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IS THE PREVALENCE OF
TAENIA TAENIAEFORMIS
IN
MICROTUS
ARVALIS
DEPENDENT ON POPULATION DENSITY?
Author(s): Elisabeth Fichet-Calvet, Patrick Giraudoux, Jean-Pierre Quéré, Richard William Ashford, and
Pierre Delattre
Source: Journal of Parasitology, 89(6):1147-1152.
Published By: American Society of Parasitologists
DOI: http://dx.doi.org/10.1645/GE-3158
URL: http://www.bioone.org/doi/full/10.1645/GE-3158
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1147
J. Parasitol., 89(6), 2003, pp. 1147–1152
q
American Society of Parasitologists 2003
IS THE PREVALENCE OF
TAENIA TAENIAEFORMIS
IN
MICROTUS ARVALIS
DEPENDENT ON POPULATION DENSITY?
Elisabeth Fichet-Calvet, Patrick Giraudoux*, Jean-Pierre Que´re´, Richard William Ashford†, and Pierre Delattre
Centre de Biologie et de Gestion des Populations, Campus de Baillarguet, CS 30016, 34988 Montferrier/Lez, France.
email: calvet@mnhn.fr
ABSTRACT
: Populations of common voles Microtus arvalis were studied as hosts of the tapeworm Taenia taeniaeformis during
a 14-yr survey. They were monitored in spring, summer, and autumn in a pastoral ecosystem in eastern France. A total of 7,574
voles were sampled during 2 multiannual population fluctuations. A third fluctuation was sampled during the increase phase only.
Overall prevalence was lowest in summer (0.6%), increased by 3 times in autumn (1.5%) and a further 5 times in spring (7.8%).
Analysis of prevalence, based on 7,384 voles, by multiple logistic regression revealed that extrinsic factors such as season and
intrinsic factors such as host age and host density have a combined effect. In the longer term, host age and host density were
positively associated with prevalence in summer. Host density was strongly associated with autumn prevalence. There was no
association between the fluctuation phase and prevalence. The study shows that a long timescale (here a multiannual survey) is
necessary to demonstrate the positive effect of host density on the prevalence of this indirectly transmitted parasite. The dem-
onstration of this relationship depends on the rodents being intermediate rather than definitive hosts.
Numerous studies of dixenous host–parasite systems in ro-
dents have focused on infection dynamics involving the simul-
taneous study of host density and prevalence. Wiger et al.
(1974) suggested that high prevalence of Taenia polyacantha
in bank voles Clethrionomys glareolus was correlated with high
density of the host. The same team (Tenora et al., 1979) found
no such relationship in another parasitic disease in C. glareolus.
Similar studies in Finland, where bank vole and grey-sided vole
C. rufocanus populations were monitored for 3 yr (Haukisalmi
et al., 1987), 10 yr (Haukisalmi et al., 1988), and 12 consecutive
yr (Haukisalmi and Henttonen, 1990), showed a negative rela-
tionship or no relationship between rodent density and the prev-
alence of intestinal helminths. In Ireland, wood mouse Apode-
mus sylvaticus populations were monitored over 3 yr (Mont-
gomery and Montgomery, 1988). Both intestinal parasites and
larval cestodes fluctuated without any specific pattern related to
host density. Likewise, in the United States, the study carried
out by Theis and Schwab (1992) did not find a density-depen-
dent relationship in deer mouse Peromyscus maniculatus in-
fected by Taenia taeniaeformis in a 4-yr longitudinal survey.
In Australia, in the house mouse Mus musculus infected with
T. taeniaeformis, again no relationship was found between den-
sity and prevalence (Singleton et al., 1993). A 10-yr survey of
kangaroo rats (Dipodomys spp.) and their intestinal cestodes
and nematodes in New Mexico showed a negative relationship
or no correlation between prevalence and host density (Decker
et al., 2001). In North Africa, a longitudinal study of the fat
sand rat Psammomys obesus infected with the tapeworm Rail-
lietina trapezoides showed no relationship between density and
prevalence (Fichet-Calvet et al., 2003).
None of these results points to a positive relationship be-
tween these 2 variables, despite the expectation of such a re-
lationship, as evidenced by monoxenous systems (Arneberg et
al., 1998; Laakkonen et al., 1998, 1999). We suggest that in
many cases the timescale was inappropriate to detect this re-
lationship, either because the study was too short in time or
Received 26 December 2002; revised 24 April 2003; accepted 24
April 2003.
* Laboratoire de Biologie Environnementale, EA3184 UsC INRA,
Universite´ de Franche-Comte´, Place Leclerc, 25030 Besanc¸on CED-
EX, France.
† Liverpool School of Tropical Medicine, Pembroke Place, Liverpool
L3 5QA, U.K.
because the authors considered several seasons with different
age structures. Also, the association between density and prev-
alence should be weaker for parasites with (1) an indirect life
cycle, (2) multiple host species, and (3) an extended free-living
stage. Only 1 study, carried out over 17 yr, has shown a positive
density–prevalence relationship, between the snowshoe hare Le-
pus americanus and several helminths (Keith et al., 1985). Fol-
lowing this exemplary work carried out on a lagomorph in Can-
ada, the aim of the present study was to conduct a long-term
study of the common vole Microtus arvalis Pallas 1778 to test
for fluctuating prevalence of the dixenous parasite Taenia taen-
iaeformis Batsch 1786. The samples described here from a 14-
yr survey provide an opportunity to address the following ques-
tion. Is prevalence dependent on vole density when season,
phase of fluctuation, and age of voles are taken into account?
MATERIALS AND METHODS
Study site
The study area occupies about 1,350 ha in Franche-Comte´, France,
10 km northwest of Pontarlier (47
8
10
9
N, 6
8
24
9
E, 850 m above sea
level), with a mean annual rainfall of 1,500 mm. The site is composed
of forest and pastoral land. The forest is mostly seminatural, composed
of mixed beech Fagus sylvatica, oak Quercus robur,firAbies alba, and
some spruce Picea abies plantations. The pastoral land is either im-
proved grassland or permanent pasture and is either open over wide
areas (open field) or enclosed by hedgerows (Delattre et al., 1988; Gi-
raudoux et al., 1997).
Trapping and sampling
Because the common vole is regarded as a pest in agriculture, pop-
ulations have been monitored since 1978 in Franche-Comte´ (Delattre et
al., 1992, 1996, 1999). From 1983 to 1996, the tapeworm T. taeniae-
formis was identified and enumerated during necropsies, and the results
are presented here. Voles were trapped from 1983 to 1993, 3 times per
year, in spring (April), in summer (July or August), and in autumn
(October); from 1994 to 1996, voles were sampled twice per year only
(April and October). French Agricultural Research Institute (INRA)
traplines were used (Spitz et al., 1974). Thirty-four traps were placed
at 3-m intervals in each line of about 100 m. Thirteen to 46 lines were
set on each occasion, totaling 966 traplines (98,532 trap nights) over
these 14 yr. Traps were left in place for 3 consecutive nights and were
visited twice daily. The voles were killed by cervical dislocation as
recommended by Mills et al. (1995).
Rodent age
The weight of the desiccated eye lens (elw) gives the best indication
of age for small mammals (Lord, 1959; Martinet, 1966; Morris, 1971).
1148 THE JOURNAL OF PARASITOLOGY, VOL. 89, NO. 6, DECEMBER 2003
F
IGURE
1. Microtus arvalis dynamics and Taenia taeniaeformis prevalences over a 14-yr period. I
5
increase, D
5
decline, R
5
recovery
after the third fluctuation, dashed lines
5
expected variation of prevalences without a summer sampling.
Eyes were removed and preserved for a minimum of 2 wk in 10%
formalin; then the lenses were extracted, dried for 2 h at 100 C, and
weighed to a precision of 0.1 mg.
Parasites
Taenia taeniaeformis is widely distributed and infects both murine
and microtine rodents. Rodents are intermediate hosts harboring the
larvae in their livers, and the wild cat Felis silvestris and the domestic
cat Felis catus are definitive hosts harboring the adult tapeworm in their
intestines (Schmidt, 1986). During necropsy of the rodents, the presence
of parasites was noted for each specimen. Le Pesteur et al. (1992) and
Beigom Kia (1996) studied the tapeworm larvae parasitizing the rodent
community in this area and found no form that could be confused with
T. taeniaeformis. The strobilocerci are easily discernible on the liver
surface; they are globular, translucent at an early stage of infection
(Murai, 1982) and yellowish-white later, and 5–10 mm in diameter. The
larvae grow very rapidly, so that by the sixth day, they are visible to
the naked eye (Beigom Kia, 1996).
Data analysis
According to Krebs and Myers (1974), the 4 different phases of mul-
tiannual vole fluctuations are defined as increase, peak, decline, and low
density. At each season, host relative density was defined by an abun-
dance index (ai) based on the mean number of voles caught per line (ai
5S
voles/
S
lines). Each phase was defined by the 3-point running
mean, integrating the density values for the preceding and following
years for the same season. It is thus a multiannual estimate of density
and cannot be confused with density values related to individual sea-
sons. Because this variable could have an impact on the prevalence, it
is included in the model. So, the season, phase, host age, and host
relative density effects on prevalence were analyzed by multiple logistic
regression using the binary factor (1
5
infected, 0
5
uninfected) as the
dependent variable and the season (3 levels, spring, summer, and au-
tumn), the phase (4 levels, see above), the host age (0.6 mg
#
elw
#
8.6 mg), and the host relative density (0.2
#
ai
#
29.9) as the inde-
pendent variables. Statistical and graphical displays were created with
S-PLUS 2000 and followed the guidelines presented by Hosmer and
Lemeshow (1989) and Venables and Ripley (1999). To avoid assump-
tions about residual distributions and subsequent inferences, the null
hypothesis of no effect of the variables in the regression model was
tested with 500 permutations of the response variable.
RESULTS
Vole population dynamics
During the study, the M. arvalis populations went through 2
multiannual fluctuations and began a third one (Fig. 1). The
FICHET-CALVET ET AL.—TAPEWORM TEMPORAL DYNAMICS IN VOLES 1149
T
ABLE
I. Distribution of Microtus arvalis captured and examined for Taenia taeniaeformis infection by season, between 1983 and 1996. elw
5
mean eye lens weight (mg) with range in brackets. NS
5
not sampled. The differences between collected and examined specimens are because
of missing values for elw.
Year
Spring
No.
collected
No.
examined elw
Summer
No.
collected
No.
examined elw
Autumn
No.
collected
No.
examined elw
1983
1984
1985
1986
1987
1988
1989
56
107
467
260
161
228
200
56
107
467
257
161
228
199
5.7 (2.1–7.6)
5.7 (3.2–7.4)
5.4 (3.8–7.4)
5.2 (3.3–6.9)
5.0 (3.4–6.8)
5.0 (3.2–7.3)
5.0 (3.8–6.9)
204
119
472
203
179
268
80
203
119
470
198
178
267
78
3.6 (1.2–8.4)
3.7 (1.5–7.2)
3.5 (1.2–7.7)
3.2 (1.4–7.2)
3.1 (1.1–6.6)
3.4 (1.5–8.6)
3.1 (1.0–6.2)
184
568
434
349
245
562
74
183
565
434
349
242
559
73
3.8 (2.0–7.2)
3.1 (1.0–7.4)
3.9 (1.9–7.9)
3.1 (1.2–7.2)
3.0 (1.2–6.5)
3.4 (1.2–6.6)
3.0 (1.6–5.1)
1990
1991
1992
1993
1994
1995
1996
48
67
23
125
40
4
17
48
66
21
125
40
4
16
4.5 (2.1–6.1)
5.2 (2.2–7.1)
5.3 (3.6–6.5)
5.6 (4.1–7.1)
5.1 (2.2–6.1)
5.6 (5.2–6.0)
5.2 (2.6–6.9)
10
277
89
182
NS
NS
NS
10
266
82
180
NS
NS
NS
3.0 (1.8–6.2)
2.8 (0.6–8.0)
3.3 (1.6–7.0)
3.3 (1.3–7.5)
NS
NS
NS
121
394
285
259
10
32
171
121
316
250
256
10
31
149
3.1 (1.4–5.6)
3.5 (1.0–8.6)
3.6 (1.4–6.3)
3.7 (1.2–5.8)
2.6 (1.5–3.4)
3.4 (2.1–4.4)
3.4 (1.6–5.9)
T
ABLE
II. Logistic regression results for Taenia taeniaeformis infection
in Microtus arvalis from 1983 to 1996. elw
5
eye lens weight (mg), ai
5
abundance index (number of voles trapped per 100 m). n
5
7,384.
Variables
Residual
df
Residual
deviance P
Null
Season (3 levels)
Host age (0.6
,
elw
,
8.6)
Host density (0.2
,
ai
,
29.9)
7,383
7,381
7,380
7,379
1,809.302
1,635.828
1,621.689
1,608.796
—
0.000
0.000
0.000
Season
3
host age
Season
3
host density
Host age
3
host density
Season
3
host age
3
host density
7,377
7,375
7,374
7,372
1,578.032
1,565.054
1,563.932
1,559.946
0.000
0.000
0.310
0.196
trapping data are shown in Table I. The first fluctuation was of
very long duration and high amplitude, lasting 8 yr, from 1983
to 1990. In 1984 and 1985, there was an extraordinary outbreak
in which the numbers of voles were similar in autumn 1984
(30 individuals/line) at the end of the breeding season and
spring 1985 (26 individuals/line) at the start of the following
season. These trapping values are indicative of densities above
1,000 individuals/ha (Spitz, 1974). The following 3 years
(1986, 1987, and 1988) showed a more classical profile, with
alternating low densities in spring (around 100 individuals/ha),
medium densities in summer (around 200–400 individuals/ha),
and high densities in autumn (around 400–600 individuals/ha).
The second fluctuation, of a lesser amplitude, lasted from 1991
to 1995. Between these 2 fluctuations, M. arvalis populations
were at low density for 2 yr (1–10 individuals/ha), with an
exceptional decline in summer 1990. The last 3 years of this
survey were characterized by local extinction, with only a few
colonies remaining in isolated spots between 1994 and 1995,
followed by a recovery in autumn 1996.
Prevalence
In total, 7,384 common voles were examined for T. taeniae-
formis infection (Table I). Higher prevalence (7.87, 95% con-
fidence interval [CI]: 6.16–8.62) was observed in spring and
was more than 5 times higher than in autumn (1.52, 95% CI:
1.13–1.97). In summer, prevalence was lower (0.6, 95% CI:
0.32–1.05). These results are illustrated in Figure 1; T. taeniae-
formis prevalence was often high in spring and then decreased
in summer and increased in autumn. This pattern was repeated
in 8 of the 11 years for which data are adequate. The 3 re-
maining years corresponded to the second high density phase
(1992 and 1993) and to very high density in spring (1985, Table
I). In the first analysis, season, host age, fluctuation phase, and
host density were included in the logistic regression. The main
effects were caused by season (P
,
0.0001), host age (P
5
0.0001), and host density (P
,
0.0001) but not the fluctuation
phase. In a second step, phase was excluded from the model,
and the results are summarized in Table II. The main variables,
season, host age, and host density remain highly significant.
The 2-way interactions, i.e., season
3
host age and season
3
host density are highly significant, whereas host age
3
host
density and the 3-way interaction season
3
host age
3
host
density are not (Table II). This means that these variables are
not strictly additive, and that the combined effect of host age
and host density on prevalence has to be considered season by
season. This is illustrated in Figure 2. In spring, the higher
prevalences were obtained in old individuals at low density. In
summer, the prevalence increased both with host age and host
density, whereas in autumn, it depended on host density only.
The present model explains 13.8% ([1809.302
2
1559.946]/
1809.302) of the total deviance.
DISCUSSION
The phase effect
Our study on M. arvalis in Franche-Comte´ allowed the iden-
tification of 2 multiannual fluctuations, each showing 4 phases:
increase, peak, decline, and low density (Krebs and Myers,
1974). The fluctuations lasted 8 and 5 yr, respectively, with
different amplitudes and duration of low density period, i.e., a
maximum of 1,000 individuals/ha during the first fluctuation
1150 THE JOURNAL OF PARASITOLOGY, VOL. 89, NO. 6, DECEMBER 2003
F
IGURE
2. Host age (elw, mg) and host density (number of voles per 100 m of trapline) effects on prevalence of Taenia taeniaeformis.
compared with 500 individuals/ha during the second one. When
the dynamics described by Delattre et al. (1992) are considered,
the first fluctuation is assumed to have actually begun 18 mo
before the start of the current study. This implies a 10-yr du-
ration for the first fluctuation. This nonperiodic pattern is very
different from those generally observed for C. glareolus (Hent-
tonen et al., 1985) and C. rufocanus (Hansen et al., 1999) in
Scandinavia. These 2 species fluctuate following a regular 4- to
5-yr pattern. In Franche-Comte´, the long period of the inter-
mediate host population fluctuations presented an opportunity
to test the relationship between population density and the prev-
alence of T. taeniaeformis. Because during peak and decline
phases the voles get nearer the forest and villages, where cats
are more often present, the expected result would be a higher
parasite transmission rate, leading to an increase in prevalence
at these times. This effect was not seen here. The common vole
is the most widely distributed mammal species in this ecosys-
tem. It belongs to a larger rodent community that includes both
grassland and forest rodents, which could interfere with parasite
transmission rate. Rodent populations fluctuate according to a
6-yr period in Arvicola terrestris (Giraudoux et al., 1997; Fi-
chet-Calvet et al., 2000) and with a variable period in C. glar-
eolus and Apodemus spp. (Raoul et al., 2001). The different
multiannual dynamics in the rodent community could contribute
to the prevalence in each species. The temporal fluctuating
prevalence of the parasite in its secondary intermediate hosts
should thus be investigated at the community level.
Rodent age effect
A positive relationship between host age and parasite prev-
alence has often been demonstrated. There are numerous ex-
amples of age–prevalence effects in rodents infected with par-
asites such as cestodes (Behnke et al., 1993, 1999), trematodes
(Duplantier and Se`ne, 2000), protozoans (Turner, 1986), bac-
teria (Godeluck et al., 1994; Fichet-Calvet et al., 2000), and
viruses (Mills et al., 1992). Kisielewska (1971) even suggested
that the prevalence of infection with intestinal helminths could
be used to indicate the mean age in M. arvalis. All these studies
indicate that with increasing age more rodents become infected.
They recruit T. taeniaeformis while foraging. This relationship
is easily measured because just a few seasons are enough to
collect rodents of all ages. Sometimes, a single well-chosen
season, when all ages are represented, is sufficient to show this
effect. This was the case for Trichuris muris and Syphacia stro-
ma infecting A. sylvaticus in samples collected in September
only (Behnke et al., 1999). In our study, the populations sam-
pled in summer and in autumn contained mostly young animals,
with a low prevalence, whereas most animals sampled in spring
were old, with a high prevalence. However, after adjustment for
age, prevalence also depends on season and density, which
complicates the interpretation of any analysis where all those
variables are not taken into account.
Rodent density effect
In this study, the rodent host is the intermediate host in a life
history that includes a carnivore; in many other studies, the
rodent is the definitive host in a life cycle that includes an
insect. A comparison is justified between the 2 life cycle pat-
terns. In short-term studies such as those described by Singleton
et al. (1993), no relation was shown between T. taeniaeformis
prevalence and domestic mouse (M. musculus) density. In me-
dium-term studies (3–4 yr), the number of homologous seasons
allowing this effect to be tested is insufficient. This led authors
to consider the prevalences observed in different seasons to
obtain a mean prevalence by year and to compare this mean
value between years. The analysis done by Theis and Schwab
(1992) did not reveal a density effect of P. maniculatus on T.
taeniaeformis prevalence. In these 2 studies, it is probable that
the combination of data from host populations with different
age structures and the lack of a temporal perspective led to this
interpretation. In another host–parasite system where the tape-
worm was also a larva, i.e., L. americanus and Taenia pisifor-
mis, Keith et al. (1985) showed that the prevalence observed in
a 17-yr study was density dependent in both juvenile and adult
hares. In this system, the effect was explained by the coinci-
dence between the abundance of the definitive host, the coyote
Canis latrans, and that of its prey. This last study is similar to
an older one, carried out over 8 consecutive years in North
Dakota. Leiby and Kritsky (1974) suggested a positive effect
of P. maniculatus density on the prevalence of Echinococcus
multilocularis, but without having demonstrated any coinci-
dence between host and prey fluctuations (definitive host red
FICHET-CALVET ET AL.—TAPEWORM TEMPORAL DYNAMICS IN VOLES 1151
fox Vulpes vulpes, reviewed in Eckert and Deplazes, 1999). In
these 4 studies, the definitive host is a carnivore whose temporal
and spatial dynamics have to be considered in order to under-
stand how the parasite fluctuates in the rodent (Giraudoux et
al., 2002). In our study area, cats, F. silvestris and F. catus,
definitive hosts of T. taeniaeformis, moved intensively to hunt
in open habitats when outbreaks of grassland voles occurred
(unpubl. data). This situation was also observed in Lorraine
(Stahl et al., 1988; Stahl and Leger, 1992), a region close to
Franche-Comte´. The cats then supposedly shifted the equilib-
rium by dispersing the eggs in grassland areas, particularly at
forest edges.
The density effect on prevalence is only detectable in a lon-
gitudinal survey over many years, including at least 1 complete
multiannual fluctuation. Because of the rapid change in the pop-
ulation structure during the year, it is impossible to distinguish
between the effects of age and those of density on the preva-
lence of an indirectly transmitted parasite in a single year.
In Finland, Haukisalmi et al. (1988) and Haukisalmi and
Henttonen (1990) explored the temporal fluctuations in preva-
lence of the intestinal cestode Cataenotaenia sp. in C. glareo-
lus. In the first approach, lasting 10 yr (Haukisalmi et al., 1988),
they observed low prevalences in increase and peak host phases
and high prevalences in decline and low-density phases. In a
second approach lasting 12 yr, Haukisalmi and Henttonen
(1990) demonstrated a negative density-dependent relationship,
although they segregated samples according to age, i.e., im-
mature against mature. A more recent study by Decker et al.
(2001) in New Mexico showed some negative density-depen-
dent relationship or independence for the analysis of kangaroo
rats Dipodomys spp. infected with several intestinal cestodes
(Hymenolepis sp., Oochoristica sp., and Raillietina sp.). These
authors considered rodent age and used a multiple logistic re-
gression to analyze their data, as we did here. Their study lasted
10 yr. It seems that the long term is not a sufficient criterion to
reveal the impact of host density on dixenous parasite preva-
lence and that the position of the host in the parasitic cycle
appears to be a second important criterion.
In our model, T. taeniaeformis prevalences are dependent on
both the age of voles and their density as well as seasons. In
spring, the prevalence is high, when the animals are old and at
low density. This may be interpreted as an effect of the con-
centration of cat feces in the few patches where voles still exist
and are still accessible to predators. In summer, density gener-
ally increases, M. arvalis becomes widespread, and age and
density interact synergistically such that an old and large pop-
ulation is more infected than a population that is either old or
large. In autumn, prevalence is more independent of age but is
higher at high population density of M. arvalis. Each of these
variables has usually been explored separately, and the temporal
fluctuations in prevalence of other dixenous parasites are in
agreement for host age, whereas they are not for host density.
These divergences could be due to 2 factors, i.e., the timescale
at which the analysis is carried out and the intermediate position
of the host (vs. definitive host) whose density is being evalu-
ated. It should be emphasized that the present model only ex-
plains 13.8% of the total deviance. This means that there are
numerous other factors, i.e., cat population behavior and dy-
namics, rodent community dynamics, and meteorological or
weather conditions, any of which could affect the prevalence
of dixenous parasites in wild rodent populations.
ACKNOWLEDGMENTS
Financial support of the Franche-Comte´ regional council is gratefully
acknowledged. Many thanks to Erica Taube and 2 anonymous reviewers
for revising and improving the manuscript in its earlier version.
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