grassland descrip- and Stewart (1980), who found forbs account tion documented 39–44 species per 4-m2 plot for approximately 1.5 times more biomass than which consisted of 4–6 grasses, 11–12 deep- grasses. Biomass of forb functional groups rooted forbs, and 23–27 shallow-rooted forbs. would be equal to, or greater than, biomass of We documented an average canopy cover of grasses in the plant community throughout moss/spikemoss/lichen of 46%, 66% of which the growing season. Robust, deep-rooted forbs comprised 2–3 species. In comparison, Mueg- dominated the biomass on site 1 and were a gler and Stewart (1980) estimated bryophytes large contributor to overall community bio- to be 5%–24% ground cover but did not iden- mass in all 3 seasons on site 2. Biomass of the tify species. shallow-rooted forbs in this grassland commu- Our data support the hypothesis that forb nity appears to have been underestimated by functional groups represent the majority of the ecologists and managers in grassland commu- richness and biomass of this grassland com- nity descriptions and management practices. munity. Forbs accounted for 83% of vascular This group is typically characterized as small, species richness in our research. Similarly, spring ephemeral plants. Our data suggest Mueggler and Stewart (1980) and Daubenmire that although small, these species are ubiqui- (1970) found 72% and 93% of total species tous enough to comprise roughly one-fourth of recorded for this habitat type to be forbs. Sims the total biomass on both sites. Furthermore, et al. (1978) found grasslands to be composed shallow-rooted forb biomass was well repre- of 3 to 4 times the number of forb species as sented throughout the entire growing season, grasses. In addition, forbs represented a greater and these plants were not merely spring proportion of plant biomass than the grasses ephemeral forbs. 2004] FORBS AS A MANAGEMENT CONSIDERATION 227

TABLE 4. ANOVA results for functional group, season, and block effects on functional group biomass at sites 1 and 2.

______Site 1 ______Site 2 Source df Mean square P-value Mean square P-value Functional group 2 1467.1 <0.0001 1156.5 <0.0001 Season 2 1312.2 <0.0001 1226.2 <0.0001 Block 3 20.7 0.834 30.4 0.408 F group* Season 4 54.9 0.548 284.2 <0.0001 Error 300 71.8 n/a 31.4 n/a

TABLE 5. Mean separations for biomass main effects at site 1. Letters represent significant differences at the α≤0.05 level. Functional group biomass was averaged over seasons. Seasonal biomass is the average of the grass, shallow-, and deep-rooted forb functional groups.

______95% confidence interval Dependent variable Biomass (g ⋅ m–2) Standard error Lower bound Upper bound Functional group Grass 27.34a 1.80 23.78 30.89 Shallow-rooted forbs 23.55a 1.89 19.80 27.30 Deep-rooted forbs 47.52b 4.60 38.39 56.64 Season Spring 19.18a 1.55 16.10 22.26 Summer 36.67b 3.36 29.00 42.34 Fall 42.29b 3.45 35.45 49.14

The term “grasslands” is misleading to the sity is equally or more important to resisting actual composition of this biome because grasses invasion than species diversity alone (Symstad typically comprise ≤20% of total plant species 2000, Dukes 2001, Tilman et al. 2001, Pokorny richness (Sims and Risser 2000). Although 3 to 2002) because of resource preemption (Tilman 4 grass species may comprise a large portion 1997, Davis and Pelsor 2001, Dukes 2001). of biomass in grasslands, forbs contribute more Therefore, species number alone may not be to community diversity (Sims et al. 1978, Sims as important as species present with different and Risser 2000). Because maintaining function- ecosystem roles (Walker 1992, Sala et al. 1996, al group diversity is suggested for maintaining Sheley et al. 1996, Diaz and Cabido 2001), optimum plant community functioning (Levine which suggests that ecosystem functioning and D’Antonio 1999, Dukes 2001), we suggest may be sensitive to functional diversity. more emphasis be placed on managing grass- Our dissection of the grassland plant com- lands for forb functional group diversity. munity into functional groups was a means to Our results indicate that greater species investigate diversity of forbs in the community. richness coincides with greater overall bio- Dissection into functional groups was also a mass or productivity. This finding is consistent means to investigate the role of groups in plant with other research suggesting increased diver- community dynamics and management. We sity is positively correlated with increased com- classified forbs into functional groups based on munity productivity and stabilization (Naeem morphology because it is thought to reflect the et al. 1994, Tilman et al. 1997, Tilman et al. life history strategies of species (Lauenroth et 2001, Anderson and Inouye 2001) due to the al. 1978, Gitay and Noble 1997) and can be more complete use of resources (Tilman 1997, useful in predicting ecosystem dynamics, such as Carpinelli 2001). Lower availabilities of re- response to disturbance or changes in nutrient sources have been suggested to decrease inva- composition (Connell and Slatyer 1977, Pickett sibility of the community by undesired species et al. 1987, Shaver et al. 1997). Maintaining (McNaughton 1993, Robinson et al. 1995). functional groups is essential for long-term per- Recent research implies that functional diver- sistence of biota within a plant community 228 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Fig. 2. Seasonal functional group biomass collected during the 2001 growing season at site 2. Letters represent biomass differences (P < 0.05) among functional groups comparable within a given season. Error bars are 1 standard error of the mean.

(Walker 1992) and may be more feasible than field sampling during the growing season pro- individual species-based management. Classi- vides (1) a better understanding of plant com- fication into functional groups allows the defin- munity composition and (2) a target plant com- ing mechanism of the group to be monitored munity for management. As a minimum, we more directly and provides a link between life recommend quantifying species diversity twice history strategies at the plant level and pro- during the growing season. By sampling once cesses at the ecosystem level (Chapin 1993, in the spring when spring forbs are beginning Westoby and Leishman 1997). Separating plants to bloom, and once in the summer at peak into functional groups is essential for understanding crop, land managers should be able standing the direction of change within the to capture approximately 95% of the diversity plant community because groups can be a in the Festuca idahoensis/Agropyron spicatum stronger determinate of ecosystem processes habitat type. In comparison, a maximum of 76% than individual species diversity (Tilman et al. of community diversity was recorded with a 1997). Furthermore, maintaining plant func- single summer field sampling. tional group diversity may be more important We also recommend land managers estab- to ecological integrity than simply maintaining lish and maintain forb species and forb func- plant species diversity (Hooper and Vitousek tional group diversity in land management 1997, Tilman et al. 1997, Mack and D’Antonio decisions. Intermediate levels of disturbance 1998), because altering functional group diver- have been proposed to maintain the highest sity could cause large effects on ecosystem levels of diversity (Connell 1978). In land man- processes. agement intermediate levels of disturbance can be obtained by regulating grazing timing MANAGEMENT AND RESEARCH and intensity and through periodic prescribed IMPLICATIONS burning. Diversity can also be maintained through careful planning of herbicide applica- We recommend that land managers recog- tions. When using herbicides, we recommend nize forb species and forb functional group carefully calibrating herbicide rates to minimize diversity in grassland classifications. Periodic effects on off-target plants, applying herbicides 2004] FORBS AS A MANAGEMENT CONSIDERATION 229 when the most indigenous vegetation is senes- Foundation and the Tribal Colleges Research cent, spot-spraying areas (versus areawide Grant Program, USDA. Special thanks to the broadcast spraying) to maintain diversity where Flying D Ranch and Turner Enterprises, Inc., individual weedy plants exist, and reseeding for assisting with this research. competitive grasses and forbs after herbicide application. LITERATURE CITED Maintaining functional group diversity ANDERSON, J.E., AND R.S. INOUYE. 2001. Landscape-scale should be a primary objective of land managers changes in plant species abundance and biodiversity because increased functional group diversity of a sagebrush steppe over 45 years. Ecological Mono- correlates with increased stability and produc- graphs 71:531–556. tivity through niche differentiation and resource BEGON, M., J.L. HARPER, AND C.R. TOWNSEND. 1990. Ecol- ogy: individuals, populations and communities. 2nd acquisition. Increasing functional diversity also edition. Blackwell Scientific Publications, Boston. decreases the risk of invasion by undesired CARPINELLI, M.F. 2001. Designing weed-resistant plant species. Indigenous forb functional groups use communities by maximizing niche occupation and resources similarly to nonindigenous forb in- resource capture. Doctoral dissertation, Montana vaders and are a critical component in com- State University, Bozeman. CHAPIN, F.S.I. 1993. Functional role of growth forms in munity invasion resistance. Besides their con- ecosystem and global processes. Pages 287–312 in tribution to ecosystem function, functional J.R. Ehleringer and C.B. Field, editors, Scaling physi- groups are a simpler unit for managing diver- ological processes: leaf to globe. Academic Press, San Diego. sity than a species-based approach because CLEMENTS, F.E. 1920. Plant indicators, the relation of plant the goal is to establish and maintain multiple communities to process and practice. Carnegie Insti- species that respond similarly to change and tute of Washington Publication, Washington, DC. collectively resist invasion. CONNELL, J.H. 1978. Diversity in tropical rain forests and coral reefs. Science 199:1302–1310. Several research needs were identified in CONNELL, J.H., AND R.O. SLATYER. 1977. Mechanisms of the study. First, a simple, repeatable sampling succession in natural communities and their role in procedure that can be applied at community community stability and organization. American and landscape scales needs to be developed. A Naturalist 111(982):1119–1144. CRONQUIST, A., A.H. HOLMGREN, N.H. HOLMGREN, J.L. simple method could encourage land man- REVEAL, AND P.K. HOLMGREN. 1977. Intermountain agers and management agencies to put more flora: vascular plants of the Intermountain West, USA. resources into monitoring if a simple effort Columbia University Press, New York. could produce a greater return in data col- DARWIN, C. 1859. The origin of species. Reprinted by Penguin Books, London. lected and handled. Next, areas on the land- DAUBENMIRE, R. 1970. Steppe vegetation of Washington. scape most susceptible to invasion need to be Washington State University Cooperative Extension, identified as focal points for maintaining diver- Pullman. sity and invasion resistance. Research also must DAVIS, M.A., AND M. PELSOR. 2001. Experimental support for a resource-based mechanistic model of invasibil- address the level of diversity, or functional group ity. Ecology Letters 4:421–428. diversity, that is needed to maintain a diverse, DIAZ, S., AND M. CABIDO. 2001. Vive la difference: plant invasion-resistant, and properly functioning functional diversity matters to ecosystem processes. ecosystem. Finally, techniques for native plant Trends in Ecology and Evolution 16:646–655. DORN, R.D. 1984. Vascular plants of Montana. Mountain propagation, establishment, and revegetation West Publishers, Cheyenne, WY. need to be improved and further developed. DUKES, J. 2001. Biodiversity and invasibility in grassland microcosms. Oecologia 126:563–568. ELTON, C.S. 1958. The ecology of invasions by animals and CKNOWLEDGMENTS A plants. University of Chicago Press, Chicago. FLOWERS, S. 1973. Mosses: Utah and the West. Brigham We greatly appreciate technical assistance Young University Press, Provo, UT. from Catherine Zabinski, and field and lab FUHLENDORF, S.D., AND D.M. ENGLE. 2001. Restoring assistance from Tracy Cashman, Shelly Grossi, heterogeneity of rangelands: ecosystem management based on evolutionary grazing patterns. BioScience Julian Calabrese, Steve Laufenberg, Kristi 51:625–632. McKinnon, Jennifer Anderson, Erin Bard, GITAY, H., AND I.R. NOBLE. 1997. What are functional types Jane Mangold, Jim Hafer, and Kirk Denny. We and how should we seek them? Pages 3–19 in T.M. thank Catherine Seibert and Dr. Sharon Smith, H.H. Shugart, and F.I. Woodward, editors, Plant functional types: their relevance to ecosystem Eversman for assisting with vegetative identi- properties and global change. Cambridge University fication. Funding was provided by the Turner Press, Cambridge. 230 WESTERN NORTH AMERICAN NATURALIST [Volume 64

GOODMAN, D. 1975. The theory of diversity-stability rela- SAS INSTITUTE, INC. 1990. SAS/STAT user’s guide. Version tionships in ecology. Quarterly Review of Biology 6, volume 2. Cary, NC. 50:237–267. SALA, O.E., W.K. LAUERONTH, S.J. MCNAUGHTON, G. RUSCH, HOGG, J.T., N.S. WEAVER, J.J. CRAIGHEAD, B.M. STEELE, AND X. ZHANG. 1996. Biodiversity and ecosystem M.L. POKORNY, R.L. REDMOND, AND F. B . F ISHER. function in grasslands. John Wiley & Sons, Chichester, 2001. Vegetative patterns in the Salmon-Selwey eco- UK. system: an improved land cover classification using SHANTZ, H.L., AND R.L. PIEMEISEL. 1924. Indicator signif- Landsat TM imagery and wilderness botanical survey. icance of the natural vegetation of the southwestern Craighead Wildlife-Wildlands Institute, Missoula, MT. desert. Journal of Agricultural Research 28:721–802. HOOPER, D.U., AND P. M . V ITOUSEK 1997. The effects of SHAVER, G.R., A.E. GIBLIN, K.T. NADELHOFFER, AND E.B. plant composition and diversity on ecosystem pro- RASTETTER. 1997. Plant functional types and ecosys- cesses. Nature 277:1302–1305. tem change in Arctic tundras. Pages 153–173 in T.M. JENSEN, M.E., L.S. PECK, AND M.V. WILSON. 1988a. A sage- Smith, H.H. Shugart, and F.I. Woodward, editors, brush community type classification for mountain- Plant functional types: their relevance to ecosystem ous northeastern Nevada rangelands. Great Basin properties and global change. Cambridge University Naturalist 48:422–433. Press, Cambridge. ______. 1988b. Vegetation characteristics of mountainous SHELEY, R.L., T.J. SVEJCAR, AND B.D. MAXWELL. 1996. A northeastern Nevada sagebrush community types. theoretical framework for developing successional Great Basin Naturalist 48:403–412. weed management strategies on rangeland. Weed KEARNEY, T.H., L.J. BRIGGS, AND H.L. SHANTZ. 1914. Indi- Technology 10:766–773. cator significance of vegetation in the Tooele Valley, SIMS, P.L., AND P. 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Princeton, NJ. SYMSTAD, A.J. 2000. A test of the effects of functional group MACCRACKEN, J.G., D.W. URESK, AND R.M. HANSEN. 1983. richness and composition on grassland invasibility. Plant community variability on a small area in south- Ecology 81:99–109. eastern Montana. Great Basin Naturalist 43:660–668. TILMAN, D. 1997. Community invasibility, recruitment limi- tation, and grassland biodiversity. Ecology 78:81–92. MACK, M.C., AND C.M. D’ANTONIO. 1998. Impacts of biological invasions on disturbance regimes. Trends in TILMAN, D., J. KNOPS, D. WEDIN, P. REICH, M. RITCHIE, Ecology and Evolution 13:195–198. AND E. SIEMANN. 1997. The influence of functional diversity and composition on ecosystem process. MCCUNE, B. 1995. Macrolichens of the northern Rocky Mountains. Mad River Press, Eureka, CA. Science 277:1300–1305. TILMAN, D., P.B. REICH, J. KNOPS, D. WEDIN, T. MIELKE, MCNAUGHTON, S.J. 1993. Biodiversity and function of AND C. LEHMAN. 2001. Diversity and productivity in grazing ecosystem. Pages 363–383 in E.D. Schulze, a long-term grassland experiment. Science 294: and H.A. Mooney, editors, Biodiveristy and ecosys- 843–845. tem function. Springer-Verlag, New York. VAN TOOREN, B.F., B. ODE, H.J. DURING, AND R. BOBBINK. MUEGGLER, W.F., AND W.L. STEWART. 1980. Grassland and 1990. Regeneration of species richness in the bryo- shrubland habitat types of western Montana. Inter- phyte layer of Dutch calk grasslands. Lindbergia 16: mountain Forest and Range Experimental Station, 153–160. Ogden, UT. WALKER, B. 1992. Biodiversity and ecological redundancy. NAEEM, S., L.J. THOMPSON, S.P. LAWLER, J.W. LAWTON, AND Conservation Biology 6:18–23. R.M. WOODFIN. 1994. Declining biodiversity can WESTOBY, M., AND. M. LEISHMAN. 1997. Categorizing plant alter the performance of ecosystems. Nature 368: species into functional types. Pages 104–121 in T.M. 734–737. Smith, H.H. Shugart, and F.I. Woodward, editors, PICKETT, S.T.A., S.L. COLLINS, AND J.J. ARMESTO. 1987. Plant functional types: their relevance to ecosystem Models, mechanisms and pathways of succession. properties and global change. Cambridge University Botanical Review 53:335–371. Press, Cambridge. PIMM, S.L. 1991. The balance of nature? University of WILLOUGHBY, M.G., M.J. ALEXANDER, AND K.M. SUNDQUIST. Chicago Press, Chicago. 1998. Range plant community types and carrying POKORNY, M.L. 2002. Plant functional group diversity as a capacity for the montane subregion. 3rd edition. mechanism for invasion resistance. Master’s thesis, Environmental Protection Lands and Forest Ser- Montana State University, Bozeman. vices, Edmonton, Alberta, Canada. ROBINSON, G.R., J.F. QUINN, AND M.L. STANTON. 1995. Invasibility of experimental habitat islands in a Cali- Received 4 November 2002 fornia winter annual grassland. Ecology 76:786–794. Accepted 3 April 2003 Western North American Naturalist 64(2), ©2004, pp. 231–248

REPRODUCTIVE ACTIVITY AND DISTRIBUTION OF BATS IN NEBRASKA

Russell A. Benedict1,2

ABSTRACT.—New geographic, reproductive, and seasonal records are presented for 11 of 13 bats inhabiting Nebraska. New geographic records are presented for 10 species, most notably Myotis lucifugus (120 miles west of nearest known record), M. septentrionalis (42 miles west of nearest record), Nycticeius humeralis (72 miles west of nearest record), and Pipistrellus subflavus (258 miles northwest of nearest record). New reproductive localities are recorded for 9 species, particularly the 1st records of breeding by Pipistrellus subflavus in Nebraska (Cherry and Dixon Counties) and the 2nd record of breeding by Lasionycteris noctivagans in Nebraska (Lancaster County). New records of timing of lactation and appearance of flying-young are reported for 7 species, and new records of seasonal activity are reported for 3 species. Lastly, captures of adult males of Lasiurus borealis and L. cinereus in summer are reported from sites across the state; summer populations of these species previously were thought to consist entirely or primarily of adult females and young in some regions. Records presented here are the result of geographic range expansion of several species and of fieldwork conducted in previously unsampled areas.

Key words: bats, Nebraska, geographic distributions, reproduction, seasonal activity.

Geographic ranges of bats inhabiting research projects. Bats were caught in mist nets Nebraska are poorly known. For instance, set across streams, ponds, roads, trails, or mine Lasionycteris noctivagans is thought to occur entrances (in 4 instances). Most bats were re- across the entire state. However, in the most leased at the point of capture once nets were recent paper summarizing distributions of bats closed for the night; however, at least 1 voucher in Nebraska (Czaplewski et al. 1979), only 15 specimen was collected for most records pre- records of this species were reported from 11 sented herein. Additionally, several records of the state’s 93 counties. Furthermore, Cza- reported here are of bats sighted or collected plewski et al. (1979) reported only 3 new spec- in buildings. Specimens collected during this imens of L. noctivagans collected since the study were deposited in the University of publishing of Distribution and Taxonomy of Nebraska State Museum (UNSM). As of the Nebraska Mammals by J.K. Jones in 1964. writing of this paper, some specimens have yet Likewise, our understanding of reproduc- to be deposited in this museum; these speci- tive activities of bats inhabiting Nebraska is mens are designated with the author’s field extremely limited. For example, Myotis cilio- number beginning with the acronym RAB. labrum occurs across the western third of the Females were classified as lactating only if state, but only 1 reproductive female was de- milk could be expressed from the mammary scribed by Jones (1964), and fewer than 12 re- glands and as post-lactating if the mammary productive females from 2 counties were re- glands were enlarged and surrounded by bare ported by Czaplewski et al. (1979). Herein, I skin but did not contain milk. Flying-young- report new geographic, reproductive, and sea- of-the-year (FYOY) were recognized by the sonal records for 11 of 13 species of bats presence of cartilaginous strips in joints be- known from Nebraska. tween phalanges of the wings. Dates of capture of flying-young and lactating females are com- METHODS pared with those known for the state. The latest date of capture of flying-young is of marginal From 1990 to 2002 bats were caught at sites value because this simply represents the latest across the state during survey work or other date at which FYOY can be distinguished from

1Department of Biology, Chemistry and Environmental Science, Christopher Newport University, 1 University Place, Newport News, VA 23606-2998; and University of Nebraska State Museum, W436 Nebraska Hall, University of Nebraska–Lincoln, Lincoln, NE 68588-0514. 2Present address: Department of Biology, Central College Box 09, 812 University Street, Pella, IA 50219.

231 232 WESTERN NORTH AMERICAN NATURALIST [Volume 64 adults. Seasonal records are presented in cases REPRODUCTIVE RECORDS.—Reproductive where individuals were caught later in the activity has been described for this species year than previously known in Nebraska. only from Sioux and Banner Counties (Fig. 1), However, few nettings were conducted during 2 of the westernmost counties in the state months when new seasonal records could (Jones 1964, Czaplewski et al. 1979). New repro- have been caught. Following are numbers of ductive records are presented from Cherry and nights netted during this study, by month: Sheridan Counties (Fig. 1), extending the known April, 2; May, 6; June, 7; July, 38; August, 20; reproductive distribution of M. ciliolabrum into September, 10; and October, 2. north central Nebraska. The farthest east repro- I present new records by county, listed ductive record presented here is approximately from west to east, then north to south. Within 160 miles east of the nearest known reproduc- each county, records are arranged by date. tive locality (Czaplewski et al. 1979). Specimens are considered new records only if Sheridan County (6 lactating females, 6 they represent new captures for a given county. FYOY): 1 lactating female released 14 July 1998 When detailing reproductive records, I de- (Beaver Creek, 7.3 miles N, 1.4 miles W Hay scribe pregnant females first, then lactating Springs), 3 lactating females released 29 July females, and finally flying-young. For nomen- 2001 (Patton Creek, 17.1 miles N, 2.75 miles clature, I follow taxonomy used by Wilson and W Rushville), and 2 lactating females released Ruff (1999) and van Zyll de Jong (1979, 1984). 30 July 2001 (Patton Creek, 17.2 miles N, 3.2 miles W Rushville). One FYOY male collected RESULTS 11 August 1998 (RAB 4315, Beaver Creek, 7.8 miles N, 1.7 miles W Hay Springs), 1 FYOY From 1990 to 2002, I conducted 87 nights female released 3 August 2000 (Larrabee of netting and caught 1154 bats of 11 species Creek, 13.4 miles N, 2 miles W Rushville), 3 (Table 1). Results are detailed in species FYOY males released 5 August 2000 (Patton accounts below. Only those bats representing Creek, 17.2 miles N, 3.2 miles W Rushville), new geographic, reproductive, or seasonal rec- and 1 FYOY female released 29 July 2001 ords are described in detail. (Patton Creek, 17.1 miles N, 2.75 miles W Rushville). Myotis ciliolabrum Cherry County (3 lactating females, 4 (western small-footed myotis) FYOY): 1 lactating M. ciliolabrum collected 28 Myotis ciliolabrum occurs across western July 2000 (RAB 4954, Minnechaduza Creek, Nebraska reaching east to the Cherry/Brown 1.35 miles N, 0.9 miles E Valentine), 1 lactat- County line along the northern tier of counties ing female released 27 July 2001 (floodplain of (Fig. 1). No new geographic records are pre- Niobrara River, 8.2 miles N, 0.3 miles E Mer- sented here. riman), and 1 lactating female released 31 July

TABLE 1. Number of bats caught during 87 nights of netting in Nebraska from 1990 to 2002. Also included are number of nights each species was caught, number of nights netted in its geographic range, and percentage of nights each species was caught in its geographic range. Number of Nights caught/ Percent nights Species bats caught nights in range caught Eptesicus fuscus 519 54/87 62.1 Nycticeius humeralis 151 26/50 52.0 Lasiurus borealis 145 38/87 43.7 Myotis septentrionalis 137 39/71 54.9 Lasiurus cinereus 95 30/87 34.5 Myotis lucifugus 42 12/71 16.9 Myotis ciliolabrum 28 14/29 48.3 Lasionycteris noctivagans 11 7/87 8.0 Pipistrellus subflavus 18 6/53 11.3 Myotis thysanodes 6 3/17 17.6 Myotis volans 2 2/17 11.2 TOTAL 1154 2004] NEW RECORDS OF BATS OF NEBRASKA 233

Dawes Cherry Keya P aha Boyd

2 Cedar Holt Brown Knox 2 Rock Dixon

Dakota Box Butte Antelope Pierce Wayne 1 Thurston Sioux Sheridan Stanton Cuming Grant Hooker Blaine p Garfield Wheeler Madison Scotts B Thomas Lou Burt luff Morrill Garden Boone

Platte Colfax Dodge Arthur McPherson Logan Custer Valley Greeley Washington

Banner e Cheye Nanc Kimball nne Saunders Douglas Keith Lincoln Sherman Howard Polk Merrick Deuel Sarpy Butler Lancaster Dawson Buffalo Hall York Seward Cass Perkins Hamilton 2 Otoe 50 km Chase Hayes Frontier Gosper Adams Clay Fillmore Saline 0 Phelps Kearney n Nemaha 50 Miles Gage Johnso Figure 1. Dund ranklin Webster Nuckolls Thayer Jefferson Myotis ciliolabrum (1) y Hitchcock Red W illow Furnas Harlan F Richardson Pawnee Nycticeius humeralis (2)

Fig. 1. Geographic distribution and new records of Myotis ciliolabrum (1) and Nycticeius humeralis (2). Shaded areas indicate geographic distribution proposed by Czaplewski et al. (1979). Open symbols are previously published records; closed symbols are new records presented in this paper. Circles are geographic records; triangles are reproductive records (triangles also indicate new geographic records in some cases; see text).

2001 (floodplain of Niobrara River, 6.2 miles S, tember; Jones 1964). However, netting was not 4.1 miles W Cody). One FYOY female collected conducted within the geographic range of M. 28 July 2000 (RAB 4956, Minnechaduza Creek, ciliolabrum during months that could have pro- 1.35 miles N, 0.9 miles E Valentine), 2 FYOY duced new dates of activity. females released 31 July 2000 (Minnechaduza Myotis lucifugus Creek, 1 mile N Valentine), and 1 FYOY male (little brown bat) released 27 July 2001 (floodplain of Niobrara River, 8.2 miles N, 0.3 miles E Merriman). Myotis lucifugus is thought to occupy 2 TIMING OF REPRODUCTIVE ACTIVITY.—Dur- geographically separated areas of Nebraska. ing this study lactating M. ciliolabrum were The eastern population apparently inhabits captured 14–31 July; a total of 10 lactating the eastern quarter of the state, but specimens females were caught during 7 nights of netting are unknown from much of northeastern Ne- (this includes a female captured in Sioux County braska (Fig. 2). The western population occu- that was not reported above because repro- pies the Pine Ridge and Niobrara River valley ductive activity is known from this county). in extreme northwestern Nebraska. GEOGRAPHIC RECORDS.—New geographic These dates are within those previously reported records are presented from Sheridan, Cherry, for this species in Nebraska (14 July–8 August) and Dixon Counties (Fig. 2). On 5 of 6 nights by Czaplewski et al. (1979). Likewise, flying- when these specimens were caught, Myotis young-of-the-year were captured 27 July–11 septentrionalis also was captured, allowing side- August during this study; 10 FYOY were cap- by-side comparison of these similar species. tured during 7 nights of netting. There are no From M. septentrionalis, M. lucifugus was dis- previous records of flying-young in Nebraska, tinguished by its longer forearm, greater weight, but Jones et al. (1983) reported FYOY as early and smaller ear with a differently shaped tra- as 26 July in the Black Hills of South Dakota. gus (Jones et al. 1983). The Dixon County SEASONAL ACTIVITY.—Myotis ciliolabrum specimen supports assertions of Jones (1964) was captured during this study 14 July–13 and Czaplewski et al. (1979) that M. lucifugus August; 28 individuals were caught during 14 occurs in northeastern Nebraska. Likewise, nights of netting (not all are reported above). the Sheridan County specimens support the These dates are within those previously reported predicted occurrence of M. lucifugus in the for this species from Nebraska (2 May–5 Sep- eastern Pine Ridge. 234 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Sioux Dawes Cherry Keya P aha Boyd

Cedar Holt nox Brown K Dixon Rock

1 Dakota Box Butte Antelope Pierce Wayne Thurston

son Stanton Cuming Sheridan Grant Hooker Blaine Garfield Wheeler Madi Scott B Thomas Loup Burt s luff Morrill Garden Boone

e Platte Colfax Dodg Banner Arthur McPherson Logan Custer Valley Greeley 2 Washington

Nance Cheye as Kimball nne Saunders Dougl Keith Lincoln Sherman Howard Butler Polk Merrick Deuel Sarpy

ard Lancaster Dawson Buffalo Hall York Sew Cass Perkins Hamilton e 50 km Oto e Chase Hayes Frontier Gosper Adams Clay Fillmore Salin 0 Phelps Kearney on Nemaha 50 Miles Gage Johns

n Du Nuckolls Thayer Jefferso dson ndy Hitchcock Red W illow Furnas Harlan Franklin Webster Pawnee Richar Figure 2. Myotis lucifugus carissima (1) Fig. 2. Geographic distribution and new records of Myotis lucifugus. Shaded areas indicate geographic distribution proposed by Czaplewski et al. (1979). Open symbols are previously published records; closed symbols are new records presented in this paper. Circles are geographic records; triangles are reproductive records (triangles also indicate new geographic records in some cases; see text).

The new specimen of M. lucifugus from and M. l. lucifugus in the east. I examined Cherry County is difficult to interpret. The specimens of both subspecies and found no nearest reported records of this species (Fig. noticeable differences in coloration. Further- 2) were 130 miles east (Czaplewski et al. 1979) more, although M. l. carissima does have a and 120 miles west (Jones 1964) of the speci- larger cranium on average, substantial overlap men reported here. Therefore, this new speci- exists between the 2 subspecies in cranial and men may indicate a large range expansion for external dimensions. Measurements of the new this species or may mark the presence of an specimen lie in the range of overlap between isolated population—either a relictual popula- the 2 subspecies, making it impossible to tion or a recent colonization. Other relictual assign the new specimen to subspecies. populations occur in this part of the Niobrara Sheridan County (4): 1 adult male collected River valley, most notably Neotoma floridana 10 August 1998 (RAB 4308, Larrabee Creek, baileyi (Jones 1964). If this specimen indicates 14.2 miles N, 2.5 miles W Rushville), 1 adult a large range extension, it could represent female released 13 August 1998 (Patton Creek, westward expansion of the eastern population 17.1 miles N, 2.75 miles W Rushville), 1 adult or eastward expansion of the western popula- male collected 4 August 2000 (RAB 4978, Larra- tion. The geography of northern Nebraska bee Creek, 14.1 miles N, 2.5 miles W Rushville), makes it more likely that the new record is and 1 FYOY female collected 5 August 2000 derived from the eastern population. Wood- (RAB 4982, Patton Creek, 17.2 miles N, 3.2 lands are now nearly contiguous along the miles W Rushville). Missouri River on Nebraska’s eastern border Cherry County (1): 1 adult female collected and connect to the valley of the Niobrara 1 August 2000 (RAB 4964, Minnechaduza River, which may allow eastern M. lucifugus to Creek, 1 mile N Valentine). extend west. On the other hand, for western Dixon County (1): 1 adult male collected 20 M. lucifugus to expand from the Pine Ridge to July 2001 (RAB 5081, Ponca State Park, 2.5 the Niobrara River valley, they would have to miles N, 0.6 miles W Ponca). cross roughly 50 or 60 miles of nearly treeless REPRODUCTIVE RECORDS.—Reproduction habitat. has been recorded in Myotis lucifugus in Sioux The subspecific identity of this new speci- and Dawes Counties in the northwest (Jones men of M. lucifugus should provide insight 1964) and Johnson County in the southeast into its origin. According to Jones (1964), 2 (Czaplewski et al. 1979). One new reproductive subspecies inhabit Nebraska, namely the paler locality is presented here. The FYOY female and slightly larger M. l. carissima in the west reported above from Sheridan County (RAB 2004] NEW RECORDS OF BATS OF NEBRASKA 235

4982) represents the first evidence of repro- Wildlife Management Area, 9.9 miles S, 9.1 duction by M. lucifugus in this county. Repro- miles E Nenzel); and 1 adult female collected, duction has been documented in adjacent 1 adult female, 1 adult male, 3 lactating females, Dawes County (Jones 1964). and 1 FYOY female released 31 July 2001 (RAB TIMING OF REPRODUCTIVE ACTIVITY.—Dur- 5087, floodplain of Niobrara River, 6.2 miles S, ing this study 12 lactating M. lucifugus were 4.1 miles W Cody). captured during the nights of 15 and 16 July Dixon County (3): 1 adult male collected 19 1998 in Sioux County (records not presented July 2001 (RAB 5078, Ponca State Park, 2.9 above because breeding has been recorded miles N, 0.3 miles W Ponca), and 2 adult males from Sioux County). The only other reported released 20 July 2001 (Ponca State Park, 2.5 date of capture of lactating M. lucifugus in miles N, 0.6 miles W Ponca). Nebraska is 24 June (Czaplewski et al. 1979). REPRODUCTIVE RECORDS.—The only re- Additionally, flying-young were captured 15 ported reproductive localities for M. septentri- July–5 August during this study; 3 FYOY were onalis in the state are in Cass County (Jones captured during 3 nights of netting (this includes 1964), Cherry County (Benedict et al. 2000), 2 bats captured in Sioux County that were not Sarpy County (Jones 1964, Geluso et al. 2004), reported above because reproductive activity and Webster County (Czaplewski et al. 1979; is known from this county). The only other date Fig. 3). Reproductive records are presented reported for flying-young M. lucifugus in Nebra- here from Sheridan, Cherry, Knox, and Lan- ska is “late July” (Czaplewski et al. 1979:6). caster Counties. These records significantly SEASONAL RECORDS.—During this study lit- expand the known reproductive distribution of tle brown bats were captured 1 July–5 Sep- M. septentrionalis in Nebraska (Fig. 3). The tember; 41 M. lucifugus were caught during Sheridan County records, a flying-young and a 12 nights of netting (not all are reported post-lactating female, provide the 1st evidence above). This species is a year-round resident of reproduction in the Pine Ridge; the previ- in eastern Nebraska (Jones 1964) and the Black ous 7 M. septentrionalis captured in this region Hills of South Dakota (Jones et al. 1983). were adult males (Benedict et al. 2000). Sheridan County (1 post-lactating female, 1 Myotis septentrionalis FYOY): 1 post-lactating female collected 4 (northern long-eared myotis) August 2000 (RAB 4979, Larrabee Creek, 14.1 Myotis septentrionalis is thought to occupy miles N, 2.5 miles W Rushville), and 1 FYOY most of the eastern half of Nebraska (Fig. 3), female collected 5 August 2000 (RAB 4989, but much of this proposed distribution is un- Patton Creek, 17.2 miles N, 3.2 miles W supported by records. Additionally, an appar- Rushville). ently isolated population recently has been Cherry County (4 lactating females, 1 FYOY): reported from the northwestern corner of the The lactating females and flying-young re- state (Benedict et al. 2000). corded above, including RAB 4970, represent GEOGRAPHIC RECORDS.—New geographic the 1st records of reproduction of M. septen- records are reported here from Dixon County trionalis in western Cherry County. and northwest Cherry County (Fig. 3). The Knox County (4 lactating females, 7 FYOY): Dixon County specimen supports claims of 1 lactating female released 21 July 2001 (creek, Jones (1964) and Czaplewski et al. (1979) that 6.5 miles N, 5.4 miles W Verdigre), and 3 lac- M. septentrionalis occurs in northeastern tating females released 22 July 2001 (Schind- Nebraska. The Cherry County specimens in- ler Creek, 5.7 miles N, 3.5 miles W Verdigre). dicate this species extends at least 42 miles One FYOY male released and 1 FYOY female farther west along the Niobrara River than collected 21 July 2001 (RAB 5082, unknown reported by Benedict et al. (2000). Given the creek, 6.5 miles N, 5.4 miles W Verdigre), and lack of suitable habitat in surrounding areas, 3 FYOY females and 2 FYOY males released M. septentrionalis likely occurs in Cherry 22 July 2001 (Schindler Creek, 5.7 miles N, County only in the valleys of the Niobrara 3.5 miles W Verdigre). River and its tributaries. Lancaster County (3 lactating females, 1 Cherry County (11): 1 adult female, 2 adult FYOY): 1 lactating female collected 12 July males, and 1 lactating female collected 1 August 1995 (RAB 3258, Salt Creek, 5.2 miles S, 0.25 2000 (RAB 4967, 4969–4971, Anderson Bridge miles W Lincoln), 1 lactating female released 236 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Sioux Dawes Cherry Keya P aha Boyd

Cedar Holt Brown Rock

Knox Dakota B ox Butte Antelope Pierce Dixon Wayne Thurston

Sheridan n Stanton Cuming Grant Hooker Blaine up Garfield Wheeler Madiso Scott B Thomas Lo Burt s luff Morrill Garden Boone

ge Platte Colfax Dod Banner Arthur McPherson Logan Custer Valley Greeley Washington

Cheyenn Nance as Kimball e Saunders Dougl Keith Lincoln Sherman Howard Butler Polk Merrick Deuel Sarpy

ard Lancaster Dawson Buffalo Hall York Sew Cass Perkins Hamilton e 50 km Oto e Chase Hayes Frontier Gosper Adams Clay Fillmore Salin 0 Phelps Kearney son Nemaha 50 Miles Gage John

Dundy Nuckolls Thayer Jefferson dson Figure 3. Hitchcock Red W illow Furnas Harlan Franklin Webster Pawnee Richar Myotis septentrionalis

Fig. 3. Geographic distribution and new records of Myotis septentrionalis. Shaded areas indicate geographic distribution proposed by Czaplewski et al. (1979). Open symbols are previously published records; closed symbols are new records presented in this paper. Circles are geographic records; triangles are reproductive records.

19 July 1995 (Salt Creek, 4.25 miles S, 0.25 but not all are recorded above. These dates miles W Lincoln), and 1 lactating female re- are within the known range of activity for this leased 13 July 1996 (Salt Creek, 5.2 miles S, species in Nebraska (21 March–16 October; 0.25 miles W Lincoln). One FYOY male col- Geluso et al. 2004). lected 12 July 1995 (RAB 3260, 5.2 miles S, Myotis thysanodes 0.25 miles W Lincoln). (fringed myotis) TIMING OF REPRODUCTIVE ACTIVITY.—Dur- ing this study 23 lactating female Myotis The fringed myotis has been recorded in septentrionalis were caught between 12 July Sioux, Dawes, and Banner Counties in north- and 1 August during 12 nights of netting (this western Nebraska (Fig. 4; Czaplewski et al. includes 12 lactating females captured in east- 1979). No reproductive data are available from ern Cherry County that were not reported Nebraska and no reproductive records are above because reproductive activity is known presented here. from this region). This study extends the GEOGRAPHIC RECORDS.—New specimens of known range of dates of lactation for this M. thysanodes are presented from northern species; previously known dates of lactating Sheridan County, supporting assertions of females for the state are 31 May–20 July (Geluso Jones (1964) and Czaplewski et al. (1979) that et al. 2004). Additionally, flying-young were this species occurs in the eastern Pine Ridge. captured 12 July–5 August; a total of 36 flying- These bats were captured roughly 28 miles young were caught during 11 nights of netting northeast of the nearest reported specimens (this includes 26 FYOY captured in eastern (Czaplewski et al. 1979). Cherry County that were not reported above Sheridan County (6): 4 adult males collected because reproductive activity is known from 17 July 1998 (RAB 4294, 4296, 4302–4303; this area). These dates are within the previ- Larrabee Creek, 13.4 miles N, 2 miles W Rush- ously known range of dates for flying-young ville), and 1 adult male released 13 August 1998 M. septentrionalis in Nebraska (3 July–5 Sep- and 29 July 2001 (both from Patton Creek, tember; Geluso et al. 2004). 17.1 miles N, 2.75 miles W Rushville). SEASONAL RECORDS.—Myotis septentrion- SEASONAL RECORDS.—During this study M. alis was captured during this study on 38 thysanodes was captured 17 July–13 August; 6 nights of netting between 11 April and 16 bats were captured during 3 nights of netting. October; 137 M. septentrionalis were caught The previously known dates of activity from 2004] NEW RECORDS OF BATS OF NEBRASKA 237

Sioux Dawes Cherry Keya P aha Boyd

Cedar Holt Brown Knox 2 Rock Dixon

Dakota Box 2 1 Butte Antelope Pierce Wayne Thurston

nton Cuming Sheridan Grant eeler Madison Sta Hooker Thomas Blaine Loup Garfield Wh Burt Scotts Bluff Morrill Garden Boone

ge Platte Colfax Dod Banner Arthur McPherson Logan Custer Valley Greeley 2 Washington

Cheyenn Nance as Kimball e Saunders Dougl Keith Lincoln Sherman Howard Butler Polk Merrick Deuel Sarpy

ard Lancaster Dawson Buffalo Hall York Sew Cass Perkins Hamilton e 50 km Oto e Chase Hayes Frontier Gosper Adams Clay Fillmore Salin 0 Phelps Kearney on Nemaha 50 Miles Gage Johns igure 4. rson Dundy Franklin Webster Nuckolls Thayer Jeffe dson Myotis thysanodes (1) Hitchcock Red W illow Furnas Harlan 2 Pawnee Richar ipistrellus subflavus (2)

Fig. 4. Geographic distribution and new records of Myotis thysanodes (1) and Pipistrellus subflavus (2). Shaded areas indicate geographic distribution proposed by Czaplewski et al. (1979). Open symbols are previously published records; closed symbols are new records presented in this paper. Circles are geographic records; triangles are reproductive records (triangles also indicate new geographic records in some cases; see text).

Nebraska are “June” to 7 August (Czaplewski dates are within the known range of activity of et al. 1979:7); this species occupies the nearby this species in the state (22 June–15 August; Black Hills of South Dakota year-round (Jones Czaplewski et al. 1979). et al. 1983). Pipistrellus subflavus Myotis volans (eastern pipistrelle) (long-legged myotis) Pipistrellus subflavus is known from 4 local- Myotis volans is known only from Sioux and ities in extreme eastern Nebraska but may Dawes Counties in the Pine Ridge of north- occur elsewhere in the southeastern corner of western Nebraska (Fig. 5; Jones 1964, Czaplew- the state (Fig. 4; Jones 1964, Geluso et al. ski et al. 1979). No reproductive records are 2004). presented here, but this species is known to GEOGRAPHIC RECORDS.—Three new geogra- breed in the state (Czaplewski et al. 1979). phic records are presented here from Dixon, GEOGRAPHIC RECORDS.—A new specimen Greeley, and Cherry Counties (Fig. 4). The is presented from northern Sheridan County, bats from Dixon and Greeley Counties were confirming predictions of Jones (1964) and captured 108 miles north and 136 miles west, Czaplewski et al. (1979) that this species occu- respectively, of the nearest known specimens pies the eastern Pine Ridge. This specimen was (Jones 1964, Geluso et al. 2004). The Cherry captured roughly 27 miles northeast of the County specimens are 258 miles northwest of nearest previously known records (Czaplewski the nearest known specimens (Jones 1964), et al. 1979). making them the farthest northwest records of Sheridan County (1): 1 adult male collected P. subflavus in North America. These new 5 August 2000 (RAB 4983, Patton Creek, 17.2 specimens are difficult to interpret in light of miles N, 3.2 miles W Rushville). what is known of this species in the state. The SEASONAL RECORDS.—During this study M. eastern pipistrelle is captured so infrequently volans was captured 16 July and 5 August; 2 in eastern Nebraska that its geographic range individuals were captured during these 2 nights and breeding status are difficult to determine of netting (this includes 1 bat caught in Sioux (Geluso et al. 2004). When combined with County that is not reported above because this previously known specimens, the new records species is known from Sioux County). These presented here could indicate this species is 238 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Sioux Dawes Cherry Keya P aha Boyd

Cedar Holt Brown Knox Rock Dixon

Dakota Box Butte Antelope Pierce Wayne Thurston

Sheridan ison Stanton Cuming Grant Hooker Thomas Blaine Loup Garfield Wheeler Mad Scotts Bluff Burt Morrill Garden Boone

e Platte Colfax Dodg Banner Arthur McPherson Logan Custer Valley Greeley Washington

Nance Cheyen glas Kimball ne Saunders Dou Keith Lincoln Sherman Howard Butler Polk Merrick Deuel Sarpy

d Lancaster Dawson Buffalo Hall York Sewar Cass Perkins Hamilton 50 km Otoe Chase Hayes Frontier Gosper Adams Clay Fillmore Saline 0 Phelps Kearney Nemaha 50 Miles Gage Johnson

on Dundy lin bster Nuckolls Thayer Jeffers on Figure 5. Hitchcock Red W illow Furnas Harlan Frank We Pawnee Richards Myotis volans

Fig. 5. Geographic distribution and new records of Myotis volans. Shaded areas indicate geographic distribution proposed by Czaplewski et al. (1979). Open symbols are previously published records; closed symbols are new records presented in this paper. Circles are geographic records; triangles are reproductive records.

continuously distributed along rivers in the REPRODUCTIVE RECORDS.—Prior to this study eastern half of the state. A more likely expla- no evidence of reproduction by Pipistrellus nation, however, is that these specimens are subflavus had been reported in Nebraska. The derived from isolated populations of this species 2 lactating females reported above, RAB 4955 located near rocky outcrops or mines that serve from Cherry County and RAB 5076 from as hibernacula. The P. subflavus from Greeley Dixon County, represent the 1st records of County were caught in a mine, and the Dixon breeding by this species in the state. and Cherry County specimens were captured TIMING OF REPRODUCTIVE ACTIVITY.—Dur- within short distances of rocky cliffs or outcrops. ing this study a total of 2 lactating female P. These isolated populations could have been subflavus were captured on 19 and 28 July. present in the past but overlooked by re- There are no previous records of lactating searchers or could represent recent coloniza- females from Nebraska. No flying-young P. tion of these areas. Considering the Greeley subflavus have been captured in Nebraska, County specimens were caught in a mine and but a bat reported by Geluso et al. (2004) may few rocky outcrops are present in this area, have been a FYOY based on lack of tooth wear. this population almost certainly represents a SEASONAL RECORDS.—During this study P. recent colonization. Pipistrellus subflavus also subflavus was captured 1 July–5 September; appears to be expanding westward in Kansas 18 bats were caught during 6 nights of netting due to the construction of mines and other (this includes 6 individuals captured in Cass structures (Sparks and Choate 1995). County that were not reported above because Cherry County (2): 1 lactating female and 1 records are known from that county). These adult male collected 28 July 2000 (RAB 4955 dates extend the known range of seasonal and 4960, Minnechaduza Creek, 1.35 miles N, activity of this species in Nebraska; previously 0.9 miles E Valentine). known dates of activity for P. subflavus Greeley County (10): 1 adult male collected, spanned 19 May–2 September (Geluso et al. and 3 adult males and 6 adult females released 2004). 31 August 2002 (RAB 5108, Happy Jack Chalk Lasionycteris noctivagans Mine, 1.2 miles S, 1 mile W Scotia). (silver-haired bat) Dixon County (1): 1 lactating female collected 19 July 2001 (RAB 5076, Ponca State Park, 2.9 Lasionycteris noctivagans has been captured miles N, 0.3 miles W Ponca). at localities across Nebraska (Fig. 6). Jones 2004] NEW RECORDS OF BATS OF NEBRASKA 239

Sioux Dawes Cherry Keya P aha Boyd

Cedar Holt Brown Knox Rock Dixon

Dakota B ox Butte Antelope Pierce Wayne Thurston

nton Cuming Sheridan Grant eeler Madison Sta Hooker Thomas Blaine Loup Garfield Wh Burt Scotts Bluff Morrill Garden Boone

ge Platte Colfax Dod Banner Arthur McPherson Logan Custer Valley Greeley Washington

Cheye Nance as Kimball nne Saunders Dougl Keith Lincoln Sherman Howard Butler Polk Merrick Deuel Sarpy

ard Lancaster Dawson Buffalo Hall York Sew Cass Perkins Hamilton e 50 km Oto Chase Hayes Gosper Adams Clay Fillmore Saline 0 Phelps Kearney son Nemaha 50 Miles Gage John

Frontier Dundy Nuckolls Thayer Jefferson dson gure 6. Hitchcock Red W illow Furnas Harlan Webster Pawnee Richar

sionycteris noctivagans Franklin

Fig. 6. New records of Lasionycteris noctivagans. Species occurs statewide. Open symbols are previously published records; closed symbols are new records presented in this paper. Circles are geographic records; triangles are reproductive records.

(1964) and Czaplewski et al. (1979) suggested 1995 (UNSM 20,765, Salt Creek, 4.35 miles S, this species may be present in the state only as 0.3 miles W Lincoln), and 1 flying-young male a migrant. collected 13 July 1996 (UNSM 26,055, Salt GEOGRAPHIC RECORDS.—New specimens of Creek, 5.2 miles S, 0.25 miles W Lincoln). the silver-haired bat are presented here from TIMING OF REPRODUCTIVE ACTIVITY.—In a Sheridan and Knox Counties, further support- single night of netting during this study, 2 lac- ing the predicted statewide distribution of this tating female L. noctivagans were caught on species (Fig. 6). 13 July. This extends the known range of dates Sheridan County (2): 1 adult male collected of lactation in this species in Nebraska; previ- and 1 adult female released 5 August 2000 (RAB ously known dates were 16 June–6 July (Geluso 4984, Patton Creek, 17.2 miles N, 3.2 miles W et al. 2004). Additionally, 2 flying-young were Rushville). caught during 2 nights of netting, 13 and 17 Knox County (1): 1 adult female released 22 July. This is the first reported capture of FYOY July 2001 (Schindler Creek, 5.7 miles N, 3.5 silver-haired bats in Nebraska. miles W Verdigre). SEASONAL RECORDS.—One new seasonal rec- REPRODUCTIVE RECORDS.—The 1st records ord for L. noctivagans is presented here. A fe- of reproduction by L. noctivagans in Nebraska male was captured by hand in a barn 26 Novem- were presented by Geluso et al. (2004) from ber 1997 (UNSM 25,283, Cuming County, 6 eastern Sarpy County (Fig. 6). New reproduc- miles W Bancroft). The bat, which was roost- tive records are presented here from Lan- ing on a stack of hay bales, did not have visible caster County. Breeding by L. noctivagans is cartilage in the phalangeal joints of the wings now confirmed in Sarpy (Geluso et al. 2004) but had little tooth wear, suggesting it was a and Lancaster Counties in Nebraska, dis- flying-young. Including this specimen, silver- pelling the idea that this species is strictly a haired bats were caught 5 May–26 November migrant in Nebraska. Whether this species during this study; 11 bats were caught during breeds in central and western Nebraska is 8 nights of netting (not all described above), unknown at the present time. and 1 bat was captured by hand. This extends Lancaster County (2 lactating females, 2 the known dates of activity for this species in FYOY): 2 lactating females released 13 July Nebraska from previously known dates that 1996 (Salt Creek, 5.2 miles S, 0.25 miles W spanned 21 April–2 October (Jones 1964, Lincoln). One FYOY male collected 17 July Geluso et al. 2004). 240 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Sioux Dawes Cherry Keya P aha Boyd

Cedar Holt Knox Rock

Dakota Box Butte Antelope Pierce Wayne Dixon Thurston

Brown nton Cuming Sheridan Grant eeler Madison Sta Hooker Thomas Blaine Loup Garfield Wh Burt Scotts Bluff Morrill Garden Boone

ge Platte Colfax Dod Arthur McPherson Logan Custer Valley Greeley Washington

Banner Cheye Nance as Kimball nne Saunders Dougl Keith Lincoln Sherman Howard Butler Polk Merrick Deuel Sarpy

ard Lancaster Dawson Buffalo Hall York Sew Cass Perkins Hamilton e 50 km Oto Chase Hayes Frontier Gosper Adams Clay Fillmore Saline 0 Phelps Kearney son Nemaha 50 Miles Gage John

Dundy Nuckolls Thayer Jefferson dson Figure 7. Hitchcock Red W illow Furnas Harlan Franklin Webster Pawnee Richar Eptesicus fuscus

Fig. 7. New records of Eptesicus fuscus. Species occurs statewide. Open symbols are previously published records; closed symbols are new records presented in this paper. Circles are geographic records; triangles are reproductive records (triangles also indicate new geographic records in some cases; see text).

Eptesicus fuscus ner, Sioux, Sheridan, Cherry, and Sarpy Coun- (big brown bat) ties (Jones 1964, Czaplewski et al. 1979, Geluso et al. 2004). New reproductive records are pre- Eptesicus fuscus occurs statewide in Nebra- sented from Dawes, Garden, Keya Paha, Boyd, ska, but records are unknown from many coun- Knox, Dixon, Saunders, Lancaster, and Cass ties (Fig. 7). Counties, supporting proposed statewide repro- GEOGRAPHIC RECORDS.—New geographic duction by E. fuscus. records are presented from Garden, Saunders, Dawes County (1 pregnant female, 10 lactat- Lancaster, and Richardson Counties (Fig. 7). ing females): 1 pregnant female collected 30 These records fill in some gaps in the distribu- June 1999 (UNSM 25,422, banks of West Ash tion of E. fuscus. Creek, 3.7 miles S, 7.8 miles E Crawford). Ten Garden County (3): 1 FYOY female and 1 lactating females released 1 July 1999 (Big Bor- adult male collected, 1 FYOY female released deaux Creek, 7.8 miles S, 3.5 miles E Chadron). 16 July 1991 (UNSM 18,803–18,804, Ash Hol- Garden County (2 FYOY): The 2 FYOY de- low State Historical Park, pond west of visitor’s scribed above (including UNSM 18,804) rep- center, 1.8 miles S, 1.1 miles E Lewellen). resent new reproductive records for Garden Saunders County (>150): Saw >150 females County. with nursing young in old coloseum 20 June Keya Paha County (6 lactating females): 6 1991 (National Guard Camp, 1.6 miles N, 2.2 lactating females released 27 July 1993 (East miles E Ashland). Middle Creek, 15.9 miles N, 0.2 miles E Johns- Lancaster County (1): 1 adult male collected town). 30 June 1995 (UNSM 20,770, old channel of Boyd County (7 lactating females, 2 FYOY): Salt Creek, 2.75 miles S, 0.4 miles W Lincoln). 7 lactating females and 2 FYOY males released During this study 49 E. fuscus were captured 23 July 2001 (Beaver Creek, 1.6 miles E in Lancaster county; only this voucher speci- Spencer). men is described. Knox County (1 lactating female, 2 FYOY): Richardson County (2): 1 adult male and 1 1 lactating female released 22 July 2001 (Schind- adult female released 3 August 2001 (Pony ler Creek, 5.7 miles N, 3.5 miles W Verdigre). Creek, 2.2 miles S, 0.4 miles E Falls City). One FYOY female released 21 July 2001 (creek REPRODUCTIVE RECORDS.—Although Eptesi- 6.5 miles N, 5.4 miles W Verdigre), and 1 FYOY cus fuscus is thought to breed across the state, male released 22 July 2001 (Schindler Creek, reproductive records are known only from Ban- 5.7 miles N, 3.5 miles W Verdigre). 2004] NEW RECORDS OF BATS OF NEBRASKA 241

Dixon County (5 lactating females, 27 FYOY): SEASONAL RECORDS.—During this project 5 lactating females released 20 July 2001 (Ponca E. fuscus was captured 7 May–16 September; State Park, 2.5 miles N, 0.6 miles W Ponca). 516 individuals were captured during 54 Six FYOY females and 8 FYOY males released nights of netting, 1 bat was collected from a 19 July 2001 (Ponca State Park, 2.9 miles N, building, and >160 E. fuscus were sighted in 0.3 miles W Ponca), and 3 FYOY females and buildings. These dates are within those known 11 FYOY males released 20 July 2001 (Ponca for this species in Nebraska (21 March–1 State Park, 2.5 miles N, 0.6 miles W Ponca). November; Geluso et al. 2004). Saunders County (>150 lactating females): Lasiurus borealis The E. fuscus with nursing young described (eastern red bat) above represent the 1st reproductive record for this species in Saunders County. Lasiurus borealis likely occurs statewide, Lancaster County (4 lactating females, 2 but captures have not been recorded in some FYOY): 3 lactating females released 9 July regions (Fig. 8). 1997 (Beal Slough, 3.1 miles S, 0.3 miles W GEOGRAPHIC RECORDS.—New geographic Lincoln), and 1 lactating female collected 8 records are presented from Sheridan, Boyd, June 1999 (RAB 4787, Salt Creek, 4.15 miles Sherman, Merrick, Dixon, and Johnson Coun- N, 0.3 miles W Lincoln). One FYOY female ties (Fig. 8), filling in some gaps in the distrib- collected 16 August 1995 (UNSM 20,798, Lin- ution of L. borealis. coln, UNL City Campus), and 1 FYOY male Sheridan County (7): 1 adult female released and 1 FYOY female released 29 August 1995 4 August 2000 (Larrabee Creek, 14.1 miles N, (Salt Creek, 3.3 miles S, 0.4 miles W Lincoln). 2.5 miles W Rushville), 3 adult females and 1 Cass County (4 females with young, 4 lactat- adult male released 5 August 2000 (Patton Creek, 17.2 miles N, 3.2 miles W Rushville), 1 ing females, 3 FYOY): 4 females with nursing adult female released 29 July 2001 (Patton young sighted at Plattsmouth Middle School Creek, 17.1 miles N, 2.75 miles W Rushville), on 2 July 1991 (Plattsmouth). One lactating and 1 adult female released 30 July 2001 (Patton female released 24 July 1995, and 2 lactating Creek, 17.2 miles N, 3.2 miles W Rushville). females released 30 July 1995 (all from pond Boyd County (4): 1 lactating female, 2 FYOY just S of Hidden Canyon Road, 1.9 miles S, males, and 1 FYOY female released 23 July 0.6 miles E Plattsmouth), and 1 lactating female 2001 (Beaver Creek, 1.6 miles E Spencer). released 1 July 1996 (mine entrance, 3 miles Sherman County (3): 2 adult males and 1 N, 8.9 miles W Plattsmouth). Three FYOY males adult female released 1 August 2001 (Muddy released 30 July 1995 (pond just S of Hidden Creek, 1 mile S, 0.75 miles E Litchfield). Canyon Road, 1.9 miles S, 0.6 miles E Platts- Merrick County (4): 3 lactating females and mouth). 1 FYOY female released 13 July 1999 (approx- TIMING OF REPRODUCTIVE ACTIVITY.—Dur- imately 3 miles S Chapman). ing this project lactating females were cap- Dixon County (21): 1 lactating female, 1 adult tured 8 June–5 August; 101 lactating females female, 7 FYOY females, and 4 FYOY males were captured on 23 nights of netting (these released 19 July 2001 (Ponca State Park, 2.9 numbers include bats not described above miles N, 0.3 miles W Ponca), and 4 FYOY because reproduction was already known from females and 4 FYOY males released 20 July counties in which they were captured). These 2001 (Ponca State Park, 2.5 miles N, 0.6 miles dates are within those reported previously for W Ponca). E. fuscus in Nebraska (31 May–5 September; Johnson County (1): 1 adult female released Jones 1964, Geluso et al. 2004). Likewise, 197 21 May 1999 (Johnson Creek, 8.8 miles S, 7 flying-young were captured 16 July–29 August miles E Burchard). during 20 nights of netting (these numbers REPRODUCTIVE RECORDS.—Although repro- include bats not described above because ductive records are more numerous for L. reproduction was already known from coun- borealis than other species, breeding has been ties in which they were captured). These dates documented only in Sioux, Morrill, Phelps, Buf- are within the known range of dates of FYOY falo, Adams, Butler, Lancaster, and Sarpy Coun- of E. fuscus in Nebraska (6 July–21 Septem- ties (Fig. 8; Czaplewski et al. 1979, Benedict ber; Geluso et al. 2004). et al. 2000, Geluso et al. 2004). Reproductive 242 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Sioux Dawes Cherry Keya P aha Boyd

Cedar Holt Knox Rock

Dakota Box Butte Antelope Pierce Wayne Dixon Thurston

Brown nton Cuming Sheridan Grant eeler Madison Sta Hooker Thomas Blaine Loup Garfield Wh Burt Scotts Bluff Morrill Garden Boone

ge Platte Colfax Dod Arthur McPherson Logan Custer Greeley Washington

Banner Valley Cheyenn Nance as Kimball e Saunders Dougl Keith Lincoln Howard Polk Merrick Deuel Sarpy tler Sherman Bu ard Lancaster Dawson Buffalo Hall York Sew Cass Perkins Hamilton e 50 km Oto Chas Hayes Gosper Adams Clay Fillmore Saline 0 e Phelps son Nemaha 50 Miles Gage John

Frontier Kearney Dundy Nuckolls Thayer Jefferson Figure 8. Hitchcock Red W illow Furnas Harlan Franklin Webster Pawnee Lasiurus borealis Richardson

Fig. 8. New records of Lasiurus borealis. Species occurs statewide. Open symbols are previously published records; closed symbols are new records presented in this paper. Circles are geographic records; triangles are reproductive records (triangles also indicate new geographic records in some cases; see text). records are presented here from Cherry, Keya Merrick County (3 lactating females, 1 Paha, Brown, Boyd, Knox, Merrick, Dixon, FYOY): The lactating females and FYOY Washington, and Cass Counties (Fig. 8), signif- described above represent new reproductive icantly expanding the known reproductive range records for Merrick County. of L. borealis in Nebraska. Dixon County (1 lactating female, 19 FYOY): Cherry County (15 FYOY): 1 FYOY male re- The lactating female and FYOY reported above leased 28 July 2000 (Minnechaduza Creek, 1.35 represent new reproductive records for Dixon miles N, 0.9 miles E Valentine), 6 FYOY females County. and 5 FYOY males released 31 July 2000 Washington County (1 lactating female, 1 (Minnechaduza Creek, 1 mile N Valentine; 1 FYOY): 1 lactating female released 30 May adult male L. borealis was collected this night, 1991, and 1 FYOY released 23 July 1992 (both RAB 4966), and 3 FYOY females released 25 from Rock Creek, 3.9 miles S, 3.7 miles E Fort July 2001 (Fort Niobrara National Wildlife Calhoun). Refuge, 2.8 miles N, 5.8 miles E Valentine). Cass County (15 FYOY): 1 FYOY male and Keya Paha County (1 lactating female): 1 lac- 1 FYOY female released 23 July 1995, and 1 tating female released 27 July 1993 (East Middle FYOY female collected, 6 FYOY females and 4 Creek, 15.9 miles N, 0.2 miles E Johnstown). FYOY males released 29 July 1995 (RAB 3272, Brown County (6 FYOY): 3 FYOY males all from pond just S of Hidden Canyon Road, and 3 FYOY females released 6 August 1998 1.9 miles S, 0.6 miles E Plattsmouth), and 2 (Keller State Recreation Area, 8.5 miles N, 4.1 FYOY females released 6 August 1995 (gravel miles E Ainsworth). road, 1.8 miles S, 0.8 miles E Plattsmouth). Boyd County (1 lactating female, 3 FYOY): TIMING OF REPRODUCTIVE ACTIVITY.—Dur- The lactating female and flying-young described ing this study 9 lactating female L. borealis above represent new reproductive records for were captured during 8 nights of netting, 30 Boyd County. May–27 July (these numbers include 2 lactat- Knox County (12 FYOY): 2 FYOY females ing females captured in Lancaster County that released 21 July 2001 (creek, 6.5 miles N, 5.4 are not reported above because reproduction miles W Verdigre), 1 FYOY female collected, 3 is known from this county). These dates extend FYOY females and 6 FYOY males released 22 known dates of lactation in this species in July 2001 (RAB 5084, Schindler Creek, 5.7 Nebraska; previously known dates of lactating miles N, 3.5 miles W Verdigre). L. borealis are 14 June–24 July (Czaplewski et 2004] NEW RECORDS OF BATS OF NEBRASKA 243 al. 1979). Lactating eastern red bats have been miles N, 2.6 miles E Hay Springs), 1 FYOY caught as late as 20 August in the Black Hills male released 14 July 1998 (Beaver Creek, 7.3 of South Dakota (Jones et al. 1983). Addition- miles N, 1.4 miles W Hay Springs), 1 lactating ally, flying-young were caught 13 July–6 August female and 1 FYOY male released 17 July during this study; 75 FYOY were caught dur- 1998 (Larrabee Creek, 13.4 miles N, 2 miles ing 16 nights of netting (these numbers in- W Rushville), 1 FYOY male collected 10 August clude 3 flying-young captured in Lancaster 1998 (UNSM 26,037, Larrabee Creek, 14.2 County that are not reported above because miles N, 2.5 miles W Rushville), 2 females col- reproduction is known from this county). These lected 11 August 1998 (RAB 4313–4314, Beaver dates extend the known capture dates of fly- Creek, 7.8 miles N, 1.7 miles W Hay Springs), ing-young L. borealis in Nebraska; previous 5 FYOY females and 1 FYOY male released, dates of FYOY spanned 10 August–5 Septem- and 1 adult male collected 13 August 1998 ber (Geluso et al. 2004). (RAB 4320, Patton Creek, 17.1 miles N, 2.75 PRESENCE OF ADULT MALES IN SUMMER.— miles W Rushville), 1 adult male released 4 Jones et al. (1983:87) noted the “paucity of August 2000 (Larrabee Creek, 14.1 miles N, adult males in Plains states in summer,” sug- 2.5 miles W Rushville), 1 adult female and 1 gesting that most males spend summer else- adult male collected, 1 adult female, 9 adult where. During this study 16 adult male L. males, 3 FYOY females, 1 FYOY male, and 3 borealis were caught during 10 nights of net- female age unknown released 5 August 2000 ting in summer at sites across Nebraska (Dawes, (RAB 4986 and 4988, Patton Creek, 17.2 miles Sheridan, Cherry, Sherman, Dixon, Lancaster, N, 3.2 miles W Rushville), 1 lactating female, Cass, and Richardson Counties). Dates of these 1 FYOY female, 1 adult female, and 3 adult captures included 1, 12, 21, 25, 29, and 31 July males released 29 July 2001 (Patton Creek, and 1, 3, 5, and 6 August. Two of these males 17.1 miles N, 2.75 miles W Rushville), and 1 were collected; RAB 4820 was collected 1 July adult male, 1 adult female, 1 FYOY female, and 1999 (Dawes County, Big Bordeaux Creek, 7.8 1 female age unknown released 30 July 2001 miles S, 3.5 miles E Chadron), and RAB 4966 (Patton Creek, 17.2 miles N, 3.2 miles W was collected 31 July 2000 (Cherry County, Rushville). Minnechaduza Creek, 1 mile N Valentine). Cherry County (3): 1 FYOY male released Although adult male L. borealis were present 28 July 2000 (Minnechaduza Creek, 1.35 miles at sites across the state during summer, they N, 0.9 miles E Valentine), 1 FYOY male released were outnumbered by adult females; 42 adult 31 July 2000 (Minnechaduza Creek, 1 mile N females were captured during this same period. Valentine), and 1 female unknown age released SEASONAL RECORDS.—Eastern red bats were 25 July 2001 (Fort Niobrara National Wildlife caught 21 May–11 September during this Refuge, 2.8 miles N, 5.8 miles E Valentine). study; 145 L. borealis were caught during 38 Boyd County (8): 4 males and 4 females re- nights of netting (not all reported above). These leased 23 July 2001 (age not checked, Beaver dates are within those reported for this species Creek, 1.6 miles E Spencer). in Nebraska (26 April–1 November; Jones Knox County (2): 1 FYOY male and 1 male 1964, Geluso et al. 2004). age unknown collected 21 July 2001 (RAB 5085–5086, Schindler Creek, 5.7 miles N, 3.5 Lasiurus cinereus miles W Verdigre). (hoary bat) Merrick County (2): 1 FYOY male released Like Lasiurus borealis, L. cinereus occurs 9 July 1996, and 1 adult male collected 13 July statewide, but captures have not been reported 1999 (RAB 4854, roughly 3 miles S Chapman). from many counties (Fig. 9). Dixon County (9): 1 female adult, 1 FYOY GEOGRAPHIC RECORDS.—New records are female, and 1 female age unknown released 19 presented from Sheridan, Cherry, Boyd, Knox, July 2001 (Ponca State Park, 2.9 miles N, 0.3 Merrick, Dixon, and Cass Counties (Fig. 9). miles W Ponca), and 1 FYOY female and 1 These specimens fill in some distributional FYOY male collected, 1 adult male, 1 post-lac- gaps for L. cinereus, especially in northern tating female, 1 FYOY female, and 1 female Nebraska. age unknown released 20 July 2001 (RAB 5079– Sheridan County (44): 1 lactating female 5080, Ponca State Park, 2.5 miles N, 0.6 miles released 13 July 1998 (White Clay Creek, 8.7 W Ponca). 244 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Sioux Dawes Cherry Keya P aha Boyd

Cedar Holt Brown Rock

Knox Dakota B ox Butte Antelope Pierce Dixon Wayne Thurston

n g Sheridan Grant Madison Stanto Cumin Hooker Thomas Blaine Loup Garfield Wheeler Burt Morrill Garden Boone Scotts Bluff ge Platte Colfax Dod Arthur McPherson Logan Custer Valley Greeley Washington

Banner ce Cheye Nan as Kimball nne Saunders Dougl Keith Lincoln Sherman Howard Polk Merrick Deuel Sarpy Butler ard Lancaster Dawson Buffalo Hall York Sew Cass Perkins Hamilton e 50 km Oto Chase Hayes Gosper Adams Fillmore Saline 0 Phelps Kearney Nemaha 50 Miles Gage Johnson

Frontier Clay son Dund bster Nuckolls Thayer Jeffer dson Figure 9. y Hitchcock Red W illow Furnas Harlan Franklin We Pawnee Richar Lasiurus cinereus

Fig. 9. New records of Lasiurus cinereus. Species occurs statewide. Open symbols are previously published records; closed symbols are new records presented in this paper. Circles are geographic records; triangles are reproductive records (triangles also indicate new geographic records in some cases; see text).

Cass County (2): 1 adult male released 23 Knox County (1 FYOY): The flying-young July 1995, and 1 FYOY female collected 29 described above represents a new reproduc- July 1995 (UNSM 26,039, pond just south of tive record for Knox County. Hidden Canyon Road, 1.9 miles S, 0.6 miles E Merrick County (1 FYOY): The flying-young Plattsmouth). described above represents a new reproduc- REPRODUCTIVE RECORDS.—Although L. cine- tive record for Merrick County. reus likely breeds throughout the state, breed- Dixon County (1 post-lactating female, 4 ing records have been reported only from FYOY): The post-lactating female and flying- Sioux, Buffalo, Lancaster, Douglas, and Sarpy young described above represent new repro- Counties (Czaplewski et al. 1979, Geluso et al. ductive records for Dixon County. 2004). New reproductive records are pre- Cass County (1 FYOY): The flying-young sented here from Dawes, Sheridan, Cherry, described above represents a new reproduc- Keya Paha, Knox, Merrick, Dixon, and Cass tive record for Cass County. Counties (Fig. 9). These records significantly TIMING OF REPRODUCTIVE ACTIVITY.—Dur- expand the known breeding range of L. ing this study lactating females were caught 1 cinereus in Nebraska. July–29 July; 15 lactating females were caught Dawes County (6 lactating females): 6 lac- during 7 nights of netting (this includes 2 lactating females released 1 July 1999 (collected tating females caught in Sioux County and 1 1 adult male this night, RAB 4821, Big Bor- from Lancaster County that were not reported deaux Creek, 7.8 miles S, 3.5 miles E Chadron). above because reproduction is known to occur Sheridan County (3 lactating females, 15 in those counties). These dates are within the FYOY): Lactating females and flying-young known dates of lactation by L. cinereus in described above represent new reproductive Nebraska (6 June–30 July; Czaplewski et al. records for Sheridan County. 1979). Additionally, flying-young were caught Cherry County (2 FYOY): Flying-young de- 9 July–13 August during this study; 26 were scribed above represent new reproductive rec- caught on 15 nights of netting (this includes 4 ords for Cherry County. FYOY caught in Sioux County that were not Keya Paha County (3 lactating females): 3 reported above because reproduction is known lactating females released 27 July 1993 (East to occur in Sioux County). This expands the Middle Creek, 15.9 miles N, 0.2 miles E Johns- known range of dates of capture of FYOY L. town). cinereus in Nebraska; previously known dates 2004] NEW RECORDS OF BATS OF NEBRASKA 245 range from “the last week of June” to 4 August records for N. humeralis are known from Web- (Czaplewski et al. 1979:16, Geluso et al. 2004). ster, Merrick, Butler, Lancaster, Johnson, Paw- PRESENCE OF ADULT MALES DURING SUM- nee, and Sarpy Counties (Jones 1964, Kunz MER.—According to Jones et al. (1983), adult 1965, Czaplewski et al. 1979, Benedict et al. males of L. cinereus are absent from Nebraska 2000, Geluso et al. 2004). New reproductive during summer except in the Pine Ridge and records are presented here from Knox, Dixon, Wildcat Hills; remaining areas are inhabited and Cass Counties (Fig. 1). These new records only by females and young at this time. Con- expand the known breeding distribution of N. trary to this hypothesis, adult male hoary bats humeralis, especially in northern Nebraska. were caught during summer on 4 occasions Knox County (1 lactating female, 13 FYOY): during this study at sites not near the Pine The lactating female and flying-young reported Ridge or Wildcat Hills (8 adult females were above represent new reproductive records for captured at these same sites during this time). Knox County. On 9 July 1991 an adult male was collected in Dixon County (8 FYOY): 1 FYOY male col- Lincoln County (UNSM 18,805, 2.5 miles N, lected and 2 FYOY males released 19 July 0.3 miles W Hershey). On 23 July 1995 an adult 2001 (RAB 5077, Ponca State Park, 2.9 miles male was released in Cass County (described N, 0.3 miles W Ponca), and 1 FYOY male and in geographic records). On 13 July 1999 an 4 FYOY females released 20 July 2001 (Ponca adult male was collected in Merrick County State Park, 2.5 miles N, 0.6 miles W Ponca). (described in geographic records), and on 20 Cass County (1 post-lactating female, 1 July 2001 an adult male was released in Dixon FYOY): 1 post-lactating female and 1 FYOY County (described in geographic records). collected 29 July 1995 (RAB 3270, 3273, pond SEASONAL RECORDS.—During this study 95 just south of Hidden Canyon Road, 1.9 miles hoary bats were caught during 30 nights of S, 0.6 miles E Plattsmouth). netting (not all reported above), 1 July–6 Sep- TIMING OF REPRODUCTIVE ACTIVITY.—Dur- tember. These dates are within those known ing this study lactating female N. humeralis for activity of this migratory species in Nebraska were caught 9 July–22 July; 17 lactating females (“May”–4 October; Czaplewski et al. 1979:15, were caught during 6 nights of netting (this Geluso et al. 2004). includes 15 lactating females caught in Lan- caster County that are not reported above be- Nycticeius humeralis cause reproductive records are known from (evening bat) this county, and 2 females from Merrick County Nycticeius humeralis is thought to occupy reported in Benedict et al. 2000). These dates southeastern Nebraska, extending north to are within those reported for lactating evening Dixon County and west to at least Webster bats from Nebraska (16 June–24 July; Kunz County (Fig. 1). Many records of this species 1965, Geluso et al. 2004). Likewise, 51 flying- have been collected recently; Jones (1964) young were caught 9 July–7 September dur- knew of only 4 specimens, all from a site in ing this study in 13 nights of netting (this Butler County. Adult males have not been includes 26 FYOY caught in Lancaster County captured in Nebraska, and none are reported that are not reported above because reproduc- in this paper. tive records are known from this county and 3 GEOGRAPHIC RECORDS.—One new record FYOY caught in Merrick County reported in presented from Knox County (Fig. 1) was col- Benedict et al. 2000). These dates extend the lected 72 miles west of the nearest known cap- known range of time when FYOY can be caught ture of this species (Benedict et al. 2000). Given in Nebraska from the previous range of 30 June– the apparently suitable habitat available, Nyc- 10 August (Czaplewski et al. 1979, Geluso et ticeius likely extends west along the Niobrara al. 2004). River at least into Boyd and Holt Counties. SEASONAL RECORDS.—During this study Knox County (16): 1 FYOY female collected, 151 N. humeralis were caught 9 May–1 Octo- 7 FYOY females, 5 FYOY males, 1 lactating fe- ber during 26 nights of netting (not all re- male, 1 adult female, and 1 post-lactating female ported above). The latest capture during this released 22 July 2001 (RAB 5083, Schindler study consisted of 1 male collected and 2 Creek, 5.7 miles N, 3.5 miles W Verdigre). females released in Lancaster County on 1 REPRODUCTIVE RECORDS.—Reproductive October 1996 (UNSM 25,282, Salt Creek, 8.15 246 WESTERN NORTH AMERICAN NATURALIST [Volume 64 miles S, 1.35 miles E Lincoln). This extends the butions of bats in Nebraska. In this paper 888 known dates of activity in the evening bat in bat specimens were examined, including all Nebraska; previously known dates of capture specimens reported in Jones (1964). How- spanned 10 May–21 September (Czaplewski et ever, when E. fuscus, L. borealis, and L. cinereus, al. 1979, Geluso et al. 2004). and bats collected from the Cass and Sarpy County mines are excluded, the authors of this DISCUSSION paper examined only 196 specimens of the remaining 9 species collected throughout the New geographic, reproductive, and sea- remainder of the state. Given the small sample sonal records are presented in this paper for sizes and limited geographic areas represented 11 of 13 species of bats known from Nebraska. in earlier publications examining bats in Nebra- The 2 species for which no new records are ska, additional fieldwork will inevitably turn reported, Tadarida brasiliensis and Corynorhi- up new records. nus townsendii, are vagrants that do not occur The 2nd factor explaining some records re- in the state on a regular basis (Czaplewski et al. ported in this paper is expanding geographic 1979, Genoways et al. 2000). The large number distributions. To recognize an expanding geo- of new records presented here is the result of graphic distribution, old records indicating the 2 factors. First, the majority of Nebraska coun- absence of the species of interest must exist ties have not been studied by mammalogists. from a location where a new record is cap- Second, several species inhabiting the state tured. Unfortunately, the limited sampling con- are expanding in geographic distribution. ducted in Nebraska in earlier parts of the 20th The primary publication describing mam- century makes it difficult to distinguish range mals in Nebraska, written by J.K. Jones, was expansion from populations that were unknown published in 1964. Although Jones used all because of lack of sampling. specimens available from museums across the Myotis septentrionalis, Pipistrellus subflavus, nation, the number of bats he examined from Eptesicus fuscus, Lasiurus borealis, and Nycti- Nebraska was not large. Jones based his pre- ceius humeralis appear to be expanding in dicted distributions on 465 specimens of bats, geographic distribution in parts of the Great although he also cited literature records for 5 Plains in response to increased forestation and construction of buildings and other artificial species. This relatively small number of speci- roost sites (Sparks and Choate 1996, Benedict mens is partly attributable to the lack of effec- et al. 2000). I believe the new geographic rec- tive trapping techniques for bats that existed ords of M. septentrionalis presented here are early in the 20th century; mist nets and bat due to range expansion because the new spec- traps were not widely used for bats until the imens were captured at a site that has been 1950s or 1960s. Most early specimens of bats studied in the past. I captured M. septentrion- were caught in insect nets, shot, or collected alis each of the 7 nights I netted along Min- by hand from buildings or mines. Of 465 spec- nechaduza Creek in Cherry County (records imens examined by Jones (1964), 115 were above and Benedict et al. 2000), but none collected from 3 mines along a 10-mile stretch were caught when other bats were collected of the Platte River in Cass and Sarpy Coun- over this same creek in the 1970s (specimens ties. Another 272 specimens examined were reported in Czaplewski et al. 1979). Addition- Eptesicus fuscus, Lasiurus borealis, or L. cine- ally, Pipistrellus subflavus reported here from reus, the most common and widespread species Greeley County likely are due to range expan- in the state. Therefore, when the 3 most com- sion given that mines were not present in this mon species and bats collected from these area 120 years ago, and this species requires geographically adjacent mines are excluded, mines, caves, or similar structures for hiberna- Jones examined only 78 specimens of bats; tion (Fujita and Kunz 1984). Most of the re- these specimens, representing 9 species, were maining new records presented here represent collected over the remaining 76,800 square specimens collected from areas where no field- miles of Nebraska. Given these small numbers, work has been conducted before. Therefore, the accuracy of Jones’s predicted distributions whether these records represent overlooked is truly impressive. A later paper by Czaplew- populations or range expansions cannot be ski et al. (1979) reexamined geographic distri- determined with certainty. 2004] NEW RECORDS OF BATS OF NEBRASKA 247

Importance of Mines thank Carl and Shirley Benedict for their sup- in Eastern Nebraska port and help in the field. I also thank people who assisted with fieldwork including V. Ashe, Mines located along the Platte River and R. Auerbach, J. Beddick, B. Bishop, S. Brant, Weeping Water Creek in Sarpy and Cass Coun- A. Burns, C. Deforest, L. Essig, K. Geluso, A. ties have been known as important hibernac- Goudy, M. Harrison, R. Hart, J. Huebschmann, ula for bats that are otherwise uncommon in J. Ivey, M. Jameson, Q. Kavan, M. Kennedy, B. eastern Nebraska, especially Myotis lucifugus Perry, Z. Roehrs, C. Rowe, and E. White. For and Pipistrellus subflavus (Jones 1964, Czaplew- support and advice, I thank H. Cones, J. ski et al. 1979). Unfortunately, these mines are Druecker, A. Fox, P. Freeman, K.N. Geluso, H. being closed or otherwise modified, and their Genoways, J. Grimes, T. Labedz, and G. Webb. value for hibernating bats is diminishing. The I also thank landowners who granted access to mine from which many specimens examined their land, especially the Brownlows, L. Thomas, by Jones (1964) and Czaplewski et al. (1979) T. Rose, V. Zoucha, and the Happy Jack Mine were collected, described in these publications Association. I also thank Mike Fritz and other as 0.5–1 mile W Meadow, was sealed shut in the personnel of the Nebraska Game and Parks 1980s. At one time this mine contained many Commission (especially from Ash Hollow State bats; miners claimed it had the “largest con- Historical Park, Ponca State Park, and Valen- centration north of Carlsbad, New Mexico” tine Fish Hatchery), the City of Valentine, the (Burchett and Reed 1967:53). City of Lincoln Parks and Recreation, and Fort Likewise, a mine I netted several times Niobrara National Wildlife Refuge. Lastly, I (described above as 3 miles N, 8.9 miles W thank K.N. Geluso and 2 anonymous review- Plattsmouth) was substantially modified by the ers for comments that improved this paper. landowner in June 1996. His modifications involved placing a gated steel culvert in the LITERATURE CITED mine entrance and then closing the remainder of the opening with soil. The culvert allowed BENEDICT, R.A., H.H. GENOWAYS, AND P. W. F REEMAN. 2000. bats to pass but prevented access by humans. Shifting distributional patterns of mammals in Nebra- When I netted the mine in August 2000, bats ska. Transactions of the Nebraska Academy of Sci- were using the culverts as designed, but the ences 26:55–84. BURCHETT, R.R., AND E.C. REED. 1967. Centennial guide- impact of these modifications could not be de- book to the geology of southeastern Nebraska. Univer- termined because data were lacking from the sity of Nebraska Conservation and Survey Division, mine prior to the addition of the culverts. Fur- Lincoln, NE. 83 pp. thermore, the mine changed ownership dur- CZAPLEWSKI, N.J., J.P. FARNEY, J.K. JONES, JR., AND J.D. DRUECKER. 1979. Synopsis of bats of Nebraska. ing the late 1990s, and the new owner is de- Occasional Papers, The Museum, Texas Tech Univer- veloping the surrounding land into residential sity 61:1–24. acreages. Whether the new landowner will tol- FUJITA, M.S, AND T.H. KUNZ. 1984. Pipistrellus subflavus. erate a mine and the bats inhabiting it, while Mammalian Species 228:1–6. attempting to attract buyers, is questionable. GELUSO, K.N., R.A. BENEDICT, AND F. K OCK. 2004. Seasonal activity and reproduction in bats of east-central Use of mines by bats in eastern Nebraska Nebraska. Transactions of the Nebraska Academy of should be examined in detail. To my knowledge, Sciences: In press. the large mines located in and around Weep- GENOWAYS, H.H., P.W. FREEMAN, AND C. GRELL. 2000. ing Water have never been netted. I have seen Extralimital records of the Mexican free-tailed bat (Tadarida brasiliensis mexicana) in the central United bats in these mines, but the degree of use is States and their biological significance. Transactions difficult to determine because most bats are of the Nebraska Academy of Sciences 26:85–96. hidden in crevices in the rock. All of these JONES, J.K., JR. 1964. Distribution and taxonomy of mam- mines likely represent important sites for bats mals of Nebraska. Publications of the Museum of in eastern Nebraska and should be a conserva- Natural History, University of Kansas 16:1–356. JONES, J.K., JR., D.M. ARMSTRONG, R.S. HOFFMANN, AND tion priority in the state. C. JONES. 1983. Mammals of the Northern Great Plains. University of Nebraska Press, Lincoln, NE. ACKNOWLEDGMENTS 375 pp. KUNZ, T.H. 1965. Notes on some Nebraska bats. Transac- I thank my wife, Mary, and daughters, Sarah tions of the Kansas Academy of Science 68:201–203. SPARKS, D.W., AND J.R. CHOATE. 1995. New distributional and Emily, for their understanding and the records for mammals in Kansas. Prairie Naturalist many bats they removed from mist nets. I 27:185–192. 248 WESTERN NORTH AMERICAN NATURALIST [Volume 64

VAN ZYLL DE YONG, C.G. 1979. Distribution and system- WILSON, D.E., AND S. RUFF, EDITORS. 1999. The Smith- atic relationships of long-eared Myotis in western sonian book of North American mammals. Smithson- Canada. Canadian Journal of Zoology 57:987–994. ian Institution Press, Washington, DC. 750 pp. ______. 1984. Taxonomic relationships of Nearctic small- footed bats of the Myotis leibii group (Chiroptera: Received 22 August 2002 Vespertilionidae). Canadian Journal of Zoology 62: Accepted 27 May 2003 2519–2526. Western North American Naturalist 64(2), ©2004, pp. 249–256

FEEDING BEHAVIOR AND PERFORMANCE OF A RABBITBRUSH LEAF-BEETLE (TRIRHABDA LEWISII) FEEDING ON CHRYSOTHAMNUS NAUSEOSUS REGROWTH AFTER FIRE

Ann L. Herzig1,2 and Cynthia Skema1

ABSTRACT.—Fire often positively affects the growth and nutrient content of plants regrowing after a burn. These changes have been associated with preferential feeding by herbivores in burned areas. In this study in southeastern Wyoming, Chrysothamnus nauseosus Pursh (rubber rabbitbrush) regrowing after a fire produced new shoots with a distinct growth form. Shoots were longer than those on unburned control sites and had longer leaves with longer inter- nodes between leaves. We conducted feeding trials to detect whether C. nauseosus shoots regrowing after fire were nutritionally superior to shoots from unburned plants for the specialist leaf beetle, Trirhabda lewisii Crotch (Coleoptera: Chrysomelidae). We also measured C:N ratios and nitrogen and water contents of leaves from burned and unburned plants. Trirhabda lewisii adults preferred shoots from burned plants when given a choice. The beetles ate similar amounts of burned and unburned plants when fed only a single type. Females that were fed either burned or unburned plants did not differ in number of eggs laid. Chemical analyses revealed no significant differences in nitrogen or water content of leaves from burned versus unburned plants. Carbon-to-nitrogen ratio of burned plants was marginally lower compared with unburned plants. In contrast to previous studies, which suggest that herbivore attraction to burned areas leads to enhanced performance, our study shows that performance is not necessarily enhanced after fire.

Key words: Trirhabda lewisii, Chrysothamnus nauseosus, fire, herbivory, prescribed burn, leaf nutritional quality.

Fire is a catastrophic disturbance that causes al. 1998), and lepidopterans (Negron-Ortiz and changes in the physical environment and in Gorchov 2000). Researchers have suggested community composition. In general, these that the attractiveness of plant growth in burned changes can lead to enhanced productivity areas is due to more succulent or more tender and vigorous plant growth (i.e., relatively rapid plant tissue (Leege 1968, Vieira et al. 1996), growth that results in larger-sized plant parts) more accessible new growth (Miller and Wat- following a fire (Hadley and Kieckhefer 1963, son 1973, Carlson et al. 1993), and an increase Daubenmire 1968, Old 1969, Christensen and in nutritional value, particularly higher nitro- Muller 1975, Lyon et al. 1978, Rundel and gen levels (Smith and Owensby 1972, Miller Parsons 1980, Boerner 1982, Knapp 1985, and Watson 1973, Carlson et al. 1993, Negron- Romo et al. 1993, Whelan 1995, Throop and Ortiz and Gorchov 2000). Nitrogen and water Fay 1999). Enhanced plant growth can have are 2 key plant components affecting insect cascading effects in the community. Many herbivore performance (Mattson and Scriber studies have documented selective feeding by 1987). More vigorous plant growth, in general, herbivores in previously burned areas (Dauben- is preferred by many insect herbivores and mire 1968). Herbivores that show this behav- can enhance survival of insects that feed with- ior are a large and varied group, including ver- in plant tissue, such as leaf gallers (Price 1991). tebrates such as elk (Leege 1968), cattle (Smith In this investigation we observed Chryso- and Owensby 1972), sheep, deer, grouse (Miller thamnus nauseosus Pursh (Compositae), rub- and Watson 1973), waterfowl, muskrat (Smith ber rabbitbrush, producing shoots that had a and Kadlec 1985), and bison (Vinton et al. 1993); strikingly different morphology following a and insects, such as grasshoppers (Stein et al. prescribed burn in southeastern Wyoming. 1992, Porter and Redak 1997), gall midges Chrysothamnus nauseosus is a deciduous shrub (Vieira et al. 1996), homopterans (Cancelado most commonly found in intermountain desert and Yonke 1970), hemipterans (Steinbauer et scrub; it is often associated with Artemisia

1Department of Biology, Bryn Mawr College, Bryn Mawr, PA 19010. 2Corresponding author. Present address: 147 Weston Rd., Berkshire, NY 13736.

249 250 WESTERN NORTH AMERICAN NATURALIST [Volume 64 tridentata Nutt., big sagebrush (Flora of North tion. Chrysothamnus nauseosus at the site grows America Editorial Committee 1993). This low in a band at the edge of the riparian zone, shrub flowers in a capitulum of yellow florets extending as far as 50 m up the adjacent hill- from August through October. Chrysothamnus side. The area we sampled covers approxi- nauseosus ranges from southern British Colum- mately 2 ha. Chrysothamnus nauseosus is the bia to Saskatchewan and south to California, dominant plant in this zone. Vegetation in this Texas, and New Mexico and is commonly found zone, a mix of grass and shrubs, is described growing in disturbed areas, such as along road- as sagebrush steppe (Knight 1994). Fire and sides and around prairie dog mounds (Britton drought are common disturbances in sagebrush 1970). steppe ecosystems. Water is most available to We investigated whether the distinctive, plants in the spring, at the time of snowmelt, post-fire regrowth of C. nauseosus was nutri- and becomes limiting by mid- to late summer tionally superior for a specialist rabbitbrush- (Knight 1994). Chrysothamnus nauseosus in this feeding beetle, Trirhabda lewisii Crotch (Cole- area typically initiates new growth in late May. optera: Chrysomelidae). Trirhabda lewisii spe- The growing season generally ends in early cializes on C. nauseosus and C. viscidiflorus October. (Hogue 1970), with both larvae and adults feed- In March 1997 this area was the site of a ing on foliage. Trirhabda lewisii is univoltine, prescribed burn that left a mosaic of burned overwintering in the egg stage. Larvae hatch and unburned areas. At our site a footpath that in early spring (late May at our study sites) follows the creek and meanders through the and begin feeding on newly expanding leaves. zone of C. nauseosus separated burned and un- Larvae develop through 3 instars and then burned sections. The other common shrub in pupate in the upper layer of soil for about 2 the area, A. tridentata, was killed by the fire. weeks in early summer. Adults emerge in late Chrysothamnus nauseous shrubs were burned June or early July, mate, feed, and, throughout to the ground in the burned area, but by the the remainder of the summer, lay eggs in the next growing season, when we conducted our soil at the base of the host plant. Adults die study, new sprouts were growing from the with the onset of cold weather in early autumn. base of their charred stumps. The ground was Beetles in the genus Trirhabda are notorious blackened during the burn, but the fire was for reaching tremendously high population not so intense as to consume all plant litter. levels at which they can cause complete defo- Some charred litter remained. In repeated sur- liation and even death of their host plants veys at our site early in the season, we found (Hogue 1970). Trirhabda beetles disperse as no T. lewisii larvae in the burned area. young adults (Messina 1982, Herzig 1995). During this period, beetles could colonize a METHODS burned area to feed on resprouting foliage. Plant Characteristics Therefore, feeding trials in this study were conducted on adult beetles in July–August fol- Plant morphology was quantified to describe lowing the fire, at the time new adults started the long-leafed, elongated stems of C. nauseo- to appear in the field. We conducted feeding sus that had regenerated after the burn. We trials to determine whether fire resulted in cut shoots at the base, where they intersected foliage that was preferred by T. lewisii, whether the stem, every other day (27 July–4 August) beetles ate more foliage from burned or un- from a total of at least 50 different C. nauseo- burned plants to compensate for possible sus plants, 25 burned and 25 unburned. We nutritional differences, and whether beetle sampled discrete areas within our study area fecundity increased when fed foliage from on each sampling occasion to ensure that we burned plants. selected shoots from different plants each time. We sampled 1 or 2 shoots from each plant for STUDY SITE a total of 100 shoots. Shoots of any one plant are presumably more similar than shoots from Our field site was along French Creek in different plants. To control for this plant effect the Sheep Mountain region of the Medicine in our data, we took the most conservative Bow National Forest in southeastern Wyoming, approach we could by eliminating half of our 40 km southwest of Laramie at 2350 m eleva- sample. We could not eliminate the shoots that 2004] BEETLE HERBIVORY AFTER FIRE 251 we knew came from the same plants because 2 plant types to be a lower-quality food and these were not kept separate at the time of thus compensated by eating more of this plant collection. We arranged the shoots in rank order type, and (3) fecundity trials to measure egg for each of the 3 morphological measurements production of females fed the 2 plant types. (leaf density, leaf length, shoot length) and All feeding trials were conducted in the labo- eliminated every other shoot from our sample ratory using plant cuttings. To keep foliage as before analysis. In this way we reduced the natural as possible, C. nauseosus cuttings for sample size to reflect the minimum number of the experiments were clipped early in the plants sampled and increased the variability in morning and kept in water and shade while our sample by eliminating the most similar being transported immediately back to the lab. measurements. Leaf density was measured by Beetles were given fresh cuttings every 48 counting all leaves on a shoot and dividing by hours, each day’s cuttings having been clipped the length of the shoot. Leaf length was esti- from areas of burned and unburned land adja- mated by categorizing leaves into length inter- cent to each other to minimize any effects of vals to the nearest centimeter. We conducted t microhabitat. To avoid changes in plant chem- tests to compare shoot length, leaf density, and istry that might have been induced by re- mean leaf length of previously burned and peated clippings, each cutting was taken from unburned plants. a new, unclipped plant, a single cutting per To measure change in nutrient composition plant. During the trials plant cuttings were and water content of the foliage after the fire, kept in florist’s water picks to help maintain we measured carbon, nitrogen, and water con- turgor pressure and thus the structural integ- tents of the leaves from previously burned and rity and quality of the food material. unburned plants. On 29 July we haphazardly Beetles were identified using the key in selected and cut 1 sprout from 10 burned and Hogue (1970). Beetles used in the feeding trials 10 unburned C. nauseosus plants. All leaves were collected from a population of C. nauseo- from each cutting were stripped from the stem sus 1.5 km south of Woods Landing at an ele- by hand, weighed, and then freeze-dried until vation of approximately 2320 m. This area, reaching a constant weight (approximately 24 approximately 5 km from the site of the pre- hours). The proportion of water in the leaves scribed burn, had not been recently burned. was measured as the difference between wet We transported the beetles back to the lab in and dry weights divided by wet weight. After 9-dram plastic vials and placed them in 1-L, freeze-drying, the leaves were pulverized us- clear plastic containers with mesh lids for the ing a mortar and pestle above a pool of liquid experimental trials. They were maintained at nitrogen, which cooled the leaves to brittle- 25°C under ambient light conditions. Beetles ness so they could be pulverized effectively, were placed in their experimental arenas on maximizing homogeneity within each cutting the same day they were collected from the sample. Carbon and nitrogen contents (per- field, except for those females used in prefer- centage of dry weight) were measured using ence trials; these were starved for 20–24 hours an elemental analyzer. A t test was conducted prior to testing. to test for differences in water content between To determine whether T. lewisii preferred the 2 treatments. Because nitrogen levels were leaves from previously burned or unburned expected to rise after fire, we conducted 1-tailed plants, we conducted paired-choice tests (be- t tests to detect differences in nitrogen con- tween 30 July and 7 August), replicated 15 tent and C:N ratio. times. A different, single T. lewisii female was used for each test and was housed with 2 Beetle Feeding Trials sprouts, 1 of each plant type, for 48 hours. To measure differences in T. lewisii feeding Paired sprouts contained approximately the behavior and fecundity on previously burned same number of leaves. The approximate leaf plants compared with unburned plants, we con- area of the sprouts provided to the beetles was ducted 3 types of feeding trials: (1) preference estimated prior to consumption by multiplying trials to determine whether beetles, when the length and width of each leaf and sum- given a choice, preferred shoots from previ- ming these values for all leaves on a stem. ously burned or unburned plants, (2) compen- This is a valid estimate because the long, nar- sation trials to see if beetles perceived 1 of the row leaves of C. nauseosus are approximately 252 WESTERN NORTH AMERICAN NATURALIST [Volume 64 rectangular in shape. Lengths and widths of the unburned treatment had 10 replicates the roughly rectangular-shaped bite marks were throughout the running time of the experi- measured to obtain the approximate leaf area ment. consumed. All measurements of leaves and bite RESULTS marks were made using vernier calipers. Beetles Plant Change after Fire were starved for 20–24 hours prior to their choice test. A 1-tailed, paired t test was con- Sprouts that regrew after the fire were very ducted to measure differences between the different in appearance from sprouts from amount of leaf area consumed of each sprout unburned plants. Shoots were much longer on type. the previously burned plants than on the To test whether beetles ate different amounts unburned plants (mean difference = 8.71 cm, of C. nauseosus from burned or unburned plants t = 7.32, df = 48, P < 0.001; Fig. 1A). Leaf to compensate for possible differences in nutritional quality, we placed 10 T. lewisii females in individual containers; 5 were fed sprouts from unburned plants and 5 were fed sprouts from previously burned plants for a period of 11 days (27 July to 6 August). Once the beetles had fed on the cuttings for 48 hours, old cuttings were removed and replaced with fresh sprouts. The amount of foliage consumed by the beetles was measured as in the preference experiment described above. We used the same beetle in the experiment over the entire 11 days to allow the beetle time to detect any potential nutritive differences and begin com- pensatory feeding. A t test evaluated the difference in leaf area consumed between treatment groups. Our 3rd feeding trial analyzed the effect of the 2 plant types, burned and unburned, on the fecundity of T. lewisii. We measured egg production for females fed sprouts from the 2 plant types over a 13- to 19-day interval (21 July to 8 August). Plant cuttings were replaced and eggs were removed and counted every 48 hours. For each treatment 10 groups of 4 females and 1 male (included to ensure insem- ination) were placed in individual containers. Egg production of 5 of these foursomes for each treatment was measured over 13 days and the remaining 5 of each treatment over 17 days. To measure individual female’s egg production, we placed 6 single females (each housed with 1 male) for each treatment in individual containers and measured their egg output over 19 days. To test for differences in egg output between burned and unburned treatments, t tests were conducted separately Figs. 1A–C. Shoot length (A), leaf density (B), and leaf on single females and on groups of 4 females. length (C) comparisons between shoots of unburned The escape of an entire group of 4 beetles in Chrysothamnus nauseosus and shoots from plants that were burned the previous winter. Bars show the mean the burned treatment on 5 August resulted in ± from 25 shoots 1 sx–; * indicates significant differences at only 9 replicate foursomes for that treatment; P < 0.001. 2004] BEETLE HERBIVORY AFTER FIRE 253

± TABLE 1. Mean carbon-to-nitrogen ratio, percent nitrogen, and percent water ( 1 sx–) in leaves of Chrysothamnus nauseosus sprouts from plants that were either previously burned or not affected by fire. N = 10 sprouts for each treatment. P-values for 1-tailed t tests are shown for C:N ratio and % N. P-value for 2-tailed t test is shown for % water. Leaf measurement Unburned Burned tP C:N ratio 19.2 (±0.6) 17.7 (±0.6) 1.74 0.055 % N 2.5 (±0.1) 2.6 (±0.1) –1.09 0.15 % water 69.4 (±2.4) 67.3 (±1.1) 0.76 0.45

density was significantly lower on stems of in the foliage would increase after fire, because burned C. nauseosus (mean difference = –0.37 this increase has been reported previously in leaves ⋅ cm−1 stem, t = −4.13, df = 48, P < numerous studies (Daubenmire 1968, Rundel 0.001; Fig. 1B). Leaves from burned plants and Parsons 1980, Kituku et al. 1992, Radho- were significantly longer than those from un- Toly et al. 2001). However, other studies have burned plants (mean difference = 1.49 cm, t = shown no change in foliar nitrogen levels or 7.18, df = 48, P < 0.001; Fig. 1C). mixed results (Daubenmire 1968, Carlson et al. The carbon-to-nitrogen ratio of leaves from 1993, Knight 1994, Wambolt et al. 1996). The burned C. nauseosus was marginally lower than lack of a pronounced increase in nitrogen lev- from unburned plants (P = 0.055; Table 1). els in this study could be due either to partic- Nitrogen and water contents of the leaves ularities in how C. nauseosus aquires nutrients were not significantly different between burned or to the timing of our sample. Mature C. nau- and unburned plants (Table 1). seosus plants are one of the most deeply rooted plants in shrub-dominated Great Basin Beetle Feeding Trials communities; they do not take up summer Trirhabda lewisii preferred leaves from rain, apparently lacking active roots at shallow burned C. nauseosus in the paired-choice tests depths and relying on moisture deeper in the (mean difference = 0.39 cm2, t = 1.96, df = 14, soil (Donovan and Ehleringer 1994). This may P = 0.04; Fig. 2). In the compensation trials limit their ability to take up nitrogen at the beetles ate similar amounts of sprouts from soil surface that may become available after a burned and unburned plants (mean difference fire. In addition, in contrast to other Great = 0.07 cm2, t = 0.32, df = 8, P = 0.37; Fig. 3). Basin shrub species, C. nauseosus appears Females fed burned or unburned plants did not unable to exploit nitrogen when available in differ in the number of eggs laid (singletons: short-duration pulses (Bilbrough and Caldwell mean difference = 0.03 eggs, t = 0.46, df = 10, 1997) as would occur after a burn. Alterna- P = 0.66; foursomes: mean difference = 0.03 tively, we might have found no difference in eggs, t = 0.59, df = 18, P = 0.56; Fig. 4). nitrogen levels in our sample in early August because leaf composition had changed over DISCUSSION the season. While increases in nitrogen levels in some plants can persist into the 2nd grow- Chrysothamnus nauseosus regrowth after fire ing season after a fire (e.g., Rundel and Par- was morphologically very different from that sons 1980, Hobbs and Schimel 1984, Redman of unburned plants. The plants produced elon- et al. 1993), other studies have shown that gated shoots with longer leaves. A profusion of changes in leaf chemistry following fire can be rapid vegetative growth with a distinctive mor- of short duration, disappearing after a few phology is commonly observed after a fire months (Knapp 1985) or gradually declining (Kituku et al. 1992, Stein et al. 1992, Romo et al. with time since the burn (Anderson and 1993, Vieira et al. 1996, Throop and Fay 1999, Menges 1997). Radho-Toly et al. 2001). Surprisingly, despite a Studies on other Trirhabda species have striking change in morphology after the burn, shown that the quality of host foliage can affect we found that C. nauseosus shoots from burned beetle behavior and performance. Host plant sites showed little difference in nitrogen and foliage with higher nitrogen content is pre- water content compared with shoots from un- ferred in the field by T. geminata (Wisdom burned sites. We anticipated that nitrogen levels 1985) and can increase egg output for T. 254 WESTERN NORTH AMERICAN NATURALIST [Volume 64 )/beetle/48h 2

Singletons Foursomes Amount eaten (cm

Fig. 4. Mean number of eggs laid per beetle per 48 ± hours ( 1 sx–). Open bars = beetles fed unburned shoots, solid bars = beetles fed shoots that had resprouted from Fig. 2. Mean percentage of leaf material eaten from the ± burned plants. Measurements for singletons were aver- total provided per beetle in 48 hours ( 1 sx–) when beetles aged for 6 single females over 19 days. Measurements for were presented with a shoot from an unburned C. nauseo- foursomes were averaged from 2 groups of beetles: group sus and a shoot from a previously burned plant. N = 15 1 consisted of 5 sets of 4 females over 17 days, group 2 for each treatment; * indicates P < 0.05. consisted of 5 sets of 4 females over 13 days. NS indicates P > 0.05.

Johnson et al. (1985) found that T. diducta larvae and adults compensated for lower nitrogen levels in foliage by eating more, thus

)/beetle/48h maintaining a constant daily intake of nitro- 2 gen. Trirhabda bacharidis adults prefer more tender leaves of their host plant (Krischik and Denno 1990). There could be effects of fire on T. lewisii in the field that we were unable to measure in the lab. Differences in microhabitat or plant architecture can cause a preference by an herbivore for one plant population over another Amount eaten (cm in natural conditions (Tabashnik and Slansky 1987). The texture of the landscape was more Fig. 3. Mean amount of leaf material eaten in 48 hours open after the fire, a condition that can pro- ± per beetle ( 1 sx–) when beetles were presented with mote faster development in insects (Cappuc- shoots from either previously burned or unburned C. nau- cino and Root 1992). More open stands where seosus. N = 5 for each treatment; NS indicates P > 0.05. fire-susceptible plants have been killed, such as A. tridentata at our site, might be easier to find without neighboring plants masking the canadensis (Brown and Weis 1995). The nitro- host odor, resulting in higher colonization rates gen content of foliage in these studies varied on plants after a burn. Morrow et al. (1989) by 3.4% (Wisdom and Rodriguez 1983, Wis- showed that Trirhabda canadensis adults move dom 1985) and 0.7% (Brown and Weis 1995), toward pure stands of their host plant over differences much greater than the mean dif- stands that contain a mixture of plant species. ference of 0.1% found in C. nauseosus foliage At our study site we did not observe large from burned and unburned areas in this study. numbers of beetles colonizing the burned area. 2004] BEETLE HERBIVORY AFTER FIRE 255

Although numerous studies have shown BRITTON, N.L. 1970. Illustrated flora of the northern United that vigorous growth following a fire is attrac- States and Canada. Dover Publications, New York. BROWN, D.G., AND A.E. WEIS. 1995. Direct and indirect tive to some insect herbivores (Cancelado and effects of prior grazing of goldenrod upon the per- Yonke 1970, Stein et al. 1992, Vieira et al. 1996, formance of a leaf beetle. Ecology 76:426–436. Porter and Redak 1997, Steinbauer et al. 1998, CANCELADO, R., AND T.R. YONKE. 1970. Effect of prairie Negron-Ortiz and Gorchov 2000, Radho-Toly burning on insect populations. Journal of the Kansas et al. 2001), studies that measure insect per- Entomological Society 43:274–281. CAPPUCCINO, N., AND R.B. ROOT. 1992. The significance of formance after a fire are rare and show mixed host patch edges to the colonization and develop- results. Vieira et al. (1996) found increased sur- ment of Corythucha marmorata (Hemiptera: Tingi- vival of gall midges in a burned site compared dae). Ecological Entomology 17:109–113. to an unburned site. In contrast, McCullough CARLSON, P.C., G.W. TANNER, J.M. WOOD, AND S.R. HUM- PHREY. 1993. Fire in key deer habitat improves and Kulman (1991) found lower survival of browse, prevents succession and preserves endemic jack pine budworm in burned versus clearcut herbs. Journal of Wildlife Management 57:914–928. sites. Rieske (2002) found no difference in rel- CHRISTENSEN, N.L., AND C.H. MULLER. 1975. Effects of fire ative growth rate or development time in on factors controlling plant growth in Adenostoma gyspy moth larvae fed chestnut oak seedlings chaparral. Ecological Monographs 45:29–55. DAUBENMIRE, R. 1968. Ecology of fire in grassland. Ad- from burned and unburned areas despite vances in Ecological Research 5:209–266. slightly higher foliar nitrogen levels (0.17% DONOVAN, L.A., AND J.R. EHLERINGER. 1994. Water stress higher) in seedlings from burned areas. Our and use of summer precipitation in a Great Basin study shows that despite a preference for the shrub community. Functional Ecology 8:289–297. morphologically distinct foliage of burned ENGLE, D.M., AND T.G. B IDWELL. 2001. The response of central North American prairies to seasonal fire. Jour- plants, T. lewisii fecundity did not increase nal of Range Management 54:2–10. when fed these shoots. The effects of fire on FLORA OF NORTH AMERICA EDITORIAL COMMITTEE, EDI- herbivore performance may vary depending on TORS. 1993. Flora of North America. Volume 1. Oxford the species and systems involved. Likewise, University Press, New York. HADLEY, E.B., AND B.J. KIECKHEFER. 1963. Productivity the effects of a fire on an ecosystem can vary of two prairie grasses in relation to fire frequency. depending on its severity and timing (Dauben- Ecology 44:389–395. mire 1968, Boerner 1980, Engle and Bidwell HERZIG, A.L. 1995. Effects of population density on long- 2001). The prevailing dogma that herbivore distance dispersal in the goldenrod beetle Trirhabda attraction to plant regrowth in burned areas is virgata. Ecology 76:2044–2054. HOBBS, N.T., AND D.S. SCHIMEL. 1984. Fire effects on nitro- due to changes in nutritional quality that lead gen mineralization and fixation in mountain shrub to enhanced performance for the herbivore is and grassland communities. Journal of Range Man- not well supported. agement 37:402–405. HOGUE, S.M. 1970. Biosystematics of the genus Trirhabda LeConte of America north of Mexico (Chrysomeli- ACKNOWLEDGMENTS dae: Coleoptera). Doctoral dissertation, University of Idaho, Moscow. 212 pp. We thank M.C. Witmer for his advice on JOHNSON, N.D., S.A. BRAIN, AND P.R. EHRLICH. 1985. The the chemical analyses and helpful comments role of leaf resin in the interaction between Eriodic- on the manuscript, and C. Martinez del Rio tyon californicum (Hydrophyllaceae) and its herbi- for use of his lab facilities at the University of vore, Trirhabda diducta (Chrysomelidae). Oecologia 66:106–110. Wyoming. We thank 2 anonymous reviewers KITUKU, V.M., J. POWELL, M.A. SMITH, AND R.A. OLSON. for providing useful suggestions on the manu- 1992. Increasing bitterbrush nutrient quality with script. This research was made possible by a 2,4-D, mowing, and burning in southcentral Wyo- grant from the Bryn Mawr College Under- ming. Journal of Range Management 45:488–493. graduate Research Fund. KNAPP, A.K. 1985. Effect of fire and drought on ecophysiology of Andropogon gerardii and Panicum virgatum in a tallgrass prairie. Ecology 66:1309–1320. LITERATURE CITED KNIGHT, D.H. 1994. Mountains and plains: the ecology of Wyoming landscapes. Yale University Press, New ANDERSON, R.C., AND E.S. MENGES. 1997. Effects of fire on Haven, CT. sandhill herbs: nutrients, mycorrhizae, and biomass KRISCHIK, V.A., AND R.F. DENNO. 1990. Patterns of growth, allocation. American Journal of Botany 84:938–948. reproduction, defense, and herbivory in the dioe- BILBROUGH, C.J., AND M.M. CALDWELL. 1997. Exploitation cious shrub Baccharis halimifolia (Compositae). of springtime ephemeral N pulses by six Great Basin Oecologia 83:182–190. plant species. Ecology 78:231–243. LEEGE, T.A. 1968. Prescribed burning for elk in northern BOERNER, R.E.J. 1982. Fire and nutrient cycling in tem- Idaho. Proceedings of the Tall Timber Fire Ecology perate ecosystems. BioScience 32(3):187–192 Conference 8:235–253. 256 WESTERN NORTH AMERICAN NATURALIST [Volume 64

LYON, L.J., H.S. CRAWFORD, E. CZUHAI, R.L. FREDRIKSEN, RUNDEL, P.W., AND D.J. PARSONS. 1980. Nutrient changes in R.F. HARLOW, L.J. METZ, AND H.A. PEARSON. 1978. two chaparral shrubs along a fire-induced age gradi- Effects of fire on fauna: a state of knowledge review. ent. American Journal of Botany 67:51–58. USDA Forest Service, General Technical Report SMITH, E.F., AND C.E. OWENSBY. 1972. Effects of fire on WO-6. true prairie grasslands. Proceedings of the Tall Tim- MATTSON, W.J., AND J.M. SCRIBER. 1987. Nutritional ecol- bers Fire Ecology Conference 12:9–22. ogy of insect folivores of woody plants: nitrogen, SMITH, L.M., AND J.A. KADLEC. 1985. Fire and herbivory water, fiber, and mineral considerations. Pages 105– in a great salt lake marsh. Ecology 66:259–265. 146 in F. Slansky and J.G. Rodriguez, editors, Nutri- STEIN, S.J., P.W. PRICE, W.G. ABRAHAMSON, AND C.F. SAC- tional ecology of insects, mites, spiders, and related CHI. 1992. The effect of fire on stimulating willow invertebrates. John Wiley and Sons, Inc., New York. regrowth and subsequent attack by grasshoppers MCCULLOUGH, D.G., AND H.M. KULMAN. 1991. Differences and elk. Oikos 65:190–196. in foliage quality of young jack pine (Pinus banksiana STEINBAUER, M.J., A.R. CLARKE, AND S.C. PATERSON. 1998. Lamb.) on burned and clearcut sites: effects on jack Changes in eucalypt architecture and the foraging pine budworm (Choristoneura pinus pinus Freeman). behavior and development of Amorbus obscuricornis Oecologia 87:135–145. (Hemiptera: Coreidae). Bulletin of Entomological MESSINA, F.J. 1982. Timing of dispersal and ovarian devel- Research 88:641–651. opment in goldenrod leaf beetles Trirhabda virgata TABASHNIK, B.E., AND F. S LANSKY, JR. 1987. Nutritional ecol- and T. borealis. Annals of the Entomological Society ogy of forb foliage-chewing insects. Pages 71–103 in of America 74:641–646. F. Slansky and J.G. Rodriguez, editors, Nutritional MILLER, G.R., AND A. WATSON. 1973. Some effects of fire ecology of insects, mites, spiders, and related inver- on vertebrate herbivores in the Scottish highlands. tebrates. John Wiley and Sons, Inc., New York. Proceedings of the Tall Timbers Fire Ecology Con- THROOP, H.L., AND P.A. FAY. 1999. Effects of fire, browsers ference 13:39–64. and gallers on New Jersey tea (Ceanothus herba- MORROW, P.A., D.W. TONKYN, AND R.J. GOLDBURG. 1989. ceous) growth and reproduction. American Midland Patch colonization by Trirhabda canadensis (Coleop- Naturalist 141:51–58. tera: Chrysomelidae): effects of plant species compo- VIEIRA, E.M., I. ANDRADE, AND P. W. P RICE. 1996. Fire sition and wind. Oecologia 81:43–50. effects on a Palicourea rigida (Rubiaceae) gall midge: NEGRON-ORTIZ, V., AND D.L. GORCHOV. 2000. Effects of a test of the plant vigor hypothesis. Biotropica 28: fire season and postfire herbivory on the cycad Zamia 210–217. pumila (Zamiaceae) in slash pine savanna, Everglades VINTON, M.A., D.C. HARTNETT, E.J. FINCK, AND J.M. BRIGGS. National Park, Florida. International Journal of Plant 1993. Interactive effects of fire, bison (Bison bison) Sciences 161:659–669 grazing and plant community composition in tall- OLD, S.M. 1969. Microclimate, fire and plant production grass prairie. American Midland Naturalist 129:10–18. in Illinois prairie. Ecological Monographs 39:355–384. WAMBOLT, C.L., W.W. FRAAS, AND M.R. FRISINA. 1996. Var- PORTER, E.E., AND R.A. REDAK. 1997. Diet of migratory iation in bitterbrush (Purshia tridentata Pursh) crude grasshopper (Orthoptera: Acrididae) in a California protein in southwestern Montana. Great Basin Natu- native grassland and the effect of prescribed spring ralist 56:205–210. burning. Population Ecology 26:234–240. WHELAN, R.J. 1995. The ecology of fire. Cambridge Uni- PRICE, P.W. 1991. The plant vigor hypothesis and herbi- versity Press, Cambridge, UK. vore attack. Oikos 62:244–251. WISDOM, C.S. 1985. Use of chemical variation and preda- RADHO-TOLY, S., J.D. MAJER, AND C. YATES. 2001. Impact tion as plant defenses by Encelia farinosa against a of fire on leaf nutrients, arthropod fauna and her- specialist herbivore. Journal of Chemical Ecology bivory of native and exotic eucalypts in Kings Park, 11:1553–1565. Perth, Western Australia. Australian Ecology 26: WISDOM, C.S., AND E. RODRIGUEZ. 1983. Seasonal age- 500–506. specific measurements of the sesquiterpene lactones RIESKE, L.K. 2002. Wildfire alters oak growth, foliar chem- and chromenes of Encelia farinosa. Biochemical Sys- istry, and herbivory. Forest Ecology and Manage- tematics and Ecology 11:345–352. ment 168:91–99. ROMO, J.T., P.L. GRILZ, R.E. REDMANN, AND E.A. DRIVER. Received 5 April 2002 1993. Standing crop, biomass allocation patterns and Accepted 16 July 2003 soil-plant water relations in Symphoricarpos occidentalis Hook. following autumn or spring burning. American Midland Naturalist 130:106–115. Western North American Naturalist 64(2), ©2004, pp. 257–258

DISCOVERY OF THE CENTIPEDE SCOLOPOCRYPTOPS GRACILIS WOOD IN MONTANA (SCOLOPENDROMORPHA: SCOLOPOCRYPTOPIDAE)

Rowland M. Shelley1 and Diana L. Six2

Key words: Scolopocryptops gracilis, “northern population,” Idaho, Montana, Missoula County.

The centipede Scolopocryptops gracilis Wood The specimens were collected in pitfall traps occupies 3 segregated areas in North America that were placed on a regular grid as part of a west of the Rocky Mountains (Shelley 2002): study on arthropod communities in knapweed- (1) an inverted triangularly shaped northern invaded and uninvaded savannas of the north- region in southeastern Washington, northeastern ern Rocky Mountains (Six and Ortega unpub- Oregon, and north central Idaho that extends lished data). Collection data are as follows: (1) southward to the vicinity of Boise; (2) an irreg- the adult from Petty Pasture is deposited in ularly shaped main area that ranges from the National Museum of Natural History, Smith- northern California to Lake Tahoe and south- sonian Institution, Washington, DC (NMNH); ward west of the crest of the Sierra Nevada to and (2) other specimens are housed in the 1st Ensenada, Baja California Norté, with an east- author’s institution (NCSM). ward extension through the Mojave Desert into MONTANA: Missoula Co., ca. 25 miles (40 southwestern Utah and northwestern Arizona; km) W Missoula, Petty Pasture, ca. 0.6 miles and (3) an isolated site in Salt Lake County, (0.9 km) E Petty Creek and 2.5 miles (4.0 km) Utah. The easternmost record of the “northern S Petty Creek Fishing Access (GPS X696200, population” is a site along Moose Creek in the Y5202000) [4300 feet (1311 m) elevation], 1 Selway-Bitterroot Wilderness Area, Nez Perce adult, 1 subadult, 1 juvenile, 25–26 May 1999, National Forest, approximately 25 miles (40 km) D. Six (NCSM, NMNH); and Lower Madison west of the border with Montana. In May and Gulch, 1.1 miles (1.7 km) W, 1.4 miles (2.2 km) June 1999, the 2nd author collected 2 adults, 1 S Petty Creek Fishing Access (GPS X697050, subadult, and 1 juvenile of S. gracilis near Petty Y5204000) [4400 feet (1341 m) elevation], 1 Creek fishing access, Lolo National Forest, adult, 9 June 1999, D. Six (NCSM). Missoula County, Montana, around 25 miles Both sites consist of montane savannas on (40 km) west of Missoula and 50 miles (80 km) steep slopes (average 30%) with scattered pon- northeast of Moose Creek. This is the 2nd rep- derosa pine (Pinus ponderosa Dougl. Ex Laws.; resentative of the Scolopendromorpha recorded 60% of trees), Douglas-fir [Pseudotsuga men- from the state, the 1st being Scolopendra poly- ziesii (Mirb.) Franco; 40% of trees], and shrubs morpha Wood (Scolopendridae) from Big Horn, [primarily serviceberry, Amelanchier alnifolia Rosebud, and Treasure Counties in the plains (Nutt.), and snowberry, Symphoricarpos albus of southeastern Montana (Shelley 2002). Along (L.) Blake], which are located within a matrix with the 2 sites in Whitman County, Washing- of denser Douglas-fir–dominated coniferous ton, at about the same latitude, these records forest. Understory vegetation at the sites con- form the known northern distributional limits sists of bluebunch wheatgrass [Agropyron spi- for both this population and the species as a catum (Pursh.) Scribn.] and other common whole. The distribution of the northern popu- bunchgrasses including Idaho fescue (Festuca lation is shown in Figure 1, although we can- idahoensis Elmer), Sandberg’s bluegrass (Poa not place the records from Saddleback Moun- sandbergii Vasey), and June grass [Koeleria tain, Oregon, and Idaho Pass, Idaho (Shelley macrantha (Ledeb.) Schultes]. The native forb 2002), which may lie outside this area. community is highly diverse but with major

1Research Laboratory, North Carolina State Museum of Natural Sciences, 4301 Reedy Creek Road, Raleigh, NC 27607; e-mail: rowland.shelley@ ncmail.net. 2School of Forestry, University of Montana, Missoula, MT 59812; e-mail: [email protected].

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Madison Gulch. Shelley (2002) suggests that the density of the pilosity on these append- ages represents sexual dimorphism, with females being sparsely hirsute and males possessing dense clusters of setae in a “bottlebrush” arrangement on the last 3 or 4 podomeres. The discovery of S. gracilis in Missoula County suggests that the centipede also occurs in Mineral and Ravalli Counties, adjacent counties to the west and south, respectively. Occurrence to the east in Granite and Well Counties, and to the north in Lake County seems less likely, but the centipede fauna of western Montana has been poorly sampled, and additional discoveries would not be sur- prising; conceivably, S. gracilis could range eastward to the western slope of the Rocky Mountain Front, the crest of which forms the Continental Divide. Loomis and Schmitt (1971) published copious, detailed records of millipeds from western Montana based on intensive sampling in every county west of the Divide, but they did not mention sympatric centipedes, which presumably were ignored. Modern workers must now reexamine this Fig. 1. Distribution of the northern population of Scolo- pocryptops gracilis. ALB, Alberta; BC, British Columbia; area to gather the other myriapods that occur ID, Idaho; MT, Montana; OR, Oregon; WA, Washington. in these environments.

We thank W.A. Shear, Hampden-Sydney College, for bringing this discovery to the 1st components of arrowleaf balsamroot [Balsa- author’s attention, and R.S. Zack, Washington morhiza sagittata (Pursh.) Nutt.], lupine (Lupi- State University, for advice on Idaho localities. nus spp.), yarrow [Achillea millefolium (L.)], We also thank Yvette Ortega for conducting and blue-eyed Mary (Collinsia parvifolia pitfall trapping and developing site descrip- Lindl.; Ortega unpublished data). The lower tions. Trapping efforts were funded by the Madison Gulch site is moderately invaded by Wildlife Ecology Research Unit of the Rocky the exotic pest plant spotted knapweed (Cen- Mountain Research Station (RMRS) and by the taurea maculosa Lam.). Bitterroot Ecosystem Management Research The adults measure 42.5 mm and 45.0 mm Project, a partnership between the RMRS, the long and both are 3.3 mm wide; the subadult Bitterroot National Forest, and the University is 31.2 mm long and 2.3 mm wide, and the of Montana. juvenile is 27.2 mm long and 1.2 mm wide. The cephalic plate is faintly margined caudo- LITERATURE CITED laterad in the adults and not margined in the other specimens, and the 2nd antennomere is LOOMIS, H.F., AND R. SCHMITT. 1971. The ecology, distri- moderately hirsute dorsad in all individuals, bution, and taxonomy of the millipeds of Montana less so than the 3rd and more so than the 1st, west of the Continental Divide. Northwest Science 45:107–131. but the pilosity is markedly less in the juvenile SHELLEY, R.M. 2002. A synopsis of the North American and this article is only slightly more hirsute centipedes of the order Scolopendromorpha (Chilo- that the basal one. Complete paramedian dorsal poda). Virginia Museum of Natural History Memoir sutures begin on tergite 2 and extend through 5:1–108. 22 on all specimens. The ultimate legs are Received 10 June 2003 missing from the individuals from Petty Pasture Accepted 29 January 2004 and are sparsely hirsute on those from lower Western North American Naturalist 64(2), ©2004, pp. 259–264

HABITAT USE BY BRUSH MICE (PEROMYSCUS BOYLII) IN SOUTHEASTERN ARIZONA

Amy B. Gottesman1, Michael L. Morrison2, and Paul R. Krausman1

Key words: Arizona, brush mouse, habitat, hantavirus, Peromyscus boylii.

Hantavirus pulmonary syndrome (HPS) is a these areas desirable for recreation and homes. group of zoonotic diseases transmitted from Consequently, a high possibility exists for rodents to humans. Transmission occurs pri- human-rodent interactions in these areas. To marily through inhalation of excrement, in the avoid potential risks and to aid in the predic- form of dust, from an infected rodent (Tsai tion of future HPS outbreaks, more knowledge 1987, Wells et al. 1997). Hantavirus pulmonary about the ecology of brush mice is needed. syndrome came to the attention of biologists Our objectives were to determine which habi- after an outbreak in the southwestern United tat characteristics are unique to areas used by States in 1993 (Mills et al. 1999a). Following brush mice, seasonally and by sex, in the Santa this outbreak, researchers began exploration Rita Experimental Range (SRER) in south- into the cause of this illness. Deer mice (Pero- eastern Arizona and to determine if brush myscus maniculatus) were the principal carri- mice use artificial structures (e.g., cabins, sheds) ers (Nichol et al. 1993, Childs et al. 1994). when available. We used radiotelemetry to Since the initial outbreak, the virus has been assess mouse habitat use, which has advan- identified in >25 states in the United States tages over the use of live-trapping (e.g., Hall and in numerous species of rodents, including and Morrison 1997, Bias and Morrison 1999). the brush mouse (P. boylii). We conducted our study near the Florida Ongoing studies have identified brush mice Headquarters of the SRER, Pima County, as a primary host of Sin Nombre virus (i.e., the approximately 48 km south of Tucson, Arizona. etiologic agent of HPS) in southern Arizona SRER (20,234 ha) is representative of the (Abbott et al. 1999, Kuenzi et al. 1999, Mills et 8,094,000 ha of the semidesert, grass-shrub al. 1999b). In southeastern and central Arizona, range found throughout the Southwest. SRER adult male brush mice have a greater prevalence is located on a broad, sloping plain, cut by of the virus compared with other species of numerous shallow, dry washes, with elevations Peromyscus (Abbott et al. 1999, Kuenzi et al. from 883 m to 1372 m (Martin 1966). The ele- 1999). Information on habitat use of the genus vation of our study site ranges from 1270 m to Peromyscus is available (Brown 1964, King 1968, 1350 m. Temperatures ranged from a mean of Price 1984, Snyder and Best 1988, Scott and 16.5°C in winter (September–December) to Dueser 1992), but recent habitat data for brush 24.5°C in summer (May–August), with an annual mice are scarce. mean temperature of 17.8°C (National Oceanic Hantavirus pulmonary syndrome is often and Atmospheric Administration 2001). Annual found concentrated in specific areas, and this mean rain and snowfall were 53 cm and 11.2 cm has been related to habitat for the host (Abbott (measured at SRER), respectively, about aver- et al. 1999, Kuenzi et al. 1999). In southeastern age for the area (National Oceanic and Atmos- Arizona, brush mice are most abundant in pheric Administration 2001). association with riparian vegetation along water- Two main vegetation types, semidesert grass- courses (Kuenzi et al. 1999). Due to the avail- land (upland) and oak-riparian, occur at these ability of water and shade, humans also find elevations. The upland is characterized by

1School of Renewable Natural Resources, University of Arizona, Biological Sciences East 325, Tucson, AZ 85721. 2Corresponding author. Great Basin Institute, University of Nevada, Reno, NV 89557-0031.

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Lehmann lovegrass (Eragrostis lehmanniana), Holohill Systems, Ltd., Carp, ON, Canada). We three-awn (Aristida spp.), prickly pear cactus did not collar juveniles and subadults because (Opuntia spp.), ocotillo (Fouquieria splendens), the collars could not be adjusted for growth. acacia (Acacia spp.), and mesquite (Prosopis We toe-clipped animals to ensure we did not velutina). The oak-riparian vegetation type, repeatedly sample the same individual through- which occurs in drainages where water flow is out our study. seasonally intermittent, is characterized by de- Animals were anaesthetized with Metofane™ ciduous trees, including Arizona white oak for processing. We secured collars, averaging (Quercus arizonica), netleaf hackberry (Celtis ~6.0% of the body weight of brush mice, reticulata), and an understory characterized by around the animal’s neck by tightening a crimp mimosa (Mimosa biuncifera) and various grasses around the collar. By design, we attempted to (Martin 1966). radio-collar up to 5 animals per month. A vari- We established 3 trapping webs (Kuenzi et ety of conditions, including transmitter mal- al. 1999) as areas for monthly trapping from function (prior to attachment) and failure to April 2000 to March 2001. Trap locations were capture an adequate number of adults, resulted within webs, consisting of 12 trap lines, each in 3–5 animals being radio-collared monthly. with 12 traps per line. All lines radiated out Radio-collars transmitted for approximately 100 m from the web’s center. The first 4 trap 4 weeks. locations of each line nearest the web’s center We released each animal at its capture loca- were set 5 m apart, with the remaining 8 traps tion and did not attempt to locate a mouse for set 10 m apart. Each web had 144 trap loca- ≥6 hour following release. We located animals tions in vegetation ranging from grassland to from signals picked up by portable receivers riparian deciduous and oak (Quercus spp.) (Telonics, Mesa, AZ, and AVM Instrument woodland. This trapping configuration was Company, Livermore, CA) and a 2-element Yagi established as part of a related study on hanta- antenna. virus prevalence at SRER (M.L. Morrison un- We monitored approximately 5 animals, 3 published data). Brush mice select riparian evenings per week, 3 times per evening (i.e., vegetation at the SRER (Morrison et al. 2002). 1800, 2100, and 0100) each month. These times Each month, therefore, we set only the 6 trap were selected to spread our observations across locations farthest from the web’s center with the nocturnal period and thus sample various Sherman live-traps (7.6 × 8.9 × 22.9 cm) on the activity periods. Because of thick vegetation 5 downslope trap lines that entered riparian and our travel time between study animals, we vegetation to catch animals to be radio-collared could visit each animal only about 3 times (90 traps total). Riparian and upland vegetation nightly. We located signals (multiple fixes) well types are clearly separated in our study loca- away from the animal to avoid disturbing its tions. To increase chances of catching brush activities. We gathered locations each month mice, we set 18 additional traps in a straight until the collars failed, the animal died, or the line on each side of a stream (36 total) at a ripar- animal left the area. ian site next to buildings at the Florida Head- We determined percent cover of grass, quarters. Brush mice caught on this riparian line shrubs (i.e., vegetation <1.5 m, excluding were considered living “near” (within ~200 m) grasses), trees (i.e., vegetation ≥1.5 m), succu- artificial structures. All other captures were lents, bare ground, rocks, and litter (i.e., leaf defined as living “far” (>1000 m) from artifi- litter, downed vegetation, and dead debris) at cial structures. All traps were run for 3 con- each relocation using the line-intercept method secutive nights during each monthly session. (Canfield 1941, Etchberger and Krausman We set traps in late afternoon, each con- 1997). We randomly laid two 6-m transects per- taining a small handful of polyester fiberfill for pendicular to each other through the center of thermal protection and baited with approxi- the point, counting all vegetation touching or mately 8.5 g of a 30:70 combination of oatmeal passing over or under the transect as a percent- and peanut butter. We checked traps at dawn age of the line. Later these data were used to and identified, processed, and radio-collared calculate percent cover. Percent bare ground, the first 5 healthy adult animals captured (trans- litter, and rocks were quantified in the same mitters averaged 1.24 g, MD-2C Mouse Style, manner as the vegetation composition. 2004] NOTES 261

Using a spherical densiometer (Forest Den- Thirteen animals ceased movement within 2 siometers, Arlington, VA), we calculated cover weeks, preventing us from receiving enough produced by overstory. We took 4 readings from data for analysis (i.e., movement to ≥3 discrete the midpoints of each transect (i.e., at 1.5 m locations). Attempts to recover apparently sta- and 4.5 m along both 6-m transects). We mea- tionary radios were difficult because of the sured horizontal cover (i.e., any habitat variable substantial number of large rocks and amount contributing to a horizontally obstructed view) of down wood used as den sites, and because with a Robel pole at these same midpoints of our desire not to disturb the study site. These (Robel et al. 1970). We measured litter depth activities did, however, cause several signals to at the transect midpoints. Values for these move, indicating that these animals were variables were combined to obtain an average alive; hence we chose to cease our efforts and for each plot. We recorded slope, aspect, vegeta- exclude these data from our analyses because tion association, and distances to the nearest of the uncertain condition of the animals. We tree, artificial structure, and seasonally inter- also lost signals from 3 transmitters before suf- mittent channel for each plot. ficient data were collected. We thus collected We selected a random plot near each animal data on use of habitat variables for 14 males location plot measured by walking 6 m to 60 m and 14 females on 231 plots and compared in a random direction. We followed the distance these data with 231 paired, random plots. Not and direction from the center of the original all animals could be located during every telem- animal location plot, where we subsequently etry session, and we did not resample vegeta- carried out all the same measurements. tion plots when subsequent locations for an Analysis of variance (ANOVA) was used to animal were identical (e.g., den sites). Thus, quantify the difference between random and the total number of plots sampled was lower animal locations (nonrandom points) for the than the potential number of relocations of an mean percent of grass, shrubs, trees, succulents, animal. leaf litter, rocks, bare ground, cover (horizon- We did not detect significant differences in tal and canopy); slope and aspect; litter depth; habitat use between sexes (P > 0.15 for all and all distance measurements in brush mouse variables). Brush mouse (sexes and seasons habitat. General vegetative association was not included in this analysis because random and combined) habitat was characterized by 74% nonrandom plots were always in the same (sx– = 77.8) tree cover, 60% (sx– = 58.4) leaf lit- type. We blocked our data by individual ani- ter cover, 21% (sx– = 17.6) shrub cover, and mal to account for variation between the areas 16% (sx– = 11.1) rock cover. Overall, brush mice each animal used. We paired each random and were most frequently relocated in the riparian nonrandom point within each animal’s group area (67% of total relocations), followed by of points and grouped variables by spring uplands (17%) and the creek channel (16%). (January to April), summer (May to August), The majority (55%) of nonrandom plots were and winter (September to December). By con- within 10 m of a seasonally intermittent channel. trasting differences between means of the Random (95%) and nonrandom (100%) plots paired nonrandom and random plots for each were within 10 m of a tree. Litter depth, aspect, habitat variable, we identified features of brush and all distance measurements did not differ mouse habitat used disproportionately by indi- significantly between random and nonrandom viduals. Mean responses between males and plots. females were compared for all variables mea- We trapped and radio-located 7 animals near sured. When necessary, we used a (log + 1) the Florida Headquarters on the SRER. Only transformation to meet the assumptions of 3 animals were found in or around buildings ANOVA. Nontransformed data are presented, during radio-telemetry. Two of the mice were and the magnitude of difference between ran- inside and around a few storage sheds. They dom and nonrandom habitat plots is discussed. were found inside structures 16% and 27% of Statistical tests were considered significant the time. The 3rd animal was using an area when P < 0.05 (JMP IN Statistical Software, around a human-inhabited cabin, but never Version 4.0, 2001). entered the building. We did not observe any Of 47 radio-collared brush mice (26 males, animal travel >50 m to be in or near any arti- 21 females), 3 died shortly after being released. ficial structures. 262 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Although litter was significantly different Goodwin and Hungerford 1979, Hoffmeister during all seasons and formed a substantial 1986). Rocks and dense vegetation may protect part of mouse habitat (i.e., 45%–75% cover), mice from avian and mammalian predators the use of litter never varied by more than and provide a thermal buffer from extreme 1.2X between random and nonrandom plots. weather fluctuations that occur in southeastern Likewise, tree cover (all species combined) also Arizona. Rocks were utilized more extensively formed a substantial and consistent (i.e., in winter and spring than in summer, suggest- 70%–93%) proportion of mouse habitat in all ing heightened importance of this resource for seasons. In summer, mice used plots with sig- protection in times when vegetation is less ± dense than during summer monsoon months. nificantly more tree cover (93% 5.1 sx–) than ± In addition, freezing temperatures are possi- random plots (72% 5.1 sx–). Brush mice used areas with significantly ble during these months (National Oceanic higher rock cover in winter and spring months. and Atmospheric Administration 2001). In winter, brush mice used areas with 1.8X Previous studies suggested that understory ± vegetation is the critical factor establishing the more rock cover (22% 2.4 sx–) than random ± structure of desert riparian animal communities areas (12% 1.7 sx–). In spring, brush mice used areas with 2.4X more rock cover (19% ± (Szaro and Belfit 1987, Andersen and Nelson ± 1999). Horizontal cover, which is correlated 3.6 sx–) than random areas (8% 2.5 sx–). We found shrub use to be statistically significant with denseness of the understory, is significant in spring, with nonrandom plots containing all year. This supports the idea that plant com- ± munity structure is an important feature to 1.5X more shrubs (21% 3.6 sx–) than random ± brush mice. plots (14% 3.3 sx–). No significant difference was found in cover Slope was significant in our study during of succulent plants in random and nonrandom summer. In summer, brush mice used areas almost twice as steep as random areas. However, plots. In spring, however, nonrandom plots most steep areas were actually a by-product of had 4.5X the amount of succulent plants (9% ± channel banks, which oftentimes were nearly 3.2 s–) that random plots had (2% + 1.7 s–). x x vertical. Our slope results may reflect the fact Horizontal cover was used substantially by that brush mice inhabit riparian watercourses brush mice in spring, summer, and winter. In in this area rather than reveal anything extreme- spring, nonrandom plots had 2.4X the amount ± ly important about slope in brush mouse habi- of horizontal cover (78% 7.7 sx–) that random ± tat. However, previous studies have found brush plots had (33% 6.8 sx–). Nonrandom plots in mice selecting steep areas (Brown 1964, Wilson summer had 2.0X more horizontal cover (52% ± ± 1968, Geluso 1971, Goodwin and Hungerford 4.1 sx–) than random plots (27% 3.0 sx–). In 1979). Further, the seasonal significance might winter, nonrandom plots had 1.6X more hori- warrant additional research into the role of ± zontal cover (14% 2.1 sx–) than random plots slope in brush mouse habitat. ± (9% 2.0 sx–). The average slope was 1.5X Of 7 animals tracked near buildings, 3 used ± greater in nonrandom plots (15% 2.4 sx–) com- storage sheds, which were the structures clos- ± pared with random plots (10% 2.4 sx–) during est to the riparian area. However, none of the summer. 3 animals were found inside any human habi- Because we concentrated our trapping efforts tations (i.e., homes or offices), likely because in riparian vegetation, we were not surprised such buildings were farther from the wash than that most radio-collared mice were found in the structures where we located the mice. The that vegetative type. Brush mice are known, storage sheds were, however, frequented by however, to preferentially use riparian vegeta- humans. Furthermore, even a single visit to tion (Morrison et al. 2002). Although our study these sheds presents an opportunity for an was limited in time and geographic coverage, infected mouse to defecate, making it danger- brush mice in our southeastern Arizona study ous to disregard risk of disease transmission to area used rocky areas surrounded by dense humans. The animals likely lived in the area and cover. This complements previous findings, simply used what was immediately available where brush mice were most commonly found to them. Our sample size of radio-tagged mice in association with rocks and heavy brush was small, however, and so our results should (Jameson 1951, Brown 1964, Garner 1967, be verified by additional studies. 2004] NOTES 263

Mills et al. (1999b) recognized that patterns ETCHBERGER, R.C., AND P.R. KRAUSMAN. 1997. Evaluation of HPS in rodents differ between sites and of five methods for measuring desert vegetation. Wild- species. Therefore, if an understanding of HPS life Society Bulletin 25:604–609. GARNER, H.W. 1967. An ecological study of the brush is to be achieved, host species must be identified mouse, Peromyscus boylii, in western Texas. Texas and studied in areas where there is a threat of Journal of Science 19:285–291. disease. At SRER about 9% of brush mice GELUSO, K.N. 1971. Habitat distribution of Peromyscus in tested positive for Sin Nombre virus (M.L. the Black Mesa region of Oklahoma. Journal of Morrison unpublished data). These animals Mammalogy 52:605–607. GOODWIN, J.G., AND C.R. HUNGERFORD. 1979. Rodent live in areas with high cover of rocks and population densities and food habits in Arizona pon- understory vegetation along riparian water- derosa pine forests. United States Forest Service, courses and do not appear to seek out struc- Research Paper RM-214:1–12. tures occupied by humans. They will, however, HALL, L.S., AND M.L. MORRISON. 1997. Den and relocation site characteristics and home ranges of Pero- use human structures already present in their myscus truei in the White Mountains of California. home areas. Great Basin Naturalist 57:124–130. HOFFMEISTER, D.F. 1986. Mammals of Arizona. Univer- We thank C. Brown and J. Avey for use of the sity of Arizona Press and the Arizona Game and Fish Department, Tucson, AZ. 602 pp. Florida Headquarters on the SRER and their JAMESON, E.W., JR. 1951. Local distribution of white-footed help on all parts of this project. P. Guertin pro- mice, Peromyscus maniculatus and P. boylei, in the vided crucial assistance with all facets of radio- northern Sierra Nevada, California. Journal of Mam- telemetry, including equipment, supplies, and malogy 32:197–203. analysis. B. Steidl, Y. Petryszyn, J. Waters, and KING, J.A., EDITOR. 1968. Biology of Peromyscus (Rodentia). American Society of Mammalogists. 2 anonymous referees provided helpful guid- KUENZI, A.J., M.L. MORRISON, D.E. SWANN, P.C. HARDY, ance with manuscript review. We were assisted AND G.T. DOWNARD. 1999. A longitudinal study of by countless volunteers and technicians through- Sin Nombre virus prevalence in rodents, southeastern out the course of this project, especially A. Arizona. Emerging Infectious Diseases 5:113–117. Heydlauff, M. Bucci, B. Brochu, E. Stitt, R. MARTIN, S.C. 1966. The Santa Rita Experimental Range. U.S. Department of Agriculture, Green Valley, AZ. Thornton, J. Duke, C. Manoli, and the Arizona MILLS, J.N., T.L. YATES, T.G. KSIAZEK, C.J. PETERS, AND Agricultural Experiment Station. This study J.E. CHILDS. 1999a. Long-term studies of hantavirus was funded by the Center for Disease Control reservoir populations in the southwestern United (CDC) and Prevention; we thank J. Mills for States: rationale, potential, and methods. Emerging project management. Infectious Diseases 5:95–101. MILLS, J.N., T.G. KSIAZEK, C.J. PETERS, AND J.E. CHILDS. 1999b. Long-term studies of hantavirus reservoir LITERATURE CITED populations in the southwestern United States: a synthesis. Emerging Infectious Diseases 5:135–142. ABBOTT, K.D., T.G. KSIAZEK, AND J.N. MILLS. 1999. Long- MORRISON, M.L., A.J. KUENZI, C.F. BROWN, AND D.E. term hantavirus persistence in rodent populations in SWANN. 2002. Habitat use and abundance trends of central Arizona. Emerging Infectious Diseases 5: rodents in southeastern Arizona. Southwestern Nat- 102–112. uralist 47:519–526. ANDERSEN, D.C., AND S.M. NELSON. 1999. Rodent use of NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION. anthropogenic and “natural” desert riparian habitat, 2001. Climatological data annual summary, Arizona. lower Colorado River, Arizona. Regulated Rivers: National Climate Data Center, Asheville, NC. Research and Management 15:377–393. NICHOL, S.T., C.F. SPIROPOULOU, S. MORZUNOV, P.E. ROLLIN, BIAS, M.A., AND M.L. MORRISON. 1999. Movements and T.G. K SIAZEK, H. FELDMAN, A. SANCHEZ, ET AL. 1993. home range of salt marsh harvest mice. Southwest- Genetic identification of a hantavirus associated with ern Naturalist 44:348–353. an outbreak of acute respiratory illness. Science 262: BROWN, L.N. 1964. Ecology of three species of Pero- 914–917. myscus from southern Missouri. Journal of Mammal- PRICE, M.V. 1984. Microhabitat use in rodent communities: ogy 45:189–202. predator avoidance or foraging economics? Nether- CANFIELD, R.H. 1941. Application of the line interception lands Journal of Zoology 34:63–80. method in sampling range vegetation. Journal of ROBEL, R.J., J.N. BRIGGS, A.D. DAYTON, AND L.C. HULBERT. Forestry 39:388–394. 1970. Relationships between visual obstruction mea- CHILDS, J.E., T.G. KSIAZEK, C.F. SPIROPOULOU, J.W. KREBS, surements and weight of grassland vegetation. Jour- S. MORZUNOV, G.O. MAUPIN, K.L. GAGE, ET AL. 1994. nal of Range Management 23:295–297. Serologic and genetic identification of Peromyscus SCOTT, D.E., AND R.D. DEUSER. 1992. Habitat use by in- maniculatus as the primary rodent reservoir for a sular populations of Mus and Peromyscus: what is the new hantavirus in the southwestern United States. role of competition? Journal of Animal Ecology 61: Journal of Infectious Disease 169:1271–1280. 329–338. 264 WESTERN NORTH AMERICAN NATURALIST [Volume 64

SZARO, R.C., AND S.C. BELFIT. 1987. Small mammal use of Hantavirus transmission in the United States. Emerg- a desert riparian island and its adjacent scrub habitat. ing Infectious Diseases 3:361–365. United States Forest Service, Rocky Mountain For- WILSON, D.E. 1968. Ecological distribution of the genus est Range Experimental Station, Technical Report Peromyscus. Southwestern Naturalist 13:267–274. RM-473. TSAI, T.F. 1987. Hemorrhagic fever with renal syndrome: Received 18 October 2002 mode of transmission to humans. Laboratory Animal Accepted 9 June 2003 Sciences 37:428–430. WELLS, R.M., J. YOUNG, R.J. WILLIAMS, L.R. ARMSTRONG, K. BUSICO, A.S. KHAN, T.G. KSIAZEK, ET AL. 1997. Western North American Naturalist 64(2), ©2004, pp. 265–268

IMPORTANCE OF OUTCROSSING FOR FRUIT PRODUCTION IN SLICKSPOT PEPPERGRASS, LEPIDIUM PAPILLIFERUM L. (BRASSICACEAE)

Ian Robertson1

Key words: slickspot peppergrass, Lepidium papilliferum, outcrossing, self-pollination.

Plants with insect-mediated pollination are greater understanding of this species’ life his- often assumed to be obligate outcrossers; i.e., tory, including its breeding system, so that pollen must be supplied from flowers of other sound management decisions can be made. individuals for pollination and subsequent fruit Flowering in L. papilliferum extends from production. Indeed, many flowers with insect- early May to mid-July. Reaching 5–40 cm in mediated pollination exhibit incompatibility to height, the plant has numerous, multi-flowered their own pollen or have a separation in time inflorescences that terminate at the branches. between pollen production and maturation of The small flowers have white petals, and fila- the stigma on a given flower (Proctor et al. ments of the anthers are covered with club- 1996). However, because the breeding systems shaped hairs. By the end of the flowering of plants are diverse and include varying levels period, large amounts of orbicular, flattened of outcrossing and selfing, experiments are re- seed about 3 mm in length are produced. quired to determine whether pollination in a Insects, including species from several fami- particular species occurs via outcrossing, self- lies of Hymenoptera (Apidae, Halictidae, Col- pollination, or both. Here I report the results of letidae, Vespidae, Sphecidae), Coleoptera (Mely- such a study on slickspot peppergrass, Lepid- ridae, Dermestidae), and Diptera (Syrphidae), ium papilliferum L. (Brassicaceae), a rare mus- frequent L. papilliferum flowers and are nec- tard endemic to sagebrush-steppe habitat in essary for pollination and fruit production southwestern Idaho. (Robertson 2002, Robertson and Klemash 2003). Within sagebrush areas, L. papilliferum is However, it is not clear whether the plant relies restricted to microsites known as “slick spots,” on outcrossed pollination, self-pollination, or which are characterized by their high levels of both. Making this distinction for L. papilliferum clay or salt and higher soil water retention than is important from a conservation perspective surrounding areas (Meyer 1995). Currently, because continued fragmentation of the plant’s there are approximately 60 known sites in habitat will likely reduce the plant’s opportu- Idaho with slick spots that contain L. papil- nity for outcrossing and in the process lead to liferum populations (Moseley 1994, U.S. Fish a loss of genetic diversity within populations. and Wildlife Service 2002). General degrada- I conducted an experiment to determine tion of sagebrush-steppe habitat from sources the breeding system of L. papilliferum from such as wildfire, livestock grazing, irrigated early May to mid-July 2002 at 3 sites in south- agriculture, exotic species invasions, and urban western Idaho. The sites, which are being development has contributed to the plant’s used as part of a longer-term study on the pol- rapid decline and increasingly fragmented dis- lination biology of L. papilliferum, are sepa- tribution over the past century (Moseley 1994). rated from one another by at least 20 km that In July 2002, L. papilliferum was proposed for includes areas of irrigated agriculture and listing as an endangered species by the United rangeland. States Fish and Wildlife Service. Uncertainty At the onset of the experiment, 48 similarly surrounding long-term viability of L. papillif- sized plants with unopened (i.e., virgin) flowers erum makes it imperative that biologists gain were enclosed individually within cylindrical,

1Department of Biology, Boise State University, 1910 University Drive, Boise, ID 83725.

265 266 WESTERN NORTH AMERICAN NATURALIST [Volume 64 insect-proof cages (5–15 cm diameter, 10–20 self-pollination treatments, several individuals cm height) made from 10-mm hardware cloth in both groups did produce fruits. Distributions covered with fine bridal veil (0.25-mm mesh). of percent fruit set in the control and self-polli- Cages were fixed securely to the substrate nation treatments were highly skewed (Fig. 2). with small pegs to minimize the possibility Insect visitations are crucial for pollination that insects could enter at the base. A previous and fruit production in L. papilliferum (Robert- study (Robertson and Klemash 2003) showed son and Klemash 2003). A wide variety of in- that cages do not reduce plant survival or insects are commonly observed flying from plant hibit fruit production. to plant both within and between slick spots at The caged plants were divided randomly and a site, contacting many flowers in the process in equal number into 1 of 3 groups: control, (Robertson and Klemash 2003). Although the self-pollination treatment, and cross-pollina- rate and distribution of pollen dispersal among tion treatment. All 3 groups were represented flowers and between populations is not known at each of the 3 sites. Experimental manipula- for L. papilliferum, it is clear from the present tion began once a plant was in full bloom. For study that most, if not all, fruit production is the self-pollination treatment, I snipped a achieved via outcrossing. small inflorescence of opened flowers from the The presence of mature fruit on some plants plant and then brushed it gently over other in the self-pollination treatment suggests either opened flowers on the same plant. The cross- that self-pollination is possible in L. papillif- pollination experiment was similar in tech- erum, at least to a small extent, or that insects nique except that the inflorescence used for found their way into a few cages and cross- brush pollination came from a different plant pollinated some of the flowers. The latter ex- growing at least 2 m away. As a sham opera- planation seems more likely given that 25% of tion, control and cross-pollination plants had a the plants in the treatment produced no fruit, small inflorescence snipped off and discarded. more than half of the plants produced less The manipulations were repeated within a week. than 5% fruit, and none had fruit sets as high In early to mid-July, once plants had ceased as the median for the cross-pollination treat- flowering, I determined percent fruit set for ment. If L. papilliferum had a general ability each plant by collecting 1–3 inflorescences to self-pollinate, a higher and more-or-less and counting the number of wilting flower normal distribution of percent fruit sets would pedicels (i.e., unpollinated flowers) and seed- be expected rather than the low and highly bearing fruits. skewed distribution that was observed. Never- Two plants in the cross-pollination treatment theless, it is worth noting that the genus Lep- and 3 control plants wilted and died before idium includes a number of species known to the end of the experiment. This frequency of be self-compatible; however, these species, die-off is typical for L. papilliferum in the field unlike L. papilliferum, tend to have reduced (Robertson unpublished data). Nonparametric floral structures (J.L. Bowman, University of statistics were used in the analysis of fruit pro- California, Davis, personal communication). duction because percent fruit sets within the The production of small fruit sets in less control and self-pollination experiments were than half of the control plants may again sug- not normally distributed. Median percent fruit gest insect contamination within cages as the set in control plants and self-pollination plants cause. The possibility of wind-mediated self- was 0% and 5%, respectively. In contrast, or cross-pollination is remote given that the median percent fruit set in cross-pollinated structures of L. papilliferum flowers and pollen plants was 40%. The overall difference in per- grains are not consistent with those of anemo- cent fruit set between groups was statistically philous species, which generally produce copi- significant and caused by the higher percent ous amounts of smooth-surfaced pollen and fruit set in the cross-pollination treatment have an exposed stigma and long stamens with (Fig. 1; Kruskal-Wallis test, H = 17.3, df = 2, exposed anthers (Proctor et al. 1996). Repro- P < 0.001); there was no significant difference ductive structures of L. papilliferum are rela- in percent fruit set between the control and tively protected within the flower’s corolla, self-pollination treatments (Mann-Whitney U and pollen production in this species could test, Z = 1.3, P = 0.2). Although median per- not be described as copious (Robertson percent fruit set was low in both the control and sonal observation). 2004] NOTES 267

Fig. 1. Box plot chart showing results of the hand-pollination experiment. Top, middle, and bottom horizontal lines of a box show the 75th, 50th (median in bold), and 25th percentiles, respectively. Vertical lines extend from the 10th to the 90th percentiles. Sample sizes are given in parentheses below the dashed line.

The apparent reliance of L. papilliferum on insect-mediated cross-pollination has implications for management and conservation of the species. Over the past century populations of the plant have become increasingly fragmented due to both human activity and altered habitat resulting from wildfire and exotic species invasions (Moseley 1994). A population of L. papilliferum that becomes isolated from other Fig. 2. Frequency distribution of percent fruit set in the populations risks losing genetic diversity that control and self-pollination treatment. is normally maintained via outcrossing. Ade- quate levels of genetic diversity and gene flow are generally viewed as critical to the survival of threatened or endangered species because torical, and distance to the nearest population. they help to ensure individual fitness through One could also examine the effects of genetic a maintenance of heterozygosity, and they pro- variability within populations on individual vide for the long-term viability of a species in pollination success, fruit production, and off- the face of environmental change (Haig 1998). spring vigor. Thus, understanding the popula- For a species that relies on outcrossing, loss of tion genetics of L. papilliferum may provide genetic diversity and gene flow may lead to valuable insight into the effects of habitat frag- reductions in pollination success and even mentation on outcrossing and gene flow be- infertility. Thus, management efforts for L. tween populations. papilliferum should consider the effects of land use on the movement of insects between Funding for this research was provided by populations. Unfortunately, documenting long- the Idaho Army National Guard (IDARNG) distance insect movement and pollen transfer and a Boise State University Faculty Research has proven difficult in pollination studies (Proc- Grant to the author. Staff from the Bureau of tor et al. 1996). An alternative approach for L. Land Management and IDARNG assisted in papilliferum would be to examine the current site selection. I am grateful to Danielle Kle- amount of genetic variability within and be- mash for her assistance in the field and labora- tween populations and to relate this informa- tory, as well as Ann DeBolt, Lara Hannon, tion to population size, both current and his- Marjorie McHenry, Dana Quinney, Wilma 268 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Robertson, and Jay Weaver for helpful discus- ROBERTSON, I.C. 2002. Insect-mediated pollination of sion at various stages of the project. Lepidium papilliferum. Unpublished report on file at State of Idaho Military Division, Boise. ROBERTSON, I.C., AND D. KLEMASH. 2003. Insect-mediated LITERATURE CITED pollination in slickspot peppergrass, Lepidium papilliferum L., and its implications for population viabil- HAIG, S.M. 1998. Molecular contributions to conservation. ity. Western North American Naturalist 63:333–342. Ecology 79:413–425. U.S. FISH AND WILDLIFE SERVICE. 2002. Endangered and MEYER, S.E. 1995. Autecology and population biology of threatened wildlife and plants; listing the plant Lep- Lepidium papilliferum. Unpublished report on file at idium papilliferum (slickspot peppergrass) as endan- State of Idaho Military Division, Boise. gered. Federal Registry Vol. 67, No. 135 (Monday, 15 MOSELEY, R.K. 1994. Report on the conservation status of July 2002). Lepidium papilliferum. Idaho Department of Fish and Game, Conservation Data Center. Received 23 September 2002 PROCTOR, M., P. YEO, AND A. LACK. 1996. The natural history Accepted 5 May 2003 of pollination. Timber Press, Portland, OR. 479 pp. Western North American Naturalist 64(2), ©2004, pp. 269–272

ARE DESERT BASINS EFFECTIVE BARRIERS TO MOVEMENTS OF RELOCATED BLACK BEARS (URSUS AMERICANUS)?

Jon P. Beckmann1,2,3 and Carl W. Lackey4

Key words: black bears, relocation, desert, Ursus americanus, Lake Tahoe.

During the last 10–20 years many areas have the aim of removing nuisance individuals. experienced an increase in number of conflicts We capitalized on the extent to which desert between black bears (Ursus americanus) and basins separate the Sierra Nevada and adjacent humans, and such an increase in conflicts has Great Basin ranges to examine the effectiveness been disproportional to human population of relocation efforts. The Great Basin Desert growth. This is especially true in western North represents a unique opportunity to evaluate America, where rapid urban sprawl has led to the efficacy of relocation of nuisance bears encroachment into areas adjacent to U.S. pub- because desert floors, which can be greater lic lands that have historically contained large than 64 km wide, separate mountain ranges carnivores. For example, from 1990 to 2000 the where bears occur. Further, desert basins are human population in the Lake Tahoe basin in- often large areas of unsuitable desert habitat creased by 26% and the number of complaints (e.g., large expanses of sagebrush [Artemisia by citizens concerning black bears increased spp.]) that bears do not use (Goodrich 1990, by more than tenfold during the same time Beckmann 2002, Beckmann and Berger 2003). period (Goodrich 1990, Beckmann 2002). In However, bears will occasionally make rela- Nevada, as in other areas of western North tively short movements through areas consist- America, human–bear interactions have in- ing of sagebrush in order to reach patchily dis- cluded loss of pets, localized predation on live- tributed suitable habitat (e.g., cone-producing stock, property damage, and even human deaths trees) in this arid landscape. Thus, we wanted (approximately 45 deaths from black bears since to test whether these expansive desert basins 1900 in North America; Herrero 2002). could prohibit movements of relocated bears Many state and federal entities seek non- between mountain ranges. lethal solutions (i.e., relocation or deterrents) The current distribution of black bears in for dealing with “nuisance” carnivores, espe- Nevada is restricted to extreme western por- cially black bears. Yet there is a paucity of rig- tions of the state in the Carson Range of the orous study on the effectiveness of the most Sierra Nevada, and in the Sweetwater, Pine common nonlethal techniques management Nut, and Wassuk Ranges (Goodrich 1990), agencies currently use to alter the behavior of which are areas with high peaks and deep can- nuisance bears, although exceptions clearly exist yons (Grayson 1993); these ranges were the (e.g., Gillin et al. 1994, Ternent and Garshelis focus of our work. We utilized urban areas in 1999, Clark et al. 2002). A survey conducted by western Nevada such as Reno, Carson City, the Virginia Department of Game and Inland Incline Village, Glenbrook, Stateline, Minden, Fisheries in 2001 revealed that 33 states, and Gardnerville, when capturing urban- including Nevada, currently manage black bears interface bears. Bears in this region are at the and respond to citizen complaints about nui- edge of their known range in the Great Basin, sance bears (D. Kocka, Virginia Department of with the nearest eastern bear population Game and Inland Fisheries, personal commu- found in the Wasatch Range, Utah, about 750 nication). Of those states, 26 relocate bears with km away (Goodrich 1990). Although black bears

1Program in Ecology, Evolution, and Conservation Biology, University of Nevada, Reno, NV 89512. 2Department of Environmental and Resource Sciences, University of Nevada, Reno, NV 89512. 3Wildlife Conservation Society, Teton Field Office, Moose, WY 83012. 4Nevada Division of Wildlife, 1100 Valley Road, Reno, NV 89512.

269 270 WESTERN NORTH AMERICAN NATURALIST [Volume 64 are listed as a game species in Nevada, there and from the ground. We assigned Universal has never been a legal harvest. Transverse Mercator (UTM) coordinates to We captured bears by using culvert traps each location from a GPS unit onboard the air- and hounds from 1 July 1997 to 1 April 2002. craft or from standard triangulation methods We tranquilized and weighed the bears and (Heezen and Tester 1967, Hupp and Ratti 1983, attached radio-collars with mortality sensors Samuel and Fuller 1994) on the ground. Loca- (Advanced Telemetry Systems, Isanti, MN; see tions for each relocated individual were mapped Beckmann 2002 for details) to individual bears. using ArcView 3.2 software. Telemetry points Age was estimated from annuli of the 1st upper were recorded from the air every 3 days for premolar (PM1), the standard tooth for age each individual until their return. However, analysis in black bears (Matson’s Laboratory, once a bear was within 5 km of the urban cen- Milltown, MT; Stoneberg and Jonkel 1966). ter from which it was originally captured, we Animals were classified as cubs (<1.5 years), located the bear every day to determine the juveniles (1.5–3 years), or adults (≥3 years). exact date of return. A bear was considered to To examine whether desert basins serve as have returned the 1st time it was located inside effective barriers to movements of relocated the city limits from which it was captured, as black bears, we selected 8 adult (≥3 years) defined on coverage maps from the year 2000 male bears from a total of 71 bears that were in ArcView 3.2. We also estimated the total dis- captured inside urban areas and relocated tance (km) of unsuitable sagebrush (Artemisia them to different mountain ranges. Relocation spp.) and agricultural habitats in basins (using was defined as an individual being moved ≥25 vegetation coverage maps in ArcView 3.2) that km from its capture site to a release site in a a bear had to cross to return to its original mountain range different from the one in which point of capture (Table 1). Some bears had to it was captured. In each case bears were relo- cross several basins of unsuitable habitat to cated to sites that had a known bear population return. For these individuals we estimated the based on telemetry studies at the time of re- minimum distance of inappropriate habitat lease (Beckmann 2002). We relocated only adult that the bear had to cross in each basin and male bears for several reasons: (1) 93% of all then summed these values for total distance. adult bears captured in urban centers in the We used Pearson correlation (r) analyses to Lake Tahoe basin and the western Great Basin test for relationships between the period of were males, (2) females often had cubs and we time that elapsed (days) before a bear returned did not want to heighten mortality risks to and the distance (km) the bear was moved, the cubs via additional travel that might include weight (kg) of the relocated bear, and the age crossing roads, and (3) we eliminated both sex (years) of the relocated bear (SAS 2001). A and various age categories (i.e., juveniles and probability level of P < 0.05 was used for all cubs) as confounding factors when analyzing statistical tests. Means ± 1s are given unless our results. Additionally, because of cost con- otherwise noted. straints and public relations reasons, we were The mean distance that all 8 adult male allowed to relocate only 10% of bears captured bears were moved was 58.6 km ± 27.4 km in urban areas by the Nevada Division of (Table 1). Of the 8 relocated animals, all re- Wildlife (NDOW). turned to the urban center where they were The 8 bears were moved varying distances captured within 18 days (Table 1). In all 8 between their point of capture in urban cen- instances the bears remained at the relocation ters and the target mountain range for reloca- site for at least 1 night before moving, regard- tion (see Table 1 for distances). Of the 8 indi- less of the time of day the bear was released. viduals, 2 (#34, 56) were relocated in the The mean number of days for all bears to spring (March–May), 3 (#2, 19, 36) in summer return was 15.1 ± 2.2 (Table 1). The period of (June–August), and 3 (#24, 25, 26) during fall time for a bear to return to the urban site of months (September–November). Once a bear capture was not correlated with distance that was relocated, we followed the individual using an individual was moved (r = 0.44, df = 6, P telemetry to determine its location and to = 0.2713) nor with its mass (r = –0.15, df = 6, monitor the rate of return to the initial capture P = 0.7148) nor with its age (r = –0.22, df = region. Animals were located, weather permit- 6, P = 0.6058). No individuals died during ting, from a Cessna 206 fixed-wing airplane their movements from the release site to the 2004] NOTES 271

TABLE 1. Summary of 8 collared adult (≥3 years) male black bears (Ursus americanus) relocated from urban areas to a different mountain range at the interface of the Sierra Nevada (Lake Tahoe basin) and the western Great Basin Desert. Relocation was defined as an individual being moved ≥25 km from its point of capture to a different mountain range within the Great Basin Desert. Age was estimated from annuli of the 1st upper premolar (PM1). Total unsuitable distance (km) is the distance of unsuitable sagebrush (Artemisia spp.) and agricultural habitats that a bear had to cross to return to its original point of capture. Six (#2, 24, 25, 26, 34, 56) bears had to cross ≥2 basins of unsuitable habitat in order to return. Means ± 1s are given. Total unsuitable Days elapsed ID # Age Weight (kg) Distance relocated (km) distance (km) until return 29154 76.8 32 15 19 9 191 25.6 16 12 24 10 200 65.6 32 15 25 5 82 43.2 28 14 26 9 186 104 64 18 34 3 84 76.8 35 16 36 3 73 25.6 16 18 56 5 100 51.5 25 13 Mean 6.6 ± 2.9 133.8 ± 54.5 58.6 ± 27.4 31 ± 15.1 15.1 ± 2.2

original capture site despite the fact that in all prisingly, the distance that bears were moved cases bears had to cross either U.S. Highway was not correlated with the amount of time it 395 or U.S. Highway 50, and in some cases took an individual to return to the original site both 4-lane highways in western Nevada to of capture. This was likely because of the rela- return to their original home range. However, tively small distances that we were able to in 2 instances (#56 and #19) relocated bears move bears (<105 km in all cases), given the were hit by vehicles that had slowed down limited habitat suitable for bears in the xeric enough to prevent serious injury to either the climate of the western Great Basin. Further, bear or people inside the vehicles. Both inci- we did not want to move any bears to moun- dents occurred on 2-lane, mountain highways tain ranges in which they had not historically crossing the Carson Range of the Sierra Nevada occurred, thus limiting the maximum distance from the Great Basin Desert into the Lake that we could relocate any bear. Tahoe basin. The vehicle strike rate for collared bears that Results of this study indicate that reloca- were not relocated during this study was 17%. tion of nuisance bears is not an effective man- The fact that two (25%) relocated bears in this agement option for reducing the number of study were struck by vehicles during their negative interactions between bears and efforts to return to their point of capture fur- humans, at least in the Lake Tahoe basin and ther suggests that relocation may ultimately adjacent Great Basin Desert ranges. Addition- have a negative impact on populations. This is ally, based on our sample, desert basins are especially true if agencies are relocating female ineffective barriers to movement of bears from bears with cubs, assuming that females also one mountain range to another, even for time would attempt to return to their original home periods <2 weeks. Even bears that were relo- range in a manner similar to males. However, cated across multiple desert mountain ranges given that males have a greater tendency to and basins (n = 6) or >100 km (n = 1) from move long distances, the impacts of long-dis- their original mountain range of capture tance relocation on females and cubs may be returned. Although our sample sizes are small different—an issue that awaits further investi- within a season, it appears that time of year gation from biologists. did not impact the rate at which relocated Because of conservation concerns associ- bears returned to their original location of ated with the current high levels of mortality capture. It is unlikely that a lack of potential of bears in urban areas from negative interac- mates in release sites influenced a male bear’s tions with humans in this region, where <300 homing tendency, given that radio-collared bears occur (Goodrich 1990, Beckmann 2002), adult females were present at each release site we examined relocation as a potential non- during this study (see Beckmann 2002). Sur- lethal tool to reduce bear and human conflicts. 272 WESTERN NORTH AMERICAN NATURALIST [Volume 64

Because relocation is not an effective manage- BECKMANN, J.P., AND J. BERGER. 2003. Using black bears ment option, at least in western Nevada, we to test ideal-free distribution models experimentally. suggest that to protect bears at the interface of Journal of Mammalogy 84:594–606. CLARK, J.E., F.T. VAN MANEN, AND M.R. PELTON. 2002. the northern Sierra Nevada and the western Correlates of success for on-site releases of nuisance Great Basin, including the Lake Tahoe basin, black bears in Great Smoky Mountains National ordinances and laws requiring the use of bear- Park. Wildlife Society Bulletin 30:104–111. proof dumpsters are badly needed. Good plan- GILLIN, C.M., P.M. HAMMOND, AND C.M. PETERSON. 1994. Evaluation of an aversive conditioning technique ning and subsequent management, based on a used on female grizzly bears in the Yellowstone Eco- combination of life history and ecological data, system. International Conference on Bear Research will continue to be an obvious requisite action and Management 9:503–512. to ensure the persistence of a species depen- GOODRICH, J.M. 1990. Ecology, conservation, and manage- dent on profitable foraging in human zones. ment of two western Great Basin black bear populations. Master’s thesis, University of Nevada, Reno. Once this can be achieved, especially in areas GRAYSON, D.K. 1993. The desert’s past: a natural prehistory outside national parks where legal compliance of the Great Basin. Smithsonian Institution Press, that favors biodiversity tends to be weaker, our Washington, DC. 356 pp. ability to assure the persistence of this large HEEZEN, K.L., AND J.R. TESTER. 1967. Evaluation of radio- carnivore on U.S. public lands will improve. tracking by triangulation with special reference to deer movements. Journal of Wildlife Management 31:124–141. ACKNOWLEDGMENTS HERRERO, S. 2002. Bear attacks: their causes and avoidance. Revised edition. Lyons Press, New York. 282 pp. We thank the University of Nevada, Reno, HUPP, J.W., AND J.T. RATTI. 1983. A test of radiotelemetry Nevada Agricultural Experiment Station, Neva- triangulation accuracy in heterogeneous environments. Proceedings of the International Wildlife and da Division of Wildlife (NDOW), the U.S. Biotelemetry Conference 4:31–46. National Science Foundation, and the Wildlife SAMUEL, M.D., AND M.R. FULLER. 1994. Wildlife Radio- Conservation Society for funding. We thank J. telemetry. Pages 370–418 in T.A. Bookhout, editor, Berger for his helpful insights and comments Research and management techniques for wildlife on this manuscript. We are also extremely and habitats. The Wildlife Society, Bethesda, MD. SAS INSTITUTE. 2001. SAS software: usage and reference. grateful for the many hours of safe flights pro- Version 8.02. SAS Institute, Cary, NC. vided by M. Wiklanski, J. Kelly, and the entire STONEBERG, R.P., AND C.J. JONKEL. 1966. Age determination staff at El Aero Services in Carson City, Nevada. of black bears by cementum layers. Journal of Wildlife We thank J. Nelson, DVM, who graciously vol- Management 30:411–414. TERNENT, M.A., AND D.L. GARSHELIS. 1999. Taste-aversion unteered many hours of his time. We also thank conditioning to reduce nuisance activity by black K. Krauter for hours spent helping us build bears in a Minnesota military reservation. Wildlife maps in ArcView. Finally, we thank S. Shea and Society Bulletin 27:720–728. G. Bracket who assisted us in the field. Received 6 February 2003 Accepted 5 May 2003 LITERATURE CITED

BECKMANN, J.P. 2002. Changing dynamics of a population of black bears (Ursus americanus): causes and consequences. Doctoral dissertation, University of Nevada, Reno. Western North American Naturalist 64(2), © 2004, p. 273

BOOK REVIEW

The Animal Mind. James L. Gould and Carol average reader interested in glancing at the Grant Gould. Scientific American Library, whole subject. This is especially true for the New York. 1999. $19.95, paperback; 236 discussion of visual information (p. 15), classi- pages. ISBN 0-7167-6035-5. cal conditioning (p. 56), and foraging and communication in honey bees (Ch. 5). The bias There are few tasks as difficult as trying to toward honey bees probably stems from the understand how people think, let alone how authors’ work and interest in honey bees, as animals think. But good insights can be ob- evidenced by their 1988 book on that topic tained through proper review of the knowl- (The Honey Bee, Scientific American Library). edge gained by scientists over years of behav- Although I found few typos or misspellings, ioral, sociological, and psychological research. I was often distracted by the unusual spelling To take that knowledge and summarize it into of cooperation, coordinates, microorganisms, a text suitable for the average naturalist is reexamination, and preexisting (spelled coöper- another challenging task, one that is suitably ation, coördinates, microörganisms, reëxami- mastered by James and Carol Grant Gould in nation, and preëxisting). Also distracting were The Animal Mind. a bizarre word choice when referring to geese The book is extremely well presented with that imprinted on Konrad Lorenz as “ducks” glossy cover, high-quality paper, and wide (page 37) and an ephemeral but abusive use of margins. Containing 10 chapters, this book acronyms (pp. 46–50), one of which comes covers topics as general as the nature of learn- again 31 pages later (p. 81) without a reminder. ing (Ch. 3) to a very specific and detailed case These shortcomings were compensated by great study of invertebrate cognition (Ch. 5). Each examples (digger wasps on pp. 39–43), engag- chapter begins with a well-chosen quote relating anecdotes (Clever Hans in the Prologue), ing to the chapter and preparing the reader and concise wording. Humor is sparse in the for its content. An example is the quote in the text (but one figure is a Larson cartoon, p. 38) Prologue: “Who taught the raven in a drought and sometimes subtle, as evidenced on p. 170: to throw pebbles into a hollow tree, where she “When it comes to the skills that make us able espied water, that the water might rise so as to dominate other species, humans are clearly she could come to it?” (Francis Bacon, The the smartest of all animals (with the possible Advancement of Learning, 1605). exception of the domestic house cat).” The book is also well illustrated with over Overall, I believe the book is slightly too 140 figures, only one of which, the photograph technical to make it to the coffee or bedside of Donald R. Griffin on page 4, is of poor qual- table. However, for naturalists keenly inter- ity. Photographs of researchers (e.g., Ivan ested in better understanding how animals Pavlov on p. 46, B.F. Skinner on p. 51) add a can do “smart” things, or for undergraduate neat personal element to the text. Many sim- students of animal behavior, The Animal Mind ple graphs also provide visual illustration of is a good overall review of the topic. concepts, facilitating for the reader the understanding of concepts. The text is well written Serge Lariviere, Ph.D. and in a style accessible for the most part to 88 St-Edouard all. Some sections are too technical or may Levis, Quebec cover certain topics in too much detail for the Canada, G6V 6G3

FOR THE BIRDS: BOOK REVIEWS OF A TRIO OF GUIDES AND AN ENCYCLOPEDIA

Among the plethora of books to review, 3 and her birds intimately. He is well qualified bird guides and a large, much acclaimed ency- to organize a birders guide. In compiling this clopedia all appeared more or less at the same book, he has recruited 39 authors to write var- time. The guides are all of different genres. ious parts of chapters or regions with which they are particularly familiar. This is the clas- National Geographic Photography Field sic American Birding Association bird-finding Guide: Birds. Rulon E. Simmons with guide that reviews the state, geographic region photographs by Bates Littlehales. National by geographic region, giving locations to find Geographic Books, Washington, DC. 2002. birds along certain routes within each region. $21.95, paperback; 159 page, 1 to several The text lists places to stay in the region, photographs per page. ISBN 0-7922-6878-4. details on transportation to and from the area, and birds one can expect at various locations This is a “how-to” guide for photographing discussed. birds. Lavish photographs help illustrate tech- The appendices give a checklist of specific niques while the text offers the reader some locations, organizations of interest to birders, a interesting biology along the way. Topical mat- gazetteer and Alaska pronunciation guide, ref- ter includes such items as what makes a good erences and selected readings, and lastly a list photograph, getting started, luring birds, stalk- of mammals, reptiles, amphibians, and fishes ing, nesting, blinds, using different light, of Alaska. This is a must for anyone going to favorite locations for photographing birds (a Alaska intent upon bird-watching. run through most states and provinces starting in Alaska and ending in Canada), useful infor- Monterey Birds: Status and Distribution of mation, and web sites. Every few pages there Birds in Monterey County, California. 2nd are side bars providing tips relating to the edition. Don Roberson. Monterey Peninsula subject matter. Audubon Society, Carmel, CA (distributor The author addresses frequently asked ques- ABA Sales, Colorado Springs, CO). 2002. tions about what equipment to use for best $21.95, paper; 536 pages + viii + 16 color results, tips for getting close to the birds you plates, many B&W photos, maps for most want to photograph, how to take advantage of breeding species accounts + 3 appendices. challenging weather conditions, and how to ISBN 0-9615798-2-X. make interesting backgrounds for bird photography. This is an instructive booklet for those There are 482 species of birds verified for who want to photograph birds. Monterey County, and the bulk of this book, starting on page 72, consists of species accounts. A Birders Guide to Alaska. George C. West. As preface material to the accounts, the author American Birding Association, Inc., ABA gives 32 pages of birding routes, a discussion Birdfinding Guide, Colorado Springs, CO. of birding services and resources within the 2002. $28.95, paper with wire O-binding; county, and 26 pages of material that intro- 586 pages + vii, 83 route maps + 47 insert duces the species accounts. Each account has maps + 3 color maps, 63 pen-and-ink a bar graph showing the temporal period and author’s drawings, 2 color photographs, 5 numerical status in the county. Accounts of appendices. ISBN 1-878788-19-1. breeding species are accompanied by a map highlighting distribution within Monterey George West, a long-time resident of Alaska County. The accounts vary in length but are who arrived there in 1963, knows the state consistent with what is known about the

274 2004] BOOK REVIEWS 275 species there. Many photographs are repro- haps the Firefly Encyclopedia purchased copy- duced, mainly for vagrants or rarities, as verifi- rights. Some format and layout are also the cation of the species identity. same for both encyclopedias. Of special interest are 2 pages of history of Both encyclopedias have a suite of contri- the California Condor (Gymnogyps californi- buting authors covering various chapters, some anus) that ranged into Monterey County until 80 in the older versus more than 140 in the 1980, and data on its recent reintroduction newer book, though many are the same people. into the county. Three pairs hatched wild-laid When the same authors give an account for a eggs in 2002. specific family in both books, much of the Appendix A is a chronology of species indi- material is the same, but this is to be expected cating the first Monterey record since 1900. considering space constraints for each family Other appendices cover unsuccessful introduc- account. The Firefly has a strange method of tions and escaped exotic species, selected rec- presenting bird names. Conventionally, the ords published in the first edition (1985) but Sandhill Crane, for example, is capitalized for not in this one, and lastly a checklist indicat- both names. The Firefly book uses an initial cap- ing the occurrence and status of each species ital letter for the first name but not the second. by month and duplicating the bar graph that The Firefly book marches through the bird accompanies each species account. For those world family by family using the older but interested in birds of California, in general, or more classical system devised by Alexander birding within Monterey County, in particular, Wetmore, the Wetmorian system, although this is a very useful book. there is a discussion of newer classifications based on molecular evidence. The molecular Firefly Encyclopedia of Birds. Edited by system (mainly DNA) is much harder to repre- Christopher Perrins. Firefly Books Ltd., sent because the families do not seem to fall Toronto, Canada. 2003. $59.95, hardcover; out in the same neat and somewhat clean cate- 640 pages, 2000 color photographs + range gories. Each family is accompanied by a “Fact- maps + hundreds of illustrations + glos- file” that briefly details the physical features, sary and index. ISBN 1-55297-777-3. distribution, evolutionary history, classification, some breeding biology, and conservation sta- In some ways this book is a disappointment tus for that family. This is most useful. Some despite all its acclaim. In part it is new mater- families have photo essays, such as the cranes, ial, especially the photographs, but in part it is showing the dance of the Japanese Crane. The a hybrid of 2 other books that Perrins also topical matter for each family follows a similar edited: Birds: Their Life, Their Ways, Their format and sequence. As an example, the dis- World published by the Reader’s Digest Asso- cussion topics for one of the better-known fami- ciation in 1979 (basically world bird families) lies, the Kingfishers, are form and function, and The Encyclopedia of Birds published by distribution patterns, diet, breeding biology, Facts on File in 1985 (basically world bird and conservation and environment. families). The Firefly Encyclopedia contains For my picky quarrel with the Firefly Ency- many of the same pieces of artwork as the pre- clopedia, it is a wonderful contribution, it is in vious books. For example, the heads of the print whereas the Reader’s Digest book is out various rails on page 208 of the Firefly Ency- of print, and it is within relatively easy mone- clopedia come from page 236 of Reader’s tary reach of most people. I recommend it. Digest Birds, while the artwork for the families of mesites, finfoots and seriemas, pages 219, Clayton M. White 222 and 223 in the Firefly Encyclopedia, comes Department of Integrative Biology from pages 158 and 159 of the older encyclo- Brigham Young University pedia. Perhaps this is to be expected because Provo, UT 84602 the same person edited the two books, or per- CONTENTS

(Continued from back cover)

Book Review The Animal Mind by James L. Gould and Carol Grant Gould...... Serge Lariviere 273 National Geographic Photography Field Guide: Birds by Rulon E. Simmons ...... Clayton M. White 274 A Birders Guide to Alaska by George C. West...... Clayton M. White 274 Monterey Birds: Status and Distribution of Birds in Monterey County, California by Don Roberson ...... Clayton M. White 274 Firefly Encyclopedia of Birds by Christopher Perrins ...... Clayton M. White 275

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