Ecology, 83(1), 2002, pp.

164–175
q 2002 by the Ecological Society of America

THE EFFECT OF HOST DENSITY ON ECTOPARASITE DISTRIBUTION:

AN EXAMPLE OF A RODENT PARASITIZED BY FLEAS
BORIS KRASNOV,1,3 IRINA KHOKHLOVA,2 AND GEORGY SHENBROT1
1Ramon Science Center, Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev,
P.O. Box 194, Mizpe Ramon, Israel
2Wyler Department of Desert Agriculture, Jacob Blaustein Institute for Desert Research,

Ben-Gurion University of the Negev, Beer Sheva, Israel

Abstract. The pattern of parasitism of the flea species Xenopsylla dipodilli and Nos-
opsyllus iranus theodori on the desert rodent species Gerbillus dasyurus was studied to
test the hypothesis that the relationships between flea abundance and host density conform
to pre-existing models of R. M. Anderson and R. M. May, with the correction that the
density of those host individuals that possess permanent burrows (residents) is substituted
for the overall host density. It was predicted that: (1) the intensity of flea infestation would
increase in curvilinear fashion with increase of host density to a plateau that would be
attained at a lower level of host density than would be expected from the basic model, and
(2) the prevalence of flea infestation plotted against host density would be hump-shaped.
The results indicated that intensity of flea infestation increased in either curvilinear fashion
to an asymptote (for X. dipodilli) or linearly (for N. i. theodori) with increase of host
density. As host density increased, the prevalence of infestation changed either unimodally
(X. dipodilli) or logarithmically (N. i. theodori). In addition, there was a positive relationship
between the mean number of fleas per host and the percentage of hosts infested. Both basic
and corrected models describing the relationships between flea burden and host density fit
the observational data well. However, simulations of the fraction of resident hosts dem-
onstrated that this parameter influences the relationship between host density and flea burden
only when residents comprise #50% of all host individuals.
Key words: ectoparasite; flea burden; Gerbillus dasyurus; host density; Nosopsyllus iranus theo-
dori; parasitism; rodent; Xenopsylla dipodilli.

INTRODUCTION the mean number of parasites per infested host (parasite

Unlike most free-living species, the geographic
range of parasites consists of a set of more or less
uniform inhabited ‘‘islands’’ or patches, represented by
their host organisms, and the environment between
these patches is absolutely unfavorable. The distribu-
tion of a parasite population across a host population
is characterized by their aggregation, or overdispersion.
Most individuals of the overdispersed parasite occur
on a few host individuals, while most host individuals
have a only a few parasites or none at all (Anderson
and May 1978, Poulin 1993). This particular distri-
bution of parasite individuals among hosts has impor-
tant consequences for different aspects of the evolu-
tionary ecology of parasites. For example, overdisper-
sion can explain the density dependence of the intensity
of intraspecific competition (Shostak and Scott 1993)
and the biased sex ratio (Morand et al. 1993) in par-
asites.
The basic models of Anderson and May (Anderson
and May 1978, May and Anderson 1978), implying the
overdispersed distribution of parasites, predicted that
Manuscript received 17 April 2000; revised 20 December
2000; accepted 17 January 2001.
3 Present address: Ramon Science Center, P.O. Box 194,
Mizpe Ramon 80600 Israel. E-mail: krasnov@bgumail.bgu.ac.il
164
burden or intensity of infestation) would increase in a
curvilinear fashion to a plateau with increasing host
density (Dobson 1990). This is due to the increased
probability that a parasite transmission stage would
meet a host. However, only a few empirical studies of
this prediction have been conducted (Haukisalmi and
Hentonnen 1990, Arneberg et al. 1998). Another com-
ponent of parasite abundance, namely, prevalence of
infestation (percentage of infested hosts), was not con-
sidered in the framework of the model of Anderson and
May (1978). Nevertheless, the prevalence of infestation
could be expected to increase with increasing host den-
sity. The argument for this can be the same as that for
the intensity of infestation, namely, that under high host
density there is an increased probability that the par-
asite transmission stage will be transmitted. Another
explanation follows metapopulation theory: parasites
infesting different host individuals are analogous to
free-living organisms inhabiting discrete patches, and
the percentage of occupation of the latter increases with
the decrease of patch isolation (Thomas and Hanski
1997). This correlation between host density and prev-
alence of infestation has been supported by empirical
studies (Arneberg et al. 1998).
Most studies related to parasite evolutionary ecology
and host–parasite relationships were made on endo-
January 2002 HOST DENSITY AND ECTOPARASITE DISTRIBUTION
PLATE 1. Wagner’s gerbil (Gerbillus dasyurus). Photo by G. Shenbrot.
parasites, mainly helminths. A host represents an ul-
timate habitat for an endoparasite, providing it with a
place for living, foraging, and mating. Thus, hosts may
be considered as habitat patches for most endopara-
sites. Unlike endoparasites, ectoparasites are influ-
enced not only by characters of the host, but also by
characters of their off-host environment, because their
contact with the host is usually intermittent. The range
of off-host:on-host ratio of different ectoparasite taxa
is very broad, varying from almost constant occurrence
on the host lice (Anoplura), to sporadically attacking
host ticks (Ixodidae) and sand flies (Phlebotomidae).
Fleas (Siphonaptera) take a median position in this
range, alternating between periods when they occur on
the body of their host and periods when they occur in
its burrow or nest. Fleas are permanent satellites of
higher vertebrates, being most abundant and diverse on
small burrowing mammals. The female flea of some
species oviposits while on the host, but the eggs typ-
ically drop off into the nest or burrow (e.g., Pectin-
octenus pavlovskii, Leptopsylla segnis [Vasiliev 1961,
cited by Vatschenok 1988]). Other species mate and
oviposit both on-host and off-host (e.g., Xenopsylla
cheopis). Nevertheless, in nearly all cases, larval and
pupal development is entirely off-host. The larvae are
not parasitic (except for a single species, Uropsylla
tasmanica [see Vatschenok 1988]) and feed on debris
and materials found in the burrow and/or nest of the
host. The larvae of the third instar spin a cocoon, cam-
ouflaging it by adhering particles of the substrate.
Therefore, the habitat patch of a flea should be con-
sidered not only as a particular host, but rather as a
particular host with a particular burrow or nest in a
particular habitat. This complex host–habitat–parasite
relationship can change the expectations derived from
the basic models.
Indeed, the increase of density in rodent populations,
165
particularly in solitary species, often results in a surplus
of individuals that have no individual home ranges
(Brandt 1992, Gliwicz 1992 and references therein). In
theory, these homeless individuals should not be pu-
tative hosts for fleas, because they do not possess bur-
rows that are necessary for flea reproduction and de-
velopment of pre-imaginal stages. In turn, the density
of resident hosts is determined by the carrying capacity
of the given habitat. For example, this carrying capacity
can be dependent on the number of available burrows
or places for burrowing, all else being equal. If the flea
burden increases in a curvilinear fashion to a plateau
with increasing host density, the breakpoint of this
curve should be determined by the density of resident
hosts rather than by the overall density of the hosts.
Consequently, the flea burden should decrease with the
proportion of resident individuals, under the same over-
all abundance of the host and the same overall abun-
dance of parasites. The plateau of the flea burden curve
should be lower than is expected from the basic model.
If the resident hosts alone support the flea popula-
tion, the prevalence of infestation should increase with
the increase of host density, until the habitat becomes
saturated with residents (e.g., all available burrows oc-
cupied). Under higher host density, the prevalence of
flea infestation should decrease, since the resident ro-
dents would compose an ever-decreasing fraction of
the overall host population. Thus, the prevalence of
flea infestation plotted against host density is expected
to be hump-shaped.
The small gerbilline rodent, Gerbillus dasyurus
(Wagner, 1842) (body mass is 20–24 g), occupies a
variety of habitats in the Negev Highlands, Israel
(Shenbrot et al. 1997; see Plate 1). The density of G.
dasyurus varies across habitats, being highest in loess
hills and lowest on gravel plains (Krasnov et al. 1996).
The fraction of transient (nonresident) individuals
166 BORIS KRASNOV ET AL.
varies both among habitats and between years. This
fraction reaches as high as 50% in high-density years
in loess hills (Gromov et al. 2000) and is even higher
on gravel plains, where the majority of individuals are
transient (Khokhlova et al. 1994). Young individuals
of G. dasyurus have been observed mainly from April
to September, whereas the last pregnant females oc-
curred in October (Shenbrot et al. 1997). This indicates
that the spring and summer parts of breeding period
were successful, while the pups of late autumn repro-
duction tended not to survive. In addition, the dispersal
of young gerbils occurred mainly in late spring and
summer (I. S. Khokhlova and B. R. Krasnov, unpub-
lished data). Two types of burrows of G. dasyurus have
been described (Shenbrot et al. 1997): (1) simple bur-
rows of small depth, without nests, and (2) complex,
deeper, burrows with a spherical nest made from dried
plant material. It appears that resident individuals use
complex burrows, whereas transients have to be sat-
isfied with simple burrows, if any. We recorded fleas
in complex burrows of G. dasyurus, whereas no fleas
were found in simple burrows (B. R. Krasnov and G.
I. Shenbrot, unpublished data). Nevertheless, each bur-
row of either type is occupied by one adult individual
(Shenbrot et al. 1997).
G. dasyurus is parasitized mainly by two flea species,
Xenopsylla dipodilli Smit, 1960, and Nosopsyllus ir-
anus theodori Smit, 1960 (Krasnov et al. 1998, 1999).
X. dipodilli occurs on G. dasyurus throughout the year,
although the abundance of this flea in winter is ex-
tremely low (Krasnov et al. 1997). In contrast with X.
dipodilli, N. i. theodori is a winter flea. No imago has
been found on G. dasyurus between April and Decem-
ber (Krasnov et al. 1997). Thus, these two fleas alter-
nate on G. dasyurus. These flea species occur also on
other rodents in the area (Krasnov et al. 1997, 1999).
However, extremely low abundances and sporadicity
of these fleas on rodents other than G. dasyurus suggest
that this has no any significant effect on the host–par-
asite population dynamics.
We hypothesized that the relationships between flea
abundance and host density conform to the basic mod-
els of Anderson and May (1978), with the following
correction: flea abundance is influenced by the abun-
dance of resident hosts, rather than overall host density.
We predicted that the intensity of flea infestation would
increase with an increase in host density in a curvilinear
fashion to a plateau that would be attained at a lower
level of host density than expected from the basic mod-
el. In addition, we predicted that the prevalence of flea
infestation plotted against host density would be hump-
shaped. To test these predictions, we studied the pattern
of parasitism of the fleas X. dipodilli and N. i. theodori
on G. dasyurus in the Negev desert.
METHODS
Study area
The study was conducted in the Ramon erosion
cirque, Negev Highlands, Israel. The Ramon erosion
Ecology, Vol. 83, No. 1
cirque is an area of about 200 km2 and is situated at
the southern boundary of the Negev Highlands (308359
N, 348459 E). The diverse habitats represented in the
Ramon cirque, range from sandy dunes in the north-
eastern parts of the cirque to sandstone rocks on the
rims. The climate is characterized by hot, dry summers
(mean daily air temperature of July is 348C) and rel-
atively cold winters (mean daily temperature of January
is 12.58C). There is a sharp decrease in annual rainfall
from 100 mm on the north rim to 56 mm in the bottom
of the cirque.
Rodent trapping and flea collection
Rodents were trapped on seven 1-ha plots from sum-
mer 1992 until summer 1993 and on 16 1-ha plots from
summer 1994 until summer 1995. The first seven plots
were sampled every 2–3 mo. Other plots were sampled
every 6 mo. Plots were selected to represent the main
substrate and vegetation gradients. Each plot was sam-
pled during 3–5 consecutive days, using 50 Sherman
live traps (Sherman Traps, Tallahasse, Florida, USA)
placed in a grid at 5 3 5 stations, with two traps per
station and an interval of 20 m between stations. The
overall density of G. dasyurus was evaluated as the
minimal number of individuals known to be alive. An
individual was considered resident if it was captured
either: (1) at least once in each of three consecutive
trapping periods, each 2–3 mo apart (in 1992–1993),
or (2) at least once in each of two consecutive trapping
periods, each 6 mo apart (in 1994–1995). This deter-
mination of resident vs. transient status can produce
some bias toward finding transients. In other words,
we could erroneously attribute the transient status to
resident gerbil (e.g., if it died by some unknown rea-
sons during the study period) but could not erroneously
attribute the resident status to transient gerbil. How-
ever, the individual composition of G. daysurus pop-
ulations has been shown to be very stable (Shenbrot et
al. 1997), suggesting that this potential bias could be
considered negligible.
We collected fleas from each individual rodent only
when it was captured the first time. The animal’s fur
was combed thoroughly, using a toothbrush over a
white plastic bath, and fleas were carefully collected.
Each rodent was sexed, weighed, marked by toe clip-
ping, and released. In total, 657 gerbils were captured,
and 945 X. dipodilli and 320 N. i. theodori were col-
lected.
The models
We used the models presented by Anderson and May
(1978), May and Anderson (1978), Grenfell (1992),
and Arneberg et al. (1998). These models describe the
dynamics of populations of host (H ) and parasite (P).
The main assumptions of the basic models are that: (1)
host population growth is density dependent, given that
there is no parasite-induced reduction of host repro-
duction, (2) hosts are long-lived, relative to their par-
January 2002 HOST DENSITY AND ECTOPARASITE DISTRIBUTION 167

TABLE 1. Description of the parameters of the basic model (adapted from Anderson and May
1978, Dobson 1990, Arneberg et al. 1998).

Parameter Description
a Instantaneous birth rate of host (per host per unit time)
b Instantaneous death rate of host due to causes other than parasite (per
host per unit time)
a Instantaneous host death rate due to parasite influence (per host per unit
time)
b Instantaneous rate of host reproduction reductions due to parasite influ-
ence (per host per unit time)
à Severity of density dependence in host population growth
l Instantaneous birth rate of parasite transmission stages (per parasite per
unit time) (the transmission stage for fleas is the adult imago)
m Instantaneous death rate of parasites due to either natural or host induced
(e.g., autogrooming) causes
H0 Transmission efficiency constant, varying inversely with the proportion of
parasite transmission stages that infest individuals of the host popula-
tion (see Anderson and May [1978] for further explanations)
k Parameter of the negative binomial distribution, varying inversely with
the degree of overdispersion; it measures the degree of aggregation of
the parasites within host population

asites, and (3) the frequency of parasites within hosts and transient host individuals. This transmission can
follows the negative binomial distribution. occur either when individuals visit alien burrows or
The basic model utilizes the following equations: through direct contact between host individuals (Kras-
nov and Knyazeva 1983). Consequently,
dH
5 (a 2 b 2 ÃH )H 2 (a 1 b)P (1)
dt dH
5 (a 2 ÃS)S 2 bH (3)
dt
dP lPH dP lPS (k 1 1)P 2
5 2 (b 1 ÃH 1 a 1 m)P 5 2 (b 1 ÃS 1 m)P 2 m . (4)
dt H0 1 H dt H0 1 H kH
The parasite burden (M ) is the mean number of par-
(k 1 1)P 2 asites per infested host, so the rate of changes in par-
2 (a 1 m) . (2)
kH asite burden is
The parameters of the model are presented in Table 1. dM dP /H
5
The model assumes that a parasite induces mortality dt dt
of a host (Anderson and May 1978, May and Anderson
lMS m(k 1 1) 2
1978). However, Arneberg et al. (1998) argued that the 5 2 (b 1 ÃS 1 m)M 2 M
positive relationship between host density and parasite H0 1 H k
abundance would also be expected when parasites have S S2
no pathogenic effects. Although the negative influence 2a M 1 Ã M 1 bM. (5)
H H
of flea parasitism on the fitness of a rodent host has
been reported for Synosternus cleopatrae on Gerbillus At equilibrium (dH/dt 5 dp/dt 5 dM/dt 5 0),
andersoni allenbyi (Lehmann 1992), no effect of flea
infestation on body conditions or on the survival of G.
dasyurus was found (Krasnov et al. 1997).
Thus, given that fleas neither induce host mortality
M5
[ lS
H0 1 H
S
2m2a 2 12
H
S
H
ÃS 1
k
m(k 1 1)
.2 ][ ]
(6)
nor reduce host reproduction, a 5 b 5 0 is assumed.
Further, we assumed that the dynamics of fleas is in- Eq. 6 was applied for X. dipodilli in spring and summer.
fluenced by the density of those host individuals that N. i. theodori occurs on its host during the period when
are resident and have permanent burrows (S ). This den- host does not reproduce (a 5 0). Consequently, this
sity is limited by the carrying capacity of the habitat, equation for N. i. theodori was transformed as
for example, by the number of available burrows. In
addition, only resident host individuals reproduce. Fur-
thermore, we assume that all host individuals are equal-
M5
[ lS
H0 1 H
2m 121
S
H
ÃS 2
k
m(k 1 1)][
.
] (7)

ly susceptible to parasitism by fleas, and thus, the trans- Hereafter, Eqs. 6 and 7 are referred to as ‘‘corrected’’
mission of fleas from individual to individual, or from models. They are collapsed into the equations of the
burrow to burrow, can be performed by both resident basic model, if S 5 H.
168 BORIS KRASNOV ET AL. Ecology, Vol. 83, No. 1

TABLE 2. Parameters of frequency distribution of X. dipo-
dilli and N. i. theodori on G. dasyurus
Negative
binomial
Flea species N 2
s /X̄ Mo k x2
X. dipodilli 945 7.25 0.53 0.39 29.05
N. i. theodori 320 3.79 0.51 0.51 18.9
Note: See Statistical processing for explanation of param-
eters.
We assigned values of the birth rate of G. dasyurus
(a 5 2) based on our data both from field observations
(on average, two litters per breeding female per repro-
duction period, 1.4:1 male:female ratio, 60% repro-
ductively active adult females; Shenbrot et al. 1997)
and from laboratory breeding (on average, four pups/
litter; I. S. Khokhlova and B. R. Krasnov, unpublished
data). No data are available on birth rate of transmis-
sion stages either of X. dipodilli or N. i. theodori.
Therefore, we used data on congeneric species, namely,
Xenopsylla cheopis (Samarina et al. 1968), Xenopsylla
conformis (Vatschenok 1988; B. R. Krasnov and I. S.
Khokhlova, unpublished data), and Nosopsyllus con-
similis (Alekseev 1961, Vatschenok 1988). We calcu-
lated the birth rate of flea transmission stages based on
the rate of oviposition per female per breeding season,
given that survival of pre-imaginal stages is 80%. Thus,
l was considered to be equal to 100 for X. dipodilli,
and 140 for N. i. theodori. Parameters H0, Ã, and m
were estimated from the model-fitting procedures (see
Statistical processing).
Analysis of the model concentrated on the variation
in flea burden and prevalence of infestation with chang-
es in the fraction of resident host individuals under the
same overall density. We simulated changes in this
fraction from 5% to 100% with a 5% step.
Statistical processing
Whether the negative binomial can be used as a mod-
el for the distribution of X. dipodilli and N. i. theodori
on G. dasyurus was tested using the NEGBINOM com-
puter software (Krebs 1989). The acceptance of the null
hypothesis that the negative binomial distribution fits
the data was performed using a chi-square test. In ad-
dition, three measures of aggregation were calculated:
(1) k of the negative binomial distribution, (2) variance-
to-mean ratio s2/X̄, and (3) standardized Morisita index
Mo (Krebs 1989) using the NEGBINOM program.
We applied least-squares estimation procedures via
the quasi-Newton algorithm for fitting the models of
P the relationships between host density and flea burden.
0.27 In addition, we used regression analysis for the de-
0.45 scription of the relationships between both flea burden
and prevalence of flea infestation, and both overall host
density and density of resident hosts. Samples with G.
dasyurus density ,2 were excluded from the analyses
of prevalence of infestation. Model simulations for X.
dipodilli were analyzed using a nonlinear estimation of
the breakpoint of piecewise linear regression. Those
for N. i. theodori were analyzed using linear regression.
All these calculations were performed with the statis-
tical package STATISTICA (StatSoft, 1995).
RESULTS
Flea distribution among host individuals
Distributions of both flea species on G. dasyurus
were aggregated. The aggregation is indicated by the
values of the standardized Morisita index of dispersion,
the variance-to-mean ratio and k for negative binomial
(Table 2). The negative binomial model successfully
fit the observed frequency distribution of both X. di-
podilli and N. theodori on G. dasyurus in spring–sum-
mer and winter, respectively (Table 2).
The effect of host density on flea burden
The burden of X. dipodilli (Mobs) on G. dasyurus
increased in a curvilinear fashion to a plateau with
increase in host density. This relationship could be de-
scribed significantly by logarithmic fit Mobs 5 0.4 1
0.73logH (F1,34 5 80.45, r2 5 0.69, P , 0.001). Change
in host density was accompanied by a rapid change in
flea burden until the former attained ;20 individuals/
ha. Further increase in host density did not cause
change in flea burden. Both corrected and basic models
described this relationship well (Table 3, Fig. 1), yield-
ing similar values for the parameters H0 and m.
Manipulation of the fraction of host residents while
holding all other parameters constant, produced a num-
ber of curves (Fig. 2). It may be envisaged that the
basic and corrected models differed from one another
when the fraction of residents was $50%. The break-
point of the piecewise linear regressions of flea burden

TABLE 3. Parameters of the corrected and basic model when fitted to the observed burden of
X. dipodilli or N. i. theodori in relation to density of G. dasyurus.

Variance
explained
Flea Model (%) R H0 Ã m
X. dipodilli Basic 71.5 0.84 3.6 6 1.0 9.2 6 0.7
Corrected 69.7 0.81 3.4 6 1.8 24.9 6 2.6 8.7 6 1.2
N. i. theodori Basic 81.5 0.90 17.6 6 1.9 3.7 6 0.8
Corrected 83.0 0.91 19.1 6 1.2 29.6 6 1.8 3.1 6 0.7
Note: The à term is not present in the basic model (because S 5 H).
January 2002 HOST DENSITY AND ECTOPARASITE DISTRIBUTION
FIG. 1. Dependence of X. dipodilli burden on density of
G. dasyurus (observed, triangles and solid line; expected from
corrected model, circles and dashed line; expected from basic
model, diamonds and bold dashed line).
against host density changed logarithmically with a dif-
ferent fraction of residents attaining a plateau when
this fraction achieved 50–60% (F1,18 5 2247.5, r2 5
0.99, P , 0.001; Fig. 3). In addition, the described
simulation demonstrated that the threshold of estab-
lishment (the minimal size of host population necessary
to sustain a parasite population) was higher when there
was a lower (5–30%) fraction of residents in a host
population (F1,18 5 38.2, r2 5 0.69, P , 0.001; Fig.
3). Furthermore, X. dipodilli burden decreased weakly,
albeit significantly, with an increase in the observed
percentage of resident G. dasyurus (F1,34 5 19.8, r2 5
0.35, P , 0.001). In contrast with X. dipodilli, the
burden of N. i. theodori increased linearly with an in-
crease in G. dasyurus density (F1,20 5 85.8, r2 5 0.8,
P , 0.001). As was the case with X. dipodilli, both
corrected and basic models fit this pattern well (Table
3, Fig. 4).
The results of the manipulation of the fraction of
resident hosts while holding all other parameters con-
stant are presented in Fig. 5. Again, the basic and cor-
FIG. 2. Relationships between X. dipodilli burden and G.
dasyurus density produced by manipulation of the fraction of
host residents from 5% to 100%, while holding all other pa-
rameters constant.
169
FIG. 3. Values of the breakpoint of piecewise linear re-
gression (triangles) and the threshold of establishment (cir-
cles), calculated for simulation curves of X. dipodilli burden–
G. dasyurus density in dependence on the simulated per-
centage of resident host individuals.
rected models differed from one another when the frac-
tion of residents exceeded 50%. The higher the resident
fraction, the faster was the rate of change in flea burden,
indicated by the value of the slope of linear regression,
until the fraction of residents attained 50–60% (F1,18
5 73.4, r2 5 0.80, P , 0.001; Fig. 6). As was the case
for X. dipodilli, the threshold of N. i. theodori estab-
lishment was greater with a lower fraction of residents
in a host population (F1,18 5 16.8, r2 5 0.77, P , 0.001;
Fig. 6). The observed flea burden was correlated neg-
atively with the observed percentage of resident gerbils
(F1,20 5 19.7, r2 5 0.49, P , 0.001).
The effect of host density on flea prevalence
Prevalence of infestation by X. dipodilli changed un-
imodally with an increase in overall density of G. das-
yurus. The fraction of infested gerbils peaked at a den-
sity of 20 individuals/ha, whereas it was lower under
both lower and higher gerbil density (Fig. 7). This re-
lationship can be described by the equation PI 5 50.1
FIG. 4. Dependence of N. i. theodori burden on density
of G. dasyurus (observed, triangles and solid line; expected
from corrected model, circles and dashed line; expected from
basic model, diamonds and bold dashed line).
170 BORIS KRASNOV ET AL.
FIG. 5. Relationships between G. dasyurus density and
N. i. theodori burden produced by manipulation of the fraction
of host residents from 5% to 100% while holding all other
parameters constant.
1 3.15H 2 0.1H2, where PI is prevalence of infestation
and H is host density (F2,30 5 26.8, r2 5 0.62, P ,
0.001). Prevalence of X. dipodilli infestation plotted
against density of resident hosts was also hump-shaped,
with a peak of prevalence at 12–13 individuals/ha (Fig.
7). The curve of prevalence against resident density
was steeper than the curve of prevalence against overall
density, and fitted the equation PI 5 36.0 1 8.6S 2
0.36S2, where S is density of resident individuals (F2,30
5 20.9, r2 5 0.58, P , 0.001). Coefficients of these
two regressions differed significantly ( t 5 3.64 and t
5 3.95, P , 0.01). The prevalence of infestation re-
sponded weakly, albeit significantly, to the fraction of
resident individuals in the host population being higher
with a greater percentage of residents (F1,31 5 9.6, r2
5 0.23, P , 0.001).
Prevalence of infestation by N. i. theodori increased
logarithmically with an increase in host density (F1,20
5 16.8, r2 5 0.46, P , 0.001; Fig. 8). The same was
true for the relationship between the prevalence of in-
festation and the density of resident hosts (F1,20 5
FIG. 6. Values of the slope of linear regression (triangles)
and threshold of establishment (circles) calculated for sim-
ulation curves of X. dipodilli burden–G. dasyurus density in
dependence on the simulated percentage of resident host in-
dividuals.
Ecology, Vol. 83, No. 1
FIG. 7. Relationship between the density of G. dasyurus
and prevalence of infestation by X. dipodilli, calculated for
resident gerbils only (triangles and dashed line) and for both
resident and nonresident gerbils (circles and solid line).
25.41, r2 5 0.56, P , 0.001; Fig. 8). Although these
two regressions did not differ significantly ( t 5 0.45
for intercepts and t 5 0.29 for slopes), the density of
resident hosts seemed to be a better predictor of prev-
alence of infestation than overall host density (note
higher r2 values). In contrast with X. dipodilli, no cor-
relation was found between prevalence of infestation
by N. i. theodori and the fraction of resident individuals
in the host population (F1,20 5 0.76, P . 0.3).
Relationships between flea burden and
prevalence of infestation
The burden of X. dipodilli was not correlated with
the prevalence of infestation when the former was cal-
culated as the mean number of fleas per infested gerbil
(F1,30 5 0.1, P . 0.9). However, when this parameter
was substituted with mean number of fleas across all
hosts, the relationship between flea abundance per host
FIG. 8. Relationship between the density of G. dasyurus
and prevalence of infestation by N. i. theodori, calculated for
resident gerbils only (triangles and dashed line) and for both
resident and nonresident gerbils (circles and solid line).
January 2002 HOST DENSITY AND ECTOPARASITE DISTRIBUTION
and prevalence of infestation was significantly positive
(F1,30 5 21.11, r2 5 0.41, P , 0.001). Furthermore, the
prevalence of infestation of resident gerbils increased
significantly with the burden of X. dipodilli calculated
for resident individuals only (F1,30 5 37.27, r2 5 0.55,
P , 0.001). In order to test if these relationships were
sampling artifacts, the sampling model of Hanski et al.
(1993) was applied to our observational data. This
model explained only 32% of the variance in the frac-
tion of uninfested gerbils across sampling sites. This
suggests that the increase of the prevalence of infes-
tation with the increase of flea burden cannot be con-
sidered as sampling artifact.
A positive relationship has been found between the
burden of N. i. theodori and the prevalence of infes-
tation when the burden was calculated both for infested
gerbils and for all gerbils (F1,20 5 18.53, r2 5 0.48, P
, 0.001, and F1,20 5 41.6, r2 5 0.68, P , 0.001 re-
spectively). The intensity of infestation of resident G.
dasyurus was an even better predictor of the prevalence
of infestation (F1,20 5 52.79, r2 5 0.73, P , 0.001).
The sampling model explained only 44% of variance
of the fraction of uninfested gerbils across sampling
sites.
DISCUSSION
The present study of patterns of flea parasitism on
G. dasyurus produced the following answers to ques-
tions we set out to address. The intensity of flea in-
festation increases either in a curvilinear fashion to a
plateau (for X. dipodilli) or linearly (for N. i. theodori)
with an increase in host density. The difference be-
tween overall host density and the density of resident
hosts is important for the determination of parasite bur-
den only if residents comprise ,50% of all hosts. The
percentage of infested hosts changes either unimodally
(X. dipodilli) or logarithmically (N. i. theodori) as host
density increases. There was a positive relationship be-
tween the mean number of fleas per host and the per-
centage of hosts infested. The answers were obtained
from the field data and from the analysis of a flea–
rodent relationship model, incorporating among-host
functional differences that are important for flea re-
production.
We recognize that in the real world, flea population
dynamics will be affected, among other factors, by abi-
otic parameters (ambient temperature, relative humid-
ity, etc.) that may directly influence flea reproduction
and survival (especially during pre-imaginal develop-
ment; B. R. Krasnov and I. S. Khokhlova, unpublished
data). Nevertheless, our omission of the abiotic con-
straints on the flea population dynamics is deliberate,
since our main aim is to provide quantitative insights
into the mechanisms by which hosts regulate parasite
populations. Therefore, we excluded the concept of en-
vironmental mediation of rodent–flea relationships to
simplify the manipulations. Such simplification eluci-
dates predictions of biological concern.
171
Flea burden and host density
Our field data did not allow us to successfully dis-
tinguish between the corrected and basic models of
host–parasite dynamics. However, the manipulation of
the fraction of host residents provided a set of curves
that permitted us to discriminate between these models.
A positive relationship between host density and par-
asite burden was expected from the increase of parasite
transmission rate under higher host densities (Anderson
and May 1978, May and Anderson 1978, Arneberg et
al. 1998). The greater the host density, the greater the
probability that each parasite individual or respective
transmission state (egg, larva, or imago) will contact
a host. Indeed, a positive correlation between parasite
burden and host density has been reported for both
endoparasites (Haukisalmi and Hentonnen 1990) and
ectoparasites (Zhonglai and Yaoxing 1997, 1998), al-
though other studies did not support this prediction
(Sorci et al. 1997).
The plateau attained by the curve of X. dipodilli bur-
den with an increase in host density can be explained
most easily by the limited carrying capacity of host
individuals that can harbor a limited number of para-
sites only. However, this suggests a negative impact of
parasites on hosts (Brown and Brown 1986, Lehmann
1993). No indication of an effect of fleas on gerbil body
conditions and survival was found (Krasnov et al.
1997), and no effect was assumed in the present mod-
els. Thus, the only possible explanation implicating
host carrying capacity can be that this parasite thresh-
old is very narrow, and that gerbil response to flea
number is stepwise rather than gradual. Flea abundance
below some threshold does not influence the health of
the gerbil, whereas flea abundance above the threshold
is lethal. Consequently, the observed number of fleas
on every captured gerbil was below the threshold. Fur-
thermore, the relationship between N. i. theodori and
gerbil density was linearly positive, and there was no
plateau under high gerbil density. In addition, the mean
number of fleas per infested rodent was higher for N.
i. theodori than for X. dipodilli (mean 6 1 SE; 4.8 6
0.3 fleas/rodent vs. 2.7 6 0.1 fleas/rodent). This result
suggests that the explanation of a plateau caused by
host mortality when flea intensity exceeds a specific
threshold is unsatisfactory.
An alternative explanation implies the heterogeneity
of hosts in relation to burrows as habitats for successful
flea breeding, as well as the carrying capacity of host
habitat. Flea populations can be established and main-
tained on those host individuals that own burrows (res-
idents), whereas homeless hosts can take part in flea
transmission but are unable to sustain fleas. As overall
host density increases, the number of residents attains
a particular level determined by the carrying capacity
of host habitat. Further increases in host density result
in an increase in the number of nonresidents, while the
number of residents remains stable. Because nonresi-
172 BORIS KRASNOV ET AL.
dent hosts do not participate in the siphonapteran life
cycle, the overall increase in host density after satu-
ration of a habitat by residents has no effect on the flea
burden. This can also explain the absence of a plateau
in the burden of N. i. theodori with a high density of
gerbils. In contrast to X. dipodilli, N. i. theodori is a
winter flea, reproducing in periods when neither re-
production nor dispersal of G. dasyurus occurs, so most
host individuals in a given habitat are residents
(Khokhlova et al. 1994, Shenbrot et al. 1997). If so,
each habitat in each given period is saturated by res-
idents, whereas transient homeless individuals are ab-
sent. Thus, the flea burden increases linearly with host
density. Indeed, the mean percentage of individuals
considered to be nonresidents was 17.4 6 3.1% non-
resident individuals in spring–summer (when G. das-
yurus was parasitized by X. dipodilli) and 3.1 6 1.1%
nonresident individuals in winter (when G. dasyurus
was parasitized by N. i. theodori).
Finally, it is possible that an increase in flea number
above some threshold either arouses an irritation of a
gerbil’s skin and, consequently, excessive grooming
activity of a gerbil, or induces an immune response of
a gerbil to flea salivary gland-derived molecules (Wikel
1996). Grooming activity of a host has been shown to
be one of the most significant host-induced mortality
factors for ectoparasites (Marshall 1981), and is pos-
itively correlated with the severity of infestation (Hin-
kle et al. 1998). This is why the number of fleas on an
individual host does not exceed some threshold. Fur-
thermore, in contrast to N. i. theodori, X. dipodilli has
no ctenidia that permit the flea to anchor itself within
host fur, enabling it to resist the host’s grooming effort
(Humphries 1967, Traub 1972). This can partly explain
why the mean number of fleas per infested rodent was
higher for N. i. theodori than for X. dipodilli.
Host immune responses can be also important in
modulating ectoparasite numbers. It has been reported
that different taxa of blood-feeding arthropods, includ-
ing fleas, stimulate a variety of host innate and specific
acquired immune responses (Jones 1996, Wikel 1996).
Consequently, host–ectoparasite associations are usu-
ally characterized by development of some level of
acquired resistance, which could potentially limit the
level of infestation. However, it is unknown whether
G. dasyurus is able to develop immune responses to
flea infestation. Also, a higher level of N. i. theodori
infestation in comparison with X. dipodilli infestation
seems to contradict the explanation implying host im-
mune response, given the absence of the plateau in the
former case and the presence of the plateau in the latter
case.
As mentioned previously, both basic and corrected
models describing the relationships between flea bur-
den and host density fitted the observation data well.
However, the simulations of the fraction of residents
demonstrated that this parameter influences the rela-
tionship between host density and flea burden only
Ecology, Vol. 83, No. 1
when residents comprise #50% of all host individuals.
This was true for both flea species. The only possible
role of nonresident hosts in flea dynamics is their effect
on flea transmission, given that they do not support flea
reproduction. It appears that when the percentage of
nonresidents is relatively low, they do not contribute
heavily toward flea transmission, so their influence on
flea dynamics and distribution is negligible (Khokhlova
and Knyazeva 1983). Thus, the introduction of a pa-
rameter for nonresident density into the model does not
produce any significant shift in comparison with the
basic model. However, when the fraction in the host
population is relatively high, their contribution to flea
transmission becomes significant. In such a case, a
model that takes this nonresident component into ac-
count, should describe the observational data better
than that which considers only the overall host density.
The role of resident hosts in flea dynamics is also sup-
ported by the fact that flea burden was correlated neg-
atively with the percentage of resident gerbils, showing
that all flea individuals were distributed almost exclu-
sively among resident hosts and did not occur on non-
residents. In addition, the manipulation of the fraction
of resident hosts demonstrated that the breakpoint of
the flea burden vs. host-density curve is affected by
this fraction, thus conforming to our prediction, at least
in relation to X. dipodilli. The plateaux of the simulated
curves of flea burden were lower with a lower fraction
of resident hosts under the same overall host density.
This also fits well with the hypothesis about the role
of resident hosts in flea distribution.
It is noteworthy that the threshold of establishment
(the minimal size of a host population necessary to
sustain a parasite population) was affected by the frac-
tion of residents in the host population. The lower the
percentage of resident gerbils, the greater the number
of them necessary to maintain flea reproduction. Again,
this is consistent with the assumption that only resi-
dents support flea populations. For example, if it is
surmised that the density of G. dasyurus is 2 individ-
uals/ha, but both of them are residents, then this pro-
duces two burrows for the reproduction of X. dipodilli
with a threshold of establishment equaling two. If this
is modified to assume that the density of G. dasyurus
is 20 individuals/ha, but that only two are residents,
this again produces two burrows for the reproduction
of X. dipodilli, but the threshold of establishment now
equals 20. The same relationship between the fraction
of resident hosts and threshold of establishment was
produced by manipulations of the percentage of resi-
dents for N. i. theodori. However, this pattern can be
considered as a theoretical exercise only, because non-
resident individuals comprise a very small proportion
of overall gerbil population in the period when N. i.
theodori occurs.
Flea prevalence and host density
Theoretically, the relationship between host density
and parasite prevalence is expected to be positive (at-
January 2002 HOST DENSITY AND ECTOPARASITE DISTRIBUTION
taining a plateau under high host density), given that
there are no parasite extinction events across host in-
dividuals. The explanation is that, once host density
becomes high enough for all parasites to find a host, a
further increase in host density would be inconsequen-
tial. However, field data on the relationship between
flea prevalence and host density are contradictory. For
example, the increase and stabilization of flea preva-
lence around 100% with an increase in host density
has been reported for Spermophilus richardsoni para-
sitized by Opisocrostis bruneri and Oropsylla rupestris
(Lindsay and Galloway 1997), whereas prevalence of
Xenopsylla bantorum increased with the decrease in
density of its host, Arvicanthis niloticus (Schwan
1986). Conversely, prevalence cannot be lower than a
specific eradication threshold (sensu Nee et al. 1997),
because a minimum number of hosts is required for the
parasite population to persist, analogous to a minimum
number of patches for free-living animals (Nee 1994,
Kareiva and Wennergren 1995, Hanski et al. 1996).
The prediction about the unimodal response of flea
prevalence to an increase in host density appeared to
be true for X. dipodilli, but not for N. i. theodori. If
only resident host individuals support the flea popu-
lation, the prevalence of infestation increases with an
increase in host density until all resident individuals
are infested and the habitat is saturated with residents
(all available burrows are occupied or individual home
ranges collapsed to minimal possible size). Under high-
er host density, the prevalence of flea infestation de-
creases, because the resident and infested gerbils com-
pose an ever-decreasing fraction of the overall popu-
lation. Conversely, for the above-mentioned reasons,
flea prevalence plotted against resident host density is
expected to increase, reaching a plateau. This was not
the case; the curve of prevalence against resident den-
sity was also hump-shaped, although steeper than the
curve of prevalence against overall density. An expla-
nation for this result might be that flea reproduction
and transmission have lower rates in comparison with
reproduction and dispersal of gerbils. In other words,
the rate of establishment of new patches (previously
vacant or new burrows that are being occupied either
by dispersing young gerbils or by transient adults) is
faster than the rate of their infestation. Consequently,
it is probable that, under high host density, a fraction
of resident hosts remains underused by the fleas, merely
because they cannot keep pace with gerbil reproduction
and dispersal. Indeed, the active breeding period of flea
Xenopsylla hirtipes has been reported to fall behind
active breeding and dispersal of its main host, Rhom-
bomys opimus, for 2–3 wk (Kiriakova et al. 1970). In
addition, species of Xenopsylla have only 1–3 gener-
ations/yr (Soldatkin et al. 1967 for X. gerbilli caspica,
and Zolotova et al. 1978 for X. skrjabini), so the above
scenario is feasible.
The positive relationship between prevalence and
host density for N. i. theodori can be explained by the
173
above-mentioned discussion, namely that there is an
increased probability that the transmission stage is
transmitted under high host density. The more distantly
located the patches are (i.e., density is low), the less
frequently they are occupied, due to greater difficulty
of colonization (Hanski 1994). In the case of the flea
N. i. theodori, the number of habitat patches (hosts) at
each given location does not increase, so the absence
of an unimodal curve of prevalence plotted against host
density is to be expected.
Flea burden and flea prevalence
The relationship between flea burden and flea prev-
alence is analogous to the intraspecific abundance–oc-
cupancy relationship of free-living animals. The ex-
istence of positive correlations between local density
and regional or geographic occupation have been re-
ported for a variety of taxa (Gaston et al. 1997, Gaston
1999 and references therein). Contrary to studies of
interspecific abundance–occupancy relationships, abun-
dance in the studies of intraspecific abundance–occu-
pancy relationships is usually averaged across all (oc-
cupied and unoccupied) sites (e.g., Kuno 1991 and ref-
erences therein). These relationships have been found
to be positive, although contrary cases also have been
reported (Boecken and Shachak 1998). In general, an
empirical relationship between the fraction of sites (or
samples) where a given species occurs and its mean
density can be modeled as a logistic curve (Gaston
1999).
Intraspecific studies of parasite burden (equivalent
of abundance) vs. parasite prevalence (equivalent of
percentage occupancy or Diamond’s [1975] incidence
of a species) of a parasite species across individual
hosts are related to relatively small scale (see Gaston
1999). Thus, the model can be collapsed to its linear
version. Positive relationships have been repeatedly re-
ported for helminth burden and prevalence (e.g., Bush
and Holmes 1986, Haukisalmi and Hentonnen 1994).
Analogous data for fleas have not been found.
The present results demonstrated that the burden of
both fleas correlated positively with the prevalence of
infestation, when it was calculated as the mean number
of fleas across all host individuals. These positive re-
lationships could be sampling artifacts; the number of
patches at which a species is recorded (prevalence)
could be a positive function of the mean abundance of
the species (burden) simply because locally rare species
are more difficult to detect than are locally abundant
species. However, this was not the case. The sampling
model of Hanski et al. (1993) explained a relatively
low proportion of variance of the fraction of uninfested
gerbils across sampling sites, in spite of the small scale
of present considerations. The explanation for the pos-
itive relationship between flea burden and prevalence
may be straightforward. The probability that a flea in-
fests a new host individual (patch) is higher when the
flea burden is higher. Flea colonization of new host
174 BORIS KRASNOV ET AL.
individuals is passive rather than active, and occurs
when host individuals come into direct contact with
one another or visit each other’s burrows. It is clear
that the higher the flea abundance on a flea donor, the
higher the probability of infestation in a flea recipient.
Moreover, fleas can infest nonresident hosts, but these
hosts are not able to support flea populations. This
explains why the intensity of infestation of resident
gerbils was found to be the best predictor of the prev-
alence of infestation. These results once more accen-
tuate the effect of the density of resident host individ-
uals on flea distribution.
ACKNOWLEDGMENTS
We thank M. Hastriter (Brigham Young University, Utah,
USA), S. Medvedev and V. Vatschenok (both from Zoological
Institute RAS, St. Petersburg, Russia) for their help in flea
identification. David Ward (Ben-Gurion University of the Ne-
gev, Israel) and Neil Springate (Museum of Natural History,
Great Britain) read an earlier version of the manuscript and
made helpful comments. We also thank J. S. Brown (Uni-
versity of Illinois at Chicago, USA) and two anonymous ref-
erees for their comments. Financial support during this study
was provided by Israel Ministry of Science, Israel Ministry
for New Immigrant Absorption and Local Council of Mizpe
Ramon. This is publication no. 102 of the Ramon Science
Center.
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