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First published online May 1, 2009
Journal of Experimental Biology 212, 1429-1435 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.029389
Is the feeding and reproductive performance of the flea, Xenopsylla ramesis, affected by the gender of its rodent host, Meriones crassus?
1 Desert Animal Adaptations and Husbandry, Wyler Department of Dryland
Agriculture, French Associates Institute for Agriculture and Biotechnology of
Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion
University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion,
Israel
2 Mitrani Department of Desert Ecology, Swiss Institute for Dryland
Environmental Research, Jacob Blaustein Institutes for Desert Research,
Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet
Ben-Gurion, Israel
* Author for correspondence (e-mail: krasnov{at}bgu.ac.il)
Accepted 12 March 2009
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: rodents, fleas, gender, blood meal size, egg production
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). One of the
mechanisms to maximize reproductive success is to select habitats or patches
that will lead to the greatest fitness reward
(Rosenzweig, 1981). This
statement is true for both free-living and parasitic organisms, although the
latter are rarely considered as individuals that are able to make decisions
regarding their foraging and reproductive success
(Sukhdeo, 1994). Nevertheless,
recent studies have demonstrated that parasites appear to make choices and
decisions that favour environments (=hosts) in which their reproductive
benefit is maximized (Krasnov et al.,
2002a; Krasnov et al.,
2003), although it is still unknown how they make their
cost/benefit decisions and by which means they evaluate between-host
differences.
The distribution of parasites among hosts is not random. Some host
individuals, populations or species are characterized by a higher level of
infestation by a parasite than other individuals, populations or species
(Combes, 2001;
Poulin, 2007). This suggests
that parasites prefer some hosts over others and that these preferences are
supposedly based on fitness-related decisions. For example, gender-biased
differences in infestation by parasites have been recorded in numerous
vertebrate hosts and for a variety of parasite taxa
(Zuk and McKean, 1996;
Poulin, 1996; Schalk and
Forbes, 1996; Hughes and Randolph,
2001; Tschirren et al.,
2003; Morand et al.,
2004; Krasnov et al.,
2005; Gorrell and
Schulte-Hostedde, 2008). In most higher vertebrate hosts (birds
and mammals), parasitism is male-biased, i.e. male hosts are infested more
often and/or by more parasites than female hosts, although female-biased
parasitism has also been reported
(Morales-Montor et al., 2004;
Krasnov et al., 2005). This
would suggest that in many cases male mammals or birds represent better
patches for parasites than females.
A parasite supposedly selects a host that may allow easier encounter and/or
more effective resource acquisition
(Combes, 2001). The latter
includes not only the direct extraction of resources but also the ability of a
parasite to cope with the host's defence system. These considerations have led
to two main, but not mutually exclusive, hypotheses regarding male-biased
parasitism. One hypothesis suggested that the main reason for gender-biased
parasitism is gender difference in mobility. Indeed, males of higher
vertebrates are usually more mobile than females and, thus, the chances of
males to be exposed to a larger variety and number of parasites are greater
than those of females (Tinsley,
1989; Lang, 1996).
A second hypothesis related male-biased parasitism to differences in
immunocompetence between male and female hosts because of the
immunosuppressive effect of androgens
(Zuk, 1996;
Zuk and McKean, 1996). The
relative importance of mobility and immunocompetence of hosts in the
manifestation of male-biased parasitism is still poorly understood
(Morand et al., 2004).
The majority of studies of gender-biased parasitism have been observational
and only a few experimental investigations have been carried out. These
experiments were aimed mainly to test the immunocompetence hypothesis (for a
review, see Klein, 2000) and
were host-focused, for example, they considered differential susceptibilities
of males and females to various infections
(Klein et al., 1997;
Klein, 2000). By contrast,
parasite responses to the effect of host gender have been largely neglected.
Nevertheless, if host choice by a parasite is important to maximize
reproductive success (Lomnicki,
1988), then the study of the parasite's performance in hosts
belonging to different genders is crucial for understanding the mechanisms of
infestation biases.
One of the reasons for the lack of experimental studies of parasite
performance is the difficulty in measuring this performance, although the
results of several experiments have been reported (for a review, see
Sukhdeo and Sukhdeo, 1994).
For example, Sukhdeo measured the number of larvae produced per female
Trichinella spiralis to test whether the performance of helminths
depends on the site of infection (anterior or posterior small intestine of the
rat host) (Sukhdeo, 1991).
However, such studies require complicated techniques, such as surgery and/or
sacrifice of laboratory animals. In contrast to endoparasites, ectoparasites,
such as fleas (Siphonaptera), have advantages as laboratory models. These
insects are obligatory hematophages feeding mainly on small and medium sized
mammals. Flea larvae are not usually parasitic and feed on organic debris and
materials found in the nest of the host. In most cases, larval and pupal
development is entirely off-host. After emergence from the cocoon, adult fleas
locate a host to complete the life cycle. Adults remain as permanent
satellites of their mammalian hosts, alternating periods on the host with
periods when they occur in the burrow or nest. Thus, it is possible to
manipulate flea infestation on living hosts and to monitor changes in an
individual flea over time.
In this study, we asked if and how fitness-related parameters of fleas are
affected by the gender of their hosts. To answer this question, we
investigated foraging and reproductive performance of fleas (Xenopsylla
ramesis) parasitizing male and female Meriones crassus, a
gerbilline rodent. M. crassus is one of the most common rodent
species of southern Israel. It occupies a variety of habitats and is
parasitized by several flea species, of which X. ramesis is one of
the most abundant (Krasnov et al.,
1997). In the field, male M. crassus have been found to
harbor more abundant and more species-rich flea assemblages than females,
although this difference was pronounced only in winter
(Krasnov et al., 2005). We
predicted that fleas will perform better on male than on female hosts in that:
(1) the size of a blood meal will be greater when taken from a male rather
than a female host and (2) female fleas will produce more eggs when exploiting
a male rather than a female host.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). The
strongest host response to flea bites was reported to occur 7–14 days
after flea feeding began (Hudson at al.,
1960), although this period can probably be characterized by rapid
changes and, therefore, relatively low stability of immune system function.
Nevertheless, even a single infestation by ectoparasites was reported to
induce acquired resistance (Trager,
1939). In total, we used 32 male and 30 female rodents.
Fleas
Fleas were obtained from our laboratory colony started in 1999 from
field-collected specimens on M. crassus, using the rearing procedures
described elsewhere (Krasnov et al.,
2001; Krasnov et al.,
2002b), and maintained at 25°C and 75% relative humidity (RH)
with a photoperiod of 12 h:12 h (L:D). An individual rodent host was placed in
a plastic cage that contained a steel nest box with a wire mesh floor and a
pan containing a mixture of sand and dried bovine blood as larvae nutrient
medium. Every two weeks, we collected all substrate and bedding material from
the nest box and transferred it to an incubator (see below), where the fleas
developed at 25°C air temperature and 75% RH. Air temperature was
regulated in refrigerated incubators (FOC225E, Velp Scientifica srl, Milano,
Italy), humidity was regulated using saturated salt solutions
(Winston and Bates, 1960) and
both air temperature and humidity were monitored (Fisherbrand Traceable
Humidity/Temperature Pen with Memory, Fisher Scientific International,
Somerville, NJ, USA). In total, 1240 female and 620 male fleas were used.
Experimental procedures
Fleas used in our experiments were 24–48 h old and did not feed from
emergence until experimental treatments. During the period between emergence
and experiments, these fleas were maintained in an incubator at 25°C and
75% RH. Each individual rodent was placed in a wire mesh (5x5 mm) tube
(15 cm length and 5 cm diameter) that limited movement and did not allow
self-grooming. Tubes with rodents were placed in individual white plastic
baths. Twenty female and 10 male X. ramesis were placed on each
rodent. We used more female than male fleas because the time between
consecutive matings is much shorter in male than female fleas, so that a
single male can copulate with several females during a short period
(Marshall, 1981). After
feeding on a host for 60 min, fleas were collected by brushing the fur of the
rodent with a toothbrush until all of the fleas were recovered. This procedure
takes no more than 10 min. To test for the possible confounding effect of
shedding excess water from the blood meal on body mass of fleas after feeding,
we carried out preliminary measurements in which we weighed fleas (10 males or
10 females by groups in three replicates) immediately after and every 10 min
for 60 min post-feeding on an adult male rodent. We analyzed the effect of
post-feeding period on body mass change of fleas before and after feeding
using repeated-measures analyses of variance (ANOVAs) with body mass change
per unit body mass of a starving flea as a dependent variable. Body mass
change of fleas during 60 min post-feeding did not show significant
differences (F6,12=1.27 and F6,12=0.83
for male and female fleas, respectively; P>0.34 for both). Fleas
from each host were placed in plastic cups (200 ml), of which the bottom of
each cup was covered by a thin layer of sand and small pieces of filter paper,
then transferred to an incubator and maintained at 25°C air temperature
and 92–95% RH. The feeding procedure was repeated for each group of
fleas on the same host individual every day for eight consecutive days. On the
first, fifth and eighth days of feeding, fleas (males and females separately)
were weighed (±0.01 mg, 290 SCS Precisa Balance, Precisa Instruments
AG, Dietikon, Switzerland) before and immediately after feeding and the
difference in mass was taken as blood consumption. These time intervals were
chosen because our preliminary results demonstrated that the rate of blood
consumption by X. ramesis decreases substantially after the event and
recovers after two to three days (I.S.K. and B.R.K., unpublished data).
Some fleas departed from their hosts before 60 min. We assessed the level of midgut engorgement of fleas under a light microscope (without dissection) and found that in all of them (including those that departed) more than 80% of the midgut was filled with blood. All departed fleas were likely to be those that satiated their appetite earlier than other fleas but consumed approximately the same amount of blood as fleas that did not depart from a host until the end of the experimental bout.
In total, 32 groups of fleas were fed on male rodents and 30 groups on female rodents. From these groups, we randomly selected 10 groups from male hosts and 10 groups from female hosts and measured their egg production. Every day, pieces of filter paper from each plastic cup with fleas were examined under a light microscope, and the day of oviposition from the first feeding event and the number of eggs were recorded.
The experimental design was found to be suitable and to meet requirements of the 1994 Law for the Prevention of Cruelty to Animals (Experiments on Animals) of the State of Israel (Ben-Gurion University Committee for the Ethical Care and Use of Animals in Experiments, License IL-36-9-2007).
Data analysis
Feeding success was evaluated as: (1) the absolute amount of blood consumed
per flea, (2) the mass-specific amount of blood consumed by a flea and (3) the
proportion of fleas that satiated their appetite in less than 60 min of
feeding (see above). We calculated the amount of blood consumed by a flea
(=mean blood meal size) per unit body mass as the difference between the total
mass of fleas after feeding and the total mass of fleas prior to feeding; this
value was divided by the total mass of fleas prior to feeding.
Initially, we calculated the absolute and mass-specific amount of blood consumed and the proportion of early satiated fleas separately for male and female fleas, and tested for flea gender differences in these variables using t-tests with flea gender as a grouping factor separately for male and female hosts and for each of the three days of feeding. The absolute amount of blood consumed by a female flea was greater than that of a male flea (on average, 0.066±0.003 and 0.031±0.002 mg, respectively) due to the larger body size of females. However, when between-gender differences in body size were taken into account, males and females consumed similar relative amounts of blood (0.280±0.016 and 0.265±0.020 mg mg–1 body mass, respectively, t-tests, t=0.31–1.22, P>0.10 for all). The proportion of early satiated individuals was also similar between male and female fleas, all else (host gender and day of feeding) being equal (on average, 0.131±0.009 and 0.129±0.002, respectively; t-tests, t=0.55–1.32, P>0.22 for all). Consequently, data on feeding performance of female and male fleas were pooled together.
To evaluate reproductive performance, we calculated the mean number of eggs produced per female flea per day for each group of fleas for five days after the first oviposition event. This event occurred on the fourth day of feeding in all groups of fleas. Reproductive rate was evaluated as: (1) the number of days from the first feeding event to the day with maximal egg output and (2) the number of eggs produced per day during five days of oviposition by a female.
All measurements, except for proportions, were log-transformed prior to analysis. Proportions were arcsin-transformed, which produced distributions that did not deviate significantly from normality (Kolmogorov–Smirnov tests; P>0.20 for all). The only exception was the number of days from the first feeding event to the day with maximal egg output. Frequency distribution of this variable deviated significantly from normality even after log-transformation (Kolmogorov–Smirnov test; P<0.05). Consequently, non-parametric statistics were applied. Time from the first feeding event to the day with maximal egg output was analyzed using a Mann–Whitney U-test with host gender as grouping variable.
Because the same group of fleas was fed repeatedly on the same individual rodent, we analyzed the mass-specific amount of blood consumed, the proportion of early satiated fleas and the number of eggs produced per day during five days of oviposition by a female (dependent variables) using repeated-measures ANOVAs with host gender as a between-group factor (categorical predictor) and day of feeding as within-subjects (repeated-measures) factor. Tukey's honest significant difference (HSD) tests were applied for all multiple comparisons. Untransformed data are presented in figures.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The proportion of early satiated fleas was affected by both host gender, day of feeding and the interaction between these two factors (Table 1). The first effect was manifested in the higher proportion of fleas satiated earlier when they fed on male rather than on female hosts whereas the manifestation of the second effect was that this proportion decreased from the first to the last feeding event (Fig. 2). The latter was true for male hosts (21.4±4.9% versus 11.6±2.2% on the first day and eighth day of feeding, respectively; Tukey's HSD test, P<0.001) but not for female hosts (6.4±1.6% versus 5.0±1.9% on the first day and eighth day of feeding, respectively; Tukey's HSD test, P>0.90), which was the reason behind the significance of the interaction factor.
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Egg production of female fleas differed significantly between females feeding on male and female hosts and the interaction between factors of host gender and day of oviposition was significant (Table 2). In general, fleas fed on male hosts produced significantly more eggs than those fed on female hosts except for the first and second days of oviposition, i.e. the fourth and fifth days of feeding (Tukey's HSD tests; P<0.05 versus P=0.35–0.99, respectively) (Fig. 3). Egg production within gender was significantly lower on the first day (in fleas fed on female hosts) or the first and second (in fleas fed on male hosts) days of oviposition than later (Tukey's HSD tests; P<0.05 for all comparisons) (Fig. 3).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The immune system is the main tool of defence against parasitism. This
system is aimed to discriminate between `self' and `non-self' and to minimize
the consequences of contact with foreign molecules introduced into the host by
feeding parasites. Immune defence mechanisms of vertebrates include two
components: innate and acquired (adaptive) immunities
(Janeway et al., 1999). It is
acquired immunity that is believed to play a major role in the host developing
resistance to parasites (Wakelin,
1996). In the case of ectoparasites, this is manifested by a
decrease in feeding and in the reproduction of ectoparasites exploiting hosts
that have been previously repeatedly attacked by this or closely related
parasites (Willadsen, 1980;
Fielden et al., 1992;
Rechav, 1992) [but see
Johnston and Brown and Vaughan et al.
(Johnston and Brown, 1985;
Vaughan et al., 1989)].
Immunocompetence is the general capacity of an organism to mount an immune
response against pathogens and parasites
(Schmid-Hempel, 2003). Gender
differences in immunocompetence have been reported for a variety of
homeotherms, with males being generally less immunocompetent than females
(Olsen and Kovacs, 1996;
Poulin, 1996) supposedly due
to higher levels of androgens that suppress the immune system
(Folstad and Karter, 1992).
However, the relationship between testosterone and immune function is
equivocal (Castro et al., 2001;
Rolff, 2002;
Schmid-Hempel, 2003;
Vainikka et al., 2004). For
example, Rolff proposed an alternative hypothesis explaining sexual
differences in immunocompetence due to a higher investment of females into
immune defence (Rolff, 2002).
Nevertheless, testosterone injections reduced the resistance of rodents
Myodes glareolus and Apodemus sylvaticus to parasitism of
the tick Ixodes ricinus (Hughes
and Randolph, 2001). Grieves et al. (Grieves et al., 2006) found
that testosterone levels in birds Junco hyemalis were significantly
negatively correlated with immune-related variables, suggesting that elevated
testosterone levels may compromise immune function.
Our earlier results suggest that male M. crassus are less
immunocompetent than conspecific females. Khokhlova et al. found that females
of this rodent had higher levels of circulating immune complexes than males
(Khokhlova et al., 2004). This
indicates a higher synthesis of antibodies and clearance of the antigen
through complexation in females. Göuy de Bellocq et al.
(Göuy de Bellocq et al.,
2006) used the phytohemagglutinin injection assay (PHA test)
(Smits et al., 1999) to
measure immunocompetence in M. crassus by subcutaneous injection of
vegetal lectin, a phytohemagglutinin that induces local T-cell stimulation and
proliferation that causes swelling. The PHA response was higher in
non-parasitized female than in non-parasitized male M. crassus but
this difference disappeared after the rodents were exposed to parasitism by
X. ramesis. However, no correlation between the PHA response and egg
production and blood consumption of X. ramesis was found in this
study. The reason for this could be that the PHA test in this previous study
was applied after flea infestation trials and the PHA response appeared to be
sensitive to flea infestation. Therefore, the strength of the PHA response did
not reflect the overall immunocompetence of individuals
(Göuy de Bellocq et al.,
2006). Consequently, the relationship between performance of fleas
and immunocompetence assessed by the PHA response requires further
investigation. Future experiments should involve measuring flea performance
after applying the PHA test, which would permit the avoidance of the
immuno-suppressing effect of flea infestation. However, Göuy de Bellocq
et al. (Göuy de Bellocq et al.,
2006) found a correlation between changes in rodent leucocyte
concentration after 15 days of flea parasitism and flea fitness (egg
production and hatching success) and feeding (blood meal size) variables,
implying that the host's immune response affected the reproductive physiology
of the fleas.
Apart from the present study, other studies have also suggested that gender
differences in immunocompetence can cause gender difference in parasite
performance. For example, Haas studied survival and feeding of a flea
Xenopsylla vexabilis parasitizing its rodent host, Rattus
exulans, and found that the fleas had higher survival and more blood
consumption on adult male hosts followed by adult females and juvenile males
(Haas, 1965).
The results of our present study strongly advocate that the immediate
reason behind male-biased flea parasitism is gender difference in the immune
response; however, the effect of differential mobility between males and
females on their difference in flea infestation in the field cannot be
discounted. Indeed, male M. crassus have larger home ranges than
females (Daly and Daly, 1975).
Consequently, the two mechanisms are not mutually exclusive and both
supposedly play a role in gender differences of parasitism pattern. However,
during the hot desert summer, when M. crassus do not reproduce
(Krasnov et al., 1996) and
thus testosterone levels in males are supposedly low, males and females were
equally parasitized by fleas (Krasnov et
al., 2005). This suggests that gender difference in
immunocompetence rather than gender difference in mobility may be a more
important mechanism for male-biased parasitism, especially given that male and
female M. crassus do not demonstrate seasonal changes in their home
range size (G.I. Shenbrot and B.R.K., unpublished data).
Temporal dynamics of flea responses and host-gender-related differences
require some explanation. We found that fleas consumed more blood from a male
than from a female host during the first feeding event only. The first feeding
event is critically important for fleas as the majority of fleas are able to
mate only after feeding. Newly emerged female fleas have underdeveloped
ovaries blocked with a follicular plug
(Vashchenok, 1966) whereas
newly emerged males of many species have a testicular plug that prevents the
passage of sperm from the testes to the vas deferens
(Dean and Meola, 1997). The
first blood meal is a trigger for the development of ovaries in female fleas
(Liao and Lin, 1993) and for
the dissolution of the testicular plug in males
(Kamala Bai and Prasad, 1979).
However, after the first blood meal, the relative amount of blood taken from
male hosts decreased whereas that taken from female hosts increased. The
pattern for male hosts was also supported by the decrease in the proportion of
early satiated fleas during the fifth and eighth feeding events as compared
with the first feeding event. A possible explanation is that male rodents
continued to develop resistance against fleas whereas fleas managed to
downregulate the response of female rodents. However, this explanation is
highly speculative and requires further investigation.
We also found no host-gender-related differences in the number of eggs
produced in the beginning of oviposition. The reason for this may be that
first clutches of young fleas are usually small
(Vashchenok, 1988;
Vashchenok, 1993;
Vashchenok, 2001). The rate of
egg production then increases, which is followed by a decrease. Vashchenok
studied egg production in fleas (Leptopsylla segnis) that were
allowed continuous access to a host (laboratory mouse) for 40 days
(Vashchenok, 2001). Peak egg
production occurred when a flea was 6–10 days old. Unimodality of
age-related changes in egg production have also been reported for other flea
species, such as Xenopsylla skrjabini, Xenopsylla nuttalli, Xenopsylla
gerbilli and Xenopsylla conformis (for a review, see
Krasnov, 2008). Larger blood
meals are usually associated with higher egg output in blood-feeding
arthropods (Lehane, 2005).
However, the generally low rate of first egg laying in fleas coupled with the
large amount of blood taken during the first feeding event on male hosts is
the likely reason behind an apparent contradiction between the trend of
oviposition rate to increase over time
(Fig. 3, male hosts) and the
trend of blood meal size to decrease over time
(Fig. 1, male hosts).
Experimental procedure in our present study included placing the rodents in
mesh tubes to minimize the effect of the host's behavioural defence
(anti-parasitic grooming). This might cause stress that, in turn, might affect
flea feeding. For example, some fleas fed better on unrestrained than on
restrained hosts (Bar-Zeev and Sternberg,
1962; Liu et al.,
1993). If the levels of stress were gender-specific, this might
influence our results via gender difference in the level of stress
hormones, such as blood cortisol levels. However, we believe that repeated
exposures of rodents to fleas prior to experimental treatments (see Materials
and methods) decreased the probability of this hypothetical effect because
rodents subjected to the restrained conditions every two days were likely to
be accustomed to these conditions.
In conclusion, better feeding and reproductive performance of fleas on a male seems to be the mechanism behind male-biased parasitism. However, our present study was restricted to one host species and one flea species. A question that remains is how general is the pattern and to what extent they apply to other parasite–host associations. Studies on other ectoparasite (including other fleas) and host species (including other mammals) would allow us to better understand parasite preference of host gender and whether our finding is a general phenomenon.
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Bar-Zeev, M. and Sternberg, S. (1962). Factors affecting the feeding of fleas (Xenopsylla cheopis Rothsch.) through a membrane. Entomol. Exp. Appl. 5, 60-68.
Castro, J. M., Nolan, V. and Ketterson, E. D. (2001). Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). Am. Nat. 157,408 -420.[CrossRef][Medline]
Combes, C. (2001). Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago, IL: University of Chicago Press.
Daly, M. and Daly, S. (1975). Socio-ecology of Saharan gerbils, especially Meriones libycus. Mammalia 39,289 -312.
Dean, S. R. and Meola, R. W. (1997). Effect of juvenile hormone and juvenile hormone mimics on sperm transfer from the testes of the male cat fea (Siphonaptera: Pulicidae). J. Med. Entomol. 34,485 -488.[Medline]
Fielden, L. J., Rechav, Y. and Bryson, N. R. (1992). Acquired immunity to larvae of Amblyomma marmoreum and A. hebraeum by tortoises, guinea-pigs and guinea-fowl. Med. Vet. Entomol. 6, 251-254.[Medline]
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Goüy de Bellocq, J., Krasnov, B. R., Khokhlova, I. S., Ghasaryan, L. and Pinshow, B. (2006). Immunocompetence and flea parasitism in a desert rodent. Funct. Ecol. 20,637 -646.[CrossRef]
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Johnston, C. M. and Brown, S. J. (1985). Xenopsylla cheopis: cellular expression of hypersensitivity to guinea pigs. Exp. Parasitol. 59, 81-89.[CrossRef][Medline]
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Khokhlova, I. S., Spinu, M., Krasnov, B. R. and Degen, A. A.
(2004). Immune response to fleas in a wild desert rodent: effect
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Klein, S. L. (2000). The effects of hormones on sex differences in infection: from genes to behavior. Neurosci. Biobehav. Rev. 24,627 -638.[CrossRef][Medline]
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