2010 NORTHEASTERN NATURALIST 17(2):223–228
Effect of Bot Fly Parasitism on Vertical Habitat Use by
Peromyscus leucopus
Gregory P. Klein1, Cory C. Christopher1,3, Guy N. Cameron1,*,
and Gary W. Barrett2
Abstract - Peromyscus leucopus (White-footed Mouse) use the 3-dimensional space
of their habitat. We studied whether Cuterebra fontinella (Bot Fly) larvae affected
rate of capture in traps set above ground compared to traps set on the ground in
deciduous forests in Ohio and Georgia. Rates of infestation were nearly three-fold
greater in Ohio than in Georgia. Infested animals were captured equally in traps on
the ground and in traps 1.5 m above ground in Ohio, but were captured less frequently
in traps on the ground than in traps 1.5 m above ground in Georgia. Sex of
animals did not affect these results. Infested animals were not captured in traps 4.5 m
above the ground in Georgia, suggesting a possible limit to use of vertical habitat
space by infested mice.
Introduction
Peromyscus leucopus Rafinesque (White-footed Mouse) is a common
inhabitant of eastern deciduous forest (Lackey et al. 1985). Cuterebra fontinella
Clark (Bot Fly) is an obligate parasite that uses White-footed Mice
as hosts to complete its life cycle (Catts 1982, Slansky 2007). Since mass of
Bot Fly larvae can represent up to 5% of host body mass (Munger and Karasov
1994, Slansky 2007), investigators have asked how infestations of Bot
Fly larvae affect White-footed Mice. Infestations do not affect reproduction
(Smith 1977), metabolism (Hunter and Webster 1974, Munger and Karasov
1994), survival (Munger and Karasov 1991), body condition or population
demography (Cramer and Cameron 2006), movement distance (Cramer and
Cameron 2010), or social behavior (Cramer and Cameron 2007). In fact,
contrary to expectations that animals suffer an energetic cost of infestation,
infested animals survived longer than uninfested animals (Clark and Kaufman
1990, Cramer and Cameron 2006, Jaffe et al. 2005), and animals with
multiple Bot Fly larvae survived longer than animals with a single Bot Fly
larva (Cramer and Cameron 2006). Longevity, however, may be at the expense
of decreased reproductive output by females (Burns et al. 2005).
Bot fly larvae often are located in inguinal regions of mice and may impact
movement, activity, or avoidance of predators (Dalmat 1943, Scott and
Snead 1942, Smith 1978, Wecker 1962). Some laboratory studies reported
awkward movement by infested rodents (Dunaway et al. 1967, Scott and
1Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221.
2Eugene P. Odum School of Ecology, University of Georgia, GA 30602. 3Current address
- Department of Biology, Washington University, St. Louis, MO 63130. *Corresponding
author - g.cameron@uc.edu.
224 Northeastern Naturalist Vol. 17, No. 2
Snead 1942, Smith 1978), but others found no discernable effect of infestation
on mobility (Hunter et al. 1972, Smith 1978). In addition, movement
distances or home ranges were not affected by infestations of Bot Fly larvae
(Burns et al. 2005, Cramer and Cameron 2010, Hunter et al. 1972). Additionally,
Cramer and Cameron (2010) found no difference in movement between
animals with single or multiple infestations, and females moved more than
males when infested. An experimental study by Steen et al. (2002) showed
that probability of predation was similar between infested and uninfested
Microtus townsendii Bachman (Townsend’s Vole).
The White-footed Mouse is semi-arboreal (Fitzgerald and Wolff 1988),
preferring trees for travel routes, nest sites, and day refuges (Barry et al.
1984). G.P. Klein and G.N. Cameron (unpubl. data) found that 66% of
captures of White-footed Mice were in elevated traps in eastern deciduous
forests in Ohio. In deciduous forests in the Piedmont Region of Georgia,
Jennison et al. (2006) surmised that higher infestations by Bot Fly larvae
in White-footed Mice (41.7%) than in Ochrotomys nuttalli Harlan (Golden
Mouse; 6.3–12.5%) were related to greater activity and use of the 3-dimensional
habitat by White-footed Mice, possibly resulting in higher exposure to
Bot Fly eggs. However, only general locations of oviposition sites by female
Cuterebra are known (e.g., foliage, twigs, exposed roots; Slansky 2007), so
it is unclear how infestations are manifest. No study has specifically examined
whether infestation by Bot Fly larvae hinders use of shrubs or trees by
White-footed Mice, and thus, narrows their use of the 3-dimensional habitat.
We predicted that if movement by infested mice is hampered by presence of
Bot Fly larvae, infested mice should be less likely to be caught in elevated
traps than uninfested mice.
Methods
Study sites
Study sites were located in Ohio and Georgia. Study sites in Ohio were
in East Fork Wildlife Area, approximately 39 km SE of Cincinnati (39°1'N,
84°4'W) and consisted of 6–25-ha forest fragments bordered by Glycine max
(L.) Merr. (Soybean) crops. Ohio sites contained second-growth forest dominated
by Fagus grandifolia Ehrh. (American Beech), Acer saccharum Marsh.
(Sugar Maple), Quercus rubra L. (Red Oak), Q. alba L. (White Oak), and
Carya ovata (Mill.) K. Koch (Shagbark Hickory). Undergrowth was dominated
by Toxicodendron radicans (L.) Kuntze (Poison Ivy), Parthenocissus
quinquefoila (L.) Planch (Virginia Creeper), Alliaria petiolata [Biebe] Cavara
& Grande (Garlic Mustard), Rosa multiflora Thunb. (Multiflora Rose),
and Lonicera maackii (Rupr.) Herder (Amur Honeysuckle). Study sites in
Georgia were at the HorseShoe Bend Experimental Research Site located in
Clarke County, near Athens, GA (33°57'N, 83°23'W). Habitat in the Georgia
sites was upland forest dominated by White Oak and American Beech, and
bottomland deciduous forest dominated by Betula nigra L. (River Birch).
Quercus nigra L. (Water Oak), Ligustrum sinense Lour. (Chinese Privet),
2010 G.P. Klein, C.C. Christopher, G.N. Cameron, and G.W. Barrett 225
Smilax L. (Greenbrier), Amur Honeysuckle, and L. japonica Thunb. (Japanese
Honeysuckle) were abundant in both habitats.
Trapping
In Ohio, animals were trapped on three 0.54-ha grids, with 140 traps/
grid. In Georgia, animals were trapped in 4 (in 2000) and 8 (in 2001) 0.21-ha
grids, with 12 traps/grid. In all grids, two Sherman live traps were placed at
10-m intervals—one on the ground, and another on a platform 1.5 m off the
ground, affixed to the trunk of a nearby tree. At the Georgia site in 2001, on
alternating weeks, 4 additional Sherman live traps were placed 4.5 m above
the ground in each trapping grid, alternating with traps placed on the ground
and at 1.5 m. In Ohio, trapping was conducted for 5 days each month from
June through September 2004 (2800 trap nights/grid). In Georgia, trapping
was conducted for 2 days each week from late March through early November
2000 and 2001. Trapping effort in Georgia was 1248 trap nights/plot
using ground and 1.5-m traps in 2000, and 816 trap nights/plot using ground
and 1.5-m traps and 136 trap nights/plot using 4.5-m traps in 2001.
Bot Fly larvae were present in White-footed Mice from early July through
early November in Ohio, with peaks in proportion of animals parasitized in
mid-July and early October (Cramer and Cameron 2006). In Georgia, Bot
Fly larvae were present from early June through mid-August, with a peak
in mid-July 2001 (Jennison et al. 2006). Data collected for each captured
animal included: location of capture (ground or elevated trap), body mass,
sex, hind-foot length, reproductive condition (open or closed vaginal orifice,
abdominal or scrotal testes, pregnant, or lactating), and number of Bot Fly
larvae present. All animals were marked with metal ear tags and released at
their site of capture. Trapping and handling of animals followed guidelines
of the American Society of Mammalogists (Gannon et al. 2007).
Statistical methods
We compared total number of captures in ground and elevated traps
with a 2 x 2 Chi–square contingency table (infestation status, trap location)
separately for Ohio and Georgia to determine whether the proportion
of infested animals captured in elevated traps differed from the proportion of
infested animals captured in ground traps; captures from 4.5-m elevated
traps were excluded from this analysis because none of the animals captured
in 4.5-m high traps were infested, creating a cell with a zero as data. We
also analyzed males and females in separate contingency tables for Ohio
and Georgia to determine if there was a sex effect. Finally, we analyzed data
from Georgia in 2000 and 2001 in separate contingency tables to determine
if there was a year effect at that location.
Results
Abundance of White-footed Mice varied seasonally from 2–25/ha in
Georgia and from 5–47/ha in Ohio (Christopher and Barrett 2006, Cramer
and Cameron 2006). Overall rates of infestation were 2–3 times higher in
226 Northeastern Naturalist Vol. 17, No. 2
Ohio than Georgia (Table 1). Capture ratios of infested males and females
did not differ between elevated (1.5-m high) versus ground traps in Ohio
(males: χ2 = 0.06, df = 1, P > 0.05; females: χ2 = 0.16, df = 1, P > 0.05) or
Georgia (males: χ2 = 0.07, df = 1, P > 0.05; females: χ2 = 1.66, df = 1, P >
0.05); therefore, sexes were pooled for subsequent analyses. Significantly
more infested animals were captured in elevated traps (1.5 m) compared to
ground traps in Georgia when data were pooled for 2000 and 2001 (χ2 = 4.97,
df = 1, P < 0.05; Table 1). However, when years were analyzed separately,
captures of infested animals were significantly higher in elevated traps only
during 2000 (χ2 = 4.06, df = 1, P < 0.05). In Ohio, there was no difference in
rates of capture of infested or uninfested animals between elevated (1.5-m
high) versus ground-level traps (χ2 = 0.13, df = 1, P > 0.05; Table 1).
Discussion
Contrary to our prediction, climbing movement was not hampered by
presence of Bot Fly larvae in White-footed Mice, and infested mice were
not less likely to be captured in elevated traps. Infestation by Bot Fly larvae
did not affect the ability of White-footed Mice to climb in Ohio, since
there was no difference in number of infested animals captured in ground
traps versus 1.5-m elevated traps. In Georgia, animals infested with Bot Fly
larvae occurred more often in elevated traps (1.5-m high) versus ground
traps, although this result only held for 2000. This between-year difference
in Georgia may have resulted because fewer acorns were available on the
ground during the non-mast year of 2000 compared to the mast year of 2001,
and animals may have been forced to forage more extensively in elevated
sites in 2000 (Christopher and Barrett 2006). Mast years were not a variable
in the Ohio study site because oaks were a minor part of the flora.
The finding that infestations by Bot Fly larvae did not hamper Whitefooted
Mice from climbing into above-ground vegetation contradicted our
hypothesis that mass added by Bot Fly larvae would have negative effects
upon climbing by White-footed Mice. On the other hand, none of the animals
captured in 4.5-m elevated traps in Georgia in 2000 were infested with Bot
Fly larvae, which suggests that presence of Bot Fly larvae hindered their use
of habitat beginning somewhere between 1.5 and 4.5 m off the ground. This
Table 1. The number of Peromyscus leucopus (White-footed Mice) infested with Cuterebra
fontinella (Bot Fly) larvae was significantly higher in traps elevated 1.5-m above ground than
in traps on the ground in Georgia (χ2 = 4.97, P < 0.05), but not in Ohio (χ2 = 0.13, P > 0.05). No
infested individuals were captured in elevated traps at 4.5 m in Georgia.
Georgia Ohio
Traps elevated at Ground Traps elevated Ground
1.5 m 4.5 m traps at 1.5 m traps
Infested 39 0 27 75 43
Uninfested 665 36 809 443 236
Percent infested 5.54 0 3.22 14.48 15.41
2010 G.P. Klein, C.C. Christopher, G.N. Cameron, and G.W. Barrett 227
conclusion is reinforced by the finding that animals captured in 4.5-m elevated
traps in Georgia were also captured in ground and 1.5-m elevated traps.
This finding ruled out the possibility that animals captured in 4.5-m elevated
traps were uninfested with Bot Fly larvae because they were exposed to a
different subset of the habitat as animals trapped in ground or 1.5-m elevated
traps. Our results do not address whether agility was hampered in infested
animals while they negotiated above-ground vegetation. Nevertheless, our
findings substantiate the growing body of literature that shows a surprising
lack of significant effects of infestation by Bot Fly larvae on the biology of
White-footed Mice.
Acknowledgments
We thank the staff at HorseShoe Bend Experimental Site in Georgia for field assistance
and the staff at East Fork Wildlife Area in Ohio for allowing us to conduct
studies on their property and for field assistance. Financial support for field work
and analyses was received from the Department of Biological Sciences, University
of Cincinnati, and the Odum School of Ecology, University of Georgia.
Literature Cited
Barry, R.E., Jr., M.A. Botje, and L.B. Grantham. 1984. Vertical stratification of
Peromyscus leucopus and P. maniculatus in southwestern Virginia. Journal of
Mammalogy 65:145–148.
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.
Catts, E.P. 1982. Biology of New World botflies: Cuterebridae. Annual Review of
Entomology 27:313–338.
Christopher, C.C., and G.W. Barrett. 2006. Coexistence of White-footed Mice (Peromyscus
leucopus) and Golden Mice (Ochrotomys nuttalli) in a southestern forest.
Journal of Mammalogy 87:102–107.
Clark, B.K., and D.W. Kaufman. 1990. Prevalence of botfly (Cuterebra sp.) parasitism
in populations of small mammals in eastern Kansas. American Midland
Naturalist 124:22-30.
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.
Cramer, M.J., and G.N. Cameron. 2007. Effects of Bot Fly, Cuterebra fontinella,
parasitism on male aggression and female choice in Peromyscus leucopus. Animal
Behaviour 71:1419–1427.
Cramer, M.J., and G.N. Cameron. 2010. Effects of Bot Fly parasitism on movements
of Peromyscus leucopus. American Midland Naturalist 163:455–462.
Dalmat, H.T. 1943. A contribution to the knowledge of the rodent warble flies
(Cuterebridae). Journal of Parasitology 29:311–318.
Dunaway, P.B., J.A. Payne, L.L. Lewis, and J.D. Story. 1967. Incidence and effects
of Cuterebra in Peromyscus. Journal of Mammalogy 48:38–51.
Fitzgerald, V.J., and J.O. Wolff. 1988. Behavioral responses of escaping Peromyscus
leucopus to wet and dry substrata. Journal of Mammalogy 69:825–828.
228 Northeastern Naturalist Vol. 17, No. 2
Gannon W.L., R.S. Sikes, and the Animal Care and Use Committee of the American
Society of Mammalogists. 2007. Guidelines of the American Society of Mammalogists
for the use of wild mammals in research. Journal of Mammalogy
88:809–823.
Hunter, D.M., and J.M. Webster. 1974. Effects of cuterebrid larval parasitism on
Deer-mouse metabolism. Canadian Journal of Zoology 52:209–217.
Hunter, D.M., R.M.F.S. Sadleir, and J.M. Webster. 1972. Studies on the ecology of
cuterbrid parasitism in Deermice. Canadian Journal of Zoology 50:25–29.
Jaffe, G., D.A. Zegers, M.A. Steele, and J.F. Merritt. 2005. Long-term patterns of
Botfly parasitism in Peromyscus maniculatus, P. leucopus, and Tamias striatus.
Journal of Mammalogy 86:39–45.
Jennison, C.A., L.R. Rodas, and G.W. Barrett. 2006. Cuterebra fontinella parasitism
on Peromyscus leucopus and Ochrotomys nuttalli. Southeastern Naturalist
5:157–164.
Lackey, J.A., D.G. Huckaby, and B.G. Ormiston. 1985. Peromyscus leucopus. Mammalian
Species 247:1–10.
Munger, J.C., and W.H. Karasov. 1991. Sublethal parasites in White-footed Mice:
Impact on survival and reproduction. Canadian Journal of Zoology 69:398–404.
Munger, J.C., and W.H. Karasov. 1994. Costs of Bot Fly infection in White-footed
Mice: Energy and mass flow. Canadian Journal of Zoology 72:166–173.
Scott, T.G., and E. Snead. 1942. Warbles in Peromyscus leucopus noveboracensis.
Journal of Mammalogy 23:94–95.
Slansky, F. 2007. Insect/mammal associations: Effects of cuterebrid Bot Fly parasites
on their hosts. Annual Review of Entomology 52:17–36.
Smith, D.H. 1977. Effects of experimental Bot Fly parasitism on gonad weights of
Peromyscus maniculatus. Journal of Mammalogy 58:679–681.
Smith, D.H. 1978. Effect of Bot Fly (Cuterebra) parasitism on activity patterns
of Peromyscus maniculatus in the laboratory. Journal of Wildlife Diseases
14:28–39.
Steen, H., M. Taitt, and C.J. Krebs. 2002. Risk of parasite-induced predation: An
experimental field study on Townsend's Voles (Microtus townsendii). Canadian
Journal of Zoology 80:1286–1292.
Wecker, S.C. 1962. The effects of Bot Fly parasitism on a local population of the
White-footed Mouse. Ecology 43:561–565.