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First published online June 11, 2007
Journal of Experimental Biology 210, 2121-2127 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.003236
Reproductive success in two species of desert fleas: density dependence and host effect
1 Desert Animal Adaptations and Husbandry, Wyler Department of Dryland
Agriculture, Ben-Gurion University of the Negev, Sede Boqer Campus, 84490
Midreshet Ben-Gurion, Israel
2 Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for
Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, 84490
Midreshet Ben-Gurion, Israel
3 Ramon Science Center, PO Box 194, 80600 Mizpe Ramon, Israel
* Author for correspondence (e-mail: krasnov{at}bgu.ac.il)
Accepted 4 April 2007
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Summary |
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Key words: egg production, density dependence, flea, rodent
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Introduction |
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). One of the mechanisms to achieve this is to select those
habitats (or hosts, in the case of parasites) that provide the greatest
reproductive reward. A habitat can be considered as `the best' in terms of
reproductive reward if it presents an exploiter with greater amount of
resources and/or greater ease of extraction in comparison with other habitats
(Rosenzweig, 1981;
Rosenzweig, 1991). This
statement conforms to the concept of ideal free distribution (IFD)
(Fretwell and Lucas, 1970),
predicting that animals competing for resources distribute themselves among
habitat patches in such a way that resource use per individual would be equal
across patches. In other words, animals are (a) ideal in assessing patch
quality and (b) free to enter a habitat and use the resources.
The IFD model of host choice by blood-sucking insects was developed by
Kelly and Thompson (Kelly and Thompson,
2000) who suggested that an individual blood-sucking insect should
choose a host with a high intrinsic quality, a low defensiveness and a small
number of competitors. Suitability of a host is thus assumed to be density
dependent with the negative effect of density of parasites on suitability. In
other words, this model suggests negative fitness–density relationships
given that fitness of a haematophagous parasite is directly related to its
feeding success.
However, studies of the relationship between density of haematophagous
insects on a host and their reproductive success produced contradictory
results. In some studies, negative fitness–density relationships were
demonstrated, although evidence for this was sometimes indirect. For example,
Gurtler et al. (Gurtler et al.,
1997) reported that the proportion of kissing bugs, Triatoma
infestans, feeding on humans as opposed to chickens and dogs decreased
with an increase of the density of bugs on the host. Reproductive success of a
flea, Ceratophyllus gallinae, breeding in the nest of the blue tit,
Parus caeruleus, was affected by the number of founder fleas in this
nest, although the number of eggs laid per female flea did not decrease with
an increase in flea density (Tripet and
Richner, 1999). Vashchonok
(Vashchonok, 1995) studied egg
production of Leptopsylla segnis in relation to the number of fleas
simultaneously feeding on a host (laboratory mouse). In these experiments, he
allowed fleas to stay on a restricted host (prevented from grooming) for at
least 4 days and counted the number of eggs produced per female per day. Egg
production decreased slightly but significantly with an increase in flea
density from 2–5 to 15–20. However, further increases in density
did not result in further decreases in fecundity. By contrast, under very high
densities, egg production tended to increase.
One of the reasons for the contradictory responses may be the effect of
host species, i.e. density dependence of reproductive success may be
manifested differently on different host species. This is because the negative
fitness-density relationship stems from intraspecific competition which, in
case of imagoes of ectoparasitic insects, seems to be interfering rather than
exploitative. Indeed, it does not seem feasible that the blood supply of a
host can be a limiting factor (Khokhlova
et al., 2002), whereas interference can arise because of
competition for those areas of a host body where blood is most readily
available, or may be mediated via the host. For example, if there is
a threshold of host sensitivity to parasite attacks, then its defence systems
(behavioural or immune) may be activated once exploiters attain certain
abundance (Mooring, 1995;
Shudo and Iwasa, 2001). Both
these factors can vary among host species (e.g.
Khokhlova et al., 2004a). In
addition, host body size also can play a role. For example, for the same
number of parasites the degree of crowding will be different in small-bodied
and large-bodied hosts and, consequently, the effect of density can be
manifested in a small host but not in a large host.
In this study, we examined egg production of two flea species
(Xenopsylla conformis Wagner and Xenopsylla ramesis
Rothschild) when exploiting two rodent species (Gerbillus dasyurus
Wagner and Meriones crassus Sundevall). Fleas (Siphonaptera) are
obligate haematophagous ectoparasites that occur both on the body of their
host and in its burrow. In most cases, pre-imaginal development is entirely
off-host and the larvae are not parasitic, feeding on organic debris found in
the burrow of the host. X. conformis and X. ramesis are
common flea species, and G. dasyurus and M. crassus are
common rodent species in the Negev desert
(Krasnov et al., 1996;
Krasnov et al., 1997).
We hypothesized that the reproductive success of fleas is (a) density
dependent, but (b) manifestation of density dependence varies among host
species. We predicted that fleas require less blood meals for successful egg
maturation and oviposition and produce more eggs at low than at high
densities. Average body mass of an adult M. crassus is about 80 g,
whereas that of an adult G. dasyurus is about 22 g. In addition,
M. crassus possesses `pre-invasive' immune responses against fleas
and maintains a certain degree of immunological `readiness'
(Khokhlova et al., 2004b),
whereas G. dasyurus mounts the immune response against fleas only
after being attacked (Khokhlova et al.,
2004a). Consequently, we predict that negative relationship
between reproductive parameters and density will be manifested in G.
dasyurus more so than in M. crassus.
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Materials and methods |
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;
Krasnov et al., 2002a). In
brief, an individual rodent was maintained in a plastic cage
(60x50x40 cm) with a steel nest box. A pan containing a mixture of
sand and dried bovine blood (larvae nutrient medium) was placed under the wire
mesh floor of the box. The gravid females deposited eggs in the substrate and
bedding material in the nest box. Every 2 weeks, we collected all substrate
and bedding material from the nest box and transferred it to an incubator
(FOC225E, Velp Scientifica srl, Milano, Italy), where flea developed at
25°C air temperature and 75% relative humidity (RH). The newly emerged
fleas were collected daily and placed on clean animals. Colonies of fleas were
maintained at 25°C and 75% relative humidity with a photoperiod of 12 h:12
h light:dark.
Rodents
We used immune-naïve, adult male M. crassus and G.
dasyurus from our laboratory colonies. The rodents were maintained in
plastic cages (60x50x40 cm) with dried grass as bedding material,
at 25°C with a photoperiod of 12 h:12 h light:dark. They were offered
millet seed and alfalfa (Medicago sp.) leaves ad libitum. No
water was available as the alfalfa supplied enough for their needs. Each
individual was used once in an experiment. In total, we used 40 individuals of
each rodent species.
Experimental design
We used 900 female and 500 male fleas of each species and assigned them
randomly to eight experimental treatments that differed in host species
(G. dasyurus or M. crassus) and number of simultaneously
feeding fleas [10 (5 females and 5 males), 15 (10 females and 5 males), 38 (25
females and 13 males) and 75 (50 females and 25 males)]. Each treatment was
replicated five times.
Experimental procedures
After emergence and prior to experiments, the fleas were placed in an
incubator and maintained at 25°C and 75% RH. Fleas (24- to 48-h old) used
in experiments did not feed from emergence until treatments. Rodents were
placed in wire mesh (5x5 mm) tubes (10 cm length and 3 cm diameter for
G. dasyurus and 15 cm length and 5 cm diameter for M.
crassus) that limited movement and did not allow self-grooming. Tubes
with rodents were placed into individual white plastic tubs and X.
conformis or X. ramesis were placed on each rodent for 2 h. We
then collected the fleas by brushing the hair of the rodent with a tooth-brush
until all fleas were recovered. Both X. conformis and X.
ramesis readily jumped off the host into the tub with the start of the
brushing procedure. Then, they were collected from the tub. Time from the
start of brushing until all fleas appeared in the tub ranged from 2 to 4 min
and did not depend on the number of fleas on a rodent. Therefore, time of
uninterrupted staying on a host was similar for fleas from both low and high
density treatments. Our previous experiments demonstrated that 2 h of feeding
per day is enough for egg maturation and oviposition
(Krasnov et al., 2004).
After feeding, fleas from each host were placed in plastic cups (200
cm2) the bottom of which was covered by a thin layer of sand and
small pieces of filter paper. The cups were transferred into an incubator and
maintained at 25°C air temperature and 92–95% RH. The second and
following feedings of fleas were conducted daily using the procedure described
above. Each feeding of a flea was done on a different host of the same
species. After each feeding, fleas of the respective treatment were randomly
distributed among plastic cups. Female fleas were fed once a day during the 7
days after first oviposition (per group). Pieces of filter paper from each cup
were examined thoroughly under light microscope, eggs were counted, and the
day of oviposition (from the first feeding) was recorded. The purpose for the
maintenance of fleas in groups during experiments was to ensure that they
remained in either low or high density conditions during their stay both on
and off host. It is known that solitary- and group-maintained fleas
demonstrate behavioural differences, for example in activity
(Cox et al., 1999).
Air temperature was regulated in refrigerated incubators (see above) and
humidity using saturated salt solutions
(Winston and Bates, 1960).
Temperature and humidity were monitored using Fisherbrand Traceable
Humidity/Temperature Pen with Memory (Fisher Scientific International, NJ,
USA).
The experimental protocol met the requirements of the 1994 Law for the
Prevention of Cruelty to Animals (Experiments on Animals) of the State of
Israel and was approved by the Ben-Gurion University Committee for the Ethical
Care and Use of Animals in Experiments (License IL-27-9-2003). Details on
maintenance of fleas and rodents were published elsewhere
(Krasnov et al., 2002a;
Krasnov et al., 2003a;
Krasnov et al., 2004).
Data analysis
Reproductive success was evaluated as (a) the number of blood meals until
first oviposition and (b) the number of eggs produced by a female.
Between-replicate, within-treatment variability in the number of blood meals
until first oviposition decreased with an increase in density (coefficients of
variation in this parameter were 0.17 and 0.31 at densities of 10–15
fleas and 0.00–0.12 at densities of 38–75 fleas). These variables,
except for proportions, were log-transformed and then analyzed using three-way
ANOVAs with flea and host species and flea density as independent variables.
Planned comparisons were further analyzed using univariate tests.
Non-transformed data are presented in figures. We avoided an inflated Type I
error by performing Bonferroni adjustments of alpha which resulted in an alpha
level of 0.025.
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In X. conformis, the effect of host species on the number of blood meals prior to oviposition was found at low densities (less blood meals on G. dasyurus) but not at high densities (F1,64=10.1, P<0.001; Fig. 1). Prior to the first oviposition, X. ramesis took more blood meals from M. crassus at low densities, but more blood meals from G. dasyurus at high densities (F1,64=13.2, P<0.001; Fig. 1). When feeding on G. dasyurus, females of both species required similar number of blood meals to commence oviposition, independent of density (F1,64=1.1, P>0.3; Fig. 1). There was, however, a trend of female X. conformis to consume less blood meals prior to oviposition at higher (38 or 75 fleas) than at lower (10 or 15 fleas) densities, although this effect disappeared after Bonferroni adjustment (F1,64=3.7, P>0.05; Fig. 1). By contrast, fleas feeding on M. crassus at higher densities needed less blood meals than at lower densities (F1,64=30.9 for X. ramesis and F1,64=49.7 for X. conformis, P<0.001 for both; Fig. 1).
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In general, X. ramesis produced more eggs than X. conformis (F1,64=7.1–14.4, P<0.001; Fig. 2). Although, the effect of host species was weak, there was a difference in response of fleas to different hosts in egg production (Fig. 2). Specifically, X. conformis feeding on G. dasyurus produced similar number of eggs at all density (F1,64=1.0, P>0.3), however, when feeding on M. crassus, produced significantly less eggs at the highest density (F1,64=15.4, P<0.001; Fig. 2). The number of eggs produced by X. ramesis was significantly lower at higher than at lower densities when feeding on either host species (F1,64=17.9 for G. dasyurus and F1,64=6.2 for M. crassus, P<0.01 for both; Fig. 2).
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Latency of oviposition and density
Number of blood meals taken by a flea prior to oviposition either decreased
with an increase in density (on M. crassus) or was density
independent (on G. dasyurus). These results appear to contradict
earlier observations that the amount of blood consumed by haematophagous
dipterans is closely related to its fecundity (e.g.
Takken et al., 1998). However,
it is possible that the number of blood meals necessary for egg maturation is
an indirect indicator of the relationship between feeding and reproductive
performance. A greater volume of blood taken per meal
(Krasnov et al., 2003a) and
higher efficiency of blood digestion
(Sarfati et al., 2005) can
compensate for a smaller number of blood meals. The latter depends mainly on
host blood biochemistry (Harrington et al.,
2001), whereas the former can depend on flea density either
directly or via the pattern of host immune response. The
density-dependence explanation is more feasible in our study because fleas
produced fewer eggs at higher densities (see below) and because the rodents
used in our experiments had not been exposed previously to flea parasitism.
However, the immune-response explanation cannot be ruled out completely
because (a) some degree of immunological readiness against fleas in
immune-naïve individuals can result from maternal transfer of immunity,
which occurs in M. crassus
(Khokhlova et al., 2004b) and
(b) the `post-invasive' immune response against flea parasitism can be quick,
and is known to occur in G. dasyurus
(Khokhlova et al., 2004a).
Indeed, if a high number of attackers suppress host immune responses, then the
blood intake per flea may increase and, thus, fewer feedings are needed
(Randolph, 1994). This can be
achieved either by the accumulative effect of anticlotting, antiplatelet and
vasodilatory substances contained in saliva of haematophages (for a review,
see Wikel, 1996) or by the
high cost of immune responses against large number of attackers
(Sheldon and Verhulst, 1996;
Lochmiller and Deerenberg,
2000; Schmid-Hempel and Ebert,
2003; Krasnov et al.,
2005).
Another explanation, not necessarily alternative, can be that fleas at low
densities have lower opportunities for mating
(Tripet and Richner, 1999)
and/or selection for a high quality mate
(Crowley et al., 1991),
resulting in a delay of oviposition. Furthermore, successful oviposition in
some flea species requires multiple matings
(Suter, 1964;
Humphries, 1967;
Iqbal and Humphries, 1976;
Tchumakova et al., 1978;
Hsu and Wu, 2000) which can be
achieved more easily at higher densities. The relationship between density and
mating opportunity can also explain why the number of blood meals prior to
oviposition was higher when fleas fed on M. crassus than on G.
dasyurus. This finding appears to contradict our previous findings on
X. ramesis (Krasnov et al.,
2004). However, in the present study this difference was
manifested at lower rather than at higher densities. M. crassus is
about four times larger than G. dasyurus and consequently, given that
the number of fleas on each host was the same, fleas on M. crassus
are at a lower density than those on G. dasyurus. Therefore, the
association between density, mating opportunity and the number of blood meals
prior to oviposition can be applied here and explain why at low densities
fleas fed on M. crassus started to oviposit later.
Reproductive performance and density
At higher densities, flea egg production decreased (except for X.
conformis on G. dasyurus) despite smaller number of blood meals
taken prior to oviposition. This provides strong support for the negative
fitness-density relationship in fleas.
Density dependence of flea egg production in this study might be an outcome
of intraspecific competition for a limited resource
(Izraylevich and Gerson,
1995). Although the depletion of host's blood is unlikely for a
haematophagous ectoparasite (Tripet and
Richner, 1999; Khokhlova et
al., 2002), the decreased egg production at higher densities could
be due to competition for other limiting resources. For instance, fleas may
compete for those areas of a host's body where blood is most readily available
(e.g. thinnest skin or closest position of capillary to body surface) or, in
case of grooming hosts, for those areas that are least subject to
self-grooming. Indeed, Linsdale and Tevis
(Linsdale and Tevis, 1951) and
Linsdale and Davis (Linsdale and Davis,
1956) reported that the fleas Orchopeas sexdentatus and
Anomiopsyllus falsicalifornicus on the dusky-footed wood rat
Neotoma fuscipes favoured a relatively small special `flea spot' in
the middle of the chin. Hsu et al. (Hsu et
al., 2002) found that the cat flea Ctenocephalides felis
concentrated on specific areas on the body (head and neck).
An important finding of negative density–fitness relationship in
fleas is that assumptions of the ideal free distribution (IFD) theory hold for
these insects and, thus, can be applied to explain distribution of fleas
within and between host species. For example, the application of the IFD model
to flea distribution over host populations explains the aggregation of a
parasite population across a host population
(Sutherland, 1983;
Sutherland, 1996;
Kelly and Thompson, 2000). In
our previous study, we applied the IFD-based isodar theory
(Morris, 1988) to infer
mechanisms of host selection by five flea species, each infesting two species
of desert rodents (Krasnov et al.,
2003b). Results of this application suggested that ectoparasitic
insects, like other animals, behaved as if they were able to make choices and
decisions that favoured environments in which their reproductive benefit was
maximized. Experimental testing of the fitness-related consequences of host
selection by two of these five species conformed well to mechanisms revealed
by application of the IFD-based theory
(Krasnov et al., 2004).
Effect of host species
The effect of host species on the number of blood meals necessary for
oviposition and on the number of eggs produced has been studies in fleas
(Hudson and Prince, 1958;
Seal and Bhattacharji, 1961;
Haas, 1965;
Samarina et al., 1968;
Prasad, 1969;
Krasnov et al., 2002b;
Krasnov et al., 2004). For
example, the rat fleas Xenopsylla cheopis and Xenopsylla
astia failed to reproduce when they fed on humans
(Seal and Bhattacharji, 1961)
and fecundity and egg hatchability in X. cheopis were higher when the
fleas fed on Rattus rattus than on Bandicota bengalensis
(Prasad, 1969). Parapulex
chephrenis produced more eggs when they fed on Acomys cahirinus
than on G. dasyurus, whereas the opposite was true for Xenopsylla
dipodilli (Krasnov et al.,
2002b).
Krasnov et al. (Krasnov et al.,
2004) found that X. conformis produced more eggs when
exploiting M. crassus than G. dasyurus, whereas egg
production in X. ramesis did not differ between host species. This
may explain why results of the present study showed between-host difference in
the response of reproductive success to flea density. A density-dependent
response was found in X. ramesis feeding on both hosts and in X.
conformis feeding on M. crassus, but not on G.
dasyurus. Egg production of X. conformis feeding on G.
dasyurus was generally extremely low, even at low flea densities (see
also Krasnov et al., 2004).
Consequently, the density dependence of egg production on this host possibly
was not detectable.
Results from this study conform well to the difference between natural
populations of X. conformis and X. ramesis in the strategy
of choosing between M. crassus and G. dasyurus
(Krasnov et al., 2003b). At
low densities, X. conformis demonstrated sharp selectivity and
parasitized M. crassus, and only with an increase in flea population
size was G. dasyurus also parasitized. By contrast, X.
ramesis parasitized both hosts equally at low densities and were able to
achieve similar maximum fitness under such conditions. However, with an
increase of flea population, parasite pressure on M. crassus
increased at a faster rate than that on G. dasyurus, and so at high
densities, the fleas showed a preference for M. crassus. Our results
also support the notion that the effect of density on reproductive success of
a forager is greater in those habitats where foraging is less efficient
(Morris, 1987a;
Morris, 1987b;
Morris, 1988).
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Cox, R., Stewart, P. D. and Macdonald, D. W. (1999). The ectoparasites of the European badger, Meles meles, and the behavior of the host-specific flea, Paraceras melis.J. Insect Behav. 12,245 -265.[CrossRef]
Crowley, P. H., Travers, S. E., Linton, M. C., Cohn, S. L., Sih, A. and Sargent, R. C. (1991). Mate density, predation risk, and the seasonal sequence of mate choices: a dynamic game. Am. Nat. 137,567 -596.[CrossRef]
Fretwell, S. D. and Lucas, H. L., Jr (1970). On territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheor. 19, 16-36.[CrossRef]
Gurtler, R. E., Cohen, J. E., Cecere, M. C. and Chuit, R. (1997). Shifting host choices of the vector of Chagas disease, Triatoma infestans, in relation to the availability of hosts in houses in north-west Argentina. J. Appl. Ecol. 34,699 -715.[CrossRef]
Haas, G. E. (1965). Comparative suitability of the four murine rodents of Hawaii as hosts for Xenopsylla vexabilis and X. cheopis (Siphonaptera). J. Med. Entomol. 2,75 -83.
Harrington, L. C., Edman, J. D. and Scott, T. W. (2001). Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J. Med. Entomol. 38,411 -422.[Medline]
Hsu, M.-H. and Wu, W.-J. (2000). Effects of multiple mating on female reproductive output in the cat flea (Siphonaptera: Pulicidae). J. Med. Entomol. 37,828 -834.[Medline]
Hsu, M.-H., Hsu, T.-C. and Wu, W.-J. (2002). Distribution of cat fleas (Siphonaptera: Pulicidae) on the cat. J. Med. Entomol. 39,685 -688.[Medline]
Hudson, B. W. and Prince, F. M. (1958). Culture methods for fleas Pulex irritans (L.) and Pulex simulans Baker. Bull. World Health Organ. 19,1129 -1133.
Humphries, D. A. (1967). The mating behaviour of the hen flea Ceratophyllus gallinae (Schrank) (Siphonaptera: Insecta). Anim. Behav. 15, 82-90.[CrossRef][Medline]
Iqbal, Q. J. and Humphries, D. A. (1976). Remating in the rat fea Nosopsyllus fasciatus (Bosc.). Pak. J. Zool. 8,39 -41.
Izraylevich, S. and Gerson, U. (1995). Sex ratio of Hemisarcoptes coccophagus, a mite parasitic on insects: density-dependent processes. Oikos 74,439 -446.[CrossRef]
Kelly, D. W. and Thompson, C. E. (2000). Epidemiology and optimal foraging: modeling the ideal free distribution of insect vectors. Parasitology 120,319 -327.
Khokhlova, I. S., Krasnov, B. R., Kam, M., Burdelova, N. V. and Degen, A. A. (2002). Energy cost of ectoparasitism: the flea Xenopsylla ramesis on the desert gerbil Gerbillus dasyurus.J. Zool. 258,349 -354.[CrossRef]
Khokhlova, I. S., Spinu, M., Krasnov, B. R. and Degen, A. A. (2004a). Immune responses to fleas in two rodent species differing in natural prevalence of infestation and diversity of flea assemblages. Parasitol. Res. 94,304 -311.[CrossRef][Medline]
Khokhlova, I. S., Spinu, M., Krasnov, B. R. and Degen, A. A.
(2004b). Immune response to fleas in a wild desert rodent: effect
of parasite species, parasite burden, sex of host and host parasitological
experience. J. Exp. Biol.
207,2725
-2733.
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S. and Ivanitskaya, E. Y. (1996). Spatial structure of rodent community in the Ramon erosion cirque, Negev highlands (Israel). J. Arid Environ. 32,319 -327.[CrossRef]
Krasnov, B. R., Shenbrot, G. I., Medvedev, S. G., Vatschenok, V. S. and Khokhlova, I. S. (1997). Host-habitat relation as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114,159 -173.
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2001). The effect of temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). J. Med. Entomol. 38,629 -637.[Medline]
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2002a). Time to survival under starvation in two flea species (Siphonaptera: Pulicidae) at different air temperatures and relative humidities. J. Vector Ecol. 27, 70-81.[Medline]
Krasnov, B. R., Khokhlova, I. S., Oguzoglu, I. and Burdelova, N. V. (2002b). Host discrimination by two desert fleas using an odour cue. Anim. Behav. 64, 33-40.[CrossRef]
Krasnov, B. R., Sarfati, M., Arakelyan, M. S., Khokhlova, I. S., Burdelova, N. V. and Degen, A. A. (2003a). Host-specificity and foraging efficiency in blood-sucking parasite: feeding patterns of a flea Parapulex chephrenis on two species of desert rodents. Parasitol. Res. 90,393 -399.[CrossRef][Medline]
Krasnov, B. R., Khokhlova, I. S. and Shenbrot, G. I. (2003b). Density-dependent host selection in ectoparasites: an application of isodar theory to fleas parasitizing rodents. Oecologia 134,365 -373.[Medline]
Krasnov, B. R., Khokhlova, I. S., Burdelova, N. V., Mirzoyan, N. S. and Degen, A. A. (2004). Fitness consequences of density-dependent host selection in ectoparasites: testing reproductive patterns predicted by isodar theory in fleas parasitizing rodents. J. Anim. Ecol. 73,815 -820.[CrossRef]
Krasnov, B. R., Khokhlova, I. S., Arakelyan, M. S. and Degen, A. A. (2005). Is a starving host tastier? Reproduction in fleas parasitizing food limited rodents. Funct. Ecol. 19,625 -631.[CrossRef]
Linsdale, J. M. and Davis, B. S. (1956). Taxonomic appraisal and occurrence of fleas at the Hastings Reservation in Central California. Univ. Calif. Publ. Zool. 54,293 -370.
Linsdale, J. M. and Tevis, L. P. (1951). The Dusky-Footed Wood Rat. Berkeley: University of California Press.
Lochmiller, R. L. and Deerenberg, C. (2000). Trade-offs in the evolutionary immunology: just what is the cost of immunity. Oikos 88,87 -98.[CrossRef]
Lomnicki, A. (1988). Population Ecology of Individuals. Princeton: Princeton University Press.
Mooring, M. S. (1995). The effect of tick challenge on grooming rate by impala. Anim. Behav. 50,377 -392.[CrossRef]
Morris, D. W. (1987a). Ecological scale and habitat use. Ecology 68,362 -369.[CrossRef]
Morris, D. W. (1987b). Spatial scale and the cost of density-dependent habitat selection. Evol. Ecol. 1,379 -388.[CrossRef]
Morris, D. W. (1988). Habitat-dependent population regulation and community structure. Evol. Ecol. 2,253 -269.[CrossRef]
Prasad, R. S. (1969). Influence of host on fecundity of the Indian rat flea, Xenopsylla cheopis (Roths.). J. Med. Entomol. 6,443 -447.[Medline]
Randolph, S. E. (1994). Density-dependent acquired resistance to ticks in natural hosts, independent of concurrent infection with Babesia microti. Parasitology 108,413 -419.
Rosenzweig, M. L. (1981). A theory of habitat selection. Ecology 62,327 -335.[CrossRef]
Rosenzweig, M. L. (1991). Habitat selection and population interactions: the search of mechanism. Am. Nat. 137,5 -28.[CrossRef]
Samarina, G. P., Alekseyev, A. N. and Shiranovich, P. I. (1968). The study of fertility of the rat fleas (Xenopsylla cheopis Rothsch. and Ceratophyllus fasciatus Bosc.) under their feeding on different animals. Zool. Zh. 47, 261-268 [in Russian].
Sarfati, M., Krasnov, B. R., Ghazaryan, L., Khokhlova, I. S.,
Fielden, L. J. and Degen, A. A. (2005). Energy costs of blood
digestion in a host-specific haematophagous parasite. J. Exp.
Biol. 208,2489
-2496.
Schmid-Hempel, P. and Ebert, D. (2003). On the evolutionary ecology of specific immune defence. Trends Ecol. Evol. 18,27 -32.[CrossRef]
Seal, S. C. and Bhattacharji, L. M. (1961). Epidemiological studies of plague in Calcutta, Part 1. Bionomics of two species of rat fleas and distribution, densities and resistance of rodents in relation to the epidemiology of plague in Calcutta. Indian J. Med. Res. 49,974 -1007.[Medline]
Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade offs in evolutionary ecology. Trends Ecol. Evol. 11,317 -321.[CrossRef]
Shudo, E. and Iwasa, Y. (2001). Inducible defense against pathogens and parasites: optimal choice among multiple options. J. Theor. Biol. 209,233 -247.[CrossRef][Medline]
Suter, P. R. (1964). Biologie von Echidnophaga gallinacea (Westw.) und Vergleich mit andern Verhaltenstypen bei Flöhen. Acta Trop. 21,193 -238.
Sutherland, W. J. (1983). Aggregation and the "ideal free" distribution. J. Anim. Ecol. 52,821 -828.[CrossRef]
Sutherland, W. J. (1996). From Individual Behaviour to Population Ecology. Oxford: Oxford University Press.
Takken, W., Klowden, M. J. and Chambers, G. M. (1998). Effect of body size on host seeking and blood meal utilization in Anopheles gambie sensu stricto (Diptera: Culicidae). J. Med. Entomol. 35,639 -645.[Medline]
Tchumakova, I. V., Tovkanev, F. I. and Kozlov, M. P. (1978). Dependence of the reproduction capacity of fleas (Aphaniptera) on the recurrence of mating. Parazitologiya 12,292 -296 [in Russian].[Medline]
Tripet, F. and Richner, H. (1999). Density-dependent processes in the population dynamics of a bird ectoparasite Ceratophyllus gallinae. Ecology 80,1267 -1277.
Vashchonok, V. S. (1995). The dependence of the egg-laying activity in the fleas Leptopsylla segnis (Siphonaptera: Leptopsyllidae) upon their abundance on the host. Parazitologiya 29,267 -271.[Medline]
Wikel, S. K. (ed.) (1996). The Immunology of Host-Ectoparasitic Arthropod Relationships. Wallingford: CAB International.
Winston, P. W. and Bates, D. H. (1960). Saturated solutions for the control of humidity in biological research. Ecology 41,232 -237.[CrossRef]
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