Full Issue, Vol. 65 No. 2

Western North American Naturalist

Volume 65 Number 2 Article 21

4-29-2005

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NOTES ON THE BIOGEOGRAPHY AND DORSAL COLORATION OF CICINDELA AMARGOSAE DAHL (COLEOPTERA: CARABIDAE)

Michael G. Kippenhan1,2

ABSTRACT.—The widely distributed and fragmented populations of the tiger beetle Cicindela amargosae are documented for dorsal coloration, elytral maculation, habitat, and adult escape behavior. Currently, there are 2 recognized subspecies, C. a. amargosae and C. a nyensis. The analysis of populations indicated that the variation in dorsal coloration did not coincide with the accepted subspecific criteria for this species, thus illustrating the difficulty in applying a subspecific category unequivocally to tiger beetles.

Key words: Cicindela amargosae, tiger beetle, subspecies, phenotypic variation, habitat.

Cicindela (Cicindelidia) amargosae Dahl is 1982, Werner 1994); however, Leffler (1979) a polytypic species associated with grass mar- presented distinguishing morphological and gins of moist, often alkali-encrusted areas of geographical attributes for the 2 species. Apart drainages in southern Oregon, western Nevada, from studies by Dahl (1939) and Rumpp (1956), and eastern California (Fig. 1, Table 1). There are C. amargosae has received little attention in 2 recognized subspecific forms: Cicindela entomological literature except for Leffler (1979), a. amargosae and C. a. nyensis Rumpp. Dahl who included this species as part of the Pacific (1939) described C. willistoni amargosae from Northwest tiger beetle fauna, and Freitag (1999), “four miles north of Furnace Creek, Death who listed all populations for this species out- Valley, Inyo County California.” This subspecies side Death Valley as C. a. nyensis. was separated from other geographical forms In a geographic outline of the populations of the C. willistoni group by the combination of C. amargosae, Rumpp (1956) found C. a. of bright blue-green dorsal coloration, macula- amargosae, along with C. w. pseudosenilis and tion pattern reduced to an apical lunule, and C. californica pseudoerronea Rumpp, isolated elytral punctation (Dahl 1939). Interestingly, along the natural springs associated with the Dahl (1939) believed this species to be a sub- alkali flats north of Furnace Creek, Death Valley, species of C. willistoni even though C. willis- California. Cicindela a. amargosae was not found toni pseudosenilis W. Horn was sympatric at downstream of Furnace Creek at Saratoga the type locality. In a study of the Death Val- Springs, even though C. w. pseudosenilis, C. c. ley, California, tiger beetles, Rumpp (1956) pseudoerronea, and a 3rd species, C. n. nevadica elevated C. amargosae to specific rank based LeConte, were present (Rumpp 1956). Inter- on the observations that it did not interbreed estingly, Rumpp’s tiger beetle collection at the with C. w. pseudosenilis at the type locality California Academy of Sciences includes a and there was a lack of hybrids. Utilizing color series of C. a. amargosae collected at Saratoga and body length as diagnostic criteria, Rumpp Springs in 1963. Rumpp (1956) found C. a. (1956) described C. amargosae nyensis from nyensis associated with the intermittent chan- “1.6 miles south of Springdale, Nye County, nels of the Amargosa River near Springdale, Nevada.” In addition to the allopatry from the Nye County, Nevada. Although the Death Val- nominate form, this subspecies was character- ley and Springdale populations are in close ized by its matte-black dorsal coloration, “softer” proximity to one another (<80 km), small elytra relative to the nominate form, and mountain ranges apparently are geographical smaller overall body length. Various authors barriers between the 2 type localities. Rumpp have considered C. amargosae to be a sub- (1956) believed that populations connected to specific form of C. senilis G. Horn (Boyd et. al the Springdale and Furnace Creek populations

11425 S.E. Claybourne St., Portland, OR 97202. 2C.P. Gillette Arthropod Biodiversity Museum, Colorado State University, Fort Collins, CO 80523.

145 146 WESTERN NORTH AMERICAN NATURALIST [Volume 65

(1956) assertion that dorsal color variation was due to hybridization. Because most cicindelid taxonomy relies solely on morphological characters to determine subspecific status, the consideration of ecophenotypic characters and their role in cicindelid color expressions (Pearson Lk. Alvord Lk. Warner and Vogler 2001, Schultz 2001) is often left un- 1 explored. The objective of this study is to review 2 the current distribution and habitat of C. amargosae populations throughout its range while 3 evaluating the correlation between distribu- Lk. Surprise tion and dorsal coloration and maculation. 4 METHODS AND MATERIALS 5 Lk. Lahontan 6 I reevaluated the criteria utilized by Rumpp (1956) to differentiate the subspecific forms of 7 C. amargosae. These include (1) geography 8 and allopatry, (2) dorsal coloration and elytra Lk. Rennie 10 maculation, (3) habitat and adult escape be- 9 havior, and (4) total body length. To evaluate 11 each of these criteria, I collected individuals AmargosaAmargosae R. R. of C. amargosae from locations throughout the 12 species range. In addition to specimens cap- 13 tured in the field, pinned material including the type of C. a. nyensis and paratypes of C. a. amargosae were examined from the California Academy of Sciences Collection (San Fran- cisco, California).

RESULTS AND DISCUSSION Fig. 1. Known populations of Cicindela amargosae and pluvial lakes (numbers correspond to Table 1). Geography and Allopatry Vestiges of the ancient lakes that once occu- by the Amargosa River would have individuals pied the Great Basin offer an understanding of expressing a variety of dorsal coloration indica- the present-day distribution of C. amargosae tive of hybridization. Accordingly, the popula- (Fig. 1). Leffler (1979) believed that C. amar- tions downstream of Springdale at Ash Mead- gosae inhabited the shores of pluvial Lake ows, Nye County, Nevada, were categorized as Lahontan and associated lake basins. The “hybrid,” inasmuch as individuals matched the reduction of these pluvial lakes in post-Pleis- description of both subspecific forms (Rumpp tocene times to smaller remnant lakes (Reheis 1956; Table 2). In addition, Rumpp (1956) con- 1999) can be considered a valid explanation for sidered as “hybrids” populations from north- the widespread and fragmented distribution of western Nevada and adjacent California that current populations in the northern half of the exhibited dorsal coloration described as “black, species range. Historically, it is likely the local- green and bronze.” Rumpp (1956) apparently ized distribution of the Death Valley, Califor- was unaware of C. amargosae populations out- nia, populations had a much more widespread side California and Nevada; however, Leffler range along the shores of pluvial Lake Manly, (1979) examined populations from Lake and which at one time was close to 161 km long Harney Counties, Oregon, all of which were (Sharp and Glazner 1997). Populations close to placed as C. a. nyensis. Tecopa, Inyo County, California, are associated During a study of the current distribution with remnants of ancient Lake Tecopa, which of C. amargosae in 2002 and 2004, I made num- occupied the area south of Death Valley until erous observations that contradicted Rumpp’s 500,000 years ago (Sharp and Glazner 1997). 2005] BIOGEOGRAPHY OF CINCINDELA AMARGOSAE 147

TABLE 1. Known populations of Cicindela amargosae (arranged north to south). Location Source 1. OR: Harney Co., Alvord Hot Springs MGKC, CSUCa 2. OR: Lake Co., Crumb Lake Leffler 1979b 3. CA: Modoc Co., Surprise Lake CASCc 4. NV: Wascoe Co., Gerlach CASC, MGKCd 5. CA: Lassen Co., Honey Lake CASC, MGKC 6. NV: Washoe Co., Truckee Meadows LaRivers 1946 7. NV: Esmeralda Co., Fish Lake CASC 8. NV: Nye Co., Springdale CASC, MGKC 9. CA: Inyo Co., Death Valley Nat. Mon., Furnace Creek CASC, MGKC 10. NV: Nye Co., Ash Meadows NWR CASC, MGKC 11. CA: Inyo Co., Shoshone CASC 12. CA: Inyo Co., Tecopa Hot Springs CASC 13. CA: Inyo Co., Death Valley Nat. Mon., Saratoga Springs CASC aColorado State University Collection, Fort Collins, CO bLiterature sources only cCalifornia Academy of Sciences, Golden Gate Park, San Francisco, CA dMichael G. Kippenhan Collection, Portland, OR

The Death Valley and Tecopa populations, along implications of these 2 color forms. In an eco- with populations not directly associated with logical role, color, elytral maculation, and ven- pluvial Lake Lahontan, such as Springdale and tral setae function as the primary mechanisms Ash Meadows, Nye County, Nevada, may have by which adult tiger beetles regulate body arrived via watercourses originating from the temperature (Schultz and Hadley 1987, Pear- shores of pluvial lakes and are currently asso- son and Vogler 2001). While C. a. amargosae ciated with the Amargosa River. The Fish Lake, and C. a. nyensis exhibit a very small degree of Esmeralda County, Nevada, population is asso- variation in elytral maculation and no differ- ciated with remnants of pluvial Lake Rennie. ence in ventral setae, it is the dorsal (Table 2) In June 2004 I searched for suitable habitats and ventral (Table 3) coloration that demon- along Highway 140 between Lakeview, Lake strates a marked degree of separation. While County, Oregon, and Denio, Humbolt County, studies of the thermoregulatory performance Nevada, for additional populations of C. amar- of C. amargosae’s color morphs have yet to be gosae. Even though this area has small rem- undertaken, the southwestern United States nants of pluvial lakes and alkali areas, such as tiger beetle Cicindela hornii Schaupp can be Bog Hot Valley, I discovered no populations of utilized as a model, as populations of this C. amargosae. Due to (1) the large areas of in- species have individuals expressing similar hospitable habitat between the fragmented suit- morphs of green, blue, or black dorsal color- able habitat and populations of C. amargosae, ation. Interestingly, Schultz and Hadley (1987) and (2) the general limited dispersal abilities found that the 3 color morphs of C. hornii of Cicindela sp. (Pearson and Vogler 2001), it illustrated no significant difference in regard appears unlikely that gene flow exists between to heat gain from shortwave radiation. There- populations north of the Inyo County, Califor- fore, assuming that the green and black dorsal nia, and Nye County, Nevada, populations. coloration of C. amargosae have similar thermoregulatory performance as the color morphs of Dorsal Coloration and C. hornii, evolutionary forces outside ther- Elytral Maculation moregulation have resulted in the expressed Dorsal coloration and the extent of elytral variation of dorsal coloration in C. amargosae. maculation are common morphological char- When populations of C. amargosae are ex- acters used in identifying and separating adult amined, it becomes clear that most populations tiger beetles and have traditionally been used have individuals expressing numerous dorsal to define subspecies (Pearson and Vogler 2001). color morphs (Table 2). Rumpp (1956) believed Such is the case with C. amargosae, where that populations expressing coloration of both Rumpp (1956) characterized C. a. amargosae subspecies were “hybrid,” including individuals as “green” and C. a. nyensis as “black” without with dark green dorsal coloration found at providing evidence regarding evolutionary Honey Lake, Lassen County, California, and 148 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 2. Dorsal coloration and number of specimens of Cicindela amargosae examined and relative percent of dorsal coloration.

______Dorsal coloration Location Collection Total # Blue Green-blue Green Dark green Black Alvord Hot Springs CSUC, MGKC 164 2 (1%) 162 (99%) Surprise Lake CASC 4 4 (100%) Honey Lake CASC, MGKC 43 3 (7%) 40 (93%) Gerlach CASC, MGKC 30 25 (83%) 5 (17%) Fish Lake CASC 26 26 (100%) Springdale CASC, MGKC 41 1 (2%) 40 (98%) Ash Meadows CASC, MGKC 73 7 (10%) 35 (48%) 5 (6%) 26 (36%) Furnace Creek CASC, MGKC 188 128 (68%) 59 (31.5%) 1 (0.5%) Saratoga Springs CASC 14 2 (14%) 5 (36%) 1 (7%) 6 (43%) Shoshone CASC 3 3 (100%) Tecopa Hot Springs CASC 59 7 (12%) 13 (22%) 7 (12%) 32 (54%)

Gerlach, Wascoe County, Nevada. Apparently, Habitat and Adult any connection in geologic time between the Escape Behavior drainage of Honey Lake and Gerlach with The habitat of C. a. amargosae at Furnace Furnace Creek appears unlikely (Reheis 1999). Creek, the type locality, consists of narrow In addition, the dark green dorsal coloration is rivulets where trickling water passes through associated with bronze ventral coloration, alkali-encrusted soil. This area is conspicuous which is not found in any of Rumpp’s (1956) due to the lack of vegetation and to the alkali other so-called “hybrid” populations, and therefore the plausibility of hybridization as a source encrustations that make the soil covering com- of color expression in these populations is in pletely white (Fig. 2), creating blinding reflec- question. tions during periods of sunlight. At this loca- The character state of elytral rigidity was tion C. a. amargosae adults are encountered utilized by Rumpp (1956) when differentiating along the exposed waterways where their green C. a. amargosae and C. a. nyensis. An initial dorsal coloration makes them conspicuous on analysis of living adult specimens indicates a the alkali surface. When disturbed, adults took correlation between elytral color and elytra off in strong flights between 2 m and 6 m in a rigidity; however, while this characteristic’s relatively straight pattern. Individuals would potential as a quantifiable factor in subspecific most often fly toward open, moist soil and were determination is apparent, a method of mea- active upon landing. surement has yet to be devloped. The type locality of C. a. nyensis at Spring- An additional consideration not discussed dale, Nevada, is part of the broad flood plain by Rumpp (1956) is the dorsal coloration of of the Amargosa River and is covered with sympatric tiger beetle species. Schultz (1986) alkali-resistant plants, leaving only small areas documented convergent dorsal coloration for (<12 cm2) of bare ground. A large portion of numerous populations of C. oregona LeConte the area is covered by standing water during and C. tranquebarica Herbst in the southwest- the seasonal period of adult activity (March to ern U.S. In each instance the dorsal color of May). The open areas are characterized by each species corresponded with its associated dark, muddy soil with little or no evidence of substrate color; as a result, numerous subspe- alkali development. Adults of C. a. nyensis cific names have been attributed to these pop- occur at the base of vegetation patches or on ulations. An examination of sympatric species open areas, often in standing water. When dis- present at the above sites indicates similar turbed, individuals took off in a short (<2 m) color forms (Table 4). For example, at Furnace flight that was erratic in direction. These flights Creek, the 3 species that inhabit the open are characterized by sharper, vertical ascents alkali flats, C. a. amargosae, C. c. pseudoer- terminating with the individual dropping back ronea, and C. w. pseudosenilis, all exhibit iri- into the grass, most often with no post-landing descent dorsal coloration varying from green movement. This behavior probably arose from to dark blue and may represent a case of con- the necessity to clear grass when ascending and vergent evolution. landing in areas that are partially concealed by 2005] BIOGEOGRAPHY OF CINCINDELA AMARGOSAE 149 to purple reflections to purple reflections green-blue to dark blue green to dark green to purple bronze-brown brown to black-brown dark green to black brown-green to brown brown to black-brown bronze-brown brown-green to brown black reflections to purple reflections reflections to purple reflections found at Furnace Creek, Inyo. Co., California; Gerlach, found at Furnace Cicindela amined. Cicindela californica pseudoerronea Cicindela willistoni pseudosenilis Cicindela a. amargosae Cicindela willistoni echo Cicindela h. haemorrhagica Cicindela a. amargosae Cicindela tenucincta Cicindela h. haemorrhagica Cicindela willistoni echo Cicindela terricola imperfecta Cicindela amargosae nyensis ex Cicindela amargosae 4. Dorsal coloration of associated species ABLE T ascoe Co., Nevada; and Alvord Hot Springs, Harney Oregon. urnace Creek to purplereflections to purple reflectionsto purple strong copper reflectionsblue to purple to purple strong copper reflections to purple reflections strong green reflections blue-purple to purple strong green reflections blue-green reflections copper reflections dark reflections LocationF Gerlach Alvord Hot Springs Species Dorsal coloration W 3. Ventral coloration and specimens of 3. Ventral ABLE T urnace Creek blue-green to purple to blue-green with purple to blue-green with purple with dark black with strong LocationAlvord Hot SpringsGerlach dark blue-greenSpringdale black with blue-green GenaeF green with copper black with blue-green dark blue-green dark green to purple with Proepisternum black with blue-green black with blue-green dark green to purple with black with blue-green green to blue Metaepisternum black with blue-green black with blue-green dark green with Abdomen black with blue-green Femur 150 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Fig. 2. Habitat of Cicindela amargosae at Furnace Creek, the type locality, Death Valley National Monument, Inyo Co., California. grass, thus offering a relatively high level of June 2002 and 2004, I often observed adults of immediate cover. This location is interesting C. a. nyensis at Alvord Hot Springs standing in in that as the season progresses (June) and shallow water in the cover of vegetation. When adult activity declines, the dry soil is covered disturbed, most individuals preferred to stay by a thick layer of alkali crust. within close proximity of the wet, grassy areas The habitat and habit of populations of C. with short, erratic flights. Adults that flew into a. nyensis outside the type locality were deter- the open playa were active upon landing and mined to have similar characteristics. Approxi- soon returned to the vicinity of the water. mately 80 km downstream from Springdale, Honey Lake appeared similar to Alvord Hot the habitat of the Ash Meadow population is Springs; however, since only 1 specimen was almost identical to Springdale and is also asso- encountered, observations are inconclusive. ciated with the Amargosa River. The habitat of Due to a lack of water runoff on the playa, no Alvord Hot Springs is characterized by drain- suitable habitat or specimens were located at ages from hot springs, which form large pools the Modoc County location in June 2004. of standing water on the playa (Fig. 3). During However, the description of this habitat, as well 2005] BIOGEOGRAPHY OF CINCINDELA AMARGOSAE 151

Fig. 3. Habitat of Cicindela amargosae nyensis at Alvord Hot Springs, Harney Co., Oregon.

as adult behavior (Smith and Bronson 2003), Total Body Length appears similar to the Alvord Hot Springs site. Lengths of adults were also utilized by The Gerlach population occurs in a habitat Rumpp (1956) to differentiate C. a. amargosae that can best be described as intermediate to (average length male = 11.4 mm, n = 23; female Furnace Creek and Ash Meadows. This loca- = 12.2 mm, n = 46) and C. a. nyensis (average tion is characterized by a large, open expanse length male = 10.4 mm, n = 23; female = 10.9 of alkali-encrusted soil bordered by very dense mm, n = 27). Average length of adults at the vegetation and small areas of standing water. Gerlach was 11.3 mm (n = 11) in males and Here, adults of C. amargosae were encountered 12.1 mm (n = 6) in females. at the edges of vegetation and flew into the open expanses of alkali. This area did not have CONCLUSIONS the total lack of vegetation as did Furnace Based on the analysis of the current popu- Creek, but the open areas were much more lations of C. amargosae, I conclude that dorsal exposed than either Springdale or Alvord Hot color does not necessarily correlate with geo- Springs. Similar to Gerlach, the Tecopa local- graphical distribution of subspecific forms as ity is also characterized by a large, open alkali defined by Rumpp (1956), and, in fact, most area bordered by dense vegetation, and this populations have individuals expressing a vari- location also supports individuals exhibiting ety of colors (Table 2). The correlation between color of both subspecies (Table 2). Neither the color and overall body length is consistent Fish Lake nor Saratoga Springs locations were throughout the range of C. amargosae, with examined during the course of this study. green dorsal coloration coinciding with larger 152 WESTERN NORTH AMERICAN NATURALIST [Volume 65 average length, whereas black dorsal coloration University, Fort Collins). Collecting in Death occurs in individuals of smaller average body Valley National Monument was conducted length. Even though the Gerlach population is under permit number DEVA-2002-SCI-0012, unique for the high percentage of individuals overseen by Richard Anderson. with dark green dorsal and copper ventral coloration (Tables 2, 3), this population is best LITERATURE CITED assigned to the nominate subspecies based on its elytral rigidity, elytral maculation, and over- BOYD, H.P., AND ASSOCIATES. 1982. Checklist of the Cicin- delidae. The tiger beetles. Plexus Publishing Com- all body length. pany, Marlton, NJ. 31 pp. Whatever the biological function of the DAHL, R.G. 1939. A new California tiger beetle (Cole- specific colors, there is no doubt that selection optera—Cicindelidae). Bulletin of the Brooklyn Ento- is producing convergence in color patterns mological Society 34:221–222. and color pattern variation among C. amargosae FREITAG, R. 1999. Catalogue of the tiger beetles of Canada and the United States. NRC Research Press, Ottawa, populations. It is conceivable that isolated pop- ON, Canada. 195 pp. ulations of C. amargosae could lose morphs LARIVERS, I. 1946. An annotated list of the Cicindelidae through drift such that the monomorphic pop- known to occur in Nevada (Coleoptera). Pan-Pacific ulations of C. amargosae are a result of stochas- Entomologist 22:135–141. LEFFLER, S.R. 1979. Tiger beetles of the Pacific North- tic rather than deterministic processes. The west (Coleoptera: Cicindelidae). Doctoral disserta- hybrid populations of Rumpp (1956) are those tion, University of Washington, Seattle. 791 pp. that retain the original genotypic variation for PEARSON, D.L., AND A.P. VOGLER. 2001. Tiger beetles: the color pattern and presumably remain under evolution, ecology and diversity of the cicindelids. some sort of stabilizing selection (T. Schultz Cornell University Press, Ithaca, NY. 332 pp. REHEIS, M. 1999. Extent of Pleistocene lakes in the west- personal communication). Therefore, the inter- ern Great Basin. U.S. Geological Survey Miscella- population variation of dorsal coloration is more neous Field Studies Map MF-2323, U.S. Geological likely a result of an evolutionary response to Survey, DeNevadaer, CO. ecological factors rather than hybridization. RUMPP, N.L. 1956. Tiger beetles of the genus Cicindela in southwestern Nevada and Death Valley, California, Instances such as those described here for C. and the description of two new subspecies (Cole- amargosae illustrate the complexity of colora- optera—Cicindelidae). Bulletin of the Southern Cal- tion as expressed in adult Cicindela. ifornia Academy of Science 55:131–144. SCHULTZ, T.D. 1986. Role of structural colors in predator avoidance by tiger beetles of the genus Cicindela ACKNOWLEDGMENTS (Coleoptera: Cicindelidae). Bulletin of the Entomo- logical Society of America 32:142–146. Susan Agre-Kippenhan, Boris Kondratieff, ______. 2001. Tiger beetle defenses revisited: alternative Jeff Owens, Jason Schmidt, and Calvin Water- defense strategies and coloration of two Neotropical man helped collect specimens during the course tiger beetles, Odontocheila nicraguensis Bates and of this study. Dave Brzoska (Naples, FL) pro- Pseudoxycheila trasalis Bates (Carabidae: Cicindeli- nae). Coleopterists Bulletin 55:153–163. vided collecting information. David Kavanaugh SCHULTZ, T.D., AND N.F. HADLEY 1987. Structural colors of and Roberta Brett (CASC, San Francisco, CA) tiger beetles and their role in heat transfer through provided facilities and access to the N.L. integument. Physiological Zoology 60:737–745. Rumpp collection. C. Barry Knisley (Randolph SHARP, R.P., AND A.F. GLAZNER. 1997. Geology underfoot in Death Valley and Owens Valley. Mountain Press Macon College, Ashland, VA), Richard Freitag Publishing Co., Missoula, MT. 321 pp. (Lakehead University, Thunder Bay, ON, Can- SMITH, C.R., AND L.R. BRONSON. 2003. Distribution, habi- ada), Dave L. Pearson (Arizona State University, tat preferences and seasonality of tiger beetles, genus Tempe), and Thomas Schultz (Denison Uni- Cicindela (Coleoptera: Cicindelidae) in Surprise Val- versity, Granville, OH) reviewed the manu- ley, Modoc County, California. Cicindela 35:1–22. WERNER, K. 1994. Die Käfer der Welt. Volume 20. Sciences script and offered many practical and insight- Nat, Venette, France. 196 pp. ful comments. This study would not have been possible without the direction, support, and Received 8 March 2004 patience of Boris C. Kondratieff (Colorado State Accepted 9 September 2004 Western North American Naturalist 65(2), © 2005, pp. 153–163

COMPETITIVE INTERACTIONS BETWEEN ENDANGERED KIT FOXES AND NONNATIVE RED FOXES

Howard O. Clark, Jr.1,2,3, Gregory D. Warrick4, Brian L. Cypher1, Patrick A. Kelly1, Daniel F. Williams1, and David E. Grubbs2

ABSTRACT.—We investigated interference and exploitative competition between endangered San Joaquin kit foxes (Vulpes macrotis mutica) and nonnative red foxes (V. vulpes). Seven kit foxes and 16 red foxes were radio-collared and tracked via radiotelemetry near Lost Hills, California. One kit fox was killed by a red fox. Home ranges of the 2 species did not overlap extensively. Although both species used similar habitats, they used different parcels of land. Kit foxes and red foxes primarily consumed rodents on the study site, and dietary overlap was considerable. Red foxes also may have been using dens formerly used by kit foxes. Thus, red foxes were engaging in both interference and exploitative competition with kit foxes, and red foxes constitute a potentially significant threat to kit foxes. Coyotes (Canis latrans) co-occur with kit foxes and may limit red fox abundance and distribution. Therefore, although they occasionally kill kit foxes, the presence of coyotes may benefit kit foxes by excluding red foxes.

Key words: California, competition, endangered species, kit fox, red fox, Vulpes macrotis mutica, Vulpes vulpes.

The San Joaquin kit fox is a federally en- from red foxes have been documented. Ralls dangered and state threatened species occur- and White (1995) reported 2 San Joaquin kit ring in the San Joaquin Valley, California fox mortalities due to red foxes. Also, red foxes (United States Fish and Wildlife Service 1998). have been observed using dens previously The historic range of the San Joaquin kit fox occupied by kit foxes (B. Cypher personal ob- has been significantly reduced by habitat loss servation). Other potential impacts include due to agricultural, industrial, and urban de- competition for food and disease transmission velopment. Remaining kit fox populations are (Cypher et al. 2001). Red foxes also have been threatened by continuing habitat conversion, found to adversely affect other fox species such as well as rodenticide use and interspecific as arctic foxes (Alopex lagopus; Frafjord et al. competition (United States Fish and Wildlife 1989, Hersteinsson and Macdonald 1992) and Service 1998). Nonnative red foxes are increas- swift foxes (V. velox; A. Moehrenschlager per- ing in abundance in the San Joaquin Valley sonal communication). Thus, it is important to (Jurek 1992, Lewis et al. 1999) and potentially quantify competitive interactions between kit foxes and red foxes to determine whether red could compete with kit foxes. Competitive in- foxes are a potential threat to remaining kit fox teractions between kit foxes and red foxes have populations. not been investigated. We examined competitive interactions be- Red foxes were introduced into the Sacra- tween San Joaquin kit foxes and nonnative red mento Valley of California from the midwest- foxes near Lost Hills, California, during 1998– ern United States in the 1870s (Grinnell et al. 1999. Our objectives were (1) to examine 1937, Lewis et al. 1999) and since have spread sources of mortality and space use patterns of as far south as San Luis Obispo, Orange, and both species to determine whether interfer- Los Angeles Counties, California (Jurek 1992). ence competition was occurring, and (2) to Red foxes also have appeared throughout the examine habitat use and food habits of both San Joaquin Valley, including habitats occu- species to determine whether exploitative pied by kit foxes. Adverse impacts to kit foxes competition was occurring.

1California State University–Stanislaus, Endangered Species Recovery Program, 1900 North Gateway Boulevard, Suite 101, Fresno, CA 93727. 2Department of Biology, California State University–Fresno, 2555 East San Ramon Avenue, Fresno, CA 93740. 3Corresponding author: H.T. Harvey & Associates, 423 West Fallbrook, Suite 202, Fresno, CA 93711. 4Center for Natural Lands Management, Box 20696, Bakersfield, CA 93390.

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METHODS veloped, significant expanses of natural vegetation typical of the Valley Grassland are present. Study Area Field Methods We conducted our study along an approximately 32-km segment of the California Aque- Kit foxes were captured during the non- duct (aqueduct) near the community of Lost breeding season (April–September) using Toma- Hills, Kern County, California (Fig. 1). Kit foxes hawk™ wire-mesh traps (38 × 38 × 107 cm; and red foxes co-occur in this area. The study Tomahawk, MI) baited with canned mackerel, area is predominantly flat with elevations rang- wieners, bacon, or chicken. We captured red ing from approximately 80 m in the east to 150 foxes during the dispersal season by plunging m along the Lost Hills anticline. The Lost Hills, them from drainage culverts into handling forming the western edge of the study area, are bags. The plunger consisted of lengths of plas- gentle, rolling hills that run in a northwest to tic pipe attached together with a foam ball southeast direction paralleling the aqueduct. taped to an end (O’Farrell 1987). Foxes were Climate is characterized by hot, dry summers ear-tagged, measured, weighed, and fitted with and wet, cool winters with thick fog (National radio-collars (Advanced Telemetry Systems, Climatic Data Center 2000). Weather data re- Isanti, MN). Collars contained mortality sen- corded 40 km east of Lost Hills in Wasco, Cal- sors that activated after 8 hours of nonmove- ifornia, indicate that average daily maximum ment. Each radio-collar weighed approxi- temperatures range from 13.4°C in December mately 50 g, or <3% of the animal body mass to 37.5°C in July, and average daily minimums (Cypher 1997). We released the foxes at their range from 2.1°C in December to 18.7°C in individual capture sites and then radio-tracked July. Precipitation, which averages 18.6 cm them from January 1998 to December 1999 annually, was 41.6 cm in 1998 and 14.7 cm in (Clark 2001). 1999. Radio-collared foxes found dead were ne- cropsied to determine cause of death. If the A strip of habitat approximately 60 m wide fox had contusions caused by tooth punctures, occurs along both sides of the aqueduct. This we considered predators the cause of death habitat is typical of Valley Grassland vegeta- (Roy and Dorrance 1976). When possible, we tion (Heady 1977), with red brome (Bromus measured distances between canine puncture madritensis) and filaree (Erodium spp.) domi- wounds to determine which species caused nating the herbaceous vegetation. Common the death (Disney and Spiegel 1992). If the shrubs include desert saltbush (Atriplex poly- cause of death could not be determined carpa) and spiny saltbush (A. spinifera). Honey because the carcass was badly decomposed or mesquite (Prosopis glandulosa) occurs within scavenged, it was classified as unknown. the southern portion of the study area, and a To determine space use patterns, foxes were few feral almond and pistachio trees are found radio-tracked weekly using 2 truck-mounted in areas where the aqueduct borders orchards. null tracking systems with paired 2-element Farmland covers most of the study area outside antennae (White 1985). Stations were located the aqueduct corridor. Major crops include along access roads of the aqueduct and sepa- cotton, barley, almonds, and pistachios. Less rated by approximately 800 m. Researchers at abundant crops are alfalfa, onions, lettuce, water- 2 adjacent stations simultaneously took bear- melon, olives, tomatoes, and vineyards. Annual ings on foxes. Four azimuths (referencing true crops are typically planted in late winter and north) were obtained: the azimuth to the fox harvested in the fall. After crops are harvested, from the south antenna, the azimuth to the fox the ground is disked and left bare until the fol- from the north antenna, the azimuth from the lowing spring. Pistachio and almond groves south antenna to the north antenna, and vice are drip-irrigated and harvested in October of versa. Survey grade GPS units (Pathfinder Pro each year. XR/XRS, Trimble Navigation Limited, Sunny- The west side of the study area is bounded vale, CA) were used to determine the locations by the Lost Hills oil field (approximately 1.5 km of the antenna stations. We initiated telemetry west of the aqueduct), which is primarily owned sessions approximately 1 hour before sunset and operated by private oil companies. Although and continued for approximately 4.5 hours. some portions of the oil field are heavily de- The first 3–5 hours after sunset is typically 2005] KIT FOX AND RED FOX INTERACTIONS 155

Fig. 1. Location of study site near Lost Hills, California. when kit fox activity is highest (Zoellick 1990). m (range = 74–1318 m) from the reference We collected locations on all collared foxes in transmitters. the vicinity, and successive locations on indi- To evaluate spatial overlap of foxes, we used vidual foxes were separated by ≥10 min. When the points collected throughout the year to bearings intersected <20 degrees, we discarded delineate home ranges and core areas for each locations. Locations of foxes were calculated fox, but only for those with >30 locations using methodology described in White and (Chamberlain and Leopold 2000). Home ranges Garrott (1990), and we entered these locations were delineated using the minimum convex into a GIS layer for analyses using ARC/INFO polygon (MCP) method, which provides a (Environmental Systems Research Institute, conservative estimate of space use. Core areas Redlands, CA). were delineated using the adaptive kernel Accuracy of the telemetry system was deter- method (Worton 1989). Areas within the home mined by having 2 observers gather bearings range that fell within the 25% probability con- on radio-collars (n = 30) placed at locations tour were considered core areas, defined as known only by a 3rd person. Locations derived the portion of an animal’s home range that from telemetry were then compared to the exceeded an equal-use pattern (Samuel et al. actual locations of the radio-collars (recorded 1985). Core areas can be used to denote central using a survey grade GPS unit) to determine the areas of consistent or intense use (Kaufmann average telemetric error (Springer 1979), which 1962). An ArcView program extension was used was 38 ± 7 m (range = 4–186 m). Eighty per- to delineate home ranges and core areas (Hooge cent of triangulated locations had an error of and Eichenlaub 1997). Spatial overlap between <45 m. Tracking vehicles averaged 552 ± 35 kit foxes and red foxes was calculated for each 156 WESTERN NORTH AMERICAN NATURALIST [Volume 65 animal by determining the percentage of each were grouped to simplify analyses. Horn’s index range that was overlapped by an individual of (Horn 1966), R0 , was calculated to determine the other species. the amount of overlap between diets. A Shan- To determine habitat use by the 2 fox spe- non index of dietary diversity, H′, was calcu- cies, we entered into an ARC/INFO layer the lated for each species. A 2 × 10 contingency habitat information gathered using GPS units, table chi-square test was conducted on the United States Geological Survey maps, and dietary data, and a 2 × 2 contingency table chi- ground mapping. Fox locations were plotted in square test was conducted on each item to ArcView, and each location was assigned a determine if proportional use by the 2 fox habitat type. Only those kit foxes and red foxes species was similar (Zar 1999). with overlapping home ranges were included in the habitat selection analysis. In 1998 home RESULTS range overlap between species occurred only Causes of Mortality in the southern portion of the study area, and in 1999 only in the northern portion of the During 1998–1999 we captured and radio- study area. One adult male kit fox in 1998 with collared 4 adult (2 female, 2 male) and 3 juve- an analyzed overlapping home range with a nile male kit foxes, and 16 red fox juveniles (10 red fox had an analyzed overlapping home females, 6 males). It is likely that representa- range in 1999; all other foxes were different tives from all kit fox and red fox family units individuals. To ensure data independence, we were radio-collared during this 2-year period. selected a single random location per fox per Four radio-collared kit foxes (2 adults, 2 juve- telemetry session (Swihart and Slade 1985). niles) were killed, 3 (1 adult, 2 juveniles) by Available habitat was defined as being within coyotes and 1 adult by a red fox. Eleven radio- 1.6 km of the aqueduct and 1.6 km from the collared red foxes were found dead, 9 killed by most southerly and most northerly fox locations. coyotes. Cause of death could not be deter- Utilization-availability analysis was conducted mined conclusively for 1 red fox (although prob- using the method described in Neu et al. (1974) ably a predator kill). The signal from the collar and Byers et al. (1984). To test whether foxes of another was emanating from the aqueduct used each habitat category in proportion to its and this fox was presumed to be dead. occurrence within the available area, we used Spatial Overlap the chi-square method described in Neu et al. (1974). In 1998 we delineated space use for 4 kit Habitat types included orchard, row crops, foxes and 4 red foxes. The home ranges of 3 kit aqueduct right-of-way (ROW), vineyard, grass- foxes were not overlapped by any radio-collared land, residential, and other. Orchards included red foxes. The home range of the remaining kit almonds, olives, and pistachios. Annual row fox was overlapped by 4 juvenile red foxes. crops included cotton, barley, and tomatoes. Average home range overlap was 31% (range Residential referred to any farmhouse, equip- 14%–48%) for the kit fox and 55% (range 40%– ment staging area, or farm equipment storage 81%) for the red foxes. The core area for this yard. The category “other” included small par- kit fox was partially overlapped by the home cels of tilled and miscellaneous land. Habitat range of 1 red fox, but core areas of the 2 types differed between 1998 and 1999 due to species did not overlap. The adult male kit fox fox home range overlap occurring in different with a home range overlapped by 4 juvenile red portions of the study area. foxes moved 10 km north in December 1998 To assess overlap in food use, we analyzed to pair bond with an adult female kit fox (see scats collected from trapped foxes and known Clark 2003). He remained in the area through- fox dens. A scat is defined as all fecal material out 1999. deposited in 1 event. Scats were oven-dried In 1999 space use was delineated for 10 red for 24 hours at 60°C to facilitate handling and foxes and 4 kit foxes (2 adults and 2 juveniles). to destroy cysts of zoonotic parasites. Prey re- The kit foxes were members of the same fam- mains were identified using hairs (Mayer 1952, ily group. Home ranges of 9 of the red foxes Stains 1958) and by comparing teeth, bones, did not overlap home ranges of any radio-col- scales, skin, exoskeletons, and seeds with ref- lared kit foxes. The home range of the remain- erence specimens (Roest 1991). Food items ing red fox overlapped home ranges of the 4 kit 2005] KIT FOX AND RED FOX INTERACTIONS 157 foxes. Average overlap was 24% (range 14%– 1999 use of the aqueduct ROW and orchards 36%) for the kit foxes and 11% (range 5%–14%) by kit foxes was higher than expected while for the red fox. Core areas for all 4 kit foxes use of row crops and other habitats was lower were overlapped by the home range of the red than expected (Fig. 3). For red foxes in 1999, fox, but the core area of the red fox was over- use of the aqueduct ROW was higher than lapped by the home range of only 1 kit fox. expected while use of row crops was lower Core areas of the 2 species did not overlap. than expected (Fig. 3). During the study red On 3 occasions kit foxes and red foxes were foxes sometimes used residential areas, grass- located in the same general vicinity, providing lands, and vineyards, whereas kit foxes never an opportunity to observe interactions. It is were located in these habitats. unknown whether foxes not radio-collared or Diet other animals in the area (e.g., coyotes) influenced these movements. On 26 August 1998, In 1999 we collected 207 kit fox scats, with an adult kit fox and 4 juvenile red foxes were most (204) being found at known dens during located within 0.5 km of each other. During a April (32.4%), June (64.3%), and July (1.9%). 1-hour period the kit fox maneuvered south Rodents were the most frequently occurring through the 4 red foxes and continued south item in kit fox scats (88.4%), followed by insects away from them. One red fox also moved south, (18.4%), other arthropods (11.6%), leporids but for a shorter distance than that traveled by (8.7%), human-derived items (6.3%), and birds the kit fox. (1.9%). Species of rodents occurring in kit fox On 18 November 1998 we recorded an en- scats include house mice (Mus musculus, 34.3%), counter between 2 kit foxes and 1 red fox. An deer mice (Peromyscus maniculatus, 17.9%), adult male and an adult female kit fox were pocket gophers (Thomomys bottae, 9.7%), Cal- located within 250 m of a juvenile red fox dur- ifornia voles (Microtus californicus, 3.9%), har- ing a 20-minute period. The female kit fox vest mice (Reithrodontomys megalotis, 3.4%), moved toward the initial location of the red and San Joaquin pocket mice (Perognathus in- fox, while the red fox and the male kit fox ornatus, 1.5%). In addition, 27.0% of the scats moved away from each other. contained murid rodents that could not be On 30 September 1999 we observed a juve- identified to species, and 4.8% of the scats nile red fox as it moved in a direction away contained rodents that could not be identified from an approaching adult kit fox. It then to species. Insect species include field crickets moved back toward the kit fox and finally (family Gryllidae, 9.7%), grasshoppers (family away again. The shortest distance between the Acrididae, 4.4%), ants (family Formicidae, 4.4%), 2 foxes was approximately 300 m within a 1- and beetles (order Coleoptera, 2.9%). Other minute window. On 22 November 1999 these arthropod remains were not identifiable. Bird 2 foxes again were located in close proximity, remains in scats typically consisted of a few and both foxes moved away from each other. feathers and were not identified to species. The shortest distance between the 2 foxes was Human-derived items included plastic (1.9%), approximately 100 m. string (1.9%), paper (1.5%), and rubber (1.0%). In 1999 we gathered 140 scats from known Habitat Use red fox dens in February (10%), June (67%), Habitat use by kit foxes was disproportion- and September (23%). Murids were the most ate to availability in both 1998 (χ2 = 20.0, df frequently occurring item in red fox scats = 3, P < 0.01) and 1999 (χ2 = 86.4, df = 5, P (91.4%), followed by insects (16.4%), leporids < 0.01). Likewise, habitat use by red foxes (11.4%), birds (7.1%), and human-derived items was disproportionate to availability in both 1998 (4.9%). Species of rodents that occurred in red (χ2 = 240.6, df = 3, P < 0.01) and 1999 (χ2 = fox scats include California voles (31.4%), house 88.4, df = 4, P < 0.01). In 1998 use of or- mice (28.6%), deer mice (4.3%), pocket gophers chards by kit foxes was higher than expected (2.9%), and harvest mice (0.7%). In addition, while use of row crops and other habitats was 27.1% of the scats contained murid rodents lower than expected (Fig. 2). For red foxes in that could not be identified to species, and 6.4% 1998, use of the aqueduct ROW and orchards of the scats contained rodents that could not was higher than expected while use of row be identified to species. Insect species included crops was lower than expected (Fig. 2). In ants (7.9%), field crickets (7.1%), and beetles 158 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Fig. 2. Proportional availability and use of habitat types by kit foxes and red foxes at Lost Hills, California, in 1998. A plus (+) indicates habitats for which use was greater than expected, and a minus (–) indicates habitats for which use was less than expected.

(1.4%). Bird remains in scats typically consisted fox species was high. The Shannon diversity of a few feathers and were not identified to indices for kit fox and red fox diets were 0.91 species. Human-derived items included paper and 0.90, respectively. (2.8%), plastic (0.7%), string (0.7%), and rubber (0.7%). Most of the scats contained some vege- DISCUSSION tation, such as grass and seeds of brome. Four Interference Competition scats (2.8%) contained almonds, and 1 scat contained a barley seed head. Interference competition can consist of direct Proportional item use by kit foxes differed mortality, spatial exclusion, or avoidance behav- significantly from that of red foxes (χ2 = 78.0, ior. During this investigation, 1 kit fox was df = 9, P < 0.01; Fig. 4). Proportional use of killed by a red fox, as has been observed else- voles (χ2 = 47.7, df = 1, P < 0.01) and birds where (Ralls and White 1995). Red foxes are (χ2 = 4.6, df = 1, P = 0.03) was greater among larger than kit foxes (3–7 kg vs. 2–3 kg), and therefore kit foxes are at greater risk of injury red foxes than kit foxes. Conversely, propor- or death in agonistic interactions. Red foxes tional use of deer mice (χ2 = 12.9, df = 1, P < also have been reported to kill other fox species 0.01), gophers (χ2 = 5.0, df = 1, P = 0.03), χ2 such as arctic foxes (Frafjord et al. 1989, Bailey and other items ( = 3.9, df = 1, P = 0.05) was 1992) and swift foxes (A. Moehrenschlager per- greater among kit foxes than red foxes, and use sonal communication). χ2 of orthopterans ( = 3.3, df = 1, P = 0.07) Space use patterns of kit foxes and red foxes χ2 and arthropods ( = 2.9, df = 1, P = 0.09) on the study site provided some evidence of was marginally greater. Proportional use of spatial partitioning. Kit fox and red fox family χ2 house mice ( = 1.0, df = 1, P = 0.31), un- groups occupied separate areas, although some known murids (χ2 = 2.0, df = 1, P = 0.92), interspecific home range overlap was observed. and leporids (χ2 = 0.4, df = 1, P = 0.51) did Core areas were only rarely overlapped. We not differ significantly between kit foxes and could not determine whether the observed red foxes. Diets are identical if their R0 value partitioning was a result of antagonism or ex- = 1.0; a value of zero means the diets have no ploitative competition. dietary items in common. The calculated R0 Movement patterns of kit foxes and red foxes value between kit fox and red fox diets was monitored simultaneously suggested possible 0.87, indicating the diet overlap between the avoidance behavior, although there was no way 2005] KIT FOX AND RED FOX INTERACTIONS 159

Fig. 3. Proportional availability and use of habitat types by kit foxes and red foxes at Lost Hills, California, in 1999. A plus (+) indicates habitats for which use was greater than expected, and a minus (–) indicates habitats for which use was less than expected. to verify causation. Kit foxes were observed to The aqueduct ROW may have been selec- move away from red foxes on 2 occasions. tively used by both fox species due to a rela- Both instances involved adult kit foxes avoid- tively high abundance of food. Small mammal ing red foxes. Red foxes also were observed to diversity and abundance were higher along the move away from kit foxes on 2 occasions. aqueduct ROW relative to row crops and or- However, both instances involved juvenile red chards (Clark 2001). Also, jackrabbits (Lepus foxes. Although larger than adult kit foxes, californicus) and desert cottontails (Sylvila- juvenile red foxes may be more cautious than gus audubonii) were observed more frequently adult red foxes in interspecific encounters. in the aqueduct ROW compared with other Habitat use by kit foxes and red foxes gen- habitats (H. Clark personal observation). Con- erally was similar. Both species selectively used versely, food items did not appear to be abun- some habitats (e.g., aqueduct ROW, orchards) dant in orchards (Clark 2001). Thus, the reason and avoided others (e.g., annual row crops). for the disproportionately high use of orchards These similar habitat use patterns likely increase by both fox species is unclear. the potential for interspecific encounters. Both fox species may have avoided row crops due to relatively low food availability and fre- Exploitative Competition quent disturbance. Abundance of small mam- Exploitative competition occurs between 2 mals and other foods (e.g., leporids) was rela- sympatric species when both use the same re- tively low in row crops (Clark 2001). Also, row sources. Such overlapping use patterns can crops were subjected to weekly inundation result in resource availability being limited for during irrigation. This impedes foraging and 1 or both species. For kit foxes and red foxes, precludes the establishment of earthen dens. food and dens could be limiting factors. Over- Other frequent disturbances in row crops in- lapping habitat use patterns observed on our cluded cultivation, fertilization, and pesticide study site increased the potential for exploita- application. tive competition. However, competitive pres- Both fox species consumed a diversity of sure probably was reduced because the 2 food items. During prey surveys conducted in species frequently used different parcels of 1998 and 1999, murid rodents were the most land. Red foxes also used some habitats that frequently captured small mammals on the kit foxes did not use, which also may have study site (Clark 2001), and these rodents reduced competition. were important food items in the diets of both 160 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Fig. 4. Food item use by kit foxes and red foxes at Lost Hills, California, 1999. Bars are the proportion of scats with each food item. fox species. Kit foxes also commonly consumed ing and rearing young, diurnal resting cover, other rodents including deer mice and gophers. escaping predators, and avoiding temperature Both fox species commonly consumed inverte- extremes. Thus, dens are a critical aspect of kit brates, although use by kit foxes generally was fox ecology. Conversely, red foxes primarily higher than that of red foxes. This may be an use dens just during pup rearing. White et al. artifact of gathering scat samples at pupping (2000) reported that red foxes usurped several dens, where most of the scats probably were dens that were used by kit foxes during previous from pups. Pups are not very experienced at years at a study site. Red foxes have been ob- capturing prey and consume a high proportion served using kit fox dens in the city of Bakers- of invertebrates, which are more easily cap- field (B. Cypher unpublished data). Dens being tured than vertebrate prey (Cutter 1958). Red used by red foxes are unavailable to kit foxes. foxes exhibited high use of California voles, Similarly, red foxes are expanding into arctic fox which are a commonly used food item in many range in Norway and usurping arctic fox dens other parts of their range (Samuel and Nelson (Frafjord 2003). 1982). Voles were not captured during small Role of Coyotes in Kit Fox– mammal surveys (Clark 2001), and the habitat(s) Red Fox Interactions in which red foxes were finding voles is not known. Coyotes engage in both interference and The high overlap in kit fox and red fox diets exploitative competition with kit foxes. In many indicates potential competition for food re- locations coyotes are the primary cause of kit sources. However, frequencies of occurrence fox mortality (Ralls and White 1995, Spiegel of food items differed between species, indi- 1996, Cypher et al. 2000), as was the case on cating that both species used similar items but our study site. Coyotes also use some of the did not consume them in the same proportions. same foods as kit foxes (Cypher and Spencer These differences in diet would contribute to 1998). However, kit foxes have coevolved with resource partitioning, which would help ame- coyotes and have adaptive strategies for coex- liorate competition. isting with coyotes including year-round den Competition for dens was difficult to assess. use, efficient exploitation of certain food re- Kit foxes are obligatory den users and are sources not extensively used by coyotes (e.g., found in a den almost every day (Grinnell et al. heteromyid rodents; White et al. 1995, Cypher 1937, Morrell 1972). Dens are used for bear- and Spencer 1998), and possibly some level of 2005] KIT FOX AND RED FOX INTERACTIONS 161 habitat partitioning (White et al. 1995, Warrick not reduce the abundance of coyotes, which and Cypher 1998). In general, coyotes do not are the primary source of kit fox mortality. Red competitively exclude kit foxes, and both species foxes also may engage in exploitative competi- co-occur in most areas. tion with kit foxes through use of kit fox dens Coyotes also engage in both interference and overlapping habitat use and food habit and exploitative competition with red foxes. patterns. Furthermore, the 2 species are con- Coyotes are a significant source of mortality generic, increasing the potential for disease for red foxes ( Sargeant and Allen 1989). On our transmission. Thus, nonnative red foxes in the study site coyotes were the predominant cause San Joaquin Valley constitute a potentially sig- of mortality for red foxes, killing over half the nificant threat to kit foxes (Cypher et al. 2001). red foxes we monitored. The historic ranges of The threat of red foxes to kit foxes may be red foxes and coyotes may have been rela- somewhat ameliorated by several factors. Red tively disjunct (Kamler and Ballard 2002), and foxes are less adapted to arid lands than kit therefore red foxes may not have evolved stra- foxes and may have limited ability to colonize tegies for coexisting with coyotes. Thus, coy- kit fox habitat in which free water is scarce or otes may significantly influence red fox abun- not present. Also, the presence of coyotes may dance and distribution (Dekker 1983, Voigt limit red fox abundance in optimal kit fox and Earle 1983, Major and Sherburne 1987, habitat. Conservation of large blocks of quality Sargeant et al. 1987). arid habitat with healthy coyote populations, Because of the negative effects of coyote- as called for in recovery strategies for San Joa- fox interactions to red foxes, kit foxes actually quin kit foxes (U.S. Fish and Wildlife Service might benefit from the presence of coyotes 1998), should help limit impacts of red foxes (Cypher et al. 2001). Coyotes may limit red fox on kit foxes. abundance and even prevent them from colo- nizing certain areas within the kit fox range. ACKNOWLEDGMENTS Red foxes are rarely observed in areas where coyotes are abundant (Ralls and White 1995, This study was funded by the U.S. Bureau Spiegel 1996, Cypher et al. 2000). White et al. of Reclamation, U.S. Fish and Wildlife Service, (2000) cautioned against the removal of coy- California Department of Fish and Game, and otes in kit fox habitat where red foxes also are the Fresno State University Office of the Dean. present. In essence, coyotes may constitute a Field assistance was provided by E. Sheehan, biological control strategy for red foxes. Indeed, G. Gray, A. Harpster, S. Clifton, L. Hamilton, coyotes have been proposed as a control agent T. Sandoval, R. Zwerdling-Morales, R. Batie, for red foxes in coastal areas of California M. McFall, P. Morrison, M. Selmon, J. Smith, where foxes are preying on endangered Cali- C. Van Horn Job, and J. McMullin. GIS sup- fornia Least Terns (Sterna antillarum browni) port was provided by S. Phillips and P. Brandy, and California Light-footed Clapper Rails (Ral- and administrative support was provided by C. Lopez and C.G. Lopez. K. Ralls and S. Spie- lus longirostris levipes; Jurek 1992). Coyotes gel loaned equipment, and M. Constantnescu, also have been recommended for controlling R. Anthes, and G. Schales piloted aircraft during red foxes in the Prairie Pothole Region of North aerial surveys. Various landowners provided America to reduce red fox predation on duck access to their lands. The California Depart- nests (Sargeant and Arnold 1984). ment of Water Resources permitted admit- tance to the California Aqueduct. W. Standley CONCLUSIONS provided invaluable assistance with the kit fox Red foxes engage in interference competi- literature references. Four referees made help- tion with kit foxes through direct mortality ful and constructive comments on the manu- and possibly through spatial exclusion. Preda- script. This work was a partial fulfillment of a master’s thesis for H. Clark at Fresno State tor escape mechanisms of kit foxes, such as University. den use, may not be as effective against red foxes, as the relatively similar size of the 2 LITERATURE CITED species permits red foxes to enter kit fox dens.

Kit fox mortality attributable to red foxes may BAILEY, E.P. 1992. Red foxes, Vulpes vulpes, as biological be additive, as the presence of red foxes does control agents for introduced arctic foxes, Alopex 162 WESTERN NORTH AMERICAN NATURALIST [Volume 65

lagopus, on Alaskan islands. Canadian Field-Natural- JUREK, R.M. 1992. Nonnative red foxes in California. Non- ist 106:200–205. game Bird and Mammal Section Report 92-04, Cali- BYERS, C.R., R.K. STEINHORST, AND P.R. KRAUSMAN. 1984. fornia Department of Fish and Game, Sacramento. Clarification of a technique for analysis of utilization- KAMLER, J.F., AND W. B. B ALLARD. 2002. A review of native availability data. Journal of Wildlife Management and nonnative red foxes in North America. Wildlife 48:1050–1053. Society Bulletin 30:370–379. CHAMBERLAIN, M.J., AND B.D. LEOPOLD. 2000. Spatial use KAUFMANN, J.H. 1962. Ecology and social behavior of the patterns, seasonal habitat selection, and interactions coati, Nasua narica, on Borrow Colorado Island, among adult gray foxes in Mississippi. Journal of Wild- Panama. University of California, Publications in life Management 64:742–751. Zoology 60:95–222. CLARK, H.O., JR. 2001. Endangered San Joaquin kit fox LEWIS, J.C., K.L. SALLEE, AND R.T. GOLIGHTLY, JR. 1999. and non-native red fox interspecific interactions. Introduction and range expansion of nonnative red Master’s thesis, Fresno State University, Fresno, CA. foxes (Vulpes vulpes) in California. American Mid- ______. 2003. Responses of San Joaquin kit foxes to an oil- land Naturalist 142:372–381. gas well fire. California Fish and Game 89:102–105. MAJOR, J.T., AND J.A. SHERBURNE. 1987. Interspecific rela- CUTTER, W.L. 1958. Food habits of the swift fox in north- tionships of coyotes, bobcats, and red foxes in western Texas. Journal of Mammalogy 39:527–532. ern Maine. Journal of Wildlife Management 51: CYPHER, B.L. 1997. Effects of radiocollars on San Joaquin 606–616. kit foxes. Journal of Wildlife Management 61: MAYER, W.V. 1952. The hair of California mammals with 1412–1423. keys to the dorsal guard hairs of California mam- CYPHER, B.L., H.O. CLARK, JR., P.A. KELLY, C. VAN HORN mals. American Midland Naturalist 48:480–512. OB ARRICK AND ILLIAMS J , G.D. W , D.F. 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Pages 491–514 in tions between coyotes and red foxes. Journal of Mam- M.C. Barbour and J. Major, editors, Terrestrial vege- malogy 70:631–633. tation of California. John Wiley and Sons, New York. SARGEANT, A.B., S.H. ALLEN, AND J.O. HASTINGS. 1987. Spa- HERSTEINSSON, P., AND D.W. MACDONALD. 1992. Interspe- tial relations between sympatric coyotes and red foxes cific competition and the geographical distribution in North Dakota. Journal of Wildlife Management of red and arctic foxes Vulpes vulpes and Alopex 51:285–293. lagopus. Oikos 64:505–515. SARGEANT, A.B., AND P. M . A RNOLD. 1984. Predator man- HOOGE, P.N., AND B. EICHENLAUB. 1997. Animal movement agement for ducks on waterfowl production areas in extension to ArcView, version 1.1. Alaska Biological the northern plains. Pages 161–167 in D.O. Clark, Science Center, U.S. Geological Survey, Anchorage, editor, Proceedings of the 11th vertebrate pest con- AK. trol conference. University of California, Davis. HORN, H.S. 1966. Measurement of “overlap” in compara- SPIEGEL, L.K. 1996. Studies of San Joaquin kit fox in un- tive ecological studies. American Naturalist 100: developed and oil-developed areas. California Energy 419–424. Commission, Sacramento. 2005] KIT FOX AND RED FOX INTERACTIONS 163

SPRINGER, J.T. 1979. Some sources of bias and sampling WHITE, P.J., W.H. BERRY, J.J. ELIASON, AND M.T. HANSON. error in radio triangulation. Journal of Wildlife Man- 2000. Catastrophic decrease in an isolated popula- agement 43:926–935. tion of kit foxes. Southwestern Naturalist 45:204–211. STAINS, H.J. 1958. Field key to guard hair of middle west- WHITE, P.J., K. RALLS, AND C.A. VANDERBILT WHITE. 1995. ern furbearers. Journal of Wildlife Management 22: Overlap in habitat and food use between coyotes and 95–97. San Joaquin kit foxes. Southwestern Naturalist 40: SWIHART, R.K., AND N.A. SLADE. 1985. Testing for indepen- 342–349. dence of observations in animal movements. Ecol- WORTON, B.J. 1989. Kernel methods for estimating the ogy 66:1176–1184. utilization distribution in home range studies. Ecol- UNITED STATES FISH AND WILDLIFE SERVICE. 1998. Recov- ogy 70:164–168. ery plan for upland species of the San Joaquin Valley, ZAR, J.H. 1999. Biostatistical analysis. Prentice-Hall, Engle- California. United States Fish and Wildlife Service, wood Cliffs, NJ. 663 pp. Region 1, Portland, OR. 319 pp. ZOELLICK, B.W. 1990. Activity of kit foxes in western Ari- VOIGT, D.R., AND B.D. EARLE. 1983. Avoidance of coyotes zona and sampling design of kit fox resource use. by red fox families. Journal of Wildlife Management Pages 151–155 in P.R. Krausman and N.S. Smith, 47:852–857. editors, Managing wildlife in the southwest Arizona. WARRICK, G.D., AND B.L. CYPHER. 1998. Factors affecting Chapter of The Wildlife Society, Phoenix, AZ. the spatial distribution of a kit fox population. Journal of Wildlife Management 62:707–717. Received 30 January 2004 WHITE, G.C. 1985. Optimal locations of towers for trian- Accepted 6 August 2004 gulation studies using biotelemetry. Journal of Wild- life Management 49:190–196. WHITE, G.C., AND R.A. GARROT. 1990. Analysis of wildlife radio-tracking data. Academic Press, San Diego, CA. 383 pp. Western North American Naturalist 65(2), © 2005, pp. 164–169

RANGE EXTENSION AND ECOLOGICAL INFORMATION FOR ORCONECTES VIRILIS (HAGEN 1870) (DECAPODA: CAMBARIDAE) IN IDAHO, USA

William H. Clark1,3 and Gary T. Lester2

ABSTRACT.—We report the 1st record of the crayfish Orconectes virilis (Hagen 1870) from Idaho and the Pacific North- west, USA. We also provide an updated checklist of recent Idaho crayfishes, which now includes 2 families (Astacidae and Cambaridae), 3 genera (Pacifasticus, Orconectes, and Procambarus), and 7 species and subspecies (Pacifasticus connectus (Faxon 1914), P. gambelii (Girard 1852), P. leniusculus leniusculus (Dana 1852), P. leniusculus klamathensis (Stimp- son 1857), P. leniusculus trowbridgii (Stimpson 1857), O. virilis, and Procambarus clarkii (Girard 1852). Native crayfish were not found at the O. virilis collection sites. The localities where O. virilis was found were characterized by low-gradient streams impacted by fine sediment. Aquatic invertebrates found in association with O. virilis tended to be the more pollution-tolerant taxa.

Key words: Crustacea, Decapoda, Idaho checklist, Cambaridae, Orconectes virilis, introduced species, water quality, physical habitat structure, invertebrate associates.

While identifying contract macroinverte- 1852). Miller (1960) did not find O. virilis in brate samples from Idaho waters for the Idaho Oregon. Department of Environmental Quality Benefi- cial Use Reconnaissance Program (Beneficial MATERIALS AND METHODS Use Reconnaissance Project Technical Advisory Committee 1999), taxonomists at EcoAnalysts, Field methods used to collect benthic macro- Inc. (Moscow, ID), encountered Orconectes invertebrate samples are described in detail in virilis (Hagen 1870), a species of crayfish not Beneficial Use Reconnaissance Project Tech- previously known from Idaho. Orconectes vir- nical Advisory Committee (1999). In Idaho the ilis is known from lakes and streams east of macroinvertebrates in wadeable streams were collected in 3 riffle samples per stream reach the Continental Divide in eastern Canada from using a Hess sampler with a 500-micron mesh Saskatchewan to Ontario, and in the United net (Hess 1941) with the “Canton modifica- States from Montana to Arkansas, east to New tion” (Canton and Chadwick 1984). A kick-net York and Maine (Hobbs 1972, 1974, 1989); it was used to collect additional specimens at the has been introduced into California, Utah, Ari- China Creek locality (Fig. 1). Samples were pre- zona, New Mexico, Maryland, parts of New served in 70% ETOH and stored separately in England and Tennessee, western Colorado, the field. In the laboratory the 3 samples were and parts of Canada (Riegel 1959, Hobbs 1974, composited, counted, and 500 randomly se- Bouchard 1977, Unger 1978). Invasive popu- lected individual invertebrates were identified. lations of O. virilis may be a threat to freshwa- The species was initially identified using ter biodiversity (Bouchard 1977, Chambers et Smith (2001) and Thorpe and Covich (2001). al. 1990, Hanson et al. 1990, Savino and Miller Specimens were sent to Christopher A. Taylor, 1991, Miller et al. 1992, Warren 1997, Lodge Illinois Natural History Survey, for verifica- et al. 2000). Clark and Wroten (1978) reported a tion. Voucher specimens of Orconectes virilis depauperate Idaho crayfish fauna, with only 3 are deposited in the Orma J. Smith Museum native species in the genus Pacifasticus, and 1 in- of Natural History, Albertson College of Idaho troduced species, Procambarus clarkii (Girard (ALBRCIDA), Caldwell; the EcoAnalysts, Inc.

1State Office of Technical Services, Idaho Department of Environmental Quality, 1410 North Hilton Street, Boise, ID 83706 and Orma J. Smith Museum of Natural History, Albertson College of Idaho, Caldwell, ID 83605. 2EcoAnalysts, Inc., 105 East 2nd Street, Suite #1, Moscow, ID 83843. 3Present address: Idaho Power Company, Box 70, Boise, ID 83707.

164 2005] ORCONECTES VIRILIS IN IDAHO 165

Fig. 1. Known distribution (collection localities) of Orconectes virilis (Hagen) in Idaho, USA.

TABLE 1. Water quality and habitat variables for Orconectes virilis (Hagen) in Idaho. N/A = data not taken. Variable China Creek Jim Ford Creek Date 5 August 1999 14 July 2000 Temperature (°C) 12.6 23 Dissolved oxygen (mg ⋅ L–1) 7.6 4.45 Dissolved oxygen (% saturation) 69 N/A Specific conductance (µS ⋅ cm–1) 158 N/A pH (SU) 7.5 7.4 Total dissolved solids 0.1 N/A Discharge (cfs) 0.26 1.70 Habitat type glide/pool pool Stream width (meters) 1.7 3.5 Substrate embeddedness (%) 50–75 100 ⋅ –1 NO3 + NO2 (mg L ) N/A 2.41 Total N (mg ⋅ L–1) N/A 3.11 Total P (mg ⋅ L–1) N/A 0.15 N/P ratio N/A 20.7 166 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 2. Invertebrate associates of Orconectes virilis (Hagen) in Idaho. China Creek Jim Ford Creek (both locations) Associated taxa 5 August 1999 14 July 2000

NEMATODA X OLIGOCHAETA Enchytraeidae X Lumbricina Prostoma sp. X CRUSTACEA Amphipoda Gammarus sp. X Hyalella sp. X Ostracoda X ACARI XX INSECTA Ephemeroptera Baetis tricaudatus X Centroptilum sp. X Diphetor hageni X Nixe sp. X X Paraleptophlebia sp. X PLECOPTERA Chloroperlidae X Capniidae X Perlodidae X HEMIPTERA Corixidae X X MEGALOPTERA Sialis sp. X COLEOPTERA Optioservus sp. X TRICHOPTERA Cheumatopsche sp. X Glossosoma sp. X Lepidostoma sp. X DIPTERA Dicranota sp. X Simulium sp. X X Syrphidae X

(EI), macroinvertebrate taxonomic laboratory, ALBRCIDA) 42°03′31″N, 114°46′11″W, 1530 Moscow, Idaho; and the Illinois Natural His- m elev., 29 June 2000, W.H. Clark (collection tory Survey, Champaign (INHS). event #10,233). Materials Examined RESULTS AND DISCUSSION IDAHO: Clearwater County: Jim Ford Creek: 2 specimens (EI), 0.5 m upstream from Hwy These collection records for Orconectes vir- 11 bridge, 46°22.545′N, 115°56.953′W, 918 m ilis represent the 1st report of the genus and elev., 20 October 2000, J. Davis. Jim Ford Creek: species for the State of Idaho as well as for the 1 specimen (ALBRCIDA), 10 m above hydro- Pacific Northwest, USA. The proximity of the electric diversion, 46°23.004′N, 115°56.953′W, China Creek locality (Fig. 1) to Nevada sug- 913 m elev., 20 October 2000, J. Davis. gests that the species may also be found there. IDAHO: Twin Falls County: China Creek: 1 The genus Orconectes is naturally distributed specimen (EI) 42°03′31″N, 114°46′11″W, 1530 in North America east of the Continental m elev., 5 August 1999, D. Baldwin, R. Snyder, Divide. In the northwestern United States S. Staufer, and S. Woodhead (DEQ sample and adjacent Canada, only 2 species of Orco- #1999STWFA029). China Creek: 126 speci- nectes occur: O. virilis, which is widespread in mens (3 specimens INHS, 123 specimens Montana, Wyoming, Alberta, and Saskatchewan, 2005] ORCONECTES VIRILIS IN IDAHO 167

TABLE 2. Continued. China Creek Jim Ford Creek (both locations) Associated taxa 5 August 1999 14 July 2000 Tipula sp. X Ablabesmyia sp. X Chaetocladius sp. X Chironomus sp. X Cladotanytarsus sp. X Conchapelopia sp. X Corynoneura sp. X Cricotopus sp. X Cricotopus bicinctus group X X Cryptochironomus sp. X Dicrotendipes sp. X Eukiefferiella sp. X X Eukiefferiella devonica group X Micropsectra sp. X Nanocladius sp. X Orthocladius annectens X Parametriocnemus sp. X Paratanytarsus sp. X Paratendipes sp. X Pentaneura sp. Phaenopsectra sp. X X Polypedilum sp. X Stictochironomus sp. X Tanytarsus sp. X X Tanypodinae X Thienemanniella sp. X Thienemannimyia group X X Tvetenia bavarica group X X MOLLUSCA Bivalvia Sphaeriidae X X Gastropoda Ferrisia sp. X Physa sp. X

TOTAL TAXA 30 36

with introduced populations in Utah and Pacifasticus (Pacifasticus) leniusculus klamathensis northern California; and O. immunis (Hagen (Stimpson 1857). Native to British Columbia, WA, 1870), which occurs in Montana and Wyoming OR, CA, and western ID. (Hobbs 1974, 1989) To further the general Pacifasticus (Pacifasticus) leniusculus trowbridgii knowledge of crayfish in the state of Idaho and (Stimpson 1857). Native to British Columbia, adjacent areas, we present a checklist of the WA, OR, and western ID. Introduced to CA and NV. recent species reported from Idaho. CAMBARIDAE Checklist of Recent Crayfishes Known to Occur in Idaho Orconectes (Gremicambarus) virilis (Hagen 1871). Native to Alberta, Saskatchewan, Ontario, Quebec, ASTACIDAE MT, WY, eastern CO, ND, SD, NE, KS, OK, AR, Pacifasticus (Hobbsastacus) connectus (Faxon 1914). MO, MI, WI, IA, IL, TN, IN, OH, NY, VA, NH, Native to ID and OR. MA, ME, CT, and RI. Introduced into ID, CA, Pacifasticus (Hobbsastacus) gambelii (Girard 1852). UT, CO, AZ, NM, TX, MS, AL, KY, TN, WV, VA, Native to WA, OR, ID, MT, northern CA, NV, MD, and NJ. and UT. Procambarus (Scapulicambarus) clarkii (Girard 1852). Pacifasticus (Pacifasticus) leniusculus leniusculus Native to LA and TX. Introduced throughout (Dana 1852). Native to British Columbia, OR, North America, Eurasia, Africa, some South WA, ID. Introduced in CA, NV, UT, and Europe. Pacific islands, including HI. 168 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Physical habitat and water-quality variables Rogers (EcoAnalysts, Inc.) kindly reviewed for sampling locations are presented in Table 1. a draft of this paper and offered helpful These data help describe the physical habitat comments. Sean Coyle (Idaho DEQ) made structure and summer water-quality conditions Figure 1. in which O. virilis has been found in Idaho. Table 1 shows that both waters are small-order, LITERATURE CITED low-gradient streams impacted from grazing and other agricultural practices. In the sum- BARBOUR, M.T., J. GERRITSEN, B.D. SYNDER, AND J.B. STRIB- LING. 1999. Rapid bioassessment protocols for the mer, at least, they appear to be characterized use in streams and wadeable rivers: periphyton, by warm temperatures and corresponding low benthic macroinvertebrates and fish. 2nd edition. dissolved oxygen concentrations. The stream EPA 841-B-99-002, U.S. Environmental Protection sites were characterized by low water velocity Agency, Office of Water, Washington, DC. 306 pp. and appeared to be impacted by fine sediment BENEFICIAL USE RECONNAISSANCE PROJECT TECHNICAL ADVISORY COMMITTEE. 1999. 1999 Beneficial Use (Table 1). Reconnaissance Project workplan for wadable streams. The invertebrates associated with O. virilis Idaho Division of Environmental Quality, Boise. 82 at these 2 sites are listed in Table 2. The groups pp. and taxa listed are considered to be more pol- BOUCHARD, R.W. 1977. Distribution, ecology, and system- lution tolerant as would be expected to be atic status of five poorly known western North American crayfishes (Decapoda: Astacidae and Cam- found in more degraded systems (Hilsenhoff baridae). Pages 409–423 in O.V. Linquist, editor, Fresh- 1987, Barbour et al. 1999, Relyea et al. 2000). water crayfish. University of Kupio, Kupio, Finland. Because nonindigenous crayfishes including CANTON, S.P., AND J.W. CHADWICK. 1984. A new modified O. virilis have been shown to impact fresh- Hess sampler. Progressive Fish-Culturist 46:57–59. water biodiversity including the macroinverte- CHAMBERS, P.A., J.M. HANSON, J.M. BURKE, AND E.E. PREPAS. 1990. The impact of the crayfish Orconectes brate fauna (Bouchard 1977, Chambers et al. virilis on aquatic macrophytes. Freshwater Biology 1990, Hanson et al. 1990, Miller et al. 1992, 24:81–91. Warren 1997, Lodge et al. 2000), we present CLARK, W.H., AND J.W. WROTEN. 1978. First record of the the macroinvertebrate community associated crayfish, Procambarus clarkii, from Idaho, U.S.A. (Decapoda: Cambaridae). Crustaceana 35:317–319. with O. virilis in Idaho (Table 2). These 2 loca- HANSON, J.M., P.A. CHAMBERS, AND E.E. PREPAS. 1990. tions have similar invertebrate assemblages Selective foraging by the crayfish Orconectes virilis (Table 2), with the following major differences. and its impact on macroinvertebrates. Freshwater The China Creek site had a taxa richness of Biology 24:69–80. 30, which included 1 major group not found at HESS, A.D. 1941. New limnological sampling equipment. Limnological Society of America Special Publication the Jim Ford Creek sites, and that was Tri- 6:1–5. choptera. Jim Ford Creek had a taxa richness HILSENHOFF, W.L. 1987. An improved biotic index of of 36 and included 4 major groups not found organic stream pollution. Great Lakes Entomologist in the China Creek samples: Megaloptera, 20:31–39. Nematoda, Gastropoda, and Ostracoda. HOBBS, H.H., JR. 1972. Crayfishes (Astacidae) of North and Middle America. In: Biota of freshwater ecosys- We suggest that this species be monitored tems: identification manual. U.S. Environmental in the Pacific Northwest to determine its Protection Agency, Washington, DC. 173 pp. impacts on the native invertebrate fauna in the ______. 1974. A checklist of the North and Middle Ameri- region. It is worthy of note that no native cray- can crayfishes (Decapoda: Astacidae and Cambaridae). Smithsonian Contributions to Zoology 166. 161 pp. fish were found at the 2 collection sites in ______. 1989. An illustrated checklist of the American which O. virilis occurred (Table 2). crayfishes (Decapoda: Astacidae, Cambaridae, and Parastacidae). Smithsonian Contributions to Zoology ACKNOWLEDGMENTS 480. 236 pp. LODGE, D.M., C.A. TAYLOR, D.M. HOLDICH, AND J. SKUR- The authors thank Christopher Taylor (Illi- DAL. 2000. Nonindigenous crayfishes threaten North American freshwater biodiversity. Fisheries 25(8):7–20. nois Natural History Survey) for verifying the MILLER, G.C. 1960. The taxonomy and certain biological initial identification of Orconectes virilis. John aspects of the crayfish of Oregon and Washington. Pfeiffer (EcoAnalysts, Inc.) originally identi- Master’s thesis, Oregon State College, Corvallis. 216 fied the specimens and brought them to the pp. MILLER, J.E., J.F. SAVINO, AND R.K. NEELY. 1992. Compe- attention of the second author (GTL). Sean tition for food between crayfish (Orconectes virilis) Woodhead and Darren Brant (Idaho DEQ) and the slimy sculpin (Cottus cognatus). Journal of assisted with logistical support. Christopher Freshwater Ecology 7:127–136. 2005] ORCONECTES VIRILIS IN IDAHO 169

RELYEA, C.D., G.W. MINSHALL, AND R.J. DANEHY. 2000. THORPE, J.H., AND A.P. COVICH, EDITORS. 2001. Ecology Stream insects as bioindicators of fine sediment. In: and classification of North American freshwater in- Proceedings Watershed 2000. Water Environment vertebrates. 2nd edition. Academic Press, New York. Federation Specialty Conference, Vancouver, BC. 19 1056 pp. pp + 4 appendices. UNGER, P.A. 1978. Natural history inventory of Colorado, RIEGEL, J.A. 1959. The systematics and distribution of No. 3: the crayfishes of Colorado. University of Col- crayfishes in California. California Department of orado Museum, Boulder. 20 pp. Fish and Game 45:29–50. WARREN, G.L. 1997. Nonindigenous freshwater inverte- SAVINO, J.F., AND J.E. MILLER. 1991. Crayfish (Orconectes brates. Pages 101–108 in D. Simberloff, D.C. Schmitz, virilis) feeding on young lake trout (Salvelinus namay- and T.C. Brown, editors, Strangers in paradise: im- cush): effect of rock size. Journal of Freshwater Ecol- pact and management of nonindigenous species in ogy 6:161–170. Florida. Island Press, Washington, DC. SMITH, D.G. 2001. Pennak’s freshwater invertebrates of the United States: Porifera to Crustacea. 4th edition. Received 29 December 2003 John Wiley and Sons, New York. 638 pp. Accepted 12 October 2004 Western North American Naturalist 65(2), © 2005, pp. 170–174

DISTRIBUTION OF BRECHMORHOGA CLUBSKIMMERS (ODONATA: LIBELLULIDAE) IN THE GRAND CANYON REGION, SOUTHWESTERN USA

Lawrence E. Stevens1 and Richard A. Bailowitz2

ABSTRACT.—We examined the distribution of Brechmorhoga mendax and B. pertinax (Libellulidae) in northern Ari- zona and southern Nevada. Brechmorhoga mendax occurs widely throughout the Southwest and in Arizona up to the Mogollon Rim, and up the Colorado River from the west to at least River Mile 132 (downstream from Lees Ferry, Ari- zona) at elevations of 110–1460 m. In Grand Canyon it occurs along small to large tributaries and on the mainstream at elevations below 650 m. The only previously reported locality for B. pertinax in the United States is in southeastern Ari- zona, where it was presumed to be accidental. We report B. pertinax along 5 small, perennial tributaries emanating from Redwall Formation aquifer springs on the south side of central Grand Canyon. Those springs habitats may be threatened by regional groundwater depletion. Brechmorhoga pertinax appears to be somewhat more stenotolerant in its habitat requirements than B. mendax, a finding in keeping with these differences in range. The presence of isolated populations of B. pertinax in Grand Canyon is an example of a Neotropical influence on the fauna and indicates biogeographic corridor and refuge functions of this large, deep canyon.

Key words: biogeography, Brechmorhoga, Colorado River, Grand Canyon, isolated populations, Neotropical, Odonata, springs.

Brechmorhoga mendax (Hagen 1861) and and several highly isolated populations of B. B. pertinax (Hagen 1861) are the only 2 libel- pertinax along small, perennial, spring-fed lulid clubskimmer dragonfly species reported streams emanating from the south side of Grand in the United States (Needham et al. 2000, Canyon in northern Arizona. Donnelly 2004). Brechmorhoga mendax is found across the southern plains and southwestern METHODS United States, from South Dakota to Arkansas, west to northern California, and south into We collected numerous adult Odonata dur- Mexico (Beckemeyer 1996, Needham et al. ing biological inventories of >300 aquatic 2000, Manolis 2003, Donnelly 2004). It has habitats across the 3500 m elevation gradient been reported throughout Arizona, except in in Coconino, Mohave, and Yavapai Counties, Yuma County in the southwestern corner of and in and around Grand Canyon in northern the state and in the northeast in Navajo and Arizona over the past decade (Fig. 1). These Apache Counties. It has been reported from inventories focused on water sources, particu- the Virgin River drainage in southwestern Utah larly springs, the several dozen perennial and southeastern Nevada, and in central Grand streams that are tributaries of the Colorado Canyon (Donnelly 2004). In contrast, B. perti- River, as well as natural and anthropogenic nax is very rare or accidental in the United ponds, lakes, and reservoirs (Stevens et al. States: the only previous record to our knowl- 1997, Grand Canyon Wildlands Council 2002, edge is a single specimen taken by M. Westfall 2004, RAB and LES unpublished data). By at John Hands Campground in the Chiricahua convention, distances along the Colorado River Mountains, Cochise County, Arizona, on 25–26 in Grand Canyon are measured in miles from June 1958. Brechmorhoga pertinax’s range Lees Ferry in Coconino County at the upstream extends south through Mexico, Guatemala, end of Grand Canyon. Nicaragua, and Costa Rica (Gutiérrez 1995, Specimen identities were verified by RAB, Needham et al. 2000). Here we report a more with the northern phenotype of B. pertinax limited distribution of B. mendax in Arizona distinguished from B. mendax on the basis of

1Stevens Ecological Consulting, LLC, Box 1315, Flagstaff, AZ 86002. 21331 W. Emerine Drive, Tucson, AZ 85704.

170 2005] GRAND CANYON REGION CLUBSKINNERS 171

Fig. 1. Map of the Grand Canyon region. Distances along the Colorado River are indicated (by convention) in river miles (RM) downstream from Lees Ferry, AZ (RM 0). Small numbers indicate sampling localities listed in Table 1. Local- ities for Brechmorhoga mendax are not circled. Those for B. pertinax are encircled, and all occur in a small area in Grand Canyon National Park. several features: (1) a darker, more slender form; Specimens are housed in the invertebrate col- (2) dark interpleural and metapleural stripes lection of the Museum of Northern Arizona, that are fused along the entire margins; (3) di- Flagstaff. vergent white spots on abdominal segment 7; Brechmorhoga mendax is reported to be (4) male hamules that are straighter (not as widely distributed on and around the southern curved as a question mark); (5) lack of mete- Colorado Plateau and the lower Colorado River. pisternal pale stripes; and (6) a dark metallic Our data reveal that B. mendax exists from 110 blue labrum and epicranium, with brown at m to 1460 m elevation in this region and flies the rear of the head (Needham et al. 2000). from at least 22 April to at least 20 October The abdomen:hindwing length ratio of B. (Table 1, Fig. 1). This species exists along the mendax has been described as being >1 and Colorado River and its tributaries from Parker, that of B. pertinax <1. However, in some of Arizona, north to southern Nevada and north- our B. pertinax specimens, the abdomen is western Arizona. It occurs at Warm Springs and longer than the hindwing, and this character- along the upper Muddy River (Clark County, istic appears to be unreliable. NV; U.S. Geological Survey 2003), as well as the lower Virgin River (Utah; Donnelly 2004), RESULTS AND DISCUSSION both of which are tributaries to the Colorado River. It occurs in Arizona in Mohave County Our inventories yielded 20 adult Brech- at Tassi Spring in Grand Wash (RM 285) in morhoga specimens from the Grand Canyon Lake Mead National Recreation Area. Its range region and numerous visual observations across in Grand Canyon extends upstream in Mohave a wide array of habitats in northern Arizona. and Coconino Counties, into lower Diamond 172 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 1. Brechmorhoga sampling sites and distribution in the Grand Canyon region. Land management units: ANF—Apache National Forest; CNF—Coconino National Forest; CV—Camp Verde, AZ; FWS—U.S. Fish and Wild- life Service; GCNP—Grand Canyon National Park; GCNRA—Glen Canyon National Recreation Area; LMNRA—Lake Mead National Recreation Area; SCWA—Sycamore Canyon Wilderness Area (Prescott National Forest); TNF—Tonto National Forest. Numbers indicate collection site localities (Table 1). “X” designates an observation or collection; “0” designates no Brechmorhoga detection; asterisk indicates specimen observed by LES. Detections Elevation Elevation ______Site Site name State County Land unit (m) (ft.) B. mendax B. pertinax 1 Muddy R. NV Clark FWS 430 1411 X 0 2Tassi Spr. AZ Mohave LMNRA 400 1312 X 0 3 Diamond Cr. AZ Coconino GCNP 420 1378 X 0 4 Spring Cyn. Spr. AZ Mohave GCNP 460 1509 X 0 5 Lower Havasu Cr. AZ Coconino GCNP 570 1870 X 0 6Kanab Cr. AZ Mohave GCNP 580 1903 0 0 7 Deer Cr. AZ Coconino GCNP 650 2133 0 0 8Tapeats Cr. AZ Coconino GCNP 650 2133 0 0 9 Stone Cr.* AZ Coconino GCNP 650 2133 X 0 10 Galloway Cr. mouth AZ Coconino GCNP 650 2133 X 0 11 Shinumo Cr. AZ Coconino GCNP 700 2297 0 0 12 Crystal Cr. AZ Coconino GCNP 720 2362 0 0 13 Boucher Cr. AZ Coconino GCNP 1000 3281 0 0 14 Hermit Cr. AZ Coconino GCNP 1100 3609 0 X 15 Monument Cr. AZ Coconino GCNP 1150 3773 0 X 16 Garden Cr. AZ Coconino GCNP 1150 3773 0 X 17 Pipe Cr. AZ Coconino GCNP 1150 3773 0 X 18 East Grapevine Spr. AZ Coconino GCNP 1120 3675 0 X 19 Cottonwood Cr. AZ Coconino GCNP 1120 3675 0 0 20 Bright Angel Cr. AZ Coconino GCNP 740 2428 0 0 21 Nankoweap Cr. AZ Coconino GCNP 860 2822 0 0 22 Little Colorado R. AZ Coconino GCNP 820 2690 0 0 23 Paria R. AZ Coconino GCNRA 940 3084 0 0 24 Sycamore Cr. AZ Yavapai SCWA 1000 3281 X 0 25 Verde R. at I-10 AZ Yavapai CV 1050 3445 X 0 26 Oak Cr. AZ Coconino CNF 1460 4790 X 0 26 East Verde R. AZ Gila TNF ca 1300 4265 X 0 27 Blue R. AZ Apache ANF ca 1300 4265 X 0

Creek (RM 225) and Spring Canyon (RM 204; localities in Arizona’s northeastern counties are and probably the larval specimens identified in drainages that flow southward in the White to genus by Oberlin et al. 1999), and into cen- Mountains in the Salt-Gila River basin. tral Grand Canyon at least to RM 132, but it Brechmorhoga mendax is riparian in its adult has not been detected in upper Grand Canyon. stages, rarely straying from the moderately We and our colleagues also detected B. mendax swift-flowing water of small to large streams in Coconino County along lower Sycamore throughout its range. It patrols relatively large Creek in Sycamore Canyon Wilderness Area (>50 m long) territories along these often (12 km N of Clarkdale; LES, 9 Sept.) and along heavily vegetated streams, and it occurs in low Oak Creek up to an elevation of 1450 m (C. densities along the highly regulated Colorado Olsen, 14 July; L. Haury, 2 August); Greenlee River in Grand Canyon (e.g., RM 132, 600 m County along the Blue River (D. Danforth, 20 elevation; LES, 17 August 2004). July); Gila County on the East Verde River Brechmorhoga pertinax occurs in Central northeast of Payson (P. Savacevi, 29 June); and America, and northward to east central Sonora Yavapai County in the Verde River drainage and along the east side of the Sierra Madre along the southern margin of the Colorado Occidental in Mexico. In Grand Canyon this Plateau, from Camp Verde at the Interstate 17 species has been detected at 5 perennial, bridge (29 Aug), at elevations of 1000–1050 m spring-fed tributaries on the south side of the (LES). Reports of this species in northeastern Colorado River, from RM 81 to RM 95 (all Arizona have yet to be substantiated: the only localities in Coconino County) at elevations of 2005] GRAND CANYON REGION CLUBSKINNERS 173

850–1150 m (Table 1, Fig. 1). It flies from at (RM 136), or Kanab (RM 143) Creeks, except least 19 July until at least 21 October, a flight a visual observation by LES at Stone Creek range far longer than the 25 June–3 July pre- (RM 132) in August 2004. Water chemistry, viously reported by Needham et al. (2000). climate and flow changes, fidelity of Brech- Our farthest upstream record in the Colorado morhoga to the stream habitats of their larval River drainage was from East Grapevine Spring stages, adult territorial and reproductive on the Tonto Trail (N36.04279°, W112.01381°) behavior (Alcock 1989, Cordoba 1994), sam- at 1120 m elevation. No Brechmorhoga were pling effort, and the vagaries of colonization detected at apparently suitable habitat 5 km for this rather low-vagility, relatively stenotol- east in the Cottonwood Creek drainage, despite erant species may account for its apparently intensive collecting efforts there from 2000 to restricted distribution in Grand Canyon. 2003. Brechmorhoga pertinax occurred west of Biogeographically, Grand Canyon’s aquatic Grapevine Creek in 4 other perennial spring- and wetland invertebrate fauna reflects a minor fed creeks with runout streams >100 m, includ- Neotropical influence. With this report, Brech- ing Pipe Creek (N36.07316°, W112.10249°), morhoga pertinax joins the ranks of Ochterus Indian Gardens (N36.08005°, W112.12668°), rotundus (Hemiptera: Ochteridae; Polhemus Monument Creek (N36.06290°, W112.17489°), and Polhemus 1976) and Polypedilum (Tripo- and Hermit Creek (N36.08207°, W112.21489°). dura) obelos Sublette and Sasa (Diptera: Chiro- The springs supporting these streams are nomidae; Sublette et al. 1998) as Neotropical threatened by regional groundwater extraction aquatic invertebrates with disjunct ranges ex- on the Coconino Platform, south of Grand tending from Guatemala or southern Mexico Canyon. into isolated microhabitats in Grand Canyon. The relatively fast-flowing runs and small The extent and duration of isolation of Grand pools in streams at which B. pertinax was Canyon B. pertinax from Mexican populations detected are geomorphically and geochemi- remains to be determined through genetics cally consistent with descriptions of its larval analyses. However, the persistence of B. perti- habitat in Central America (Gutiérrez 1995). nax and other rare aquatic and wetland plant The small streams supporting B. pertinax in and invertebrate populations may be jeopar- Grand Canyon were rather similar in flow and dized by the depletion of deep aquifers and water chemistry: flows were typically small, the dewatering of Grand Canyon springs (Grand averaging 0.04–19.3 L ⋅ s−1; mean water tem- Canyon Wildlands Council 2002, 2004). perature ranged from 14.7°C to 18.0°C, except Grand Canyon has been recognized as an for East Grapevine Spring, which averaged important corridor of desert habitat through 11.1°C and is more variable; pH varied from an otherwise inhospitable, high-elevation land- 7.5 to 8.4; mean specific conductance ranged scape, but its biogeographic function as a refuge from 393 to 1037 µS ⋅ cm−1; and mean field for isolated or endemic taxa is only recently ⋅ −1 CaCO3 varied from 187.5 to 301.7 mg L (J. becoming apparent. The Colorado River and Rihs, NPS hydrologist, Grand Canyon, written its tributaries serve as a partial range corridor communication). In contrast, the streams sup- through the high-elevation Colorado Plateau for porting B. mendax varied rather widely in flow numerous desert riparian species. The range (up to 4359 L ⋅ s−1) and geochemistry (specific of B. mendax extends partway upstream through conductance may exceed 1120 µS ⋅ cm−1). Grand Canyon, a range similar to that of sev- Although both the larval and adult habitats eral common desert plant species including seem appropriate and sampling has been in- Yucca whipplei, Foquieria splendens, Ferocactus tensive, Brechmorhoga were not detected at cylindraceus, and Larrea tridentata (Phillips et East Boucher Spring or “Erhart Spring” in al. 1987). In contrast, B. pertinax populations Boucher Canyon (RM 96), immediately west in the United States appear to be restricted to of Hermit Creek. Also, Brechmorhoga have a few remote spring-fed stream refugia with yet to be detected along north side tributaries relatively uniform water quality at slightly higher of the Colorado River in central and eastern elevations in central Grand Canyon. Grand Canyon, including Nankoweap (RM Other Grand Canyon taxa displaying a sim- 53), Bright Angel (RM 88), Crystal (RM 98), ilar refugial response to this landscape include Shinumo (RM 109), Tapeats (RM 134), Deer the following: the previously mentioned, highly 174 WESTERN NORTH AMERICAN NATURALIST [Volume 65 restricted Octerus rotundus (Polhemus and DONNELLY, T.W. 2004. Distribution of North American Polhemus 1976); endemic McDougall’s flave- Odonata, part II: Macromiidae, Corduliidae and Libellulidae. Bulletin of American Odonatology 8: ria (Flaveria mcdougallii), which occupies a 1–32. few remote springs in middle Grand Canyon GRAND CANYON WILDLANDS COUNCIL, INC. 2002. A hydro- (Phillips et al. 1987); endemic Cicindela hem- logical and biological inventory of springs, seeps and orrhagica arizonae Wickham (Coleoptera: ponds of the Arizona Strip, final report. Arizona Department of Water Resources, Water Protection Cicindelidae), the range of which almost exactly Fund, Phoenix. overlaps that of B. pertinax (Stevens and ______. 2004. Biological inventory and assessment of ten Huber 2004); and endemic Grand Canyon rat- South Rim springs in Grand Canyon National Park: tlesnakes (Crotalus viridis abyssus; Reed and final report. Grand Canyon Wildlands Council Report, Flagstaff, AZ. Douglas 2002). The rarity of refugial and en- GUTIÉRREZ, R.N. 1995. Nayade de Brechmorhoga pertinax demic taxa has been attributed to Pleistocene- (Odonata: Libellulidae). Anales del Instituto de Bio- Holocene climate changes and the limited logía Universidad Nacional Autonoma de Mexico time this region has existed as desert habitat Serie Zoología 66:181–187. HAGEN, H.A. 1861. Synopsis of the Neuroptera of North (Stevens and Huber 2004), but this hypothesis America, with a list of the South American species. may need revision as additional refugial taxa Smithsonian Miscellaneous Collections 4:1–347. are identified in Grand Canyon. Overall, the MANOLIS, T. 2003. Dragonflies and damselflies of Califor- discovery of isolated B. pertinax populations in nia. University of California Press, Berkeley. NEEDHAM, J.G., M.J. WESTFALL, JR., AND M.L. MAY. 2000. Grand Canyon is consistent with an emerging Dragonflies of North America. Revised edition. Sci- understanding of invertebrate biogeography entific Publishers, Gainesville, FL. and conservation issues in this large, deep OBERLIN, G.E., J.P. SHANNON, AND D.W. BLINN. 1999. canyon ecoregion. Watershed influence on the macroinvertebrate fauna of ten major tributaries of the Colorado River through Grand Canyon, Arizona. Southwestern Naturalist 44: ACKNOWLEDGMENTS 17–30. PHILLIPS, B.G., A.M. PHILLIPS III, AND M.A. SCHMIDT- This project was partially funded by Grand BERNZOTT. 1987. Annotated checklist of vascular Canyon Wildlands Council, Inc. and National plants of Grand Canyon National Park. Grand Canyon Natural History Association Monograph 7. Grand Park Service Contract WPF-230, through the Canyon, Arizona. Arizona Water Protection Fund. We particu- POLHEMUS, J.T., AND D.A. POLHEMUS. 1976. Aquatic and larly thank John Rihs, NPS hydrologist, for semi-aquatic Heteroptera of Grand Canyon (Insecta: project support. We extend our gratitude to Hemiptera). Great Basin Naturalist 36:221–226. Margaret Erhart, Terry Griswold, Ann Hadley, REED, R.N., AND M.E. DOUGLAS. 2002. Ecology of the Grand Canyon rattlesnake (Crotalus viridis abyssus) Loren Haury, Krissy Killoy, Eric North, and in the Little Colorado River Canyon, Arizona. South- Bianca Perla for enthusiastic field assistance western Naturalist 47:30–39. during inventories. We thank Sandy Upson STEVENS, L.E., AND R.L. HUBER. 2004. Biogeography of and Douglas Danforth for taxonomic advice. tiger beetles (Cicindelidae) in the Grand Canyon Chris Brod (Spatial Science Solutions, LLC) ecoregion, Arizona and Utah. Cicindela 35:41–67. STEVENS, L.E., J.P. SHANNON, AND D.W. BLINN. 1997. provided invaluable assistance with georefer- Benthic ecology of the Colorado River in Grand encing and map preparation. We thank Boris Canyon: dam and geomorphic influences. Regulated Kondratieff and 2 anonymous reviewers for Rivers: Research & Management 13:129–149. helpful editorial comments. SUBLETTE, J.E., L.E. STEVENS, AND J.P. SHANNON. 1998. Chironomidae (Diptera) of the Colorado River, Grand Canyon, Arizona, USA, I: systematics and ecology. LITERATURE CITED Great Basin Naturalist 58:97–146. U.S. GEOLOGICAL SURVEY. 2003. Dragonflies and dam- ALCOCK, J. 1989. The mating system of Brechmorhoga per- selflies (Odonata) of the United States: Odonata of tinax (Hagen): the evolution of brief patrolling bouts Clark County, Nevada. Available on-line at http:// in a “territorial” dragonfly (Odonata: Libellulidae). www.npwrc.usgs.gov/resource/distr/insects/dfly/nv/ Journal of Insect Behavior 2:49–62. toc.htm. BECKEMEYER, R.J. 1996. First record of Brechmorhoga mendax from Kansas. Argia 8:29–30. Received 8 June 2004 CORDOBA, A.A. 1994. Some observations on reproductive Accepted 3 November 2004 behavior in Brechmorhoga vivax Calv. (Anisoptera: Libellulidae). Notulae Odonatologicae 4:51–53. Western North American Naturalist 65(2), © 2005, pp. 175–185

NONRESPONSE OF NATIVE COTTONWOOD TREES TO WATER ADDITIONS DURING SUMMER DROUGHT

Greg Cox1,2, Dylan Fischer1,3,4,5, Stephen C. Hart1,3, and T.G. Whitham2,3

ABSTRACT.—Studies have demonstrated that some riparian trees may switch their reliance on surface soil water (unsaturated or vadose zone) to groundwater (saturated zone) sources during the growing season in association with changes in moisture availability. A closely related question is: How do these trees respond to pulse increases in water availability in previously dry zones? We tested the whole-tree physiological response of 6 natural Populus genotypes to water additions during the peak of summer drought in northern Utah, USA. We found clear evidence that trees were insensitive to water additions to the surface soil that were twice the magnitude of whole-tree transpiration rates. Our results suggest that some cottonwoods may have little immediate transpiration or leaf conductance response to pulse soil moisture increases. This lack of response may be related to a water-use strategy associated with regional climate patterns (i.e., genetic or environmental programming), cavitation recovery, or other physical determinants of water use such as depth to groundwater. Our data suggest that it is important to consider potential nonresponsiveness to changes in soil water availability when evaluating the impact of climate change on these important and productive ecosystems.

Key words: sap flow, cottonwood, drought, water addition, conductance, water potential, Populus.

Studies that examine cottonwood (Populus the context of implications for silviculture spp.) response to increasing soil moisture are (Marron et al. 2002) rather than in terms of the important for several reasons. First, cotton- functioning of native forests (Horton et al. 2001a, woods are dominant trees of many western 2001b). Understanding how cottonwoods re- intermountain river ecosystems of the United spond to changing water availability is impor- States. Populus angustifolia (narrow leaf cotton- tant to conservation and restoration for this wood), P. fremontii (Fremont cottonwood), and threatened habitat (cottonwood riparian forests). their natural hybrids are often described as Cottonwoods may alternate water source facultative phreatophytes (Snyder and Williams use between groundwater and surface soil 2000, Horton et al. 2001a, 2001b, 2003; but moisture (Smith et al. 1991, 1998, Rood et al. see Busch et al. 1992). They are generally re- 2003) or act as obligate phreatophytes (Busch stricted to riparian areas where they are the et al. 1992) by depending entirely on ground- dominant plant species and play a major role in water. For instance, in the spring, cottonwoods ecosystem processes (Driebe and Whitham may derive water mostly from near-surface 2000, Schweitzer et al. 2004, Fischer et al. 2004). sources and in the summer mostly from deeper Second, it is important to know how riparian groundwater sources (Zhang et al. 1999). Cotton- species may respond to altered hydrological wood response to surface moisture may also patterns induced by global change. For exam- be dependent on life history and adaptation to ple, many modeling efforts predict increased local weather patterns. For example, isotope pulse-event summer rainfall in the southwest- studies in regions where summer precipitation ern U.S. (National Assessment Synthesis Team and soil surface moisture are historically unre- 2002), but knowledge of intermountain and liable have found evidence that cottonwoods southwestern riparian species responses to these do not use vadose zone water (i.e., Busch et al. rainfall events is incomplete. Finally, many stud- 1992, Horton et al. 2003). Thus, it is unclear ies on cottonwood responses to water additions whether cottonwoods are able to use water have been conducted in plantations. Results sources when water becomes suddenly avail- from these studies have been interpreted in able where it was previously scarce.

1School of Forestry, Northern Arizona University, Flagstaff, AZ 86011. 2Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011. 3Merriam-Powell Center for Environmental Research, Northern Arizona University, Flagstaff, AZ 86011. 4Environmental Studies Program, Evergreen State College, Olympia, WA 98505. 5Corresponding author.

175 176 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Cottonwood trees also have highly adapt- perature is 32.1°C for August (climatic data able root systems and have been documented summaries for Ogden Sugar House Weather to show rapid growth in response to changes Station; http://www.wrcc.dri.edu/summary/ in water and nutrient availability (Pregitzer and climsmslc.html [accessed 21 July 2004]). In Friend 1996). These rapid responses suggest August 2002 drought for the area was rated as that these trees may be capable of responding severe to extreme by the National Drought physiologically to short-term surface water Mitigation Center (http://www.drought.unl.edu additions through the rapid root growth and [accessed 21 July 2004]). Between 1 August and uptake of surface moisture. If this were the 5 September 2002 (the period of this study), case, we would expect that short-term water 1.0 mm of precipitation (19.1 mm below aver- additions and intense pulse summer rainfall age for August; see above) fell, and average events (Loik et al. 2004) would quickly stimu- daytime and daily air temperatures were 24.9°C, late surface fine root regrowth and tree tran- and 23.6°C, respectively. However, in previ- spiration and would improve tree water status. ous recent years more significant precipitation A short-term response (within 3 weeks) to sur- had been documented during this period. For face water is important to consider because it example, in 2001 we recorded 7.36 mm of pre- is unlikely that a longer response time could cipitation between 1 August and 5 September have ecologically important consequences for focused (83%) in 2 individual pulse events. vegetative response to pulse precipitation events In 1991 cuttings from P. fremontii, P. angus- (see Loik et al. 2004). Another key study of a tifolia, and their hybrids were taken from indi- facultative phreatophyte found that water up- viduals growing along the nearby Weber River. take from the surface soil occurred only after These cuttings were then planted at 4-m spac- 4 weeks of a watering treatment (Devitt et al. ing at the Ogden Nature Center in a drainage 1997). thought to have been historically occupied by We hypothesized that increasing water avail- cottonwood riparian forests. Cuttings were from ability in the upper reaches of the soil profile trees of known genotype based on previous during a drought would increase whole-tree RFLP work (see Martinsen et al. 2001 for water use and plant water status. To address details). Minirhizotron measurements down to this hypothesis, we posed 3 questions: (1) Do a depth of 45 cm in this “restored” forest ver- whole-tree water use and canopy conductance sus 7 other natural stands along the Weber respond to water additions in native cotton- River do not indicate a difference in fine root wood genotypes? (2) Does cottonwood whole- growth morphology (data not shown). tree physiology vary differently with changes Experimental Watering in surface soil moisture versus measured leaf Treatment predawn water potentials? (3) What roles do tree architecture and drought-induced leaf Measurements of sap flux density of the loss play in possible mitigation of the negative study trees began on 1 August (day of year consequences of low surface soil moisture? [DOY] 214), and experimental watering treatments began on 12 August (DOY 226). Experi- MATERIALS AND METHODS mental watering treatments were begun after we collected sap flux density data for 12 days, Study Site allowing for a baseline sap flux density rate to Our study site is a restored riparian area at be established for each study tree. Our study the Ogden Nature Center (41°11′N, 111°56′W; trees consisted of 6 P. angustifolia, 4 backcross elevation 1370 m) in Ogden, Utah. The site hybrids, and 2 F1 hybrid genotypes. For each receives approximately 440 mm of precipita- genotype we had 2 tree replicates: one would tion annually, with an average of 20.1 mm in receive the watering treatment, and the other August. Along the Weber River drainage, sur- would serve as the control. Those receiving face soil moisture generally declines from late the treatment were administered extra water spring into summer and fall (http://waterdata. via drip irrigation and bucket watering applied usgs.gov/ut/nwis/rt [accessed 21 July 2004]). to the ground evenly beneath individual tree Soil moisture is at its lowest when tempera- canopies (see Fig. 1). Treatment trees were tures are at their highest. Mean annual air clumped together or spatially isolated in an temperature is 10.4°C, and mean daily air tem- effort to avoid extra water diffusing through 2005] COTTONWOOD WATER RESPONSE DURING DROUGHT 177

Fig. 1. Physiological responses of watered (W) and unwatered (U) cottonwood trees over time in a common garden –2 –1 environment near Ogden, UT: A, leaf-specific transpiration (El; liters H2O m leaf area d ) plotted with vapor pressure deficit (VPD); B, gravimetric soil water content (SWC) plotted with the amount of water added (L) to watered trees; C, Ψ Ψ predawn ( pre) and midday ( mid) water potentials. Error bars represent 1 standard error.

the soil to the root zone of the control trees. (median for our watered treatment). This tran- Watered trees were at least 50 m from un- spirational rate could easily occur at our site watered trees and were separated by a 30-cm- given that potential evapotranspiration aver- deep trench or a road. Watering treatment aged 5.2 mm d–1 ± 0.14 (s) over the study continued until the end of the study on 5 Sep- period. tember (DOY 248). By this time each treat- Gravimetric soil water content (105ºC, 48 ment tree had received 935 L of water more hours) was measured 4 times throughout the than each control tree; averaged over the entire course of the study. Measurements were taken period that the irrigation treatment was applied, once at the beginning of the study, once just this amount is equivalent to an increase in before treatment began, once midway through water addition of 42.5 L tree–1 d–1. If com- treatment, and once again at the end of the pletely transpired, this would equal about 2 study. Soil samples (0–15 cm depth) were taken mm d–1 for a tree with a crown area of 20 m2 within the same area of each tree, 0.5 m north 178 WESTERN NORTH AMERICAN NATURALIST [Volume 65 from the bole using a 1-cm-diameter soil corer. ments were taken on mid-canopy branch tips The depth of 15 cm was justified because (1) between 0400 and 0600 hours for predawn Ψ these are rocky riparian soils in which repeat- water potential estimates ( pre) and between able deeper measurements are difficult, and 1400 and 1600 hours from sun-exposed parts Ψ (2) root distribution in trenches and minirhi- of the tree for midday water potential ( mid) zotron measurements suggest that about half values. Branches from each tree were mea- of surface roots are in the first 15 cm (data not sured until 2 measurements within 0.1 MPa shown). were obtained, and these were averaged to obtain a mean value for the tree. Whole-tree Physiology Canopy conductance and whole-tree hydrau- We measured sap flux and transpiration for lic conductance were determined for each study –2 –1 each study tree (g H2O m sapwood s ) using tree. Mean leaf-specific canopy conductance the Granier sap flux method at the base of the (Gc) was calculated over 15-minute periods for live crown in each study tree from DOY 214 each tree with the following model used by to 248 during 2002 (Granier 1987, Granier and Fischer et al. (2002), which substitutes vapor Loustau 1994, Granier et al. 1996, Clearwater pressure deficit for the difference in water et al. 1999). The Granier method uses a heated potential between leaf and air (Montieth and probe inserted 10 cm above a nonheated probe Unsworth 1990): in the sapwood. Each probe is 2 cm long with a copper constantan wire thermocouple inserted Gc = El /(VPD/Ap), (1) inside at the midpoint. We calculated sap flux where Gc is canopy conductance, El is leaf density based on the temperature difference –2 –1 between the heated and nonheated probe by specific transpiration rate (L H2O m LA s ), Granier’s empirical equation (Granier 1987, VPD is vapor pressure deficit (kPa), and Ap is average atmospheric pressure for the location Clearwater et al. 1999). Sensors were placed at of the study (~86.1 kPa for our site). up to 4 depths (0–2 cm, 2–4 cm, 4–6 cm, and Whole-tree hydraulic conductance was cal- 6–8 cm), depending on the diameter of the culated in a manner similar to that of Ryan et tree. In all cases we attempted to measure the al. (2000) and Fischer et al. (2002): entire length of the hydroactive xylem from the bark to the heartwood. Sensors were placed K = E /(Ψ –Ψ ), (2) at 1 randomly chosen aspect on each tree to h l pre mid randomize over aspect effects. Data were col- where Kh is whole-tree hydraulic conductance lected every 30 seconds and averages stored –2 –1 –1 (g H2O m s MPa ). Calculation of Kh was every 15 minutes using a Campbell Scientific limited to those dates when water potential CR10X data logger and a Campbell Scientific was measured. AM416 multiplexer (Logan, UT). Whole-tree We determined projected leaf area and sap- sap flux was calculated by apportioning sap wood area of each study tree. Leaf area was flux density rates from each probe to its corre- estimated for all trees using an allometric sponding sapwood area and summing data equation based on branch diameter. We devel- from all sapwood areas. Transpiration was ex- oped the equation by removing 3 branches of pressed as total daily whole-tree leaf specific 3 size classes from each tree at the end of our –2 –1 transpiration rate (El; L H2O m LA d ), study. All leaves were removed, dried (72 hours which was calculated by dividing whole-tree at 70°C), and weighed. A subsample of 10 sap flux by whole-tree leaf area (LA; see below). leaves from each branch was used to deter- On all trees used for sap flux measurements, mine specific leaf area (m2 kg–1) using an we measured predawn and midday plant water Agvis Imaging System (Decagon Devices, Pull- potentials with a pressure chamber (PMS man, WA). To estimate projected leaf area, we Instruments, Corvallis, OR; Ritchie and Hink- multiplied dried leaf weights from each branch ley 1975) 5 times during the last 10 days of the by specific leaf area. These data were combined study. Predawn values provide an estimate of with data from a previous study from other the soil water potential in the rooting zone of trees at the site (Fischer et al. 2004) to con- the tree, while midday water potentials provide struct a more robust equation for estimation of an estimate of tree water stress (Ritchie and projected leaf area (cm2) based on the diame- Hinckley 1975, Koide et al. 1990). Measure- ters (cm) of removed branches (r2 = 0.86, P < 2005] COTTONWOOD WATER RESPONSE DURING DROUGHT 179

0.01, leaf area = –32730.66 + 17007.86 * and weekly averages were also used to evalu- (branch diameter) + 4634.64 * (branch diame- ate irrigation effects. ter – 3.03)2). This equation was applied to the diameter at the base of the live crown (DBLC) RESULTS to yield an estimate of projected leaf area for each tree. To evaluate the accuracy of this Mean daily transpiration (El) was similar approach, we compared this branch-based esti- between watered trees and unwatered trees mate with whole-canopy leaf area estimates prior to experimental water additions (P = measured on other nearby trees; these 2 0.95, Fig. 1A), as was mean daily canopy con- approaches gave similar values (data not shown). ductance (Gc; P = 0.93; data not shown). Sapwood area (SA) was estimated using tree- Gravimetric soil water content also was similar cores for each tree, taken at the same height between watered and unwatered trees prior to and aspect as the sap flux sensors (base of the the watering treatment (P = 0.06; Fig. 1B). live crown), and visually distinguishing between Water addition significantly increased the light-colored sapwood and dark-colored heart- gravimetric soil water content (P = 0.03). wood. During the study period gravimetric soil water We determined whole-tree leaf loss over content under watered trees increased signifi- ± ± the course of the study for each study tree. On cantly from 5.9% ( 0.41 sx–) to 22.7% ( 0.98 sx–; DOY 229, before significant drought-induced P = 0.03); during the same period, gravimetric leaf loss, a litter bucket was placed under the soil water content among unwatered trees ± canopy of each tree. At the end of the study, decreased significantly from 7.0% ( 0.67 sx–) to ± we collected litter in each bucket, dried (72 6.2% ( 0.41 sx–; P = 0.02; Fig. 1B). Although hours at 70°C) it, and then weighed it. Using supplemental watering was effective in increas- the mass of each sample and the specific leaf ing surface soil moisture, El (P = 0.47; Fig. area values, we calculated leaf area loss. Crown 1A), Gc (P = 0.84; Fig. 2B), and whole tree area of each tree was estimated using perpen- hydraulic conductance (Kh; P = 0.63) were dicular measurements of crown diameter and not significantly different between watered Ψ Ψ using the average of the values to calculate and unwatered trees. Both pre and mid also crown area. This value was divided by bucket were similar between watered and unwatered Ψ Ψ area, and the result was multiplied by leaf area trees ( pre: P = 0.83, mid: P = 0.62), with Ψ Ψ from each bucket to estimate total crown leaf pre averaging about –0.54 MPa and mid loss during the course of the study. approximately –1.58 MPa during the measure- Air temperature and relative humidity were ment period (Fig. 1C). measured in an open field near the study site We found a significant inverse linear rela- Ψ 2 using a Campbell Scientific CS500 air temper- tionship between pre and Gc (P = 0.02, r = ature and humidity measurement probe (Logan, 0.44; Fig. 2A). However, there was no relation- UT, USA). We collected weather data every 30 ship between soil gravimetric water content seconds and averaged it hourly with a Camp- and Gc (P = 0.47; Fig. 2B). Similarly, we found bell Scientific CR10X data logger (Logan, UT). a significant inverse relationship between Ψ 2 We calculated vapor pressure deficit (VPD) pre and El (P = 0.04, r = 0.35; Fig. 2C), but from ambient temperature and relative humid- there was no significant relationship between ity measurements, assuming relative humidity gravimetric soil water content and El (P = inside the leaves was 100% (Montieth and 0.34; Fig. 2D). Relationships between VPD Unsworth 1990). and El were significant (P < 0.05, Fig. 3A) for All statistical analyses were done with the both watered trees (r2 = 0.33) and unwatered SAS JMP-IN statistical package (Version 4.0.4, trees (r2 = 0.21), as were relationships between α 2 SAS Institute, Cary, NC), with an of 0.05. VPD and Gc (P < 0.01, r = 0.42 [watered] Relationships among tree characteristics and and 0.44 [unwatered]; Fig. 3B). Slopes of re- physiological and environmental parameters sponse curves for Gc versus VPD relationships were analyzed using least-squares linear re- had overlapping 95% confidence intervals be- gression. Paired t tests of overall means were tween watered and unwatered trees and thus used to evaluate irrigation treatment effects on were not considered different. physiological variables; repeated measures Both El and Gc were not significantly cor- analyses of variance (RM ANOVAs) on daily related with either DBLC (P = 0.17 and 0.20, 180 WESTERN NORTH AMERICAN NATURALIST [Volume 65

–2 –1 Fig. 2. Soil and plant water relations during irrigation. Canopy conductance (Gc; L H2O m d ) versus predawn Ψ –2 water potential ( pre, A) and gravimetric soil water content (%, B). Leaf-specific transpiration (El; L H2O m leaf area –1 Ψ d ) versus predawn water potential ( pre, C) and gravimetric soil water content (%, D). For panels B and D, watered trees are represented on the right and unwatered trees on the left. respectively) or LA:SA ratios (P = 0.12 and water from the unsaturated (vadose) zone (i.e., 0.18, respectively; Fig. 4A). Whole-tree hydrau- part of the soil profile above the groundwater lic conductance (Kh) was unrelated to DBLC table and the capillary fringe zone), acting as (P = 0.14); however, a significant (P = 0.02, r2 facultative phreatophytes (Smith et al. 1991, = 0.43) inverse power (y = m * x–b) relation- Snyder and Williams 2000). Other research ship was found between Kh and the LA:SA ratio suggests that the principal source of water for (Fig. 4B). El was also related to Kh, but this is tree uptake may shift through a growing sea- likely driven by the calculation of Kh (eq. 2). son (Zhang et al. 1999), and cottonwood trees Supplemental watering had no detectable are known to have plastic and adaptable root effect on leaf abscission during drought; percent systems (Pregitzer and Friend 1996). However, leaf area lost was similar between watered and significant evidence exists to support an alter- unwatered trees (P = 0.29; data not shown). native hypothesis that cottonwoods exhibit re- Furthermore, we found no significant relation- sponse to surface water commensurate with the ships between percent leaf area lost and Kh, climatic history of their region. For example, Gc, or El (P = 0.90, 0.39, and 0.53, respec- Busch et al. (1992) did not find evidence of tively). However, leaf area loss was negatively soil moisture uptake at a study site that has Ψ 2 correlated with pre (r = 0.37, P = 0.04), historically unreliable summer precipitation suggesting that low water availability may have patterns, and this suggested phreatophytic be- led to leaf loss. Study trees lost between 0% havior. Conversely, Snyder and Williams (2000) and 29% of their leaf area during the course of found evidence of soil moisture uptake at a the study (mean leaf loss = 9%, median leaf study site where summer monsoonal pulse rain- loss = 4%), and leaf area varied from 75.2 m2 fall events are common. Our study site has a to 505.2 m2 among study trees (Table 1). historically predictable summer drought, and our results are consistent with this regional DISCUSSION climate hypothesis. Despite (1) successful increases in soil mois- Previous research has suggested that at cer- ture within the upper 15 cm of soil (Fig. 1), (2) tain times of the year cottonwood trees access observations that most study trees showed some 2005] COTTONWOOD WATER RESPONSE DURING DROUGHT 181

Fig. 3. Environmental control of whole-tree physiology: A, leaf-specific transpiration (El) versus vapor pressure deficit (VPD) for watered (filled circles) and unwatered trees (unfilled circles); B, leaf-specific canopy conductance (Gc) versus vapor pressure deficit (VPD) for watered (filled circles) and unwatered trees (unfilled circles). signs of water stress (e.g., yellowing of leaf tips more water per day than unwatered control and loss of leaves), and (3) environmental con- trees (Fig. 1). Sap flux measurements scaled to ditions conducive to water availability limiting the whole-tree level indicate that both watered growth (e.g., lack of recent precipitation, high and unwatered trees transpired an average of VPD, summer drought), our results indicate 24.7 L water d–1. Hence, water additions should that watered trees did not increase their rates have been more than enough to stimulate tran- of leaf-specific transpiration, canopy conduc- spiration rates that were low compared with tance, or whole-tree hydraulic conductance rela- other studies (Zhang et al. 1999, Schaeffer et tive to trees that did not receive supplemental al. 2000, Nagler et al. 2003). Similarly, canopy water (Fig. 2). Averaged over the entire exper- conductance was relatively low in all trees over imental period, watered trees received 42.5 L our study period (e.g., Zhang et al. 1999, Horton 182 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 1. Selected characteristics of trees monitored in this study. Clone codes serve as markers for individual genotypes but otherwise have no relation to cross type. Cross types are A (Populus angustifolia), B (backcross hybrids), and F1 (F1 hybrids). Diameter at Leaf area: base of live Sapwood sapwood area Clone Status crown (cm) Cross type Leaf area (m2) area (cm2)(m2 cm–2) wc-5 Unwatered 13.9 A 75.2 149.1 0.50 wc-5 Watered 17.6 A 125.1 167.5 0.75 1008 Unwatered 21.3 A 187.7 203 0.92 1008 Watered 16.4 A 107.5 105.6 1.02 t-15 Unwatered 19.3 A 152.3 161.8 0.91 t-15 Watered 20.5 A 173.1 173 1.00 996 Unwatered 22.5 B 210.7 225.9 0.93 996 Watered 17.7 B 126.6 105.8 1.20 11 Unwatered 18.3 B 136 99.9 1.36 11 Watered 22.9 B 218.7 221.7 0.99 1994 Unwatered 34.2 F1 505.2 704.9 0.72 1994 Watered 30.7 F1 403.8 775.2 0.52

tion in soil moisture in a study by Braatne et al. (1992). We conclude that during the height of summer drought, any uptake of increased soil moisture was insufficient to influence important physiological variables such as hydraulic conductance, canopy conductance, or transpiration. This may be consistent with factors other than water limiting both photosynthesis and, by default, water use as has been found in at least 1 other species in our region (Snyder et al. 2004). We speculate there are several other possible explanations for the lack of response to water additions in our study trees. First, greater loss of leaf area in unwatered trees relative to watered trees may have partially compensated for lower water availability to the trees, reducing any differences in leaf-specific transpiration rates. However, we found no difference in leaf area loss between watered and unwatered trees, suggesting that this potential mechanism cannot account for the lack of physiological Fig. 4. Architectural controls of whole-tree physiology; responsiveness to water additions in our study A, leaf-specific transpiration (El) versus leaf area to sap- trees. Nevertheless, we recognize that our mea- wood area ratio (LA:SA); B, whole-tree hydraulic conductance (K ) versus LA:SA. sure of leaf area lost due to drought was some- h what coarse, and so we cannot entirely rule out this possible mechanism for the lack in physi- et al. 2001a; but see Fischer et al. 2004), but ological response of the cottonwood trees to hydraulic conductance was not exceptionally water additions. low compared with other angiosperms (Becker Second, xylem dysfunction in the roots of et al. 1999). Dickmann et al. (1994) also found study trees might have impaired uptake of no difference in net photosynthesis rates be- water supplied to the trees by irrigation treat- tween irrigated and nonirrigated cottonwood ments. Cottonwoods are mostly drought intol- saplings, and our results are consistent with erant, limited to riparian corridors, and depen- responses of Populus clones to a 40% reduc- dent on groundwater, and they typically have 2005] COTTONWOOD WATER RESPONSE DURING DROUGHT 183 high vulnerability to cavitation (Blake et al. tated root tissues; Sperry and Saliendra 1994, Ψ 1996). On day 245 of the study, mid of study Hacke and Sauter 1996, Sperry and Iked, 1997), trees averaged –2.0 MPa (Fig. 1); this value may be avoidance of embolism repair in such corresponds to approximately a 70% loss of tissues during seasonal drought periods. This hydraulic conductivity in stems due to xylem level of genetic specificity would not be sur- embolism according to one P. angustifolia vul- prising given the extensive documented genetic nerability curve (Tyree et al. 1994), and poten- variation in cottonwood water-stress tolerance, tially 100% loss in some tissues according to root growth, and water use (Tschaplinski and Blake et al. (1996). Because we did not assess Blake 1989a, 1989b, Blake et al. 1996, Pregitzer the origin of the water transpired by trees in and Friend 1996, Fischer et al. 2004). When our current study, we cannot conclude un- surface soil moisture levels are more consis- equivocally that they did not take up surface tently high, whole-tree response to soil mois- Ψ soil moisture. However, since mid values ture increases may be more common. indicate high levels of stem xylem embolism We found a significant relationship between Ψ (but see Blake et al. 1996) and since roots are average daily El and pre, and average daily Ψ more susceptible to xylem embolism than Gc and pre. However, in both cases the rela- stems (Sperry and Saliendra 1994, Hacke and tionship was opposite of our hypothesized re- Sauter 1996, Sperry and Ikeda 1997), it is lationship; both El and Gc decreased rather Ψ probable that xylem dysfunction occurred dur- than increased with increasing pre values ing our study period. If significant xylem dys- (Fig. 2). This pattern may be partially due to function did occur in surface roots, and if the high transpiration rates of some cotton- embolism repair in cavitated roots was too wood trees and their poor stomatal regulation slow to reestablish function, then this might (Stettler et al. 1996, Fischer et al. 2004); the account for the lack of physiological response relatively high transpiration rates may have led in cottonwoods to the irrigation treatment in to progressively poor whole-plant water status Ψ our study. (as measured by lower pre values), reflecting Finally, it is possible that our irrigation that some cottonwood trees seem to operate treatments, which lasted 3 weeks, may not with a small margin of safety from cavitation have been long enough to elicit a physiological events (Blake et al. 1996). Furthermore, these response. For instance, Devitt et al. (1997) statistically significant negative correlations found a physiological response to surface irri- may be somewhat spurious given that they gation in trees from arid environments after 4 were fairly weak (r2 = 0.35 and 0.44, respec- weeks. However, given that sporadic pulse tively) and occurred over a fairly narrow range Ψ precipitation events are common and short- of pre values (–0.45 to –0.65 MPa). lived in the region (Loik et al. 2004), it is unlikely Our results suggest that, while some species that a 4-week response time to increased sur- may show strong physiologic responses to pulse face moisture is ecologically meaningful unless increases in soil moisture (Donovan and early precipitation events are harbingers of Ehleringer 1994, Cui and Caldwell 1997; also prolonged wet periods. Thus, a lack of response see Ogle and Reynolds 2004, Schwinning and within the time frame used in our study may Sala 2004), some cottonwood trees may exhibit be ecologically equivalent to a lack of response. little immediate physiological response to in- This lack of responsiveness in cottonwoods creases in soil moisture from precipitation to surface water additions may reflect an evo- events. This lack of response may be related to lutionary constraint on soil water uptake due a water-use strategy associated with regional to a long regional history of low summer precip- climate patterns, cavitation recovery, or other itation in northern Utah. For example, lack of physical determinants of water use such as significant response to soil moisture may be a depth to groundwater. Cottonwood riparian successful carbon allocation strategy of cotton- forests represent some of the most biologically woods. The timing of our irrigation treatments productive ecosystems in the West, and our corresponded with a period of seasonally dry data suggest that it is important to consider soils, when infrequent rains only temporarily potential nonresponsiveness to changes in soil elevate soil moisture. A long-term evolution- water availability when evaluating the impact ary response, maximizing carbon allocation and of climate change on these important and pro- limiting unnecessary growth (i.e., easily cavi- ductive ecosystems. 184 WESTERN NORTH AMERICAN NATURALIST [Volume 65

ACKNOWLEDGMENTS DRIEBE, E., AND T.G. W HITHAM. 2000. Cottonwood hybridization affects tannin and nitrogen content of leaf lit- We thank the Ogden Nature Center for ter and alters decomposition. Oecologia 123:99–107. FISCHER, D.G., T.E. KOLB, AND L.E. DEWALD. 2002. supporting our common garden facilities and Changes in whole-tree water relations during onto- the Mill Creek Youth Center juvenile deten- geny of Pinus flexilis and Pinus ponderosa in a high- tion facility for helping logistically. We thank elevation meadow. Tree Physiology 22:675–685. National Science Foundation grant DEB- FISCHER, D.G., S.C. HART, T.G. WHITHAM, G.D. MARTINSEN, AND P. K EIM. 2004. Ecosystem implications of genetic 0078280 and a Research Experience for Under- variation in water-use of a dominant riparian tree. graduates award under NSF grant DEB- Oecologia 139:188–197. 0078280 for financial support. We also thank GRANIER, A. 1987. Evaluation of transpiration in a Dou- Nathan Lojewski, Kevin Simonin, Gina Wimp, glas-fir stand by means of sap flow measurements. Jen Schweitzer, Tom Kolb, A.J. Thompson, and Tree Physiology 3:309–320. GRANIER, A., AND D. LOUSTAU. 1994. Measuring and mod- the Hart and Whitham laboratories for field eling the transpiration of a maritime pine canopy assistance, consultation, and providing com- from sap-flow data. Agricultural and Forest Meteo- ments on earlier versions of the manuscript. rology 51:309–319. Finally, we thank R.W. Baumann and 2 anony- GRANIER, A., P. BIRON, N. BREDA, J.-Y. PONTAILLER, AND B. mous reviewers for thoughtful reviews of this SAUGIER. 1996. Transpiration of trees and forest stands: short and long term monitoring using sapflow manuscript. methods. Global Change Biology 2:265–274. HACKE, U., AND J.J. SAUTER. 1996. Drought-induced xylem LITERATURE CITED dysfunction in petioles, branches, and roots of Popu- lus balsamifera L. and Alnus glutinosa (L.) Gaertn. BECKER, P., M.T. TYREE, AND M. TSUDA. 1999. Hydraulic Plant Physiology 111:413–417. conductances of angiosperms versus conifers: similar HORTON, J.L., T.E. KOLB, AND S.C. HART. 2001a. Physio- transport sufficiency at the whole-plant level. Tree logical response to groundwater depth varies among Physiology 19:445–452. species and with river flow regulation. Ecological BLAKE, T.J., J. SPERRY, T.J. TSCHAPLINSKI, AND S.S. WANG. Applications 11:1046–1059. 1996. Water relations. Pages 401–422 in R.F. Stettler, ______. 2001b. Responses of riparian trees to interannual H.D. Bradshaw, Jr., P.E. Heilman, and T.M. Hinckley, variation in ground water depth in a semi-arid river editors, Biology of Populus and its implications for basin. Plant, Cell and Environment 24:293–304. management and conservation. NRC-CNRC, Ottawa, HORTON, J.L., S.C. HART, AND T.E. KOLB. 2003. Physiolog- ON. ical condition and water source use of Sonoran BRAATNE, J.H., T.M. HINCKLEY, AND R.F. STETTLER. 1992. Desert riparian trees at the Bill Williams River, Ari- Influence of soil water on the physiological and mor- zona, USA. Isotopes in Environmental and Health phological components of plant water balance in Studies 39:69–82. OIDE OBICHAUX ORSE AND Populus trichocarpa, Populus deltoides and their F1 K , R.T., R.H. R , S.R. M , C.M. hybrids. Tree Physiology 11:325–339 SMITH. 1990. Plant water status, hydraulic resistance BUSCH, D.E., N.L. INGRAHAM, AND S.D. SMITH. 1992. Water and capacitance. Pages 161–178 in R.W. Pearcy, J.R. uptake in woody riparian phreatophytes of the south- Ehleringer, H.A. Mooney, and P.W. Rundel, editors, western United States: a stable isotope study. Eco- Plant physiological ecology: field methods and logical Applications 2:450–459. instrumentation. Kluwer Academic Publishers, Dor- CLEARWATER, M.J., F.C. MEINZER, J.L. ANDRADE, G. GOLD- drecht. STEIN, AND N.M. HOLBROOK. 1999. Potential errors LOIK, M.E., D.D. BRESHEARS, W.K. 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LAND SNAIL DIVERSITY IN WIND CAVE NATIONAL PARK, SOUTH DAKOTA

Tamara K. Anderson1

ABSTRACT.—Eighty-two soil samples and additional hand-collection in Wind Cave National Park yielded over 2000 terrestrial gastropod specimens. The specimens represent 26 different species, including a South Dakota species of concern, Vertigo arthuri. New South Dakota state records for Gastrocopta pellucida and Vertigo tridentata were recorded. Samples from grassland habitats were less likely to contain snails and had lower species richness than samples from either forest or shrubland habitats. Canyons, creek beds, bases of limestone cliffs, and shrublands are important habitats for snails in the park.

Key words: land snails, South Dakota, national parks, gastropod, diversity.

Pilsbry (1948:978) commented that “the munities. Strong relationships between snails molluscan fauna of the upper Missouri valley and vegetation communities have long been still remain[s] almost unknown.” More than 50 recognized (i.e., Shimek 1930, Burch 1956). years later, only a limited number of general Vegetation provides food and shelter for snails, works have been issued on terrestrial mollusks and the structure and density of the vegetation in the Great Plains (see Leonard 1959, and determine thermal and moisture conditions portions of Burch 1962, Hubricht 1985). In for soil-dwelling species. This study provides 1985, Hubricht still included South Dakota as information on land snail richness, distribu- one of the states most in need of snail surveys. tion, and local habitat relationships in WCNP Indeed, for the northern Great Plains, more that may help improve land snail habitat con- questions remain than have been answered on servation. molluscan diversity, distribution, taxonomy, and natural variation. The lack of information STUDY AREA makes management and conservation efforts difficult. Although conservation priorities for The Black Hills is a unique area biologi- land snails can be set using museum records cally and geologically (Froiland 1999). It is 900 alone (Heller and Safriel 1995), if few museum m to 1200 m higher than the surrounding Great records exist for a region (such as the Black Plains, and the area was not glaciated during Hills), the priorities will be less reliable. The the Pleistocene. The Black Hills also serves as National Park Service’s Resource Challenge a biological nexus where eastern, western, Initiative emphasizes the need to inventory northern, and southern ranges of many organ- natural resources in the national parks to bet- isms meet. A description of the wide variety of ter manage these resources (NPS 2000). vegetation communities in the Black Hills can The purpose of this study was to survey be found in Larson and Johnson (1999). Wind land snail species at Wind Cave National Park Cave National Park (WCNP) is located at the (hereafter referred to as WCNP). A survey of southern end of the Black Hills in southwest- snails in WCNP has not been conducted pre- ern South Dakota (Fig. 1). Famous for its viously, although surveys have been conducted underground wonders as home to the 6th elsewhere in South Dakota (Henderson 1927, largest cave in the world, WCNP also includes Jones 1932, Over 1942, Roscoe 1954, 1955), 11,454 ha of aboveground habitats, ranging including other parts of the Black Hills (Frest from mixed grasslands to ponderosa pine and Johannes 2002, Jass et al. 2002). I sampled (Pinus ponderosa) stands, to canyons in lime- land snails in many WCNP vegetation com- stone and sandstone.

1University of Colorado Museum, Boulder, CO. Present address: 285 Smith Street, Lander, WY 82520.

186 2005] LAND SNAILS OF WIND CAVE NATIONAL PARK 187

Fig. 1. Species richness varied across WCNP. Several locations (especially canyons/creekbeds) had high richness levels.

MATERIALS AND METHODS has been used successfully in other studies (Emberton et al. 1996, Nekola 1999). In this Fieldwork was conducted in May and June study I took samples from moist areas with 2002. Points for soil sampling were located in good litter cover or small, rocky debris, if such 27 different vegetation types (Table 1; as de- areas were available within the vegetation type. fined by park vegetation surveys and satellite When vegetation types did not contain such mapping research of Cogan et al. 1999) to microhabitats, I selected the sample location maximize the potential diversity of snails found. Three locations distributed around the park in that was most representative of that vegetation each habitat type were sampled where possi- type. ble. Specific locations of samples within these GPS locations (UTM coordinates, WGS 1984 vegetation types were selected on the ground Datum) of the sampling sites were recorded to maximize richness per sample. Maximizing using Garmin (GPS 12XL) and Trimble (Geo- richness by selecting likely microhabitats Explorer 3, version 1.04) units. GPS locations 188 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 1. Habitats sampled in Wind Cave National Park. Vegetation classes are described by the dominant vegetation in that habitat class and were used for selecting sampling sites (Cogan et al. 1999). General habitat category refers to forest (F), grassland (G), or shrubland (S). General habitat No. of species Vegetation class description category (F,G,S) identified Purple three-awn/ fetid marigold herbaceous G 0 Ponderosa pine on limestone cliff F 11 Redbeds (silt/sandstone) with sparse vegetation — 0 Little bluestem/ grama grass/ threadleaf sedge herbaceous with burned pine F 7 Chokecherry shrubland with burned pine S 5 Western wheatgrass/ Kentucky bluegrass complex with burned pine G 3 Emergent wetland complex — 2 Little bluestem/ grama grass/ threadleaf sedge herbaceous G 2 Western wheatgrass/ Kentucky bluegrass complex G 3 Introduced weedy graminoid herbaceous vegetation G 3 Needle and thread/ blue grama/ threadleaf sedge herbaceous G 1 Mountain mahogany/ side-oats grama shrubland (15%–50% cover) S 8 Mountain mahogany/ side-oats grama shrubland (50%–100% cover) S 11 Leadplant shrubland S 4 Chokecherry shrubland S 8 Snowberry shrubland S 2 Creeping juniper/ little bluestem shrubland S 8 Plains cottonwood/ western snowberry F 5 Boxelder/ chokecherry S 6 Bur oak stand F 12 Green ash/ elm/ snowberry F 7 Birch/ aspen stand F 7 Ponderosa pine woodland complex I F 0 Ponderosa pine/ little bluestem F 8 Ponderosa pine/ chokecherry F 2 Ponderosa pine woodland complex II F 2 Young ponderosa pine dense cover F 4

were used to create maps with ArcView software Therefore vegetation classes were grouped into (version 8.2; ESRI 2001). At each sampling general habitat categories: grassland, shrubland, location, 3.8 L of soil and litter was collected and forest. These general habitat categories were from within a 0.25-m2 quadrat. Soils were sifted used to determine if a relationship existed be- through a sieve series (Newark and Hubbard tween snail species richness or abundance brands), from 4 mm (#5 mesh size) to 0.25 mm among habitats. (#60). Soil from each sieve layer was visually searched and any snails or shells were removed. RESULTS Individual shells were examined under a micro- I collected 82 soil samples, of which 59 scope, counted, and identified to species where contained snails and/or shells. An additional 6 possible. In several samples, shells were bro- areas were spot-searched for snails, and snails ken or immature and could not be positively were found at 2 of these areas (Dry Creek and identified. Cold Brook Canyon). Over 2000 whole and Additional locations along watersheds were broken shells were examined, with 1738 iden- searched visually for snails. At 6 of these loca- tified to species. Live specimens were found at tions, I also took canyon/creekbed soil samples only 6 locations. Twenty-six different species for analysis. Two soil samples were also taken were identified (Table 2). Specimens have been in a prairie dog (Cynomys ludovicianus) town deposited at the Field Museum of Natural after a prairie dog researcher reported finding History in Chicago. shells in soil prairie dogs kicked out of their burrows. Species Descriptions The many different individual vegetation Identification of most species was fairly classes with few samples did not allow a robust straightforward using Pilsbry (1946, 1948) and analysis of vegetation versus snail presence. Burch (1962). Because live specimens were 2005] LAND SNAILS OF WIND CAVE NATIONAL PARK 189

TABLE 2. Land snail species and number of sites detected in WCNP, with taxonomy according to Turgeon et al. (1998), except as otherwise noted. Average per site refers to the average number of individuals in the samples where that species was found (i.e., includes only samples that contained that species). Habitat categories are F (forest), G (grassland), S (shrubland), and C (canyon/creek bed). Because canyons also may be somewhat forested, that category (C) is not distinct. Number Average Habitat types Species (common name) of sites per site (F,S,C) Catinella sp. 13 3 F,S,C Cionella lubrica (glossy pillar) 3 4 F Columella columella alticola (mellow column) 2 3 F Deroceras laeve (meadow slug) 2 2 C Discus catskillensis (angular disc) 3 3 F Discus whitneyi (forest disc) 5 8 F,C Euconulus fulvus (brown hive) 13 8 F,G,S,C Gastrocopta armifera (armed snaggletooth) 20 4 F,S Gastrocopta holzingeri (lambda snaggletooth) 21 11 F,G,S,C Gastrocopta pellucida (slim snaggletooth) 1 4 S Gastrocopta procera (wing snaggletooth) 8 4 F,S Hawaiia minuscula (minute gem) 6 7 F,G,S,C Nesovitrea binneyana (blue glass) 24 8 F,S,C Nesovitrea electrina (amber glass) 1 5 F Pupilla blandi (Rocky Mountain column) 3 5 S,C Pupilla hebes (crestless column) 1 32 F Pupilla muscorum (widespread column) 13 2 F,G,S,C Pupoides albilabris (white-lip dagger) 5 2 F,G,S Striatura milium (fine-ribbed striate) 1 2 F Vallonia gracilicosta (multirib vallonia) 35 17 F,G,S,C Vallonia parvula (trumpet vallonia) 11 15 F,G,S,C Vallonia pulchella (lovely vallonia) 7 9 F,S Vertigo arthuria 24F,S Vertigo tridentata (honey vertigo) 1 1 F Vitrina alaskanab 46F,S,C Zonitoides arboreus (quick gloss) 2 1 S,C aNo common name is listed in Turgeon et al. (1998). bTurgeon et al. (1998) list Vitrina pellucida as the “western glass-snail.” However, Pilsbry (1946) considered South Dakota specimens to be V. alaskana, and that convention is followed here. not available for most species (see below for assigning succineids to species (Burch 1962, discussion of the lack of living specimens), Hoagland and Davis 1987). Since no living shell characters alone were used for identifica- specimens of Catinella were found, the WCNP tion. Scientific names from this study follow samples could not confidently be assigned to a Turgeon et al. (1998). A few points to note on particular species. the identifications are explored here. COLUMELLA.—Specimens tended to be CATINELLA.—Specimens in the genus Cati- cylindrical as is the Columella columella alti- nella were not assigned to species level. Suc- cola pictured in Jass et al. (2002), and they are cineids (including Catinella, Oxyloma, and Suc- therefore identified as such. The only Colu- cinea) have few shell characteristics that can mella species Frest and Johannes (2002) iden- be used for identification purposes. The speci- tified was C. simplex, which narrows at the top mens in this study were assigned to the genus of the shell. It remains unclear whether the 2 Catinella based on work by Burch (1962:67) species reside in different portions of the that describes Catinella with a “shell relatively Black Hills, or if the WCNP specimens show small, generally 11 mm or less in length, dull; different variation in shape than the Frest and spire long, almost as long as the shell aper- Johannes (2002) specimens. ture.” Frest and Johannes (2002:70) state that GASTROCOPTA.—Several Gastrocopta species “shell characters of Catinella gelida are suffi- were identified. All except Gastrocopta pellu- ciently distinctive as to make it unlikely to be cida had been reported previously from South confused with other described North American Dakota. Gastrocopta pellucida is distinguished succineids.” In contrast, others have cautioned from other Gastrocopta by its narrow diame- against the use of shell characters alone in ter, tooth structure, and thin lip (Pilsbry 1948, 190 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 3. Comparison of WCNP gastropod species found in studies from the Black Hills and western South Dakota. Frest and Jass Roscoe Current Johannes et al. Over (1954, Species study (2002) (2002) (1942)a 1956)a Anguispira alternata x Arion fasciatus x Carychium exiguum xxx Carychium exile xx Catinella sp. x x Catinella gelida x Cionella lubrica xxc xx Columella columella alticola x Columella simplex xx Deroceras laeve xxxxx Discus catskillensis xx Discus whitneyi xxx x Discus shimeki xx Euconulus fulvus xx xx Gastrocopta agna x Gastrocopta armifera xxxxx Gastrocopta clappi x Gastrocopta contracta xx Gastrocopta holzingeri xx xx Gastrocopta pentodon xxx Gastrocopta pellucida x Gastrocopta procera xxxxx Gastrocopta tappaniana xx Helicodiscus eigenmanni x Helicodiscus parallelus xx Helicodiscus singleyanus x Hawaiia minuscula xxx x Limax maximus x Nesovitrea binneyana xx x Nesovitrea electrina xx Oreohelix cooperi xxx Polita hammonisb x Polygyra monodon x Punctum pygmaeum x Punctum minutissimum xx Punctum californicum xx Pupilla blandi xx xx Pupilla hebes xx Pupilla muscorum xxx Pupilla syngenes x

Burch 1962). The previously reported range and number of ribs on the shell (see Burch included Florida west to California with reports 1962). However, the specimens from this sur- as far north as Colorado and isolated locations vey did not neatly fit in the defined categories, in New Jersey and Maryland (Pilsbry 1948, generally having rib numbers within the range Burch 1962, Hubricht 1985). for multiple species. Frest and Johannes (2002) PUPILLA.—Two of the Pupilla species identi- include 3 ribbed Vallonia species—V. gracili- fied in this study, P. hebes and P. muscorum, costa, V. cyclophorella, and V. perspectiva—in were also found by Jass et al. (2002). The 3rd, their report from the Black Hills. However, a P. blandi, was the only Pupilla found by Frest recent revision of the genus Vallonia, which and Johannes (2002). Further analysis is needed includes specimens from all over the world, to determine whether these species are re- found considerable variability within Rocky stricted to different portions of the Black Hills. Mountain populations of V. gracilicosta (Ger- VALLONIA.—The main shell characteristics ber 1996). For the purposes of this study, used to define differences in Vallonia species larger specimens (>2 mm) were considered V. include shell diameter, umbilicus diameter, gracilicosta, while smaller specimens (<2 mm) 2005] LAND SNAILS OF WIND CAVE NATIONAL PARK 191

TABLE 3. Continued. Frest and Jass Roscoe Current Johannes et al. Over (1954, Species study (2002) (2002) (1942)a 1956)a Pupoides albilabris xxxxx Pupoides inornatus xx Stenotrema leai x Striatura milium xx Strobilops labyrinthica x Succinea avara xx Succinea grosvenorii xx Succinea haydeni xx Succinea higginsi xx Succinea indiana x Succinea nuttalliana xx Succinea ovalis x Succinea stretchiana x Vallonia albula x Vallonia costata xx Vallonia cyclophorella xx x Vallonia gracilicosta xxxxx Vallonia parvula xxx Vallonia perspectiva xxx Vallonia pulchella xx xx Vertigo arthuri xx Vertigo concinula x Vertigo elatior x Vertigo gouldi x Vertigo milium xx Vertigo modesta xx Vertigo ovata xx Vertigo paradoxa x Vertigo tridentata x Vitrina alaskana/pellucidad xx xx Zoogenetes harpa x Zonitoides arboreus xxxxx Zonitoides minuscula x Zonitoides nitida xx Zonitoides singleyana x aThese studies report species from areas of eastern South Dakota as well. bThe identity of Over’s (1942) Polita hammonis is unclear. Polita was a former name for Oxychilus, but the only hammonis in the Zonitinae recorded in Pilsbry is a species of Nesovitrea. Over (1942) may have been referring to Nesovitrea electrina or N. binneyana. cFrest and Johannes refer to their specimens as Choclicopa lubricella. Choclicopa is considered a synonym of Cionella (Pilsbry 1948, Turgeon et al. 1998). Tur- geon et al. (1998) state that C. lubrica is the only species found in North America. Hubricht (1985) recognizes both species, but offers no distinction between them. For the purposes of this table, they are considered the same entity. dOnly Vitrina pellucida is recognized by Turgeon et al. (1998). Other sources mention only V. alaskana in the western U.S. (Hubricht 1985). Pilsbry (1946:502) states that V. alaskana is distinct from the European V. pellucida. were considered V. parvula. These assignments the teeth (Pilsbry 1948). Vertigo arthuri is a follow Burch (1962), but a more conservative species whose distribution is not fully under- assignment would be to consider all Vallonia stood. Originally it was recognized only from specimens as V. gracilicosta. North Dakota (Pilsbry 1948). It had been pre- Vallonia pulchella has no ribs and so should viously identified in the Black Hills by Frest be easy to distinguish from other Vallonia. How- and Johannes (2002) and has been recently ever, in the current study, ribs on a few older reported by Nekola (2002) from upper Mid- Vallonia specimens were wearing off, which west locations. could result in worn shells being incorrectly Vertigo tridentata, with only 3 teeth, was not identified. In this study specimens with no sign previously reported from South Dakota. The of ribs were considered to be V. pulchella. previously recognized range for V. tridentata VERTIGO.—Two Vertigo species were found: stretched from Maine south to Tennessee in V. arthuri and V. tridentata. These species are the east and Minnesota south to Texas in the differentiated by the number and position of west (Pilsbry 1948, Burch 1962, Hubricht 1985). 192 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Richness and Habitat earlier studies. Both were rare in WCNP, with Characteristics only a single location each. Individual soil samples contained from 0 to Notably absent from WCNP are specimens 210 shells. WCNP contains 35% of the land of Oreohelix. Although fairly common on snail diversity known for western South Dakota shaded talus slopes in more northern areas of (Table 3). On average, samples with snails con- the Black Hills, Oreohelix becomes less fre- tained 29 individuals of 3 different species. quent in the central and southern areas of the Sixty-three samples from WCNP contained 3 Black Hills (Frest and Johannes 2002). Jass et or fewer species. Common species dominated al. (2002) also did not find any evidence of the samples, with just 5 species (Vallonia gra- Oreohelix in their study, which included the cilicosta, Gastrocopta holzingeri, Nesovitrea extreme southern Black Hills. The southern binneyana, Vallonia parvula, and Euconulus extent of the Black Hills differs in soil type, fulvus) accounting for 75% of the individuals geology, moisture, and number of deciduous identified. trees (Froiland 1999). Any or all of these fac- Snail shells were found in at least 1 sample tors may contribute to slight differences in from all surveyed vegetation types except pur- snail communities. ple three-awn/fetid marigold herbaceous com- The South Dakota Department of Game, munity and redbeds (silt/sandstone) with sparse Fish and Parks includes 5 gastropods among vegetation. Chi-square analyses showed that their rare species: Vertigo arthuri, Vertigo para- general habitat categories (forest, grassland, doxa, Discus shimekii, Catinella gelida, and shrubland) were significantly different in the Oreohelix strigosa cooperi (SDDGFP 2001). number of sites where snails were present. Vertigo arthuri was found in WCNP. The Cati- Samples from grassland habitats were more nella specimens found here may be C. gelida likely to contain no snails. but cannot be confidently assigned to species Species richness also varied across the land- without analysis of internal anatomy. The other scape (Fig. 1), but the highest levels appear 3 species were not found in WCNP, although centered along creek beds in canyons. Species they have been reported elsewhere in the Black richness was also lower in grassland habitats Hills (Frest and Johannes 2002). than in either forests or shrubland habitats. Species Richness A few species were associated with a particular habitat category or categories. Table 2 A previous Black Hills study reported 0 to shows associations between snail species and 17 species per site with an average of 4.3 their preferred habitats. Cionella lubrica and when only sites with snails present were Columella columella alticola were found only included (Frest and Johannes 2002). A few in forested habitat. Deroceras laeve was found species (Discus whitneyi, Zonitoides arboreus, only in canyons or along creek beds. Nesovit- Euconulus fulvus, Nesovitrea binneyana, and rea binneyana was more abundant in forests Vitrina pellucida) also dominated Frest and than in either grasslands or shrublands, al- Johannes’s (2002) study. Their reported domi- though it was present in all habitats. Gastro- nance is based on occurrence, not abundance, copta armifera was equally abundant in shrub- since they did not count all individuals. Never- lands and forests. Other species tested showed theless, the frequency of D. whitneyi, Z. arbor- no difference in abundance among habitat eus, and V. pellucida is interesting since these types. species were relatively rare at WCNP. This may be attributable to site selection because DISCUSSION Frest and James (2002) focused on moister habitats and talus slopes, which are rare in Comparison of Species List WCNP, rather than more evenly sampling with Other Studies across all vegetation types. The species found in this study are similar Species richness in the Black Hills is not to those found in other studies in the region unlike results from Beetle’s (1997) study in (i.e., Over 1942, Roscoe 1954, 1955, Frest and Yellowstone aspen stands, which reported 3 to Johannes 2002, Jass et al. 2002; Table 3). Two 5 snails per stand. These stands were studied species reported here, Gastrocopta pellucida after a wildfire burned the area. Richness in- and Vertigo tridentata, were not reported in creased to 11 species in a “damp site . . . [with] 2005] LAND SNAILS OF WIND CAVE NATIONAL PARK 193 favorable litter, soil, and moisture” (Beetle Shells in the drier climates of the Great Plains 1997:8). likely persist slightly longer, but even so, shells Studies from other regions have reported recovered in this study must represent snails even higher levels of species richness. In Wis- that were alive within the recent past. A 3rd consin, 1-m2 quadrats averaged 6.6 species explanation is that during these unfavorable (Nekola and Smith 1999). A study including drought conditions, snails in WCNP have sought sites across the Great Lakes region found 11% refuge in areas not sampled. Unfortunately, of samples contained 24 or more species (Nekola these hypotheses cannot be tested with the 1999). These observed richness numbers are available data. far below the 61 species ⋅ km–2 reported from Size of Specimens a tropical rainforest in Malaysian Borneo (Schilthuizen and Rutjes 2001). Emberton Several species of WCNP land snails were (1995) reported that the highest diversity of smaller in size than reported in previous de- terrestrial gastropods in the United States was scriptions. Cionella lubrica was 2.8 mm tall 44 species in <4 ha found by Leslie Hubricht and had only 4 whorls although they are listed in the mountains of Kentucky. Coniferous in Pilsbry (1948) as being 5–6.5 mm and hav- forests and grasslands are expected to have ing 5.5 to 6 whorls. Vitrina alaskana speci- lower diversities of land snails than other mens ranged from 2.3 mm to 3.8 mm in diam- habitat types (Solem 1984). eter, although Pilsbry (1946) described them Observed numbers per sample (Table 2) are as 5 mm or larger. WCNP snails were only also lower than in other studies. Van Es and slightly smaller than those in Alberta aspen/ Boag (1981) found an average of 11.6 Vitrina poplar forests (Van Es and Boag 1981). For alaskana, 48.9 Discus whitneyi, and 27.3 example, their Vitrina alaskana specimens aver- Euconulus fulvus per sample. It is not clear aged 4.35 mm (n = 152). Pilsbry (1948:932) whether their litter samples from 0.5-m2 areas discussed a small form of Pupilla blandi east of in size represent the same volume of soil as in the Rocky Mountains, adding that “it is proba- the WCNP study. Because their study also bly a ‘hunger form’ occupying arid situations.” occurred in a forest in Alberta with abundant Since this phenomenon was observed in sev- deciduous trees (Populus spp.), it is expected eral species, WCNP may not be optimal for that more snails would be present. maximizing growth. Few Living Specimens Habitat Type The low number of living specimens col- Seven generalist species (Euconulus fulvus, lected in WCNP cannot be easily explained. Gastrocopta holzingeri, Hawaiia minuscula, Frest and Johannes (2002) do not indicate what Pupilla muscorum, Pupoides albilabris, Vallo- percentage of their findings were alive but sug- nia gracilicosta, and Vallonia parvula) were gest that living snails were commonly observed. found in all habitats (Table 2), while other Emberton et al. (1996) found soil samples had species were more specialized. For example, fewer live samples than other sampling meth- Deroceras laeve was found only in canyon/ ods, but they reported living representatives creek bed areas. Cionella lubrica and Colu- of 28% of snail species in soil samples. mella columella were only in forest habitat. One potential explanation for the low num- Nesovitrea binneyana was more abundant in ber of live specimens is a possible die-off of forested habitat. Gastrocopta pellucida was snails. One of the main factors in snail death is found only at 1 site in shrubland. Nesovitrea dessication (Solem 1984). Snail populations may electrina, Striatura milium, and Pupilla hebes fluctuate with environmental stress, and since were also only at 1 location. Discus catskillen- WCNP has been under drought conditions for sis may prefer forested habitat, although it was the past few years, it is likely many snails have also found in a wetland sample. died. Another explanation is that shells col- Some shrubland areas were also important lected are only remains from a time period snail habitats at WCNP. Six of the 12 samples when the habitat was more suitable for snails. from mountain mahogany (Cercocarpus mon- Pearce (2002, personal communication) found tanus), chokecherry (Prunus virginiana), and that shells in eastern forests exist in the soil creeping juniper ( Juniperus horizontalis) sites about 30 years before completely decaying. had species richnesses of 5 or higher. 194 WESTERN NORTH AMERICAN NATURALIST [Volume 65

No species were found only in grasslands, ACKNOWLEDGMENTS in contrast to the ordination analyses of Nekola (2003) that showed many snail species, includ- This project was funded by NPS Contract ing several found at WCNP (Cochlicopa lubrica, P1505020021. Collection permits were obtained Discus whitneyi, Nesovitrea electrina, Gastro- from NPS (WICA-2002-SCI-0028) and South copta armifera, Gastrocopta procera, Pupilla Dakota (License 33). Special thanks go to Barb muscorum, Pupoides albilabris, Vallonia parvula, Muenchau of WCNP, Ed Delaney formerly and Vallonia pulchella) appeared to be grass- of WCNP, and Jochen Gerber of the Field land specialists. Nekola incorporated more Museum of Natural History. samples across a much larger spatial scale which gives his results more credence. How- LITERATURE CITED ever, because the grasslands of the Great Lakes BEETLE, D.E. 1989. Checklist of recent Mollusca of Wyo- region of Nekola’s study are moister than the ming, USA. Great Basin Naturalist 49:637–645. arid region of western South Dakota, those ______. 1997. Recolonization of burned aspen groves by grasslands may be able to support more species. land snails. Yellowstone Science 5:6–8. Nekola apparently did not sample shrubland, BURCH, J.B. 1956. Distribution of land snails in plant associations in eastern Virginia. Nautilus 70:60–64. which may have influenced the preferences ______. 1962. How to know the eastern land snails. shown at WCNP. Brown Company Publishers, Dubuque, IA. 214 pp. Earlier studies questioned whether snails COGAN, D., H. MARRIOTT, J. VONLOH, AND M.J. PUCHER- occupy coniferous forests in western North ELLI. 1999. USGS-NPS Vegetation Mapping Pro- gram Wind Cave National Park, South Dakota. U.S. America. Karlin’s (1961) surveys across Mon- Department of the Interior, Technical Memorandum tana, Colorado, and New Mexico reported that 8260-99-03. 99% of snails occurred within forests where EMBERTON, K.C. 1995. Land-snail community morpholo- deciduous trees were a significant component. gies of the highest-diversity sites of Madagascar, North Kralka (1986) also found most snail species America, and New Zealand, with recommended alternatives to height-diameter plots. Malacologia preferred areas dominated by deciduous vege- 36:43–66. tation in Alberta, Canada. He did note that EMBERTON, K.C., T.A. PEARCE, AND R. RANDALANA.1996. Vertigo gouldi preferred coniferous habitats. Quantitatively sampling land-snail species richness WCNP data and those of Frest and Johannes in Madagascan rainforests. Malacologia 38:203–212. ENSZ, H.H. 1990. Soil survey of Custer and Pennington (2002) contradict those findings, since most counties, Black Hills parts, South Dakota. USDA, WCNP forest sites are dominated by pon- Soil Conservation Service. derosa pine. Locasciulli and Boag (1987) also ESRI. 2001. ArcView 8.2. ESRI, Redlands, CA found the highest densities of snails in conifer- FORD, R. 2002. Wind Cave National Forest soils. Unpub- ous forests in Alberta. Although the most lished report to Wind Cave National Park. FREST, T.J., AND E.J. JOHANNES. 2002. Land snail survey of diverse (12 species) location in WCNP was a the Black Hills National Forest, South Dakota and stand of bur oak, Quercus macrocarpa, a cliff Wyoming, summary report 1991–2001. Contract 43- site dominated by ponderosa pine had 7 species. 67TO-8-1085. Final report to the USDA Forest Ser- Carbonate cliffs and canyons often provide im- vice, Custer, SD. FROILAND, S.G. 1999. Natural history of the Black Hills portant habitats for snails (Beetle 1989, Nekola and Badlands. Center for Western Studies, Sioux Falls, and Smith 1999). Two samples along Dry Creek SD. 225 pp. contained over 300 individuals and 11 species GERBER, J. 1996. Revision der gattung Vallonia Risso 1826 total. In WCNP these areas tend to have cal- (Mollusca: Gastropoda: Valloniidae) [Revision of the careous soils (Ensz 1990, Ford 2002). genus Vallonia]. Schriften zur Malakozoologie 8:1–227. HELLER, J., AND U.N. SAFRIEL. 1995. Setting priorities for the conservation of land snail faunas. Pages 91–110 CONCLUSIONS in A.C. van Bruggen, S.M. Wells, and T.C.M. Kemper- man, editors, Biodiversity and conservation of the WCNP supports a relatively high diversity Mollusca. Backhuys Publishers, Oegstgeest-Leiden, of land snails, with 35% of the regional species The Netherlands. HENDERSON, J. 1927. Some South Dakota Mollusca. Nau- represented. Recent droughts have probably tilus 41:19–20. affected snail populations in the park, based HOAGLAND, K.E., AND G.M. DAVIS. 1987. The succineid on the large number of empty shells found in snail fauna of Chittenango Falls, New York: taxonomic this study. Riparian areas (especially Dry Creek status with comparisons to other relevant taxa. Pro- ceedings of the Academy of Natural Sciences of and Cold Creek), shrubland, and limestone Philadelphia 139:465–526. cliffs are especially important for WCNP snail HUBRICHT, L. 1985. The distributions of the native land diversity and should be managed with care. mollusks of the eastern United States. Fieldiana 2005] LAND SNAILS OF WIND CAVE NATIONAL PARK 195

Zoology No. 24, Field Museum of Natural History, PEARCE, T.A. 2002. When a snail dies in the forest, how Chicago, IL. long will the shell persist? Abstract. Page 83 in R.T. JASS, C.N., J.I. MEAD, A.D. MORRISON, AND L.D. AGEN- Dillon, Jr., editor, Program and abstracts of the 68th BROAD. 2002. Late Pleistocene mollusks from the meeting of the American Malacological Society, southern Black Hills, South Dakota. Western North Charleston, SC. American Naturalist 62:129–140. PILSBRY, H.A. 1946. Land Mollusca of North America JONES, D.T. 1932. Mollusks in the vicinity of Yankton, (north of Mexico), volume 2, part 1. Monograph 3, South Dakota. Nautilus 45:115–118. Academy of Natural Sciences of Philadelphia. KARLIN, E.J. 1961. Ecological relationships between vege- ______. 1948. Land Mollusca of North America (north of tation and the distribution of land snails in Montana, Mexico), volume 2, part 2. Monograph 3, Academy Colorado and New Mexico. American Midland Nat- of Natural Sciences of Philadelphia. uralist 65:60–66. ROSCOE, E.J. 1954. Terrestrial gastropods from the Black KRALKA, R.A. 1986. Population characteristics of terres- Hills, Lawrence County, South Dakota. Proceedings trial gastropods in boreal forest habitats. American of the Utah Academy of Sciences, Arts and Letters Midland Naturalist 115:156–164. 31:67–72. LARSON, G.E., AND J.R. JOHNSON. 1999. Plants of the Black ______. 1955. Additional South Dakota terrestrial gastro- Hills and Bear Lodge Mountains. South Dakota State pod records. American Midland Naturalist 54:511–512. University, Brookings. 608 pp. SCHILTHUIZEN, M., AND H.A. RUTJES. 2001. Land snail LEONARD, A.B. 1959. Handbook of gastropods in Kansas. diversity in a square kilometre of tropical rainforest Museum of Natural History Miscellaneous Publica- in Sabah, Malaysian Borneo. Journal of Molluscan tion 20, University of Kansas, Lawrence. 224 pp. Studies 67:417–423. LOCASCIULLI, O., AND D.A. BOAG. 1987. Microdistribution SHIMEK, B. 1930. Land snails as indicators of ecological of terrestrial snails (Stylommatophora) in forest litter. conditions. Ecology 11:673–686. Canadian Field-Naturalist 101:76–81. SOLEM, A. 1984. A world model of land snail diversity and NPS. 2000. Resource Challenge Initiative. National Park abundance. Pages 6–22 in A. Solem and A.C. van Service. http://www.nature.nps.gov/challenge/bro- Bruggen, editors, World-wide snails: biogeographi- chures/brochure2.html. cal studies on non-marine Mollusca. E.J. Brill, Lei- NEKOLA, J.C. 1999. Terrestrial gastropod richness of car- den, The Netherlands. bonate cliff and associated habitats in the Great SDDGFP. 2001. Rare, threatened, and endangered animal Lakes region of North America. Malacologia 41: species tracked by the South Dakota Natural Her- 231–252. itage Program. South Dakota Department of Game, ______. 2002. Effects of fire management on richness and Fish and Parks. www.state.sd.us/gfp/Diversity/Rare abundance of central North American grassland land Animal.htm. snail faunas. Animal Biodiversity and Conservation TURGEON, D.D., J.F. QUINN, JR., A.E. BOGAN, E.V. COAN, 25:53–66. F. G . H OCHBERG, W.G. LYONS, P.M. MIKKELSEN, ET AL. ______. 2003. Large-scale terrestrial gastropod commu- 1998. Common and scientific names of aquatic in- nity composition patterns in the Great Lakes region vertebrates from the United States and Canada: mol- of North America. Diversity and Distributions 9: lusks. 2nd edition. American Fisheries Society, Spe- 55–71. cial Publication 26, Bethesda, MD. NEKOLA, J.C., AND T.M. S MITH. 1999. Terrestrial gastropod VAN ES, J., AND D.A. BOAG. 1981. Terrestrial molluscs of richness patterns in Wisconsin carbonate cliff com- central Alberta. Canadian Field-Naturalist 95:75–79. munities. Malacologia 41:253–269. OVER, W.H. 1942. Mollusca of South Dakota. Natural His- Received 23 April 2003 tory Studies 5. University of South Dakota, Vermil- Accepted 4 October 2004 lion. Western North American Naturalist 65(2), © 2005, pp. 196–201

INFLUENCE OF GRASSLAND TYPE, NEST TYPE, AND SHRUB ENCROACHMENT ON PREDATION OF ARTIFICIAL NESTS IN CHIHUAHUAN DESERT GRASSLANDS

Lisa C. Mason1, Martha J. Desmond1,2, and M. Sofia Agudelo1

ABSTRACT.—Nest predation on artificial nests was examined in relation to nest type, grassland type, and shrub encroachment in Chihuahuan Desert grasslands in southern New Mexico. Open-cup ground, open-cup shrub, and spherical shrub nests (n = 210), mimicking Eastern Meadowlarks (Sturnella magna), Black-throated Sparrows (Amphispiza bilineata), and Cactus Wrens (Campylorhynchus brunneicapillus), were placed in 10 grasslands of tobosa (Pleuraphis mutica) and black grama (Bouteloua eripoda) with low and heavy levels of mesquite encroachment. Nest predation varied among nest types, grassland types, and shrub encroachment, with highest levels of predation occurring on open-cup shrub nests in tobosa grasslands with heavy shrub encroachment. We detected a significant interaction between nest type and shrub encroachment, but not between grassland type and nest type or grassland type and shrub encroachment. Combined predation rates from the 3 nest types were positively associated with shrub density. The encroachment of shrubs into desert grasslands may act as a corridor for a diversity of species historically not associated with desert grasslands to occupy or move through a patch, increasing vulnerability to nest predation.

Key words: predation, desertification, shrub encroachment, desert grasslands, artificial nests, nest type, Coturnix Quail, passerines, tobosa, black grama.

Nest predation on eggs and nestlings pro- past 150 years. This desertification of the land- foundly affects reproductive success of birds scape has been primarily attributed to the in- and is considered the primary cause of nest troduction of domestic livestock to the region failure in most land birds (Ricklefts 1969, Roten- in the late 1800s combined with periodic berry and Wiens 1989, Major et al. 1994, Martin drought (Buffington and Herbel 1965, Fredrick- 1995). Birds have evolved numerous defenses son et al. 1998, Kerley and Whitford 2000). to reduce predation risk, and studies have Former open grasslands dominated by black shown increased rates of nest predation to be grama (Bouteloua eripoda) and tobosa (Pleura- associated with habitat fragmentation, nest lo- phis mutica), the 2 grassland types diagnostic cation within a patch, and nest type (Donovan of Chihuahuan Desert grasslands, are being et al. 1995, Robinson et al. 1995, Dion et al. replaced by shrubs, primarily honey mesquite 2000, Flaspohler et al. 2001, Manolis et al. (Prosopis glandulosa) and creosote bush (Larrea 2002). In the desert Southwest nest construc- tridentata). For example, on the USDA Jorna- tion of most passerine nests can be divided da Long Term Experimental Range (LTER) in into 3 categories: open-cup ground nests such southern New Mexico, plots with >90% grass as Horned Larks (Eremophila alpestris) and cover in the 1950s had <25% grass cover by Eastern Meadowlarks (Sturnella magna), open- 1963 (Buffington and Herbel 1965). cup shrub nests within 3 m of the ground such The system-level response to these land- as Black-throated Sparrows (Amphispiza bilin- scape-scale changes has not been thoroughly eata) and Cassin’s Sparrows (Aimophila cassinii), investigated. Whitford (1997) found that species and spherical shrub nests within 3 m of the richness, diversity, and abundance of birds and ground such as Cactus Wrens (Campylorhyn- small mammals were higher in desertified sites. chus brunneicapillus) and Verdins (Auriparus He attributed this to grassland species persist- flaviceps). ing while shrub-adapted species colonized The transformation of desert grasslands to a these sites. Pidgeon et al. (2001) found avian shrub-dominated system in the Chihuahuan diversity was highest in mesquite-dominated Desert has been an ongoing process over the plots compared to black grama grasslands and

1Department of Fishery and Wildlife Sciences, Box 30003, MSC 4901, New Mexico State University, Las Cruces, NM 88003. 2Corresponding author.

196 2005] NEST PREDATION 197

2 other shrub community types. While similar- burrograss (Scleropogon brevifolius), fluffgrass ities were apparent among communities, they (Dasyochloa pulchela), snakeweed (Gutierrezia found that 30% of the avifauna was unique to spp.), creosote bush (Larrea tridentata), tar- each of the 4 vegetation communities. They bush (Flourensia cernua), soaptree and torrey suggest shrub encroachment has resulted in a yucca (Yucca elata and Y. torreyi), and cane major turnover in the avifauna of the region. cholla (Opuntia imbricata). Annual precipita- In addition to these observed shifts in avian tion averages 23 cm but can be variable, and and mammalian species composition, Kerley most rainfall comes in the form of monsoonal and Whitford (2000) report that rodents have summer rains between July and September replaced ants as the primary granivore in the (Brown 1982). Chihuahuan Desert. Shifts in ecosystem structure and function METHODS will have long-term consequences on survival and reproduction of associated fauna. We were We selected 10 grassland patches from the particularly interested in the effects of this Jornada LTER’s GIS database of cover types shift on nest predation in birds. Many species based on 3 criteria: dominant grassland type of small mammals and birds are nest preda- (black grama or tobosa), size of the grassland tors, and the higher diversity and abundance patch, and level of shrub encroachment. We of these taxa in desertified sites in the south- attempted to select an even number of open western United States may contribute to a and shrub-encroached tobosa and black grama shift in the role of predation on avian nests in grasslands and to avoid complications due to this system. We hypothesized nest predation grassland patch size. With one exception (19 ha) in tobosa and black grama grassland patches all grassland patches were >40 ha (19–522 ha), would not differ between patch type but would and all transects were located centrally within differ between high and low levels of shrub each patch to avoid edge effects. The center of encroachment, with higher rates of predation each grassland patch was selected from the in shrub-encroached sites. We hypothesized GIS database, its coordinates determined, and that predation rates and types of predators a 1050-m transect was established using the would differ among the 3 nest types due to center of the plot as the transect center. variability in detection. We predicted predation Artificial nests were placed in patches begin- rates would be highest for open-cup ground ning 28 June and monitored every 4 days over nests and lowest for spherical shrub nests due a 12-day period, mimicking the incubation per- to differences in accessibility and concealment iod of most passerines (Davison and Bollinger from predators. Spherical shrub nests have 2000, Dion et al. 2000). Data collection was greater concealment of nest contents than completed by 13 July. In the desert Southwest open-cup nests, and others have suggested peak nesting is timed with the monsoonal rains open-cup ground nests experience higher rates (Mendez 2000, Agudelo and Desmond unpub- of predation in grassland systems (Martin lished data), which typically arrive in mid-July. 1993a). We predicted small mammals would Three types of artificial nests were used in this be the primary predator on ground nests, study: open-cup ground nests, open-cup shrub whereas avian predators would be the primary nests, and spherical (enclosed) shrub nests. We predator for both types of shrub nests. constructed open-cup ground nests by creating a small scrape within a grass clump and STUDY AREA lining the scrape with live and dead grass to mimic the natural nest of an Eastern Meadow- Research was conducted during summer lark. Open-cup shrub nests and spherical shrub 2003 on the USDA Jornada LTER, located 30 nests were commercial finch and canary nests miles north of Las Cruces, New Mexico. This constructed of wicker and hemp, respectively. area is primarily a mosaic of black grama, Open-cup shrub nests were lined with dead tobosa, and dropseed (Sporobolus spp.) grass- grass to mimic the natural nest of a Black- lands in various stages of desertification, in- throated Sparrow, and spherical shrub nests cluding heavy mesquite encroachment and were lined with dead grass and covered with coppice dune formation. Other dominant veg- natural vegetation, small sticks, and forbs to etation includes three-awns (Aristida spp.), mimic the natural nest of a Cactus Wren. These 198 WESTERN NORTH AMERICAN NATURALIST [Volume 65 nests were placed in shrubs 1–2 m from the nest type (open-cup ground, open-cup shrub, ground. Commercial canary nests, constructed or spherical shrub) using a 3-way analysis of of hemp, were stained to achieve a more nat- variance. Rates of predation among nests placed ural color and along with finch nests were left in cholla, mesquite, and yucca shrubs were ex- outside for a week prior to use in this study to amined using a 1-way analysis of variance for take on a natural odor. Attempts were made to spherical and open-cup shrub nests combined. mimic the design and placement of natural Simple linear regression was used to examine nests such that artificial nests would not be the association between predation rate and more conspicuous to a visual predator (Martin shrub density. 1987, 1995). Twenty-one nests, spaced 50 m apart, were RESULTS placed within each grassland patch at alternat- ing distances of 18 m from the transect line or Of 210 nests placed in Chihuahuan Desert to the nearest appropriate shrub or grass patch. grasslands, 89 (39%) were lost to predation. We alternated nest types and recorded their Rates of predation varied among nest types coordinates with a GPS unit. Two eggs were (F2,18 = 4.77, P = 0.022), with significantly placed within each nest, a Japanese Quail higher predation on open-cup shrub nests; (Coturnix coturnix) egg and an artificial egg. 60% of open-cup shrub nests, 41% of spherical Artificial eggs were constructed from a non- shrub nests, and 16% of open-cup ground hardening modeling clay, permoplast, and were nests were lost to predators throughout the modeled to mimic quail eggs. Nests were con- study (Table 1). Predation also varied between sidered predated if the quail egg was missing grassland types (F1,18 = 7.94, P = 0.011; Table or damaged or the nest destroyed (Dion et al. 1) with significantly higher rates of predation 2000). Clay eggs were used to determine preda- on tobosa grasslands. Grassland patches were tor type and not rates of predation (Davison divided into 4 open and 6 shrub-encroached and Bollinger 2000, Part and Wretenberg 2002). sites based on shrub counts within 3000-m2 To determine predator type when a quail transects; sites with low shrub encroachment egg was damaged or destroyed, we analyzed had 26–94 shrubs per transect (≤ 313 shrubs ⋅ the clay eggs. Marks left on clay eggs were ha–1) compared to 156–282 shrubs per transect compared to the dentition of native species, (520–940 shrubs ⋅ ha–1) at high encroached and these nest predators were divided into sites. A detectable difference was found in broad categories, including small mammals, nest predation between grassland patches larger mammals, avian, and snakes. Avian pred- with high and low shrub encroachment (F1,18 ators are typically thought to leave a single = 8.63 P = 0.009; Table 1), with significantly narrow hole in the egg or an obvious beak mark. higher predation on the high shrub-encroached A destroyed nest site or teeth and claw marks sites. A significant interaction was detected in the clay eggs are generally considered mam- between nest type and shrub encroachment malian predation. Snakes leave the nest site (F2,18 = 3.65, P = 0.047). No interactions were undisturbed or may create a hole in the nest detected between nest type and grassland bottom, removing the quail egg but leaving no type, shrub encroachment and grassland type, marks on clay eggs (Davison and Bollinger or among all 3 variables (P > 0.05). Rates of 2000, Dion et al. 2000, Pietz and Granfors predation did not differ among nests located 2000). We handled all nests, nest material, and in cholla, mesquite, and yucca shrubs (P > eggs using latex gloves, and our boots were 0.05; Table 2). Overall, predation was found to washed upon arrival at each study site. increase linearly with the number of shrubs We counted all shrubs along a 1000 × 3-m (R2= 0.47, df = 9, P = 0.028). transect in the center of each plot. These Determination of nest predators using per- shrub counts were used as a relative index of moplast eggs was difficult to confirm, and no shrub encroachment within each patch and strong quantitative determination could be were used to classify sites as relatively open or made. Avian predators appeared to be the most shrub encroached. common predator, followed by mammals and We tested whether predation rates differed possibly snakes. However, 28% of the permo- as a function of grassland type (black grama vs. plast eggs analyzed could not be grouped into tobosa), shrub encroachment (high vs. low), and a predator category. 2005] NEST PREDATION 199

TABLE 1. Rates of nest predation in relation to nest type, grassland type, and shrub encroachment in desert grasslands in southern New Mexico. O.C. ground and O.C. shrub represent open-cup ground and shrub nests, respectively. The number of nests for each nest type is presented in parentheses. Nest type Grassland type Shrub encroachment Predation rate O.C. ground (7) Black grama Low 0.14 O.C. ground (21) Black grama High 0.09 O.C. ground (21) Tobosa Low 0.24 O.C. ground (21) Tobosa High 0.14 O.C. shrub (7) Black grama Low 0.14 O.C. shrub (21) Black grama High 0.48 O.C. shrub (21) Tobosa Low 0.48 O.C. shrub (21) Tobosa High 1.00 Spherical shrub (7) Black grama Low 0.00 Spherical shrub (21) Black grama High 0.29 Spherical shrub (21) Tobosa Low 0.14 Spherical shrub (21) Tobosa High 0.86

TABLE 2. Rates of nest predation of artificial nests in shrub types among plots prevented a thorough southern New Mexico in relation to shrub type. Fourteen investigation of the interaction of shrub and nests are not included in this table because they were placed in other shrub types including creosote bush, tar- grassland type and the effect of patch size. bush, ephedra, and acacia spp. Contrary to our prediction, nests in shrubs were more vulnerable to predation than open- Nest substrate N Predation rate cup ground nests. This was particularly true Mesquite 61 0.58 for open-cup shrub nests, which appeared more Cholla 39 0.50 vulnerable to visual predators. Visual cues for Yucca 26 0.37 locating nests seemed important; most preda- Ground 70 0.14 tors leaving marks on permoplast eggs left marks consistent with avian predators. How- ever, recent studies using video cameras have concluded that identification of specific preda- DISCUSSION tors based on sign left at the nest can be misleading (Pietz and Granfors 2000, Thompson Predation rates did vary between the 2 grass- and Burhans 2003). Specifically, snakes will land types, with higher predation in tobosa- sometimes leave a hole in the bottom of the dominated grasslands. This is contrary to our nest, and contrary to common belief, large prediction and was likely related to several mammals will often leave the nest site undis- factors that could not be controlled in our site turbed (Pietz and Granfors 2000, Thompson selection. Although no differences were de- and Burhans 2003). Open-cup ground nests tected in rates of predation among shrub types, appeared to be better concealed and more dif- rates of predation were lower for yuccas com- ficult for predators to locate regardless of the pared with mesquite and cholla, and this shrub level of shrub encroachment. This agrees with type occurred almost exclusively in black grama Vander Haegen et al. (2000), who found a pos- grasslands. The predominance of cholla and itive relationship between patch size and pre- mesquite in tobosa grasslands and mesquite dation rates for shrub-nesting species such as and yucca in black grama grasslands may have Sage Thrashers and Brewer’s Sparrows but no contributed to a cumulative difference in pre- relationship for the ground-nesting Vesper dation rates among grassland types. Although Sparrow. However, Davison and Bollinger we attempted to control for grassland size, 2 of (2000) found no difference in predation rates our tobosa grassland patches were <50 ha (19 between ground and elevated nests in Conser- and 42), and all shrub nests within each of vation Reserve Program grasslands in Illinois. these 2 patches were destroyed by predators, Several studies (Major and Kendal 1996, Part suggesting patch size may influence predation and Wretenberg 2002) using artificial nests to rates within desert grasslands. However, the measure vulnerability of nest predation have limited number of plots and the distribution of cautioned that rates of predation differ between 200 WESTERN NORTH AMERICAN NATURALIST [Volume 65 real and artificial nests because they are per- Herbel 1965, Neilson 1986, Schlesinger et al. ceived differently by predators. Activity of 1990). Desertified sites may be easier for pred- adult birds at the nest site may attract preda- ators to search because of the clumped distri- tors (Roper and Goldstein 1997), or differen- bution of resource patches. The higher avian tial search modes among predator types such and mammalian diversity observed in deserti- as olfactory versus visual cues may result in dif- fied sites (Whitford 1997, Kerley and Whitford ferential rates of predation (Major and Kendal 2000, Pidgeon et al. 2001) may support a higher 1995, Martin 1993b). Relative rates of preda- abundance of predators as well as a spatially tion on artificial nests can, however, be com- clumped distribution of potential prey sources. pared among patch types and nest types and Predators may concentrate in desertified areas are useful for identifying vulnerability to pre- because they are easier to search and have a dation and potential predators (Sieving et al. higher density of prey including nesting birds. 1998, Dion et al. 2000). Davison and Bollinger To confirm these results, we recommend that (2000) found similar rates of predation between this experiment be repeated on natural nests real and artificial nests in grasslands in Illinois within open and shrub-encroached Chihua- when artificial nests more closely mimicked huan Desert grasslands. natural nests. In this study it appears that the combination of shrub encroachment and search ACKNOWLEDGMENTS behavior likely interacted to increase rates of nest predation. However, the significant inter- We are particularly grateful to the staff at action detected between shrub encroachment the Jornada LTER, including B. Nolan, E. and nest type and the positive association of Fredrickson, E. Garcia, and G. Yao for access predation with shrub density indicate that shrub and assistance in location of study plots. D. encroachment may be a major factor affecting Ginter and C. Turner assisted with data collec- predation on nests in this habitat. tion. This study was supported by funds from More traditional studies of fragmentation, the International Arid Lands Consortium, New with clearly defined edges, have demonstrated Mexico State University, and the National Sci- that forest or grassland fragmentation con- ence Foundation–funded ADVANCE Institu- tributes to increased rates of predation and tional Transformation Program at New Mexico brood parasitism (Flaspholer et al. 2001, Mano- State University, fund #NSF 0123690. This is lis et al. 2002). In this study the encroachment a contribution to the New Mexico State Uni- of shrubs into grassland patches is a form of versity, College of Agriculture and Home Eco- nomics, Agricultural Experiment Station. fragmentation, but the ecotone between the 2 habitat types is less clearly defined. The in- LITERATURE CITED creased presence of shrubs throughout grassland patches in the desert Southwest may act BROWN, D.E. 1982. Biotic communities of the American as a corridor for a diversity of species histori- Southwest—United States and Mexico. Desert Plants cally not associated with desert grasslands to 4:123–179. occupy or move through the patch. Other stud- BUFFINGTON, L.C., AND C.H. HERBEL. 1965. Vegetation changes in a semidesert grassland range from 1858– ies have reported higher abundance and diver- 1963. Ecological Monographs 35:139–164. sity of small mammals and birds in desertified DAVISON, W., AND E. BOLLINGER. 2000. Predation rates on sites (Whitford 1997, Pidgeon et al. 2001). 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Species-specific edge effects on nest success tribution of vegetative cover from a homoge- and breeding bird density in a forested landscape. Ecological Applications 11:32–46. neous distribution to a spatially clumped or FREDRICKSON, E., K.M. HAVSTAD, R. ESTELL, AND P. H YDER. heterogeneous distribution (Buffington and 1998. Perspectives on desertification: southwestern 2005] NEST PREDATION 201

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REPRODUCTIVE CHARACTERISTICS OF TWO SYNTOPIC LIZARD SPECIES, SCELOPORUS GADOVIAE AND SCELOPORUS JALAPAE (SQUAMATA: PHRYNOSOMATIDAE), FROM TEHUACÁN VALLEY, PUEBLA, MÉXICO

Aurelio Ramírez-Bautista1, América L. Ortíz-Cruz2, Ma. Del Coro Arizmendi2, and Jorge Campos2

ABSTRACT.—We studied the reproductive characteristics of 2 syntopic lizard species, Sceloporus gadoviae and Scelo- porus jalapae (Phrynosomatidae). Specimens of S. gadoviae (N = 105) and S. jalapae (N = 41) were collected in a tropical arid forest from Tehuacán Valley, Puebla, México. Males of S. gadoviae reached sexual maturity at the same snout- vent length (SVL; 45.0 mm) as S. jalapae, and a similar pattern occurred in females of both species (SVL; 41.0 and 42.0 mm, respectively). Males of S. gadoviae exhibited reproductive activity throughout the year, with a longer activity during the dry (November to May) and part of the wet season (June to September). In contrast, reproductive activity in S. jalapae males occurred during the wet season (July to September). Females of S. gadoviae showed continuous reproduction, whereas females of S. jalapae exhibited seasonal reproduction. Mean SVL of sexually mature females was higher – ± ± ± for S. gadoviae (x sx– = 50.4 0.52) than for S. jalapae (46.0 0.54, P < 0.0001). Mean clutch size for S. gadoviae was lower (3.9 ± 0.14 eggs) than for S. jalapae (5.6 ± 0.43). There was no significant correlation between snout-vent length of females and clutch size of S. gadoviae (r2 = 0.22, P > 0.05) or S. jalapae (r2 = 0.48, P > 0.05). Our study suggests that although both species inhabit the same environment, they have different reproductive characteristics.

Key words: Sceloporus gadoviae, Sceloporus jalapae, Mexico, reproductive cycle, clutch size, Reptilia, Sauria, Phrynosomatidae.

Descriptive studies have been conducted on ity has been associated with rainfall, tempera- squamate reproduction in many different envi- ture, and photoperiod (Marion 1982, Ramírez- ronments of Mexico, such as temperate high Bautista et al. 1998). elevation (Guillette 1982, Ramírez-Bautista et Variation in reproductive characteristics with- al. 1998, 2002), tropical rain forest (Benabib in and among populations also is associated 1994), and tropical dry forest (Ramírez-Bautista with seasonal and annual environmental fluc- and Vitt 1997, 1998, Lemos-Espinal et al. 1999), tuations (Ballinger 1977, Benabib 1994). Envi- but very few studies have been conducted in ronmental factors such as food availability, tropical arid habitats (Ramírez-Bautista 2003). precipitation, and temperature can affect growth These studies have provided data to allow con- rates, survivorship, clutch size, clutch frequency, textualization of the reproductive patterns in and age and size at maturity (Ballinger 1977, each environment. For example, reproduction Dunham 1982, Benabib 1994). During the of many lizard species from seasonal tropical past 2 decades, studies have shown that a por- and temperate environments is cyclical (Guil- tion of life history variation among species is lette 1982, Ramírez-Bautista and Vitt 1997, historical (Dunham and Miles 1985, Vitt 1992). 1998), with courtship, mating, and copulation That is, related species tend to be more simi- occurring at the onset of the rainy season lar in life history characteristics than unre- (Ramírez-Bautista and Vitt 1997). Egg produc- lated ones (Miles and Dunham 1992, Valdéz- tion and incubation usually occur at the onset González and Ramírez-Bautista 2002). For of the rainy season, with hatchlings emerging example, SVL at sexual maturity, clutch and at the end of the rainy season (Ramírez-Bau- egg size, and clutch frequency in the genus tista and Vitt 1998). Seasonal reproductive activ- Sceloporus are more similar within species

1Corresponding author: Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, A.P. 1-69 Plaza Juárez, C.P. 42001, Pachuca, Hidalgo, México. 2Unidad de Biología, Tecnología y Prototipos (UBIPRO), FES-Iztacala, Universidad Nacional Autónoma de México. Av. de los Barrios s/n, Los Reyes Izta- cala, Tlalnepantla, Estado de México C.P. 54090, A.P. 314, México City, México.

202 2005] REPRODUCTION IN TWO SYNTOPIC LIZARDS 203 groups (scalaris, spinosus, torquatus) than be- phytic brushland, deciduous tropical forest, tween them (Valdéz-González and Ramírez- and columnar cacti (Dávila et al. 1993). Bautista 2002). However, many of the data used We collected data for S. gadoviae (72 females in these conclusions were based on lizard and 33 males) and S. jalapae (24 females and species of small and medium size from the wet 17 males) from January to December, except tropics and temperate regions (Guillette 1982, March and April (for S. gadoviae) and January, Benabib 1994, Ramírez-Bautista et al. 2002). April, June, October, and December (for S. At present, few studies exist on reproductive jalapae) during the period 1999–2002. Because patterns from tropical arid lizards (Ramírez- samples were often small for individual months Bautista 2003). Thus, one might suspect that and varied considerably among years, we pooled the often extreme seasonality of temperate the data to describe general annual reproduc- regions could result in reproductive cycles tive characteristics. We measured snout-vent and patterns different from those that might length (SVL) of the lizards to the nearest 1.0 be observed in tropical arid environments mm, after which they were sacrificed and fixed (Tinkle et al. 1970). with 10% formalin and subjected to gonadal Although the life histories of several species examination. of Sceloporus have been intensively studied During the gonadal examination of females, (Benabib 1994, Valdéz-González and Ramírez- we counted the number of vitellogenic folli- Bautista 2002), little has been published on cles or oviductal eggs and recorded the length reproductive characteristics of the Mexican and width of left and right vitellogenic follicles endemic species Sceloporus gadoviae and S. or freshly ovulated eggs to the nearest 0.1 jalapae from Tehuacán Valley, Puebla, México mm. Length and width of the gonads were (Ramírez-Bautista 2003). Sceloporus gadoviae used to obtain follicular and egg volume (V) belongs to the gadoviae group, and S. jalapae using the formula for volume of an ellipsoid to the jalapae group (Wiens and Reeder 1997). (Selby 1965): In this study we focused on male and female reproductive characteristics of the small-sized V = 4/3πa2b, lizard species S. gadoviae and S. jalapae. We addressed the following questions: (1) Do where a is half the shortest diameter and b is males and females become sexually mature at half the longest diameter. The smallest female the same size? (2) Do males and females differ (considering SVL) with either the largest vitel- in morphological traits? (3) What is the annual logenic follicles or oviductal eggs was used to reproductive cycle for these species? (4) How estimate minimum size at maturity. Clutch size large are their clutches? (5) Is clutch size was determined by counting eggs in the oviduct related to female size? (6) Are reproductive or vitellogenic follicles of adult females during characteristics of both species similar to other the reproductive season (Ramírez-Bautista et al. populations and other spiny lizards of similar 2000, 2002). We calculated a Pearson’s product- body size? This study adds to a growing body moment correlation coefficient to test for a of data for groups of species that have been relationship between clutch size and SVL of relatively underrepresented in large compara- females. tive studies. Males were recorded as sexually mature if they contained enlarged testes and convoluted MATERIALS AND METHODS epidymides typically associated with sperm production (Goldberg and Lowe 1966). Data This study was conducted at Tehuacán on lizard SVL and organ volume were trans- Valley, Puebla, near Zapotitlán Salinas, México formed to log (base 10) for linearized regres- (18°07′18″N, 97°39′06″W) at an elevation of sions. Because organ volume usually varies 1420 m. The climate is dry and temperate, with SVL, we first calculated regressions of with most precipitation occurring during the log10-transformed organ volume data against summer months (June–September); the dry log10 of female SVL. For regressions that were season is from November to May. Mean annual significant (indicating a body size effect), we temperature is 21°C (range 17°–24°C), and calculated residuals from the relationship of precipitation is 450 mm (García 1981). Domi- organ volume to SVL (all variables log10-trans- nant vegetation consists of thorn forest, xero- formed) to produce SVL-adjusted variables. 204 WESTERN NORTH AMERICAN NATURALIST [Volume 65

We used these residuals to describe the organ Male Reproductive Cycle volume and reproductive cycles (for S. gado- There were significant positive relationships viae). This technique maintains variation be- between male log10 SVL and log10 testes vol- cause of extrinsic factors while minimizing the 2 ume (r = 0.65, F1,31 = 55.7, P < 0.0001, N = confounding effect of individual variation in 2 33), log10 fat body mass (r = 0.13, F1,31 = SVL (Valdéz-González and Ramírez-Bautista 2 4.32, P < 0.05), and log10 liver mass (r = 2002). We performed 1-way ANOVA on the 0.29, P < 0.001) in S. gadoviae. In contrast, in organ volumes (with month as the factor) to S. jalapae there were no relationships between determine whether significant monthly varia- male log10 SVL and log10 testes volume (F1,15 tion existed, including only those months for = 0.125, P > 0.05) or log10 fat body mass which N ≥ 3 (Ramírez-Bautista et al. 2000). (F1,12 = 0.462, P > 0.05), but there was a sig- Variables used to test sexual size differences nificant positive relationship between male were snout-vent length (SVL, mm), head length log10 SVL and log10 liver mass (F1,11 = 36.53, P (HL, mm), forearm length (FL, mm), and tibia < 0.0001). ANOVAs on the residuals of these length (TL, mm) of females and males. Resid- regressions revealed significant variation among uals of SVL regressions were calculated for months in testes volume (F9,23 = 2.35, P < these morphological variables. We then used 0.05), but not in fat body mass (F9,23 = 0.759, these residuals to examine sexual size differ- P > 0.05) or liver mass (F9,18 = 0.655, P > ences between mature males and females, and 0.05) for S. gadoviae (Fig. 1). For S. jalapae, performed a Mann-Whitney U-test on HL, variation was not significant among months for FL, and TL. We used a cutoff of P < 0.05 to testes volume (F3,13 = 2.55, P > 0.05), fat assess statistical significance. Results are body mass (F1,13 = 1.55, P > 0.05), or liver ± expressed as untransformed mean sx–. Statis- mass (F3,9 = 1.78, P > 0.05). In S. gadoviae, tical analyses were performed with StatView testicular volume increased from January IV (Abacus Concepts 1992). Specimens are de- through July and again in October, November, posited at the Colección Nacional de Anfibios and December (Fig. 1). In contrast, testicular – y Reptiles (CNAR), Universidad Nacional volume in S. jalapae increased in July (x = – Autónoma de México in México City. 14.0 ± 4.4 mm3), August (x = 20.6 ± 4.3 mm3), and September (x– = 34.2 ± 11.5 mm3). RESULTS Female Reproductive Body Size and Cycle Sexual Maturity There was a significant linear relationship between female log10 SVL and log10 gonadal In S. gadoviae sexually mature males ranged 2 volume (r = 0.21, F1,69 = 16.0, P < 0.0005), in size from 45.0 to 73.0 mm SVL, and females 2 log10 fat body mass (r = 0.11, F1,69 = 5.69, P ranged from 41.0 to 67.0 mm SVL, whereas 2 < 0.005), and log10 liver mass (r = 0.23, F1,67 the range in S. jalapae was 45.0–62.0 mm SVL = 3.75, P < 0.05) in S. gadoviae, but not in S. and 42.0–50.0 mm SVL, respectively (Table 1). jalapae (r2 = 0.07, r2 = 0.13, r2 = 0.06, all P Males of both S. gadoviae (Z = –4.75, P < > 0.05, respectively). ANOVAs on residuals of 0.0001) and S. jalapae (Mann-Whitney U test, these regressions revealed significant variation Z = –2.70, P = 0.001) were larger in SVL than among months on gonadal volume (F10,60 = females (Table 2). Mean SVL of females was 4.32, P < 0.0001), fat body mass (F10,60 = 8.81, higher in S. gadoviae than in S. jalapae females P < 0.0001), and liver mass (F10,58 = 2.55, P < (Z = –4.89, P < 0.0001), and the males exhib- 0.05) in S. gadoviae (Fig. 2). In contrast, in S. ited a similar pattern (Z = –3.84, P < 0.0001). jalapae only gonad volume varied significantly Males of S. gadoviae also had larger HL (Z = among months (F6,15 = 3.25, P < 0.05). –5.25, P < 0.0001), FL (Z = – 4.85, P < 0.0001), Sceloporus gadoviae females have continu- and TL (Z = –4.19, P < 0.0001) than females ous reproduction. The average female gonadal (Table 2), and the same pattern was observed volume began to increase in October and con- in S. jalapae for HL (Z = – 4.38, P < 0.0001), tinued until July of the following year; volume FL (Z = –4.16, P < 0.0001), and TL (Z = then decreased from July to October (Fig. 2). –4.49, P < 0.0001). In contrast, reproductive activity in S. jalapae 2005] REPRODUCTION IN TWO SYNTOPIC LIZARDS 205

± TABLE 1. Reproductive characteristics of Sceloporus gadoviae and S. jalapae from Tehuacán Valley. Mean sx– (range, sample size). Characteristics S. gadoviae S. jalapae Maximum reproductive activity of males November–July July–September Maximum reproductive activity of females January–December May–September Vitellogenic follicles 3.9 ± 0.19 (2–5, N = 14) 3.2 ± 0.49 (2–4, N = 5) Oviductal eggs 3.9 ± 0.14 (2–5, N = 21) 5.6 ± 0.43 (4–8, N = 10) Oviductal egg volume (mm3) 263.9 ± 17.0 (170.4–501.6, N = 20) 172.4 ± 10.7 (120.1–198.7, N = 9) Vitellogenic follicles (mm3) 56.0 ± 12.1 (3.2–142.6, N = 17) 17.4 ± 9.3 (3.9–40.6, N = 4) Neonates SVL (mm) 25.0 23.0 Adult male SVL (mm) 57.5 ± 1.3 (45.0–73.0, N = 33) 49.3 ± 1.1 (45.0–62.0, N = 17) Adult female SVL (mm) 50.4 ± 0.52 (41.0–67.0, N = 72) 46.0 ± 0.54 (42.0–50.0, N = 24)

± TABLE 2. Mean values ( 1 sx–) of morphological characteristics (HL = head length, FL = femur length, and TL = tibia length) of sexually mature females (N = 72) and males (N = 33) of Sceloporus gadoviae and S. jalapae (N = 24 and 17, respectively). We used the Mann-Whitney U test (P < 0.001 = *, P < 0.0001 = **) in determining differences between the sexes for each species.

______S. gadoviae ______S. jalapae Characteristics Males Females Test P Males Females Test P HL (mm) 13.5 ± 0.24 12.0 ± 0.08 Z = –5.25 ** 11.3 ± 0.14 9.8 ± 0.09 Z = –4.38 ** FL (mm) 14.4 ± 0.27 13.1 ± 0.15 Z = –4.85 ** 12.2 ± 0.15 10.2 ± 0.10 Z = –4.16 ** TL (mm) 12.9 ± 0.36 10.7 ± 0.09 Z = –4.91 ** 10.8 ± 0.17 9.0 ± 0.14 Z = –4.49 ** SVL (mm) 57.5 ± 1.3 50.4 ± 0.52 Z = –4.75 ** 49.3 ± 1.1 46.0 ± 0.54 Z = –2.70 *

seems to be seasonal; gonadal volume increased females was significantly correlated with female – ± 3 – ± 2 in May (x = 24.2 2.3 mm ), July (x = 92.5 SVL in S. gadoviae (r = 0.69, F1,19 = 17.1, P 3 – 3 2 53.5 mm ), August (x = 157.0 ± 15.8 mm ), < 0.001) and S. jalapae (r = 0.72, F1,9 = 8.81, and September (x– = 109.6 ± 52.1 mm3) in P < 0.01). Three of 21 S. gadoviae females females with vitellogenic follicles or oviductal (14.3%) had both vitellogenic follicles and ovi- eggs. Females of S. gadoviae were found with ductal eggs at the same time, suggesting that oviductal eggs from January to December, but females of this species might lay 2 or more with a maximum egg production from May to clutches during the reproductive season, but September. In contrast, females of S. jalapae this was not the case with females of S. jalapae. were found with vitellogenic follicles and ovi- Egg production for S. gadoviae occurred throughout the year, but the peak was from ductal eggs from March to September. May to September, while the peak for S. jala- Clutch Size pae was from July to September. The volume of vitellogenic follicles of S. Mean clutch size of vitellogenic follicles of gadoviae was different from that of oviductal S. gadoviae was not different from that of eggs (Z = –5.18, P < 0.0001); a similar pattern oviductal eggs (Z = –1.42, P > 0.05; Table 1). was observed for S. jalapae (Z = –2.78, P < Considering both egg classes, mean clutch 0.005; Table 1). size was 3.9 ± 0.11 eggs (range 2–5, N = 35; Table 1). In contrast, in S. jalapae females the DISCUSSION mean clutch size of vitellogenic follicles was different from that of oviductal eggs (Z = –2.69, Sceloporus gadoviae and S. jalapae males P = 0.005; Table 1). Clutch size was higher in reached sexual maturity at the same size, and S. jalapae than in S. gadoviae (Z = –3.35, P < both species showed sexual dimorphism, where- 0.005). Clutch size was not related to female by males were large than females. This is com- 2 SVL in S. gadoviae (r = 0.22, F1,33 = 1.67, P mon among other species of the genus Scelo- 2 > 0.05) nor in S. jalapae (r = 0.48, F1,4 = porus (Fitch 1978, Benabib 1994, Ramírez- 0.90, P > 0.05). However, total egg mass in Bautista and Gutiérrez-Mayén 2003). Males of 206 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Fig. 2. Female gonad, fat body, and liver mass cycles of Sceloporus gadoviae from Tehuacán Valley, Puebla, Méx- Fig. 1. Male testes, fat body, and liver cycles of Scelo- ± ico. Data are mean ( 1 sx–) residuals from a regression of porus gadoviae from Tehuacán Valley, Puebla, México. log gonadal volume (mm3), fat body mass (g), liver mass ± 10 Data are mean ( 1 sx–) residuals from a regression of log10 (g) against log SVL. testes volume (mm3), liver mass (g), fat body mass (g) 10 against log10 SVL. son (July–August), larger males of both species both species were larger in other morphologi- were observed on cactus (S. jalapae) and on cal structures (HL, FL, TL). Sexual dimorphism rocks (S. gadoviae), exhibiting their bright ven- in S. gadoviae and S. jalapae, as in other spe- tral region to smaller males and driving the cies of the genus, may be a response of sexual smaller individuals from their areas as occurs in selection, with larger males having an advantage other lizard species (Trivers 1976, Ruby 1981). over smaller ones in obtaining mates (Fitch The reproductive cycles of S. gadoviae and 1981, Stamps 1983, Shine 1989). Sexual selec- S. jalapae differ in timing and duration. The tion can help maintain large body size in male male reproductive period of S. gadoviae was lizards if larger males mate more frequently during the dry (November to May) and wet than smaller ones. During the reproductive sea- (June to September) seasons. In contrast, males 2005] REPRODUCTION IN TWO SYNTOPIC LIZARDS 207 of S. jalapae showed a seasonal reproductive could result from a demographic response that period during the wet season (July to Septem- may influence clutch size and egg size or vol- ber). These data suggest that both species have ume as in other species (Dunham 1982, Bena- different reproductive requirements, even bib 1994, Ramírez-Bautista and Vitt 1997, 1998) though they inhabit the same area. Sceloporus and congeners (Ramírez-Bautista et al. 2002, jalapae seems to be responding to the envi- Valdéz-González and Ramírez-Bautista 2002). ronmental factors of the wet season as shown The smaller clutch size and the larger egg by other species inhabiting tropical dry forest volume for S. gadoviae compared with S. jala- (Ramírez-Bautista and Vitt 1997, 1998). Male pae might be considered a reproductive strat- and female reproductive cycles in S. jalapae egy because production of several clutches of appear to be synchronized because females small size might subject offspring to excessive showed vitellogenic follicles and oviductal eggs predation. The larger egg volume in S. gado- from May to September; this pattern is similar viae results in hatchlings with a larger SVL to other oviparous lizard species inhabiting (25.0 mm) than the smaller egg volume clutches arid environments (Jones and Ballinger 1987, of S. jalapae (SVL = 23.0 mm). These data Smith et al. 1995). show that S. gadoviae females have smaller Reproductive cycles for both sexes of S. clutch sizes, laying 2 or more clutches during gadoviae are synchronized from January to the reproductive season, but the hatchlings December. In S. gadoviae the longer repro- are larger in SVL than hatchlings of S. jalapae ductive season, larger clutch size, larger ovi- females from a single egg clutch. This pattern ductal egg volume, and smaller mean SVL of is similar to other small-bodied species with sexually mature adult females than other popu- multiple egg clutches (Benabib 1994, Ramírez- lations of the same species could be influenced Bautista and Vitt 1998). by contrasting conditions of precipitation (450 Although both species belong to the Phry- vs. 730 mm), altitude (1420 vs. 600 m), and nosomatidae family, if the difference in clutch temperature (21°C vs. 27.8°C) in the Tehuacán size between the 2 species does not reflect Valley and Cañón del Zopilote (Lemos-Espinal their phylogeny, it might be a response to dif- et al. 1999). Another difference associated with ferent environmental pressure. Most small- the longer reproductive season is that individ- bodied species of this family have multiple ual females may lay 2 or more clutches rather egg clutches of small size. However, exceptions than a single clutch as occurs in other small- exist such as in S. siniferus (5.0 eggs; Fitch bodied species (Ramírez-Bautista et al. 1995). 1978), S. pyrocephalus (5.8 eggs; Ramírez- Differences in the reproductive character- Bautista and Oliver-Becerril 2004), and S. istics between S. gadoviae and S. jalapae, such jalapae (5.6 eggs; this study) with a single egg as reproductive period, snout-vent length of clutch. Although clutch sizes differ between adults, mean number of vitellogenic follicles, both species, S. jalapae is closer to species of clutch size, and oviductal egg volume, suggest smaller clutch size than to other large-bodied that each species is responding in a different species (Valdéz-González and Ramírez-Bautista way to environmental cues. Differences in re- 2002). The variation among populations of the productive characteristics between both species same or different species of this family (Phry- could reflect their phylogenetic distance (dif- nosomatidae) could reflect either adaptive different groups) and the microhabitat used by ferences that evolved as a result of different each species (Miles and Dunham 1992). Re- environments or proximate effects of different sources such as food abundance are strongly environments (Dunham and Miles 1985, Vitt correlated with precipitation in several envi- 1990, 1992). ronments, and variation in resource abundance Females of S. gadoviae are able to lay 2 or in turn is related to variations in reproductive more clutches during the reproductive season. characteristics in many lizard species (Ballinger Like most small-bodied species, some S. gado- 1977, Benabib 1994, Ramírez-Bautista and Vitt viae females (14.3%) are capable of laying 2 or 1997, 1998). This could be the case for the more clutches during reproduction, since populations of S. gadoviae because both females vitellogenic follicles and oviductal eggs were and males are larger at sexual maturity (mean present at the same time. This pattern is simi- SVL) than S. jalapae of either sex. The varia- lar to other oviparous species of small body tion in body size of females of both species size found in tropical dry forest, tropical wet 208 WESTERN NORTH AMERICAN NATURALIST [Volume 65 forest, and temperate zones (Dunham 1982, grafía, Universidad Nacional Autónoma de México, Benabib 1994, Ramírez-Bautista et al. 1995, México City. GOLDBERG, S.R., AND C.H. LOWE. 1966. The reproductive Ramírez-Bautista and Vitt 1998). cycle of the western whiptail lizard (Cnemidophorus Much remains to be learned about the re- tigris) in southern Arizona. Journal of Morphology productive cycles of the lizards Sceloporus 118:543–548. gadoviae and S. jalapae, especially those in- GUILLETTE, L.J., JR. 1982. The evolution of viviparity and placentation in the high elevation, Mexican lizard habiting tropical arid environments. It is clear Sceloporus aeneus. Herpetologica 38:94–103. that S. gadoviae has multiple clutches during JONES, S.M., AND R.E. BALLINGER. 1987. Comparative life the reproductive season, but data do not exist histories of Holbrookia maculata and Sceloporus undu- about clutch frequency for the small-bodied latus in western Nebraska. Ecology 68:1828–1838. lizard S. jalapae. Our data in this present study LEMOS-ESPINAL, J.A., G.R. SMITH, AND R.E. BALLINGER. 1999. Reproduction in Gadow’s spiny lizard, Scelo- suggest that further research in other regions porus gadoviae (Phrynosomatidae), from arid tropical of the geographic range of both species is nec- México. Southwestern Naturalist 44:57–63. essary to provide additional information about MARION, K.R. 1982. Reproductive cues for gonadal devel- variations in their reproductive characteristics. opment in temperate reptiles: temperature and photoperiod effects on the testicular cycle of the lizard Sceloporus undulates. Herpetologica 38:26–39. ACKNOWLEDGMENTS MILES, D.B., AND A.E. DUNHAM. 1992. Comparative analyses of phylogenetic effects in the life-history patterns We thank V. Mata-Silva and L. Oliver for of iguanid reptiles. American Naturalist 139:848–869. their assistance in the field, A. Valiente for RAMÍREZ-BAUTISTA, A. 2003. Some reproductive characteristics of a tropical arid lizard assemblage from permitting us to use his home while we gath- Zapotitlán Salinas, Puebla, México. Herpetological ered data in the field, R. León-Rico for logistic Review 34:328–331. help, D. Gernandt for reading the initial ver- RAMÍREZ-BAUTISTA, A., AND G. GUTIÉRREZ-MAYÉN. 2003. sion of this manuscript, and the anonymous re- Reproductive ecology of Sceloporus utiformis (Sauria: Phrynosomatidae) from a tropical dry forest of Méx- viewers for critical comments and suggestions ico. Journal of Herpetology 37:1–10. on the manuscript. This study was supported RAMÍREZ-BAUTISTA, A., AND V. O LIVER-BECERRIL. 2004. by PAPCA 1, PROMEP and UAEHGO-PTC- Reproduction in the boulder spiny lizard, Sceloporus 165 projects. pyrocephalus (Sauria: Phrynosomatidae), from a tropical dry forest of México. Journal of Herpetology 38:225–231. LITERATURE CITED RAMÍREZ-BAUTISTA, A., AND L.J. VITT. 1997. Reproduction in the lizard Anolis nebulosus (Polychrotidae) from ABACUS CONCEPTS. 1992. Statview IV. Abacus Concepts, the Pacific coast of México. Herpetologica 53:423–431. Inc., Berkeley, CA. ______. 1998. Reproductive biology of Urosaurus bicari- BALLINGER, R.E. 1977. Reproductive strategies: food avail- natus (Sauria: Phrynosomatidae) from a tropical dry ability as a source of proximal variation in a lizard. forest of México. Southwestern Naturalist 43:381–390. Ecology 58:628–635. RAMÍREZ-BAUTISTA, A., C. BALDERAS-VALDIVIA, AND L.J. BENABIB, M. 1994. Reproduction and lipid utilization of VITT. 2000. Reproductive ecology of the whiptail tropical populations of Sceloporus variabilis. Herpe- lizard Cnemidophorus lineatissimus (Squamata: Tei- tological Monographs 8:160–180. idae) in a tropical dry forest. Copeia 2000:712–722. DÁVILA, P., J.L. VILLASEÑOR, R. MEDINA, A. RAMÍREZ, A. RAMÍREZ-BAUTISTA, A., J. BARBA-TORRES, AND L.J. VITT. SALINAS, J. SÁNCHEZ-KEN, AND P. T ENORIO. 1993. List- 1998. Reproductive cycle and brood size of Eumeces ados florísticos de México X. Flora del Valle de Tehua- lynxe from Pinal de Amoles, Queretaro, México. cán-Cuicatlán. Instituto de Biología, Universidad Journal of Herpetology 32:18–24. Nacional Autónoma de México, México City. 195 pp. RAMÍREZ-BAUTISTA, A., O. RAMOS-FLORES, AND J.W. SITES, DUNHAM, A.E. 1982. Demographic and life-history varia- JR. 2002. Reproductive cycle of the spiny lizard tion among populations of the iguanid lizard Uro- Sceloporus jarrovii (Sauria: Phrynosomatidae) from saurus ornatus: implications for the study of life-his- north-central México. Journal of Herpetology 36: tory phenomena in lizards. Herpetologica 38:208–221. 225–233. DUNHAM, A.E., AND D.B. MILES. 1985. Patterns of covari- RAMÍREZ-BAUTISTA, A., Z. URIBE-PEÑA, AND L.J. GUIL- ations in life history traits of squamate reptiles: the LETTE, JR. 1995. Reproductive biology of the lizard effects of size and phylogeny reconsidered. Ameri- Urosaurus bicarinatus bicarinatus (Reptilia: Phryno- can Naturalist 126:231–257. somatidae) from Río Balsas Basin, México. Herpeto- FITCH, H.S. 1978. Sexual size difference in the genus logica 51: 24–33. Sceloporus. University of Kansas Sciences Bulletin RUBY, D.E. 1981. Phenotypic correlates of male reproduc- 51:441–461. tive success in the lizard, Sceloporus jarrovi. Pages ______. 1981. Sexual size differences in reptiles. University 96–107 in R.D. Alexander and D.W. Tinkle, editors, of Kansas Museum Natural History Miscellaneous Natural selection and social behavior. Chiron Press, Publication 70:1–72. New York. GARCÍA, E. 1981. Modificaciones al sistema de clasificación SELBY, S.M. 1965. Standard math tables. 14th edition. climática de Köppen. 3rd edition. Instituto de Geo- Chemical Rubber Co., Cleveland, OH. 2005] REPRODUCTION IN TWO SYNTOPIC LIZARDS 209

SHINE, R. 1989. Ecological causes for the evolution of sex- Sceloporus horridus and Sceloporus spinosus (Squa- ual dimorphism: a review of the evidence. Quarterly mata: Phrynosomatidae), from México. Journal of Review of Biology 64:419–461. Herpetology 36:36–43. SMITH, G.R., R.E. BALLINGER, AND B.R. ROSE. 1995. Repro- VITT, L.J. 1990. The influence of foraging mode and phy- duction in Sceloporus virgatus from the Chiricahua logeny on seasonality of tropical lizard reproduction. Mountains of southeastern Arizona with emphasis Papéis Avulsos Zoologia (São Paulo) 37:107–123. on annual variation. Herpetologica 51:342–349. ______. 1992. Diversity of reproduction strategies among STAMPS, J.A. 1983. Sexual selection, sexual dimorphism, Brazilian lizards and snakes: the significance of line- and territoriality. Pages 169–204 in R.B. Huey, E.R. age and adaptation. Pages 135–149 in W.C. Hamlett, Pianka, and T.W. Schoener, editors, Lizard ecology: editor, Reproductive biology of South American ver- studies of a model organism. Harvard University tebrates. Springer-Verlag, New York. Press, Cambridge, MA. WIENS, J.J., AND T.W. R EEDER. 1997. Phylogeny of the TINKLE, D.W., H.M. WILBUR, AND S. TILLEY. 1970. Evolu- spiny lizards (Sceloporus) based on molecular and tionary strategies in lizard reproduction. Evolution morphological evidence. Herpetological Monographs 24:55–74. 11:1–101. TRIVERS, R.L. 1976. Sexual selection and resource accruing abilities in Anolis garmani. Evolution 30:253–269. Received 17 May 2004 VALDÉZ-GONZÁLEZ, M.A., AND A. RAMÍREZ-BAUTISTA. 2002. Accepted 3 November 2004 Reproductive characteristics of the spiny lizards, Western North American Naturalist 65(2), © 2005, pp. 210–214

FLEAS ASSOCIATED WITH THE NORTHERN POCKET GOPHER (THOMOMYS TALPOIDES) IN ELBERT COUNTY, COLORADO

Helen K. Pigage1, Jon C. Pigage2, and James F. Tillman2

ABSTRACT.—We collected 532 fleas, 526 of which were Foxella ignota ignota, from 247 northern pocket gophers, Thomomys talpoides, in Elbert County, Colorado, over 13 months. Other fleas included 1 Hystrichopsylla dippiei ssp., 3 Spicata rara, 1 Oropsylla idahoensis, and 1 female flea tentatively identified as Oropsylla (Opisocrostis)sp. These are new records for H. dippiei ssp. and S. rara in Elbert County. Fleas were cleared using standard methods and were placed on microscope slides in Canada balsam. The number of fleas per host ranged from 0 to 26. The highest median number of fleas per host (n = 5) was in May with a low median (n = 0) in August. Mean intensity and relative density of fleas peaked in April and May, respectively. Total flea abundance peaked from April through July. Approximately 72% of the male gophers (N = 99) were infested with fleas, whereas 57% of the females (N = 148) had fleas. Flea abundance on male gophers did not decrease nor did flea abundance on females increase as would be expected if flea breeding were influenced by hormones of the host. We suggest further randomized studies of fleas on T. talpoides to investigate parasite abundance throughout the year.

Key words: Siphonaptera, northern pocket gopher, Foxella ignota, Spicata rara, Hystrichopsylla dippiei, Oropsylla idahoensis, flea abundance.

It is widely accepted that members of the G. bursarius; westward through Montana, Wyo- flea genus Foxella Wagner, 1929 are true para- ming, and Colorado to Oregon and into Cali- sites of pocket gophers. Miller and Ward (1960) fornia, where they are found on T. bottae; and found all 4 species of Colorado pocket gophers north into Canada from Manitoba to British (Pappogeomys castanops Baird, 1852; Geomys Columbia and south into Arizona, New Mexico, bursarius Shaw, 1800; Thomomys bottae Eydoux Texas, and Mexico (R.E. Lewis personal com- and Gervais, 1836; and T. talpoides Richard- munication). According to Lewis, fleas within son, 1828) infested with Foxella ignota Baker, the complex increase in size from east to west 1895. They performed their survey during and from north to south. Holland (1985) lists 12 August 1957 in the southeastern part of Col- other species from T. talpoides, but these are orado, where the northern pocket gopher (T. typically found on ecological associates such talpoides) was the most abundant host. In an as woodrats, ground squirrels, mice, and voles. earlier study the same species of flea was re- Northern pocket gophers have an extensive covered from northern pocket gophers in Park range in North America similar to, but some- County (Eads 1949). These and other reports what smaller than, that of the genus Foxella. of F. ignota from the Rocky Mountains area The range of northern pocket gophers extends have not often indicated a subspecies designa- westward from the Dakotas and Nebraska to tion because of considerable morphological include Colorado, Wyoming, Montana, Idaho, variation (Hubbard 1947). and northward into the southern portion of the Several flea genera have been reported Canadian provinces from Manitoba to British from T. talpoides throughout its range. These Columbia. In the western United States, this include Foxella Wagner, 1929; Dactylopsylla rodent occurs east of the Cascades in Wash- Jordan, 1929; and Spicata I. Fox, 1940 (Lewis ington and Oregon but has a more limited dis- 2003). These genera can also occur on the tribution in northern California, Utah, Nevada, other 3 pocket gopher species in Colorado (G. New Mexico, and Arizona (Baker et al. 2003). bursarius, T. bottae, and P. castanops). The F. Longanecker and Burroughs (1952) studied ignota complex ranges from Indiana (Lake and the relationship between temperature, humidity, Newton Counties), where they are found on and flea abundance in burrows of the California

1HQ USAFA/DFB, Biology Department, 2355 Faculty Drive, Suite 2P389, United States Air Force Academy, CO 80840. 2Biology Department, University of Colorado, Colorado Springs, 1420 Austin Bluffs Parkway, Colorado Springs, CO 80918.

210 2005] FLEAS OF NORTHERN POCKET GOPHERS 211 ground squirrel, Spermophilus beecheyi Richard- scopically for identity and sex. Flea abundance son, 1829. They also found that numbers of was compared using descriptive statistical Hoplopsyllus anomalus Baker, 1904 varied dur- methods for differences based on time of year ing the year, with a marked increase in abun- as well as host sex. dance during the warmer months. Reichardt and Galloway (1994) studied the incidence and RESULTS prevalence of Oropsylla bruneri Baker, 1895 on S. franklinii Sabine, 1822 in Manitoba, with A total of 532 fleas were collected from 247 emphasis on the reproductive status of the T. talpoides. Of these fleas, 526 were identi- female fleas and their nondependence on the fied as F. i. ignota (269 males, 257 females), host’s hormones for timing of reproduction. 2 males and 1 female as S. rara I. Fox, 1940, They found that the proportion of female fleas 1 female as H. dippiei ssp., 1 male as O. idaho- on S. franklinii exceeded male fleas during some ensis Baker, 1904, and 1 female as Oropsylla months. Lang (1996) investigated the effect of (Opisocrostis) sp. biotic and abiotic factors on abundance of Numbers of fleas per host ranged from 0 to Oropsylla montana Baker, 1895 and H. anomalus 26, and median numbers are shown in Table 1. on S. beecheyi, and of Orchopeas sexdentatus Throughout the study the median flea infesta- Baker, 1904 on woodrats in southern Califor- tion rate remained between 0 and 2 except in nia. He found an increased abundance of O. May when it rose to 5. Mean intensity (total montana and O. sexdentatus correlated with number of fleas divided by the number of hosts decreased ambient temperature in autumn with fleas) and relative density (total number and early winter. Hoplopsyllus anomalus abun- of fleas divided by the number of hosts exam- dance, however, increased with the warmer ined) of fleas per host are also shown in Table temperatures of summer. None of the 3 species 1. While median number of fleas per host of fleas appeared hormonally synchronized peaked in May, mean intensity of fleas peaked with the breeding cycle of their hosts. Similar in April and declined slightly in May. Relative studies have not been reported regarding flea density, however, mirrored the peak of the abundance on T. talpoides. We hypothesized median in May. All 3 values dropped slightly that the number of fleas infesting this host in June and then rose slightly in July. Male might vary over the course of a calendar year pocket gophers constituted 40% of those col- because of the activity and abundance of hosts, lected; 71.7% of them had fleas, while 56.8% as well as seasonal changes in temperature of the females were infested. In all, 62.8% of and humidity. In this study we examined flea the animals had ≥1 fleas. The ratio of male to abundance on hosts but did not investigate female fleas on hosts varied by month and by abiotic factors. sex of the host animal. Except during Decem- ber, February, and July, a higher percentage of MATERIALS AND METHODS male pocket gophers had fleas than did females (Table 2). The ratio of male to female fleas for We collected 247 T. talpoides (99 males, the duration of the study was 1.05, but the ratio 148 females) in the Kiowa Creek valley, Elbert showed considerable variation by month and County, Colorado. Pocket gophers were col- by sex of the host. lected in both irrigated and nonirrigated alfalfa fields. Animals were trapped for 13 months DISCUSSION using Death-Klutch-1 (DK-1) traps (October Flea Species 2002–October 2003). Animals were placed in Ziploc® plastic bags and were stored frozen. The most abundant flea collected was F. i . When later thawed, they were brushed for ignota (526/532). This subspecies is the only fleas over a white enamel pan. Those collected member of the genus found in central Colo- were placed in 70% ethanol for short-term rado east of the Rocky Mountains, and it is the storage and later cleared in 10% KOH, neu- dominant flea on all 4 species of pocket gophers tralized, dehydrated in ethanol and then in in Colorado. Miller and Ward (1960) did not xylene, and finally mounted on slides using designate which subspecies of F. ignota or of T. Canada balsam. Fleas were examined micro- talpoides they collected. We assume that it 212 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 1. Median number, range, mean intensity (total number of fleas/number of hosts with fleas), and relative densities (total number of fleas/number of hosts examined) of fleas on all Thomomys talpoides (2002–2003), Elbert Co., Col- orado, by month. Median numbers Range of Mean Relative Month of fleas flea numbers intensity density October 1 0–5 1.75 1.08 November 1 0–6 3.2 1.52 December 0.5 0–2 1.4 0.7 January 1 0–4 1.69 1.1 February 1 0–8 2.73 2.05 March 1 0–5 1.86 1.18 April 0.5 0–23 7.25 3.63 May 5 0–16 6 5.57 June 1 0–17 3.25 2.83 July 2 0–15 5.15 3.05 August 0 0–9 2.54 1.14 September 1 0–11 3.43 2.09 October 1 0–26 4 3.33

was F. i. ignota from T. talpoides populations if H. dippiei ssp. can occur on ecological associ- they trapped on the eastern side of the Front ates that use pocket gopher burrows. Range. Oropsylla idahoensis has a wide distribution Some members of the genus Spicata have in western North America, including collections been described as possible nest fleas (Hub- from Colorado ground squirrels (Hubbard bard 1947). Spicata rara was first collected 1947). According to Lewis (2002), O. idahoen- from T. talpoides in Jackson County, Colorado, sis has an equally broad host range, having by I. Fox (1940) and subsequently reported from been reported from 54 species, 5 of which are Thomomys sp. in Iron County, Utah (Stark birds. A few thirteen-lined ground squirrels, 1959). Additional, but limited, collections have S. tridecemlineatus, were found in pocket been made in Montezuma County, Colorado, gopher burrows during our study, suggesting and in Big Horn County, Wyoming (Lewis that this host was the source of the single O. 2003). Thus far, all collection sites are sepa- idahoensis collected. rated by 150–300 miles. Lewis suggested that The single flea identified as Oropsylla (Opiso- S. rara might be a “winter species,” with higher crostis) sp. was a female. It may belong to the population numbers present in pocket gopher species O. idahoensis or other closely related burrows during the winter months. The 3 speci- species, but males are required for a specific mens we collected were taken in January, Feb- identification. ruary, and May, thus supporting this assertion. Flea Abundance Very few S. rara have been collected from any single locale, but with this new Elbert County The number of fleas present on T. talpoides record, we believe that S. rara is widely dis- not only varied seasonally but also varied by persed in low numbers throughout Colorado sex of the host. Seasonal abundance was simi- and adjacent montane regions. lar to that which Longanecker and Burroughs Hystrichopsylla dippiei ssp. was first reported (1952) described for H. anomalus from S. beech- from mustelids, but it has also been taken eyi in California. As the temperature increased from a wide array of sciurids, cricetids, and from April through July, so too did the total geomyid rodents including T. talpoides (Hub- number of fleas collected from T. talpoides. bard 1947, Holland 1985). Lewis and Lewis Although we did not measure temperature and (1994) stated that members of this genus show humidity levels within pocket gopher burrows, little host specificity, occurring on many dif- we assumed that temperatures rose and humid- ferent species of small mammals. According to ity increased in warmer months in the burrows. Hubbard (1947) and Holland (1957), these large Reichardt and Galloway (1994) live-trapped fleas are usually collected as single individuals S. franklinii biweekly and found that female or in groups of 2 and 3. Unlike S. rara, however, fleas outnumbered male fleas during most of 2005] FLEAS OF NORTHERN POCKET GOPHERS 213

TABLE 2. Flea infestation on male and female Thomomys talpoides in (2002–2003) Elbert Co., Colorado, by month. The standard deviation is ±0.197 for males and ±0.167 for females, and the number of hosts is in parentheses after each percent. Number of Percent of Ratio of : Percent of Ratio of : Month T. talpoides T. talpoides with fleas fleas on hosts T. talpoides with fleas fleas on hosts October 26 73 (11) 1.38 53 (15) 2 November 21 57 (7) 2 50 (14) 0.53 December 10 33 (3) 0 57 (7) 1 January 20 78 (9) 0.5 55 (11) 2.5 February 20 71 (7) 3.5 77 (13) 0.77 March 11 100 (4) 4 43 (7) 0.67 April 16 60 (10) 1.72 33 (6) 1.25 May 14 100 (4) 1.18 90 (10) 1.08 June 23 83 (6) 0.67 76 (17) 0.84 July 22 50 (6) 0.58 63 (16) 1.18 August 29 57 (12) 0.8 33 (17) 0.5 September 23 70 (10) 1.56 54 (13) 1.27 October 12 90 (10) 0.46 50 (2) 1 MEANS 71 (99) 1.41 56 (148) 1.13

their study, except during early May and late and Larson et al. (1996), because the numbers June or early July. They suggested that the of fleas peaked during a period of 3–4 months, temporarily altered sex ratio represented newly possibly related to changes in ambient temper- emerged male fleas. We found that male F. ature and relative humidity within the burrows. ignota outnumbered female F. ignota about During the summer months, when many half the time on hosts of both sexes (Table 2) young-of-the-year are present, factors such as and that there was a large peak in the male-to- increased temperature, elevated humidity in female ratio from March though May, with the burrows, and greater numbers of gophers smaller peaks in December and October. This might account for the higher numbers of fleas may represent a postemergent increase of male (Table 1). fleas. Further studies of F. i. ignota in Colorado Mead-Briggs et al. (1975) reported the could explore the timing of flea reproduction, migration of the rabbit flea, Spilopsyllus cuni- numbers of individuals produced in one pocket culi (Dale), from bucks to does of Oryctolagus gopher burrow, and the sex ratio of the newly cuniculus (L.) in response to reproductive emerged cohort. A yearlong study to monitor cues. Does yielded greater numbers of fleas temperature and relative humidity in the bur- than males during mid- to late pregnancy. Our rows would be interesting but labor intensive. study indicated no evidence of a similar hor- Such data might explain seasonal fluctuations in flea abundance and elucidate their popula- monally induced migration of F. i. ignota onto tion dynamics on northern pocket gophers. female pocket gophers. The percent of male pocket gophers with fleas from March through ACKNOWLEDGMENTS June was greater than that for females even though these months encompass the host’s We thank Charles Carnahan of the Carna- breeding season (Hansen 1960). The ratio of han Ranches, Darren Oljkers of the Oljkers fleas on female pocket gophers did not increase Ranch, and the Peaceful Valley Scout Ranch during this time, as would be expected if hor- for permission to collect northern pocket monal changes during pregnancy of these ani- gophers on their lands. We gratefully acknowl- mals led to synchronization of flea breeding. edge R.E. Lewis for verification of flea identi- Male T. talpoides exhibited a higher percent- fication, D.L. Hall for assistance with statisti- age of flea infestation than females for all but 3 cal analysis, O.R. Larson for critiquing the months (Table 2). This may be a collection manuscript, the 2003 Animal Ecology class from artifact, but it is similar to the findings of Lon- University of Colorado, Colorado Springs, and ganecker and Burroughs (1952), Lang (1996), K. Whelan for assistance in collecting animals. 214 WESTERN NORTH AMERICAN NATURALIST [Volume 65

LITERATURE CITED Ceratophyllidae: Ceratophyllinae). Journal of Vector Ecology 27:184–206. BAKER, R.J., R.D. BRADLEY, AND L.R. MCALILEY, JR. 2003. ______. 2003. A review of the North American flea genus Pocket gophers: Geomyidae. Pages 276–287 in G.A. Spicata I. Fox, 1940 (Siphonaptera: Ceratophyllidae). Feldhamer, B.C. Thompson, and J.A. Chapman, edi- Proceedings of the Entomological Society of Wash- tors, Wild mammals of North America: biology, man- ington 105:876–882. agement and conservation. The Johns Hopkins Uni- LEWIS, R.E., AND J.H. LEWIS. 1994. Siphonaptera of North versity Press, Baltimore. America north of Mexico: Hystrichopsyllidae s. str. EADS, R.B. 1949. Recent collections of Colorado fleas. Jour- Journal of Medical Entomology 31:795–812. nal of Economic Entomology 42:144. LONGANECKER, D.S., AND A.L. BURROUGHS. 1952. Sylvatic FOX, I. 1940. Siphonaptera from western United States. plague studies, IX. Studies of the microclimate of Journal of the Washington Academy of Science 30: the California ground squirrel burrow and its rela- 272–275. tion to seasonal changes in the flea population. Ecol- HANSEN, R.M. 1960. Age and reproductive characteristics ogy 33:488–499. of mountain pocket gophers in Colorado. Journal of MEAD-BRIGGS, A.R., J.A. VAUGHAN, AND B.D. RENNISON. Mammalogy 41:323–335. 1975. Seasonal variation in numbers of the rabbit HOLLAND, G.P. 1957. Notes on the genus Hystrichopsylla flea on the wild rabbit. Parasitology 70:103–118. Rothschild in the New World, with descriptions of MILLER, R.S., AND R.A. WARD. 1960. Ectoparasites of one new species and two new subspecies (Siphonap- pocket gophers from Colorado. American Midland tera: Hystrichopsyllidae). Canadian Entomologist 89: Naturalist 64:382–391. 309–324. REICHARDT, T.R., AND T.D. G ALLOWAY. 1994. Seasonal ______. 1985. The fleas of Canada, Alaska and Greenland occurrence and reproductive status of Opisocrostis (Siphonaptera). Memoirs of the Entomological Soci- bruneri (Siphonaptera: Ceratophyllidae), a flea on ety of Canada 130. Franklin’s ground squirrel, Spermophilus franklinii HUBBARD, C.A. 1947. Fleas of western North America. (Rodentia: Sciuridae) near Birds Hill Park, Manitoba. Iowa State College Press, Ames. Journal of Medical Entomology 31:105–113. LANG, J.D. 1996. Factors affecting the seasonal abundance STARK, H.E. 1959. The Siphonaptera of Utah: their taxon- of ground squirrel and woodrat fleas (Siphonaptera) omy, distribution, host relations, and medical impor- in San Diego County, California. Journal of Medical tance. U.S. Department of Health, Education, and Entomology 33:790–804. Welfare, Centers for Disease Control, Atlanta, GA. LARSON, O.R., R.G. SCHWAB, AND A. FAIRBROTHER. 1996. Seasonal occurrence of fleas (Siphonaptera) on deer Received 28 June 2004 mice (Peromyscus maniculatus) in northern Califor- Accepted 12 October 2004 nia. Journal of Vector Ecology 21:31–36. LEWIS, R.E. 2002. A review of the North American species of Oropsylla Wagner and Ioff, 1926 (Siphonaptera: Western North American Naturalist 65(2), © 2005, pp. 215–222

DISTRIBUTION, FORAGING BEHAVIOR, AND CAPTURE RESULTS OF THE SPOTTED BAT (EUDERMA MACULATUM) IN CENTRAL OREGON

Thomas J. Rodhouse1,2, Maureen F. McCaffrey1, and R. Gerald Wright3

ABSTRACT.—The spotted bat (Euderma maculatum) has been virtually unknown in Oregon despite the existence of potential habitat in many areas of the state. In 2002 and 2003 we searched for spotted bats along the John Day, Deschutes, and Crooked Rivers and at a remote dry canyon southeast of the city of Bend in central Oregon. The species was documented through the use of mist-nets, a bat detector, and recognition of audible spotted bat calls. Spotted bats were found at 11 locations in 6 Oregon counties. Nightly activity patterns of spotted bats were unpredictable. Spotted bats were found in 78% of search areas but on only 48% of survey nights. We observed spotted bats foraging above fields and low upland slopes adjacent to rivers and creeks and along the rims of cliffs. Estimated flying heights of spotted bats ranged from 3 m to 50 m aboveground. The species was difficult to capture and was captured only after considerable experimentation with methods and materials. Three spotted bats were captured toward the end of the project in 2003 and accounted for only 0.5% of all bats captured during the study. Although we attached radio transmitters to 2 spotted bats, we found no roost locations. We believe additional spotted bat surveys in Oregon are warranted, especially in higher-elevation habitats, but recommend that to increase their effectiveness, surveys accommodate the unique foraging behavior of the species.

Key words: spotted bat, Euderma maculatum, distribution, foraging behavior, capture results, Oregon.

The spotted bat, Euderma maculatum, is have led to the identification of new localities widespread throughout arid portions of west- in habitats similar to those that exist in central ern North America, but it is patchily distrib- Oregon (Sarell and McGuiness 1993, Doering uted and only locally common within its range and Keller 1998, Pierson and Rainey 1998, (Fenton et al. 1987, Navo et al. 1992, Pierson Geluso 2000, Gitzen et al. 2001). Approximate- and Rainey 1998, Geluso 2000). Unique habitat ly two-thirds of the state of Oregon lies east of requirements, namely the presence of large the Cascade mountain range and contains num- cliffs and water, appear to limit its distribution erous steeply walled canyons and meadow (Luce 2005). But even within areas of appar- complexes characteristic of the Intermountain ently suitable habitat, spotted bats are often West. These landscapes are typical of spotted absent or infrequently encountered (Geluso bat habitat (e.g., Pierson and Rainey 1998), 2000). This apparent rarity has prompted most and the lack of documented spotted bat activ- regional and state authorities to list the species ity in the region is incongruous with the avail- either as threatened or of concern (Luce 2005). ability of apparently suitable habitat. Only 2 In Oregon the species has remained largely voucher specimens exist for Oregon, and the unknown and the state wildlife agency has not only other state records come from 3 isolated yet assigned it a conservation status (Verts and reports based on audible detections made dur- Carraway 1998, Csuti et al. 2001, Oregon Nat- ing the 1990s along the Snake River on the ural Heritage Program 2001). Oregon border (McMahon et al. 1981, Barss Maps of the predicted distribution of the and Forbes 1984, Ormsbee and Risdal 2004). spotted bat have consistently shown central The most westerly of the historic Oregon Oregon to be on the periphery of its range records came from a dead specimen found in (Watkins 1977, Hall 1981, Verts and Carraway 1984 in a cliff along the John Day River, but 1998, Csuti et al. 2001). However, recent sur- no effort had been made to determine if the veys for spotted bats in surrounding states species regularly occurred there (Barss and

1Department of Fish and Wildlife Resources, University of Idaho, Moscow, ID 83844-1136. 2Corresponding author: 365 NW State St., Bend, OR 97701. 3USGS, Idaho Cooperative Fish and Wildlife Research Unit, University of Idaho, Moscow, ID 83844-1136.

215 216 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Forbes 1984). In July 2002, as part of an ongo- steppe vegetation consists of open woodlands ing National Park Service (NPS) mammal of western juniper ( Juniperus occidentalis), inventory, we began a search for spotted bats sagebrush (Artemisia tridentata), and a variety in the John Day River valley. The survey effort of annual and perennial grasses. Irrigated agri- continued through October 2003 and was ex- cultural fields or previously cultivated old panded to include areas along the Deschutes fields are present along the riverine floodplain and Crooked Rivers west of the John Day terraces and on top of rimrock plateaus near Basin and a dry canyon east of the town of all search areas except the Dry River area (area Bend, southwest of the Crooked River. The 14, Table 1). objectives of this study were (1) to determine if spotted bats were present in the historic METHODS locality reported by Barss and Forbes (1984), (2) to identify new localities along the John This study was conducted simultaneously Day River and adjacent drainages, and (3) to with ongoing mammal inventory work and a capture the species in order to obtain photo- telemetry project involving other species of graphic vouchers and information on sex, age, bats in the John Day Fossil Beds National and reproductive condition. Monument. We conducted surveys in 2002 from 15 July to 10 September. In 2003 they STUDY AREA were conducted from 1 May to 18 October. During the course of the study, we visited 24 We searched for spotted bats in 14 search survey sites, grouped into 14 search areas. areas located along a 290-km section of the Survey site selection was based on suitability John Day River and 3 major tributaries; at for mist-netting and proximity to large cliff selected locations on the Deschutes and complexes. Single visits were made to 11 sur- Crooked Rivers, a large parallel drainage lo- vey sites, and 13 sites had 2 or more visits cated to the west of the John Day basin; and at made during the study. Survey activities con- Dry River canyon, 27 km east of the town of ducted during site visits included mist-net- Bend, in north central Oregon (see Fig. 1). ting, recording of echolocation calls, and audio- Our search areas were located near large cliffs visual observations of passing spotted bats. and rimrock features in Deschutes, Gilliam, Durations of site visits were variable and were Grant, Jefferson, Wasco, and Wheeler Counties. dictated by weather and logistical considera- Along the John Day River, most search areas tions. The average visit was 3.5 hours, with visits were concentrated around the 3 widely sepa- ranging from 20 minutes to 9 hours. On some rated units of the John Day Fossil Beds nights we visited more than 1 site. Incidental National Monument (areas 2–9, Table 1). One observations of spotted bats were made while search area was located at the mouth of a large conducting other project activities throughout upland cave 4.5 km off the John Day River the study. (area 7, Table 1). The Dry River search area Spotted bats produce distinctive echoloca- (area 14, Table 1) was approximately 20 km tion calls audible to the unaided human ear, from the Crooked River, which is a much greater and the detection of these calls was the pri- distance from a perennial creek or river than mary method of observation (Woodsworth et the other 13 search areas. Search area eleva- al. 1981, Leonard and Fenton 1984). Large tions range from 180 m to 1278 m. Elevations of hand-held spotlights were used in conjunction nearby buttes and plateaus range from 1200 m with audible detections to illuminate spotted to 1600 m. The climate of the study region is bats and to aid in estimating flying height, semiarid, dominated by hot, dry summers and direction of travel, and other observations of cool, dry winters. Mean annual precipitation foraging behavior. Each observation was cate- from weather stations near search areas for the gorized as a “pass,” since most observations period 1973–2003 ranged from 20 cm to 27 cm consisted of bats flying past an observer. Most (Oregon Climate Service 2003). Juniper-sage- passes were discrete, unidirectional events, brush steppe vegetation dominates all search although some events included long periods areas, except along the narrow riparian zones, (e.g., 1–20 minutes) during which individual where black cottonwood (Populus trichocarpa) bats remained within hearing or spotlight dis- and willows (Salix spp.) are common. Upland tance of an observer. The presence of multiple 2005] SPOTTED BAT IN CENTRAL OREGON 217

Fig. 1. Search areas included in the 2002–2003 survey of spotted bats in central Oregon. Search area numbers correspond with those listed in Table 1. The inset map shows historic spotted bat localities in the state of Oregon. individuals was determined by illuminating Park, CA, USA) was used to record spotted bat >1 bat simultaneously, by observing a passing calls and supplement audiovisual observations. bat at the same time a captured bat was still in This tool was useful primarily as a means of hand, and by hearing calls in clearly distin- aiding in species identification and providing guishable directions. Foraging height estimates a vouchering system. Recordings were also were aided by comparing flying height of illu- made of calls produced by hand-released spot- minated bats to the tops of nearby visible ted bats captured late in the project. structures such as telephone poles and tree- Mist-nets were employed throughout the tops. project both to complete the goals of the NPS An Anabat bat echolocation recording and inventory and to try to specifically capture analysis system (Titley Electronics, Ballina, spotted bats for this project. Spotted bats are NSW, Australia; Corben Scientific, Rohnert difficult to capture in many areas (Navo et al. 218 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 1. Search areas included in the 2002–2003 survey of spotted bats in central Oregon. Names are based on the nearest significant geographic feature. Location coordinates are provided in the Universal Transverse Mercator (UTM) projection, using the North American Datum of 1927 (NAD27). Grant County locations are in UTM Zone 11; all others are in zone 10. The detection column refers to the detection method used, where A indicates audible, V indicates visual, R indicates recording, and C indicates capture. The area number corresponds to numbers used in Figure 1. The abbre- viation JDFBNM is used for the John Day Fossil Beds National Monument. Area # County Name UTM X UTM Y Detection 1 Gilliam J.S. Burres State Park 697960 5038845 A 2Wasco/Wheeler Clarno 699850 4976410 A,V,R,C 3 Wheeler Pine Creek 703965 4976114 A,V,R 4 Wheeler Bridge Creek, JDFBNM 718039 4948023 A,V 5 Grant Kimberly 291203 4959041 None 6 Grant Cathedral Rock, JDFBNM 290690 4945426 A 7 Grant Big Basin 293551 4941486 A,V,C 8 Grant Goose Rock, JDFBNM 290113 4939115 None 9 Grant Picture Gorge, JDFBNM 290556 4934514 None 10 Jefferson The Cove Palisades State Park 638427 4934143 A, V 11 Jefferson Lake Billy Chinook 635424 4931695 A 12 Jefferson P.S. Ogden Scenic State Wayside 643950 4916520 A,V 13 Deschutes Smith Rocks State Park 648365 4914226 A,V 14 Deschutes Dry River 660697 4863341 A

1992, Gitzen et al. 2001), and extensive effort areas (78%) on 38 of 80 survey nights (48%). was made to catch the species in our study area. Incidental observations of spotted bats were Mist-nets of various lengths (2.6–18 m) were made on 12 additional nights. A total of 138 placed across pools and channels of open water spotted bat passes were observed throughout along the John Day River and tributaries, across the study. At Pine Creek and Clarno (areas 2, open fields, across a cave opening, and on top 3), where survey effort was most intense, spot- of a cliff. Using aluminum electrical conduit, ted bats were active during all months of the we elevated nets as high as 4.5 m aboveground study, from May through October. Several in- to try to intercept high-flying bats. cidental observations of spotted bats were Radio-transmitters were attached to 2 cap- made along Pine Creek during April 2003. We tured spotted bats. Transmitters weighing 0.51 also found spotted bats repeatedly at Smith g (LB-2 model, Holohil, Inc. Guelph, Canada) Rocks State Park (area 13) in June, August, and September 2003. At all other search areas, were attached with Skin-Bond surgical adhe- spotted bats were encountered only during sive (Smith and Nephew, Ltd., Largo, FL, USA) August–October. The species was found in all to the intra-scapular region of the bats. Trans- 6 Oregon counties where search areas were mitters weighed less than 5% of the mass of located. Multiple individuals were found at 5 instrumented bats. Bats were tracked using re- sites in 4 search areas (areas 2, 4, 13, 14), and ceivers with omni-directional magnetic vehi- repeat observations of multiple individuals cle roof antennas and 5-element hand-held were made at 3 of those locations (areas 2, 13). directional antennas (Wildlife Materials, Inc, We never confirmed more than 3 individuals Carbondale, IL). The University of Idaho Ani- at a time. mal Care and Use Committee approved all Two male spotted bats were captured on capture and handling procedures used during different nights at 1 location on the John Day the study. River (area 2), and a 3rd individual was captured in a different location along the John Day RESULTS River (area 7) but escaped from the net before it could be processed. Both male bats were In total, we spent 343 hours of mist-netting, instrumented with radio transmitters during recording, and audiovisual observations dur- late August and early September 2003, but ing 80 nights. Spotted bats were encountered roosts were not located despite extensive search- at 14 of 24 survey sites (58%) in 11 of 14 search ing. After searching for 4 days and nights, we 2005] SPOTTED BAT IN CENTRAL OREGON 219 briefly encountered 1 bat foraging approxi- that site during 5 additional nights of mist-net- mately 8 km upriver from the capture site, but ting. we could not relocate it again. The 2nd bat was Spotted bats were repeatedly encountered tracked upriver for several hours after being foraging high over irrigated fields and old fields, released but was not relocated on subsequent low upland slopes of juniper and sagebrush, days and nights. and along the rims of cliffs. Estimates of flying Spotted bats were active at all hours of the height made for 61 passes ranged from 3 m to night during the study. The earliest observed 50 m, and average flying height was 20 m. No flights of the species were recorded at Smith spotted bats were observed coming down to Rocks (area 13) on the Crooked River. There, drink, although bats were occasionally observed spotted bats were observed flying within 38 flying high over water. Likewise, on no occa- minutes after civil sunset in dusky, low-light sion did we observe spotted bats flying low conditions. At the Dry River canyon (area 14), enough for standard use of mist-nets to be spotted bats were first heard 43 minutes after effective. Only after considerable effort and sunset. Along the John Day River, the earliest experimentation with elevated nets were we observation was made in the Clarno area (area able to capture the species. The most success- 2) 63 minutes after sunset, although spotted ful net configuration consisted of four 12-m bats normally did not arrive there until much nets erected on 4.5-m poles placed along the later in the evening. As a point of reference, rim of a cliff overlooking the John Day River emergence times of western small-footed myotis (area 2). This net arrangement was placed where (Myotis ciliolabrum) and pallid bats (Antrozous spotted bats had been previously observed pallidus) tracked to day roosts in the John Day cresting low over the top of the cliff. A 3rd Valley during the same study period averaged spotted bat was captured in a mist-net placed 24 minutes and 47 minutes after sunset, re- across the mouth of a large upland cave (area spectively. Dawn observations of spotted bats 7). Although this net was not elevated, the were also made on several occasions, includ- cave itself is located in the middle of a steep, ing one made 78 minutes before civil sunrise. cliff-like slope. Spotted bats accounted for We noted considerable variability in the only 3 of 548 bat captures (0.5 %) made during presence and timing of spotted bats at survey 300 hours of netting on 65 nights. However, sites. While spotted bats were repeatedly en- this rate is much higher when effort includes countered at many sites, the species was never only the number of hours that elevated nets encountered at some locations with seemingly were employed. Elevated nets were employed ideal habitat (e.g., large cliffs along rivers; for 87 hours on 15 nights, and spotted bats areas 5, 8, 9). One incidental observation made accounted for 2 of 16 bats caught. A total of 14 at Cathedral Rock (area 6) was the only detec- species of bats were captured during the entire tion made at that site, despite 3 other nights of study period, but only 6 species were caught formal surveys conducted there. At 7 sites in elevated nets. where spotted bats were encountered at least once, the species was detected in only 25 of 53 DISCUSSION visits lasting 1 hour or more. During visits to Smith Rocks (area 13) when observers were in Prior to this study, only 1 spotted bat had place before sunset, spotted bats were first been captured in Oregon (McMahon et al. detected 38 and 39 minutes after sunset. The 1981). That record and those from Barss and predictability in the timing of the initial arrival Forbes (1984) and the 3 records from the Snake of spotted bats there was not consistent with River (Ormsbee and Risdal 2004) suggested a observations made in other areas. During 2 pattern of random and rare occurrences in the consecutive visits to 1 site in Pine Creek (area state. A search for spotted bats in eastern Ore- 3), 1st arrival in the 2nd visit occurred 30 min- gon in 1983 failed to document the species, utes after 1st arrival on the previous night, and further supporting this perception (Fenton et both 1st arrivals occurred more than 3 hours al. 1987). While the spotted bat has an unde- after sunset. Along Bridge Creek (area 4), we termined conservation status with the Oregon observed 2 spotted bats flying together 4 hours Department of Fish and Wildlife, the Oregon after sunset; no other passes were recorded at Natural Heritage Program placed the spotted 220 WESTERN NORTH AMERICAN NATURALIST [Volume 65 bat on a list of species at risk of extirpation and crete flight paths, making them more suscepti- peripheral species (Oregon Natural Heritage ble to capture (Poche 1981, Geluso 2000). Program 2001). Our results suggest that spotted While we propose that spotted bats may be bats may be much more common and wide- relatively common in central Oregon, we found spread in Oregon than historic evidence sug- night-to-night activity somewhat variable. The gests. Spotted bats appear to be well established species was encountered in 78% of search areas, in the lower Deschutes and John Day basins. but on only 48% of survey nights. Spotted bats The presence of spotted bats at the Dry River arrived early and regularly at the Smith Rocks canyon southeast of Bend provides evidence area but were much less predictable along the that the species may occur widely in drier up- John Day River. Spotted bats were once con- lands far from large water bodies as well. sidered a late-emerging species, but several stud- In a recent review of the literature, Luce ies have demonstrated the species to emerge (2005) also suggested that spotted bats might relatively early (Easterla 1965, Wai-ping and be more common than historic records indi- Fenton 1989, Navo et al 1992). Our results are cate. Our study and others (Pierson and Rainey consistent with this, and we believe that per- 1998, Geluso 2000) that have specifically ceptions of spotted bat emergence times are searched for spotted bats in suitable habitat influenced by the distance of an observation have added many new localities in recent years. point to roosts. We interpret our results to sug- This may be due to an increasing reliance on gest that spotted bats were roosting close to audible detections rather than capture results. our observation points at Smith Rocks State While some investigators have suggested that Park and Dry River canyon and much farther spotted bat capture results adequately repre- away from observations made along the John sent abundance, our results suggest otherwise Day River. In the sites where spotted bats were (Fenton et al. 1983, Berna 1990). Without con- encountered early, the intervals between passes certed effort using alternative methods, spot- became longer as the night progressed. These ted bats would not have been captured at all late-night activity patterns resembled those in in our study area, perhaps leading to the spu- sites with consistently late first-arrival encoun- rious conclusion that the species was absent ters. It may be that the predictability in spot- from the region. Navo et al. (1992) and Gitzen ted bat activity patterns declines as bats fly et al. (2001) also reported that the species was farther from roosts. difficult to capture. Pierson and Rainey (1998) An additional consideration to the issue of reported captures from only 4 of 28 new spot- variability in the timing and presence of spotted bat localities in California. Geluso (2000) ted bats at search areas is that of transient reported multiple captures of spotted bats bats. It seems likely that at least some of the from some locations in Nevada but reported bats encountered in May, June, and July were that the species had not been successfully cap- roosting locally as “resident” bats. However, tured in several other locations where it had the disappearance of the 2 male spotted bats been detected acoustically. fitted with radio transmitters late in August Clearly, the high-flying behavior of foraging and September provides some evidence of spotted bats encountered in our study played transience, and this behavior may account for a significant role in capture difficulty. Navo et some of the variability observed during the al. (1992) regularly observed the species flying study. It may also account for the single en- 10 m or more aboveground and did not observe counters at search areas where multiple surveys the species flying low enough to be caught in were made (areas 4, 6, 7). All encounters at mist-nets. Others have reported this behavior these sites occurred in August and September. as well, and we know of at least 1 other investi- Several investigators have hypothesized that gator resorting to unusual mist-net tactics sim- spotted bats undertake localized migrations to ilar to ours to catch spotted bats (Jason Williams, higher elevations in midsummer and return to Nevada Division of Wildlife, personal com- lower elevations in late August and September munication). In areas where the species has (Poche 1981, Berna 1990, and Geluso 2000). been more easily captured in mist-nets, topog- Likewise, Rabe et al. (1998) demonstrated raphy and limited open water may force spot- that spotted bats are capable of undertaking ted bats to fly at lower heights or in more dis- long daily movements over 30 km. Very little 2005] SPOTTED BAT IN CENTRAL OREGON 221 additional information is available on this topic, ACKNOWLEDGMENTS but it may be that spotted bats travel considerable distances in central Oregon between This project was conducted through fund- roosting and foraging areas and between sum- ing from the National Park Service Natural mer roosts and winter hibernacula. Resource Challenge Fund (subagreeement 20, Woodsworth et al. (1981) reported remark- cooperative agreement CA9000-95-018), a grant able regularity in the arrival, direction, and from the Pacific Northwest Cooperative Eco- duration of foraging spotted bats on consecu- logical Studies Unit (cooperative agreement tive nights in southern British Columbia. Sev- CA9088-A-0008), and additional materials and eral other surveys have successfully relied on support from Ken Hyde of the John Day Fossil short (e.g., ≤20 minutes) observation periods Beds National Monument. We thank Pat Orms- (Fenton et al. 1987, Navo et al. 1992, Pierson bee for making the Oregon Bat Database avail- and Rainey 1998). Based on our experience in able to us. We also thank Bob Luce for provid- central Oregon, however, surveys may be ing us with a copy of the forthcoming USFS more effective if longer observation periods Region 2 spotted bat conservation assessment. are used. While some survey objectives may We thank Matt Smith for his assistance in the best be served by many short observations, field. We are especially grateful to the Confed- these also may lead to the conclusion that erated Tribes of Warm Springs for providing spotted bats are absent from areas where they access to Pine Creek Ranch and to Kelly actually occur. McGreer for providing access to private land Despite our assertion that spotted bats are along the John Day River. We are indebted to more common than previously believed in the Oregon Museum of Science Industry for Oregon, the species is certainly much less providing room and board at the Hancock concentrated and locally abundant than, for Field Station. David Waldien provided helpful example, species of Myotis where dozens of comments on an earlier draft of this manu- individuals can be captured during a single script. We thank Burr Betts and an anonymous night. We were unable to confirm concentra- reviewer for their thoughtful review of this tions of more than 3 individual spotted bats manuscript. during our study, although this was a conservative estimate. It is entirely plausible that, LITERATURE CITED even as new surveys dramatically increase the BARSS, J.M., AND R.B. FORBES. 1984. A spotted bat (Euder- number of known spotted bat localities through- ma maculatum) from north-central Oregon. Murrelet out its range, the species will continue to be 65:80. perceived as rare and require conservation BERNA, H.J. 1990. Seven bat species from the Kaibab Plateau, Arizona, with a new record of Euderma attention. Much needs to be learned about the maculatum. Southwestern Naturalist 35:354–356. species before this can be ascertained. We CSUTI, B., T.A. O’NEIL, M.M. SHAGHNESSY, E.P. GAINES, strongly recommend that additional surveys AND J.C. HAK. 2001. Atlas of Oregon wildlife. Ore- be conducted in Oregon in the many areas gon State University Press, Corvallis. 525 pp. of potential habitat that have not yet been DOERING, R.W., AND B.L. KELLER. 1998. A survey of the bat species of the Bruneau-Jarbridge River area of searched. Higher-elevation forest habitats in southwestern Idaho with special reference to the eastern Oregon where open meadows and cliffs occurrence of the spotted bat (Euderma maculatum). are present seem to us to be particularly im- Idaho Bureau of Land Management Technical Bul- portant areas to investigate. There may also be letin 98-18. 29 pp. EASTERLA, D.A. 1965. The spotted bat in Utah. Journal of areas of suitable habitat in the southwestern Mammalogy 46:665–668. portion of the state where semiarid conditions FENTON, B.B., H.G. MERRIAM, AND G.L. HOLROYD. 1983. extend west of the Cascade Mountains. The Bats of Kootenay, Glacier, and Mount Revelstoke discovery of spotted bats in Siskiyou County, National Parks in Canada: identification by echolocation calls, distribution, and biology. Canadian Jour- California, less than 50 miles from the Oregon nal of Zoology 61:2503–2508. border, certainly suggests that this may be FENTON, M.B., D.C. TENNANT, AND J. WYSZECKI. 1987. worthwhile (Pierson and Rainey 1998). Only Using echolocation calls to measure the distribution after more of the distribution and habitat asso- of bats: the case of Euderma maculatum. Journal of ciation gaps have been filled can a meaningful Mammalogy 68:142–144. GELUSO, K. 2000. Distribution of the spotted bat (Euder- spotted bat conservation status be determined ma maculatum) in Nevada, including notes on repro- for Oregon. duction. Southwestern Naturalist 45:347–352. 222 WESTERN NORTH AMERICAN NATURALIST [Volume 65

GITZEN, R.A., S.D. WEST, AND J.A. BAUMGARDT. 2001. A PIERSON, E.D., AND W.E. RAINEY. 1998. Distribution of record of the spotted bat (Euderma maculatum) from the spotted bat, Euderma maculatum, in California. Crescent Bar, Washington. Northwestern Naturalist Journal of Mammalogy 79:1296–1305. 82:28–30. POCHE, R.M. 1981. Ecology of the spotted bat (Euderma HALL, E.R. 1981. The mammals of North America. John maculatum) in southwest Utah. Utah Division of Wild- Wiley and Sons, New York. 690 pp. life Resources Publication 81-1. 63 pp. LEONARD, M.L., AND M.B. FENTON. 1984. Echolocation RABE, M.J., M.S. SIDERS, C.R. MILLER, AND T.K. SNOW. calls of Euderma maculatum (Vespertilionidae): use 1998. Long foraging distance for a spotted bat (Eud- in orientation and communication. Journal of Mam- erma maculatum) in northern Arizona. Southwestern malogy 65:122–126. Naturalist 43:266–269. LUCE, R.J. 2005. Spotted bat (Euderma maculatum): a tech- SARELL, M.J., AND K.P. MCGUINNESS. 1993. Rare bats of nical conservation assessment [on line]. USDA Forest the shrub-steppe ecosystem of eastern Washington. Service, Rocky Mountain Region. Available at: http:// Unpublished report, Washington Department of Wild- www.fs.fed.us/r2/projects/scp/assessments/spotted- life Nongame Program, Olympia. 23 pp. bat.pdf. VERTS, B.J., AND L.N. CARRAWAY. 1998. Land mammals of MCMAHON, E.E., C.C. OAKLEY, AND S.F. CROSS. 1981. Oregon. University of California Press, Berkeley. First record of the spotted bat (Euderma maculatum) 668 pp. from Oregon. Great Basin Naturalist 41:270. WAI-PING, V., AND M.B. FENTON. 1989. Ecology of the NAVO, K.W., J.A. GORE, AND G.T. SKIBA. 1992. Observa- spotted bat (Euderma maculatum) roosting and for- tions on the spotted bat, Euderma maculatum, in aging behavior. Journal of Mammalogy 70:617–622. northwestern Colorado. Journal of Mammalogy 73: WATKINS, L.C. 1977. Euderma maculatum. Mammalian 547–551. Species 77:1–4. OREGON CLIMATE SERVICE. 2003. Zone climate data WOODSWORTH, G.C., G.P. BELL, AND M.B. FENTON. 1981. archives. Oregon State University College of Oceanic Observations of the echolocation, feeding behavior, and Atmospheric Sciences, Corvallis. Available at: and habitat use of Euderma maculatum (Chiroptera: http://www.ocs.orst.edu/allzone. Vespertilionidae) in southcentral British Columbia. OREGON NATURAL HERITAGE PROGRAM. 2001. Rare, threat- Canadian Journal of Zoology 59:1099–1102. ened, and endangered plants and animals of Oregon. Oregon Natural Heritage Program, Portland. 94 pp. Received 29 January 2004 Available at: http://www.oregonstate.edu/ornhic/pub- Accepted 3 August 2004 lications.html. ORMSBEE, P.C., AND L.L. RISDAL. 2004. Oregon bat database. USDA Forest Service, Willamette National For- est, Eugene, OR. Western North American Naturalist 65(2), © 2005, pp. 223–228

HABITAT AND NESTING BIOLOGY OF MOUNTAIN PLOVERS IN WYOMING

Regan E. Plumb1, Stanley H. Anderson1, and Fritz L. Knopf2

ABSTRACT.—Although previous research has considered habitat associations and breeding biology of Mountain Plovers in Wyoming at discrete sites, no study has considered these attributes at a statewide scale. We located 55 Mountain Plover nests in 6 counties across Wyoming during 2002 and 2003. Nests occurred in 2 general habitat types: grassland and desert-shrub. Mean estimated hatch date was 26 June (n = 31) in 2002 and 21 June (n = 24) in 2003. Mean hatch date was not related to latitude or elevation. Hatch success of nests was inferred in 2003 by the presence of eggshell fragments in the nest scrape. Eggs in 14 of 22 (64%) known-fate nests hatched. All grassland sites and 90% of desert sites were host to ungulate grazers, although prairie dogs were absent at 64% of nest sites. Nest plots had less grass coverage and reduced grass height compared with random plots. More than 50% of nests occurred on elevated plateaus. The Mountain Plover’s tendency to nest on arid, elevated plateaus further substantiates claims that the bird is also a disturbed-prairie species.

Key words: Mountain Plover, Charadrius montanus, nest site, hatching success, Wyoming, shortgrass prairie.

The Mountain Plover (Charadrius montanus) Knopf and Miller (1994) reported 32% bare is endemic to the grasslands of North America, ground at nest sites in Colorado and suggest that particularly the western Great Plains and Col- 30% bare ground is a minimum habitat require- orado Plateau. It nests in shortgrass prairie ment for nesting Mountain Plovers. Ellison et al. habitats historically used by large assemblages (2001) found reduced grass cover at nest sites of herbivores, specifically bison (Bison bison), in Utah, while Parrish et al. (1993) reported pronghorn (Antelocapra americana), and prairie 72% bare ground at nest sites and 79% bare dogs (Cynomys spp.), and in more xeric, desert ground in Wyoming. Beauvais and Smith (2003) shrub zones to the west (Knopf 1996). How- were able to correctly classify 87% of points in ever, this tendency for Mountain Plovers to an independent data set using a model that select native habitats with substantial bare predicted Mountain Plover presence as a func- ground, coupled with its former cohabitation tion of cover and slope in western Wyoming. with large herds of bison, pronghorn, elk, and These studies indicate that bare ground or, prairie dogs, has led some to argue that it is a conversely, lack of vegetative cover, may be one disturbed-prairie or semidesert species rather of the most influential predictors of Mountain than a shortgrass associate (Knopf and Miller Plover nesting habitat, particularly on the shrub-steppe. 1994). Laun (1957) found the bird on the arid Our study objectives were to (1) describe mixed-grass plains surrounding Laramie, where nesting phenology of breeding birds across the sheep and cattle grazing has occurred for over state, (2) report on hatching success of Moun- 100 years. In the southern portion of their tain Plover nests in Wyoming relative to other range, Mountain Plovers also nest on recently regions, (3) describe major vegetative associa- plowed fields, often with comparable success tions at nest sites, and (4) report on presence to rangeland nesters (Dreitz et al. in press). of grazing at nest sites. Likewise, wintering birds in California make extensive use of cultivated farmlands, land STUDY AREAS that was once native prairie supporting tule elk (Cervus elaphus), pronghorn, and kangaroo Nest searching was conducted throughout rats (Dipodomys spp.; Knopf and Rupert 1995). the state at locations where historic records of

1Wyoming Cooperative Fish and Wildlife Research Unit, University of Wyoming, Dept. 3166, 1000 E. University Ave., Laramie, WY 82071-3166. 2U.S. Geological Survey, Fort Collins Science Center, 2150-C Centre Avenue, Fort Collins, CO 80526-8118.

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Mountain Plover sightings occurred. We focused study area. The landscape is grazed by domes- search efforts at sites with high densities of tic sheep and cattle, pronghorn antelope, and records in Wyoming Game and Fish Depart- wild horses. White-tailed prairie dog (Cynomys ment files. High-density sites include grass- leucurus) colonies are common throughout. land landscapes in the Powder River, Shirley, Nest searching also occurred in numerous and Laramie Basins, and desert-shrub zones low-density areas including lands managed by in the Big Horn, Great Divide, and Washakie the Kemmerer Field Office of the Bureau of Basins. The Powder River basin study sites are Land Management (Lincoln County), the desert located on Thunder Basin National Grassland. landscape west of Flaming Gorge Reservoir The Laramie and Shirley Basin sites include (Sweetwater County), and Hannah Basin in portions of the Laramie Plains extending north central Wyoming (Carbon County). Few breed- and west from Laramie to Medicine Bow and ing birds and no nests were located in low- Foote Creek Rim, and the central portion of density areas. For this reason, low-density sites Shirley Basin, roughly delineated by the 2 inter- are not described in detail. sections of Wyoming Highways 77 and 487 in northeastern Carbon County. These basins are METHODS characterized by interspersed short- and mixed- Nest Searches grass prairie. Shortgrass species that occur include blue grama (Bouteloua gracilis) and Nest searches in 2002 were conducted in buffalo grass (Buchloe dactyloides). Commonly areas with historic Mountain Plover sightings, occurring mixed-grass species include needle- and in 2003 in areas previously established as and-thread grass (Stipa comata), western wheat- concentration areas for breeding plovers (Plumb grass (Agropyron smithii), Sandberg bluegrass 2004; breeding concentration areas were sites (Poa sandbergii), threadleaf sedge (Carex filafo- that averaged >30 Mountain Plover detec- lia), Indian ricegrass (Oryzopsis hymenoides), tions in 2002). Survey protocol was modeled and pricklypear cactus (Opuntia polyacantha). after Mountain Plover guidelines (U.S. Fish and Shrub species including big sagebrush (Arte- Wildlife Service 2002). Driving transects were misia tridentata), budsage (A. spinescens), and conducted along an established paved or dirt fourwing saltbush (Atriplex canescens) are also road. Stops were made at 0.25-mile intervals present. Black-tailed prairie dog (Cynomys for visual scans. Scans were conducted outside ludovicianus) colonies are common, and graz- the vehicle and lasted long enough for a 360° ing by domestic cattle and pronghorn antelope panorama. Nest searching occurred on sites is pervasive. Wind power development occurs where plovers showed signs of breeding activ- in portions of the Laramie Basin. ity upon detection (e.g., head bobbing, seated Primary desert-shrub sites include the position, courtship displays, or unwillingness Mexican Flats, located west of the town of to leave immediate area; U.S. Fish and Wild- Dad between Wamsutter and Baggs in the life Service 2002). Washakie Basin, a portion of the Great Divide Data Collection at Nest Basin of the Red Desert located south of Cyclone Rim in northern Sweetwater County, At least 2 eggs from each clutch were floated and parts of the Big Horn Basin near Cody in water to estimate clutch age and to approxi- and Powell (Park County) and Greybull (Big mate hatch date (Alberico 1995, Mabee 1997). Horn County), particularly Polecat and Chap- We revisited nests soon after projected hatch man Benches. These shrubland areas are typi- date to verify hatch. The relationship of pro- fied by saline soils and are dominated by jected hatch date to nest elevation and latitude greasewood (Sarcobatus vermiculatus), shad- was evaluated using linear regression. scale (Atriplex confertifolia), fourwing salt- Hatch success of at least 1 egg was inferred bush, and Gardner saltbush (A. gardneri), with by the presence of small eggshell fragments in winterfat (Ceratoides lanata), cushion plants, the nest scrape (Mabee 1997). Adult Mountain and pricklypear cactus interspersed. A mosaic Plovers remove large shell parts from the nest is often formed with stands of big sagebrush, as eggs hatch, but chicks breaking through the saltbush, and greasewood. Mixed-grass species eggshell leave small pipped fragments. We are also present. Oil and gas development is collected addled or abandoned eggs at this common, particularly in the Mexican Flats time for embryo aging. 2005] MOUNTAIN PLOVERS NESTING IN WYOMING 225

Fig. 1. Mountain Plover nest sites located in Wyoming in 2002 and 2003.

In 2002 vegetation was sampled at four 1.0- taken (Garmin 12). This method did not allow m2 plots at each nest site. The 1st plot was for relocation of nests. In 2003 we marked centered on the nest, and consecutive plots nests with 2 small stones labeled with Xs and were spaced at distances of 25, 50, and 100 m placed them precisely 1 m to the north and from the nest along a straight-line transect in a south of the scrape. GPS locations and detailed randomly selected cardinal direction deter- descriptions of the immediate nest environ- mined by 2 coin tosses. We generated 4 random ment were taken. plots in the vicinity of each nest by traveling along the nearest road for an arbitrarily chosen RESULTS distance of 1.6 km, randomly selecting a cardi- Clutch Size and nal direction by coin tosses, and sampling 1.0- Breeding Phenology 2 m plots at 0-, 25-, 50-, and 100-m increments Between 28 May and 10 July 2002, we along a straight-line transect. Plots were delin- located 31 Mountain Plover nests. An addi- eated with a meter stick, and coverage by vege- tional 24 nests were found between 22 May tation classes, including bare ground and grass, and 26 June 2003 (Fig. 1). Of 55 clutches, 51 2 was estimated for all 1.0-m plots. Nest plots (93%) had 3 eggs and 4 (7%) had 2 eggs. Pro- were compared to respective random plots using jected hatch date ranged from 6 June to 24 α Student’s t test ( = 0.05) for all nests. July 2002 and from 7 June to 7 July 2003. Evidences of disturbance regimes, including Average projected hatch date was 26 June grazing by wild or domestic ungulates, prairie 2002 and 21 June 2003. Egg hatch date was dog activity, or industrial development visible influenced by neither nest elevation (r2 = within 400 m of nest sites, were described. We 0.02, P = 0.36, n = 55) nor latitude (r2 = 0.05, also considered general topography at the nest P = 0.18, n = 41). site (i.e., plateaus versus open plains or basins). In 2002 we marked nests by placing a rock Hatch Success and Condition on the road shoulder immediately perpendic- of Unhatched Eggs ular to the nest. Distance from the road to the Eggs successfully hatched in 14 of 22 (64%) nest was paced and GPS coordinates were revisited nests in 2003 as indicated by the 226 WESTERN NORTH AMERICAN NATURALIST [Volume 65

± 2 TABLE 1. Comparison of mean grass and mean bare ground coverage (% sx–) of 1.0-m grassland and desert nest plots and 1.0-m2 random plots at 4 distances from nest or random start point. Plots sampled in 2002.

______GRASS COVERAGE ______Grassland sites (n = 18) ______Desert sites (n = 13) Nest plot Random plot Nest plot Random plot ta (P)b 0 m 13.9 ± 3.3 20.3 ± 3.0 8.5 ± 1.4 23.5 ± 7.3 –2.50 (0.02) 25 m 20.0 ± 2.4 19.7 ± 1.8 13.5 ± 3.3 19.2 ± 3.3 –0.86 (0.40) 50 m 19.0 ± 3.0 17.8 ± 1.7 15.8 ± 4.5 18.5 ± 4.1 0.27 (0.79) 100 m 19.4 ± 3.8 19.7 ± 4.6 16.5 ± 4.4 16.5 ± 3.8 0.20 (0.84)

______BARE GROUND COVERAGE ______Grassland sites (n = 18) ______Desert sites (n = 13) Nest plot Random plot Nest plot Random plot ta (P)b 0 m 47.2 ± 4.5 35.3 ± 4.4 61.2 ± 5.6 56.2 ± 8.3 1.53 (0.13) 25 m 42.2 ± 4.6 44.2 ± 3.3 60.0 ± 6.6 51.9 ± 3.7 1.10 (0.28) 50 m 56.9 ± 4.3 46.4 ± 3.8 63.9 ± 7.0 56.9 ± 6.8 1.09 (0.28) 100 m 48.9 ± 4.6 41.9 ± 5.4 56.9 ± 5.9 53.1 ± 6.7 0.36 (0.72) aDegrees of freedom range from 48 to 59. bReported t tests are for grassland and desert samples combined.

± 2 2 TABLE 2. Comparison of mean grass height ( sx–) in centimeters of 1.0-m grassland and desert nest plots and 1.0-m random plots at 4 distances from nest or random start point. Plots sampled in 2002.

______GRASS HEIGHT ______Grassland sites (n = 18) ______Desert sites (n = 13) Nest plot Random plot Nest plot Random plot ta (P)b 0 m 5.88 ± 0.57 7.39 ± 1.26 4.09 ± 0.58 7.00 ± 0.92 –2.14 (0.04) 25 m 6.67 ± 0.49 6.94 ± 0.60 6.00 ± 0.75 7.17 ± 0.51 –1.02 (0.31) 50 m 7.78 ± 0.61 6.61 ± 0.55 6.40 ± 0.82 6.75 ± 0.90 0.90 (0.37) 100 m 9.47 ± 1.67 6.47 ± 0.83 7.27 ± 1.57 8.80 ± 0.63 0.96 (0.34) aDegrees of freedom range from 40 to 55. bReported t tests are for grassland and desert samples combined.

presence of shell fragments in the nest cup. Of Nest Habitat Attributes the remaining 8 clutches, 5 were devoid of Bare ground was the largest component of eggshell fragments although predation could 1.0-m2 nest plots in both grassland and desert be confirmed in only 1 case. The remaining 3 areas (Table 1). Nest plots at 0 m had less grass clutches had been abandoned, and all eggs coverage (Table 1) and reduced grass height were collected. Also, 4 eggs were collected from (Table 2) than corresponding random plots in otherwise successful clutches. Nests were not all cases. There was no difference in grass cov- revisited in 2002. In total, 13 eggs were col- erage, bare ground coverage, or grass height lected from 6 nests and their contents exam- between nest plots and corresponding random ined. Shell thickness was not quantified, but 9 plots at distances ≥25 m. eggs had shells that appeared thinner than All grassland nest sites and most desert others and were noticeably fragile. Eight of nest sites showed evidence of grazing in 2002 the 13 were either infertile or had minimally and 2003, predominantly by domestic cattle developed embryos (<3 days). The remaining and sheep. Pronghorn and wild horses were 5 were moderately developed (≈8–17 days). also present at some sites. Prairie dogs were 2005] MOUNTAIN PLOVERS NESTING IN WYOMING 227 present on 17 of 32 grassland nest sites (53%; desert ground-nesters like the Mountain Plover black-tailed) and 3 of 23 desert sites (13%; because it boasts vast expanses of rangeland white-tailed). Thirty-four of 55 nests (62%) were where habitat is kept open through grazing. located on plateaus elevated at least 100 m above Although some studies have shown strong surrounding terrain. The remaining 21 nests selection for black-tailed prairie dog colonies occurred in broad basins or on high plains. by Mountain Plovers breeding at mixed-grass prairie sites (Knowles et al. 1982, Olson and DISCUSSION Edge 1985, Dinsmore et al. 2003), prairie dogs Hatch Success and Condition were absent at many of our Mountain Plover of Unhatched Eggs nest sites in Wyoming. Black-tailed prairie dogs were present at 53% of grassland sites and Our hatch rate across Wyoming was similar white-tailed prairie dogs at 13% of desert to Graul’s (1975) findings on the Pawnee Na- sites. Similarly, Parrish et al. (1993) reported tional Grassland, Weld County, Colorado, where that Mountain Plovers in the Powder River at least 1 egg hatched in 65% of 80 nests, and basin did not have a strong affinity for black- was higher than those reported by Knopf and tailed prairie dog towns on Thunder Basin Rupert (1996; 26%–50%), also on the Pawnee National Grassland, with only 1 of 15 nests National Grassland. Dinsmore et al. (2003) re- occurring on a town. Pervasive livestock grazing ported that at least 1 egg hatched in 58% of may be adequate at Wyoming sites to attract 600 monitored nests on the Charles M. Russell breeding plovers in the absence of prairie dog National Wildlife Refuge, Philips County, Mon- colonies. Alternatively, soil quality, precipita- tana. Mountain Plover nest failure is often attrib- tion levels, and vegetative cover may be ade- uted to predation or flooding (Miller and Knopf quately low to curb the need for additional 1993, Knopf and Rupert 1996, Dinsmore et al. landscape disturbance. 2003), and these variable nest success rates It is notable that 62% of nests found were might be expected as predator populations, hab- located on plateaus elevated at least 100 m itat quality, and climatic conditions fluctuate. above surrounding terrain, particularly since Nest Habitat Attributes most surveys were not conducted on plateaus. Mountain Plovers also select plateaus for nesting Results from this study are in accordance in Philips County, Montana (Knopf personal with previous reports that Mountain Plover communication 2003). Elevated plateaus may nesting habitat is typified by 27%–72% bare host a greater bare ground component than ground (Olson and Edge 1985, Parrish et al. the surrounding landscape due to increased 1993, Knopf and Miller 1994) and minimal wind scour and precipitation runoff. The Moun- grass coverage. Plovers have also been shown tain Plover’s tendency to nest on arid, elevated to use cultivated fields for nesting and brood- rearing (Knopf and Rupert 1999, Dreitz et al. plateaus further substantiates claims that the in press). On average, our nest plots were 53% bird is also a disturbed-desert species rather bare ground. This value is higher than results than a strict associate of the shortgrass prairie. from Colorado and Montana (32%) and is likely due to the large number of Wyoming nest sites LITERATURE CITED in xeric landscapes where bare ground accounts ALBERICO, J.A.R. 1995. Floating eggs to estimate incuba- for >50% of coverage at random sites and tion stage does not affect hatchability. Wildlife Soci- >60% of coverage at nest sites. ety Bulletin 23:212–216. Ungulate grazers were present at all grass- BEAUVAIS, G.P., AND R. SMITH. 2003. Model of breeding land and most desert sites. Thus, open-range habitat of the Mountain Plover (Charadrius montanus) livestock grazing is compatible with Mountain in western Wyoming. Western North American Nat- uralist 63:88–96. Plover reproduction (Kantrud and Kologiski DINSMORE, S.D, G.C. WHITE, AND F.L. KNOPF. 2003. 1982, Knopf 1996). When correctly managed, Annual survival and population estimates of Moun- open-range grazing emulates presettlement tain Plovers in southern Phillips County, Montana. conditions much more effectively than do urban Ecological Applications 13:1013–1026. DREITZ, V.J., M.B. WUNDER, AND F. L. KNOPF. 2005. Move- development and cultivation, both of which ment and home ranges of Mountain Plovers raising are more pervasive in surrounding states. Thus, broods in three Colorado landscapes. Wilson Bulletin: Wyoming is of unique value to shortgrass and In press. 228 WESTERN NORTH AMERICAN NATURALIST [Volume 65

ELLISON MANNING, A.E., AND C.M. WHITE. 2001. Breed- LAUN, H.C. 1957. A life history study of the Mountain ing biology of Mountain Plovers, Charadrius mon- Plover, Eupoda montana townsend, on the Laramie tanus, in the Uinta Basin. Western North American Plains, Albany County, Wyoming. Master’s thesis, Naturalist 61:223–228. University of Wyoming, Laramie. GRAUL, W.D. 1975. Breeding biology of the Mountain MABEE, T.J. 1997. Using eggshell evidence to determine Plover. Wilson Bulletin 87:6–31. nest fate of shorebirds. Wilson Bulletin 109:307–313. KANTRUD, H.A., AND R.L. KOLOGISKI. 1982. Effects of MILLER, B.J., AND F. L . K NOPF. 1993. Growth and survival soils and grazing on breeding birds of uncultivated of Mountain Plovers. Journal of Field Ornithology upland grasslands of the northern Great Plains. Un- 64:500–506. published report, United States Department of the OLSON, S.L., AND D. EDGE. 1985. Nest site selection by Interior, Fish and Wildlife Service. Mountain Plovers in north central Montana. Journal KNOPF, F.L. 1996. Mountain Plover (Charadrius montanus). of Range Management 38:280–282. In: A. Poole and F. Gill, editors, The Birds of North PARRISH, T.L., S.H. ANDERSON, AND W. F. O ELKLAUS.1993. America, No. 211. The Academy of Natural Sciences, Mountain Plover habitat selection in the Powder River Philadelphia, PA, and The Ornithologists’ Union, Basin, Wyoming. Prairie Naturalist 25:219–226. Washington, DC. PLUMB, R.E. 2004. Minimum population size and concen- KNOPF, F.L., AND B.J. MILLER.1994. Charadrius montanus— tration areas of Mountain Plovers breeding in Wyo- montane, grassland, or bare-ground plover? Auk ming. Master’s thesis, University of Wyoming, 111:504–506. Laramie. KNOPF, F.L., AND J.R. RUPERT. 1995. Habits and habitats of U.S. FISH AND WILDLIFE SERVICE 2002. Mountain Plover Mountain Plovers in California. Condor 97:743–751. survey guidelines. 28–35. ______. 1999. Use of cultivated fields by breeding Moun- Received 26 January 2004 tain Plovers in Colorado. Studies in Avian Biology Accepted 15 April 2004 19:81–86. KNOWLES, C.J., C.J. STONER, AND S.P. GIEB. 1982. Selec- tive use of black-tailed prairie dog towns by Moun- tain Plovers. Condor 84:71–74. Western North American Naturalist 65(2), © 2005, pp. 229–232

WHITE-BREASTED NUTHATCH (SITTA CAROLINENSIS) FECAL SAC DISPERSAL IN NORTHWESTERN NEVADA

Norman H. Weitzel1

ABSTRACT.—Field research on the dispersal of fecal sacs by parent White-breasted Nuthatches (Sitta carolinensis) was conducted on the eastern slopes of the Sierra Nevada in northwestern Nevada. Fecal sacs were dropped 6–60 m from the nest, with 56% of the total droppings (n = 66) being dropped 48–60 m away. Ninety-five percent of sac dispersal was in the southwest quadrant, the food-foraging site. Also, 75% of non-sac flights during the nestling phase were in the direction of the foraging area, a dead, mature Jeffrey pine (Pinus jeffreyi). Fecal sac dispersal by parent White- breasted Nuthatches may reduce or eliminate detection of nestlings by avian predators.

Key words: fecal sac dispersal, White-breasted Nuthatch, Sitta carolinensis, Nevada.

Fecal sac dispersal by parent White-breasted The White-breasted Nuthatches are year-round Nuthatches (Sitta carolinensis) has not been residents nesting in May. reported in the literature, although Tree Swal- Although observations and fecal sac counts lows (Tachycinete bicolor), White-crowned were made in 2001 and 2002, only in 2003 did Sparrows (Zonotrichia leucophrys), and East- I record accurate and reliable data to support ern Bluebirds (Sialia sialis) have been fre- this study. My observations during the nestling quently reported. phase (3–19 May) were made daily between Upon removal, fecal sacs can be consumed, 0700 and 1600 with 10 × 50 binoculars and a dropped, placed on substrate, or a combination 40-power spotting scope from the dining and of these possibilities. While many passerines great rooms of my home 34 m east of the nest. do not remove nestling feces, parent White- Also, observations were made from a blind 6 m breasted Nuthatches remove and disperse fecal southeast of the nest and another blind 26 m sacs away from the nest. Petit and Petit (1988) south of the nest. I was able to accurately count concluded that the significance of fecal sac and mark fecal sac droppings as or where they removal deserves attention in the future, and were dropped by making an extensive survey Lang et al. (2002) observed that this parental of bare ground, driveway and parking area, and behavior remains a neglected topic. mowed grasses in the remaining area (Fig. 1). The purpose of this study was to contribute The nest cavity was 2.7 m above the ground to our knowledge of fecal sac dispersal by par- in a dead, partially delimbed Jeffrey pine snag ent White-breasted Nuthatches during the 3.7 m in height. From the nest as point of origin, nestling stage. I established northwest, northeast, southwest, and southeast quadrants (Fig. 1). I recorded STUDY AREA AND METHODS the distance and direction of sac dispersal and tabulated flights with and without fecal sacs. This field study of fecal sac dispersal by parent White-breasted Nuthatches was made RESULTS AND DISCUSSION 19 km south of Reno, Nevada, at 1828 m elevation, on the eastern slopes of the Sierra Distance of Dispersal Nevada. Big sagebrush (Artemisia tridentata), Parent White-breasted Nuthatches dispersed mountain mahogany (Cercocarpus ledifolius), fecal sacs 6–60 m from the nest, with 56% of and other aridland vegetation give way to total droppings (n = 66) being dropped 48–60 m mature ponderosa pine (Pinus ponderosa) and away. Seventeen percent were dropped at the Jeffrey pine (Pinus jeffreyi) of higher elevation. end distance of 60 m (Fig. 2). This dropping

116805 Mt. Rose Highway, Reno, NV 89511.

229 230 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Fig. 1. Map of the White-breasted Nuthatch nest-foraging area, sac-dropping points, and quadrant origins at the White-breasted Nuthatch nest. distance was opposite of what I reported the southeast quadrant, 1% in the northwest (Weitzel 2003) in Western Bluebirds (Sialia quadrant, and 0% in the northeast quadrant mexicana), where 56% of the sacs were dropped (Fig. 3). In the southwest quadrant, a standing, within 20 m of the nest. I attributed this 3-year-dead, mature Jeffrey pine was the pre- greater dispersal distance by White-breasted dominant foraging site. It had an abundance of Nuthatches to nestling protection behavior by various stages of bark beetles, termites, ants, the parents because of common and ever-pre- bugs, and other insects, as well as arachnids sent predators: Black-billed Magpies (Pica and other arthropods. Parent White-breasted pica), Scrub Jays (Aphelocoma coerulescens), Nuthatches collected food items at the dead Steller Jays (Cyanocitta stelleri), and Euro- tree and delivered them to the nestlings. Most pean Starlings (Sturnus vulgaris). In my West- flights with and without fecal sacs were in the ern Bluebird field study, predators were absent. direction of the dead pine tree in the south- Tree Swallow parents dispersed fecal sacs 20– west quadrant (Fig. 3). I found that 95% of 50 m away (Weatherhead 1984), approximately fecal-sac flights and 75% of non-sac flights 40 m in Prothonotary Warblers (Protonotaria were in the direction of the foraging pine. All citrea; Petit and Petit 1987), and 91 m ± 11 m but 6 fecal sacs dropped in the southwest in Eastern Bluebirds (Lang et al. 2002). quadrant were within a narrow, 12-m, nest-to- foraging-pine corridor even though 65 other Direction of Dispersal pines grew there (Fig. 1). Most flights from the Ninety-five percent of total fecal sac dis- nest were to the foraging area during the nest- persals were in the southwest quadrant, 4% in ling phase in Western Bluebirds (Weitzel 2003). 2005] FECAL SAC DISPERSAL IN WHITE-BREASTED NUTHATCHES 231

Fig. 2. Distance of fecal sac droppings (n = 66) from the nest by White-breasted Nuthatches.

Fig. 3. Comparison of flights with and without fecal sacs by White-breasted Nuthatches

When a Tree Swallow made a sac-carrying flight, distance from the nest (Fig. 4). These data sug- it apparently flew to a foraging area after drop- gest that as the nestlings aged, parental invest- ping the fecal sac (Weatherhead 1984). Petit et ment increased and the brood became more al. (1989) suggested that when dispersing fecal valuable. Weitzel (2003) found this parental sacs, birds do not have to deviate from preferred behavior true in Western Bluebirds. foraging pathways. I did not observe any attempt Many passerines dispose of fecal sacs in var- by parent White-breasted Nuthatches to dis- ious patterns from the nest so as to reduce or perse sacs at random 360° around the nest. eliminate detection of nestlings by predators. As the nestlings aged from day 1 to day 16, The pattern depends on the species and eco- fecal sac droppings increased in number and logical factors such as the presence or absence 232 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Fig. 4. Distance of fecal sac droppings from hatching to fledging in White-breasted Nuthatches. (n) = number of sac droppings. of predators and a dependable food source. ______. 1988. Reply to Weatherhead: a problem of inter- Greater attention in field research is given to preting stated hypotheses rather than “intentions.” Condor 90:519–521. food items brought to the nest than to fecal PETIT, K.E., L.J. PETIT, AND D.R. PETIT. 1989. Fecal sac sacs brought out. Complete understanding of removal: do the pattern and distance of dispersal fecal sac dispersal requires future field studies. affect the chance of nest predation? Condor 91: 479–482. WEATHERHEAD, P.J. 1984. Fecal sac removal by Tree Swal- LITERATURE CITED lows: the cost of cleanliness. Condor 86:187–191. WEITZEL, N.H. 2003. Western Bluebird (Sialia mexicana) LANG, J.D., C.A. STRAIGHT, AND P.A. GOWATY. 2002. Obser- fecal sac dispersal at Kellogg, Oregon. Western North vations of fecal sac dispersal by Eastern Bluebirds. American Naturalist 63:268–270. Condor 104:205–207. PETIT, D.R., AND L.J. PETIT. 1987. Fecal sac dispersal by Received 30 December 2003 Prothonotary Warblers: Weatherhead’s hypothesis re- Accepted 2 June 2004 evaluated. Condor 89:610–613. Western North American Naturalist 65(2), © 2005, pp. 233–241

INFLUENCE OF SOIL WATER AVAILABILITY ON COMPETITION AMONG LEAFY SPURGE (EUPHORBIA ESULA) AND GRASSES

Matthew James Rinella1 and Roger Leslie Sheley2

ABSTRACT.—Some perturbations differentially influence invasive plant and grass production. For example, growth regulator herbicides and biological control agents can dramatically reduce leafy spurge production while having little or no influence on grass production, and overgrazing can reduce grass production while not substantially influencing leafy spurge production because cattle typically ingest little or no leafy spurge. To predict how grass production will respond to a perturbation that influences only leafy spurge and to predict how leafy spurge production will respond to a perturbation that affects only grasses, competitive relationships must be understood. Seeding mixtures of leafy spurge and 2 grasses were planted in experiments and grown for 127 days to determine whether different water application regimes influenced competition among these 3 species. Competition became less intense as the number of water applications increased. If this finding holds true under field conditions, then it indicates that competition is less intense in years and locations with numerous precipitation events. Competitive interactions (i.e., competition coefficients) were less variable when water was applied more frequently, but the ability of models to account for variation in plant weight (i.e., r2) was not influenced by the frequency of water application. This suggests that models will predict invasive plant and grass biomass with equal accuracy in years with few or many precipitation events. Competitive effects were similar regardless of grass species, which suggests that grasses might be considered collectively in predicting response to perturbations in the field.

Key words: competition, invasive plants, soil water, rangeland.

Competitive relationships between invasive conditions (Moloney 1990, Briones et al. 1998, plants and grasses partially regulate plant com- Keddy et al. 2000), the relationship between munity response to invasive plant management. competition intensity and plant productivity For example, the change in grass biomass pro- has been a point of contention between ecolo- duction that results from invasive plant con- gists (Grime 1973, Newman 1973, Reader et trol and the change in invasive plant biomass al. 1994). Grime (2001) believes the prepon- that results from grass seeding partially depend derance of evidence indicates a positive rela- on competition intensity. Therefore, incomplete tionship between competition intensity and understanding of competitive relationships will plant productivity. However, at least one elab- result in imprecise predictions of management- orate study suggests that wide productivity induced shifts in invasive plant and grass gradients are necessary to detect changes in abundances. competition intensity, and therefore variation Developing a more complete understand- in plant productivity might not strongly influ- ing of competitive relationships between inva- ence competition intensity within the produc- sive plants and grasses requires knowing if these tivity range that a single invasive plant species relationships vary temporally and/or spatially. occupies (Reader et al. 1994). If competitive relationships between invasive Water availability often governs plant pro- plants and grasses do vary temporally and spa- ductivity in the semiarid regions where many tially, a substantial portion of this variation is invasive plants occur, and water availability likely related to temporal and spatial variation varies with precipitation and soil water-hold- in plant productivity, which can be attributed ing characteristics (e.g., very coarse soils main- to variation in environmental conditions such as tain less plant-available water; Bailey 1979). nutrient and water availability (Grime 2001). The ability of soil to hold water is regulated by While it has been shown that some aspects soil type, landscape position, and soil manage- of plant competition do vary with environmental ment practices, among other factors (Afyuni et

1USDA-ARS, 243 Fort Keogh Road, Miles, City, MT 59301. 2Corresponding author: USDA-ARS, 67826-A Highway 205, Burns, OR 97720.

233 234 WESTERN NORTH AMERICAN NATURALIST [Volume 65 al. 1993, Gomez et al. 2002). If plant productiv- number of water applications (i.e., plant pro- ity (i.e., water availability) influences competi- ductivity). Because the factors that limit plant tion intensity between grasses and invasive growth are different at varying levels of water plants in semiarid regions, per-unit-biomass availability, we hypothesized that (3) the mag- competitive relationships will vary temporally nitude of variation in competitive relation- and spatially with plant-available soil water. ships would change with water availability. If Per-unit-biomass competitive relationships observed, this change would reflect different can also vary by species, and a single invasive magnitudes of variation in the underlying fac- plant species can grow in association with dif- tors that limit plant growth (e.g., soil nutrient ferent grasses within each of several habitat availability) at different levels of soil water. types it infests. For example, spotted knapweed (Centaurea maculata) grows in association with MATERIALS AND METHODS western wheatgrass (Agropyron smithii), Ken- Procedures tucky bluegrass (Poa pratensis), needle-and- thread (Stipa comata), blue grama (Bouteloua Plastic pots (7.6-L) were filled with a pas- gracilis), crested wheatgrass (Agropyron crista- teurized soil mixture containing equal parts of tum), rough fescue (Festuca scabrella), blue- a silt loam soil (classification unknown), washed bunch wheatgrass (Pseudoroegneria spicatum), concrete sand, and Canadian sphagnum peat prairie junegrass (Koeleria cristata), Idaho fes- moss. The wetting agent AquaGro® 2000 G was cue (Festuca idahoensis), and other grasses (Fay added at 0.5 kg ⋅ m–3, and the mixture was et al. 1991, Sheley et al. 2000). Studying com- steam pasteurized at 80°C. petitive relationships between spotted knap- Percent germination of leafy spurge, Ken- weed and each of these grasses would require tucky bluegrass, and western wheatgrass was resource-intensive experiments. The number estimated by sowing 30 seeds of each species of by-species competitive relationships that in 1-L pots in a greenhouse (1 pot per species). need to be estimated will further increase if Seeds were covered with approximately 2 mm per-unit-biomass competitive effects vary con- of soil, and the soil was misted with water siderably by species because some regions har- every other day for 20 days. We then calcu- bor many invasive plant species. Using a small lated the following ratio for each type of seed: number of grasses to study the magnitude of seedlings emerged:seeds planted. These ratios variation in by-species competitive effects will were used to adjust seeding rates and achieve elucidate the quantity of species-specific in- target plant densities. quiries needed to understand competition be- Target densities were 0, 670, 1340, and tween an invasive plant species and all grasses 2010 plants ⋅ m–2 for each species. Three addi- with which the invasive plant commonly co- tion series matrices consisting of all possible exists. seed density combinations were established (4 Our objective was to determine the influ- Kentucky bluegrass densities × 4 western wheat- ence of soil water on competition among leafy grass densities × 4 leafy spurge densities = 64 spurge, Kentucky bluegrass, and western pots per density matrix × 3 density matrices = wheatgrass in a greenhouse. Leafy spurge is a 192 pots per experiment) in the 7.6-L pots cool-season, nonnative, perennial invasive plant (Spitters 1983). These density matrices also that infests close to 1.2 million ha in 29 states contained between 2 and 8 isolated plants of in the USA (Lajeunesse et al. 1999). Kentucky each species (depending on survival). bluegrass is a cool-season, nonnative, peren- Density matrices were arranged in a com- nial grass that occurs throughout much of the pletely randomized design in a greenhouse. United States. Western wheatgrass is a native, Pots were periodically rearranged to average cool-season, rhizomatous, perennial grass that the influence of environmental gradients across occurs in many rangeland ecosystems of the all plants. Greenhouse photoperiod was ex- western United States and Canada (Taylor and tended to 14 hours with 1000-W metal halide Lacey 1994). These grasses often grow in asso- bulbs, and temperature was maintained at ciation with leafy spurge. approximately 22°C during the light period It was hypothesized that per-unit-plant- and 18°C during the dark period. Seeds were abundance competitive relationships would uniformly scattered over the soil surface and not vary (1) by grass species and (2) with the covered with about 2 mm of soil. To encourage 2005] COMPETITION OF LEAFY SPURGE AND GRASSES 235 germination, we misted the soil surface with from each measurement period were included water every other day for 27 days. After the until a pot received its final water application misting period (28 days after planting), all pots and pot matric pressure reached 1.5 MPa (per- were watered to capacity. Pots in 2 density manent wilting point). If pots did not reach matrices were watered to capacity 61 days 1.5 MPa by the end of the experiment, then all after planting, and 1 of these matrices was matric pressure measurements were included watered to capacity a 3rd time 94 days after in the average. planting. Hereafter, pots watered once, twice, Plant Data Analysis or 3 times will be said to have received dry, intermediate, or wet treatments, respectively. Plant data were fit to the following inverse After receiving final water applications, plants yield models by minimizing the sum of squared in the pots were harvested by clipping at the errors (Spitters 1983). soil surface upon showing signs of severe water stress, or 127 days after planting, whichever 1/pwls = B + Bls,den*denls occurred first. All plants were then dried to a + Bkb,bio*biokb + Bww,bio*bioww (1) ° constant weight at 50 C. The experiment was 1/pwkb = B + Bkb,den*denkb conducted during the winter of 1999 (run 1) + Bls,bio*biols + Bww,bio*bioww (2) and was repeated during the winter of 2000 (run 2). 1/pwww = B + Bww,den*denww + Bls,bio*biols + Bkb,bio*biokb (3) Soil Water Sampling Inverse plant weight was used to linearize To determine gravimetric water content, relationships. The subscripts ls, kb, and ww pots were weighed the day before each water- denote leafy spurge, Kentucky bluegrass, and ing, and pots that were watered were reweighed western wheatgrass, respectively. The response the day after watering. Pots were weighed variable 1/pw is the inverse of average individ- after harvest, and soil was removed and thor- ual plant weight per pot. Regression coeffi- oughly mixed. We took a uniform sample from cients without subscripts (Bs) are intercept each pot, each of which was weighed, dried to terms and Bs subscripted with den and bio are ° a constant weight at 50 C, and reweighed to competition coefficients that describe the in- determine soil dry weight (soil dry weight = fluence of plant density and biomass, respec- × post-harvest soil weight sample dry weight / tively. Density was used to describe intraspe- sample wet weight – pot weight). Two soil cific competition instead of biomass because samples were submitted to the Montana State of the complex relationship between pw and University Soil Testing Laboratory where pres- bio. Models were independently fit to data from sure plate analysis was used to determine grav- the dry, intermediate, and wet treatments to imetric water content at matric pressures of yield a total of 9 models (9 models = 3 water 0.01, 0.03, 0.1, 0.5, and 1.5 MPa. treatments × 3 species). Plant Sampling Regression coefficients of 1, 2, and 3 were compared to test the null hypothesis that per- Number of plants per pot of each species unit-plant-abundance competitive effects do was counted at harvest. Aboveground biomass not vary with the number of water applica- of each species was determined after plants tions and also to test the null hypothesis that were dried to a constant weight at 50°C. per-unit-plant-abundance competitive effects Soil Data Analysis do not vary by species. Density coefficients were compared within a species across water The van Genuchten (1980) water retention treatments, and biomass coefficients were com- relationship was fit to pressure plate analysis pared across species when comparing within a data by minimizing the sum of squared errors water treatment and within a species when (r2 = 0.98) to estimate the relationship be- comparing across water treatments. Standard tween matric pressure and gravimetric water deviations of regression coefficients were eval- content. An index of overall matric pressure uated to test the null hypothesis that the mag- was calculated by computing the average of nitude of variation in competitive relationships matric pressure measurements. Measurements would change with water availability. 236 WESTERN NORTH AMERICAN NATURALIST [Volume 65

The following model: Influence of Competition on Leafy Spurge ampsp = B + Bls, bio*biols + Individual Plant Weight B *bio + B *bio (4) kb, bio kb ww, bio ww Leafy spurge density became less nega- in which amp is an index of average matric tively related to leafy spurge individual plant pressure, was used to assess whether or not weight as the number of water applications the 3 species used the same amount of water increased in run 1 (Table 1), while the intensity in producing a unit of biomass. This model of this intraspecific competition was unrelated was fit to data from each water treatment to to water treatment in run 2. Kentucky bluegrass yield a total of 3 models. and western wheatgrass biomass negatively A bootstrap algorithm was used to compare affected leafy spurge plant weight in the dry and regression coefficients (Efron and Tibshirani intermediate treatments but did not negatively 1993, Hjorth 1994). Cases from data sets were affect plant weight in the wet treatment in run randomly selected with replacement and in- 1. The competitive effect of grasses on leafy serted into a bootstrap sample until the num- spurge did not vary significantly with water ber of cases was equal to the number of cases treatments in run 2, and per-unit-biomass effects in the original data set, and the model of inter- of Kentucky bluegrass and western wheatgrass est was then fit to the bootstrap sample to gen- on leafy spurge were similar to one another in erate least-squares estimates of X and Y. For both runs. this example, the variables X and Y are regression coefficients that are being compared, and Influence of Competition the least-squares estimate of X is greater than on Kentucky Bluegrass that of Y. These steps were repeated 1000 Individual Plant Weight times to generate vectors (x and y) of bootstrap Kentucky bluegrass density had a similar regression coefficient estimates with 1000 ele- negative effect on Kentucky bluegrass individ- ments. The number of cases in which xi > yj ual plant weight in the dry and intermediate was evaluated for i = 1, 2,…1000 and j = 1, treatments but had little or no effect in the 2,…1000. This resulted in x * y = 1,000,000 wet treatment in run 1 (Table 2). Kentucky blue- comparisons. The quantity (1 – (number of cases grass density had a negative effect on Ken- where xi > yj) / 1,000,000) * 2 is a 2-tailed tucky bluegrass plant weight in run 2, but the hypothesis test of HO: (X = Y). When regres- relationship was independent of water treat- sion coefficients were compared to 0, a similar ment. The effect of western wheatgrass and approach was used with each observation in leafy spurge biomass on Kentucky bluegrass the vector of bootstrap regression coefficient plant weight diminished as the number of water estimates compared to 0. P-values were calcu- applications increased in both runs. Western lated independently for each comparison and wheatgrass was more competitive with Ken- were not adjusted to provide “tablewise” or tucky bluegrass than was leafy spurge in both “experimentwise” error protection. runs. RESULTS Influence of Competition on Western Wheatgrass Regression coefficients in tables will be ref- Individual Plant Weight erenced without the letter B, the comma (,) will be replaced by a hyphen (-), and the coef- Western wheatgrass density had a greater ficients will not be subscripted. For example, negative effect on western wheatgrass individual plant weight in the dry and intermediate Bls,bio = ls-bio and Bls,den = ls-den. Because the dependent variable is inverse plant weight, treatments than in the wet treatment in both the magnitude of competition coefficients and runs (Table 3). Similarly, Kentucky bluegrass competition intensity is positively related. and leafy spurge became less competitive with In interpreting results it is important to western wheatgrass as the number of water remember that matric pressure is negatively applications increased in both runs. Kentucky related to soil water content. Therefore, as bluegrass was less competitive with western water availability decreases, matric pressure wheatgrass than was leafy spurge in the dry increases. and intermediate treatments in both runs, and 2005] COMPETITION OF LEAFY SPURGE AND GRASSES 237

TABLE 1. Competition coefficient estimates, r2, standard deviations (s) of coefficient estimates, and comparisons of coefficients at the 5% level of confidence. The coefficients are from a multiple linear regression model fit to data from a greenhouse study with inverse of leafy spurge individual plant weight as the dependent variable and leafy spurge plant density and western wheatgrass and Kentucky bluegrass plant biomass as the independent variables. Water Competition Coefficient Run treatment r2 coefficients estimates s Comparisons of regression coefficients ≠ 1 Dry 0.18 ls-den 0.38 0.16 =lsintermediate lswet ≠ Dry kb-bio 11.79 5.11 =wwdry =kbintermediate kbwet ≠ Dry ww-bio 5.82 4.74 =wwintermediate wwwet ≠ Intermediate 0.45 ls-den 0.26 0.17 lswet 1 Intermediate kb-bio 6.24 2.14 =wwintermediate kbwet Intermediate ww-bio 8.15 2.15 =wwwet Wet 0.34 ls-den –0.13 0.02 Wetkb-bio –0.23 0.23 =wwwet Wetww-bio –0.12 0.24

2 Dry 0.38 ls-den 0.56 0.21 =lsintermediate =lswet Dry kb-bio 9.74 5.06 =wwdry =kbintermediate =kbwet Dry ww-bio 22.00 5.62 =wwintermediate =wwwet ≠ Intermediate 0.53 ls-den 0.71 0.18 lswet Intermediate kb-bio 9.30 2.63 =wwintermediate =kbwet Intermediate ww-bio 14.64 2.40 =wwwet Wet 0.54 ls-den 0.25 0.26 Wetkb-bio 1.64 1.78 =wwwet Wetww-bio 1.86 1.90

TABLE 2. Competition coefficient estimates, r2, standard deviations (s) of coefficient estimates, and comparisons of coefficients at the 5% level of confidence. The coefficients are from a multiple linear regression model fit to data from a greenhouse study with inverse of Kentucky bluegrass individual plant weight as the dependent variable and Kentucky bluegrass plant density and western wheatgrass and leafy spurge biomass as the independent variables. Water Competition Coefficient Run treatment r2 coefficients estimates s Comparisons of regression coefficients ≠ 1 Dry 0.44 kb-den 0.62 0.23 =kbintermediate kbwet ≠ ≠ Dry ww-bio 11.58 3.87 =lsdry wwintermediate wwwet ≠ ≠ Dry ls-bio 24.50 6.64 lsintermediate lswet ≠ Intermediate 0.83 kb-den 0.33 0.04 kbwet ≠ Intermediate ww-bio 3.58 0.61 lsintermediate =wwwet ≠ Intermediate ls-bio 7.93 1.59 lswet Wet 0.47 kb-den 0.15 0.05 Wetww-bio 1.93 0.59 =wwwet Wetls-bio 2.91 1.59

≠ 2 Dry 0.60 kb-den 0.18 0.15 =kbintermediate kbwet ≠ ≠ ≠ Dry ww-bio 17.07 2.56 lsdry wwintermediate wwwet ≠ ≠ Dry ls-bio 46.99 9.17 lsintermediate lswet Intermediate 0.71 kb-den 0.20 0.05 =kbwet ≠ ≠ Intermediate ww-bio 4.71 0.53 lsintermediate wwwet ≠ Intermediate ls-bio 11.45 2.59 lswet Wet 0.41 kb-den 0.10 0.05 ≠ Wetww-bio 1.86 0.33 wwwet Wetls-bio 3.36 1.89 238 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 3. Competition coefficient estimates, r2, standard deviations (s) of coefficient estimates, and comparisons of coefficients at the 5% level of confidence. The coefficients are from a multiple linear regression model fit to data from a greenhouse study with inverse of western wheatgrass individual plant weight as the dependent variable and western wheatgrass plant density and leafy spurge and Kentucky bluegrass plant biomass as independent variables. Water Competition Coefficient Run treatment r2 coefficients estimates s Comparisons of regression coefficients ≠ ≠ 1 Dry 0.60 ww-den 0.37 0.07 wwintermediate wwwet ≠ Dry kb-bio 3.97 1.85 lsintermediate =kbintermediate =kbwet ≠ ≠ Dry ls-bio 13.58 2.08 lsintermediate lswet Intermediate 0.79 ww-den 0.21 0.02 =wwwet ≠ Intermediate kb-bio 1.28 0.19 lsintermediate =kbwet Intermediate ls-bio 2.49 0.41 =lswet Wet 0.57 ww-den 0.18 0.03 ≠ Wetkb-bio 1.09 0.18 lswet Wetls-bio –0.16 0.54

≠ ≠ 2 Dry 0.75 ww-den 0.55 0.06 wwintermediate wwwet ≠ ≠ ≠ Dry kb-bio 4.52 1.04 lsintermediate kbintermediate kbwet ≠ ≠ Dry ls-bio 17.62 3.65 lsintermediate lswet ≠ Intermediate 0.71 ww-den 0.32 0.03 wwwet ≠ Intermediate kb-bio 1.44 0.42 lsintermediate =kbwet ≠ Intermediate ls-bio 7.98 1.80 lswet Wet 0.69 ww-den 0.22 0.02 Wetkb-bio 1.02 0.22 =lswet Wetls-bio 2.70 1.11 this relationship was reversed in the wet treatment in run 2, leafy spurge used more water ment in run 1. Kentucky bluegrass and leafy in producing a unit of biomass than did the spurge had a similar competitive effect on grasses, and western wheatgrass used more western wheatgrass plant weight in the wet water in producing a unit of biomass than did treatment in run 2. Kentucky bluegrass. In the intermediate and wet treatments in run 1, leafy spurge used less Influence of Water Availability water in producing a unit of biomass than did on Variation in grasses, while the opposite was true for these Competition Intensity 2 treatments in run 2. With few exceptions, estimates of the standard deviation of competition coefficients de- DISCUSSION creased or stayed the same as the number of water applications increased. This indicates There are 2 prevalent competing theories that there was less variation in competitive regarding the influence of plant productivity effects when water was applied more frequently. on competition. One theory contends that com- On the other hand, there was no clear relation- petition becomes more intense as plant pro- ship between r2 of models and the number of ductivity increases because plant biomass water applications. Whereas the competitive increases, which results in increased competi- interactions were less variable when water was tion for light and space (Grime 1973, 2001, applied more frequently, factors not included Keddy 1989). The other theory predicts that in models 1, 2, and 3 (e.g., plant diseases and competition is similar in habitats with high genetics and nutrient availability) caused and low productivity because belowground greater random error when water was applied competition for nutrients is more intense in more frequently. habitats with low standing crop (Newman 1973, Wilson and Tilman 1991). In this view, the in- Influence of Plant Biomass tensity of above- and belowground competition on Average Matric Pressure is negatively related, so that net competition Leafy spurge and grasses had a similar intensity remains similar along productivity effect on average matric pressure in the dry gradients. Several field studies have relied on treatment in run 1 (Table 4). In the dry treat- the response of a target plant to removal of 2005] COMPETITION OF LEAFY SPURGE AND GRASSES 239

TABLE 4. Model r2 and coefficient estimates for multiple linear regression model with average matric pressure as the dependent variable and plant biomasses as independent variables in a greenhouse study.

Water______Regression coefficients Run treatment r2 kb-bio ww-bio ls-bio 1 Dry 0.37 –0.05aa 0.01a –0.02a Intermediate 0.40 0.09a 0.04a –0.03b Wet 0.37 0.09a 0.09a –0.01b

2 Dry 0.41 0.05a 0.16b 0.44c Intermediate 0.24 0.05a 0.06a 0.18b Wet 0.44 0.08a 0.14a 0.55b aCoefficients within a row that are followed by the same letter are not significantly different at the 5% level of confidence. surrounding vegetation as a measure of com- that competition intensity will decrease when petition intensity along productivity gradients, high supplies of new resources become avail- and differences in competition intensity have able (Huston and DeAngelis 1994). If compe- (Del Moral 1983, Reader and Best 1989) and tition does become less intense as the number have not (Wilson and Tilman 1991, 1993) been of precipitation events increases in the field, detected. competition between grasses and leafy spurge In this greenhouse study competition inten- is less intense in years and locations with both sity stayed similar or decreased as the number frequent and substantial precipitation events. of water applications (i.e., plant productivity) These greenhouse experiments contribute increased (Tables 1–3), and therefore the null to our ultimate goal of developing models that hypothesis that competition would be unaf- predict invasive plant and grass biomass re- fected by the frequency of water application is sponse to management strategies in the field. rejected. Competition staying similar is con- The fact that competition coefficient standard sistent with one of the prevalent theories that deviations tended to decrease as the number relates competition intensity to plant produc- of water applications increased suggests that tivity (Newman 1973, Wilson and Tilman 1991), models will predict plant biomass more accu- but an inverse relationship between competi- rately in wet years (Tables 1–3). However, there tion intensity and frequency of water applica- was no clear relationship between the impor- tion is inconsistent with both theories. This tance of competition (model r2) and the num- finding is also inconsistent with studies in which ber of water applications (Tables 1–3; Welden interspecific competition among 3 desert plants and Slauson 1986), which suggests that mod- and intraspecific competition of a desert annual els will account for variation in plant biomass intensified when water was added in the field equally well in years with few and many pre- (Kadmon 1995, Briones et al. 1998). All plants cipitation events. It appears that the influence were still quite small (<25 cm in height) by of competition became less variable when water the end of these greenhouse experiments, sig- was applied more frequently, but other factors nifying that competition for light may not have that cause variation in plant weight (disease, offset competition for water in treatments that genetics, nutrients) had a more pronounced resulted in high water availability (i.e., treat- effect when water was applied more frequently. ments with low seeding densities and 3 water The null hypothesis that variation in competi- applications). tion intensity is related to the number of water Competition intensity decreased when water applications is not rejected. supply was increased in a field experiment The competitive influence of Kentucky blue- that studied competition between tree seed- grass biomass on leafy spurge plant weight lings and herbaceous species (Davis et al. 1998), was similar to that of western wheatgrass bio- which is similar to the findings of these green- mass regardless of water treatment (Table 1). house experiments. One explanation for the The null hypothesis that per-unit abundance inverse relationship between competition in- competitive effects of the grasses are similar is tensity and water availability found in both not rejected. Biesboer et al. (1994) reported experiments is supplied by a theory predicting that 5 grasses did not affect leafy spurge shoot 240 WESTERN NORTH AMERICAN NATURALIST [Volume 65 weight in a greenhouse, but these grasses did field and greenhouse results are similar, results decrease root weight with the magnitude of from future greenhouse studies might be viewed the effect depending on the grass species. Dif- with more confidence. ferent grass species also affect leafy spurge aboveground biomass production differently LITERATURE CITED in the field (Ferrell et al. 1992, Biesboer et al. 1994, Lym and Tober 1997). However, unlike AFYUNI, M.M., D.K. CASSEL, AND W. P. R OBARGE. 1993. Effect of landscape position on soil water and corn the analysis reported in this manuscript, the silage yield. Soil Science Society of America Journal effect of a grass species was confounded by 57:1573–1580. the amount of biomass the species produced AGUIAR, M.R., W.K. LAUENROTH, AND D.P. PETERS.2001. in these studies, and all of the grasses may Intensity of intra- and interspecific competition in have competed similarly if competitive effects coexisting shortgrass species. Journal of Ecology 89: 40–47. were expressed on a per-unit-biomass basis. BAILEY, H.P. 1979. Semi-arid climates: their definition and Several studies support the theory that per- distribution. In: A.E. Hall, G.H. Cannell, and H.W. unit-biomass competitive effects of many plant Lawton, editors, Agriculture in semi-arid environ- species are similar (Goldberg 1987, Mitchell ments. Springer-Verlag, Berlin, Germany. BAKKE, A.L. 1936. Leafy spurge (Euphorbia esula L.). Iowa et al. 1999, Aguiar et al. 2001, Peltzer and Kochy Agricultural Experiment Station Research Bulletin 2001). If our results hold true in the field, 198:209–245. Kentucky bluegrass, western wheatgrass, and BIESBOER, D.D., B. DARVEAUX, AND KOUKKARI.1994. Con- probably other grasses may be considered col- trolling leafy spurge and Canada thistle by competitive species. Minnesota Department of Transportation, lectively in estimating the influence of grass St. Paul. 78 pp. production on leafy spurge production. BRIONES, O., C. MONTANA, AND E. EZCURRA. 1998. Com- Results from this greenhouse study might petition intensity as a function of resource availabil- improve our ability to predict the influence of ity in a semiarid ecosystem. Oecologia 116:365–372. environmental conditions on relationships DAVIS, M.A., K.J. WRAGE, AND P. B . R EICH. 1998. Competi- tion between tree seedlings and herbaceous vegeta- between invasive plants and grasses if conclu- tion: support for a theory of resource supply and sions can be extrapolated to natural condi- demand. Journal of Ecology 86:652–661. tions. However, conclusions should be viewed DEL MORAL, R. 1983. Competition as a control mechanism very cautiously because there are substantial in subalpine meadows. American Journal of Botany differences between greenhouse and field con- 70:232–245. EFRON, B., AND R. TIBSHIRANI. 1993. An introduction to ditions. An even-aged, somewhat even-sized the bootstrap. Chapman & Hall, New York. cohort of juvenile plants was used in this study, FAY, P.K., E.S. DAVIS, C.A. LACEY, AND T.K. CHICOINE. while most biomass is attributed to mature 1991. Chemical control of spotted knapweed (Cen- plants in the field. This resulted in a contrived taurea maculosa) in Montana. Pages 303–315 in L.F. James, J.O. Evans, M.H. Ralphs, and R.D. Child, partitioning of soil resources because leafy editors, Noxious range weeds. Westview Press Inc., spurge was not capable of accumulating re- Boulder, CO. sources from substantially deeper depths than FERRELL, M.A., T.D. WHITSON, D.W. KOCH, AND A.E. grasses, as is the case in the field (Bakke 1936). GADE. 1992. The control of leafy spurge (Euphorbia esula L.) by the interaction of herbicides and peren- Grasses and leafy spurge attained similar heights nial grasses. Pages I-54–I-56 in Research Progress in this study, while leafy spurge is usually Report, Western Society of Weed Science. taller than grasses in the field. Pots with high GOLDBERG, D.E. 1987. Neighborhood competition in an densities of leafy spurge may have misrepre- old-field plant community. Ecology 68:1211–1223. sented high-density patches of leafy spurge, be- GOMEZ, A., R.F. POWERS, M.J. SINGER, AND W.R. HORWATH. 2002. Soil compaction effects on growth of young cause leafy spurge may be a better competitor ponderosa pine following litter removal in Califor- for light under field conditions. Also, evidence nia’s Sierra Nevada. Soil Science Society of America suggests that shading can decrease plant water Journal 66:1334–1343. stress in dry soils, which indicates that compe- GRIME, J.P. 1973. Competitive exclusion in herbaceous vegetation. Nature 242:344–347. tition for water may diminish with plant ______. 2001. Plant strategies, vegetation processes, and height (Salisbury and Chandler 1993). Results ecosystem properties. 2nd edition. John Wiley & Sons from this study provide some insight into the Ltd., West Sussex, England. influence of water availability on competition HJORTH, J.S.U. 1994. Computer intensive statistical meth- between grasses and leafy spurge, but it will ods. Chapman & Hall, London, England. HUSTON, M.A., AND D.L. DEANGELIS. 1994. Competition be necessary to compare results to field exper- and coexistence: the effects of resource transport iment results to substantiate the findings. If and supply rates. American Naturalist 144:954–977. 2005] COMPETITION OF LEAFY SPURGE AND GRASSES 241

KADMON, R. 1995. Plant competition along soil moisture intercontinental study with Poa pratensis. Ecology gradients: a field experiment with the desert annual 75:1753–1760. Stipa capensis. Journal of Ecology 83:253–262. SALISBURY, C.D., AND J.M. CHANDLER. 1993. Interaction KEDDY, P., C. GAUDET, AND L.H. FRASER. 2000. Effects of of cotton (Gossypium hirsutum) and velvetleaf (Abu- low and high nutrients on the competitive hierarchy tilon theophrasti) plants for water is affected by their of 26 shoreline plants. Journal of Ecology 88:413–423. interaction for light. Weed Science 41:69–74. KEDDY, P.A.1989. Competition. Chapman & Hall, London, SHELEY, R.L., C.A. DUNCAN, M.B. HALSTVEDT, AND J.S. England. JACOBS. 2000. Spotted knapweed and grass response LAJEUNESSE, S., R. SHELEY, C. DUNCAN, AND R. LYM. 1999. to herbicide treatments. Journal of Range Manage- Leafy spurge. Pages 249–260 in R.L. Sheley and J.K. ment 53:176–182. Petroff, editors, Biology and management of noxious SPITTERS, C.J.T. 1983. An alternative approach to the analy- rangeland weeds. Oregon State University Press, sis of mixed cropping experiments. 1. Estimation of Corvallis. competition coefficients. Netherlands Journal of Agri- LYM, R.G., AND D.A. TOBER. 1997. Competitive grasses for cultural Science 31:1–11. leafy spurge (Euphorbia esula) reduction. Weed Tech- TAYLOR, J.E., AND J.R. LACEY. 1994. Range plants of Mon- nology 11:782–792. tana. Extension Bulletin 122, Montana State Univer- MITCHELL, R.J., B.R. ZUTTER, D.H. GJERSTAD, G.R. GLOVER, sity Extension Service, Bozeman. 124 pp. AND C.W. WOOD. 1999. Competition among sec- VAN GENUCHTEN, M.T. 1980. A closed-form equation for ondary-successional pine communities: a field study predicting the hydraulic conductivity of unsaturated of effects and responses. Ecology 80:857–872. soils. Soil Science Society of America Journal 44: MOLONEY, K.A. 1990. Shifting demographic control of a 892–898. perennial bunchgrass along a natural habitat gradi- WELDEN, C.W., AND W.L. SLAUSON. 1986. The intensity of ent. Ecology 71:1133–1143. competition versus its importance: an overlooked NEWMAN, E.I. 1973. Competition and diversity in herba- distinction and some implications. Quarterly Review ceous vegetation. Nature 244:310–311. of Biology 61:23–43. PELTZER, D.A., AND M. KOCHY. 2001. Competitive effects WILSON, S.D., AND D. TILMAN. 1991. Components of plant of grasses and woody plants in mixed-grass prairie. competition along an experimental gradient of nitro- Journal of Ecology 89:519–527. gen availability. Ecology 72:1050–1065. READER, R.J., AND B.J. BEST. 1989. Variation in competi- ______. 1993. Plant competition and resource availability tion along an environmental gradient: Hieracium in response to disturbance and fertilization. Ecology floribundum in an abandoned pasture. Journal of 74:599–611. Ecology 77:673–684. READER, R.J., S.D. WILSON, J.W. BELCHER, I. WISHEU, P.A. Received 16 September 2003 KEDDY, D. TILMAN, E.C. MORRIS, ET AL. 1994. Plant Accepted 7 October 2004 competition in relation to neighbor biomass: an Western North American Naturalist 65(2), © 2005, pp. 242–247

NUTRIENT RELATIONSHIPS BETWEEN OROBANCHE FASCICULATA NUTT. AND ITS HOST ARTEMISIA PYGMAEA GRAY IN THE UINTA BASIN OF UTAH, USA

Jack D. Brotherson1,3, Brenda T. Simmons2, Terry Ball4, and W. Ralph Anderson1

ABSTRACT.—Patterns of mineral nutrient uptake and distribution within the roots, stems, and leaves of Artemisia pygmaea and in the vascular parasite Orobanche fasciculata were investigated. All nutrients studied were magnified over concentrations found in the soil into the host and parasite. Nitrogen, phosphorus, potassium, and zinc were magnified along the flow gradient of soil-roots-stems-leaves of the host. All others increased in the roots and then decreased in the stems and leaves. Orobanche fasciculata concentrated phosphorus, potassium, and sodium over soil and root concentrations while excluding to some degree all others.

Key words: Orobanche fasciculata, Artemisia pygmaea, mineral nutrient uptake, host and parasite interaction.

Orobanche fasciculata Nutt. (clustered can have primary and secondary haustoria, the broomrape or clustered cancerroot) belongs to former located where the shoot of the parasite the Orobanchaceae or broomrape family, mem- emerges and the latter where the roots from bers of which are parasitic on the roots of the parasite attach to the roots of the host. Par- flowering plants (Reuter 1986, Welsh et al. 1993, asites that develop more advanced haustoria Wolfe and dePamphilis 1997). The genus have little or no root system. Such is the case Orobanche contains over 100 species (Parker with O. fasciculata (Kuijt 1969). The main pur- and Riches 1993), all of which are annual or pose of the haustorium is uptake of water, monocarpic (Kuijt 1969), obligate, herbaceous organic compounds, and mineral nutrients from parasites (Parker and Riches 1993). Orobanche the host plant. fasciculata parasitizes a variety of host species, Orobanche species are found in over 58 especially species of Artemisia (Welsh et al. countries, with some species having large pop- 1993). It is purplish to yellowish in color and ulations in areas of intensive agriculture (Jor- grows in a split stem to between 5 cm and 10 dan and Nile River valleys) and other species cm above the soil surface (Welsh et al. 1993). being endemic to small, localized areas (Sauer- Seeds of Orobanche spp. germinate after born 1991). Generally, they grow in infertile being stimulated chemically from 1 to 2 weeks soils, such as the alkaline soils of the Middle by exudates from the host’s root (Sauerborn East. Few Orobanche species grow in acidic 1991, Parker and Riches 1993). Upon germi- soils, as the lower pH causes the seeds to ger- nation Orobanche seed develops a radicle that minate at distances so far from the host that grows in the direction of the chemical stimuli contact between parasite seedling and host of the host’s root. This distance is generally root is not accomplished, thus resulting in the not more than a few centimeters from the seedling’s eventual death (Parker and Riches Orobanche seed. Once the radicle reaches the 1993). Most Orobanche species are found in the host root, a haustorium (that part of the para- Mediterranean region with its characteristic site that grows inside the host) is produced, climate, but are also found in humid, subtropi- which attaches the Orobanche seedling to the cal, arid, semiarid, and temperate climates. They host. The haustorium is also the site where the are associated with both irrigated and nonirri- bud and shoot of the parasite emerge and gated lands (Sauerborn 1991). Orobanche fasci- elongate (Parker and Riches 1993). A parasite culata is endemic to North America, ranging

1Department of Integrative Biology, Brigham Young University, Provo, UT 84602. 2275 West Juniper Avenue #1073, Gilbert, AZ 85233. 3Corresponding author: 435 WIDB, Department of Integrative Biology, Brigham Young University, Provo, UT 84602. 4Department of Ancient Scripture, Brigham Young University, Provo, UT 84602.

242 2005] NUTRIENT DYNAMICS BETWEEN OROBANCHE AND ARTEMISIA 243 in distribution from the Yukon Territory, south of Hill Creek. The study site covers 0.8–1.2 ha to Mexico, east to Michigan, and west to Cali- and is located on highly clay loam Green fornia. Within this range, O. fasciculata is asso- River shale soils underlain by fractured sand- ciated with sand dune ecosystems, arid shrub- stone layers called Hill Creek Rock, which has lands and grasslands, pinyon/juniper wood- been mined and used as ornamental building lands, aspen, and fir communities up to 3260 m material. Artemisia pygmaea is the dominant in elevation (Reuter 1986, Welsh et al. 1993). shrub on the site, although its population den- However, O. fasciculata is an uncommon spe- sities are low. Low-growing shrubs and grasses cies. As such, several states have listed it as including Eriogonum corymbosum, Elymus spi- rare (Indiana and the province of Ontario), catus, Atriplex confertifolia, Stipa, hymenoides, threatened (Wisconsin and Michigan), and even and Artemisia tridentata dominate areas adja- endangered (Illinois; Sheviak 1978, Bacone cent to the study area (Brotherson 1967). and Hedge 1980, Argus and White 1982, Soils are shallow, sandy clay loams, residual Brynildson and Alverson 1982, Beaman et al. in nature, sandstone based, and rocky. Calcare- 1985). No listing of O. fasciculata as threat- ous and basic, they contain elevated levels of ened or endangered is known in Utah. soluble salts in the upper 46 cm of the soil Other than taxonomic studies, little research profile. Clay increases with depth to 15 cm has been done on O. fasciculata. Reuter (1986) and then decreases. Cation exchange capacity studied the habitat and reproductive ecology ranges from 20 to 25 meq per 100 grams of of O. fasciculata in a sand dune ecosystem in soil and increases with depth. Calcium, potas- Wisconsin. She concluded that O. fasciculata sium, and sodium concentrations decrease with has the ability to reproduce parthenogeneti- depth while magnesium increases (Brotherson cally, that it produces many seeds which dis- 1967). Macronutrient concentrations are low perse across long distances and yet as a species (<215 ppm), with nitrogen, phosphorus, potas- would be considered uncommon, a fact thought sium, and sodium being the lowest. Micro- to be associated with parasite seed dispersal nutrients were more abundant than macro- and host growth dynamics. nutrients. Artemisia pygmaea Gray, or pygmy sage- The area receives between 30 and 40 cm of brush, is found in Arizona, Nevada, and Utah rain annually, 10–20 cm falling as snow from growing in shallow, infertile calcareous soils October to April and 10–20 cm from summer (Ward 1953). It has been collected in 13 coun- thunderstorms between May and September. ties from Utah’s desert and mountainous During the winter months temperature lows regions where it grows on clay loam soils asso- average between –18° and –16°C, while mean ciated with Green River shale, igneous and highs range from –2° to 0°C. In the summer calcareous gravels, and dolomitic outcrops or lower temperatures average 9° to 13°C and gravels (Welsh et al. 1993). A dwarf shrub the highs range from 27° to 31°C (Greer et al. (0.5–2 dm tall), A. pygmaea grows in patches 1981). and is not useful as browse (McArthur et al. The study site has had a grazing history of 1979). Welsh et al. (1993) indicate A. pygmaea primarily wild horses, mule deer, and rabbits. is often associated with rare plant species, such Occasional sheep and cattle grazing has also as O. fasciculata. occurred. The purpose of this study is to analyze the host-parasite relationships between A. pygmaea METHODS Gray and O. fasciculata Nutt. regarding nutrient Field Methods uptake and transfer between host and parasite on populations found in the Uinta Basin of Data were taken in August 1986 and 1987. Utah, USA. Data taken during 1986 reflect nutrient flows from the soil to A. pygmaea roots to O. fascicu- STUDY SITE lata. The 1987 samples include data taken to reflect nutrient flows from soil to roots to stems The study site is located 20.5 km (33 miles) and leaves of the host plants along with the south of Ouray, Utah, on the Ute Indian Reser- soil-root-parasite relationship. We collected a vation in Duchesne County. The site is on a total of 20 soil samples, 10 per year. Fifty-eight gentle 2%–3%, west-facing slope on the plateau plant samples were also collected during the 244 WESTERN NORTH AMERICAN NATURALIST [Volume 65

2-year study, 20 in 1986 and 38 in 1987. Those the means of each element to identify any that taken in 1986 include 10 of A. pygmaea roots varied significantly in concentration between and 10 of O. fasciculata; the 1987 samples mir- the soil, A. pygmaea plant parts, and O. fascic- rored the 1986 samples with the addition of 9 ulata. The results were then analyzed to deter- stem and 9 leaf samples of A. pygmaea. Plant mine the amount of each element that O. fas- and soil samples were collected as a set, with ciculata was taking from the roots of A. pyg- the plants sampled being randomly selected maea and the concentrations of each nutrient from across the study site with the use of a along the gradient (i.e., from roots to stems to random numbers table. Once the plants to be leaves) of A. pygmaea. Plant nomenclature fol- sampled were selected, a soil sample was col- lows Welch et al. 1993. lected within the root zone and packaged for transport to the laboratory for later analysis to RESULTS AND DISCUSSION determine available nutrients for the plant. Plant samples were divided into roots, stems, Mean ion concentrations (ppm) for each leaves, and associated parasites and were indi- nutrient studied in the soil, in the roots, stems, vidually packaged in air-breathing bags for and leaves of A. pygmaea, and in O. fasciculata transport to the laboratory where they were are found in Table 1. This table shows patterns dried at room temperature (23°C) in a Napco of nutrient enrichment with respect to ion model 630 drying oven. movement from soil to A. pygmaea roots then to stems and leaves, and from soil to A. pyg- Lab and Statistical Methods maea roots to parasite. The soil nutrient concentration levels (macro- and micronutrients) All soil and plant samples collected from were low, reflecting the poor quality of the the field were analyzed by the Brigham Young soil. Nitrogen, phosphorus, potassium, and zinc University Soil and Plant Analysis Laboratory showed an increase in concentration along the for nutrient content of both macro- and micro- flow gradient in A. pygmaea. Magnesium, iron, nutrients in 1990. Macronutrients analyzed and manganese increased through the stems were nitrogen (N), phosphorus (P), potassium and then decreased in the leaves to concentra- (K), calcium (Ca), sodium (Na), and magnesium tions less than the roots. Such selective exclu- (Mg). Micronutrients were zinc (Zn), iron (Fe), sion of magnesium and iron may be related to manganese (Mn), and copper (Cu). Exchange- high potassium levels in the leaf in that ele- able calcium, magnesium, potassium, and sodi- vated levels of potassium have been shown to um in the soil were extracted using a buffered induce deficiencies in these ions. The low lev- neutral 1.0 normal ammonium acetate solution els of manganese may be due to A. pygmaea’s (Jackson 1958, Hesse 1971, Jones 1973). DTPA selective exclusion of manganese along with a (diethylene-triaminepentaacetic acid) was used decreased capacity to translocate manganese to extract iron, zinc, manganese, and copper from stems to leaves (Treshow 1970). from the soil (Lindsay and Norvell 1969). Soil Calcium and sodium increased from the phosphorus and nitrogen were determined soil to the roots and then decreased or re- using sodium bicarbonate and macro-Kjeldahl mained static, respectively, as they flowed from procedures, respectively (Olsen et al. 1954, the stems to the leaves. Individual element Jackson 1958). uptake can often be inhibited by the presence Individual plant samples were ground and of other elements (Bargagli 1998). The signifi- passed through a 20-mm-mesh screen using a cant decrease of calcium may be due to high Thomas-Wiley mill. Ion concentrations of nitro- potassium levels, which have been shown in gen, phosphorus, potassium, calcium, magne- some plants to impair calcium absorption. The sium, sodium, iron, zinc, manganese, and cop- 2 ions may compete for common transport per in the plant tissue were identified using mechanisms in membranes and on transport procedures described by Graham et al. (1970). proteins (Bargagli 1998). Potassium, which acts Mean concentrations, standard deviations, with sodium or even substitutes for it, may minimums, and maximums were calculated for unbalance calcium to sodium ratios. If ratios of each element analyzed in both the soil and potassium or sodium to calcium are too high, plant material. Tukey’s Honestly Significant calcium deficiency may be induced (Treshow Difference (HSD) tests were conducted on 1970). Copper increased in concentration in 2005] NUTRIENT DYNAMICS BETWEEN OROBANCHE AND ARTEMISIA 245

TABLE 1. Means (ppm) and significant differences in nutrient concentrations for plant parts and the soil. All values are significantly different (P ≤ 0.05) from each other unless otherwise noted.* Nutrient Soil Root Stems Leaves O. fasciculata Nitrogen 6 7200 8800 12200 4600 Phosphorus 7 400 600 700 1000 Potassium 214 4400 c 8900 cf 12600 f 19600 Calcium 9116 a 28500 g 23100 fg 16700 fi 13300 ai Sodium 30 bj 1000 300 fj 300 bf 1600 Magnesium 900 7400 ec 8800 cf 6000 efi 3600 i Zinc 0.41 24 c 37 cf 33 f 18 Iron 11 2242 c 2834 c 1260 i 1196 i Manganese 11 66 e 101 63 ei 43 i Copper 3 22 15 fh 18 f 13 h Macronutrients* 10300 41400 edg 41200 fgh 35700 efi 38100 dhi Micronutrients 26 2355 g 2977 g 1374 fi 1269 i

*Values are not significantly different between the following: a = soil – Orobanche f = stems – leaves b = soil – roots g = stems – roots c = roots – stems h = stems – Orobanche d = roots – Orobanche i = leaves – Orobanche e = roots – leaves j = stems – soil

TABLE 2. Ratios (ppm plant part/ ppm soil) between each plant part of A. pygmaea compared with the soil for all nutrients. For example, a ratio of 1200 indicates that A. pygmaea roots have that much greater concentration of a nutrient than found in the soil. Nutrient Root O. fasciculata Stem Leaves Nitrogen 1200 767 1467 2033 Phosphorus 57 143 86 100 Potassium 21 92 42 59 Calcium 3 1 3 2 Sodium 33 53 10 10 Magnesium 8 4 10 7 Zinc 59 44 66 80 Iron 204 109 258 115 Manganese 6 4 9 6 Copper 7 4 5 6 Macronutrients 4 4 4 4 Micronutrients 91 49 115 5

the roots, decreased in the stems, and then enhanced when these ions exist in the divalent showed a slight increase again in the leaves. form, a form that allows them to adhere more Table 1 illustrates the relationship between strongly to roots. nutrient concentrations in the soil and corre- Table 2 also shows that although nutrients sponding nutrient concentrations in the roots are higher in O. fasciculata than in the soil, of A. pygmaea and in the parasite O. fascicu- this parasite does exclude some nutrients over lata. As shown, nutrient levels in the plant others. For example, O. fasciculata takes up mirror nutrient levels in the soil. In other calcium on a 1:1 ratio with the soil (Table 2). words, if nutrient concentrations are high in This is probably due to interactions between the soil, they will be correspondingly high in high levels of sodium and potassium, which the plant tissues. This phenomenon, termed have been shown to inhibit calcium absorption luxury consumption, asserts that a plant will in other plants (Boynton and Burrell 1944). absorb and accumulate more nutrients than it Compared with A. pygmaea roots, O. fasci- needs simply because the nutrients are more culata absorbed significantly higher concen- abundant in the soil (Treshow 1970, Brother- trations (x– = 2.83 times) of phosphorus, potas- son 1992). Further, the uptake of the micronu- sium, and sodium. Otherwise, O. fasciculata trients zinc, iron, manganese, and copper is contained the lowest concentrations (x– = 0.59 246 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 3. Ratios (ppm/ppm) of mineral nutrient concentrations in the soil and plant parts according to nutrient flow from the soil to roots to stems to leaves and to Orobanche fasciculata. Nutrient Roots/Soil Stems/Roots Leaves/Stems Orobanche/Roots Nitrogen 1200 1.22 1.39 0.64 Phosphorus 57 1.5 1.17 2.5 Potassium 21 2.02 1.42 4.45 Calcium 3 0.81 0.72 0.47 Sodium 33 0.3 1 1.6 Magnesium 8 1.2 0.68 0.49 Zinc 59 1.13 1.22 0.75 Iron 195 1.26 0.44 0.53 Manganese 6 1.53 0.62 0.65 Copper 8 0.68 1.2 0.59 Macronutrients 4 1 0.87 0.92 Micronutrients 91 1.26 0.05 0.54

Fig. 1. Ratio of nutrients in Orobanche fasciculata compared with nutrient levels in Artemisia pygmaea roots. times) of all other macro- and micronutrients important to Orobanche’s physiology. Phos- (N, Ca, Mg, Zn, Fe, Mn, and Cu; Table 3). phorus, for example, is a major component of Concentrations of all nutrients were signifi- adenosine triphosphate (ATP), which must be cantly different (P < 0.05) between roots of A. present in high amounts to provide energy for pygmaea and O. fasciculata. Differences be- nutrient uptake. Potassium and sodium would tween nutrient concentrations in O. fascicu- likely be absorbed in high quantities because lata and other plant organs also existed. How- they act in osmotic regulation of cellular fluids ever, such differences appear to be of little and produce an osmotic potential in the body value in explaining patterns of nutrient uptake of the parasite that when in combination with in the parasite since it parasitizes roots only. the parasite’s production of mannitol will aid Table 3 presents the nutrient concentration in the uptake of all other needed nutrients gradients (i.e., parasites to root, stem to root, (Parker and Riches 1993). Without such en- and leaf to stem ratios) of A. pygmaea and O. hancement of the parasite’s osmotic potential, fasciculata according to the path of nutrient the parasite would be unable to take up enough flow. All nutrient concentration gradients show nutrients for its survival. In contrast to A. pyg- a negative relationship (<1.0) between host maea, O. fasciculata is very selective in its roots and parasite except for phosphorus, nutrient uptake, as is illustrated by its exclud- potassium, and sodium (Table 3). Magnifica- ing or reducing uptake of major quantities of tion of these nutrients by the parasite may be most of the sampled nutrients in the study luxury consumption or it may be that they are (Fig. 1). 2005] NUTRIENT DYNAMICS BETWEEN OROBANCHE AND ARTEMISIA 247

For example, Orobanche species are lim- GRAHAM, R.D., C. LLANO, AND A. ULRICO. 1970. Rapid ited in their use of inorganic nitrogen (NO ) preparation of plant samples for cation analysis. 3 Communications in Soil Science and Plant Analysis because they do not synthesize nitrate reduc- 1:373–382. tase (Parker and Riches 1993). Instead, O. fas- GREER, D.C., K.D. GURGEL, H.A. CHRISTY, AND G.B. PETER- ciculata and other Orobanche spp. utilize SON. 1981. Atlas of Utah. Weber State College, Ogden, ammonium nitrogen, which can be metabo- UT, and Brigham Young University Press, Provo, UT. lized with glutamine synthetase in the GS1 300 pp. HESSE, P.R. 1971. Textbook of soil chemical analysis. form. It is also presumed that these parasites William Clowes and Sons, Ltd., London. 520 pp. can obtain their necessary amino acids directly JACKSON, M.L. 1958. Soil chemical analysis. Prentice-Hall, from the host’s xylem and phloem (Parker and Inc., Englewood Cliffs, NJ. 498 pp. Riches 1993). The nitrogen balance between JONES, J.B. 1973. Soil testing in the United States. Com- munications in Soil Science and Plant Analysis 4: A. pygmaea and O. fasciculata is delicate as 307–322. increased nitrogen levels in the host plant KUIJT, J. 1969. The biology of parasitic flowering plants. would allow the host to reverse the osmotic University of California Press, Berkeley and Los potential in favor of itself, thus decreasing the Angeles. 246 pp. vigor and even killing the parasite (Sauerborn LINDSAY, W.L., AND W.A. NORVELL. 1969. Equilibrium relationships of Zn2+, Fe3+, Ca2+ and H+ with 1991). EDTA and ETPA in soil. Soil Society of America Host plants can be damaged or even killed Proceedings 33:62–68. when parasitized by Orobanche spp. When MCARTHUR, E.D., A.C. BLAUER, A.P. PLUMMER, AND R. heavily parasitized, host plant growth declines STEVENS. 1979. Characteristics and hybridization of important Intermountain shrubs. III. Sunflower fam- or even stops and severe wilting occurs in some ily. Research Paper INT-220, USDA Forest Service, instances (Sauerborn 1991). Biomass produc- Intermountain Forest and Range Experiment Sta- tion has been shown to be severely reduced or tion, Ogden, UT. 82 pp. even eliminated in crop plants when heavily OLSEN, S.R., C.V. COLE, F.S. WATANABE, AND L.A. DEAN. parasitized by Orobanche (Sauerborn 1991). 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular 939. LITERATURE CITED PARKER, C., AND C.R. RICHES. 1993. Parasitic weeds of the world: biology and control. CAB International, Wall- ARGUS, G.W., AND D.W. WHITE. 1982. The rare vascular ingford, Oxon, UK. plants of Ontario. Syllogeus series 14. Botany Divi- REUTER, B.C. 1986. The habitat, reproductive ecology and sion, National Museum of Natural Sciences, Ottawa, host relations of Orobanche fasciculata Nutt. (Oro- Canada. 63 pp. banchaceae) in Wisconsin. Bulletin of the Torrey BACONE, J.A., AND C.L. HEDGE. 1980. A preliminary list Botanical Club 113:110–117. of endangered and threatened plants in Indiana. SAUERBORN, J. 1991. Parasitic flowering plants: ecology Proceedings of the Indiana Academy of Science 89: and management. Margraf Scientific Books, Weiker- 359–371. sheim, Germany. 127 pp. BARGAGLI, R. 1998. Trace elements in terrestrial plants: an SHEVIAK, C.J. 1978. Proposed list for state endangered/ ecophysiological approach to biomonitoring and threatened status plants. Natural Land Institute, biorecovery. Springer-Verlag, Georgetown, TX. 324 Rockford, IL. pp. TRESHOW, M. 1970. Environment and plant response. BEAMAN, J.H., E.A. BOURDO, F.W. CASE, S.R. CRISPIN, D. McGraw-Hill Book Company, New York. 422 pp. HENSON, R.W. PIPPEN, A.A. REZNICEK, ET AL. 1985. WARD, G.H. 1953. Artemisia, section Seriphidium, in North Endangered and threatened vascular plants in Michi- America: a cytotaxonomic study. Contributions from gan. II. Third biennial review proposed list. Michigan the Dudley Herbarium 4:155–205. Botany 24:99–116. WELSH, S.L., N.D. ATWOOD, S. GOODRICH, AND L.C. HIG- BOYNTON, D., AND A.B. BURRELL. 1944. Potassium-induced GINS. 1993. A Utah flora. Brigham Young University magnesium deficiency in the McIntosh apple tree. Press, Provo, UT. 986 pp. Soil Science. 58:441–454. WOLFE, A.D., AND C.W. DEPAMPHILIS. 1997. Alternate BROTHERSON, J.D. 1967. A study of certain community re- paths of evolution for the photosynthetic gene rbsL lationships of Eriogonum corymbosum Benth. in DC in four nonphotosynthetic species of Orobanche. in the Uinta Basin, Utah. Unpublished master’s the- Plant Molecular Biology 33:965–977. sis, Brigham Young University, Provo, UT. ______. 1992. Mineral-nutrient concentrations in the Received 5 February 2002 mountain mahogany species Cercocarpus montanus Accepted 20 August 2004 and Cercocarpus intricatus and in their associated soils. Journal of Plant Nutrition 15:49–67. 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PILFERING OF STORED SEEDS AND THE RELATIVE COSTS OF SCATTER-HOARDING VERSUS LARDER-HOARDING IN YELLOW PINE CHIPMUNKS

Stephen B. Vander Wall1, Elaine C. H. Hager1, and Kellie M. Kuhn1

ABSTRACT.—Yellow pine chipmunks (Tamias amoenus) scatter-hoard food during summer and autumn but must form a larder as a winter food source before winter begins. Yellow pine chipmunks do not larder-hoard large quantities of food during the summer, apparently because a summer larder could not be defended from pilferers. We tested the assumption that the rate of pilferage from an unguarded larder would be significantly greater than the rate of pilferage from surface caches (which are also unguarded by yellow pine chipmunks) during the summer and autumn. Buried plastic buckets were used as artificial nests containing larders of 1000 sunflower seeds or 200 Jeffrey pine (Pinus jeffreyi) seeds. The pilferage of larder contents was monitored daily and compared to pilferage of surface caches. Animals (yellow pine chipmunks and deer mice, Peromyscus maniculatus) removed sunflower seeds from caches much faster than from larders, but caches of Jeffrey pine seeds disappeared much more slowly than pine seeds in larders. Further, animals removed pine seeds from larders more quickly than they did sunflower seeds from larders. The difference between seed species was probably because sunflower seeds have much stronger odors, which rodents readily detect, and because chipmunks prefer pine seeds over sunflower seeds. Yellow pine chipmunks must spend a considerable portion of their time foraging for seeds and may not be able to defend a large larder during summer.

Key words: food storage, granivory, Peromyscus maniculatus, pilferage, Tamias amoenus.

Food storage takes 2 general forms. Larder- has led to a wealth of studies that have exam- hoarding is the accumulating of a relatively ined cache spacing (Stapanian and Smith 1978, large quantity of food at one or a few locations Clarkson et al. 1986), cache retrieval (Sherry as the result of numerous foraging excursions. et al. 1981, Brodin 1994), cache pilferage (Van- The larder is almost always in some sort of der Wall and Jenkins 2003), and other aspects cavity (e.g., underground chamber, hollow tree). of cache dynamics. On the other hand, little is An important trait of a larder is that its contents known about the contents and characteristics change over time; larder size is the sum of re- of larders (Horne et al. 1998). Because larders peated provisioning visits minus consumption. are often large and valuable to the hoarder, Scatter-hoarding, on the other hand, is charac- animals hide them better than caches. Animals terized by spacing food items in or on the sur- can be seen delivering food to their burrow, face of some substrate such as soil, bark, or but manipulation of food within larders is sel- foliage. Natural cavities are seldom involved. dom observed (the larders of red squirrels, Because each cache is usually the result of one Tamiasciurus hudsonicus, and acorn wood- visit to the site, contents of caches generally peckers, Melanerpes formicivorus, are notable do not change; they are simply present or exceptions). The burrow or nest of an animal absent. Hereafter, we will use “cache” to refer often has to be excavated to examine the con- to scatter-hoarded food and “larder” to refer to tents of a larder, although in some instances larder-hoarded food. artificial dens or nests can be used to monitor The caches of many scatter-hoarding rodents larder contents (Horne et al. 1998). For most and birds have been well characterized (e.g., animals, destruction of larders during excava- Haftorn 1956, Macdonald 1976, Cowie et al. tion makes it difficult to monitor how they 1981, James and Verbeek 1983, Daly et al. 1992, change over time. Descriptions of larder con- Waite and Reeve 1993, Vander Wall 2003) be- tents (e.g., Broadbooks 1958, Smith 1968, Elliott cause it is often easy to observe these animals 1978, Post et al. 1993, Dearing 1997) are often make caches and examine cache contents. This little more than snapshots of the larders at a

1Department of Biology and the Program in Ecology, Evolution and Conservation Biology, University of Nevada, Reno, NV 89557.

248 2005] PILFERING OF CHIPMUNK LARDERS 249 point in time; numerous larders must be sam- store it in the floor and walls of their winter pled to understand how animals use them over nests. Because they do not deposit body fat seasons or years. and do not forage during winter, failure to It is important to have a better understanding accumulate a sufficiently large winter larder of larders and how animals use them. Seasonal would likely result in death before spring. changes in larder size and composition have The objective of this study was to investi- implications for survival (Novakowski 1967, gate ecological reasons why yellow pine chip- Seeley and Visscher 1985, Dearing 1997). Some munks refrain from larder-hoarding during animals that prepare both caches and larders summer. Because these chipmunks store food switch from scatter-hoarding to larder-hoard- throughout summer and autumn, and because ing food seasonally (Clarke and Kramer 1994, they need to have a large larder by winter, it is K.M. Kuhn unpublished data). In some taxa not clear why they do not form a larder during (e.g., sciurid and heteromyid rodents), differ- summer and maintain it until winter when ent species store food in different ways. For they need it. A large accumulation of seeds in example, fox squirrels (Sciurus niger) scatter- a nest chamber would be attractive to other hoard (Stapanian and Smith 1978), whereas animals, and so it would have to be defended red squirrels usually larder-hoard food (Smith to prevent pilferage. But larder defense takes 1968, Hurly and Robertson 1990). If we are to time and restricts the movements of the larder understand better the selective pressures that owner, which would reduce the amount of influence how animals store food and how the time for searching for unstored seeds. Scatter- mode of food storage evolves, we need to under- hoarding ensures that food resources are avail- stand how larders are constructed, used, and able to the forager during periods of food sometimes exploited by other animals. scarcity. This strategy may be particularly Yellow pine chipmunks (Tamias amoenus) important in habitats where food availability is are common residents of semiarid pine forests unpredictable. Defending a larder in summer in the western United States (Broadbooks and autumn likely would reduce the amount 1958). They have relatively large home ranges of food that could be gathered and scatter- (≈2 ha) that they share with dozens of con- hoarded. The larder defensibility hypothesis is specifics and other rodents (Broadbooks 1970, based on the assumption that the rate of pil- Kuhn unpublished data). They forage primarily ferage from an unguarded larder would be sig- for seeds. Observational studies (Kuhn unpub- nificantly greater than the rate of pilferage lished data) and experiments using radioactive from caches (which are also unguarded in yel- seeds (Vander Wall 1992, 1993) provide no low pine chipmunks) during the summer and evidence that yellow pine chipmunks larder- autumn. hoard food during summer and early autumn. We tested this assumption by constructing Instead, they scatter-hoard seeds throughout artificial but realistic yellow pine chipmunk their home range at depths of 5–40 mm. Burrow nests and monitoring pilfering from larders fidelity during summer and autumn is low. placed in those nests while simultaneously They construct winter nests in late autumn of monitoring pilferage of scatter-hoarded seeds. plant fibers in a small chamber ≈20–40 cm The relatively simple and shallow nests of yel- deep with 1 or 2 narrow tunnels ≈30–50 cm low pine chipmunks make them ideal for long leading to the surface (Broadbooks 1958, studying larder pilferage using artificial nests Kuhn unpublished data). Burrow entrances are constructed with man-made materials. A series very inconspicuous, and the individuals that of experiments (Vander Wall 2000, Vander occupy the burrows are seldom seen near Wall et al. 2003) has demonstrated that chip- them. Instead, they spend most daylight hours munks and other rodents will readily adopt foraging, grooming, and interacting with other plastic buckets as temporary nests. In addition chipmunks (Kuhn unpublished data). Several to their construction, these artificial nests are weeks before the onset of winter (late October unrealistic in one important way: there is no to early November) yellow pine chipmunks nest “owner.” However, this is not an issue in construct a larder in their winter nest cham- this experiment because we seek to test the ber. During this time yellow pine chipmunks consequences of having a summer larder that transfer food from aboveground caches and is not guarded because the owner spends most 250 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Fig. 1. Cross section of a nest bucket: o = outer lid buried about 2 cm under the ground surface (s); i = inner lid constructed of styrofoam insulation 17 mm thick to moderate nest temperature; p = plywood partition (6 mm thick with a 64-mm-diameter hole) dividing nest into upper (u) and lower (l) compartments; t = plastic tray containing the larder; e = entrance made of PVC pipe connecting upper nest chamber to ground surface. The nest entrance was placed under a shrub. Three diameters of entrance pipes were used to permit access by different sized rodents.

of its time away searching for more food (as do To determine what size (species) rodents yellow pine chipmunks during summer and might pilfer artificial chipmunk larders, we autumn). used entrance pipes of 3 inside diameters: small (25 mm), medium (34 mm), and large (50 METHODS mm). In previous studies we found that an entrance pipe 34 mm wide was appropriate We conducted this study in the Whittell for yellow pine chipmunks. Henceforth, we Forest and Wildlife Area in Little Valley, refer to these as small-(S), medium-(M), and Washoe County, about 30 km south of Reno, large-(L) diameter nests, indicating the size of Nevada, USA (39°15′0″N, 119°52′35″W). Lit- the largest rodents that could potentially enter tle Valley is in the Carson Range in extreme them. Small nests accommodate deer mice western Nevada at an elevation of ≈1975 m. (Peromyscus maniculatus, 15–20 g) and juve- Open Jeffrey pine (Pinus jeffreyi) forests with nile yellow pine chipmunks. Medium nests an understory of antelope bitterbrush (Purshia permit entry of these rodents and adult yellow tridentata), greenleaf manzanita (Arctostaphy- los patula), tobacco bush (Ceanothus veluti- pine chipmunks (40–50 g). Large nests accom- nus), and Sierra chinquapin (Castanopsis sem- modate all these rodents plus long-eared chip- pervirens) dominate the lower slopes of the munks (Tamias quadrimaculatus, 70–90 g) and valley. Soil consists of decomposed granite. The golden-mantled ground squirrels (Spermophilus region experiences summer droughts from June lateralis, 150–250 g). to October. We selected 2 sites about 500 m apart and We constructed artificial nests using 7.6-L established 30 nest buckets at each site during plastic buckets 24 cm high × 22 cm wide (Fig. mid-June 2002. At each site there were 10 nests ≈ 1). A partition divided the nest bucket into 2 of each of the 3 entrance sizes spaced 20 m nearly equal-sized chambers. We placed seeds apart and arranged in regular order along a (the larder) in the bottom compartment. A transect (i.e., S, M, L, S, M, L, etc.). We con- slightly inclined segment of PVC pipe ≈60 cm ducted 2 series of trials with nest buckets at long connected the upper chamber to the the same sites, the 1st with larders consisting ground surface. The whole “nest” was buried of ≈1000 black-oil sunflower seeds (≈55 g) and under 2–5 cm of soil (bottom of nest was the 2nd with larders consisting of 200 Jeffrey 25–30 cm deep) next to a shrub such that the pine seeds (≈20 g). These larders are smaller PVC pipe met the ground near the base of the than real winter larders, which often contain shrub among plant litter. We attempted to >200 g of seeds. Jeffrey pine seeds are native, make the nest entrance inconspicuous by cov- highly preferred seeds frequently eaten by ering the entrance pipe with plant litter. rodents at this site, and sunflower seeds are 2005] PILFERING OF CHIPMUNK LARDERS 251 nonnative seeds, which we included to deter- aging rodents (Duncan et al. 2002). We also mine whether seed species influenced the rate did not use any man-made markers (e.g., pin of pilferage. At each site there were typically flags or stakes) to relocate caches because 20–50 yellow pine chipmunks, 2–13 long-eared rodents use them to find buried seeds (Vander chipmunks, 5–10 deer mice, and 2–10 golden- Wall and Peterson 1996). Instead, we used nat- mantled ground squirrels (Vander Wall 2003, ural objects (e.g., twigs, pine cones, pebbles) Roth and Vander Wall in press), all of which in unique patterns to mark stations (Vander occupy large, overlapping home ranges and Wall 1994). We monitored these caches daily exhibit little or no territoriality. immediately after examining the larders. We We initiated the sunflower seed trials on 1 conducted larder and caching trials simultane- August and the Jeffrey pine seed trials on 20 ously during dry periods (no rain during pre- August 2002 by placing a larder in the lower ceding 14 days) to limit the olfactory signal nest chamber. We visited each nest daily to emitted by seeds (Vander Wall et al. 2003). inspect larders, and, if we suspected that Digging by rodents at the cache site indicated rodents had entered the nest (e.g., presence of that seeds had been removed. seed shells, feces, foreign material in the nest Seeds pilfered from larders could be eaten, chamber), we estimated how many seeds had moved to a new larder, or scatter-hoarded on been eaten, removed, or, in 2 nests, added. We the ground surface. We hypothesized that dur- estimated eaten sunflower seeds by measuring ing summer and early autumn most seeds re- the volume of seed shells (we determined in moved from larders would be scatter-hoarded the laboratory that 1 mL of seed shells equals because that is what happens to experimental ≈5 intact seeds). Eaten pine seeds were deter- seeds placed at bait stations aboveground (e.g., mined by counting shells. The number of intact Vander Wall 2003). To determine the fate of seeds remaining was estimated by measuring seeds pilfered from larders, we established 5 seed volume and comparing it to the initial nest buckets at a location >300 m from the volume of the larder (180 mL for sunflower other sites and placed 200 radioactively labeled and 92 mL for Jeffrey pine). We identified Jeffrey pine seeds in each nest. Each nest rodent visitors by size of fecal pellets in nests, bucket was equipped with a large-diameter presence of nest material moved into nests (50 mm) entrance to permit entry of all rodent (only by deer mice), and directly by seeing species. We arranged these nests in a “+” pat- animals in or fleeing from nests. At the end of tern with 1 nest at the center and the other 4 each visit, we returned all remaining intact nests 20 m apart in cardinal directions. The seeds to the larder, reburied the nest bucket, seeds in each bucket were dyed a different and made sure the entrance was open (some color so that the origin of any relocated seeds rodents filled the PVC pipe with soil). At the could be determined. We labeled seeds by end of the sunflower trials, we removed any soaking each lot in 3 mL distilled water and remaining sunflower seeds and left the nests scandium-46 until the seeds were thoroughly empty for 2 weeks until the pine seed trials wetted, and then they were allowed to dry for began. Nest buckets remained fairly cool, reg- 2 days. A single seed could be detected from istering 19°–23°C during midday, several de- ≈30 cm using a Geiger counter. We placed the grees below ambient temperature. seeds in nest buckets on 4 September 2002. To evaluate the impact of pilfering from Nine days later we examined all larders to larders relative to scatter caches, we estab- record how many seeds had been removed or lished transects of artificial caches in the same eaten and began surveying the vicinity within area. Each cache contained 10 sunflower (ini- ≈30 m of nests with Geiger counters looking tiated 1 August) or 2 Jeffrey pine seeds (initi- for seed caches and seed shells. When we ated 20 August) buried 10 mm deep. We found a cache, we removed the seeds and established 60 caches at each site (total 120 recorded seed color, number of seeds in the caches) spaced ≈5 m apart. The cache sites cache, and cache depth. Finally, we mapped changed between the sunflower and pine seed the location of caches relative to the central trials. We did not touch seeds or the ground larder using cardinal direction as axes. near the cache sites during preparation to pre- We assessed the effects of larder entrance vent human odors from providing cues to for- diameter (small, medium, or large), storage type 252 WESTERN NORTH AMERICAN NATURALIST [Volume 65

TABLE 1. Fate of artificial sunflower seed larders (1000 seeds) after 6 days and Jeffrey pine seed larders (200 seeds) after 4 days. Data are means ± 1s. Eaten refers to seeds eaten in the nest chamber. There were 10 artificial nests for each nest entrance diameter and seed species. Species Nest entrance diameter Eaten Remaining Taken Sunflower large 103 ± 82 0 ± 0 897 ± 82 medium 129 ± 69 48 ± 214 823 ± 197 small 157 ± 133 118 ± 293 725 ± 264 Jeffrey pine large 12 ± 80 ± 0 188 ± 8 medium 15 ± 80 ± 0 185 ± 8 small 51 ± 25 0 ± 0 149 ± 25

(larder or scattered caches), and seed species 6 occasions. Nests with small entrances, on (sunflower or Jeffrey pine) on the rate of seed the other hand, disappeared more slowly, tak- removal using survival analysis and a Weibull ing an average of >5 days to be depleted once distribution (Allison 1995). The response vari- discovered. ables were the lower and upper limits on the We found chipmunk feces in large- and time a larder or cache was known to have been medium-diameter nests on 10 occasions and present, expressed as days since the beginning observed juvenile yellow pine chipmunks of a trial. As some larders were removed piece- emerging from nests with small-diameter meal over 2 or more days, we arbitrarily deemed entrances. We found deer mouse feces in small- larders removed if 50% or more of the seeds diameter nests on 2 occasions, and deer mice had been taken. We made post-hoc compar- brought nest material into small nests on 10 isons among larder entrance sizes, storage types, occasions. One of the small-diameter nest and seed species by calculating chi-square sta- buckets was adopted by a deer mouse as its tistics as described in Allison (1995). Bon Fer- nest. Over a period of 6 days, the mouse re- roni alpha levels were used to assess the signi- peatedly brought nest material into the bucket ficance of chi-square tests: α = 0.003 (0.05/15 and added seeds to the larder, increasing its tests). volume by ≈50%. New seeds brought into the nest included sunflower (from other nest buck- RESULTS ets) as well as those of bitterbrush and man- In sunflower seed trials, rodents took 89.7% zanita. We found no evidence that golden- of seeds from large-diameter nests, 82.3% mantled ground squirrels had entered large- from medium-diameter nests, and 72.5% from diameter nests. small-diameter nests within 6 days (Table 1). Scatter-hoarded sunflower seeds (10 seeds In addition, rodents ate 10.3% of seeds in large- per cache) disappeared very rapidly (Fig. 2A). diameter nests, 12.9% in medium-diameter Removal rates along 2 transects were the same: nests, and 15.7% in small-diameter nests. 98.3% per day. Seeds in scattered caches did Removal rates decreased with decreasing nest not disappear significantly faster than seeds in entrance diameter (Fig. 2A). Removal rates from large-diameter nests (χ2 = 3.48, P = 0.062), large nests averaged 93.4% per day, medium but sunflower seeds in caches disappeared 1.9 nests averaged 57.3%, and small nests 30.1%. times faster than seeds in medium-diameter Rodents removed seeds from nests with large nests (χ2 = 23.32, P < 0.0001). entrances 2.4 times faster than from nests with In the Jeffrey pine seed trials, rodents took medium entrances (χ2 = 25.23, P < 0.0001), 94.0% of seeds (n = 200) from large-diameter and they removed seeds from nests with medi- nests, 92.5% from medium-diameter nests, um entrances 2.0 times faster than those from and 74.5% from small-diameter nests (Table 1) small entrances (χ2 = 15.03, P < 0.001). Larders within 4 days. In addition, rodents ate 6.0%, in nests with large entrances usually were 7.5%, and 25.5% of seeds in large-, medium-, emptied within 1 day after being discovered and small-diameter nests, respectively. Removal (12 of 20 cases), whereas nests with medium- rates from medium- and large-diameter nests sized entrances were emptied or nearly emp- were the same, averaging 96.2% per day (χ2 = tied within 1 day of being discovered on only 0.32, P > 0.50). Removal of seeds from nests 2005] PILFERING OF CHIPMUNK LARDERS 253

4 small-diameter nests. Golden-mantled ground squirrel feces were found in 4 large-diameter nests. Scatter-hoarded Jeffrey pine seeds (2 seeds per cache) were removed very slowly. Mean rate of removal was 0.55% per day. Jeffrey pine seeds in large-diameter nests disappeared 86 times faster than seeds in scattered caches (χ2 = 297.28, P < 0.0001), seeds in medium-diameter nests disappeared 76 times faster than seeds in scattered caches (χ2 = 305.16, P < 0.0001), and seeds in small-diameter nests disappeared 27 times faster than seeds in scattered caches (χ2 = 202.52, P < 0.0001). The rate of sunflower and Jeffrey pine seed removal from nests with large entrances was not significantly different, but pines seeds were removed 3.3 times faster from medium-diameter (χ2 = 14.46, P < 0.0001) and 2.3 times faster from small-diameter (χ2 = 23.20, P < 0.0001) nests than were sunflower seeds. Fig. 2. Rates of removal of sunflower seeds (A) and Jef- However, sunflower seeds were removed 43 frey pine seeds (B) from larders and from scatter caches. Closed triangles = larders in nests with large (50 mm times faster from surface caches than pine seeds χ2 diameter) entrances; closed circles = larders in nests with ( = 352.03, P < 0.0001). medium (34 mm) entrances; closed squares = larders in In the radioactive Jeffrey pine seed experi- nests with small (25 mm) entrances; open circles = scat- ment, 4 of the nests were emptied within 3 tered caches (10 seeds for sunflower or 2 seeds for Jeffrey days, and the 5th nest was not emptied until 9 pine buried 10 mm deep) on the ground surface. days after initiation of the experiment. We found a total of 380 caches in the vicinity of the 5 experimental nests (Fig. 3). Caches from with small entrances (78.2% per day) was the first 4 nests appeared to be the work of slower, only about 0.36 and 0.32 times as fast yellow pine chipmunks (based on size, depth, as seeds in medium- and large-diameter nests and distance from the source), whereas caches (χ2 = 29.43 and χ2 = 32.90, respectively, P < from the 5th nest appeared to be made by 0.0001 for both). Larders with large or medium deer mice. The chipmunk caches (n = 258) entrances were always emptied within 1 day contained 429 seeds with 1.7 ± 0.9 seeds per of being discovered, but only 8 small-diameter cache (mean ± 1s). Mean distance between nests were emptied within 1 day of being dis- source nests and caches was 14.6 ± 9.4 m (range covered. = 0.8–53.2 m). The deer mouse caches were In the pine seed trials, deer mouse feces smaller (1.2 ± 0.7 seeds per cache), shallower, occurred in 1 large, 1 medium, and 6 small and closer to the nest bucket (5.9 ± 3.4 m, nests. One small-diameter nest bucket, the same range 0.5–17.1 m away). Overall, we accounted one as in the sunflower trial, was adopted by a for 77% of the seeds originally placed in larders. deer mouse, which moved in nest material and more seeds. By day 3 it had increased the DISCUSSION volume of the larder by 91%. New seeds included sunflower (apparently from the pre- Several lines of evidence from the nest vious trial), Jeffrey pine (from other nests or buckets indicated that chipmunks had pilfered native seeds), and those of bitterbrush and seeds from most of the medium- and large- manzanita. By day 4 the nest and larder had diameter larders. The yellow pine chipmunk been destroyed by a black bear (Ursus ameri- is the most abundant species of rodent in the cana). We found chipmunk feces in 14 large- study area (Vander Wall 2002). Long-eared diameter nests, 19 medium-diameter nests, and chipmunks are less common and cannot fit 254 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Fig. 3. Dispersion of Jeffrey pine seed caches from seeds taken from 5 nest buckets (large circles). Each symbol repre- sents a cache of seeds taken from a different larder. Crosses = central nest; open squares = north nest; closed circles = east nest; open circles = south nest; closed triangles = west nest. Closed circles represent caches apparently made by a deer mouse. All other caches appeared to be made by yellow pine chipmunks.

into the medium-sized nest entrances. We We obtained strikingly different results when found chipmunk feces in numerous buckets, larders and caches were composed of sun- and we observed yellow pine chipmunks near flower seeds than Jeffrey pine seeds (Fig. 2). or emerging from several nests. The much Rodents removed sunflower seeds from larders slower rate of removal from the small-diame- fairly rapidly, especially those with large- ter nests suggests that the smaller and less or medium-diameter entrances, but scatter- common deer mice were active in those nests. hoarded sunflower seeds disappeared signifi- In the Jeffrey pine trial, we found some evi- cantly faster than larder-hoarded sunflower dence that yellow pine chipmunks also were seeds. These data suggest that it would be entering small nests. These individuals were safer for a chipmunk to larder-hoard sunflower probably males, which are ≈10%–15% smaller seeds in a burrow with a small- or medium- than females, or juveniles. Golden-mantled sized entrance than scatter-hoard them on the ground squirrels had visited several of the ground surface because the larder-hoarded large nests in the Jeffrey pine trial, but most seeds would be pilfered at a slower rate. In activity in the large nests appeared to be that contrast, pilferage rates of scatter-hoarded Jef- of yellow pine chipmunks. This general pat- frey pine seeds were extremely slow, while tern was confirmed in the radioactive seed larder-hoarded seeds disappeared very rapidly. experiment; caches from 4 larders matched Seeds in nests with small- and medium- those made by yellow pine chipmunks, and 1 diameter entrances disappeared faster in the set of caches was similar to those made by Jeffrey pine trials than in the sunflower trials, deer mice. probably because Jeffrey pine seeds are highly 2005] PILFERING OF CHIPMUNK LARDERS 255 preferred by forest rodents. Yellow pine chip- until the owner of the burrow returns (Elliott munks readily accept sunflower seeds but 1978, Clarke and Kramer 1994). Kangaroo rats sometimes ignore them when Jeffrey pine behave similarly (Daly et al. 1992). In our ex- seeds are available. We suspect that the dra- perimental larders, a yellow pine chipmunk matic difference in rate of pilferage of surface could remove all 200 Jeffrey pine seeds in caches of sunflower and Jeffrey pine seeds 8–10 visits, which could take as little as an occurred because sunflower seeds emit rela- hour. Deer mice, which can carry only 2–4 Jef- tively strong odors. Native seeds, represented frey pine seeds per load (Vander Wall and Long- here by Jeffrey pine, have probably experi- land 1999), work much more slowly but could enced strong selection for minimizing emitted deplete a larder containing 200 seeds in a single odors (we are exploring this possibility in a night. separate series of experiments, and preliminary The radioactive seed study demonstrated a results support this hypothesis). Detected seeds simple point: most seeds pilfered from larders are more likely to be eaten whereas undetected are scatter-hoarded. This seems to be true for seeds might eventually germinate. Thus, the both yellow pine chipmunks and deer mice. strength of seed odors is likely to be inversely Because a foraging yellow pine chipmunk can- correlated with plant fitness. Sunflower seeds, not guard its larder, and because larder-hoarded on the other hand, have been subjected to seeds are likely to be pilfered and scatter- strong artificial selection for size and oil con- hoarded anyway, it would be more efficient for tent and any selection against odor has proba- the foraging chipmunk simply to scatter-hoard bly been relaxed. The difference in removal the seeds itself. This behavior would benefit a rates between sunflower and pine seeds indi- forager in 3 ways. First, it would save time cates that the nonnative sunflower seeds are traveling to and from the nest, time that could not good surrogates for native seeds in certain be invested in other activities such as addi- kinds of experiments, and that they could give tional foraging, grooming, or predator surveil- misleading results in some studies of caching lance. If food is found at some distance from behavior because of the strong odors they the nest, which is generally the case for yellow emit. In this study we regard the test of rela- pine chipmunks, a scatter-hoarding forager is tive pilferage rates in larders versus caches likely to be much more efficient than one that using sunflower seeds to be invalid because larder-hoards because of reduced travel time. the pilferage rates of scattered caches differed Second, by caching seeds itself (rather than so strikingly from those of caches of natural having them cached by a pilferer), the forager Jeffrey pine seed (Fig. 2). We recommend that retains a recovery advantage relative to other sunflower seeds not be used in studies of animals with which it shares its home range. cache pilferage; native seeds are more likely to The individual that makes caches retains spa- yield meaningful results. tial memories of its cache sites (Jacobs and Scatter-hoarded Jeffrey pine seeds appear Liman 1991, Vander Wall 1991, Jacobs 1992). to be relatively safe from pilferers compared Pilferers lack these memories and must depend with unguarded larder-hoarded seeds. Scatter- on olfaction, which works poorly when the soil hoarded Jeffrey pine seeds buried in dry soil is dry (Vander Wall 1995, 1998), and random appear to emit little or no detectable odors digging to find buried seeds. As long as seeds (Vander Wall 1995, 1998, 2000). If it should do not emit strong odors (which is probably rain, however, seeds become more detectable true of most native seeds in dry soil), the ani- by other rodents, but this does not appear to mal that caches a seed has a recovery advan- be too damaging to yellow pine chipmunks tage (Vander Wall and Jenkins 2003, Vander because the caches of all individuals are Wall et al. 2003). Third, by scatter-hoarding, equally vulnerable (Vander Wall 2000, Vander the cacher shields itself from catastrophic losses. Wall and Jenkins 2003). Larder-hoarded seeds, An inherent advantage of scatter-hoarding over on the other hand, are vulnerable under all larder-hoarding is that when losses occur from conditions. When eastern chipmunks (Tamias a larder, they can be catastrophic (Henry 1986), striatus), which maintain larders at all seasons whereas losses from scattered caches, although whenever excess food is available, discover an damaging, are usually far less serious. unguarded nest of a conspecific, they make re- In this experiment we did not move nest peated pilfering trips with filled cheek pouches buckets to new locations between trials. This 256 WESTERN NORTH AMERICAN NATURALIST [Volume 65 procedure allowed for the possibility that larger areas (≈2 ha), appear to scatter-hoard rodents could learn the locations of artificial seeds throughout their home range, and do not nests and return to pilfer larders repeatedly in attempt to defend their caches. Mean cache successive trials. We believe that this condi- residence time is unknown but is on the order tion accurately reflected the natural situation. of weeks (Vander Wall 2002, Vander Wall and Rodents can be expected to learn the location Joyner 1998). Yellow pine chipmunks must and explore the characteristics of all burrows eventually accumulate a large mass of food to and refuges in their home range (Elliott 1978). ensure survival over winter, but they delay for- Knowledge of these sites may become impor- mation of the winter larder until a few weeks tant when an animal is at risk of predation or before the onset of winter conditions, appar- requires a resting site. Yellow pine chipmunks ently because of the high rates of pilferage an appear to change sleeping sites frequently undefended larder is likely to experience. during summer (Kuhn unpublished data), and It is unclear whether the nest buckets might summer sleeping burrows are probably visited have influenced the rate of pilferage of artifi- frequently by other chipmunks during the day cial larders. The odor of the plastic buckets while the owner is away foraging. If we had seems weak to humans but might be easily de- moved our artificial nests to new sites be- tected by rodents. We assume that most rodents tween trials we might have underestimated initially detected artificial nests by searching the probability of larder pilferage in real sum- visually for a burrow opening, which animals mer nests. are likely to explore as potential refuges, future On 2 occasions during this study, black bears nest sites, or food sources. The odor of seeds destroyed nest buckets and consumed the and plastic may have been secondary cues, but larder. We suspect that bears first detected the this has not been established. Our daily dig- odor of plastic and learned to associate the ging and soil disturbance when we checked buckets with a food reward. Actual chipmunk nest buckets might also have served as cues to nests are probably far more difficult for bears foraging rodents. Studies of the dynamics of to detect, but this result does demonstrate an rodent larders (i.e., changes because of foraging important principle: larders are vulnerable to or pilferage) are complicated by the destruc- a wider variety of pilferers than are caches and tive nature of sampling larders over time, and when pilferage of a larder does occurs, it is so some form of artificial burrow and larder may need to be part of any experimental design. usually catastrophic. From the chipmunk’s Future studies should try to develop more perspective, this sort of pilferage is far more realistic nest chambers that can be checked destructive than pilferage from caches because easily with minimal disturbance. the larder is consumed. When caches are pilfered by other rodents, most of the seeds are ACKNOWLEDGMENTS recached elsewhere, and, consequently, the seeds are still potentially available to the ani- We thank Adam York for his help in work- mal that originally stored them (Vander Wall ing out details of the experimental design in and Jenkins 2003). pilot studies. Ying Wang assisted us with field- Food-storage behavior of yellow pine chip- work. We thank the Whittell Forest, University munks and eastern chipmunks is very differ- of Nevada, for permission to conduct the study ent. Eastern chipmunks larder-hoard exten- in Little Valley. This research was supported sively during all seasons and also scatter-hoard by NSF grant DEB-9708155. some food during the spring and summer (Elliott 1978, Clarke and Kramer 1994). Eastern LITERATURE CITED chipmunks have a relatively small home range; when they scatter-hoard, they cache most food ALLISON, P.D. 1995. Survival analysis using the SAS system: a practical guide. SAS Institute, Inc., Cary, NC. near the nest entrance and defend these caches BROADBOOKS, H.E. 1958. Life history and ecology of the from potential pilferers. Cache residence time chipmunk, Eutamias amoenus, in eastern Washing- (i.e., amount of time an average seed remains ton. University of Michigan, Museum of Zoology, at a cache site) is relatively short (≈1 hour; Miscellaneous Publications 103:1–48. ______. 1970. Home ranges and territorial behavior of the Clarke and Kramer 1994). Yellow pine chip- yellow-pine chipmunk, Eutamias amoenus. Journal munks, on the other hand, forage over much of Mammalogy 51:310–326. 2005] PILFERING OF CHIPMUNK LARDERS 257

BRODIN, A. 1994. The disappearance of caches that have ing of colony growth and reproduction. Ecological been stored by naturally foraging willow tits. Animal Entomology 10:81–88. Behaviour 47:730–732. SHERRY, D.F., J.R. KREBS, AND R.J. COWIE. 1981. Memory CLARKE, M.F., AND D.L. KRAMER. 1994. Scatter-hoarding for the location of stored food in marsh tits. Animal by a larder-hoarding rodent: intraspecific variation Behaviour 29:1260–1266. in the hoarding behaviour of the eastern chipmunk, SMITH, C.C. 1968. The adaptive nature of social organiza- Tamias striatus. Animal Behaviour 48:299–308. tion in the genus of tree squirrel Tamiasciurus. Eco- CLARKSON, K., S.F. EDEN, W.J. SUTHERLAND, AND A.I. logical Monographs 38:31–63. HOUSTON. 1986. Density dependence and magpie STAPANIAN, M.A., AND C.C. SMITH. 1978. A model for seed food hoarding. Journal of Animal Ecology 55:111–121. scatterhoarding: coevolution of fox squirrels and COWIE, R.J., J.R. KREBS, AND D.F. SHERRY. 1981. Food black walnuts. Ecology 59:884–896. storing in marsh tits. Animal Behaviour 29:1252–1259. VANDER WALL, S.B. 1991. Mechanisms of cache recovery DALY, M., L.F. JACOBS, M.I. WILSON, AND P.R. BEHRENDS. by yellow pine chipmunks. Animal Behaviour 41: 1992. Scatter hoarding by kangaroo rats (Dipodomys 851–863. merriami) and pilferage from their caches. Behav- ______. 1992. The role of animals in dispersing a “wind- ioral Ecology 3:102–111. dispersed” pine. Ecology 73:614–621. DEARING, M.D. 1997. The function of haypiles of pikas ______. 1993. Cache site selection by chipmunks (Tamias (Ochotona princeps). Journal of Mammalogy 78: spp.) and its influence on the effectiveness of seed 1156–1163. dispersal in Jeffrey pine (Pinus jeffreyi). Oecologia DUNCAN, R.S., D.G. WENNY, M.D. SPRITZER, AND C.J. 96:246–252. WHELAN. 2002. Does human scent bias seed removal ______. 1994. Removal of wind-dispersed pine seeds by studies? Ecology 83:2630–2636. ground-foraging vertebrates. Oikos 69:125–132. ELLIOTT, L. 1978. Social behavior and foraging ecology of ______. 1995. Influence of substrate water on the ability the eastern chipmunk (Tamias striatus) in the Adiron- of rodents to find buried seeds. Journal of Mammal- dack Mountains. Smithsonian Contributions to Zool- ogy 76:851–856. ogy 265:1–107. ______. 1998. Foraging success of granivorous rodents: HAFTORN, S. 1956. Contribution to the food biology of tits effects of variation in seed and soil water on olfaction. especially about storing of surplus food. Part IV. A Ecology 79:233–241. comparative analysis of Parus atricapillus L., P. crista- ______. 2000. The influence of environmental conditions tus L., and P. ater L. Kongelige Norske Videnskabers on cache recovery and cache pilferage by yellow pine Selskabs Skrifter 1956:1–54. chipmunks (Tamias amoenus) and deer mice (Peromys- HENRY, J.D. 1986. Red fox: the catlike canine. Smithsonian cus maniculatus). Behavioral Ecology 11:544–549. Institution Press, Washington, DC. ______. 2002. Masting in animal-dispersed pines facili- HORNE, E.A., M. MCDONALD, AND O.J. REICHMAN. 1998. tates seed dispersal. Ecology 83:3508–3516. Changes in cache contents over winter in artificial ______. 2003. Effects of seed size of wind-dispersed pines dens of the eastern woodrat (Neotoma floridana). (Pinus) on secondary seed dispersal and the caching Journal of Mammalogy 79:898–905. behavior of rodents. Oikos 100:25–34. HURLY, T.A., AND R.J. ROBERTSON. 1990. Variation in the VANDER WALL, S.B., M.J. BECK, J.S. BRIGGS, J.K. ROTH, food hoarding behaviour of red squirrels. Behavioral T.C. THAYER, J.L. HOLLANDER, AND J. ARMSTRONG. Ecology and Sociobiology 26:91–97. 2003. Interspecific variation in the olfactory abilities JACOBS, L.F. 1992. Memory for cache locations in Mer- of granivorous rodents. Journal of Mammalogy 84: riam’s kangaroo rats. Animal Behaviour 43:585–593. 487–496. JACOBS, L.F., AND E.R. LIMAN. 1991. Grey squirrels remem- VANDER WALL, S.B., AND S.H. JENKINS. 2003. Reciprocal ber the locations of buried nuts. Animal Behaviour pilferage and the evolution of food-hoarding behav- 41:103–110. ior. Behavioral Ecology 14:656–667. JAMES, P.C., AND N.A.M. VERBEEK. 1983. The food storage VANDER WALL, S.B., AND J.W. JOYNER. 1998. Recaching of behaviour of the northwestern crow. Behaviour 85: Jeffrey pine (Pinus jeffreyi) seeds by yellow pine 276–291. chipmunks (Tamias amoenus): potential effects on MACDONALD, D.W. 1976. Food caching by red foxes and plant reproductive success. Canadian Journal of some other carnivores. Zeitschrift fur Tierpsycholo- Zoology 76:154–162. gie 42:170–185. VANDER WALL, S.B., AND W. S. L ONGLAND. 1999. Cheek NOVAKOWSKI, N.S. 1967. The winter bioenergetics of a pouch capacities and loading rates of deer mice (Per- beaver population in northern latitudes. Canadian omyscus maniculatus). Great Basin Naturalist 59: Journal of Zoology 45:1107–1118. 278–280. POST, D.M., O.J. REICHMAN, AND D.E. WOOSTER. 1993. VANDER WALL, S.B., AND E. PETERSON. 1996. Associative Characteristics and significance of the caches of east- learning and the use of cache markers by yellow pine ern woodrats (Neotoma floridana). Journal of Mam- chipmunks (Tamias amoenus). Southwestern Natu- malogy 74:688–692. ralist 41:88–90. ROTH, J.K., AND S.B. VANDER WALL. In press. Importance WAITE, T.A., AND J.D. REEVE. 1993. Food storage in Gray of primary and secondary seed dispersal of Sierra Jays: source type and cache dispersion. Ethology bush chinquapin (Fagaceae) by scatter-hoarding 93:326–336. rodents. Ecology: In press. SEELEY, T.D., AND P.K. VISSCHER. 1985. Survival of honey- Received 11 May 2004 bees (Apis mellifera) in cold climates: the critical tim- Accepted 15 November 2004 Western North American Naturalist 65(2), © 2005, pp. 258–266

DISTRIBUTION OF THE MILLIPED VIRGOIULUS MINUTUS (BRANDT, 1841): FIRST RECORDS FROM MISSISSIPPI, OKLAHOMA, AND TEXAS (JULIDA: BLANIULIDAE)

Chris T. McAllister1, Rowland M. Shelley2, Henrik Enghoff3, and Zachary D. Ramsey1

ABSTRACT.—Virgoiulus minutus (Brandt 1841) (Julida: Blaniulidae), the only indigenous representative of the family in the New World, occurs, or can be expected, in parts or all of 24 states east of the Central Plains plus the District of Columbia; it is documented for the 1st time from Mississippi, Oklahoma, and Texas. The northern-, southern-, and westernmost localities are in Berrien County, Michigan; Putnam County, Florida; and Angelina/Rusk Counties, Texas, respectively. New England, Utah, Wyoming, Canada, and Mexico are deleted from the range, and specific localities are reported to augment previous generalized citations; those from Mexico represent misidentifications of Nopoiulus kochii (Gervais, 1847), an introduced European species that is recorded from Mexico City, Distrito Federal. Records of V. minutus from Pennsylvania, Virginia, South Carolina, Georgia, Alabama, West Virginia, Ohio, Illinois, Michigan, and Mis- souri are the 1st definite localities from these states; a sample from “Anechar,” believed to be a misspelling of “Arrochar,” a neighborhood in Staten Island, is considered the 1st definite record from New York. The published statement of occurrence in Delaware in general is the only known record of an indigenous diplopod from this state.

Key words: Virgoiulus minutus, Nopoiulus minutus, Nopoiulus kochii, Blaniulidae, Mississippi, Texas, distribution.

Shelley et al. (2005) observed that the dis- sites to fully document its distribution; to this covery of a single individual of many milliped end the 2nd author borrowed material from species from the region between the Missis- the ensuing list of repositories, which contained sippi River and the Central Plains, where dis- the 1st samples from Mississippi. tributions are usually poorly known, can alter Williams and Hefner (1928), Chamberlin and knowledge so significantly that published doc- Hoffman (1958), Loomis (1968), and Shelley umentation is in order. This was necessary (1978a, 1978b) considered V. minutus (then with the polydesmidans Scytonotus granulatus referenced as Nopoiulus minutus) to be a (Say) (Polydesmidae) and Pleuroloma flavipes European introduction, but we believe that V. Rafinesque (Xystodesmidae) (Shelley et al. minutus is an endemic Nearctic species and 2004, 2005), and is now necessary for the the only indigenous blaniulid in the New World, blaniulid julidan Virgoiulus minutus (Brandt). for the following reasons. To begin with, the Distribution statements for this species in milliped has never been encountered in Europe, most modern accounts are either general lists as have all the known Palearctic introductions, of states without specific localities or brief nor, in fact, outside the coherent range de- summary range descriptions. As part of the 1st picted in Figure 1. Second, while V. minutus author’s ongoing survey of myriapods in the does occur in urban environments, particu- “Ark-La-Tex” region, V. minutus was reported larly in the Southeast, it also is found well re- from 17 new counties in Arkansas by McAllis- moved from human influence, in contrast to ter et al. (2003), and the milliped has recently the introduced North American blaniulids that been discovered in southeastern Oklahoma occur exclusively in association with man and 4 counties in eastern Texas; coupled with either in urban environments or in agricultural a preserved sample from Angelina County, areas where they sometimes feed on crops, Texas, these represent new state records. As especially fruits like strawberries. Finally, the the only detailed locality data for V. minutus distribution pattern of V. minutus (Fig. 1) are those of McAllister et al. (2003), it is desir- counters those of all widely introduced mil- able to publish these and other unreported lipeds in North America, which occur across

1Biology Department, Texas A&M University–Texarkana, Texarkana, TX 75505. 2Research Lab, North Carolina State Museum of Natural Sciences, 4301 Reedy Creek Road, Raleigh, NC 27607. 3Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.

258 2005] DISTRIBUTION OF VIRGOIULUS MINUTUS 259

Fig. 1. Distribution of Virgoiulus minutus. The question marks in New Jersey and Delaware indicate general records from these states; that in Michigan denotes the questionable record from Saginaw County (Snider 1991). the continent to varying degrees and north and Canada—and exclusively in association into Canada, as opposed to a large, coherent with man in cities and towns. Consequently, area in a single general region. If V. minutus the distribution pattern in V. minutus, in both were introduced, we would expect it to occur urban and rural habitats in one broad, defin- across the continent—for example in New able area east of the Central Plains, is not that England, California, the Pacific Northwest, of an introduced milliped but rather, we think, 260 WESTERN NORTH AMERICAN NATURALIST [Volume 65 definitive evidence that it is indeed an indige- milliped is particularly abundant in southeast- nous species. ern pine forests that have been ravaged by the Enghoff and Shelley (1979) first raised the southern pine beetle (Dendroctonus frontalis possibility that V. minutus might be native, and Zimmerman, 1868), in which dead pine logs Enghoff (1984a:400) stated that “if not intro- are plentiful. This association with pines makes duced, it is the only indigenous blaniulid in V. minutus one of the few North American mil- America.” In an account of the introduced bla- lipeds that collectors can search for deliber- niulid Nopoiulus kochii (Gervais, 1847), Shelley ately with a high probability of success, by vis- (1988) reported that V. minutus is endemic to iting predominantly pine forests and peeling the Nearctic, and Hoffman (1999) stated that bark off decaying logs. The individuals from Virgoiulus was presumed to be endemic to Oklahoma and Bowie and Cass Counties, Texas, southeastern North America. Five other blan- were discovered in this manner; those from iulids are known from this continent, all native Oklahoma were under bark of a pine stump on European species that have been introduced the edge of a wooded area; those from Bowie by man and now occur to varying extents County were under bark of decaying pine logs across the U.S., Canada, and Mexico, primarily in a predominantly loblolly pine forest (Pinus in urban habitats (Chamberlin and Hoffman taeda L.) with scattered southern red oaks 1958, Enghoff and Shelley 1979, Enghoff 1984a, (Quercus falcata Michaux) and other hard- 1984b, Shelley 1988, 1990, 2002, Hoffman woods; and the specimen from Cass County 1999): Archiboreoiulus pallidus (Brade-Birks, was in litter associated with these trees. How- 1920), Blaniulus guttulatus (Fabricius, 1798), ever, the individuals from Newton and Rusk Proteroiulus fuscus (Am Stein, 1857), Chone- Counties, Texas, were encountered under bark iulus palmatus (N˘emec, 1895), and N. kochii. of decaying oak logs. These blaniulids are all narrow, fragile, cylin- Though plentiful, published records of V. drical (“juliform”) diplopods whose widths are minutus are somewhat difficult to trace be- roughly equivalent to the lead of a mechanical cause of its contorted nomenclatural history. pencil, and V. minutus is distinguished, even The first account was by Say (1821), who in juvenile stages, by the arrangement of the described it as “Julus pusillus,” but this bino- ocelli in a single row and by the extremely mial is preoccupied by J. pusillus Leach, 1815; short, microscopic, pleurotergal setae that are Brandt’s (1841) name, minutus, is thus the old- invisible under a stereomicroscope even at est available specific name. The main reason magnifications of around 100X. The setae are for the uncertainties, however, is confusion easily seen on other ocellate blaniulids, for between V. minutus and N. kochii, which has example P. fuscus, whose ocelli are arranged in an even more complicated nomenclatural his- 2 unequal rows, and N. kochii. As noted by tory (see Enghoff and Shelley 1979, Enghoff Enghoff and Shelley (1979), males are less 1984a). The name minutus was neglected by numerous than females in most blaniulid European diplopodologists until Chamberlin species, but they are particularly rare in V. (1921, 1922) brought it into the synonymy of minutus, which is surely parthenogenetic. To N. kochii, and Enghoff and Shelley (1979) our knowledge only 2 males have ever been showed that minutus and kochii are 2 different reported, one of which was illustrated by Eng- species. Enghoff (1984a) referred minutus to hoff and Shelley (1979, figs. 5–10). the new, monotypic genus, Virgoiulus, which Occasionally, V. minutus is found in decidu- occupies a basal position in the phylogeny of ous leaf litter, but the great majority of speci- the blaniulid subfamily Nopoiulinae and is an mens are encountered in association with endemic North American genus. decaying logs and stumps, principally pines We present below distributional data for V. and primarily beneath loose bark. Its prefer- minutus beginning with deletions that were ence for subcortical pine habitats was first rec- probably based on misidentifications of other ognized by Say (1821:106), who stated that it blaniulids or narrow-bodied representatives of was “found commonly under pine bark on the other julidan families like the Nemasomatidae. eastern shore of Virginia.” Chamberlin (1921) Subsequently, we compile published records noted that it was often found under bark of beginning with generalized range statements decaying trees but did not mention pines spe- and then provide detailed locality records. cifically, and Shelley (1978a) reported that the Missing data were not provided on vial labels, 2005] DISTRIBUTION OF VIRGOIULUS MINUTUS 261 and the number of specimens, all being females History, Smithsonian Institution, Washington, or juveniles, is provided after the institutional D.C.; UAAM–University of Arkansas Arthro- acronym except for samples with too many pod Museum, Fayetteville; UMO–Enns Ento- individuals to count, indicated by “several.” mological Museum, University of Missouri, Based on occurrences in adjacent states, we Columbia; VMNH–Virginia Museum of Nat- predict that V. minutus will be discovered in ural History, Martinsville; ZMUC–Natural southeastern Wisconsin (at least Kenosha History Museum of Denmark, Copenhagen. County) and perhaps more broadly across the southern border of the state; occurrences in DELETIONS southeastern Iowa and throughout the eastern periphery of Oklahoma are also plausible. The New England, Utah, and Wyoming; Canada; overall distribution (Fig. 1) encompasses around Mexico. Chamberlin (1921) cited N. minutus 850 miles (1360 km) north–south and 1060 miles from New England, but there are no pre- (1696 km) east–west, and can be characterized served specimens in any American repository. as follows: the United States east of the Cen- Chamberlin and Hoffman (1958) stated that tral Plains from, north–south, central Missouri, the species occurs sporadically as far west as southern Michigan, northern Illinois and Ohio, Utah, and Chamberlin (1943a, 1951) reported and Long Island, New York, to the latitude of N. minutus from Casper, Natrona County, Gainesville, Alachua County, Florida (actually Wyoming, and Salt Lake City and Salem, Salt known from Putnam County, the adjacent Lake and Utah Counties, Utah, all of which are well west of the coherent distribution shown county to the east), the Gulf Coast, and south- in Figure 1. The Utah records probably refer ern Louisiana; east–west, from the area of to Orinisobates utus (Chamberlin, 1912) (Nema- New York City, the Outer Banks of North Car- somatidae), which is common in canyons and olina, and northeastern Florida to central Mis- along watercourses in Salt Lake and Utah souri and the eastern peripheries of Texas and Counties and northern Utah in general (Eng- Oklahoma. There are no new or published hoff 1985, plus unreported specimens exam- records from Maryland and the District of ined by the 2nd author). We have not seen any Columbia, but V. minutus is expected there, so blaniulids from Casper, Wyoming, but surmise its area encompasses parts of 24 states plus that this record refers to an introduced species DC and all of 14 states: Maryland, Delaware, like N. kochii, as it is well removed from the Virginia, North and South Carolina, Georgia, known range of O. utus, whose only Wyoming Alabama, Mississippi, Tennessee, Kentucky, West records are from the Teton Mountains adja- Virginia, Indiana, Arkansas, and Louisiana. The cent to Idaho (Enghoff 1985). northernmost record is from Berrien County, Chamberlin and Hoffman (1958) included Michigan; the easternmost localities are in New eastern Canada in the range of N. minutus, York and Dare County, North Carolina; the and Loomis (1968) gave the range as the southernmost is in Putnam County, Florida; “United States and Canada.” However, Shel- and the westernmost are in Angelina and Rusk ley (1988, 2002) stated that it is not probable Counties, Texas. Acronyms of sample reposito- for any region of Canada, even the most proxi- ries are as follows: AMNH–American Museum mate part of southern Ontario (Essex County), of Natural History, New York; FMNH–Field because at that time the species was not known Museum of Natural History, Chicago, Illinois; from north of southern Ohio. We report sites FSCA–Florida State Collection of Arthropods, from Lorain County, Ohio, near metropolitan Gainesville; INHS–Illinois Natural History Sur- Cleveland, and Berrien and Hillsdale Coun- vey, Champaign; JAB–private collection of J.A. ties, Michigan, and Snider (1991) recorded Beatty, Carbondale, Illinois; MCZ–Museum of questionable occurrences from Lenawee and Comparative Zoology, Harvard University, Saginaw Counties, Michigan. These samples Cambridge, Massachusetts; MEM–Mississippi are not available and the latter is still doubtful, Entomological Museum, Mississippi State Uni- but Lenawee County is adjacent to Hillsdale versity, Starkville; MPM–Milwaukee Public and hence is plausible, so we denote it with a Museum, Milwaukee, Wisconsin; NCSM–North dot in Figure 1. Thus, while we still exclude Carolina State Museum of Natural Sciences, Canada from the distribution, V. minutus is now Raleigh; NMNH–National Museum of Natural known from only 75 miles (120 km) southwest 262 WESTERN NORTH AMERICAN NATURALIST [Volume 65 of Essex County, and discovery in southern Shelley 1979). Eastern shore in general. Acco- Ontario is plausible. mack and Northampton Cos. (Say 1821, New- Chamberlin (1943b) and Loomis (1968) port 1844, Wood 1865, Loomis 1968, Hoffman reported N. minutus from Chapultepec Park in 1999). Mexico City and Salazar, Distrito Federal, NORTH CAROLINA: North Carolina in gen- Mexico. The 2nd author recently discovered eral (Enghoff and Shelley 1979). Durham Co., the samples from Chapultepec Park at the Duke Forest (Chamberlin 1940, Causey 1940, NMNH, and the 3rd author identified them as Wray 1967, Shelley 1978a, 2000). Cleveland N. kochii. This is the 2nd Mexican record of N. Co., Kings Mountain area (Filka and Shelley kochii, the 1st being that of Jawlowski (1930), 1980, Shelley 2000). Sites in Alexander, Bertie, who recorded the synonym N. armatus Bladen, Brunswick, Carteret, Chatham, Dare, (N˘emec, 1895) (see Enghoff 1984b), from Edgecombe, Gates, Granville, Halifax, Har- Patzcuaro, Michoacan, which was reiterated nett, Jones, Lee, Macon, Madison, Moore, by Loomis (1968). Sample data follow: Dis- Orange, Pitt, Richmond, Vance, Wake, and trito Federal, Mexico City, Chapultepec Forest Wilkes Cos. (Shelley 1978a, 2000). Park, in leaf litter, , 2 , 3 juvs., 7 October SOUTH CAROLINA: South Carolina in gen- 1939, F. Bonet (NMNH). eral (Enghoff and Shelley 1979). Coastal zone in general (Shelley 1978b). PUBLISHED RECORDS GEORGIA: Georgia in general (Enghoff and Shelley 1979). “MIDDLE STATES” in general (Say 1821, FLORIDA: Florida in general (Enghoff and Brandt 1841, Golovatch and Hoffman 2000). Shelley 1979, Hoffman 1999). Escambia Co., UNITED STATES EAST OF THE MISSISSIPPI Pensacola (Bollman 1887, 1893, McNeill 1887, RIVER (Chamberlin 1921). Hoffman 1999, Shelley 2001). Sites in Gads- WIDESPREAD OVER EASTERN UNITED STATES den, Jefferson, Leon, Liberty, Putnam, and AS FAR SOUTH AS DELAWARE AND VIRGINIA AND Santa Rosa Cos. (Shelley 2001). WEST TO TENNESSEE (Chamberlin and Hoff- ALABAMA: Alabama in general (Enghoff and man 1958). Shelley 1979). EASTERN NORTH AMERICA (ALABAMA, ARKAN- TENNESSEE: Tennessee in general (Cham- SAS, FLORIDA, GEORGIA, ILLINOIS, INDIANA, berlin 1921, Chamberlin and Hoffman 1958, KENTUCKY, LOUISIANA, MISSOURI, NORTH CAR- Enghoff and Shelley 1979). ?Jefferson Co., OLINA, OHIO, PENNSYLVANIA, SOUTH CAROLINA, Mossy Creek (Bollman 1888a). Overton Co., TENNESSEE, VIRGINIA, AND WEST VIRGINIA) (Enghoff and Shelley 1979). Standing Stone St. Pk. (Loomis 1944). Sevier Co., SOUTHEASTERN NORTH AMERICA, WEST TO Gatlinburg and Great Smoky Mountains ARKANSAS, NORTH TO ILLINOIS AND PENNSYL- National Park (Chamberlin 1952). VANIA (Enghoff 1984a). KENTUCKY: Kentucky in general (Enghoff EASTERN UNITED STATES, FROM PENNSYL- and Shelley 1979). Powell Co., below Raven VANIA AND MISSOURI SOUTH TO FLORIDA AND Rock (stated by Enghoff [1979] as probably in LOUISIANA (Hoffman 1999). Kentucky, which is correct). NEW YORK: New York in general (Cham- WEST VIRGINIA:West Virginia in general berlin 1921, Bailey 1928). (Enghoff and Shelley 1979). NEW JERSEY: New Jersey in general (Cham- OHIO: Ohio in general (Chamberlin 1921, berlin 1921). Williams and Hefner 1928, Enghoff and Shel- PENNSYLVANIA: Pennsylvania in general ley 1979). (Chamberlin 1921, Enghoff and Shelley 1979, INDIANA: Indiana in general (Chamberlin Enghoff 1984a, Hoffman 1999). 1921, Enghoff and Shelley 1979). Clark Co., DELAWARE: Delaware in general (Cham- New Providence (Bollman 1888b). Marion Co., berlin 1921, Chamberlin and Hoffman 1958). Indianapolis (Bollman 1888b). Monroe Co., To the best of our knowledge, this is the only Bloomington (Bollman 1887, 1888b). Washing- published record of an indigenous milliped ton Co., Salem (Bollman 1888b). from the state of Delaware. ILLINOIS: Illinois in general (Chamberlin VIRGINIA:Virginia in general (Bollman 1887, 1921, Enghoff and Shelley 1979, Enghoff Chamberlin and Hoffman 1958, Enghoff and 1984a). 2005] DISTRIBUTION OF VIRGOIULUS MINUTUS 263

MICHIGAN: Michigan in general (Johnson ial St. Pk., Dooly Spring, 1958, N.B. Causey 1954). Lenawee and Saginaw Cos., reported (FSCA 1). Rabun Co., north slope of Rabun with a question mark (Snider 1991). Bald nr. rd. to tower, 30 May 1964, H.R. MISSOURI: Missouri in general (Enghoff and Steeves (FSCA 3). Union Co., east slope of Shelley 1979, Hoffman 1999). Brasstown Bald, S. & J. Peck (FSCA 1). First ARKANSAS: Arkansas in general (Enghoff and definite state records. Shelley 1979, Enghoff 1984a). Pulaski Co., FLORIDA: Duval Co., Jacksonville, Tree Hill Little Rock (Bollman 1888c, McAllister et al. Nature Center, 13 April 2002, R.M. Shelley 2002) and North Little Rock (=“Argenta”) (NCSM 1). Escambia Co., 11.6 miles (18.6 (Bollman 1888c, McAllister et al. 2002), sites in km) NW downtown Pensacola, jct. FL Hwys. Baxter, Bradley, Calhoun, Clarke, Craighead, C97 & C297A, 18 November 1977, R.M. Shel- Drew, Hempstead, Lincoln, Logan, Lafayette, ley (ZMUC 55). Walton Co., Basin Bayou St. Nevada, Polk, Pope, Scott, and Sevier Cos. Pk., 18 November 1977, R.M. Shelley (ZMUC (McAllister et al. 2002, 2003). 18). Washington Co., Falling Waters St. Pk., LOUISIANA: Louisiana in general (Enghoff 18 November 1977, R.M. Shelley (ZMUC 8). and Shelley 1979, Hoffman 1999). Caddo Par., ALABAMA: Baldwin Co., Jct. US Hwys. 90 & (Causey 1963, as undetermined females of the 98 W of Loxley, 22 January 1965, N.B. Causey Nemasomidae [=Nemasomatidae]). (FSCA 1). Cullman Co., nr. Cullman, Hurricane Creek Park, 6 July 1963, H.R. Steeves (FSCA NEW RECORDS 5). Franklin Co., The Dismals, 18 July 1959, H.R. Steeves (FSCA 3); Dismal Gardens, 4 PENNSYLVANIA: Franklin Co., Penn. Mar. September 1961, J. Wagner, W. Suter (FSCA (exact location unknown), 27 July 1955, W. 13); and Rock Bridge Canyon, 21 May 1961, Suter (FSCA 1). Washington Co., Mononga- H.R. Steeves (FSCA 47). Jackson Co., 7.5 miles hela, W.L. Gregg (NMNH 2). Westmoreland (12 km) N Princeton, 29 October 1960, H.R. Co., Seward, 24 July 1959, W. Suter (FSCA 8); Steeves (FSCA 1); and National Mtn., 15 March and Youngstown, 22 June 1962 (FSCA 10). 1966, S.B. Peck (MCZ 83). Jefferson Co., First definite state records. Alabama Caverns, 4 February 1961, H.R. VIRGINIA: Cumberland Co., 1.2 miles (2 Madison Co., km) SSW Columbia, 15 February & 17 March Steeves (FSCA 109). Shelta 1990, J.C. Mitchell (VMNH 4). Franklin Co., Cave (Cv.), 12 April 1965, J.E. Cooper, Sr. & 2 miles (3.2 km) N Algoma, 2 April 1958, R.L. Jr., M.L. Riser (FSCA 1) and 25 September Hoffman, R.E. Crabill, Jr. (VMNH 1). City of 1966, L. Hubricht (VMNH 16). Marion Co., Norfolk, Talbot Hall, 31 December 1959, L.J. Bear Creek, 22 June 1960, H.R. Steeves Taylor (FSCA 1). First definite state records. (FSCA 162); and Hackleburg, Davis Water NORTH CAROLINA: Macon Co., Cullasaja Mill, 25 May 1964, S. & J.W. King (FSCA 22). River Gorge nr. Van Hook Cpgd., Nantahala Marshall Co., nr. Guffey Cv., 22 March 1959 Nat. For., 9 June 1962, R.C. Graves (FSCA 3); & 27 November 1960, H.R. Steeves (FSCA and Coweeta Hydrologic Station nr. Otto, 23 14). Shelby Co., Oak Mtn. St. Pk., 26 March May 1965, S.B. Peck (FSCA 1). 1961, 22 April 1961 & 24 April 1965, H.R. SOUTH CAROLINA: Colleton Co., between Steeves, Jr. (FSCA 14, NMNH 4). Talladega Walterboro & Adams Run, December 1929, Co., Talladega Nat. For., 16 April 1960, H.R. O.F. Cook (NMNH several). Oconee Co., along Steeves (FSCA 4); and Sylacauga, 18 Septem- SC Hwy. 28 at unknown site, 29 July 1960 ber 1959, W. Suter (FSCA 19). Walker Co., nr. (AMNH 1). First definite state records. Jasper, Devil’s Ladder, 28 May 1960, H.R. GEORGIA: Atkinson Co., Pearson, 14 Sep- Steeves (FSCA 4). First definite state records. tember 1959, W. Suter (FSCA 8). Early Co., MISSISSIPPI: Forrest Co., 1.5 miles (2.4 km) Kolomoki Mounds St. Pk., 19 November 1977, from Eatonville, 1957, N.B. Causey (FSCA 1). R.M. Shelley (ZMUC 1). Fannin Co., along Kemper Co. (FMNH 1). Oktibbeha Co., 10 GA Hwy. 60, 2 miles (3.2 km) N Union Co. miles (16 km) S Starkville, Craig Springs, cot- line, 3 July 1963, R.L. Hoffman (VMNH 1). ton field, 31 December 1979, W.H. Cross Gwinnett Co., 0.5 miles (0.8 km) NW Snell- (NCSM 1). Pontotoc Co., 1 mile (1.6 km) SE ville, 24 December 1985, D.L. Stephan Ecru, 20 February 1981, W.H. Cross (MEM (NCSM 1). Lincoln Co., Elijah Clark Memor- several). Wayne Co., 5 miles (8 km) E Eucutta, 264 WESTERN NORTH AMERICAN NATURALIST [Volume 65 near Ben Martin Cv., 10 March 1963, L. Heath, 20 March 1942, H.H. Ross, Riegel Hubricht (VMNH 1). Winston Co., Louisville, (INHS 1). Putnam Co., Magnolia, 23 March 24 March 1981, R.L. Brown (MEM several). 1944, H.H. Ross (INHS 3). St. Clair Co., New state record. Marissa, 20 April 1944, H.H. Ross, M.W. San- TENNESSEE: Franklin Co., Sewanee, 9 April derson (INHS several). Sangamon Co., Sher- 1961, H.R. Steeves (FSCA 8). Morgan Co. man, 1 February 1944, M.W. Sanderson (INHS (FMNH 1). Obion Co., Reelfoot Lake St. Pk., 1). First definite state records. 28 April 1956, F.J. Etges (FSCA 1). Sevier Co., MICHIGAN: Berrien Co., Warren Dunes Great Smoky Mountains Nat. Pk., Elkmont along Lake Michigan, 30 October 1959, W. area, 8 August 1981, R.M. Shelley, H. Enghoff Suter (FSCA several). Hillsdale Co., Austin, (NCSM 3). Wilson Co., Cedars of Lebanon St. C.H. Bollman (NMNH 2). First definite state Pk., 14 April 1962, H.R. Steeves (FSCA 2). records. KENTUCKY: Edmonson Co., Mammoth Cave MISSOURI: Cole Co., Jefferson City, 29 August Nat. Pk., Mammoth Cave Hollow, 25 Septem- 1965, W.W. Dowdy (FSCA 2). Osage Co., West- ber 1960, D.E. Reichle (FSCA 31). Fayette Co., phalia, 15 November 1963, W.R. Enns (UMO Lexington, 4 February 1944, P.O. Ritcher (INHS 1). Ripley Co., 3.4 miles (5.4 km) E Orange 1), and in cave, May 1947, M.W. Sanderson Co. line on US Hwy. 160, 31 August 1977, R. (INHS several). Grayson Co., 7 miles (11.2 Chenowith (UAAM 2). First definite state km) NW Leitchfield, Rough River Lake, 27 records. May 1984, D. & M. Hildebrandt (MPM 1). ARKANSAS: Baxter Co., September 1977 Jefferson Co., Louisville, 27 September 1957, (UAAM 2). Bradley Co., 14 December 1964 R.E. Woodruff (FSCA 16). (FSCA 1). Miller Co., 1.6 miles (2.6 km) S WEST VIRGINIA: Pocahontas Co., McCloud Genoa off AR Hwy. 196, 10 March 2002, C.S. Cv., 20 April 1963, H. Zotter, N.B. Causey Harris (NCSM 1). Nevada Co., White Oak Lake (FSCA 22). First definite state record. St. Pk., 19 December 2001, C.T. McAllister OHIO: Champaign Co., 26 March 1955, (NCSM 1). Pulaski Co., Little Rock, 16 March R.E. Woodruff (FSCA 5). Jackson Co., Jack- 1962, N.B. Causey (FSCA 1). Washington Co., son (FMNH 1). Lorain Co., Oberlin, 29 July Fayetteville, 13 June 1950, N.B. Causey (FSCA 1959, W. Suter (FSCA 26). First definite state 13); Cave Creek Valley, January 1956 (FSCA 2); records. and Prairie Cove, along AR Hwy. 1, M. Hite INDIANA: Madison Co., Anderson, 25 April (FSCA 8). 1960, J.R. Rees (FSCA 1). Montgomery Co., LOUISIANA: Allen Par., 1 mile (1.6 km) N Crawfordsville (FMNH 1). Parke Co., 12.7 Reeves, along LA Hwy. 113, 20 February 1966, miles (20.3 km) N Rockville, H.S. Dybas R.E. Tandy (FSCA 2). Grant Par., Williana (FMNH 5); and 4 miles (6.4 km) W Waveland, (FMNH 1). Washington Par., 6 miles (9.6 km) along IN Hwy. 47, 27 November 1974, H.S. SW Bogalusa, 21 January 1965, N.B. Causey Dybas (FMNH 2). Porter Co., 16 April 1960, (FSCA 2). West Feliciana Par., Tunica Hills W. Suter (FSCA 1). Nature Preserve, 27 February 1971, D.A. Ross- ILLINOIS: Alexander Co., Horseshoe Lake man (FSCA 3). St. Bernard Par., Harahan, 15 Rec. Area, nr. Olive Branch, 2 December 1943, September 1944, F.G. Werner (MCZ 32). Frish, Ayars (INHS several); and Cache, 19 April OKLAHOMA: McCurtain Co., off Hwy. 259A 1944, H.H. Ross, M.W. Sanderson (INHS 2). nr. Beaver’s Bend St. Pk., 4 November 2004, Champaign Co., 2 miles (3.2 km) NE Urbana, C.T. McAllister (NCSM 14). New state record. Brownfield Woods, 1 March 1933 (INHS 1). TEXAS: Angelina Co., Lufkin, 22 August Cook Co., Chicago, 24 April 1944 (INHS 1). 1940, L. Hubricht (NMNH 1). Bowie Co., ca. De Witt Co., Weldon Springs St. Pk., 16 May 7 miles (11.2 km) SW Texarkana and 5 miles (8 1966, S.B. Peck (FSCA 17). Edgar Co., Logan, km) E Redwater, off US Hwy. 59 near NE cor- 7 March 1945, H.H. Ross, M.W. Sanderson ner of Wright Patman Lake, 11 December (INHS 1). Jackson Co., Carbondale, 10 April 2003, Z.D. Ramsey (NCSM 2). Cass Co., ca. 6 1957, J.C. Downey (JAB 1) and 2 April 1967, J. miles (9.6 km) NE Atlanta, along FM Rd. 3129, Benson (JAB 1). La Salle Co., Starved Rock 0.5 miles (0.8 km) N Bloomburg, 24 February St. Pk., 8 October 1943, H.H. Ross, M.W. 2004, Z.D. Ramsey (NCSM 1). Newton Co., Sanderson (INHS several). Piatt Co., White ca. 24 miles (38.4 km) N Newton, Canyon Rim 2005] DISTRIBUTION OF VIRGOIULUS MINUTUS 265

Trail off TX Hwy. 87, 1.6 miles (2.6 km) N jct. ______. 1888b. Catalogue of the myriapods of Indiana. FM Rd. R255 and 10.2 miles (16.3 km) N TX Proceedings of the United States National Museum 11:403–410. Hwy. 63 [15R 0430457 3442649], 7 October ______. 1888c. A preliminary list of the myriapods of 2004, R.M. Shelley (NCSM 1); and ca. 12 miles Arkansas, with descriptions of new species. Entomo- (19.2 km) NE Newton, Wild Azalea Trail off logica Americana 4:1–8. FM Rd. 1414, 6.7 miles (10.7 km) N jct. TX ______. 1893. The Myriapoda of North America. United Hwy. 87 [15R 0442598 3418623], 7 October States National Museum Bulletin 46:1–210. BRANDT, J.F. 1841. Generis Juli specierum enumeratio, 2004, R.M. Shelley (NCSM 1). Rusk Co., 2.2 adjectis plurium, quae hucusque nondum innotuerunt miles (3.5 km) E Mt. Enterprise, Griff Ross specierum brevibus descriptionibus ad Musei Acad- Trail off US Hwy. 84 [15R 034452 3532802], 6 emiae Scientarum Petropolitanae specimina factis. October 2004, R.M. Shelley (NCSM 5). New Bulletin Scientifique Publié par l’Académie Impéri- state record. ale des Sciences de St. Pétersbourg 8:97–127. CAUSEY, N.B. 1940. Ecological and systematic studies on There is also a sample with 8 females (MCZ) North Carolina myriapods. Unpublished doctoral that was collected in September 1904 at dissertation, Zoology Department, Duke University, “Anechar,” New York, which is believed to be Durham, NC. 181 pp. a misspelling for “Arrochar,” a neighborhood ______. 1963. Additional records of Louisiana millipeds. Proceedings of the Louisiana Academy of Science in Staten Island, Richmond County; because it 26:76–79. is around the same latitude as the northern- CHAMBERLIN, R.V. 1921. The Julidae and Isobatidae in most records in Illinois, Indiana, and Ohio, we North America. Proceedings of the Biological Soci- place a dot here in Figure 1. The species is not ety of Washington 34:81–84. known definitely from central and western ______. 1922. Further notes on the nomenclature of North American Julidae and Nemasomidae. Proceedings of New York, or from a latitude north of Berrien the Biological Society of Washington 35:7–10. County, Michigan. ______. 1940. On some chilopods and diplopods from North Carolina. Canadian Entomologist 72:56–59. ACKNOWLEDGMENTS ______. 1943a. Some records and descriptions of Ameri- can diplopods. Proceedings of the Biological Society We thank the following professors, cura- of Washington 56:143–152. ______. 1943b. On Mexican millipeds. Bulletin of the Uni- tors, and collection managers for providing versity of Utah 34(7) [Biological Series 8]:1–103. access to or loaning specimens to the 2nd ______. 1951. Records of American millipeds and cen- author: N.I. Platnick (AMNH), D. Summers tipeds collected by Dr. D. Elden Beck in 1950. Great (FMNH), G.B. Edwards (FSCA), K. Methven Basin Naturalist 11:27–35. (INHS), L. Leibensperger (MCZ), T.L. Schief- ______. 1952. Further records and descriptions of Ameri- fer (MEM), J.P. Jass (MPM), J.A. Coddington can millipeds. Great Basin Naturalist 12:13–34. CHAMBERLIN, R.V., AND R.L. HOFFMAN. 1958. Checklist of (NMNH), J.K. Barnes (UAAM), R.W. Sites the millipeds of North America. United States National (UMO), and R.L. Hoffman (VMNH). We also Museum Bulletin 212:1–236. thank J.A. Beatty for loaning samples in his ENGHOFF, H. 1979. The millipede genus Okeanobates private collection; J.T. McAllister III, C. Harris, (Diplopoda, Julida: Nemasomatidae). Steenstrupia 5(9):161–178. J. Hollis, and J.E. Kessler for assistance in col- ______. 1984a. A revision of the Nopoiulinae, with notes lecting; J. Hannik for placing the locality in on the classification of blaniulid millipeds (Diplo- New York; and H. Robison for advising us that poda: Julida: Blaniulidae). Senckenbergiana Biolog- “Argenta,” Arkansas, is actually North Little ica 64:393–427. Rock. The 1st author’s fieldwork was supported ______. 1984b. Revision of the millipede genus Choneiu- lus (Diplopoda, Julida, Blaniulidae). Steenstrupia in part by TAMU-T Faculty Senate Research 10(6):193–203. Enhancement Grant 200900. ______. 1985. The millipede family Nemasomatidae. With the description of a new genus, and a revision of LITERATURE CITED Orinisobates (Diplopoda: Julida). Entomologica Scan- dinavica 16:27–67. BAILEY, J.W. 1928. The Chilopoda of New York state with ENGHOFF, H., AND R.M. SHELLEY. 1979. A revision of the notes on the Diplopoda. New York State Museum millipede genus Nopoiulus (Diplopoda, Julida: Blan- Bulletin 276:5–50. iulidae). Entomologica Scandinavica 10:65–72. BOLLMAN, C.H. 1887. Notes on North American Julidae. FILKA, M.E., AND R.M. SHELLEY. 1980. The milliped fauna Annals of the New York Academy of Sciences 4: of the Kings Mountain region of North Carolina 25–44. (Arthropoda: Diplopoda). Brimleyana 4:1–42. ______. 1888a. Notes on a collection of Myriapoda from GOLOVATCH, S.I., AND R.L. HOFFMAN. 2000. On the diplo- Mossy Creek Tenn., with a description of a new pod taxa and type material of J.F. Brandt, with some species. Proceedings of the United States National descriptions and identities (Diplopoda). Fragmenta Museum 11:339–342. Faunistica Warsazawa 43(Supplement):229–249. 266 WESTERN NORTH AMERICAN NATURALIST [Volume 65

HOFFMAN, R.L. 1999. Checklist of the millipeds of North ______. 1990. A new milliped of the genus Metaxycheir and Middle America. Virginia Museum of Natural from the Pacific coast of Canada (Polydesmida: Xys- History Special Publication 8:1–584. todesmidae), with remarks on the tribe Chonaphini JAWLOWSKI, H. 1930. On European Diplopoda introduced and the western Canadian and Alaskan diplopod to America. Fragmenta Faunistica Musei Zoologici fauna. Canadian Journal of Zoologyy 68:2310–2322. Polonici 1(7):181–185. ______. 2000. Annotated checklist of the millipeds of North JOHNSON, B.M. 1954. The millipeds of Michigan. Papers Carolina (Arthropoda: Diplopoda), with remarks on of the Michigan Academy of Science, Arts, and Let- the genus Sigmoria Chamberlin (Polydesmida: Xys- ters 39:241–252. todesmidae). Journal of the Elisha Mitchell Scien- LOOMIS, H.F. 1944. Millipeds principally collected by Pro- tific Society 116(3):177–205. fessor V.E. Shelford in the eastern and southeastern ______. 2001 (2000). Annotated checklist of the millipeds states. Psyche 51(3–4):166–177. of Florida (Arthropoda: Diplopoda). Insecta Mundi ______. 1968. A checklist of the millipeds of Mexico and 14(4):241–251. Central America. United States National Museum ______. 2002. The millipeds of central Canada (Arthro- Bulletin 266:1–137. poda: Diplopoda), with reviews of the Canadian fauna MCALLISTER, C.T., C.S. HARRIS, R.M. SHELLEY, AND J.T. and diplopod faunistic studies. Canadian Journal of MCALLISTER III. 2002. Millipeds (Arthropoda: Diplo- Zoology 80:1863–1875. poda) of the Ark-La-Tex. I. New distributional and SHELLEY, R.M., C.T. MCALLISTER, AND S.B. SMITH. 2004 state records for seven counties of the west Gulf (2003). Discovery of the milliped Pleuroloma flavipes Coastal Plain of Arkansas. Journal of the Arkansas (Polydesmida: Xystodesmidae) in Texas, and other Academy of Science 56:91–94. records from west of the Mississippi River. Entomo- MCALLISTER, C.T., R.M. SHELLEY, AND J.T. MCALLISTER logical News 114:2–6. III. 2003. Millipeds (Arthropoda: Diplopoda) of the SHELLEY, R.M., C.T. MCALLISTER, AND Z.D. RAMSEY. 2005. Ark-La-Tex. III. Additional records from Arkansas. Discovery of the milliped, Scytonotus granulatus Journal of the Arkansas Academy of Science 57: (Say, 1821), in Oklahoma and Alabama, with a review 115–121. of its distribution (Polydesmida: Polydesmidae). West- MCNEILL, J. 1887. List of the myriapods found in Escam- ern North American Naturalist 65:112–117. bia County, Florida, with descriptions of six new SNIDER, R.M. 1991. Updated species lists and distribution species. Proceedings of the United States National records for the Diplopoda and Chilopoda of Michi- Museum 10:323–327. gan. Michigan Academician 24:177–194. NEWPORT, G. 1844. A list of the species of Myriapoda, WILLIAMS, S.R., AND R.A. HEFNER. 1928. The millipedes order Chilognatha, contained in the cabinets of the and centipedes of Ohio. Ohio State University Bul- British Museum, with descriptions of a new genus letin 23(7) [Ohio Biological Survey Bulletin 18]: and thirty-two new species. Annals and Magazine of 91–146. Natural History 13:263–270. WOOD, H.C. 1865. The Myriapoda of North America. SAY, T. 1821. Descriptions of the Myriapodae of the United Transactions of the American Philosophical Society States. Journal of the Academy of Natural Sciences, 13:137–248. Philadelphia 2:102–114. WRAY, D.L. 1967. Insects of North Carolina. 3rd supple- SHELLEY, R.M. 1978a. Millipeds of the eastern Piedmont ment. North Carolina Department of Agriculture, region of North Carolina, U.S.A. (Diplopoda). Jour- Division of Entomology, Raleigh. 181 pp. nal of Natural History 12:37–79. ______. 1978b. Class Diplopoda. Pages 222–223 in R.G. Received 30 April 2004 Zingmark, editor, An annotated checklist of the biota Accepted 3 August 2004 of the coastal zone of South Carolina. University of South Carolina Press, Columbia. 364 pp. ______. 1988. The millipeds of eastern Canada (Arthro- poda: Diplopoda). Canadian Journal of Zoology 66: 1638–1663. Western North American Naturalist 65(2), © 2005, pp. 267–268

DEFENSE OF PRONGHORN FAWNS BY ADULT MALE PRONGHORN AGAINST COYOTES

Kim Murray Berger1,2

Key words: pronghorn, Antilocapra americana, coyote, Canis latrans, juvenile defense.

Adult male pronghorn (Antilocapra ameri- began moving directly away from the prong- cana) have never been reported defending horn. The female pronghorn immediately re- fawns against predators (Marion and Sexton initiated the chase (1205 MST), and the male 1979, Byers 1997). Lipetz and Bekoff (1980) promptly stood and followed. The 2 prong- observed male pronghorn participating in coy- horn pursued the coyote for over 1 km, at which ote chases. However, they were uncertain of point all 3 animals left my range of view (1225 the motivation and suggested that males may MST). only appear to participate in chases and may Both pronghorn remained out of sight for actually be trying to stop females from leaving nearly an hour before returning concurrently their territories. I report here 2 instances in to the vicinity of the pre-encounter location of which an adult male pronghorn assisted female the female (1330 MST). The male began brows- pronghorn in defending fawns against searching ing, while the female commenced the vigilant coyotes (Canis latrans) in Grand Teton National behavior characteristic of mothers with hidden Park in northwestern Wyoming (43°39′N, fawns (Byers 1997). At 1426 MST, the female 110°40′W). reunited with her fawn, which had been hid- The 1st instance occurred on 16 June 2001 ing less than 100 m from the area where the while I was conducting a focal observation of a coyote had been searching. radio-collared female pronghorn to determine The 2nd instance occurred on 8 June 2004 the survival status of her fawn. At 1015 MST while I was observing 2 females (~200 m apart; the female became extremely agitated when hereafter female A and female B) to identify she noticed a coyote searching the vegetation the bedsite locations of their fawns to capture 50 m away from her. The pronghorn immedi- the fawns for radio-collaring. I already knew ately ran toward the coyote, repeatedly charg- the bedsite location of 1 fawn belonging to ing it in an attempt to drive it away from the female A because I had collared the fawn ear- area. A solitary adult male pronghorn had been lier that same day (1018 MST). At approxi- browsing approximately 0.4 km from the female. mately 1130 MST, female A reunited with her When the female began charging the coyote, uncollared fawn and allowed it to nurse. the male ceased feeding, trotted toward the Approximately 15 minutes later (1145 MST), female, and joined in the chase (1017 MST). female B also reunited with an uncollared fawn The 2 pronghorn succeeded in displacing the and allowed it to nurse. At this point I knew coyote 0.5 km from its location at the begin- the locations of 3 fawns, the fawn I had previ- ning of the encounter, whereupon it adopted a ously radio-collared plus the 2 uncollared fawns defensive, reclining posture in a shallow irriga- that had recently nursed and had subsequently tion ditch (1045 MST). For the next hour both reclined at new bedsites. pronghorn alternately stood next to, and circled, At 1210 MST, 2 coyotes approached within the reclining coyote. The pronghorn finally 150 m of the bedsite of the uncollared fawn moved about 30 m away, and the male prong- belonging to female A. Female A noticed the horn bedded down (1150 MST). The coyote coyotes and ran toward them. Female B also took this opportunity to leave the ditch and noticed the coyotes and ran to join female A.

1Wildlife Conservation Society, North America Program, Box 985, Victor, ID 83455. 2Department of Forest, Range, and Wildlife Sciences, Utah State University, Logan, UT 84321.

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Together, the 2 females began charging at the the male pronghorn was defending the male coyotes in an attempt to drive them from the or female fawn, or both, is unknown. Second, area. A solitary adult male pronghorn that had if coyotes that are recipients of male-directed been browsing in the vicinity of female A (100 aggression are more hesitant to attack prong- m away) trotted toward the 2 females (1215 horn in the future, then the behavior might be MST). The 3 pronghorn adopted a triangular explained by a purely selfish model. However, formation, with the male at the apex and the previous harassment did not appear to deter females flanking the male on either side. The coyotes from future interactions with prong- male pronghorn took up the primary defense, horn (Lipetz and Bekoff 1980). Third, male charging at the coyotes with his head lowered. pronghorn may only appear to harass coyotes Whenever a coyote succeeded in getting past and may actually be trying to stop females the male, the female on that side would step from leaving their territories (Lipetz and Bekoff forward to assist in the defense. All 3 prong- 1980). This latter supposition appears unlikely horn kept up the harassment for nearly an as there was no effort by the 2 females in- hour, at which point the coyotes left the area volved in the 2nd incidence to leave the area, (1310 MST). and the aggression exhibited by the male prong- That defense of fawns by male pronghorn horn was clearly directed at the coyotes. has not previously been reported is perhaps a A fuller understanding of the underlying result of both the isolation of females that cause(s) of male-directed aggression toward tends to occur at parturition and the difficulty coyotes will require further investigation. in knowing whether hidden fawns are present Irrespective of the cause, the observations when male pronghorn are observed harassing reported here demonstrate that male prong- coyotes. Why male pronghorn engage in fawn horn, in addition to females, do defend fawns defense is a different issue. Variation in life- from predators. time reproductive success among pronghorn males is largely a result of differences in off- This work was funded by the Biological spring survival (Byers 1997). Consequently, in Resources Division of the U.S. Geological areas where fawn mortality is chiefly attribut- Survey under Cooperative Agreement able to predation, reproductive males might 01CRAG0031, and Earth Friends Foundation. increase their own fitness by defending from I thank Joel Berger for discussions and Mike predators fawns they sired. However, for this Oehler, Becky Pierce, and an anonymous to be a satisfactory explanation of the interac- reviewer for helpful comments. tions I described, males would either have to recognize their offspring or have a high proba- LITERATURE CITED bility of being in areas where females bore their offspring. Evidence in support of these BERGER, J. 1986. Wild horses of the Great Basin: social regulation and population size. University of Chicago suppositions is weak given the ephemeral Press, Chicago, IL. 326 pp. nature of social groups, which, as is the case BYERS, J.A. 1997. American pronghorn: social adaptations with most polygynous ungulates, precludes de- and the ghosts of predators past. University of Chicago termination of paternity (Sinclair 1979, Berger Press, Chicago, IL. 300 pp. 1986, Byers 1997). LIPETZ, V.E., AND M. BEKOFF. 1980. Possible function of predator harassment in pronghorn antelopes. Jour- Several alternatives might also explain why nal of Mammalogy 61:741–743. male pronghorn engage in fawn defense. First, MARION, K.R., AND O.J. SEXTON. 1979. Protective behav- nonpaternal males might protect fawns as a ior by male pronghorn, Antilocapra americana form of future reproductive investment because (Artiodactyla). Southwestern Naturalist 24:709–10. SINCLAIR, A.R.E. 1979. The African buffalo: a study of re- opportunities for mating increase with a source limitation of populations. University of Chicago greater number of surviving females. This idea Press, Chicago, IL. 355 pp. suggests that males should defend female rather than male fawns. In the 2nd observa- Received 5 February 2004 tion reported above, the 2 fawns closest to the Accepted 28 October 2004 coyotes were a male and a female. Whether Western North American Naturalist 65(2), © 2005, pp. 269–273

REFUGIA FROM BROWSING AS REFERENCE SITES FOR RESTORATION PLANNING

William J. Ripple1,2 and Robert L. Beschta1

Key words: refugia, ungulate browsing, woody browse species, predation risk, livestock grazing

In the western U.S., deciduous woody species times have had significant impacts on vegeta- along riparian systems provide important eco- tion (National Research Council 2002a). Thus, logical functions. For example, they stabilize there is an increased need for restoration of stream banks and impart hydraulic resistance deciduous woody species at landscape scales. during overbank flows, enhance deposition of Such restorations would be facilitated if refer- organic matter and fine sediment on floodplains, ence sites existed that were relatively unim- support general food webs of aquatic and ripar- pacted by ungulate herbivory (i.e., refugia) since ian organisms, moderate water temperatures they (1) can provide an understanding of vege- and microclimates, and recruit large wood tation dynamics without the effects of her- (National Research Council 2002b). Measures bivory, (2) help define the degree and extent of of biodiversity, biomass, and number of rare degradation in woody plant communities for species are often much greater in riparian habi- other portions of a landscape, (3) may assist in tats than on adjacent uplands (Knopf et al. 1988). setting restoration priorities, and (4) may provide Deciduous woody species on upland sites pro- important “targets” for restoration programs. vide for watershed protection, aesthetics, wood In landscapes that have experienced the fiber, and habitats that also help support a effects of widespread and sustained herbivory wide variety of wildlife and avian species (Bar- from ungulates (either domestic or wild), refu- tos 2001, National Research Council 2002a). gia from browsing can be created with fenced Despite their significance to western ecosys- exclosures (Brookshire et al. 2002, Sarr 2002), tems, deciduous woody species have been in provided that sufficient seed or bud banks re- decline (Braatne et al. 1996, Kay 1997, Bartos main. Unfortunately, such exclosures are seldom 2001). Many western riparian systems have available. Yet, even within a heavily browsed been diminished in total area (Swift 1984) while landscape we suggest there will often exist many that remain often have been altered or scattered refugia sites with deciduous woody degraded by various human activities and land species; such sites are often small in area but uses (Wigington and Beschta 2000). may contain a relatively diverse plant commu- While the causes of loss and alteration of nity structure and composition. Where such woody species during a period of increasing refugia have persisted is notable as they typi- Euro-American influence are multiple, high cally occur in locations where there are multi- levels of herbivory from domestic ungulates ple impediments to ungulate access. The im- have often degraded ecosystem structure and portance of these sites is that they provide a function. Such degradation includes impacts glimpse of the potential structure and compo- to habitats of numerous species of vertebrates sition of plant communities where ungulate and invertebrates, various food web interac- herbivory is not of overriding significance and tions, and nutrient cycling (Fleischner 1994, may represent an initial approximation of what Braatne et al. 1996, Belsky and Blumenthal other areas in a landscape might become if 1997, Donahue 1999, Rooney and Waller 2003). herbivory levels were reduced or curtailed. Even where land has been set aside within the Because refugia are often visually different National Park system, native ungulates some- (e.g., high contrast, taller plants, higher plant

1College of Forestry, Oregon State University, Corvallis, OR 97331. 2Corresponding author.

269 270 WESTERN NORTH AMERICAN NATURALIST [Volume 65 densities) relative to the general landscape, servation because of cascading effects upon they are typically easy to locate. In the follow- lower trophic levels (Smith et al. 2003, Ripple ing discussion, we identify numerous types of and Beschta 2004). Refugia created through “impediments” to browsing that have contrib- risk-sensitive foraging involve predator/prey uted to the maintenance of refugia. interactions whereby areas of low browsing Several studies have described the role of intensity occur, either in conjunction with exist- natural physical barriers to animal movement ing physical barriers or independent of them. in creating refugia. At the microsite scale, Changes in prey behavior due to the presence Rooney (1997) described how herbaceous veg- of predators are referred to as predation-risk etation growing on the tops of boulders effects. These behavioral modifications include escaped deer browsing. Schreiner et al. (1996) changes in habitat use, patch selection, and discovered shrub refugia behind log barriers choices of feeding sites (Lima and Dill 1990). created by fallen conifers in Olympic National This process can produce low populations of Park. They found several species of shrubs in herbivores in a predator’s core use area, thus these refugia that successfully produced flow- creating refugia for woody browse species ers and fruit unlike the majority of the shrubs through lower herbivory. For example, in re- growing nearby in the open. They concluded sponse to the presence of predators, researchers that these refugial shrub patches may provide have documented increased concentrations of critical seed sources for recolonization of the ungulates in buffer zones away from both mam- floodplain by species that might otherwise be malian predators (Mech 1977, White et al. 1998, absent. Ripple and Larsen (2001) found that Ripple et al. 2001) and human hunters (Lalib- fallen conifers killed by the 1988 fires in Yel- erte and Ripple 2003). lowstone National Park could be dense enough Predation-risk effects on prey animals, in to provide local refugia, allowing aspen recruit- combination with varying terrain conditions, ment with high levels of ungulate browsing can also create “invisible impediments” to nearby (Fig. 1). Beschta and Ripple (2005) iden- browsing and have apparently been caused by tified increased cottonwood recruitment occur- sport hunters as well as wolves. For example, ring between highways and terrain features St. John (1995) concluded that aspen stands such as steep slopes and rivers that reduced within 500 m of roads were less impacted by the presence of animals. Larsen and Ripple wild ungulates than those farther away, suggest- (2003) discovered a lack of aspen recruitment ing that elk adjusted their foraging behavior to across the northern range in Yellowstone avoid human contact and possible predation National Park except for stands growing in the by humans. Other researchers found that aspen midst of scree deposits. They concluded that were heavily browsed on U.S. Air Force land the scree protected the aspen from ungulate that was utilized year-round by a large elk browsing. The scale of the refugia in the above population but where sport hunting was not case studies ranges from 1 to several thousand permitted. Conversely, this property is sur- square meters. Yet, physical barriers also have rounded by national forest land where hunting been described at much larger scales where is allowed and the aspen stands were mini- terrain features such as mesas and buttes im- mally browsed (McCain et al. 2003). peded ungulate access and created refugia Ripple and Beschta (2003) proposed that, (Jameson et al. 1962, Ambos et al. 2000). following the reintroduction of wolves in Yel- It is important to recognize that the wide- lowstone National Park, a “terrain fear factor” spread loss of major predators such a wolves has been playing an important role in the (Canis lupus) early in the 20th century allowed selective release of cottonwood and willow ungulates to browse with a reduced threat of from long-term browsing suppression by elk. predation. In addition to the often widespread In their predation-risk hypothesis, they sug- effects of domestic ungulates, woody plant gested that elk would increasingly forage at communities can be profoundly affected by sites that allow early detection, avoidance, and native ungulates when top predators are re- successful escape from wolves. They found moved from ecosystems (Leopold et al. 1947, cottonwood and willow to be releasing at Terborgh et al. 1999, Ripple and Larsen 2000, potentially high-risk sites with limited visibil- Beschta 2003, Soulé et al. 2003) and evidence ity of approaching wolves and/or with terrain is growing on the importance of predator con- impediments to escape from an attack, such as 2005] NOTES 271

Fig. 1. Protected aspen sprouts growing among coarse woody debris on the Blacktail Plateau in Yellowstone National Park (example of a physical barrier to browsing). See Ripple and Larsen (2001) for details on aspen recruitment in locations where dead trees have created a jackstraw barrier to ungulate movement. In 2003 the aspen sapling to the left of the white pole was approximately 4 m tall (see arrow), while aspen sprouts growing nearby outside the woody debris were less than 1 m tall. high terraces, steep cutbanks, and nearby gul- represent atypical conditions for pre-European lies (Fig. 2). plant communities. There are several limitations to the use of Realizing the potential limitations of local refugia as reference sites. Because they are refugia as examples of these conditions, we typically of limited size and spatial distribu- nevertheless suggest that the identification tion, their locations may not be representative and use of refugia can be important in under- of the broader landscape (i.e., different abiotic standing the role of ungulate herbivory on conditions, geographically or topographically western landscapes and their potential for re- biased). In such situations they provide little covery. We propose 3 situations where refugia opportunity for developing statistical inferences. for deciduous woody browse species are likely Refugia may maintain certain rare species, but to persist: (1) Where the browsing is predomi- in some cases overall community composition nantly from domestic ungulates, physical bar- and functioning can be different from the larger riers to site access will control the occurrence landscape in need of restoration. Information of refugia. (2) Where wild ungulates are pre- identifying the historical level of ungulate use sent but natural predators are not, both physi- often is lacking for these sites, and levels of cal barriers and predation risk associated with browsing may be occurring, of which a certain human hunting will tend to control the occur- amount would represent a natural condition rence of refugia. (3) Where natural predators (e.g., Schreiner et al. 1996). Finally, a total lack have a significant presence, physical barriers of browsing (such as a fenced exclosure) might and terrain features that affect the perceived 272 WESTERN NORTH AMERICAN NATURALIST [Volume 65

Fig. 2. Willow and cottonwood recruitment occurring on an island of the Lamar River in northern Yellowstone National Park. This island is considered to be an area of high predation risk (example of an invisible impediment to browsing). See Ripple and Beschta (2003) for details on how the plants on this island were released, due to changes in elk browsing patterns, after the reintroduction of wolves in the mid-1990s. In contrast, stream banks in the low-predation-risk area extending from the island toward the distant mature cottonwood stands on the floodplain (right center of photograph) have no recruiting willows or cottonwood. The mature cottonwood stands also occupy low-risk sites, and cottonwood recruitment was essentially terminated after wolves were extirpated from the park in the mid-1920s (Beschta 2003).

predation risk of prey animals at varying spatial LITERATURE CITED scales will influence the number, size, and spatial distribution of refugia. While the occur- AMBOS, N., G. ROBERTSON, AND J. DOUGLAS. 2000. Dutch- woman Butte: a relict grassland in Arizona. Range- rence of refugia may be sufficiently common lands 22:3–8. in some landscapes to provide adequate refer- BARTOS, D.L. 2001. Landscape dynamics of aspen and ence sites for restoration purposes, additional conifer forests. Pages 5–13 in Sustaining aspen in sites could be targeted for livestock or native western landscapes: symposium proceedings. USDA Forest Service Proceedings RM-RS-P-18. ungulate exclusion using fenced exclosures to BELSKY, A.J., AND D.M. BLUMENTHAL. 1997. Effects of live- ensure a full portfolio of reference sites. In stock grazing on stand dynamics and soils in upland some extreme cases, refugia might be the only forest of the interior West. Conservation Biology 11: places where certain native species still occur, 315–327. BESCHTA, R.L. 2003. Cottonwood, elk, and wolves in the and these sites can serve as important genetic Lamar Valley of Yellowstone National Park. Ecologi- repositories. We suggest that identification of cal Applications 13:1295–1309. refugia across watersheds and landscapes is BESCHTA, R.L., AND W. J. R IPPLE. 2005. Rapid assessment needed to better understand reference condi- of riparian cottonwoods: Middle Fork John Day River, northeastern Oregon. Ecological Restoration 23: In tions for woody browse species that may have press. existed prior to the widespread influences of BRAATNE, J.H., S.B. ROOD, AND P.E. HEILMAN. 1996. Life domestic ungulates and the effects of native history, ecology, and conservation of riparian cotton- ungulates where major predators have been woods in North America. Pages 57–85 in R.F. Stet- tler, H.D. Bradshaw, Jr., P.E. Heilman, and T.M. extirpated. Hinckley, editors, Biology of Populus and its implications for management and conservation. National The authors thank Daniel Sarr, 2 anony- Research Council of Canada, Ottawa, ON, Canada. mous reviewers, and an associate editor for BROOKSHIRE, E.N.J., J.B. KAUFFMAN, D. LYTJEN, AND N. OTTING. 2002. Cumulative effects of wild ungulate providing helpful comments on an early draft and livestock herbivory on riparian willows. Oecolo- of this paper. gia 132:559–566. 2005] NOTES 273

DONAHUE, D.L. 1999. The western range revisited. Uni- lowstone National Park. Forest Ecology and Man- versity of Oklahoma Press, Norman. agement 184:299–313. FLEISCHNER, T.L. 1994. Ecological costs of livestock graz- ______. 2004. Wolves and the ecology of fear: can preda- ing in western North America. Conservation Biology tion risk structure ecosystems? BioScience 54:755– 8:629–644. 766. JAMESON, D.A., J.A. WILLIAMS, AND E.W. WILTON. 1962. ROONEY, T.P. 1997. Escaping herbivory: refuge effects on Vegetation and soils of Fishtail Mesa, Arizona. Ecol- the morphology and shoot demography of the clonal ogy 43:403–410. forest herb Maianthemum canadens. Journal of the KAY, C.E. 1997. Is aspen doomed? Journal of Forestry Torrey Botanical Society 124:280–285. 95:4–11. ROONEY, T.P., AND D.M. WALLER. 2003. Direct and indi- KNOPF, F.L., R.R. JOHNSON, T. RICH, F.B. SAMSON, AND R.C. rect effects of white-tailed deer in forest ecosystems. SZARO. 1988. Conservation of riparian ecosystems in Forest Ecology and Management 181:165–176. the United States. Wilson Bulletin 100:272–284. SARR, D.A. 2002. Riparian livestock exclosure research in LALIBERTE, A.S., AND W. J. R IPPLE. 2003. Wildlife encoun- the western United States: a critique and some rec- ters by Lewis and Clark: a spatial analysis of Native ommendations. Environmental Management 30: American/wildlife interactions. Bioscience 53:994– 516–526. 1003. SCHREINER, E.G., K.A. KRUEGER, P.J. HAPPE, AND D.B. LARSEN, E.J., AND W. J. R IPPLE. 2003. Aspen age structure HOUSTON. 1996. Understory patch dynamics and in the northern Yellowstone ecosystem: USA. Forest ungulate herbivory in old-growth forests of Olympic Ecology and Management 179:469–482. National Park, Washington. Canadian Journal of For- LEOPOLD, A., L.K. SOWLS, AND D.L. SPENCER. 1947. A sur- est Research 26:255–265. vey of over-populated deer ranges in the United SMITH, D.W., R.O. PETERSON, AND D.B. HOUSTON. 2003. States. Journal of Wildlife Management 11:162–183. Yellowstone after wolves. Bioscience 53:330–340. LIMA, S.L., AND L.M. DILL. 1990. Behavioral decisions SOULÉ, M.E., J.A. ESTES, J. BERGER, AND C. MARTINEZ made under the risk of predation: a review and pros- DEL RIO. 2003. Ecological effectiveness: conserva- pectus. Canadian Journal of Zoology 68:619–640. tion goals for interactive species. Conservation Biol- MCCAIN, E.B., J.I. ZLOTOFF, AND J.J. EBERSOLE. 2003. ogy 17:1238–1250. Effects of elk browsing on aspen stand characteristics, ST. JOHN, R.A. 1995. Aspen stand recruitment and ungu- Rampart Range, Colorado. Western North American late impacts: Gardiner Ranger District, Gardiner. Naturalist 63:129–132. Master’s thesis, University of Montana, Missoula. MECH, L.D. 1977. Wolf-pack buffer zones as prey reser- SWIFT, B.L. 1984. Status of riparian ecosystems in the voirs. Science 198:320–321. United States. Water Resources Bulletin 20:223–228. NATIONAL RESEARCH COUNCIL. 2002a. Ecological dynam- TERBORGH, J., J.A. ESTES, P. PAQUET, K. RALLS, D. BOYD- ics on Yellowstone’s Northern Range. National Acad- HEIGHER, B.J. MILLER, AND R.F. NOSS. 1999. The emy Press, Washington, DC. role of top carnivores in regulating terrestrial ecosys- ______. 2002b. Riparian areas: functions and strategies for tems. Pages 39–64 in J. Terborgh and M. Soulé, edi- management. National Academy Press, Washington, tors, Continental conservation: scientific foundations DC. of regional reserve networks. Island Press, Washing- RIPPLE, W.J., AND E.J. LARSEN. 2000. Historic aspen recruit- ton, DC. ment, elk, and wolves in northern Yellowstone Na- WHITE, C.A., C.E. OLMSTED, AND C.E. KAY. 1998. Aspen, tional Park, USA. Biological Conservation 95:361–370. elk, and fire in the Rocky Mountain national parks of ______. 2001. The role of coarse woody debris in aspen North America. Wildlife Society Bulletin 26:449–462. regeneration. Western Journal of Applied Forestry WIGINGTON, W.J., AND R.L. BESCHTA, EDITORS. 2000. 16:61–64. Riparian ecology and management in multi-land use RIPPLE, W.J., E.J. LARSEN, R.A. RENKIN, AND D.W. SMITH. watersheds. American Water Resources Association, 2001. Trophic cascades among wolves, elk, and aspen Bethesda, MD. on Yellowstone National Park’s northern range. Bio- logical Conservation 102:227–234. Received 3 January 2004 RIPPLE, W.J., AND R.L. BESCHTA. 2003. Wolf reintroduc- Accepted 28 June 2004 tion, predation risk, and cottonwood recovery in Yel- Western North American Naturalist 65(2), © 2005, pp. 274–277

IMPACT OF A CATASTROPHIC FLOODING EVENT ON RIPARIAN BIRDS

Natalie J. S. Turley1 and Anthonie M. A. Holthuijzen1

Key words: birds, flooding, disturbance, site tenacity, riparian, catastrophic disturbance, Hells Canyon.

Few studies have evaluated the impacts of River. Riparian vegetation cover types generally flooding on riparian bird communities (Brown followed the classification system described and Johnson 1987, Knopf and Sedgwick 1987). by Cowardin et al. (1979) and modified for Most research has focused on inundation of Habitat Evaluation Procedures (HEP; U.S. the riparian zone rather than structurally dev- Fish and Wildlife Service 1981). Each plot was astating flooding events. Floods in mountain permanently marked and coordinates were streams are often brief and catastrophic, due to established using a Global Positioning System rapid movement of water, coarse sediment, and (Geo Explorer II, Trimble Navigation Limited, woody debris down steep slopes and channels Sunnyvale, CA). During January 1997, twenty- (Swanson et al. 1998). Here, we describe the seven plots located in 8 tributaries experi- effect of a catastrophic flooding event on ripar- enced high to severe flooding disturbance. ian bird communities in west central Idaho Flood damage was patchy within a tributary, and northeastern Oregon. This event provided with damaged or even completely denuded us with an opportunity to compare bird com- patches interspersed with undamaged ones. munities at riparian sites before and after flood Vegetation at 8 plots was categorized as “highly damage. Specifically, we investigated whether disturbed” and at 19 plots as “severely dis- overall bird abundances and individual species turbed.” In “highly disturbed” plots most her- abundances differed at sites pre- (1995, 1996) baceous, small- and larger-diameter woody and post-flood (1997, 1998). species were impacted, whereas at “severely We conducted our research along tribu- disturbed” plots nearly all vegetation was taries to the Snake River in the Hells Canyon removed. reach, situated in west central Idaho and north- In 1995 we measured shrub and tree cover eastern Oregon. Moderate to steep slopes at 13 of 27 plots that were flooded in 1997; characterize the area. Grasslands and upland these 13 plots were resampled in 1998 (6 shrub habitat are interspersed and found up- highly disturbed and 7 severely disturbed). slope of the riparian zone. White alder (Alnus We used the line-intercept method (Müller- rhombifolia) was the most common tree species Dombois and Ellenberg 1974) to determine found in the riparian communities sampled. percent canopy cover for the shrub and tree Other common tree and shrub species included layers. Tree and shrub canopies, identified to netleaf hackberry (Celtis reticulata), rocky species, were projected vertically to the tape, mountain maple (Acer glabrum), hawthorn and the length of line segments covered by (Crataegus spp.), blue elderberry (Sambucus woody plant species was recorded (Hays et al. cerulea), poison ivy (Toxicodendron rydbergii), 1981). We used simple paired t tests to evalu- and chokecherry (Prunus virginiana). ate percent tree and shrub canopy cover pre- In 1995, as part of a larger study (Turley and and post-flood. Average percent shrub cover Holthuijzen 2000), we established 288 bird was higher before flooding in 1995 (80.3%) survey plots in homogenous patches of Forested than after flooding in 1998 (20.4%; 1-tailed Wetland and Scrub-Shrub Wetland habitat paired t test: t =4.90, P < 0.001). Likewise, cover types along 57 tributaries to the Snake average percent tree cover was higher before

1Idaho Power Company, Environmental Affairs Department, Box 70, Boise, ID 83707.

274 2005] NOTES 275

TABLE 1. Number of plots at which a species was observed and relative abundance (birds/count and standard errors) of 8 bird species at 27 plots in Hells Canyon, Idaho and Oregon, 1995–96 and 1997–98.

b ______Number of plots ______Relative abundances Foraging Pre-flood Post-flood Pre-flood Post-flood Species guilda (1995–96) (1997–98) (1995–96) (1997–98) P-value Lazuli Bunting LCF 10 15 0.29 (0.06) 0.42 (0.08) 0.226 (Passerina amoena) Yellow-breasted Chat LCF 5 4 0.11 (0.04) 0.07 (0.03) 0.742 (Icteria virens) Black-capped Chickadee LCG 9 3 0.24 (0.08) 0.06 (0.03) 0.078 (Poecile atricapilla) Yellow Warbler LCG 9 2 0.20 (0.05) 0.03 (0.03) 0.004 (Dendroica petechia) Nashville Warbler LCG 6 0 0.09 (0.04) 0 0.032 (Vermivora ruficapilla) Spotted Towhee GF 13 12 0.24 (0.06) 0.21 (0.05) 0.626 (Pipilo maculatus) Red-eyed Vireoc UCG 6 8 0.11 (0.04) 0.22 (0.07) 0.376 (Vireo olivaceus) American Dipper RBG 0 5 0 0.06 (0.03) 0.062 (Cinclus mexicanus) All birds 2.04 (0.25) 1.56 (0.19) 0.197 aLCF–lower-canopy forager, GF–ground forager, LCG–lower-canopy gleaner, UCG–upper-canopy gleaner, RBP–riparian bottom gleaner (De Graaf et al. 1985). bA total of 85 surveys were conducted pre-flood and 86 surveys post-flood. cRed-eyed Vireos relative abundances are based on June surveys, the only time the species was observed. flooding (77.6%) than after flooding (33.6%; due to vegetation structure and observer limi- t =5.04, P < 0.001). tations, and maximize species detections (Petit Riparian zones along tributaries of the et al. 1995). We excluded birds flying over the Snake River are generally narrow. We sampled plots from further analyses. Surveys began up available tributaries where the riparian zone to 30 minutes before sunrise and were com- was at least 40 m in width. We used fixed-radii pleted no later than 5 hours after sunrise. Bird plots (20-m plots) and conducted point counts surveys were not conducted during inclement at each plot. From 1995 through 1998, we weather conditions such as strong winds intended to survey each plot twice during the (>20 km ⋅ hour–1) or rain (Robbins 1981). breeding season (May and June). However, in We calculated the relative abundance of May 1995 only 4 plots were established and each bird species individually and all bird surveyed. In May 1997 we surveyed only 5 species combined as the total number of indi- plots because many plot markers washed away vidual birds observed divided by the number during the flood and had to be reestablished. of times a plot was surveyed during pre- and During May 1996 and 1998 and June 1995– post-flood periods. Relative abundances were 1998 point counts were conducted at all 27 calculated only for species observed on at least plots. Hence, we conducted 31 surveys in 5 plots, either pre- or post-flood. Because rela- 1995, 54 in 1996, 32 in 1997, and 54 in 1998. tive abundance estimates were not normally We conducted point counts following stan- distributed, we used the Wilcoxon matched- dard protocols (Ralph et al. 1995) to minimize pairs signed rank test to compare relative bias and make bird detectability rates as con- abundances of individual species and pooled sistent as possible. Fixed-radius point counts across all species between pre- and post-flood are effective in providing indices of abun- periods (Zar 1984). Also, we classified all bird dance between treatments (Petit et al. 1995). species observed into foraging guilds for bird We chose 10-minute counts to maximize species community analysis (Table 1). detection since travel time between plots was Forty bird species were observed at the plots. often greater than 15 minutes (Buskirk and Bird species richness was highest in 1996 (23 McDonald 1995, Dawson et al. 1995, Ralph et species) and lowest in 1997 (15 species). Over- al. 1995). Radii of less than 50 m reduce bias all relative bird abundances declined, but not 276 WESTERN NORTH AMERICAN NATURALIST [Volume 65 significantly, between pre- and post-flood peri- damaged sites, habitat was unavailable and both ods (P = 0.197; Table 1). Relative abundance species were not observed in 1998 (Table 1). of lower-canopy foragers (Lazuli Bunting [Pas- Other foraging guilds did not decline and serina amoena] and Yellow-breasted Chat [Icte- some species appeared to show site tenacity. ria virens]), a ground forager (Spotted Towhee During both 1997 and 1998, the Red-eyed [Pipilo maculatus]), and an upper-canopy Vireo was observed in small clumps of live gleaner (Red-eyed Vireo [Vireo olivaceus]) was alders in tributaries that had been otherwise similar between pre- and post-flood periods scoured of vegetation (Turley personal observa- (P > 0.20; Table 1). Relative abundance of Yel- tion), exhibiting apparent site tenacity. Two low Warblers (Dendroica petechia) and Nash- common species, Lazuli Bunting (lower-canopy ville Warblers (Vermivora ruficapilla), lower- forager) and Spotted Towhee (ground forager), canopy gleaners, was higher pre-flood than were often observed in upland habitat adjacent post-flood (Yellow Warbler: P = 0.004; Nash- to riparian habitats in Hells Canyon (Turley ville Warbler: P = 0.032). Relative abundance and Holthuijzen 2000) and were the 2 most of American Dippers (Cinclus mexicanus) was frequently observed species at flood-damaged higher post-flood than pre-flood but was not sites. These species and other lower-canopy significant (P = 0.062). Relative abundance of foragers, as well as ground foragers, may be Black-capped Chickadees (Poecile atricapilla) able to forage outside the riparian zone and was lower post-flood than pre-flood, but was remain at a site even with reduced riparian not significant (P = 0.078). habitat available. Brown and Johnson (1987) evaluated the The American Dipper, a riparian bottom impacts of high-water releases on bird species feeder, had highest abundances the 2nd year nesting in the zone of inundation along the following flooding disturbance. This bird species Colorado River in the Grand Canyon. They was uncommonly observed in the study area. reported that, similar to our findings, several Of 288 riparian plots we sampled (Turley and species exhibited declines attributed to nest Holthuijzen 2000), the American Dipper was inundation and loss of habitat, while other observed at only 8 plots: 1 plot in 1995, 6 plots species experienced unexpected increases. in 1997 and 1998 with flooding damage, and 1 Likewise, Knopf and Sedgwick (1987) found plot in 1998 with mild flooding disturbance that populations of Brown Thrashers (Toxo s- (Turley unpublished data). Lamberti et al. (1991) toma rufum) and Spotted Towhees, both forag- found that debris-flow disturbance of riparian ing and nesting on or near the ground, did not vegetation opened up the canopy, resulting in significantly decline during a flood year that increased light levels in the stream, which led inundated an area along the South Platte in to several years of increased primary produc- Colorado. Declines, however, were reported tivity by aquatic plants and increased secondary the year following the flood. Knopf and Sedg- productivity in communities of invertebrates wick (1987) suggested that site tenacity may that graze on aquatic vegetation. Thus, Ameri- explain the similarity in pre-flood bird densi- can Dippers may have responded to increased ties and those during a flood year; unsuccess- densities of aquatic insects. ful nesting is a likely result of riparian zone Response of birds to flooding likely depends inundation, which in turn brought about lower on the disturbance magnitude of the flood and densities in the year following flooding. In life history traits of the individual species. other habitats time lags in bird response to Riparian patches within a tributary that remain disturbance also were observed probably due intact and even disturbed patches may pro- to site tenacity of breeding individuals (Wiens vide foraging and nesting habitat for some bird and Rotenberry 1985). In Hells Canyon lower- species during the recovery of the system. Also, canopy gleaners may have been displaced, adjacent upland habitat may provide foraging presumably to areas that provided sufficient habitat for some riparian species. At our sites foraging and nesting substrates. Yellow Warbler where average percent shrub cover declined and Nashville Warbler prefer early successional from 80.3% to 20.4% and average percent tree habitats such as thickets or open forest with cover declined from 77.6% to 33.6%, we found shrubby undergrowth (Williams 1996, Lowther that flooding damage displaced lower-canopy et al. 1999). Because the shrub understory was gleaners whereas other guilds continued to use either greatly reduced or absent at our flood- the sites. 2005] NOTES 277

We gratefully acknowledge all research of North America, No. 454. The Academy of Natural assistants involved in this study. A. Moser, Sciences, Philadelphia, PA, and The American Orni- thologists’ Union, Washington, DC. Idaho Power Company, and 2 anonymous MÜLLER-DOMBOIS, D., AND H. ELLENBERG. 1974. Aims reviewers provided valuable comments on and methods of vegetation ecology. John Wiley and earlier versions of the manuscript. The re- Sons, New York. search was funded by Idaho Power Company, PETIT, D.R., L.J. PETIT, V.A. SAAB, AND T.E. MARTIN.1995. an IDACORP Company. Fixed-radius point counts in forests: factors influencing effectiveness and efficiency. Pages 49–56 in C.J. Ralph, J.R. Sauer, and S. Droege, technical editors, LITERATURE CITED Monitoring bird populations by point counts. Gen- eral Technical Report PSW-GTR-149, USDA Forest BROWN, B.T., AND R.R. JOHNSON. 1987. Fluctuating flows Service, Pacific Southwest Research Station, Albany, from Glen Canyon Dam and their effect on breeding CA. birds of the Colorado River. Glen Canyon Environ- RALPH, C.J., S. DROEGE, AND J.R. SAUER. 1995. Managing mental Studies, GCES/23/87, Bureau of Reclama- and monitoring birds using point counts: standards tion, Upper Colorado Region, Salt Lake City, UT. and applications. Pages 161–175 in C.J. Ralph, J.R. BUSKIRK, W.H., AND J.L. MCDONALD. 1995. Comparison Sauer, and S. Droege, technical editors, Monitoring of point count sampling regimes for monitoring for- bird populations by point counts. General Technical est birds. Pages 25–34 in C.J. Ralph, J.R. Sauer, and Report PSW-GTR-149, USDA Forest Service, Pacific S. Droege, technical editors, Monitoring bird popu- Southwest Research Station, Albany, CA. lations by point counts. General Technical Report ROBBINS, C.S. 1981. Bird activity levels related to weather. PSW-GTR-149, USDA Forest Service, Pacific South- Studies in Avian Biology 6:301–310. west Research Station, Albany, CA. SWANSON, F.J., S.L. JOHNSON, S.V. GREGORY, AND S.A. COWARDIN, L.M., V. CARTER, F.C. GOLET, AND E.T. LAROE. ACKER. 1998. Flood disturbance in a forested moun- 1979. Classification of wetlands and deepwater habi- tain landscape: interaction of land use and floods. tats of the United States. U.S. Fish and Wildlife Ser- BioScience 48:681–689. vice, Washington, DC. 131 pp. TURLEY, N.J.S., AND A.M.A. HOLTHUIJZEN. 2000. An inves- DAWSON, D.K., D.R. SMITH, AND C.S. ROBBINS. 1995. tigation of avian communities and avian habitat rela- Point count length and detection of forest Neotropi- tionships in the Hells Canyon Study Area. Technical cal migrant birds. Pages 35–43 in C.J. Ralph, J.R. Report E.3.2-1 in License application for the Hells Sauer, and S. Droege, technical editors, Monitoring Canyon Complex. Idaho Power Company, Boise. bird populations by point counts. General Technical U.S. FISH AND WILDLIFE SERVICE. 1981. Standards for the Report PSW-GTR-149, USDA Forest Service, Pacific development of habitat suitability index models. Southwest Research Station, Albany, CA. Manual 103, U.S. Department of the Interior, Fish DE GRAAF, R.M., N.G. TILGHMAN, AND S.H. ANDERSON. and Wildlife Service, Ecological Services, Washing- 1985. Research: foraging guilds of North American ton, DC. birds. Environmental Management 9:493–536. WIENS, J.A., AND J.T. ROTENBERRY. 1985. Response of HAYS, R.L., C. SUMMERS, AND W. S EITZ. 1981. Estimating breeding passerine birds to rangeland alteration in a wildlife habitat variables. Western Energy and Land North American shrubsteppe locality. Journal of Use Team, Office of Biological Service, Fort Collins, Applied Ecology 22:655–668. CO. WILLIAMS, J.M. 1996. Nashville Warbler (Vermivora rufi- KNOPF, F.L., AND J.A. SEDGWICK. 1987. Latent population capilla). In: A. Poole and F. Gill, editors, The birds of responses of summer birds to a catastrophic, climato- North America, No. 205. The Academy of Natural logical event. Condor 89:869–873. Sciences, Philadelphia, PA, and The American Orni- LAMBERTI, G.A., S.V. GREGORY, L.R. ASHKENAS, R.C. WILD- thologists’ Union, Washington, DC. MAN, AND K.M.S. MOORE. 1991. Stream ecosystem ZAR, J.H. 1984. Biostatistical analysis. 2nd edition. Prentice- recovery following a catastrophic debris flow. Cana- Hall, Inc., Englewood Cliffs, NJ. 718 pp. dian Journal of Fisheries and Aquatic Sciences 48: 196–208. Received 14 July 2003 LOWTHER, P.E., C. CELADA, N.K. KLEIN, C.C. RIMMER, Accepted 12 October 2004 AND D.A. SPECTOR. 1999. Yellow Warbler (Dendroica petechia). In: A. Poole and F. Gill, editors, The Birds Western North American Naturalist 65(2), © 2005, pp. 278–279

BOOK REVIEW

Lott, Dale F. 2002. American bison, a natural canines, and see a perfect match. Even the history. University of California Press, flesh was so well-preserved that when the Berkeley, California. 229 pp. ISBN 0-520- corpse had yielded all it secrets Dale and his 23338-7 (cloth: alkaline paper). colleagues made an acceptable stew with a bit of the meat.” You gotta read this book. Since you are Dr. Lott spent his earliest years on the already browsing a review in this journal, you National Bison Range in Montana, and by his are almost certainly the audience to whom it is own admission his first encounters were of directed (natural historians and conservation- bison not as symbols of the West, the squan- ists broadly defined) and you will appreciate dering of a natural resource, or a conservation the style. In this book Dr. Lott tells enough triumph. They were simply the animals he had about the natural history of bison to whet the seen most frequently as a youngster. The generalist’s appetite and yet to engage the sense of wonder in this gray-haired youngster specialist in thinking in broader concepts. I is still evident when he describes bulls fight- learned more of the basics of buffalo, a term ing: “I once saw a bull somersaulted backward he prefers to bison in many applications, than by such a charge: 2,000 pounds of bull flipped I thought I would ever need. But now I feel I upside down like a lawn chair in a gust of better understand the history of this animal wind.” You might think gems like this would that filled the grassland sea of the continent’s only pepper the prose, but waits were short to midsection. the next one and were welcome to me, just as Clearly, Dr. Lott knows that of which he the words I’ve heard from master western sto- speaks, yet doesn’t flaunt it on the pages like rytellers huddled around smoky sagebrush the pompous academic most of us can become fires on a hundred hillsides of the West. at times. As he unfolded story after well- I loved how the honest, open style flowed woven story of these creatures and those with while facts were wound around each other to which they share (shared) the prairies, my present an image of the objectivity that sci- eyes flew across the pages in anticipation of ence needs. The openness might inspire skep- the next homey turn of words, like “from grass ticism in some about “observed reality” in these to gas and chips” to describe the digestion beasts, but that cynicism should disappear in process of these ruminants. Or, “even when respecting the mantra hymn of his flinty- they’re getting serious, cows’ clashes seem jawed ecologist friend, Steve Minta: “‘Where’s more comic than cosmic. I’ve seen cows uri- the data?’, and all the lyrics just repeat the title.” nate thousands of times and wallow thousands I believe Dr. Lott presents the data fairly, and of time, but only once have I seen a cow put those who want to check up on that can comb urinating and wallowing together as a threat- through the bibliography of reasonable length ening bull would do.” Or, “It’s a sobering fact and coverage near the end of the book. that 12 to 13 percent of a bottle of Dom He also notes at length the several contro- Perignon Champagne is bacteria pee.” Or, in versies that face the bison and its ecosystem, speaking of a particularly well-preserved foremost the brucellosis dilemma of the Greater 36,000-year-old bison that was frozen in blue Yellowstone System and the potential loss of coppery mud, “the tooth and claw marks in his wild bison through introgression with domes- hide were still so clear that Dale (Guthrie) ticated bison he dubs “buffattle.” Recognizing could take an American lion’s skull, place its that somehow wild buffalo, commercial buf- canine teeth on the marks left by the killer’s falo, and commercial cattle need to share some

278 2005] BOOK REVIEW 279

Great Plains resources, he nonetheless laments, als to tens. Advocates for and against bison “The public is more than willing to lose money were vocal then. The Great Slaughter “choice” raising wild bison . . . and we should be will- was taken then and the gene pool was bottle- ing to consider resolving this paradox: Bison necked severely. This narrowing has shaped bison is the only wild animal in the United the possibilities of what we can hope to accom- States that is not allowed to live as a wild ani- plish with bison conservation now. Attitudes mal . . . anywhere in its original range.” Lest must be plumbed and a reasonable solution or someone charge him with one-sidedness in his solutions to the issues addressed soon. This book fascination with bison and his advocacy of will serve well to popularize at least some of their protection and restoration, he defuses the possibilities. It should also be a model as with, “At bottom, wildlife management in our each of us addresses our own advocacy issues society uses biological knowledge to imple- in the conservation or eradication of our ment individual values as they are expressed favorite plants, bugs, birds, and bacteria. You through our political system. I am an expert gotta read this book. on my own values, and I don’t hesitate to ad- vocate them.” This is a clear enough statement C. Riley Nelson on advocacy yet leaves the political implemen- Department of Integrative Biology tation open to public debate. Brigham Young University, Public debate occurred in the late 1800s Provo, Utah 84602 and herds declined from millions of individu- rileynelson@byu

CONTENTS

(Continued from back cover)

Articles (continued) Distribution of the milliped Virgoiulus minutus (Brandt, 1841): first records from Mississippi, Oklahoma, and Texas (Julida: Blaniulidae) . . . . Chris T. McAllister, Rowland M. Shelley, Henrik Enghoff, and Zachary D. Ramsey 258 Notes Defense of pronghorn fawns by adult male pronghorn against coyotes . . . Kim Murray Berger 267 Refugia from browsing as reference sites for restoration planning ...... William J. Ripple and Robert L. Beschta 269 Impact of a catastrophic flooding event on riparian birds ...... Natalie J. S. Turley and Anthonie M. A. Holthuijzen 274 Book Review American bison, a natural history by Dale F. Lott ...... C. Riley Nelson 278