Effect of Cuterebra fontinella (Mouse Bot Fly) on the Movement of Peromyscus leucopus (White-footed Mouse)
Allison B. Johnson, Tyler J. Barzee, Kasey D. Holbert, Samantha L. Poarch, and Jonathan J. Storm
Southeastern Naturalist, Volume 17, Issue 4 (2018): 597–604
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22001188 SOUTHEASTERN NATURALIST 1V7o(4l.) :1579,7 N–6o0. 44
Effect of Cuterebra fontinella (Mouse Bot Fly) on the
Movement of Peromyscus leucopus (White-footed Mouse)
Allison B. Johnson1, Tyler J. Barzee2,3, Kasey D. Holbert4, Samantha L. Poarch1,5,
and Jonathan J. Storm1,*
Abstract - Peromyscus leucopus (White-footed Mouse) is a common host for Cuterebra
fontinella (Bot Fly), but few studies of this interaction in the southeastern US exist. We assessed
the movement of White-footed Mice infested with Bot Flies at 9 riparian woodland
sites in Spartanburg County, SC. Our objectives were to determine the prevalence of bot
warbles, lumps under the skin containing Bot Fly larva, on White-footed Mice and if the
warbles reduced mouse movement. We found that 17.4% of mice had bot warbles during
the August trapping period, with a mean intensity of 1.21 ± 0.09 (SE) per mouse. Male and
female mice did not differ in the prevalence of bot infestation. Bot-infested mice did not
differ from uninfested mice in their mean squared distance from center of activity (MSD).
During May, mice that later became infested with a bot warble in August, did not differ in
MSD from mice that did not become infested, suggesting that greater movement does not
heighten the risk of infestation. Our data show that bot warbles do not reduce the movement
of White-footed Mice and our findings add to the growing consensus that Bot Flies do not
have a strong negative effect on the ecology of White-footed Mice.
Introduction
Peromyscus leucopus Rafinesque (White-footed Mouse) is a common host for
Cuterebra fontinella Clark (Mouse Bot Fly, hereafter Bot Fly). Female Bot Flies lay
eggs on vegetation and debris near the ground. The sticky eggs adhere to a passing
host and the larvae hatch in response to the host’s body heat. Larvae then enter the
host’s body through an external opening (e.g., nostrils) and travel through the body
cavity before embedding as a subcutaneous lump, termed a warble, typically in the
inguinal region (Catts 1982, Slansky 2007). Once embedded, larvae grow to a mass
of ~1.0 g, or roughly 5% of the body mass of the typical adult White-footed Mouse
(Munger and Karasov 1994).
Within White-footed Mouse populations, the prevalence and intensity of Bot
Flies may differ by sex. For example, Brown and Fuller (2006) found that in environmentally
stressful floodplain environments, bot warbles were more prevalent
in males. Xia and Millar (1990) hypothesized that male mice should have a higher
1Division of Natural Sciences and Engineering, University of South Carolina Upstate,
Spartanburg, SC, 29303. 2Department of Environmental Engineering and Earth Sciences,
Clemson University, Clemson, SC 29631. 3Current address - Department of Biological and
Agricultural Engineering, University of California Davis, Davis, CA 95616. 4Department
of Biological Sciences, Clemson University, Clemson, SC 29631. 5Current address - University
of Florida College of Veterinary Medicine, Gainesville, FL 32608. *Corresponding
author - jstorm@uscupstate.edu.
Manuscript Editor: Michael Cove
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infestation rate because they have a larger home-range than females (Schug et al.
1991, Wolff 1989) and are more likely to passively encounter Bot Fly eggs. Most
studies, however, have found no difference in infestation between sexes (Clark and
Kaufman 1990, Cramer and Cameron 2006, Jaffe et al. 2005, Timm and Cook 1979,
Wecker 1962).
Despite the substantial size of bot warbles and their location within the inguinal
region, they do not appear to hinder the distance moved by mice (Burns et al. 2005,
Cramer and Cameron 2010, Goertz 1966, Hunter, 1972) nor do they alter food
intake (Munger and Karasov 1994). Most studies, though, have focused on comparing
the movement of infested mice to individuals that are not infested at the same
time (but see Cramer and Cameron 2010). One problem with this approach is that it
does not account for individual differences in movement. For example, individuals
may move less because they are infested, or perhaps individuals that move less are
less likely to become infested. In the laboratory, Peromyscus maniculatus Wagner
(Deer Mice) infested with a single bot warble exhibited no difference from uninfested
mice in their ability to locomote and evade predation from Mustela erminea
L. (Ermine). Infested mice were less active than uninfested mice, though, and spent
less time running (Smith 1978).
Although there have been several field studies on the effect of Bot Flies on Whitefooted
Mice (Cramer and Cameron 2006, Jaffe et al. 2005, Timm and Cook 1979,
Wolf and Batzli 2001), relatively few have been done in the southeastern US (but see
Jennison et al. 2006, Klein et al. 2010). In this study, we sought to determine: (1) the
prevalence and intensity of Bot Flies in White-footed Mice, (2) whether bot warbles
reduced the movement of infested mice, and (3) whether mice with larger movements
before the bot season were more likely to become infested.
Field-site Description
Our 9 study sites were mature riparian woodlands in Spartanburg County, SC,
in the northern Piedmont region of the state (Table 1). Study sites were separated
by a mean ± SE of 14.9 km ± 1.1 km, and there were no movements of Whitefooted
Mice between sites. Study sites were a mixture of public (n = 5) and private
Table 1. Location of 9 study sites in Spartanburg County, SC during 2013–2015. Peromyscus leucopus
(White-footed Mouse) infested with Cuterebra fontinella (Bot Fly) were encountered during at least
1 year at each site.
Site Locality (latitude, longitude) Year(s) of Bot-infested mouse capture
1 34°47'58"N, 81°59'51"W 2014
2 34°48'18"N, 81°59'54"W 2014
3 34°55'40"N, 81°46'35"W 2013
4 34°56'2"N, 81°46'39"W 2013
5 34°59'45"N, 81°57'8"W 2013, 2014
6 34°59'9"N, 81°57'49"W 2013
7 35° 0'18"N, 81°57'47"W 2013
8 35° 0'19"N, 81°58'19"W 2014
9 35° 1'1"N, 81°59'1"W 2014, 2015
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(n = 4) land. Each site consisted of mixed deciduous–coniferous forest dominated
by Quercus alba L. (White Oak), Carya tomentosa (Lam. ex Poir.) Nutt. (Mockernut
Hickory), Fagus grandifolia Ehrh. (American Beech), Liquidambar styraciflua
L. (Sweetgum), and Pinus taeda L. (Loblolly Pine). The understory consisted of
Lonicera japonica (Thunb.) (Japanese Honeysuckle), Smilax spp. (greenbriars),
Microstegium vimineum (Trin.) A. Camus (Japanese Stiltgrass), and Vitis rotundifolia
Michx. (Muscadine).
Methods
We live-captured White-footed Mice from 2013 to 2015. During each trapping
session, we baited 125 Sherman live traps (7.6 cm x 8.9 cm x 22.9 cm; H.B.
Sherman Traps, Inc., Tallahassee, FL) with a mixture of oatmeal, sunflower seeds,
and bacon bits, and placed traps in a 5 m x 25 m grid (0.96 ha) with 10-m spacing
between traps at each of the sites. We checked traps for 7 consecutive days during
May and August. We trapped each site for 2–3 consecutive years.
We ear-tagged mice (Monel #1005-1P, National Band and Tag Company, Newport,
KY) and recorded standard measurements for each individual: sex, body
mass, age class (juvenile or adult), hindfoot length, tail length, and the number of
visible warbles. We used the combination of hindfoot and tail length, as well as
mass and coloration, to aid in distinguishing White-footed Mice from Deer Mice
and P. gossypinus Le Conte (Cotton Mouse) (Reed et al. 2004, Webster et al. 1985).
We live-captured and handled animals following the guidelines of the American
Society of Mammalogists (Sikes et al. 2016), and our procedures were approved
by the University of South Carolina Animal Care and Use Committee (Protocol
#2161-100806-042114).
At each site, we calculated the prevalence of Bot Flies as the proportion of
mice that were visibly infested and defined intensity as the number of visible bot
warbles in each individual (Bush et al. 1997). We only calculated bot prevalence
and intensity for sites that had at least 1 infested individual and only during the
August period because we observed no instances of bot warbles in May. We used
a chi-square goodness-of-fit test to test whether there was a difference in Bot Fly
infestation between male and female mice.
To determine the movement pattern of mice during a trapping session, we used
the mean squared distance from center of activity (MSD; Slade and Swihart 1983).
We used MSD because it is unbiased with regard to the number of times each individual
is captured and it exhibits a positive relationship with home-range size
(Slade and Russell 1998). Following the recommendation of Slade and Swihart
(1983), we only included individuals in MSD calculations if they had been captured
at least 3 times during a trapping session. MSD has been used in previous studies
(Cramer and Cameron 2010, Klein and Cameron 2012) to estimate the effect of Bot
Flies on the movement of White-footed Mice. Each individual’s MSD was calculated
as:
MSD = Σ([xi - x̅ ]2 + [yi - y̅ ]2) / n,
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where n is the number of captures for a given individual, xi
is the x coordinate of a
given capture, yi
is the y coordinate of a given capture, and an individual’s center
of activity is represented as the mean of their x and y captures during the trapping
session, x̅ and y̅ .
We performed 2 separate analyses to determine whether Bot Flies reduced the
MSD of infested mice. First, to control for seasonal variation in movement, we
used a 2-way ANOVA to compare the MSD of infested and uninfested mice during
August. Sex and bot status were the independent variables. Next, we controlled for
individual variation by using a repeated-measures ANOVA to compare the MSD
of mice captured in both May and August. In this latter analysis, bot status and
trapping month were independent variables. Increased movement has the potential
to increase the likelihood of bot infestation; thus, we used this repeated measures
design to determine whether mice infested with a bot in August had a larger MSD
during May than mice that did not become infested.
MSD data can be biased for individuals whose center of activity is at the edge
of the grid, as their home range and movements may be mostly outside the trapping
area. This situation could lead to an artificially low MSD for these mice relative to
individuals that have a center of activity in the middle of the grid (Cramer and Cameron
2010). To check for this bias within the May trapping period, we performed
a 2-sample t-test comparing the MSD of individuals with a center of activity in
the outer 10 m of the trapping grid to those with a center of activity in the middle of
the grid. For the August data, we performed a 2-way ANOVA to determine if MSD
was influenced by either the center of activity (edge or middle of grid) or bot status.
We performed statistical analyses in Minitab 17 (Minitab Inc, State College, PA)
and log-transformed data to achieve normality. Data are presented as mean ± SE.
Results
We captured infested mice in August during 2 years at 2 sites and during a single
year at the other 7 sites (Table 1). Across all years, 17.4% of all mice captured (n =
218) in August were infested with 1–3 bot warbles. We found that 84.2% of infested
mice (n = 38) had a single warble, with a mean intensity of 1.21 ± 0.09 SE warbles
per mouse. We also found no strong difference in bot prevalence between male (n =
132, 21.2% infested) and female White-footed Mice (n = 86, 11.6% infested) (χ² =
2.75, df = 1, P = 0.097).
When considering all White-footed Mice captured during August, we found no
effect of sex (F1,140 = 0.78, P = 0.379; Fig. 1) or bot status (F1,140 = 0.05, P = 0.821)
on the MSD. In addition, there was no interaction between sex and bot status (F1,140
= 2.27, P = 0.134) on the MSD.
We used a repeated-measures ANOVA to compare the MSD of individuals captured
in both May and August and found no effect of bot status (F1,90 = 0.17, P =
0.678; Fig. 2) or trapping month (F1,90 = 0.31, P = 0.581) on the MSD. Using a
Tukey pairwise comparison, we found no difference in MSD during May for mice
that did (141.4 m2 ± 70.0 m2) and did not (189.9 m2 ± 29.4 m2) have a bot warble in
August (t = 0.93, P = 0.788).
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Figure 1. Mean ± SE squared distance from the center of activity (MSD) for Peromyscus
leucopus (White-footed Mouse) at 9 field sites in Spartanburg County, SC, during August
2013–2015. Of the 94 males, 18 (19.2% of males) were infested by Cuterebra fontinella
(Bot Fly), whereas 9 of the 50 females (18.0% of females) were infested. There was no effect
of sex or bot warbles on the MSD.
Figure 2. Mean ± SE squared distance from the center of activity (MSD) for Peromyscus
leucopus (White-footed Mouse) captured during both May and August 2013–2015 in
Spartanburg County, SC. Of the 48 individuals captured in May, 10 were subsequently
infested with a Cuterebra fontinella (Bot Fly) in August, whereas 38 individuals were
not infested in August. During May, there was no difference in MSD between mice that did
and did not become infested in August.
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During May, there was no difference between the MSD of mice with a center of
activity at the edge versus those in the middle of the trapping grid (t = 1.36, df =
164, P = 0.177). During August, there was a significant effect of trapping-grid location
on the MSD (F1,141 = 9.51, P = 0.002), with mice in the center of the grid having
a 29.5% larger MSD than individuals from the edge (t = 3.08, P = 0.002). There
was, however, no effect of bot status on the MSD (F1,141 = 0.230, P = 0.631) and no
interaction between center of activity and bot status (F1,141 = 1.24, P = 0.268).
Discussion
Similar to previous studies, we observed bot warbles in White-footed Mice during
August, but not May. Bot warbles are generally most abundant in mice during
July–September (Catts 1982, Hunter 1972, Miller and Getz 1969). We observed
variation across sites in bot presence, which likely resulted from the patchy dispersion
of Bot Flies across the landscape (Catts 1982, Miller and Getz 1969). Prior
studies have also found bot prevalence to be variable between sites (Miller and Getz
1969, Wolf and Batzli 2001). Across all years, the prevalence of bot infestation was
17.4%, which is similar to prior studies that found mean infestation rates of 3–25%
(Clark and Kaufman 1990, Dunaway et al. 1967, Jaffe et al. 2005, Klein et al. 2010).
We did not find a sex difference in bot prevalence, which agrees with the findings
of several studies (Clark and Kaufman 1990, Cramer and Cameron 2006, Jaffe et al.
2005, Timm and Cook 1979). In addition, most individuals harbored a single bot,
which agrees with previous reports (Cramer and Cameron 2006, 2010; Dunaway et
al. 1967, Tim and Cook 1979; Wolf and Batzli, 2001).
We found that infested mice did not have a reduced MSD relative to uninfested
mice, a result found in previous studies (Burns et al. 2005, Cramer and Cameron
2010, Hunter 1972). Given that White-footed Mice are territorial (Barko et al. 2003),
infested mice may have to move as much as uninfested mice in order to forage and
defend their territory (Nupp and Swihart 1996). In addition, mice infested with a bot
warble in August did not have a larger MSD in May than mice that did not become
infested. This finding suggests that bot-infested mice are not individuals with a larger
MSD that might increase their chance of acquiring a bot warble; rather it likely reflects
the life history of Bot Flies, as the eggs are often deposited near a host burrow
(Catts 1982) and mice do not have to move far to become infested.
Similar to prior studies of White-footed Mice in the northern end of their range,
our results suggest that Bot Flies do not reduce the movement of mice. Perhaps the
short-term nature of bot infection, often lasting just 19–26 d (Catts 1982), is one
reason for the lack of a change in movement. Future work should address whether
Bot Flies reduce the speed of movement or alter the microhabitat use of foraging
White-footed Mice. Changes in these behaviors may influence the survival and
overall fitness of bot-infested mice.
Acknowledgments
We thank the following individuals for assistance with fieldwork: R. Dolewski, B.
Doornbos, A. Faso, N. Hyatt, J. Johnson, T. Khleborod, C. Kross, D. Kunda, J. Kwasniewski,
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R. Lever, A. Modarres, J. Morrissey, A. O’Brien, D. Patel, E. Phifer, J. Price, A. Russell, M.
Storm, M. Sudduth, S. Wilkes, and N. Varakin. We are grateful to J. Boyles, V. Connors, and
J.O. Whitaker Jr for comments on the manuscript. We appreciate the University of South
Carolina Office of Research for a Magellan Scholar fellowship provided to S.L. Poarch, the
University of South Carolina Upstate Faculty Excellence Committee for funds provided to
J.J. Storm, and the Office of Sponsored Awards and Research Support for funds provided
to S.L. Poarch and A.B. Johnson.
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