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Small mammals and ground-dwelling invertebrates associated with active and controlled colonies of black-tailed prairie dogs (Cynomys ludovicianus).

Prairie dogs (Cynomys) once inhabited North American prairies from southern Canada to north-central Mexico, and from the eastern Rocky Mountains to the tall-grass prairies of the Great Plains (Hall, 1981). They were among the most numerous grassland herbivores and had a significant impact on nutrient cycling, plant succession, and biodiversity in the prairie ecosystem (Coppock et al., 1983; Archer et al., 1987; Weltzin et al., 1997). Over the past century, the extent of populations of prairie dogs has decreased by [less than or equal to]98% (Miller and Ceballos, 1994). In Texas, the range of the black-tailed prairie dog was estimated to have declined from ca. 330,000,000 ha in 1905 to ca. 37,500 ha in 1977 (Cheatam, 1977). The decline in abundance and distribution was principally the result of eradication programs, introduction of sylvatic plague, unregulated shooting, and habitat loss (Van Putten and Miller, 1999). As a result of these declines, the status of the black-tailed prairie dog was evaluated recently by the United States Fish and Wildlife Service, and a multi-state conservation strategy for the species was developed (United States Fish and Wildlife Service,

Despite conservation concerns, use of toxicants to control prairie dogs remains a common practice. Previous studies have examined the impact of zinc phosphide and strychnine (common rodenticides used to control populations of prairie dogs) on non-target species (Deisch et al., 1989, 1990; Apa et al., 1991). These toxicants are applied with baits, commonly oats, which allow non-target species to ingest the rodenticides. Aluminum phosphide, a fumigant for burrows, commonly known as Phostoxin[R] (Degeshe Company, Inc., Weyers Cave, Virginia), is now being used as a method to control prairie dogs (Moline and Demarais, 1987). Tablets placed in burrows release hydrogen-phosphide gas that acts as a toxic fumigant, suffocating inhabitants. Phostoxin[R] was ca. 95% effective in controlling black-tailed prairie dogs (Salmon et al., 1982), and almost 100% effective in controlling ground squirrels (Spermoryhilus; Moline and Demarais, 1987). In addition to causing direct mortality to prairie dogs and other occupants of burrows, Phostoxin[R] may indirectly affect non-target species as treated burrows are closed and remain inaccessible for shelter and other uses. Nontarget species also may be impacted by changes to the local vegetative community that may result from elimination of prairie dogs from an area (Matt and Hein, 1978; Cid et al., 1991).

Many species are closely associated with colonies, and black-tailed prairie dogs may function as keystone species within the prairie ecosystem (Miller and Ceballos, 1994; Kothar et al., 1999; Van Putten and Miller, 1999; Lomolino and Smith, 2003). Prairie dogs modify the vegetative structure and composition of their habitat, and these changes may affect other grassland species (Whicker and Detling, 1988). Compared to non-colonized, mixed-grass prairies, colonies of prairie dogs support greater numbers of small mammals, arthropods, birds, and predators (O'Melia et al., 1982; Agnew et al., 1986; Krueger, 1986; Miller et al., 1990; Sharps and Uresk, 1990; Shipley and Reading, 2006). Densities of North American deermice (Peromyscus maniculatus) and northern grasshopper mice (Onychomys leucogaster) were 3-4 times greater on colonies than on non-colonized areas in South Dakota (Agnew et al., 1986), and northern grasshopper mice were closely associated with colonies of prairie dogs in Colorado and Oklahoma (Lomolino and Smith, 2003; Shipley and Reading, 2006). Burrows provide shelter for many other species, from burrowing owls (Athene cunicularia) to prairie rattlesnakes (Crotalus viridis; Kothar et al., 1999), and grasshoppers and beetles occupy bare ground created by prairie dogs around their burrows (Russell and Detling, 2003; Bangert and Slobodchikoff, 2004).

No study has addressed effects of Phostoxin[R] on non-target species associated with prairie dogs. At our study site in the Texas Panhandle, Phostoxin[R] was used to control black-tailed prairie dogs in areas of special concern for safety and security reasons. We examined seasonal differences in small mammal and ground-dwelling invertebrate communities occurring on active colonies of prairie dogs, Phostoxin[R]treated colonies, and non-colonized sites to determine differences in occurrence of species among treatments and possible impacts of Phostoxin[R] on non-target organisms.

MATERIALS AND METHODS--We conducted this study on the Pantex Plant, 27 km NE Amarillo, Carson County, Texas, which is administered by the United States Department of Energy-National Nuclear Security Administration. Topography at the site was relatively flat with several playa lakes, and average elevation was 1,067 m. The study area was characterized by short grass prairie dominated by buffalo grass (Buchloe dactyloides) and blue grama (Bouteloua gracilis), with scattered clumps of prickly pear (Opuntia). About 70% of the site was farmed or grazed. Cattle were managed under a rotational grazing system and vegetation on some areas of the Pantex Plant was mechanically shredded to reduce danger of fire.

We assessed abundances of small mammals and ground-dwelling invertebrates in areas representing three treatments: active colonies of prairie dogs, colonies treated with Phostoxin[R], and areas of short-grass prairie that historically had not supported prairie dogs. Nine sites, representing three replications of each treatment were selected. All nine sites had similar topography and vegetation, and were separated by [greater than or equal to]250 m. Application of Phostoxin[R] occurred in early spring 1998, 1999, and between sampling periods in winter and spring during 2000. Immediately after tablets of Phostoxin[R] were placed into burrows, the burrows were plugged with newspaper and covered with soil to contain the fumigant and prevent inhabitants from escaping.

A trapping array of 100 Sherman live traps arranged at 10-m intervals in a 100 by 100-m grid was established at each of the nine sites (Deisch et al., 1990; Jones et al., 1996). During spring 2000-summer 2001, trapping was conducted during 6 periods: 8-29 May 2000 (spring), 11 June-20 August 2000 (summer), 26 October-3 December 2000 (autumn), 26 January-26 February 2001 (winter), 20 April-28 May 2001 (spring) and 19 June-26 August 2001 (summer). During each period, small mammals were trapped for 3 consecutive nights at each study site. Three or four sampling areas were trapped simultaneously. Before dark, traps were set and baited with a mixture of rolled oats and hearts of sunflower seeds. U-shaped metal wires were placed over traps and into the ground to prevent traps from being blown from their original location. All traps were checked the following morning. During autumn, winter, and early spring, cotton balls were placed into traps to reduce risk of hypothermia (Jones et al., 1996). Captured small mammals were marked with numbered ear tags (1005 size 1; National Band and Tag Company, Newport, Kentucky), weighed to the nearest gram, identified to species, and sex and age class (juvenile or adult) were determined.

An X-shaped array of drift fences and pitfall traps was established at the center of each of the trapping arrays to capture ground-dwelling invertebrates (Corn, 1994). Pitfall traps were arranged in arrays of five traps, with one 19-L bucket in the center, and a 19-L bucket buried 10 m away in each ordinal direction. Blackcloth, silt fencing ca. 0.7 m in height (Specialty Converting and Supply, Nashville, Georgia) was placed between each of the buckets to direct organisms into the pitfalls (Gibbons and Semlitsch, 1982). The base of the fencing was entrenched in the ground and covered with soil to provide stability and to facilitate movement of animals (Dodd and Scott, 1994). Small blocks of untreated wood (ca. 7 [cm.sup.2]) were placed in the bottom of buckets to prevent drowning of incidentally captured small mammals (McCaffrey, 2001). Pitfall trapping was conducted during May 2000-August 2001, in concert with trapping periods. Pitfall traps at each study site were opened for 3 consecutive nights/ session. During periods of moderate weather, traps were opened the first evening and checked each morning and evening for the duration of the session. During periods with hot (>30[degrees]C) daytime temperatures, traps were opened the first evening, but closed each morning and reopened each evening to prevent overheating of captured animals.

All captured individuals were identified to species (small mammals) or family (invertebrates). To further sample ground-dwelling invertebrates and herptofauna, we also used cover-boards (Fellers and Drost, 1994). Sheets of plywood measuring ca. 60 by 90 cm were placed at the four corners of each trapping array. On the final day of each trapping session, cover-boards were lifted and all species observed beneath were identified and counted.

We used catch-per-unit effort to determine relative abundances of small mammals at each sampling area, where captured animals were removed from the population by marking (Lancia and Bishir, 1996). For the three most-commonly captured species, North American deermice, plains harvest mice, and northern grasshopper mice, individual estimates of relative abundance were calculated. Counts of invertebrates observed under cover-boards or captured in pitfall traps at each study site were combined to produce relative abundances of invertebrates.

A two-way repeated-measures analysis of variance (ANOVA) was used to test for differences in abundances of invertebrates and small mammals through time (seasons) and among treatments (active, Phostoxin[R]-treated, and non-colonized). Due to weather conditions that made some sites inaccessible, only five of nine sites were trapped during winter and one site was not trapped during spring 2001. As a result, data from the sampling session in winter are not included in analyses and we used the PROC MIXED procedure in SAS version 8.0 (SAS Institute, Inc., Cary, North Carolina) to allow for missing data for spring (Littell et al., 1996). In cases where statistically significant differences among treatments or seasons were detected, differences of least square means were used to separate means.

RESULTS--During May 2000-August 2001, we captured 227 small mammals representing 11 species (Table 1). Seven species were captured on active sites, 7 species on Phostoxin[R]-treated sites, and 11 species on non-colonized sites. Seven species (Baiomys taylori, Chaetodipus hisryidus, O. leucogaster, P. maniculatus, R. montanus, Sigmidon hispidus, and Spernyophilus tridecemlineatus) were on all treatments. The most common species observed on all three treatments was the

North American deermouse, representing 48% of captures at active colonies, 53% at Phostoxin[R]treated colonies, and 44% at non-colonized sites. Northern grasshopper mice were more abundant (F = 4.67, d[Florin] = 2,6, P = 0.059) on active colonies than on Phostoxin[R]-treated or noncolonized sites. Total abundance of small mammals (F = 0.01, d[Florin] = 2,6, P = 0.992), species composition (F = 0.38, d[Florin] = 2,6, P = 0.697), and abundances of North American deermice and plains harvest mice did not differ among treatments (F = 0.16, d[Florin] = 2,6, P = 0.859 and F = 4.67, d[Florin] = 2,6, P = 0.442, respectively). Total abundance of small mammals (F = 3.51, d[Florin] = 4,23, P = 0.023), species composition (F = 3.61, d[Florin] = 4,23, P = 0.019), and abundances of the North American deermouse and plains harvest mouse (F = 4.47, d[Florin] = 4,23, P = 0.008 and F = 2.85, d[Florin] = 4,23, P = 0.047, respectively) did differ among seasons. Abundances of small mammals were significantly lower in summer 2001 than during the other seasons. Rates of capture in summer 2001 averaged 0.004 captures/trap night, whereas rates of capture over the previous seasons averaged 0.017 captures/trap night (Table 2).

Data from pitfall trapping during spring 2000, autumn 2000, and winter 2001 were not included in this analysis, as periods of freezing temperatures prevented us from trapping some sites during these periods. Therefore, during summer 2000, spring 2001, and summer 2001, we captured 167 individual ground-dwelling invertebrates representing five families in pitfall traps or under cover-boards. Overall abundance of ground-dwelling invertebrates collected from pitfall traps and cover-boards was greater (F = 8.50, d[Florin] = 2,6, P = 0.015) on active colonies than on Phostoxin[R]-treated colonies or non-colonized sites. Abundance of invertebrates was not different across seasons (F = 0.54, d[Florin] = 2,11, P = 0.596).

Four families, crickets and grasshoppers (Gryllacrididae), scarab beetles (Scarabaedidae), ground beetles (Carabidae), and wolf spiders (Lycosidae) were captured on each treatment. Carabidae was the most abundant family, representing 42% of invertebrates, whereas scarab beetles accounted for 27%, crickets and grasshoppers for 26%, and wolf spiders for 5%. Ground beetles were captured in all seasons on all treatments, whereas scarab beetles were captured in all seasons on all treatments, except in active colonies in summer 2000. One tarantula (Theraphosidae) was observed in summer 2001 at a non-colonized site. Ants (Formicidae) were at seven of the nine sites sampled, but were not included here because accurate counts were not possible under cover-boards.

DISCUSSION--Our findings for small mammals differed from studies in South Dakota and Oklahoma, which indicated that total abundance of rodents and abundance of deermice were greater on colonies of prairie dogs than on noncolonized sites (O'Melia et al., 1982; Agnew, 1983; Agnew et al., 1986; Deisch et al., 1990). These differences may be due to structure of vegetation present where each study was performed (Shipley and Reading, 2006). Prairie dogs alter vegetation by decreasing canopy cover and height of plants (Archer et al., 1984). In areas with taller grass, such as sites studied in South Dakota and Oklahoma, these activities provide areas of open space, with little vegetational cover, which may attract species, such as deermice and thirteen-lined ground squirrels (S. tridecemlineatus; O'Melia et al., 1982; Agnew et al., 1986; Deisch et al., 1990). In the grazed short-grass communities at the Pantex Plant, activities by prairie dogs may have less effect on structure of the vegetational community because canopy cover and height of plants already are reduced (Sims et al., 1978). With short-grass prairie covering much of the Pantex Plant, in addition to sites with colonies of prairie dogs, species adapted to this habitat might have little need to concentrate on colonies of prairie dogs.

For northern grasshopper mice, which were more abundant on active colonies than on Phostoxin[R]-treated colonies or non-colonized sites, the attraction to active colonies may be based on foraging resources. Invertebrates, which compose a significant portion of diet of the northern grasshopper mouse (Flake, 1973; Davis and Schmidly, 1994), also were more abundant in colonies of prairie dogs. Koford (1958) suggested that burrows of prairie dogs were used by ground beetles and recent research supports the idea that grasshoppers select colonies of prairie dogs due to presence of bare ground and increased forbs (Russell and Deding, 2003). Abundances of invertebrates are greater on active colonies compared to adjacent prairie (Olson, 1985). Greater abundances of beetles and grasshoppers on active colonies might provide an incentive for northern grasshopper mice to use these areas.

Northern grasshopper mice also are known to use burrows of other species for shelter and nesting sites (Agnew, 1983; Agnew et al., 1986; Stapp, 1997). Stapp (1997) reported that northern grasshopper mice selected for areas containing pocket gopher (Thomomys, Geomys) mounds over random sites. Other investigations, conducted in a variety of types of prairies, detected higher abundances of northern grasshopper mice on active colonies of prairie dogs than on non-colonized sites (O'Melia et al., 1982; Agnew et al., 1986; Lomolino and Smith, 2003; Shipley and Reading, 2006). At the Pantex Plant, northern grasshopper mice may be impacted directly by Phostoxin[R]. Northern grasshopper mice inhabiting burrows of prairie dogs that were treated with Phostoxin[R] probably experience the same rates of mortality (i.e., 95-100%) exhibited by ground squirrels and prairie dogs (Salmon et al., 1982; Moline and Demarais, 1987). Treatment with Phostoxin[R] might result in an initial decrease in number of northern grasshopper mice through direct mortality, and long-term reductions in populations may result as mice are unable to use the plugged burrows.

Populations of small mammals showed a marked decrease during summer 2001. This pattern was likely the result of drought conditions during this period, as rainfall during June-August 2001 totaled only 8.68 cm compared to a 30-year average of 24.23 cm. These conditions also may have affected plants, resulting in failure of many plants to produce seeds (White et al., 1996). Seeds are important in the diet of granivorous rodents (e.g., deermice and plains harvest mice), and a shortage of food may have resulted in reduced populations of rodents (Mutze et al., 1991; Morton et al., 1995).

Colonies of prairie dogs at the Pantex Plant provide important habitat for northern grasshopper mice and ground-dwelling invertebrates, but they appear to be less important to other species of small mammals. Northern grasshopper mice and ground-dwelling invertebrates were negatively impacted by use of Phostoxin[R] to control populations of prairie dogs. We suspect that long-term control of prairie dogs with Phostoxin[R] may effect other species, as the exclusion of prairie dogs from an area will result in changes to the vegetational community, although perhaps less so than in areas with taller grass. Additionally, without maintenance by prairie dogs, burrows will deteriorate and become unusable by other species that may use them for shelter.

This research was funded by the United States Department of Energy-National Nuclear Security Administration in cooperation with BWXT Pantex, LLC, and Texas Tech University, Department of Range, Wildlife and Fisheries Management. We thank M. Keck and M. Schoenhals for assistance with on-site coordination and access and W. Ballard for assistance in preparing this manuscript. We also thank D. Butler, C. Gresham, J. Kamler, C. Perchellet, J. Reed, K White, and A. Stein for assistance with field work and R. Carrera for translating the abstract. This is manuscript T-9-1153 of the College of Agricultural Sciences and Natural Resources, Texas Tech University.

Submitted 8 October 2007. Accepted 29 November 2008.


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Department of Natural Resources Management, Texas Tech University, Lubbock, TX 79409 (REM, MCW)

BWXT Pantex, LLC Pantex Plant, Amarillo, TX 79120 (JDR)

Present address of REM. School of Natural Resources, University of Arizona, Tucson, AZ 85721

Associate Editor was Earl G. Zimmerman.

* Correspondent.
TABLE 1--Average number of small mammals captured per 100 trap nights
at active, Phostoxin[R]-treated, and non-colonized sites, during
spring 2000-summer 2001(a) at the Pan tex Plant, Carson County, Texas.

 Species Active Phostoxin[R]-treated

Baiomys taylori 0.06 0.56
Chaetodipus hispidus 0.12 0.06
Microtus ochrogaster 0 0
Onychomys leucogaster 1.44 0.11
Perognathus flavescens 0 0
Perognathus merriami 0 0
Peromyscus maniculatus 2.25 2.44
Reithrodontomys montanus 0.44 1.11
Sigmodon hispidus 0.25 0.06
 tridecemlineatus 0.06 0.28

 Species Non-colonized

Baiomys taylori 0.31
Chaetodipus hispidus 0.13
Microtus ochrogaster 0.06
Onychomys leucogaster 0.13
Perognathus flavescens 0.06
Perognathus merriami 0.06
Peromyscus maniculatus 1.88
Reithrodontomys montanus 1.13
Sigmodon hispidus 0.38
 tridecemlineatus 0.13

(a) Data from winter 2000 were not included.

TABLE 2--Captures of small mammals per trap night and (total number
of species caught) at active, Phostoxin[R]-treated, and non-colonized
sites, during spring 2000-summer 2001(a) at the Pantex Plant, Carson
County, Texas.

Sites Spring 2000 Summer 2000 Autumn 2000

Active 0.02 (5) 0.01 (5) 0.03 (5)
Phostoxin[R]-treated 0.03 (3) 0.01 (3) 0.04 (4)
Non-colonized 0.02 (7) 0.02 (7) 0.02 (2)

Sites Winter 2000 Spring 2001 Summer 2001

Active <0.01 (1) 0.02 (2) 0.01 (3)
Phostoxin[R]-treated 0.01 (3) 0.01 (3) <0.01 (1)
Non-colonized 0.01 (1) 0.01 (4) <0.01 (3)

(a) There were 900 trap nights/treatment/season with the exception
of winter 2000, when there were 300 trap nights for active and
non-colonized sites.
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Author:McCaffrey, Rachel E.; Wallace, Mark C.; Ray, James D.
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1USA
Date:Sep 1, 2009
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