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Volume 73—1993

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Responses of Intestinal Nematodes in White-footed Mouse (Peromyscus leucopus) Populations to Rangeland Modification

Jon C. Boren1, Robert L. Lochmiller1, James F. Boggs1, and Scott T. McMurry1, David M. Leslie, Jr.2, David M. Engle3, and Hellen E. Jordan4

1Department of Zoology, Oklahoma State University, Stillwater, OK 74078
2U.S. Fish and Wildlife Service, Oklahoma Cooperative Fisheries and Wildlife Research Unit, Oklahoma State University, Stillwater, OK 74078
3Department of Agronomy, Oklahoma State University, Stillwater, OK 74078
4Department of Parasitology, Microbiology, and Public Health, Oklahoma State University, Stillwater, OK

Received: 1992 Nov 23; Revised: 1993 Apr 16

Introduction Methods Results Discussion References Table of Contents Home

We evaluated the influence of five brush management treatments using the herbicides tebuthiuron and triclopyr, with or without prescribed burning, on the gastrointestinal helminths of white-footed mouse (Peromyscus leucopus) populations on the Cross Timbers Experimental Range in Payne County, Oklahoma. We recovered three helminth species (Syphacia peromysci, Nippostrongylus muris, and one unidentified species of Trichuris) in 99 white-footed mice collected in March and June 1986. Overall prevalence of infection for S. peromysci (61.6%) and N. muris (14.2%) was not significantly influenced by month of collection. Prevalence of N. muris infection was significantly greater on untreated control pastures (40.0%) than those subjected to brush removal (7.6%). Prevalence of N. muris infections was greater on untreated pastures (40%) than on those treated with herbicide (7.6%). Mean abundances for S. peromysci were significantly greater on pastures receiving tebuthiuron than triclopyr treatments. Type of herbicide applied could have influenced S. peromysci populations indirectly by altering feeding and habitat use patterns of white-footed mice. Microclimate changes resulting from herbicide applications probably influenced the survival of eggs and infective larvae of N. muris.


Introduction Methods Results Discussion References Table of Contents Home

Composition of helminth communities varies considerably among host populations across geographic regions (1-4). Much of this variation has been attributed to differences in soil moisture and plant communities. Similarly, natural successional and man-induced disturbances of the habitat that alter a variety of abiotic and biotic components can influence the helminth community within a resident host population. Habitat modifications that alter the structure and composition of vegetation can influence both vertebrate and invertebrate populations that serve as either primary or intermediate hosts for a variety of parasite species. For example, several studies have demonstrated that herbicide- and fire-induced alterations of habitats influence the diversity and abundance of small mammals (5, 6) and arthropods (7-10).

Earlier studies by Issac (11) and Bendell (12) reported changes in helminth communities of black-tailed deer (Odocoileus hemionus columbianus) and blue grouse (Dendragapus obscurus), respectively, following wildfires. Similarly, Seip and Bunnell (13) noted significant reductions in Protostrongylus sp. infections among Stone's sheep (Ovis dalli stonei) that used annually burned alpine ranges.

Our recent studies have shown that applications of herbicides and burning, which alter structure and composition of vegetation in the habitat, can influence the prevalence of cestodes and abundance and frequency distribution of nematodes in cottontail rabbit (Sylvilagus floridanus) populations (14, 15). We present additional evidence in

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this paper that man-induced habitat modifications can influence host-parasite relationships on cross timbers rangeland. Specifically, we examined the abundance and prevalence of Syphacia peromysci and Nippostrongylus muris infections in populations of white-footed mice (Peromyscus leucopus) inhabiting rangelands altered by applications of herbicide and prescribed fire.


Introduction Methods Results Discussion References Table of Contents Home

White-footed mice were collected on the Cross Timbers Experimental Range (CTER), located approximately 11 km west of Stillwater, Oklahoma (36°2' to 36°4'N, 97°9' to 97°11'W). The CTER is a 648-ha research area composed of blackjack oak (Quercus marilandica)-post oak (Q. stellata) and eastern redcedar (Juniperus virginiana) upland forest intermixed with tallgrass prairie (16). The CTER includes 20 fenced experimental pastures, each of 32.4 ha, representing four replications each of four commonly used brush management treatments, using combinations of herbicide and annual prescribed burning applications, and an untreated reference area. The five experimental treatments were: 1) tebuthiuron (N-[5-(1,1-dimethylethyl)-1,3,4-thiadiazol-2-yl]-N,N'-dimethylurea), a soil-applied herbicide (Elanco, Products Co., Division of Eli Lilly and Co., Indianapolis, IN 46285, USA) applied aerially at 2.0 kg per ha in March 1983; 2) tebuthiuron applied as in treatment 1 with annual prescribed burning in April, 1985 and 1986; 3) triclopyr ([3,5,6-trichloro-2-pyridinyl)oxy]acetic acid), a foliage-applied herbicide (Dow Chemical Co., Midland, MI 48674, USA) applied aerially at 2.2 kg per ha in June 1983; 4) triclopyr applied as in treatment 3 with annual prescribed burning in April, 1985 and 1986; and 5) untreated reference area. All experimental pastures were moderately grazed by cattle during spring and summer of each year.

Populations of white-footed mice were sampled in upland post oak-blackjack oak savannas by removal snap-trapping using a randomly placed 8 × 8 grid (15-m spacing between stations) on each pasture. Two replications of each of the five experimental treatments were sampled in March and June 1986 and adequate numbers of adult mice were collected from all treatments. Trapping grids were relocated to unsampled areas prior to sampling in June. Mice were returned to the laboratory and total recovery of gastrointestinal helminths was undertaken using irrigation and lavage. The specifics of these techniques have been described (14). Representative samples of helminths recovered from this study have been deposited in the U. S. National Parasite Collection (Beltsville, Maryland 20705, USA, Accession Nos. 80492-80493).

Abundances for S. peromysci were independently rank transformed (17) prior to data analysis. Differences among experimental treatments were examined by using a two-way analysis of variance for the ranked abundances of S. peromysci with treatment and month as main effects [general linear model procedure, PROC GLM (18)]. A priori specific contrasts were used to compare variation in abundance among brush treatment components (burned herbicide-treated versus unburned herbicide-treated, tebuthiuron- treated versus triclopyr-treated, untreated versus treated). Prevalence of S. peromysci and N. muris was subjected to chi-square analysis for determination of heterogeneity among experimental brush treatments. A priori specific contrasts (2 × 2 contingency tables corrected for continuity with Haber's (19) correction) were used to compare variation in prevalence among brush treatment components as described above. Data were pooled across seasons or treatment categories only if statistical interactions were not indicated.


Introduction Methods Results Discussion References Table of Contents Home

Three nematode species (S. peromysci, N. muris, Trichuris sp.) were recovered from a total of 99 white-footed mice on the CTER. Only one female Trichuris of unknown species was recovered (Table 1). Both S. peromysci and N. muris were represented on all five experimental brush treatments. Overall prevalence of infection for S. peromysci (62.6%) and N. muris (14.2%) were not significantly influenced (X2 = 1.068, df = 1, P > 0.100; X2 = 2.078, df = 1, P > 0.100, respectively) by month of collection (Table 1). Since no statistical interactions between months were indicated we pooled data from the two collections for analysis of treatment effects.

Prevalence of S. peromysci infections in white-footed mouse populations from

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burned herbicide treatments (73.0%) tended to be greater (X2 = 3.453, df = 1, P < 0.100) than on unburned herbicide treatments (52.4%). Prevalence also tended to be greater (X2 = 3.439, df = 1, P < 0.100) on all tebuthiuron (72.5%) than all triclopyr (51.3%) treatments, but differences were not significant.

In contrast, prevalence of infection for N. muris was significantly (X2 = 14.285, df = 4, P < 0.01) influenced by experimental brush treatments. Prevalence was significantly greater (X2 =12.902, df = 1, P < 0.001) on untreated controls (40.0%) than on herbicidetreated pastures (7.6%). Prescribed burning and type of herbicides applied had no significant influence on prevalence for N. muris.

Although prevalence of S. peromysci showed no significant difference between collection dates, abundance and intensity of infections were greater in March than June (Table 2). Overall, intensity of infection for S. peromysci ranged from 1 to 2789 worms/host. Mean ranked abundances for S. peromysci were significantly influenced by experimental brush treatments (P < 0.041) and season (P <0.020). Specific contrasts indicated that abundances were significantly greater (P < 0.034) on tebuthiuron (177.2 worms/host) than triclopyr (125.1 worms/host) treatments; no other specific contrasts were significant.

Abundance and intensity of infection for N. muris was highest in animals from untreated control pastures. Intensity of infections ranged from 1 to 3 worms/infected host (Table 2). Of the white-footed mice infected with N. muris, only 28.6% (4 of 14) had more than one worm, and 75% of these animals were from untreated control pastures.


Introduction Methods Results Discussion References Table of Contents Home

Although white-footed mice are widely distributed throughout the United States, relatively little is known of their nematode parasite fauna as related to habitat. Harkema (20) and Leiby (21) noted that species diversity of helminth infections in Peromyscus species tends to be low in comparison to that in larger rodent species. We have made similar observations in small mammal communities from central Oklahoma; two prominent gastrointestinal parasite species were documented in the white-footed mouse

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compared to five species in Sigmodon hispidus, three in Neotoma floridana, and seven in Sylvilagus floridanus (22).

Syphacia peromysci were recovered primarily from the cecum and have been reported in surveys of white-footed mice in North Carolina (20), Maryland (23), and Kentucky (23). This oxyurid pinworm has been widely reported in other species of Peromyscus as well (21,24). In contrast to S. peromysci, infections of N. muris and Trichuris sp. in Peromyscus have not been widely reported. Unlike infections in the genus Peromyscus (21, 24), abundance of infection for N. muris in a common host, Rattus norvegicus, often exceeds 100 worms/host (20, 25).

Brush removal with herbicides appeared to influence the abundance and prevalence of S. peromysci and N. muris in white-footed mouse populations on the CTER. Triclopyr and tebuthiuron applied on the CTER significantly altered the vegetation community by decreasing woody overstory and increasing herbaceous understory production. Detailed descriptions of how herbicides and prescribed burning influenced vegetation on the CTER are available (26, 27).

The greater abundances of S. peromysci infections, and tendency for greater prevalence, in white-footed mouse populations on tebuthiuron than triclopyr treatments may be attributed more to a clumped distribution of preferred habitats than differences in microclimatic factors. The universal distribution of S. peromysci among Peromyscus spp., including harsh and environments in Utah (24), suggest that this pinworm has eggs resistant to extremes in temperature and moisture. Vegetation structural characteristics were dissimilar between tebuthiuron and triclopyr treatments, with a greater abundance and distribution of preferred woody cover on triclopyr-treated pastures (26, 27). Tebuthiuron was more efficient at preventing resprouting of woody vegetation after canopy removal and also was effective against a greater number of woody species compared to triclopyr. As a result, feeding and other habitat-use behaviors of white-footed mice may have been more concentrated on tebuthiuron treatments with a limited distribution of preferred habitat types. Observed differences did not appear to be related to host density, as relative population densities (catch per unit effort) of white-footed mice were found to be significantly greater on triclopyr than tebuthiuron treatments on the CTER (28).

Differences in the prevalence of N. muris infections between untreated pastures and those subjected to brush removal could be a reflection of more suitable microclimatic conditions for survival of eggs and larvae. Infective larvae of N. muris primarily enter the host by boring through the skin, although some infections may be acquired orally (25). Moisture is required for the development of eggs and larvae of N. muris, and conditions similar to those found in fresh feces are ideal (25). Eggs and larvae apparently are susceptible to damage by direct sunlight and high temperature (20,25). The greater amount of forest floor material (14) and shade provided by the woody overstory on untreated control pastures compared to herbicide-treated pastures probably protected eggs and larvae of N. muris from desiccation.

Our study indicates that habitat alterations which modify the structure or composition of rangeland vegetation can potentially alter host-parasite community relationships in small mammals. The impact of habitat modifications on any particular species of helminth is undoubtedly correlated with life cycle, mode of transmission, resistance to microclimatic changes, and effects on host behavior and habitat use. It is possible that similar alterations in host-parasite communities could occur in livestock and other wildlife species grazing brush-treated rangeland.


This research was supported by the Oklahoma Agricultural Experiment Station, National Science Foundation (BSR-8657043), National Rifle Association, and Oklahoma Cooperative Wildlife and Fisheries Research Unit (U.S. Fish and Wildlife Service, Oklahoma State University, Oklahoma Department of Wildlife Conservation, and Wildlife Management Institute cooperating). This is journal article 5797 of the Oklahoma Agricultural Experiment Station.


Introduction Methods Results Discussion References Table of Contents Home

1.   Kinsella, J.M., Comparison of Helminth Parasites of the Cotton Rat, Sigmodon hispidus, from Several Habitats in Florida. Am. Mus. Novitates 2540, 1-12 (1974).

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3.   Martin, J.L., and Huffman, D.G., An Analysis of the Community and Population Dynamics of the Helminths of Sigmodon hispidus (Rodentia: Criceditae) from Three Central Texas Vegetational Regions. Proc. Helminthol. Soc. Wash. 47, 247-255 (1980).

4.   Pence, D.B., Crum, J.M., and Conti, J.A., Ecological Analyses of Helminth Populations in the Black Bear, Ursus americanus, from North America. J. Parasitol. 69, 933-950 (1983).

5.   Kirkland, G.L., Population and Community Responses of Small Mammals to 2,4,5-T. U.S. For. Serv. Res. Note PNW-314, Washington, DC (1978).

6.   Santillo, D.J., Leslie, D.M., Jr., and Brown, P.W., Responses of Small Mammals and Habitat to Glyphosphate Application on Clearcuts. J. Wildl. Manage. 53, 164-172 (1989).

7.   Guerra, R.T., Bueno, C.R., and Schubart, H.O., Preliminary Evaluation of the Effects of the Herbicide Paraquat and Conventional Plowing on the Soil Mesofauna in the Manaus-Amazonias Region. Acta Amazon 12, 7-14 (1982).

8.   Seastedt, T.R., Belowground Macroarthropods of Annually Burned and Unburned Tallgrass Prairie. Am. Midl. Nat. 111, 405-408 (1984).

9.   Seastedt, T.R., Microarthropods of Burned and Unburned Tallgrass Prairie. J. Kansas Entomol. Soc. 57, 468-476 (1984).

10.   Warren, S.D., Scifres, C.J., and Teel, P.D., Response of Grassland Arthropods to Burning: A Review. Agric. Ecosyst. Environ. 19, 105-130 (1987).

11.   Issac, L.A., Fire - a Tool not a Blanket Rule in Douglas Fir Ecology. Proc. Tall Timbers Fire Ecol. Conf. 2, 1-17 (1963).

12.   Bendell, J.F., Effects of Fire on Birds and Mammals, In: Fire and Ecosystems (Kozlowski, T. T., and Ahlgren, C.E., Eds.), Academic Press, New York (1974) pp. 73-138.

13.   Seip, D.R., and Bunnell, F.L., Nutrition of Stone's Sheep on Burned and Unburned Ranges. J. Wildl. Manage. 49, 397-405 (1985).

14.   Boggs, J.F., McMurry, S.T., Leslie, D.M., Jr., Engle, D.M., and Lochmiller R.L., Influence of Habitat Modification on the Intestinal Helminth Community Ecology of Cottontail Rabbit Populations. J. Wildl. Dis. 26,157-169 (1990).

15.   Boggs, J.F., McMurry, S.T., Leslie, D.M., Jr., Engle, D.M., and Lochmiller R.L., Parasitism of Cottontail Rabbits (Sylvilagus floridanus) by Obeliscoides cuniculi in Response to Habitat Modification in the Cross Timbers of Oklahoma. J. Helminthol. Soc. Wash. 57, 146-152 (1990).

16.   Ewing, A.L., Stritzke, J.F., and Kulbeth, J.D., Vegetation of the Cross Timbers Experimental Range, Payne County, Oklahoma. Okla. Agric. Exp. Sta. Res. Rep. P-856 (1984).

17.   Conover, W.J., and Iman, R., Rank Transformations as a Bridge Between Parametric and Nonparametric Statistics. Am. Stat. 35, 124-129 (1981).

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24.   Grundmann, A.W., and Frandsen, J.C., Definitive Host Relationships of the

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Helminth Parasites of the Deer Mouse, Peromyscus maniculatus, in the Bonneville Basin of Utah. J. Parasitol, 46, 673-677 (1960).

25.   Yokogawa, S., The Development of Heligmosomum muris Yokogawa, a Nematode from the Intestine of the Wild Rat. Parasitol. 14, 127-166 (1922).

26.   Engle, D.M., Stritzke, J.F., and McCollum F.T., Brush Management on the Cross Timbers Experimental Range: II. Herbaceous Plant Responses. Okla. Agric. Exp. Sta. Rep. MP-119 (1987) pp. 103-109.

27.   Stritzke, J.F., Engle, D.M., and McCollum, F.T., Brush Management on the Cross Timbers Experimental Range: I. Brush Problems and Responses to Herbicides. Okla. Agr. Exp. Sta. Rep. MP-119 (1987) pp. 99-102.

28.   McMurry, S.T., Effects of Habitat Modification with Herbicide and Prescribed Burning on Small Mammal Populations Inhabiting Cross Timbers Rangeland in Oklahoma. M.S. Thesis, Oklahoma State University, Stillwater, OK (1989).