Printer Friendly

Effects of bot fly parasitism on movements of Peromyscus leucopus.


Study of individual movement reveals how individuals perceive and respond to their environment. Movements are intricately related to use of space, in terms of home range and defense of territory (Slade and Russell, 1998). Movements also provide a perspective to explain individual patterns of behavior, including but not limited to habitat selection, territoriality and foraging. Moreover, studies of movement behavior also aid in our understanding of population-level phenomena, such as dispersal (Johnson et al., 1992; Stapp and van Horne, 1997).

Movements are intimately related to size of home range (Stickel, 1960; Wolff, 1985), which has been studied extensively for Peromyscus leucopus, a common inhabitant of eastern deciduous forests. Males generally have larger home ranges, which overlap with smaller home ranges of females, and are used by males to gain access to reproductive females (Wolff, 1989). Females, on the other hand, use home ranges for feeding, nesting and rearing young. Differential use of space has further implications for reproductive success and survival, and emphasizes the importance of understanding those factors that affect movements.

Parasitism of Peromyscus leucopus by bot flies (Cuterebra fontinella) may affect movements of individual mice, because these fly larvae are large relative to the size of their hosts (Scott and Snead, 1942; Dalmat, 1943; Wecker, 1962), and they are usually found in inguinal regions of hosts (Cogley, 1991). In the laboratory, Smith (1978a) found that animals infested with bot flies were less active and spent less time in specific locomotor activity (e.g., running on an exercise wheel). In nature, such behavior could translate into shorter or less frequent movements and thus smaller home ranges, which may affect access to resources, such as food, mates or nesting sites (Wolff, 1989). Although field evidence for reduced movements by infested P. leucopus is lacking (Goertz, 1966; Hunter et al., 1972; Burns et al., 2005), individual Peromyscus difficilis moved less during seasons when bot fly prevalence was high (Galindo-Leal, 1997). One problem with these studies was that movements of infested animals were compared to movements of uninfested animals (Munger and Karasov, 1991). It was not clear whether animals moved less because they were infested, or whether animals that moved less became infested. One way to address this question would be to measure movements of the same animal before and during infestation.

Some researchers have suggested that multiple infestations have a more pronounced effect upon movement than single infestations. Many report that mice infested with bot fly larvae had difficulty with locomotion (Scott and Snead, 1942; Sealander, 1961; Wecker, 1962; Childs and Cosgrove, 1966), which was exacerbated when several larvae were present (Dunaway et al., 1967). In the laboratory, mice with more than one bot fly larva were subject to increased predation, presumably because they were easier to capture (Smith, 1978b). In addition, Gingrich and Barrett (1976) found that there was a threshold level of infestation before an immune response could be measured, suggesting that single infestations do not have as strong an effect as multiple infestations.

Infestation also may affect a host's use of space via resource use and predation risk. First, animals may have different dietary needs while they are infested. Assuming resources are not uniformly distributed within the environment, infested mice may alter their use of space to obtain nutrients necessary for reproduction and survival. Physiological studies demonstrated that individuals infested with bot flies have a lower concentration of blood proteins (Dunaway et al., 1967; Hunter and Webster, 1974), and gain weight with the onset of infestation (Hunter and Webster, 1974; Cramer and Cameron, 2006). Second, predators can locate infested mice more easily (Smith, 1978b), and infested mice may alter their patterns of activity to spend more time in areas with more ground cover to avoid predation. A change in activity may not be reflected in size of an individual's home range, but could be determined by comparing where mice spend their time when infested compared to when they are uninfested within their home range.

The objective of this study was to assess whether movement or use of space by white-footed deermice was altered in response to infestation by bot flies. We predicted that: (1) animals would move shorter distances from their center of activity when they were infested compared to when they were uninfested, (2) animals with multiple bot fly infestations would move shorter distances from their center of activity than those that harbored a single larva and (3) individuals would have a different center of activity when infested compared to when they were uninfested.


This study was conducted at East Fork Wildlife Area (39[degrees]1'N, 84[degrees]4'W), Williamsburg, Ohio. Habitat was primarily eastern deciduous forest, punctuated by fields in varying stages of succession. Common tree species included sugar maple (Acer saccharum), beech (Fagus grandifolia), red oak (Quercus rubra), white oak (Q. alba), shagbark hickory (Carya ovata), Ohio buckeye (Aesculus glabra) and wild black cherry (Prunus serotina). Undergrowth was dominated by poison ivy (Toxicodendron radicans), Virginia creeper (Parthenocissus quinquefolia), garlic mustard (Alliaria petiolata), mutiflora rose (Rosa multiflora) and Amur honeysuckle (Lonicera maackii).

Four 0.25-ha grids were established, each consisting of 36 Sherman live-traps, placed in a 6 x 6 configuration, with a spacing interval of 10 m. Although grid size was fairly small, it was still larger than reported home range sizes (0.1 ha) for Peromyscus leucopus (Lackey et al., 1985). Average distance between grids was 807 m (range: 381-1391 m). Mice were never found to move among grids. Each site was trapped weekly during the peak period of bot fly infestation from July through September 2002 and 2003 (Catts, 1982; Cramer and Cameron, 2006). Traps were set at least one hour prior to sunset (1930 h) and were checked the following morning (0600 h). In some cases, traps were checked approximately four hours after sunset (2330 h), encompassing the period of maximal activity for white-footed deermice (Bruseo and Barry, 1995). Time of trap check had minimal effect on capture success: the same number of captures was obtained by checking traps in the morning as during the night (Cramer and Cameron, 2006). Traps were baited with a mixture of rolled oats and sunflower seeds. Data collected for each capture were: sex, body weight, body length, mil length, hind foot length, number of visible bot fly infestations and number and condition of bot fly wounds. Length of hind foot was used to differentiate P. leucopus from P. maniculatus bairdii (Whitaker and Hamilton, 1998). Each animal was uniquely marked with a metal ear tag (#1005 Size 1 Monel, National Band and Tag Co., Newport, Kentucky, USA), and was released at its site of capture. Animals were trapped and handled following the Animal Care and Use Guidelines adopted by the American Society of Mammalogists (Animal Care and Use Committee, 1998), and trapping protocol was approved by the University of Cincinnati Institutional Animal Care and Use Committee (2002: 00-06-21-02; 2003: 03-03-17-01).

Movement was quantified by computing the mean squared distance from center of activity (MSD; Slade and Swihart, 1983). This index was used because it is unbiased with respect to number of captures and it is positively correlated with size of home range (Slade and Russell, 1998). Each capture of a given individual was assigned X and Y coordinates. The mean of all X and Y coordinates for an individual was calculated to define a center of activity (CA). MSD was computed as the sum of the differences between each capture and this center of activity squared. To reduce the seasonal amount of variation in movement (Cummings and Vessey, 1994), MSD was only calculated for summer.

Slade and Swihart (1983) suggested a minimum of three captures were necessary to estimate movement using MSD. Because we subdivided the capture history of each individual into infested and uninfested periods, the minimum number of captures was occasionally as low as two. Therefore, to determine whether number of captures affected MSD, we calculated MSD sequentially for the first two captures, the first three captures, up to the first seven captures for each animal. These MSD values were compared with a repeated measures analysis of variance (ANOVA) to determine if number of captures affected MSD.

Data were analyzed with a repeated measures analysis of variance (ANOVA). Repeated measures were necessary because MSD was calculated for those captures when an individual was uninfested and for those captures when it was infested. This repeated measures approach controlled for variation among individuals (Zar, 1999). Independent variables were sex and infestation status. Infestation status was based on the maximum number of simultaneous bot fly infestations observed (single infestations vs. multiple infestations). All results are presented are mean [+ or -] standard error. Statistical analyses were conducted with SYSTAT (Version 12, Systat Software, Inc., Chicago, Illinois).

A potential bias with MSD concerns individuals captured at the edge of the trapping grids. Individuals caught primarily on the edge may have inaccurate MSD values because movements that occurred outside of the trapping grid would not be included in the index. Nevertheless, our use of a repeated measures design eliminated this bias because individuals were just as likely to be captured at the edge regardless of their infestation status. This assumption was tested prior to analysis by first comparing recapture probabilities for individuals with centers of activity within a 10 m border along the edge of each trapping grid to those with centers of activity in the center of the grid with a t-test. If there was a significant bias in the recapture probabilities, the assumption was further tested by comparing MSD values for individuals on the edge to those in the center of the grid. This was assessed using a repeated measures ANOVA with location (edge vs. center) as an independent factor, and MSD values (infested vs. uninfested) as the repeated measure.

A multi-response permutation procedure (MRPP) was used to compare centers of activity (CA) for individuals when they were infested by bot flies to CA when these same individuals were not infested. Males and females were analyzed separately. MRPP tests response variables based on an a priori grouping variable (Zimmerman et al., 1985). MRPP calculates Euclidean distance between all members of each group, calculates all possible permutations of the data regardless of group membership, and calculates a probability of obtaining the observed distance by chance (Zimmerman et al., 1985). The test statistic, [delta], is compared to a Type III Pearson probability distribution (Mielke et al., 1981). For this specific analysis, the response variables were the X and Y coordinates of centers of activity for individuals when they were infested and uninfested. The grouping variable was infestation status (infested vs. uninfested). A significant result indicates that the center of activity differs with infestation status. The Blossom Statistical Software package (version 2005.11.23) was used to conduct the MRPP test (Cade and Richards, 2005).


Mice were trapped for a total of 3492 traplights. The number of trapnights differed for each grid (Site 1 = 720 trapnights, Site 2 = 1044 trapnights, Site 3 = 828 trapnights, Site 4 = 900 trapnights). For this study, a total of 46 animals (26 males and 20 females) were analyzed. There was no effect of number of captures on MSD ([F.sub.5,195] = 0.33, P = 0.90, n = 40), and this effect did not vary among individuals (Pillai Trace = 0.11, [F.sub.5,35] = 0.83, P = 0.54). Therefore, animals with [greater than or equal to] 2 captures while infested or uninfested were included in the analyses. There was a significant bias in terms of recapture probabilities: individuals in the center of the trapping grids were more likely to be recaptured than those from the edge of the grids ([t.sub.44] = 2.02, P = 0.05). However, even though MSD was higher for individuals from the center of the grids ([F.sub.1,44] = 11.31, P = 0.002), there was no effect of infestation status on this difference ([F.sub.1, 44] = 0.03, P = 0.86).

An additional potential bias was the density of hosts at each trapping site. Based on weekly calculations of minimum number of individuals known to be alive (MNA) on each grid, there was a significant difference in abundance among sites ([F.sub.3,100] = 5.58, P = 0.001). However, there was no significant effect of site on MSD ([F.sub.3,42] = 0.30, P = 0.82).

MSD was significantly higher for males (218.2 [+ or -] 24.3 [m.sup.2]) than females (145.6 [+ or -] 14.2 [m.sup.2]; [F.sub.1,41] = 5.53, P = 0.02; Fig. 1a). There was no effect ofinfestation within individuals ([F.sub.1,41] = 0.61, P = 0.44), but there was a marginally significant interaction between sex and infestation ([F.sub.1,41] = 3.41, P = 0.07). Further analysis of this interaction indicated that infestation did not affect MSD for males (infested MSD = 235.9 [+ or -] 39.5 [m.sup.2], uninfested MSD = 200.4 [+ or -] 25.5 [m.sup.2]; [F.sub.1,41] = 0.87, P = 0.36; Fig. 1a), but there was a trend toward increased movement for females (infested MSD = 183.4 [+ or -] 22.8 [m.sup.2], uninfested MSD = 107.9 [+ or -] 18.9 [m.sup.2]; [F.sub.1,41] = 2.99, P = 0.09; Fig. 1a). Animals with multiple or single infestations had similar values of MSD ([F.sub.1,41] = 0.30, P = 0.59; Fig. 1b). MSD was similar for males with single (248.0 [+ or -] 61.2 [m.sup.2]) or multiple (206.6 [+ or -] 48.8 [m.sup.2]) infestations; the same was true for females (single infested MSD = 122.1 [+ or -] 28.8 [m.sup.2], multiple infested MSD = 97.8 [+ or -] 18.7 [m.sup.2]). There were no significant interactions (sex x status: [F.sub.1,41] = 0.40, P = 0.53; infestation x status: [F.sub.1,41] = 2.48, P = 0.12; infestation x sex x status: [F.sub.1,41] = 0.07, P = 0.80).


Infestation did not affect centers of activity of males or females. Observed distance between centers of activity was equivalent regardless of infestation status for both males ([delta] = 26.41, T = 1.04, P = 0.97) and females ([delta] = 27.58, T = 1.35, P > 0.99).


Bot fly infestation had no apparent effect on movement of male or female Peromyscus leucopus. Although individual females tended to move more when they were infested, this trend was not statistically significant, and females did not move their centers of activity or show a different response to number of infestations. This differential response between males and females could not be attributed to a different number of captures of an individual when infested or uninfested because MSD was independent of the number of captures. These results run counter to the accepted knowledge that bot flies, as parasites, incur some cost for their hosts. However, determination of a cost of harboring bot fly larvae has been elusive at best (Jaffe et al., 2005; Cramer and Cameron, 2006). Even among infested individuals, there was no difference in terms of movement between individuals who had a single infestation and those who had several simultaneous infestations.

Reasons that males and females maintain their home ranges in the face of bot fly infestation may differ. For example, males defend territories to gain access to females (Wolff, 1989) and, in fact, search for females (Myton, 1974; Korytko and Vessey, 1991). Consequences of failing to patrol their home ranges could affect fitness of males, and thus they likely would exhibit the same movement patterns regardless of their infestation status. Females, on the other hand, do not search for males but defend smaller territories centered on nest sites (Wolff, 1989), which are more localized in space and easier to defend. However, there is a potential for bot fly infestation to interfere with reproduction (Cramer and Cameron, 2006) and females may increase size of home ranges when infested to ensure that they have sufficient energy and nutrients for successful reproduction.

Absence of effects of multiple infestations on MSD for either sex was not consistent with conventional wisdom that presence of multiple bot fly larvae makes movement awkward for hosts (Scott and Snead, 1942; Wecker, 1962; Dunaway et al., 1967). One reason that we did not observe effects of multiple infestations ma), be the scale at which our observations were taken. Using live-trapping to monitor movements does not generate the fine-scale tracking of nightly movements that may be required to quantify an effect of parasitism on movement. Other techniques, such fluorescent powder (Graves et al., 1988), spool-and-line (Boonstra and Craine, 1986), or radio telemetry, may provide precise measures of individual movements within a given night necessary to detect subtle differences due to parasitism. In addition, laboratory studies investigating the effects of boy fly larva size and location on the mechanics of locomotion would resolve this issue.

Difficulty of documenting costs of bot fly parasitism has led some to conclude that this interaction may not be parasitism (Jaffe et al., 2005; Cramer and Cameron, 2006). Although we did not measure fitness directly, restriction of movement is consistent with limiting access to resources which could be important for reproduction and survival. We found no evidence of a cost of infestation by bot flies expressed as reduced movement for either males or females. Females are more sensitive to changes in food resources than males (Wolff, 1985), and are under additional pressure to obtain resources to support pregnancy and lactation, which could be a problem during bot fly infestation (Munger and Karasov, 1994). This potential cost could decrease fecundity; in fact, infested females have fewer litters per year than uninfested females (Burns et al., 2005).

Use of non-trapping techniques could demonstrate differences in substrate use with the onset of infestation, and could be used to quantify three-dimensional spatial use of habitat, which is important in small mammal interactions (Pruett et al., 2002). Smith (1978b) suggested that Peromyscus infested with bot flies climb less, a phenomenon that has been observed in the field (Cramer, personal observation). Decline in climbing activity may increase predation rates, which may in turn add to our understanding of the cost of bot fly parasitism. Future studies with more precise measures of movement are needed to increase our understanding of the effect of bot fly infestation on movement.

Acknowledgments.--Assistance in the field was provided by several volunteers, including D. McCubbin, A. Mattingly, K. Roberts and G. Klein. T. Kane, K. Petren, M. Polak, N. Solomon and G. Uetz provided much advice and assistance. Discussions with G. Klein greatly improved this manuscript. Additional comments from Lee Drickamer and three anonymous reviewers helped strengthen the manuscript. Financial support was provided by the Department of Biological Sciences at the University of Cincinnati through several teaching assistantships and a Weiman Summer Research Grant.



ANIMAL CAPE AND USE COMMITTEE. 1998. Guidelines for the capture, handling, and care of mammals as approved by the American Society of Mammalogists. J. Mammal., 79:1416-1431.

BOONSTRA , R. AND I. T. M. CRAINE. 1986. Natal nest location and small mammal tracking with a spool and line technique. Can. J. Zool., 64:1034-1036.

BRUSEO, J. A. AND R. E. BARRY, JR. 1995. Temporal activity of syntopic Peromyscus in the central Appalachians. J. Mammal., 76:78-82.

BURNS, C. E., B.J. GOODWIN AND R. S. OSTFELD. 2005. A prescription for longer life? Bot fly parasitism of the white-footed mouse. Ecology, 86:753-761.

CABE, B. S. AND J. D. RICHARDS. 2005. User manual for Blossom statistical software. U.S. Geological Survey, Fort Collins Science Center, Fort Collins, Colordao.

CATTS, E. P. 1982. Biology of new world bot flies: Cuterebfidae. Ann. Rev. Entom., 27:313-338.

CHILDS, H. E., JR. AND G. E. COSGROVE. 1966. A Study of pathological conditions in wild rodents in radioactive areas. American Midland Naturalist, 76:309-324.

COGLEY, T. P. 1991. Warble development by the rodent bot Cuterebra fontinella (Diptera: Cuterebridae) in the deer mouse. Veterinary Parasitology, 38:275-288.

CRAMER, M.J. AND G. N. CAMERON. 2006. Effects of bot fly (Cuterebra fontinella) parasitism on a population of white-footed mice (Peromyscus leucopus). Journal of Mammalogy, 87:1103-1111.

CUMMINGS, J. R. AND S. H. VESSEY. 1994. Agricultural influences on movement patterns of white-footed mice (Peromyscus leucopus). Am. Midl. Nat., 132:209-218.

DALMAT, H. T. 1943. A contribution to the knowledge of the rodent warble flies (Cuterebridae). J. Parasit., 29:311-318.

DUNAWAV, P. B., J. A. PAVNE, L. L. LEWIS AND J. D. STORY. 1967. Incidence and effects of Cuterebra in Peromyscus. J. Mammal., 48:38-51.

GALINDO-LEAL, C. 1997. Infestation of rock mice (Peromyscus difficilis) by botflies: ecological consequences of differences between sexes. J. Mammal., 78:900-907.

GINGRICH, R. E. AND C. C. BARRETT. 1976. Natural and acquired resistance in rodent hosts to myiasis by Cuterebra fontinella. J. Med. Entom., 13:61-65.

GOERTZ, J. W. 1966. Incidence of warbles in some Oklahoma rodents. Am. Midl. Nat., 75:242-245.

GRAVES, S.,J. MALDONABO AND J. O. WOLFF. 1988. Use of ground and arboreal microhabitats by Peromyscus leucopus and Peromyscus maniculatus. Can. J. Zool., 66:277-278.

HUNTER, D. M. AND J. M. WEBSTER. 1974. Effects of cuterebrid larval parasitism on deer-mouse metabolism. Can. J. Zool., 52:209-217.

--, R. M. F. S. SADLIER AND J. M. WEBSTER. 1972. Studies on the ecology of cuterebrid parasitism in deermice. Can. J. Zool., 50:25-29.

JAFFE, G., D. A. ZEGERS, S, M. A. STEELE AND J. F. MERRITT. 2005. Long-term patterns of botfly parasitism in Peromyscus maniculatus, P. leucopus, and Tamias striatus. J. Mammal., 86:39-45.

JOHNSON, A. R., J. A. WIENS, B. T. MILNE AND T. O. CRIST. 1992. Animal movements and population dynamics in heterogeneous landscapes. Landscape Ecology, 7:63-75.

KORYTKO, A. I. AND S. H. VESSEY. 1991. Agonistic and spacing behaviour in white-footed mice, Peromyscus leucopus. Anim. Behav., 42:913-919.

LACKEY, J. A., D. G. HUCKABY AND B. G. ORMISTON. 1985. Peromyscus leucopus. Mammal. Spec., 247:1-I0.

MIELKE, P. W., JR., K. J. BERRY, P.J. BROCKWELL AND J. S. WILLIAMS. 1981. A class of nonparametric tests based on multiresponse permutation procedures. Biometrika, 68:720-724.

MUNGER, J. C. AND W. H. KARASOV. 1991. Sublethal parasites in white-footed mice: impact on survival and reproduction. Can. J. Zool., 69:398-404.

--AND--. 1994. Costs of bot fly infection in white-footed mice: energy and mass flow. Can. J. Zool., 72:166-173.

MYTON, B. 1974. Utilization of space by Peromyscus leucopus and other small mammals. Ecology, 55:277-290.

PRUETT, A. L., C. C. CHRISTOPHER AND G. W. BARRETT. 2002. Effects of a forested riparian peninsula on mean home range size of the golden mouse (Ochrotomys nuttali) and the white-footed mouse (Peromyscus leucopus). Georg. J. Sci., 60:201-208.

SCOTT, T. G. AND E. SNEAD. 1942. Warbles in Peromyscus leucopus noveboracensis. J. Mammal., 23:94-95.

SEALANDER, J. A. 1961. Hematological values in deer mice in relation to botfly infection. J. Mammal., 42:57-60.

SLADE, N. A. AND L. A. RUSSELL. 1998. Distances as indices to movements and home-range size from trapping records of small mammals. J. Mammal., 79:346-351.

--AND R. K. SWIHART. 1983. Home range indices for the hispid cotton rat (Sigmodon hispidus) in northeastern Kansas. J. Mammal., 64:580-590.

SMITH, D. H. 1978a. Effects of bot fly (Cuterebra) parasitism on activity patterns of Peromyscus maniculatus in the laboratory. J. Wildl. Dis., 14:28-39.

--. 1978b. Vulnerability of bot fly (Cuterebra) infected Peromyscus maniculatus to shorttail weasel predation in the laboratory. J. Wildl. Dis., 14:40-51.

STAPP, P. AND B. VAN HORNE. 1997. Response of deer mice (Peromyscus maniculatus) to shrubs in shortgrass prairie: linking small-scale movements and the spatial distribution of individuals. Func. Ecol., 11:644-651.

STICKEL, L. F. 1960. Peromyscus ranges at high and low population densities. J. Mammal., 41:433-441.

WECKER, S. C. 1962. The effects of bot fly parasitism on a local population of the white-footed mouse. Ecology, 43:561-565.

WHITAKER, J. O., JR. AND W. J. HAMILTON, JR. 1998. Mammals of the eastern United States, 3rd edition. Cornell University Press, Ithaca, New York.

WOLFF, J. O. 1985. The effects of density, food, and interspecific interference on home range size in Peromyscus leucopus and Peromyscus maniculatus. Can. J. Zool., 63:2657-2662.

--. 1989. Social behavior, p. 271-291. In: G. L. Kirkland Jr. and J. N. Layne (eds.). Advances in the study of Peromyscus (Rodentia). Texas Tech University, Lubbock, Texas.

ZAR, J. H. 1999. Biostatistical analysis, 4th edition. Prentice Hall, Upper Saddle River, New Jersey.

ZIMMERMAN, G. M., H. GOETZ AND P. W. MIELKE, JR. 1985. Use of an improved statistical method for group comparisons to study effects of prairie fire. Ecology, 66:606-611.


University of Notre Dame Environmental Research Center, Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana 46556



Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221

(1) Corresponding author
COPYRIGHT 2010 University of Notre Dame, Department of Biological Sciences
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2010 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Cramer, Michael J.; Cameron, Guy N.
Publication:The American Midland Naturalist
Article Type:Report
Geographic Code:1USA
Date:Apr 1, 2010
Previous Article:Temporal variation in terrestrial invertebrate consumption by laughing gulls in New York.
Next Article:Magnitudinal asymmetries in seed production in vaccinium corymbosum: anomaly or not?

Terms of use | Privacy policy | Copyright © 2021 Farlex, Inc. | Feedback | For webmasters