Male hosts are responsible for the transmission of a trophically transmitted parasite,
Pterygodermatites peromysci, to the intermediate host in the absence of
Lien T. Luong*, Daniel A. Grear, Peter J. Hudson
Center for Infectious Disease Dynamics, Department of Biology, 208 Mueller Laboratory, The Pennsylvania State University, University Park, PA 16802, USA
a r t i c l ei n f o
Received 13 March 2009
Received in revised form 30 March 2009
Accepted 31 March 2009
Indirect life cycle
a b s t r a c t
Field studies have identified that male-biased infection can lead to increased rates of transmission, so we
examined the relative importance of host sex on the transmission of a trophically transmitted parasite
(Pterygodermatites peromysci) where there is no sex-biased infection. We experimentally reduced infec-
tion levels in either male or female white-footed mice (Peromyscus leucopus) on independent trapping
grids with an anthelmintic and recorded subsequent infection levels in the intermediate host, the camel
cricket (Ceuthophilus pallidipes). We found that anthelmintic treatment significantly reduced the preva-
lence of infection among crickets in both treatment groups compared with the control, and at a rate pro-
portional to the number of mice de-wormed, indicating prevalence was not affected by the sex of the
shedding definitive host. In contrast, parasite abundance in crickets was higher on the grids where
females were treated compared with the grids where males were treated. These findings indicate that
male hosts contribute disproportionately more infective stages to the environment and may therefore
be responsible for the majority of parasite transmission even when there is no discernable sex-biased
infection. We also investigated whether variation in nematode length between male and female hosts
could account for this male-biased infectivity, but found no evidence to support that hypothesis.
? 2009 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
A number of studies have found that the majority of parasite
transmission events can be attributed to a minority of infected
hosts such that specific functional groups serve as the primary
shedders of infective stages (Anderson and May, 1991; Woolhouse
et al., 1997; Perkins et al., 2003; Ferrari et al., 2004; Lloyd-Smith
et al., 2005). Comparative studies have demonstrated that males
are more likely to be infected than females and tend to carry higher
parasite intensities, particularly nematode infections of mammals
(Poulin, 1996a; Schalk and Forbes, 1997; Moore and Wilson,
2002). However, while a male bias in parasitism appears to impli-
cate male hosts in driving the parasite dynamics, some have ar-
gued that the sex bias is often relatively small (<5%) and that this
may not be epidemiologically important (Wilson et al., 2002).
Evidence of between-host heterogeneity in transmission has
been documented in only a handful of host–parasite systems. Per-
kins et al. (2003) measured the number of potential transmission
events of tick-borne encephalitis by recording the distribution of
co-feeding on yellow-necked mice (Apodemus flavicollis) and found
that the sexually active males of high body mass were responsible
for more than 90% of the transmission potential. In an experimen-
tal study, Ferrari et al. (2004) treated either male or female yellow-
necked mice with an anthelmintic to remove the most common
nematode, Heligmosomoides polygyrus, and found that when males
were treated, the level of infection amongst the untreated females
fell, but in sites where females were treated the prevalence of
infection among males remained unchanged. Both of these studies
concluded that male hosts were primarily responsible for driving
parasite transmission but there was also evidence of sex-biased
infection; males were more likely to be infected and had higher
intensities of infection. While these studies show that sex-biased
infection is epidemiologically important they do not tell us if the
findings were simply a consequence of higher susceptibility in
the males or whether the male infectivity per parasite was also
Even in the absence of sex-biased infection, males could still be
important if they simply shed more infective stages and/or those
stages are more likely to result in an infection. Variations in the
transmission process can be generated by any one or a combina-
tion of processes: (i) differential production of infective stages,
(ii) differential survival of free living stages, (iii) differential expo-
sure to infective stages, and (iv) differential establishment of para-
sites (Anderson and May, 1991; Keeling et al., 2001). Therefore,
sex-biased transmission can arise if intrinsic differences between
0020-7519/$36.00 ? 2009 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
* Corresponding author. Tel.: +1 814 865 0522; fax: +1 814 865 9131.
E-mail address: firstname.lastname@example.org (L.T. Luong).
International Journal for Parasitology 39 (2009) 1263–1268
Contents lists available at ScienceDirect
International Journal for Parasitology
journal homepage: www.elsevier.com/locate/ijpara
male and female hosts lead to variation in infectivity (via mecha-
nisms i and ii) independently of sex-biased parasitism (via mecha-
nisms iii and iv).
Among helminth infections, variation in infectivity per host is a
product of the number of parasites and egg output per parasite
(Michel, 1969; Ractliffe and LeJambre, 1971; Stear et al., 1997).
Moreover, intrinsic differences between hosts can not only influ-
ence the probability of parasite establishment, but also helminth
growth, survival, size and consequently per capita fecundity (Key-
mer and Slater, 1987; Stear et al., 1995, 1997; Poulin, 1996b;
Tompkins and Hudson, 1999; Wilkes et al., 2004). Consequently,
hosts that harbour larger, more fecund worms should exhibit rela-
tively high shedding rates and hence contribute more infective
stages to the environment than those hosts that carry smaller
and less fecund worms. In this way, shedding rates can vary be-
tween functional host groups even if worm intensity does not. This
leads to the question, ‘Can differences in infectivity between sexes
exist in the absence of sex-biased infection?’.
We address this question by using a parasite–host system with
no male bias in infection and a random distribution of parasites
(Fig. 1; Vandegrift and Hudson, in press). We focus on the white-
footed mouse (Peromyscus leucopus) and its trophically transmitted
nematode, Pterygodermatites peromysci. Since the parasite has a
complex life cycle, we use the intermediate host, a camel cricket
(Ceuthophilus pallidipes) as a means of sampling infective stages
in the environment. This approach provides an alternative to the
conventional egg per gram (EPG) of faeces method of measuring
host infectivity. One drawback of EPG data is that not all eggs shed
into the environment are fertile or have the potential to be infec-
tive (Keymer and Anderson, 1979; Keymer, 1982; Bush et al.,
2001; Hansen et al., 2004) and second, variation in exposure and
susceptibility between male and female hosts can contribute addi-
tional variation to the transmission process. We circumvent these
confounding factors by using the intermediate host as a proxy for
infectivity of the definitive host. Although the crickets may exhibit
variation in exposure and/or susceptibility, this individual-level
heterogeneity is not expected to manifest at the population level
where we estimate infectivity and it is therefore unlikely to influ-
ence the outcome of our experiment.
We test the hypothesis that heterogeneities in parasite trans-
mission, in the form of male-biased infectivity, can arise indepen-
dently of differential establishment rate by experimentally
manipulating the levels of infection in either male or female hosts.
We selectively reduced the number of definitive hosts shedding
infective eggs into the environment, and estimated infectivity as
the level of infection in the camel cricket. If parasite recruitment
rate in crickets is not influenced by host sex, but simply by the
availability of infected hosts (shedders) in the population, we ex-
pect the level of infection among crickets in either treatment group
to be lower compared with the untreated control group, but not
significantly different from each other. In particular, we predict
that the infection levels will be reduced at a rate proportional to
the number of mice treated in the population, independent of the
sex we treated. Alternatively, if infectivity is sex-biased such that
male hosts are more effective at shedding and/or disseminating
infective stages than female hosts, we predict lower levels of infec-
tion among crickets collected from areas where males were treated
compared with where females were treated.
In addition, we examined a potential mechanism underlying the
between-host variation in infectivity by quantifying the variation
in mean nematode length between male and female hosts. A major
component of parasite transmission is the rate at which infective
stages such as eggs are shed into the environment. Intrinsic differ-
ences between individual hosts can influence parasite survival,
developmental, growth and fecundity (Poulin, 1996b; Paterson
and Viney, 2002). Furthermore, numerous studies have demon-
strated that nematode fecundity is positively correlated with nem-
atode size (Ractliffe and LeJambre, 1971; Michael and Bundy, 1989;
Skorping et al., 1991 Stear et al., 1995, 1997; Tompkins and Hud-
son, 1999). Consequently, some hosts may harbour relatively
small, less fecund nematodes while others harbour larger and more
fecund nematodes, potentially generating variation in shedding
rates and hence infectivity. If variation in nematode size accounts
for male-biased infectivity, we would expect male hosts to harbour
larger nematodes than female hosts.
2. Materials and methods
2.1. Study system
The gastrointestinal nematode P. peromysci infects the small
intestine of the white-footed mouse (P. leucopus) and has a 5-week
pre-patent period (Luong, unpublished data; also see Oswald,
1958b). Parasite eggs pass into the host faeces and are ingested
by the intermediate host, the camel cricket (C. pallidipes). The L1
hatches in the midgut, penetrates the hemocoel and develops to
an encysted infective L3 over a period of 10–12 days (Oswald,
1958a). Susceptible mice become infected when they ingest crick-
ets harbouring infective cysts (Oswald, 1958b; O’Brien and Etges,
1981). Cricket eggs hatch in late summer and early instar nymphs
over-winter to become the next years breeding adults, which ma-
ture in late summer (Lavoie et al., 2007).
2.2. Trapping and treating mice
A total of nine trapping grids were established in open hard-
wood forests of central Pennsylvania. Each grid was separated by
a minimum of 200 m, a sufficient distance given that mice were
rarely observed moving between adjacent grids. Of the 870 cap-
tures, only four mice moved between adjacent grids and were re-
corded for a maximum of two consecutive trap nights before
settling on a different grid for the remainder of their captures. Each
grid consisted of 64 multi-capture live traps (Ugglan, Graham,
Sweden) located at 10 m intervals in a 8 ? 8 linear configuration.
Fig. 1. The relationship between log variance and log mean of parasite (Pterygo-
dermatites peromysci) abundance for adult mice on the four extensive trapping sites
for each year from 2003 to 2007. The dotted line represents the 1:1 relationship
where the variance equals the mean, as expected for a random distribution, and the
solid line is the fitted regression line weighted for sample size (modified from
Vandegrift and Hudson, in press).
L.T. Luong et al./International Journal for Parasitology 39 (2009) 1263–1268
Grids were checked for 2 consecutive days every other week from
April 29 to September 10, 2008, totalling 10 trapping sessions for
all grids. Individual mice were tagged with a s.c. passive induced
transponder for individual identification (TrovanTM, EIDAP, Alberta,
Canada). In three replicate grids, males alone received an anthel-
mintic treatment, on three other replicate grids females received
treatment, and on three control grids no mice were treated. Trea-
ted mice were orally administered 1 ll/g of Levamisole Hydrochlo-
ride (dose: 36 mg/kg, AgriLabs?, Missouri, USA) on the third
trapping session and again at each subsequent capture; control
mice were given sterilized water. A preliminary experiment was
conducted during the summer of 2007 to verify the efficacy of
the anthelmintic drug, which was shown to be effective for at least
2 weeks, but for no longer than 4 weeks. Hence, treating mice in
the present study every 2 weeks should be sufficient to prevent
infection (Luong, unpublished data). This experiment was con-
ducted with the approval of the Pennsylvania State Animal Care
Committee (IACUC #23268, ‘‘Transmission Dynamics of Disease
in Wildlife Reservoir Hosts”).
2.3. Transmission to the intermediate host
Camel crickets (C. pallidipes) were collected using pitfall traps
located in close proximity to every other mouse trap, and on alter-
nating rows of each grid (total = 16 traps/grid). The pitfall traps
were set and checked on the same schedule as the mouse trapping
sessions. During the months of August and September, we aug-
mented our collection effort by setting bait (oatmeal flakes) trails
adjacent to the mouse traps and collecting crickets from the bait.
Note there was no significant difference in infection prevalence
for crickets collected in pitfalls versus bait trails (Fisher’s Exact
test, two-tailed, P > 0.05). Prevalence of infection was calculated
as the number of infected crickets divided by the total number dis-
sected. The parasite abundance for a treatment group was mea-
sured as the total number of cysts recovered divided by the total
number of crickets collected, including uninfected individuals.
The developmental stage and caudal femur length (estimate of
body size) of each cricket were also recorded.
To verify that the cysts were P. peromysci larvae, a representa-
tive sample of infective cysts were fed to 22 laboratory white-
footed mice. After a 4–6 week period of development, mice were
necropsied and worms were identified as P. peromysci based on
2.4. Nematode length
Since animals from the present study could not be sampled
destructively, adult stages of the nematode were obtained from
necropsies of animals collected at the end of various unrelated field
experiments conducted between 2003 and 2007 between the
months of August and October; only nematodes recovered from
hosts in control groups from previous experiments were included.
Upon dissection, nematodes were immediately transferred to and
stored in a preservative of 90% ethanol and 10% glycerol. Individual
nematodes were photographed under a stereomicroscope (Leica?
S6E) with a digital camera (Nikon?Coolpix 4500); nematode
length was then measured with the ImageJ software package.
2.5. Statistical analyses
Statistical analyses were performed in R (www.r-project.org). A
generalized linear model (GLM) with binomial errors was used to
analyze parasite prevalence among treatment and control groups.
Differences in parasite abundance were analyzed with negative
binomial errors. Explanatory variables included cricket size, trap-
ping month, grid and anthelmintic treatment. Significance levels
were based on the deviance explained by each factor following
stepwise deletion, retaining variables with P < 0.05 based on v2-
statistics. An a posteriori Helmert contrast was employed to test
for differences between specific treatment groups. We calculated
the expected level of infection based on the proportion of mice
treated in the grids, i.e., assuming no sex-biased transmission.
For example, the expected
grids = (proportion infection of control) ? (proportion infection of
control) ? (proportion males treated), and so on for infection prev-
alence in female-treated grids. The expected mean parasite abun-
dance in each treatment group was calculated in a similar
manner; this value was then used to generate a distribution of
the expected number of cysts per cricket, based on a Poisson distri-
bution. Although the predictions of this experiment are directional,
we use two-tailed tests throughout. Nematode lengths were com-
pared between host sexes using a generalized linear model with a
Poisson error structure. Fixed host factors included body mass, sex
and intensity of infection (number of nematodes per infected host).
3.1. Anthelmintic treatment of mice
We caught 870 white-footed mice over the course of 200 trap
nights and if a mouse was re-caught during a subsequent trap ses-
sion then it was defined a resident. A total of 67 resident mice were
captured on the control grids. On the female-treated grids, a total
of 70 resident mice were caught and tagged, of these 33 females
(47.1%) received the anthelmintic treatment. On the male-treated
grids, 36 males out of the 65 (55.4%) resident mice were treated.
3.2. Prevalence of infection in the intermediate host
The prevalence of infection was not significantly different be-
tween the treatment and control grids prior to treatment, i.e., for
the month of May (deviance (=sum of squares) = 2.26, degrees of
freedom (D.F.) = 2, P = 0.32). Anthelmintic treatment of the defini-
tive host reduced the prevalence of infection among crickets in
the manipulated grids (Fig. 2a). The analysis on prevalence of infec-
tion in crickets post-treatment (June–September) revealed a signif-
icant effect of the anthelmintic treatment (minimal model,
deviance = 8.47, D.F. = 2, P = 0.01) and month (deviance = 32.3,
D.F. = 1, P < 0.001), all other factors and interactions were not sig-
nificant. The prevalence of infected crickets was higher in the con-
trol grids (% mean ± standard error (SE) = 12.5 ± 2.0%) than either
the female-treated (% mean ± SE = 7.4% ± 1.5%) or the male-treated
(6.4 ± 1.5%) grids. Given the significance of month, further analyses
were performed for the months of August and September.
Although we did not detect a significant effect of the anthelmintic
on cricket infection prevalence in August (deviance = 3.40, D.F. = 2,
P = 0.18), the anthelmintic treatment did have a significant effect in
September (deviance = 8.26, D.F. = 2, P = 0.02) in that, the preva-
lence of infection in crickets was significantly higher in the control
grids thaneither thefemale-treated
(coeff.) = ?1.41, SE = 0.61, z = ?2.32, P = 0.02) or male-treated grids
(coeff. = ?1.82, SE = 0.74, z = ?2.48, P = 0.01). An a posteriori com-
parison of the prevalence of infection between the treated grids
showed no significant difference between the two treatment
groups (coeff. = ?0.60, z = ?1.44, P = 0.15).
To account for differences in the proportion of the mouse pop-
ulation treated on the female-treated (47.1%) and male-treated
grids (55.4%), we compared the observed levels of infection among
crickets with the expected values for September and found that the
relative reduction in infection corresponded closely to the propor-
tion of mice de-wormed in each treatment group (Table 1). The
L.T. Luong et al./International Journal for Parasitology 39 (2009) 1263–1268
observed decrease in prevalence for female-treated grids was not
significantly different (goodness-of-fit test, v2= 2.22, D.F. = 1,
P = 0.14) from the expected levels given the proportion of mice
de-wormed (Table 1). Likewise, the magnitude of reduction for
male-treated grids was as predicted based on the number of mice
treated (v2= 0.04, D.F. = 1, P = 0.85).
3.3. Parasite abundance in the intermediate host
Prior to commencing treatment, parasite abundance was com-
parable across all the treatment and control grids (deviance = 0.59,
D.F. = 2, P = 0.75). Our analysis on the post-treatment parasite
abundance in crickets (Fig. 2b) showed a significant effect of month
(deviance = 50.2, D.F. = 1, P < 0.001), treatment (deviance = 10.6,
D.F. = 2, P = 0.005), and month ? treatment interaction (devi-
ance = 18.8, D.F. = 4, P = 0.001). The mean parasite abundance over
the entire sampling periodwas
(mean ± SE = 0.52 ± 0.17),lower
(0.33 ± 0.11), and lowest on male-treated grids (0.24 ± 0.13). Due
to the strong effect of month, September was analyzed separately
on control grids
to test for the simple effect of treatment. Here the anthelmintic
treatment was the only significant explanatory variable in the min-
imal model (deviance = 12.9, D.F. = 2, P = 0.002). Relative to the
control grids, male-treated grids showed a stronger effect size
(coeff. = ?3.25, SE = 0.97, z = ?3.37, P < 0.001) than female-treated
grids (coeff. = ?1.70, SE = 0.80, z = ?2.12, P = 0.03). The a posteriori
pairwise comparison revealed a lower parasite abundance in male-
treated grids (0.12 ± 0.24) compared with female-treated grids
(0.55 ± 0.84) and this difference was nearly significant with a
two-tailed test (z = 1.77, P = 0.07).
Taking into consideration the proportion of mice treated, we
calculated the expected parasite abundance for September (Table
1). The observed parasite abundance in crickets from the female-
treated grids was not statistically different from the expected val-
ues (t-statistic = 1.17, D.F. = 63, P = 0.25); however the observed
parasite abundance in male-treated grids deviated significantly
from the expected values (t-statistic = 3.01, D.F. = 57, P = 0.004).
When females were treated, parasite abundance in crickets simply
reflected the proportion of mice treated, but when males were
treated the reduction in parasite abundance was significantly
greater. These results suggest that males contributed dispropor-
tionately more infective stages that infected crickets than
Overall, the frequency distribution of parasitic cysts amongst
the crickets had an aggregated distribution that did not differ sig-
nificantly from a negative binomial probability distribution
(k = 0.04, P = 0.54). Most crickets harboured either no cysts or less
than two, while a few harboured in excess of 20 cysts and the
majority of the cysts in the cricket population were recovered from
crickets in the control and female-treated grids (Fig. 3).
3.4. Nematode length
For nematode body lengths, we measured 164 P. peromysci from
92 adult mice for a mean length of 18.46 mm ± 0.36 SE. Mean nem-
atode length was not significantly affected by any of the host fac-
tors (P > 0.05). The average worm length was 18.24 mm ± 0.60 SE
among male mice and 18.39 mm ± 0.83 SE among female mice,
the difference was not statistically different (P > 0.05).
The aim of our study was to test whether sex-biased infectivity
can arise in the absence of parasite aggregation and sex-biased par-
asitism. By manipulating the level of infection in replicate mouse
populations, we reduced the proportion of mice shedding infective
stages that subsequently infected crickets. We estimated infectiv-
ity of the definitive host by measuring the infection levels in the
intermediate host and showed that the rate of parasite recruitment
in crickets is directly influenced by the abundance of infected mice.
Fig. 2. Infection rates of Pterygodermatites peromysci in the intermediate cricket
host (Ceuthophilus pallidipes) collected from control (black), female-treated (gray),
and male-treated (dashed) grids over time. (a) Mean prevalence of infection among
crickets. Sample size for May in male-treated grids was insufficient to calculate
prevalence. (b) Mean parasite abundance in crickets. Vertical arrow indicates time
point when anthelmintic treatment was initiated. Error bars indicate ± standard
Observed and expected numbers of crickets infected and uninfected in September
given the proportion of mice treated in each of the treatment groups. The values in
parentheses indicate the proportion of mouse populations treated in each group.
Expected values were calculated based a control prevalence of 35.1% and 1.39 cysts/
cricket (see Section 2 for full explanation).
Host sex treatedObservedExpected
Female (47.1 %)
L.T. Luong et al./International Journal for Parasitology 39 (2009) 1263–1268
The prevalence of infection in the crickets was reduced in both
treatment groups to a level that was proportional to the number
of hosts shedding and there was no difference based on whether
males or females were responsible for the shedding. When females
served as the main shedders of parasite eggs, parasite abundance
among the crickets was significantly lower than when males
served as the primary shedders, indicating that males are indeed
responsible for more transmission than females. The higher para-
site abundance among the grids with the males shedding was
due primarily to a few heavily infected crickets, suggesting that
males are contributing disproportionately more infective stages
than females. Overall our results provide evidence to support the
hypothesis that there is male-biased parasite transmission in a sys-
tem with no male bias in infection and a random distribution of
Our finding of sex-biased transmission is consistent with an
experimental study by Ferrari et al. (2004) where authors demon-
strated that male mice were driving the transmission of an intesti-
nal nematode. However our results go further in three distinct
ways. Firstly, Ferrari et al. (2004) recorded prevalence in the sus-
ceptible host to test for sex-biased transmission and yet individual
variation in exposure and susceptibility, especially between the
sexes, can contribute additional variation to the transmission pro-
cess. We bypassed this confounding factor to some extent by
focusing on a parasite with a complex life cycle and used the inter-
mediate host as a proxy for infectivity (i.e., shedding rate of in-
fected host). Although the cricket host may present its own set of
transmission barriers arising from individual variation in exposure
and/or susceptibility, this individual-level heterogeneity should
not be apparent at the population level of the crickets where we
do the estimation. Second, Ferrari et al. (2004) examined a system
where there was sex-biased parasitism to begin with and so it was
not clear if the sex-biased transmission was simply a consequence
of the variation in the sex-biased parasitism or whether males
were responsible for more infection. Third, the parasite was aggre-
gated in the host population and the individuals in the tail of the
distribution were primarily males and it may be that the individu-
als in the tail are important for driving the infection.
A possible limitation in our study is the sampling method for
the intermediate host in that pitfall traps and bait trails tend to
be biased towards animals that are active. There is also a possibil-
ity that infected crickets experience reduced activity relative to
uninfected crickets; if so we may have underestimated the level
of infection among crickets. Such a sampling bias, however, would
suggest that our findings actually err on the conservative side. Also,
the same method was applied consistently across all treatment
groups and should therefore not influence the differences observed
between the treatment groups. A second possible concern is that
local environmental conditions (e.g., humidity and temperature)
may vary between grids and potentially influence the infectivity
of the eggs to the intermediate host. Yet our analyses show that
grid and its interaction with treatment were not significant factors
in the statistical models; hence there was no evidence of any sys-
tematic bias between the grids.
Due to the random distribution of parasites per definitive host
in this study system (Vandegrift and Hudson, in press), we can rule
out mechanisms that produce differential exposure and suscepti-
bility in the definitive host as a source of sex-biased infectivity.
However, physiological factors such as immune response can con-
ceivably give rise to differences in infectivity, for instance if male
hosts harboured larger helminth parasites than female hosts (Pou-
lin, 1996b). However we found no evidence to support this hypoth-
esis; the mean nematode length was comparable for male and
female hosts. Still, other factors such as duration of egg shedding,
behavioural differences, and variation in contact rates between
male and female hosts may also generate a male bias in infectivity.
Further research is needed to understand the mechanism(s) under-
lying the heterogeneity in infectivity.
Few studies have reported on the infection level of the interme-
diate host following anthelmintic treatment of the definitive host;
further, our study is the first that we are aware of to do so by selec-
tively treating male and female hosts. Parr and Gray (2000) re-
ported a significant reduction in the prevalence of Fasciola
hepatica in snails when all the definitive hosts were de-wormed.
Similarly, an urban baiting experiment showed that the proportion
of vole intermediate hosts infected with Echinococcus multilocularis
was lower in areas where foxes of both sexes received an anthel-
mintic treatment compared with untreated areas (Hegglin et al.,
2003). Sampling the intermediate host not only provides a rela-
tively easy method for assessing the efficacy of an anthelmintic
treatment; it also allows for successive data collection essential
for understanding the temporal dynamics of parasitism, informa-
tion that would otherwise be lost in the destructive sampling of
definitive hosts. Consequently, we found evidence that the effect
of the treatment increased with time, implying a time lag in the re-
sponse of crickets to the anthelmintic treatment. This may have
been a consequence of the extrinsic incubation period, accumula-
tion of cysts in individual crickets over time, ontogenetic changes
in the feeding habits of the crickets, and/or seasonal changes in
the cricket population. Further work is needed to identify the rela-
tive importance of these mechanisms in generating potential sea-
sonal dynamics in the parasite transmission process (Vandegrift
and Hudson, in press).
In conclusion, we experimentally demonstrated a male bias in
the infectivity of a trophically transmitted parasite, notwithstand-
ing a random parasite aggregation and lack of sex-biased parasit-
ism in the definitive host population. These results suggest that
variation in host infectivity can arise independently of differential
exposure and susceptibility mechanisms that underlie sex-biased
parasitism. Importantly, male definitive hosts appeared to be dis-
proportionately more responsible for the majority of transmission
to the intermediate host. Identifying the functional group respon-
sible for transmission is not only useful for understanding parasite
transmission dynamics, but is also informative for targeting the
vulnerable host groups in disease intervention programs (Wool-
house et al., 1997). Sex-biased parasite transmission can also have
potentially important evolutionary implications as a result of dif-
ferential selection pressures on males and females. For instance,
Fig. 3. Frequency distribution of Pterygodermatites peromysci cysts in the interme-
diate cricket host (Ceuthophilus pallidipes) collected from control (black), female-
treated (gray) and male-treated (hatched) grids. Uninfected crickets (n = 751) were
excluded for ease of interpretation.
L.T. Luong et al./International Journal for Parasitology 39 (2009) 1263–1268
if an evolutionary trade-off between the costs of virulence and the Download full-text
benefits of transmission exists, the nature of that trade-off will de-
pend in part on the host responsible for the majority of transmis-
sions (Skorping and Jensen, 2004). As a consequence, the optimal
virulence and cost of parasitism may be different for male and fe-
We are grateful to the many undergraduate students who pro-
vided assistance in the field and to J. Sinclair and B. Bozick for their
technical support in both the laboratory and field. Also, thank you
to I. Cattadori for helpful comments on the manuscript. Special
thanks to T. Cohn for helping us identify the camel cricket to spe-
cies. This research was funded by the National Science Foundation
(Grant No. 0520468).
Anderson, R.M., May, R.M., 1991. Infectious Diseases of Humans: Dynamics and
Control. Oxford University Press, Oxford, UK.
Bush, A.O., Fernandez, J.C., Esch, G.W., Seed, J.R., 2001. Population concepts. In:
Parasitism: The Diversity and Ecology of Animal Parasites. Cambridge
University Press, Cambridge, pp.312–330.
Ferrari, N., Cattadori, I.M., Nespereira, J., Rizzoli, A., Hudson, P.J., 2004. The role of
host sex in parasite dynamics: field experiments on the yellow-necked mouse
Apodemus flavicollis. Ecol. Lett. 7, 88–94.
Hansen, F., Jeltsch, F., Tackmann, K., Staubach, C., Thulke, H.H., 2004. Processes
leading to a spatial aggregation of Echinococcus multilocularis in its natural
intermediate host Microtus arvalis. Int. J. Parasitol. 34, 37–44.
Hegglin, D., Ward, P.I., Deplazes, P., 2003. Anthelmintic baiting of foxes against
urban contamination with Echinococcus multilocularis. Emerg. Infect. Dis. 9,
Keeling, M.J., Woolhouse, M.E.J., Shaw, D.J., Matthews, L., Chase-Topping, M.,
Haydon, D.T., Cornell, S.J., Kappey, J., Wilesmith, J., Grenfell, B.T., 2001.
Dynamics of the 2001 UK foot and mouth epidemic: stochastic dispersal in a
heterogeneous landscape. Science 294, 813–817.
Keymer, A.E., 1982. The dynamics of infection of Tribolium confusum by Hymenolepis
diminuta: the influence of exposure time and host density. Parasitology 84,
Keymer, A.E., Anderson, R.M., 1979. Dynamics of infection of Tribolium confusum by
Hymenolepis diminuta: influence of infective stage density and spatial
distribution. Parasitology 79, 195–207.
Keymer, A.E., Slater, A.F.G., 1987. Helminth fecundity: density dependence or
statistical illusion? Parasitol. Today 3, 56–58.
Lavoie, K.H., Helf, K.L., Poulson, T.L., 2007. The biology and ecology of North
American cave crickets. J. Cave Karst Studies 69, 114–134.
Lloyd-Smith, J.O., Schreiber, S.J., Kopp, P.E., Getz, W.M., 2005. Super spreading and
the effect of individual variation on disease emergence. Nature 438, 355–359.
Michael, E., Bundy, D.A.P., 1989. Density dependence in establishment, growth, and
worm fecundity in intestinal helminthiasis: the population biology of Trichuris
muris (Nematoda) infection in CBA/Ca mice. Parasitology 98, 451–458.
Michel, J.F., 1969. The epidemiology and control of some nematode infections of
grazing animals. Adv. Parasitol. 7, 211–282.
Moore, S.L., Wilson, K., 2002. Parasites as a viability cost of sexual selection in
natural populations of mammals. Science 297, 2015–2018.
O’Brien,R.T., Etges,F.J.,1981. Overwintering
Pterygodermatites coloradensis (Nematoda, Rictulariidae) in Kentucky and
Ohio. Ohio J. Sci. 81, 114–119.
Oswald, V.H., 1958a. Studies on Rictularia coloradensis Hall, 1916 (Nematoda:
Thelaziidae). II. Development in the definitive host. Trans. Am. Microsc. Soc. 77,
Oswald, V.H., 1958b. Studies on Rictularia coloradensis Hall, 1916 (Nematoda:
Thelaziidae). I. Larval development in the intermediate host. Trans. Am.
Microsc. Soc. 77, 229–240.
Parr, S.L., Gray, J.S., 2000. A strategic dosing scheme for the control of fasciolosis in
cattle and sheep in Ireland. Vet. Parasitol. 88, 187–197.
Paterson, S., Viney, M.E., 2002. Host immune responses are necessary for density
dependence in nematode infections. Parasitology 125, 283–292.
Perkins, S.E., Cattadori, I.M., Tagliapietra, V., Rizzoli, A.P., Hudson, P.J., 2003.
Empirical evidence for key hosts in persistence of a tick-borne disease. Int. J.
Parasitol. 33, 909–917.
Poulin, R., 1996a. Sexual inequalities in the helminth infections: a cost of being
male? Am. Nat. 147, 287–295.
Poulin, R., 1996b. Helminth growth in vertebrate hosts: does host sex matter? Int. J.
Parasitol. 26, 1311–1315.
Ractliffe, L.H., LeJambre, L.F., 1971. Increase of rate of egg production with growth in
some intestinal nematodes of sheep and horses. Int. J. Parasitol. 1, 153–156.
Schalk, G., Forbes, M.R., 1997. Male biases in parasitism of mammals: effects of
study type, host age, and parasite taxon. Oikos 78, 67–74.
Skorping, A., Jensen, K.H., 2004. Disease dynamics: all caused by males? Trends Ecol.
Evol. 19, 219–220.
Skorping, A., Read, A.F., Keymer, A.E., 1991. Life-history covariation in intestinal
nematodes of mammals. Oikos 60, 365–372.
Stear, M.J., Bairden, K., Duncan, J.L., Holmes, P.H., McKellar, Q.A., Park, M., Strain, S.,
Murray, M., Bishop, S.C., Gettinby, G., 1997. How hosts control worms. Nature
Stear, M.J., Bishop, S.C., Doligalska, M., Duncan, J.L., Holmes, P.H., Irvine, J., McCririe,
L., McKellar, Q.A., Sinski, E., Murray, M., 1995. Regulation of egg production,
worm burden, worm length and worm fecundity by host responses in sheep
infected with Ostertagia circumcincta. Parasite Immunol. 17, 643–652.
Tompkins, D.M., Hudson, P.J., 1999. Regulation of nematode fecundity in the ring-
necked pheasant(Phasianus colchicus):
Parasitology 118, 417–423.
Vandegrift, K., Hudson, P.J., in press. Could parasites destabilize mouse populations?
The potential role of Pterygodermatities peromysci in the population dynamics of
free-living mice Peromyscus leucopus. Int. J. Parasitol. 39, 1253–1262.
Wilkes, C.P., Thompson, F.J., Gardener, M.P., Paterson, S., Viney, M.E., 2004. The
effect of the host immune response on the parasitic nematode Strongyloides
ratti. Parasitology 128, 661–669.
Wilson, K., Bjornstad, O.N., Dobson, A.P., Merler, S., Poglayen, G., Randolf, S.E., Read,
A.F., Skorping, A., 2002. Heterogeneities in macroparasite infections: patterns
and processes. In: Hudson, P.J., Rizzoli, A., Grenfell, B.T., Heesterbeek, H.,
Dobson, A.P. (Eds.), The Ecology of Wildlife Disease. Oxford University Press,
Oxford, pp. 6–44.
Woolhouse, M.E.J., Dye, C., Etard, J.F., Smith, T., Charlwood, J.D., Garnett, G.P., Hagan,
P., Hii, J.L.K., Ndhlovu, P.D., Quinnell, R.J., Watts, C.H., Chandiwana, S.K.,
Anderson, R.M., 1997. Heterogeneities in the transmission of infectious
agents: implications for the design of control programs. Proc. Natl. Acad. Sci.
USA 94, 338–342.
L.T. Luong et al./International Journal for Parasitology 39 (2009) 1263–1268