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This is to certify that the

thesis entitled l

ECOLOGICAL .ASPECTS OF A MAMMALIAN - ‘
HOST-PARASITE SYSTEM ‘ l

presented by
Allan Christopher Carmichael
has been accepted towards fulfillment

of the requirements for

M.S. (kgvpm Zoology

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Major professor

October 11, 1979

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ECOLOGICAL ASPECTS’OF A MAMMALIAN
HOST—PARASITE SYSTEM

By

Allan Christopher Carmichael

A THESIS

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

MASTER OF SCIENCE

Department of Zoology

1979

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ABSTRACT

ECOLOGICAL ASPECTS OF A MAMMALIAN
HOST-PARASITE SYSTEM

By

 

Allan Christopher Carmichael

Field work was conducted in order to examine some of
the ecological parameters involved in shaping and maintain-
ing a naturally-occurring host-parasite system involving the

helminth fauna of the meadow vole, Microtus pennsylvanicus.

 

Special consideration was given to the blood fluke,
Schistosomatium douthitti. Two questionswereexamined:

(1) What is the spatial and temporal distribution of a para-
site population within a host population? and (2) Does a
parasite population affect a host population in terms of
reproductive output? The data indicate that populations of
voles living near water incur a higher parasite burden when
compared with local populations of voles inhabiting drier
upland sites. These parasite burdens differ both in compo-
sition and intensity. Differential reproductive output
between voles from different habitat types was not clearly
demonstrated. Data on host biology are brought to bear on
an analysis of the host—parasite interaction as a coevolu-

tionary system.

 

 

ACKNOWLEDGEMENTS

I wish to thank the members of my guidance committee,
Rollin H. Baker (Chairperson), Jeffrey F. Williams, John A.
King and John N. Studt for their support and encouragement
on this project. Field work was supported by a grant from
the Michigan Department of Natural Resources and was con—
ducted at the Rose Lake Wildlife Research Area. Laboratory
space and equipment were generouslynmdeavailable by
Jeffrey F. Williams. Field assistance was provided by a
grant from the Office of the Dean of the College of Natural
Science.

Also acknowledged are Anne Zajac for her technical
assistance in the lab; Richard Hill for his suggestions
concerning this study; and Georjean Madery, without whose
cheerful help during field work, this project would not

have been possible.

ii

 

 

 

TABLE OF CONTENTS

Acknowledgements
List of Tables

List of Figures.
INTRODUCTION

THE STUDY AREA .
MATERIALS AND METHODS.

RESULTS.

Vole Populations
Numbers. .
Reproduction . .
Male Reproductive condition.
Female Reproductive Condition.

Parasites. . .
Parasite Species
Statistical Tests.
DISCUSSION .
Distribution of Parasites.
Behavior of Vole Populations

Relationship Between the Meadow Vole and its
Parasitic Fauna. .

46
46
51

54

 

 

 

iv

 

Page
Schistosomatium douthitti and Microtus
pennsylvanicus as a Host— Parasite System:
Synthesis and Speculation. . . . . . . . . . 58
Summary. . . . . . . . . . . . . . . . . . . . . . . 65

BIBLIOGRAPHY . . . . . . . . . . . . . . . . . . . . . 68

 

 

 

 

Table

Table

Table

Table

Table

Table

Table

Table

LIST OF TABLES

Total number of captures of marked
animals on each grid, including
recaptures . . . . . .

Distribution of captures on each grid
according to weight—defined age class
and summed across the study period .

Number of marked voles removed during the
final trapping period. . . . . . . . .

Reproductive characteristics of animals
captured on each grid summed across all
trapping periods

Number of embryos removed from individual
pregnant voles upon autopsy.

Number of voles parasitized (and
percentages) according to individual
species and grid . . . . . .

Numbers (and percentages) of parasitized
and nonparasitized voles on each grid.

Average distance of capture in meters
from the water's edge of "parasitized"
and "unparasitized" voles. . . . .

18

22

22

23

33

34

37

43

 

 

Figure

Figure

Figure

Figure

Figure

Figure

H

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U)

U1

LIST OF FIGURES

Minimum number of voles alive on each
grid during the study.

Proportion of male voles with testes
in the scrotal position on each grid
during each trapping period.

Proportion of female voles with

preforate vaginal openings on each grid

during each trapping period.

Proportion of female voles with
enlarged nipples on each grid during
each trapping period . .

Grid II. Capture sites and frequencies
of capture of four representative
meadow voles . . .

Grid III: Capture sites and frequencies

of capture of four representative
meadow voles .

vi

25-26

28-29

30—31

39-40

41—42

 

 

 

INTRODUCTION

Ecological aspects of parasitic interactions have long
been neglected in deference to the more immediate concerns
of disease control and prevention. Much information has
been obtained relating to the impact of the environment
upon parasitic life cycles. This information has been
restricted largely to parasites of man and domestic mam-
mals and a number of important syntheses have resulted,
including those of MacDonald (1965), Crofton (1963) and
Cohen (1977). Up until recently, most information concern-
ing the ecology of parasites inhabiting wild mammals was
derived from life—history studies and surveys of host popu—
lations. The recent expansion of the literature in this
field reflects a growing awareness of the fact that a more
complete understanding of the ecological aspects of para-
sitic relationships may lead to more effective control of
these organisms and the diseases they produce (see Kennedy,
1975, and Kennedy, ed., 1976). This field of study has
been characterized by Kennedy (1975 1) as follows:
"Ecological animal parasitology is concerned with the dis-
tribution and abundance of parasites. This includes their

distribution and abundance in space, in time and in

 

 

 

different hosts, and involves consideration of the factors
regulating host-parasite interactions at both the individ-
ual and population level. It is above all concerned with
the quantitative as well as qualitative relationships
between parasites and their hosts."

In contrast with many parasitic relationships of
importance to medical and veterinary research, parasites
which occur in populations of wild mammals may not cause
disease and debilitation. Harmful interactions may in many
cases result from human perturbation. Naturally-occurring,
host—parasite systems often appear to represent complex and
somewhat stable coevolutionary systems in which detrimental
effects on the individual host areminimized while the
probability of parasite transmission is maximized.

The study of parasite population dynamics is often
complicated by the life cycles of many of these organisms.
Regulation of population growth occurs both as a result of
biotic interactions as well as environmental impact upon
free living stages. Many recent studies concerned with
parasite ecology have focused upon parasites of ectothermic
host organisms in which competition for resources and
environmental variability are assumed to be the major
forces limiting population growth. Mammalian systems, on
the other hand, present a particularly complex situation
due to the greater ability of most mammals to respond

immunologically to parasites and to some extent regulate

 

 

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the levels of parasitic infection. The intensity of
response may vary from host to host as well as within the
lifetime of a single host, making mammalian host—parasite
systems particularly difficult to model. Nonetheless, the
examination of naturally-occurring host—parasite systems
may give some indication of the selective pressures
involved in shaping these highly coordinated systems.
Insight which will aid in determining the ecologically
significant parameters involved in maintaining such systems
may also be obtained.

The present study examined a specific naturally-
occurring host-parasite system in southcentral Michigan
consisting of the helminth fauna of the meadow vole,

Microtus pennsylvanicus. The blood fluke, Schistosomatium

 

douthitti, was chosen for an analysis of ecologically
important factors for two reasons. First, Zajac (1978)
reported high levels of infection by this species in vole
populations from the study areas during the two years pre-
vious to this study. Second, extensive reports have been
published concerning the biology of this species and its
role as a laboratory research organism. In the present
study, two questions were examined: (1) Does the local
distribution of a host population influence the composition
and prevalence of its parasite fauna? and (2) Does a
naturally-occurring parasite population affect its host

population in terms of reproductive output? The parasite

 

 

 

 

 

faunas and demographic characteristics of vole populations
from two distinct habitat types were contrasted in an
attempt to answer these questions. The extremely large
number of studies in the literature concerning the biology
of the meadow vole can aid in interpreting population
phenomena observed in this study and help to define the
nature of parasitic impact upon vole biology.

Parasitic organisms have been implicated as causal
agents in influencing microtine population fluctuations
(Christian, 1963; Christian and Davis, 1964; Chitty, 1952;
and Christian, 1961). Particular attention has been given

to the brain protozoan, Frenkelia (= Toxoplasma) microti,

 

although no definite correlations have been demonstrated
between the occurrence of this parasite and any influence
upon microtine population fluctuations (Findlay and
Middleton, 1934, and Jellison, 1971). The interplay of
stress due to crowding and increased susceptibility to
parasitic infection has been examined by a number of
authors (Davis and Read, 1958; Jackson and Farmer, 1970;
Patterson and Vessey, 1973). Recent work by Seed and his
colleagues (Seed gg 31., 1976, and Seed gt a1., 1978) has
demonstrated that splenomegaly may be used as an indica—
tion of parasitic infections in wild voles. Their hypo-
thesis that parasitism could lead to decreased reproductive
potential has refocussed attention on the role of para—

sitic infection in microtine population declines. Wiger

 

 

 

 

 

(1977) attempted, primarily through a synthesis of avail—
able literature, to relate the effects which endoparasites
have upon their hosts to models of population dynamics of
Microtus agestis. The author provides a valuable litera—
ture review, but the speculative conclusions can only be
applied to natural situations with caution.

Other parasites of microtine rodents have received
attention in the literature,a1though their role in micro-
tine population fluctuations has not been examined for the
most part. Prominent among these are a variety of blood

and digestive tract protozoans which have been studied by

 

a number of authors (Baker gt gt., 1963; Fay and Rausch,
1969; Elton gt gt., 1931; and Cox, 1970). Also, in an
interesting series of papers, Kisielweska (1970) exa—
mined what she termed the ecological organization of
intestinal helminth groupings in Clethrionomys gareolus.
A number of studies have focussed specifically on the

parasites of Microtus pennsylvanicus. Of these, Rausch and

 

Tiner (1949), Erickson (1938), and Kirner gt gt. (1958)
provide the most comprehensive review of parasitism in this
species. Notably absent from these reviews are reports of

the blood fluke, Schistosomatium douthitti. This worm, the

 

adults of which inhabit the mesenteric veins of their hosts,
appears to be primarily a parasite of microtine rodents.
Adult worms have been recovered from the mesenteric veins

of the muskrat, Ondatra zibethicus (Penner, 1938), the

 

 

    

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redbacked vole, Clethrioggmyg rutilus (Swartz, 1966) and
the meadow vole, Microtus pgnnsylvanicus (Price, 1931).
Incidental occurrence has also been reported in the porcu—
pine,Erethizondorsatum (Choquette gt gt., 1973), the

meadow jumping mouse, Zapus hudsonius (Whitaker, 1963)

 

and the white-footed mouse, Peromyscus leucopus (Zajac,
1978). '

Little work has appeared in the literature concerning
the effects of parasitism upon the reproductive output of
the host. Wiger (1977) reviewed the literature on the
impact of Trypanasoma sp. upon reproduction in their exper-
imental hosts. Weatherly (1971) examined the effects on
litter size and litter survival in mice infected with

Trichinella spiralis during gestation. More recently, Timm

 

and Cook (1979) analyzed the effect of botfly larvae on
reproduction in the white—footed mouse. The authors pre—
sent a hypothesis in which they consider this host-parasite

relationship to be stable and coevolved.

 

 

THE STUDY AREA

The composition of a parasite fauna contained within a
host species is strongly influenced by the surrounding
environment. In View of this, a brief description will be
presented of some of the major features of the study area
at the Rose Lake Wildlife Research Area in Bath Township,
Michigan (sections 22and 23, T5N, RlW, Clinton County).
Each of four trapping grids contained populations of small
rodents consisting primarily of the meadow vole (Microtus
pennsylvanicus), the meadow jumping mouse (2gpgg

hudsonius), the white—footed mouse (Peromyscus leucopus),

 

and the deer mouse (P. maniculatus). Populations of these
species were examined using a mark and recapture live trap-
ping program. Two of the grids (IIand.III)were located on
moist pond—edge sites while the other two grids (I and

IV) were located in dry upland fields. Each set of grids
was chosen for its habitat similarities.

The dominant plant species on all four grids was
brome grass (Bromus sp.). In contrast with areas of mixed
vegetation, there was little litter accumulation beneath
even dense stands of this grass. Peak growth with

flowering of brome grass in early July was followed by seed

 

 

head formation correlated with an overall decrease in
precipitation in late July and early August; new growth
was noted again in late August and early September.

The two upland grids were quite uniform in composi—
tion, consisting almost entirely of brome grass. Occa—
sional patches of goldenrod (Solidago sp.) and Soapwort

(Saponaria officinalis) grew on both grids and at least one

 

side of each grid bordered woody vegetation, a deciduous
woodland in the case of Grid IV and a hedgerow in the case
of Grid I.

Vegetation on the two mesic grids was far more hetero-
genous. Both bordered on ponds, the edges of which sup—
ported dense vegetation, chiefly cattails (Typhg sp.)
interspersed with lesser amounts of goldenrod and reed

canary grass (Phalaris aruidinacea) on Grid II, and a domi—

 

nant sedge (Carex sp.) plus reed canary grass, goldenrod

 

and joe—pye weed (Eupatorium purpureum) on Grid 111. On

 

both grids, the secondary plant species increased in density
just beyond the cattail and sedge border, respectively, and
then sharply declined in numbers about ten meters from the
water's edge. From this pointcnn both grids extended up a
gentle slope covered with brome grass. Dense stands of
dogwoods (Cornus sp.), willows (Sgttg sp.) and multiflora
rose (Rggg multiflora) at the edges of these grids dictated

an irregular trap arrangement.

 

 

Although active growth of vegetation ceased over much
of the well—drained habitat dominated by brome grass during
mid—summer, vegetation remained lush along the pond bor—
ders. It should be noted that when Grids II and III were
originally surveyed on June 11, the first row of traps was
placed within 1.5 meters of the water's edge. One month
earlier, the area covered by the first row of traps had
been completely inundated with water. Following the high
water conditions, the water level gradually receded with
the pond adjoining Grid 11 drying up completely in early
August. The pond bed remained moist, however, and sup—
ported lush growth of vegetation for the rest of the sea—
son.

A wide range of vertebrates and invertebrates was
found on or near the four grid sites. These organisms may
play an important role in parasite transmission and a few
of the major ones will be mentioned.

In general, predatory species were infrequently

observed on all grids. Garter snakes (Thamnophis sirtalis)

 

were the most common, being regularly found on all grids.
Two avian predators, the red-tailed hawk (Bgtgg
jamaicensis) and the American kestrel (thgg spaverius),
were observed over all the grids at least once during the
study. A great—horned owl (Bgtg virginiana) was seen twice
in trees adjoining Grid III. Weasels (probably Mustela

frenata) were caught occasionally in dense vegetation on

 

 

10

both pond-edge grids. Domestic cats (Fgltg ggtgg) were
observed twice on Grid I. Although never seen, the pres-
ence of raccoons (Procyon lgtgt) was evidenced on all grids
by their droppings.

An insectivore, the short-tailed shrew (Blarina
brevicauda) was frequently captured on all four grids. The
masked shrew (§2£E§ cinerceus)wasnever captured during
this study, perhaps due to a lack of sensitivity in the
trip mechanism of the traps used. Its presence has been
shown locally by means of catches in pit-fall traps by
Jacquelyn Shier (personal communication, 1979). Other mam—
mals observed on the study sites included white-tailed deer

(Odocoileus virginianus) on Grid I and the eastern chipmunk

 

(Tamias striatus) which was occasionally captured on Grid
11. One Norway rat (Rattus norvegicus) was captured on
Grid II and a house mouse (Mgg musculus) was captured once
on each of Grids I and IV.

Nesting bird species included Henslow’s sparrows

(Ammodramus henslowii) on Grid I and red—winged blackbirds

 

(Agelaius phoeniceus) on Grids II and III. Eastern meadow-

 

larks (Sturnella mgggg) and song sparrows (Melospiza
melodia) were frequently observed on all four grids.
McWhirter and Beaver (1977) give a thorough listing of the
avian species reported from this area.

Prominent among the local insect fauna were crickets

(Gryllidae) and grasshoppers (Acridadae and Tettigoniidae).

 

 

 

11

These insects and ants were commonly attracted to the bait
in the traps.

The molluscan fauna of these sites is of particular
interest when examining the ecology of local parasites
which may live in these organisms during part of their life
cycles. Land snails and slugs were common on all four

grids. Anguispira alternate was common while species of

 

the genera Mesodon and Mexomphyx were less so. Ponds
adjoining Grids II and III contained large populations of
the pulmonate snails, Lymgea elodes (note: See Clark,
1973, for synonymy and taxonomic status of this species)

and Helisoma trivolvis. Other snails collected were

 

Gytaulus parvus, Physa gyrina, Promenetus sp. and members

of the amphibious genus Succinea.

 

 

 

MATERIALS AND METHODS

Demographic data on four populations of Microtus
pennsylvanicus and several other small rodents were col-
lected on the four study sites between 20 June and 19
September 1978. This was accomplished using a live-
trapping, mark and recapture program which employed galva-
nized sheet metal live—traps produced by L. M. Leathers and
Sons, Athens, GA. These traps are 2.5" wide, 3.5" high and
11” long and have a swinging back door which allows for
inspection. In each location, a permanent grid of eight—
meter spacing consisting of 100 live traps was established.
The exact arrangement of traps varied according to the
pond edges and shrubby borders in an attempt to cover a
maximum amount of grassy area suitable for meadow voles.

A pilot trapping study determined which areas were in fact
inhabited by M. pennsylvanicus.

Trapping was conducted in seven periods separated by
seven—day intervals. Within a period, live traps at each
station on a grid were set on four consecutive evenings.
Traps were baited in the early evening with a mixture of
peanut butter and rolled oats, inspected for captured

animals and closed the following morning, and then baited

12

 

 

 

 

 

l3

and reset that evening. Trapping was not conducted during
the day to avoid trap mortality due to exposure. Grids I
and II were trapped consecutively for four nights followed
directly by four nights of trapping on Grids III and IV.
Upon first capture, individual animals were marked for
subsequent identification by toe clipping. The following
data were recorded for each new animal captured: Species,
location on the grid, toe-clip number, sex, weight and
reproductive condition. Weights were obtained to the near—
est gram using a Pesola spring scale (100 g capacity).
Voles were assigned to age classes on the basis of weight
(Krebs, gt gt., 1969) and reproductive condition was
assessed using the methods of Keller and Krebs (1970).
Male testical position was recorded as scrotal or abdomi—
nal. The female reproductive status was judged by the
condition of the nipples (either non—visible, visible or
lactating), the vaginal orifice (either perforate or non-
perforate) and the degree of closure of the pubic symphysis
(either closed, slightly open or open). Females with
obviously bulging abdomens were considered to be pregnant.
The relative value of these different indicators of female
reproductive condition will be discussed under Results.
Upon first capture within a trapping period, a com-
plete set of data was recorded for each animal. If the

animal was recaptured within the same four-night trapping

 

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14

period, only the toe—clip number and location of capture on
the grid were recorded.

Two assumptions are inherent in this trapping method.
First, it is assumed that trapability is random, so that
the results are expected to give a representative view of
the populations under examination. Second, the assumption
is made that any mortality resulting from the trapping
experience and marking by use of the toe—clip method is not
related to either sex or age of the meadow vole.

During the final trapping period, all Microtus, ggpgg
and Peromyscus spp. captured were removed alive from the
grids. The animals were then maintained for a maximum of
four days in the colony room of the MSU Museum. Internal
examinations of reproductive condition and parasite fauna
were conducted in the laboratory of Dr. Jeffrey F. Williams
at the MSU Veterinary Clinical Center. To determine the
presence of internal parasites, the voles and mice were
first given an intraperitoneal inoculation of a solution
containing a lethal dose of sodium pentabarbitol and
approximately 100 units of ammonium heparin which was used
to prevent the blood from clotting. The immobilized ani-
mals were sexed, weighed, measured and external reproduc—
tive indicators were recorded. Also at this time, a small
amount of blood was withdrawn from a suborbital puncture

using a heparinized capillary tube. The blood was used to

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15

prepare smears to check for blood protozoa and to obtain
packed-cell volumes.

Examination of the portal and mesenteric venous
systems for the presence of Schistosomatium douthitti was
carried out via perfusion using a solution of phosphate-
buffered saline. To accomplish this, the hepatic portal
vein was severed close to the liver, andthe buffered saline
solution was introduced through the dorsal aorta. The
perfusate flowing from the liver and the severed hepatic
portal vein was collected and filtered following the method
of Zajac (1978). The blood flukes thus collected were
sexed and counted under a light microscope.

The gut was next removed and examined for the presence
of metazoan parasites. Appropriate sections of the diges-
tive system were slit longitudinally and the contents were
washed and decanted in cold water. Helminths were located
and counted under a light microscope and preserved in ten
per cent buffered neutral formalin for later identifica-
tion.

The following internal organs were removed, weighed
and preserved in formalin: liver, spleen, kidneys, gonads
and adrenals.

The cranium of each Microtus was removed and the brain
surface was examined under a dissecting microscope for
visible cysts of the toxoplasma-like protozoan, Frenkelia

microti. The brains were then removed and preserved in

 

 

 

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RESULTS

The results will be presented in two sections, the
first one dealing with the demographic characteristics of
the four vole populations and the second covering the data
obtained from the parasitological examinations. Analyses of
the movements of marked voles in relation to their parasite
fauna will also be included in the second section. This
consideration will be restricted to data obtained on the
meadow vole, and information concerning any of the other

rodent species captured (Zapus hudsonius, Peromyscus spp.

 

and Mus musculus) will be presented only where appropriate.
It should be noted that no evidence of exchange of animals
between grids was ever obtained from the recapture of

marked individuals.

Vole Populations
A total of 2800 trap—nights per grid were logged

resulting in 851 captures of 108 marked voles. Table 1 pre-
sents a listing of the numbers of marked individuals on each
grid as well as the total number of captures per grid of
each sex. In addition, 68 g. hudsonius, 55 Peromyscus spp.

and one Mus musculus were also marked.

17

 

 

 

 

18

TABLE 1

TOTAL NUMBER OF CAPTURES OF MARKED ANIMALS
ON EACH GRID, INCLUDING RECAPTURES

 

Grid I Grid II Grid III Grid IV

 

Male Female Male Female Male Female Male Female

 

Number of

 

captures 150 92 119 74 174 133 38 13
Number of

marked voles 22 15 16 14 24 22 9 5
Numbers

The number of voles alive on each grid throughout the
study was calculated using the direct enumeration technique
described by Krebs (1966). In using this method, the mini-
mum number of animals alive at time t is obtained by summing
two figures: (1) the number of animals caught at time t;
and (2) the number of previously marked animals caught after
time t, but not at that time. Figure l graphs the minimum
number of voles alive on each of the four grids during the
study period. Numbers of animals range from a low of one
individual on Grid IV during the final trapping period, to a
high of 28 animals on Grid I during the sixth trapping
period.

Similar trends include an initial increase in numbers
on all grids except Grid IV, and an overall decline in num-

bers on all four grids during the final trapping period.

 

 

5-!

 

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Figure 1 .

 

Minimum number of voles alive on each grid
during the study.

 

20

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21

Dynamics of the two water-edge populations (Grid II and III)
were similar; the number of animals on both grids first
increased, peaked in mid-summer and then declined gradually
during the final trapping periods. In contrast, the growth
of the two upland populations differed greatly, both from
one another and from the two water-edge populations. The
minimum number of voles alive on Grid IV declined steadily
during the study, reaching a low point of one individual
during the final trapping period. In direct contrast with
this, the number of marked animals on Grid I increased
steadily reaching a high point of 28 animals during trapping
period six, then decreasing slightly during the final trap—
ping period. Weight class and reproductive data imply that
this increase may not be due to resident breeding but
rather to an enlargement of the subadult weight class, per—
haps due to emigration (Table 2). This point will be con—
sidered further in the next section.

During the final trapping period, all marked voles
captured were removed and held alive until parasitological
examinations could be performed. This totalled 45 animals,
numbering 17, 10, 17 and one animal removed on Grids I—IV,
respectively. Table 3 presents a listing of the marked
animals according to grid, sex and weight-defined age

class.

 

 

22

TABLE 2

DISTRIBUTION OF CAPTURES ON EACH GRID ACCORDING
TO WEIGHT—DEFINED AGE CLASS AND
SUMMED ACROSS THE STUDY PERIOD

 

Juvenile Subadult Adult

 

Male Female Male Female Male Female

 

 

Grid I 15 16 44 33 14 5

Grid 11 2 l 23 21 27 14

Grid III 6 16 42 31 24 12

Grid IV 0 5 23 3 2 0
TABLE 3

NUMBER OF MARKED VOLES REMOVED DURING
THE FINAL TRAPPING PERIOD

 

Juvenile Subadult Adult

 

Male Female Male Female Male Female Total

 

Grid
Grid
Grid

Grid

I O O 6 6 4 l 17
II 0 O 2 1 4 3 10
III 0 0 1 2 8 6 17
IV 0 O 0 0 1 0 1

 

 

23

Reproduction

Reproductive intensity was evaluated on the basis of a
number of external indicators. The use of external charac-
teristics has its limitations, but Krebs gt gt. (1969) feel
that these indicators do provide a crude measure of repro—
ductive output. Using their method, data for each external
characteristic have been summed across the whole study
period for the purpose of analysis (Table 4). Data on lit-
ter size obtained from autopsies will also be presented.
Comparisons of reproductive intensity have been limited to

Grids I—III; upland Grid IV has been eliminated because the

low number of captures and the overall decline in the number

of voles on that grid make any comparison of questionable

value.

TABLE 4

REPRODUCTIVE CHARACTERISTICS OF ANIMALS CAPTURED ON
EACH GRID SUMMED ACROSS ALL TRAPPING PERIODS

 

Grid I Grid II Grid III

 

Percentage of
males possessing 34.2 44.1 45.8
scrotal testes

Percentage of
females possessing 30.8 36.8 34.9
perforate vaginal openings

Percentage of
females possessing 24.0 30.9 23.6
enlarged nipples

 

 

24

Male Reproductive Condition

Male voles with scrotal testes were considered to be
in breeding condition. This appeared to be a reasonable
assumption since upon autopsy all males with scrotal testes
possessed clearly visible tubules in the caudal epididymus,
a condition indicative of active sperm production (Jameson,
1950). Figure 2 shows the proportion of males with testes
in the scrotal position throughout the study on each of the
three grids. The reproductive condition of males on the two
water—edge grids followed a similar pattern, with a high
proportion of males possessing scrotal testes throughout
the season. A consistently lower proportion of males were
in breeding condition at any one time on upland Grid 1.
For each grid, captures of males possessing scrotal testes
were totalled, and comparisons of the three grids were per-
formed using a Chi—square test corrected for continuity.
This test revealed no statistically significant difference
between the number of scrotal males on the two water—edge
grids (x2 = 1.02, 1 df, P > .3). In contrast, a separate
comparison of upland Grid 1 to each of the two water-edge

2 (Grids I and 11,

grids yielded significant values of X
x2 = 10.56, 1 df, P < .01; Grids 1 and 111, x2 = 17.09,
1 df, P < .001). Thus, the number of reproductively—active

male voles was significantly greater in the wet than in the

dryer habitat.

 

 

Figure 2. Proportion of male voles with testes in the
scrotal position on each grid during each
trapping period.

 

26

totem mEaaofi

N o n v m N

I l l I 1 I

m 10.10 m

2.5 OVA WA o../ /M\ ox

m

 

uoguodOJd

 

.lirlflrwl

 

27

Female Reproductive Condition

Several external sexual characteristics were used to
evaluate female reproductive condition. Because of the
extreme subjectivity involved, data concerning the degree
of closure of the pubic symphysis was not analyzed. The
most easily assessed external sexual characteristic is the
condition of the vaginal opening, although this may not be
the most reliable indicator of reproduction. Krebs gt gt.
(1969) feel that the best measure of a population's breeding
activity is the percentage of females with enlarged nipples,
indicative of lactation. In this study, the data obtained
on the enlargement of the nipples may not be entirely
accurate due to the subjectivity involved and caution should
be exercised in the interpretation of these results.

Figures 3 and 4 graph the proportion of female voles
possessing perforate vaginal openings and enlarged nipples,
respectively. These animals were captured on the three
grids throughout the study. Separate comparisons of the
numbers of females with perforate vaginal openings and
enlarged nipples were made between the three grids and were
evaluated using a Chi—square test corrected for continuity.
No statistically significant results were obtained from any
of the paired comparisons of grids for either characteristic.
Figure 3 shows that the occurrence of females with per-
forate vaginal openings was similar on the two water—edge

grids throughout the season. Grid I differed in that the

 

.fiai'lefltf. filefiéifib- ~84”

3’.“

in anvialz

 

 

 

 

Figure 3. Proportion of female voles with perforate
vaginal openings on each grid during each
trapping period.

 

 

29

moron vaQQo:.m

 

m o m _

I I i <
1
29:0 < I
MPLO Q l

N 3.0 m

om'm l
U/Qm l

 

'—-

uoguodOJd

 

 

 

Figure 4. Proportion of female voles with enlarged
nipples on each grid during each trapping
period.

 

31

more; m:_aao+h

 

m n v m N _
l I I I I j
o\
<‘a.
o
o<\
N310 m m
/ m|m\
<
m 2.0 o 0
.310 <

UOHIOdOJd.

 

 

 

32

majority of females with perforate vaginal openings was
concentrated in trapping periods four and five. It should
be noted that neither did this increase coincide with nor
was it followed by an increase in observed pregnancies.

The frequencies of observed pregnancies varied greatly
between the two habitat types. Throughout the course of the
study, only two females with obviously bulging abdomens,
indicative of pregnancy, were captured on each of the two
upland grids. Pregnant females were encountered much more
frequently on the two water-edge grids, with ten observed
on Grid II and eleven on Grid III.

Further information on reproduction was obtained in the
form of embryo counts taken from pregnant females which were
autopsied upon final removal. Table 5 lists the numbers of
embryos removed from the five pregnant females each examined
from Grids I and II, and the six females from Grid III. The
failure to find a difference between wet and dry habitats
in this and the other analyses of female reproductive

condition may be due to the relatively small sample size.

Parasites

 

Upon removal, all Microtus pennsylvanicus were examined

 

for the presence of helminthic endoparasites. Table 6 sum-
marizes the results and includes information on two proto-

zoan species. Grid IV has been eliminated from the follow-
ing statistical considerations since only one animal was

removed and examined.

 

33

TABLE 5

NUMBER OF EMBRYOS REMOVED FROM INDIVIDUAL
PREGNANT VOLES UPON AUTOPSY

 

 

 

 

Grid I Grid II Grid III
n = 5 n = 5 n = 6
7 7 6
5 7 6
5 6 6
5 6 6
5 5 6
— 5
i = 5 4 x = 6 2 i = 5.8

 

Parasite Species

As might be expected from knowledge of their life
cycles, trematode infections were entirely restricted to
voles from the two water—edge grids. Most frequently
encountered was the cecal fluke, guingueserialis
guingueserialis, with 44.4 percent on the animals from Grid
II and 47.1 percent from Grid III harboring infections.
Worm burdens ranged from one to 13 individuals with a mean
number of three worms. The second most frequently encoun—
tered trematode was the blood fluke, Schistosomatium

douthitti, which occurred at infection levels of about 11

 

 

 

 

 

 

-- L Am.HHv N -- - AN.OV H .am mammmmmmwmm
-- - -- - -- - Aa.ov. H mmmmmma mmammmmmm
-- - Am.HHv N AH.HHV H -l - N anozmamu uHHmsamUOHaoc<
-- - Am.mv H -- - Aa.0v H H asozwamu aHHmnamUOHaoc<
-- - -- - -- - Ae.©v H .am mmmmmmmmmwm
-- - Aq.mmv m -- - Ae.ov H .am mmmmmmmmm
Ao.OOHV H AG.NHV m Am.mmV m AN.GNV a mmmwwmmm mmmmmmww
M I: I Am.mv H u: n I: I owoumeHH pwflmwucwwflcb
-- - AH.sqv w As.qu q -- - mHHmHsmmwaacHsa mHHmHsmmmsacHso
-- - Am.HHV N AH.HHV H -- - HuUHausou asHumEOmoumHnom

H n c NH u a a n a mH n a

>H ust HHH wHHm HH stu H wHHo

 

QHMU QZ< mmHommm A<DQH>HQZH OH
UZHQMOOU< Ammw<HzmoMmm QZ¢V QMNHHHm<M<m mMAO> mo Mmmzbz

o mqm<H

 

35

percent on each of the two water—edge grids. Infection
levels of this parasite were quite low relative to data from
past years in the same general area (Zajac, 1978). In
addition, one unidentified trematode was collected from the
intestine of a single vole.

The occurrence of infections involving nematodes and
cestodes did not appear to be related to the presence or
absence of water. The pinworm, Syphacea obvelata, was ubiq-
uitous in its distribution, being found on all four grids
(the one animal examined from Grid IV contained an infection
of five pinworms). One whipworm, Trichuris sp., was
recovered from an animal inhabiting upland Grid I, while
five animals from Grid III harbored single infections of
this nematode. Adult cestodes were infrequently encountered
in the intestines of voles from all three grids and infec—
tion levels ranged from 11.1 to 13.3 percent. Two
anoplocephalid and one hymenolepid species of tapeworm
appear to be represented and in all but one case, single
species infections occurred. Three out of the five infec-
tions were composed of a single tapeworm. The two excep-
tions were an individual vole which contained 13 scoleces of
a small hymenolepid tapeworm (Hymenolepis sp.) and a vole
which contained a single adult of each of the two other
species of anoplocephalid tapeworms.

It should be noted that although complete data were not
recorded, small (2—3 mm) cysts were occasionally observed

in the livers of voles removed from the three grids. These

 

36

may be larvae of cestodes belonging to the genus Cladotaenia
(Rausch and Tiner, 1949), the adults of which are found in
the harrier (Circus cyaneus). Thisavian predator inhabits
the Rose Lake Area (McWhirter and Beaver, 1977) but was not
observed during this study. No large cysts indicative of
infection with Taenia spp. were observed.
Data were also collected on two protozoan species.
Examination of blood-smears reveals infections of a
trypanasome (Trypanasoma sp.), however, the prevalence was
low (7.3 percent) when compared with that obtained by '

Dunaway gt a1. (1968) from Microtus ochrggaster collected

 

in Tennessee. An extremely low prevalence (8.4 percent
overall) of the toxoplasma-likeprotozoan,Frenkelia microti
was revealed as a result of the examination of brain tissue.
The one infected individual was heavily parasitized and the
cyst stage of this protozoan was grossly visible on the
surface of the brain. Histological examination of brain
sections revealed no further occurrence of this parasite.

Although the four study sites were located within a 1.5
square mile area, no evidence of exchange of individuals
between grids was ever observed on the basis of toe-clip
and recapture data. Also water—borne infections of trema-
todes were never found in voles from the upland study site,
indicating little or no exchange of individuals from wet
areas. In contrast with this, examinations of Zapus

hudsonius collected from upland Grid IV revealed that two

 

     

37

out of 14 animals were infected with Schistosomatium
douthitti. Patterns of movement of z. hudsonius appear to
be quite different from those of the meadow vole and this

point will be discussed in more detail.

Statistical Tests
A comparison of the numbers of animals parasitized with
helminth infections from the three grids (Table 7) was per-

formed using the Fisher exact probability test. For the

TABLE 7

NUMBERS (AND PERCENTAGES) OF PARASITIZED AND
NONPARASITIZED VOLES ON EACH GRID

 

 

Parasitized Unparasitized
Grid I n = 15 7 (46.6) 8 (53.3)
Grid II n = 9 8 (88.9) 1 (11.1)
Grid III n = 17 13 (76.5) 4 (23.5)

 

purpose of this analysis, each animal was classed as being
"parasitized” if it contained an infection of at least one
parasitic helminth, or "unparasitized” if no helminths were
found upon autopsy. The null hypothesis of no difference
in the number of infected animals was examined. A paired
comparison of the two water—edge grids indicated that no
statistically significant difference existed between the
occurrence of parasitized voles (P = .42). On the basis of

this test, data from the two water-edge grids were pooled

 

38

and compared with the data from upland Grid I. A signifi—
cant value (P = .024) resulted in the rejection of the null
hypothesis of no difference in the number of parasitized
animals.

The relationship between the center of activity of a
given vole and the nature of its parasitic fauna was
examined statistically. The movements of voles on the two
water-edge grids were compared relative to the presence or
absence of g. guingueserialis and/or g. douthitti. In order
to acquire either of these parasites, an animal must at some
time forage at the water's edge, or actually enter it. The
eight-meter spacing between the individual traps allowed the
distance of capture from the water's edge to be roughly cal-
culated. Capture sites and frequencies of capture were
mapped for each vole removed from the water—edge grids.
Figures 5 and 6 illustrate maps of representative individ-
uals, four each from Grids II and III. The water's edge
lies along the right border of each map. It was noted that
individuals containing trematode infections were captured
predominantly close to the water's edge (Figure 5, a-c and
Figure 6, a—c). From these maps, the average distance away
from the water's edge at which each animal was captured was
calculated (Table 8). Voles were classed as "parasitized"
if they contained trematode infections and as "unparasitized"
in their absence. A Mann—Whitney U test was used to exa-

mine the one-tailed alternative hypothesis stating that the

 

Figure 5.

39

Grid II: Capture sites and frequencies of
capture of four representative meadow voles.
The water's edge lies along the right border
of each map. Below, sex, total number of
captures and parasites found upon autopsy
are given for each animal.

(a) Female: 7 captures
Schistosomatium douthitti
l Quingueserialis
guingueserialis

 

(b) Male: 15 captures
2 g. guingueserialis
(c) Female: 6 captures

1 g. guingueserialis

(d) Female: 13 captures
no parasites found

40

X=CAPTURE SITES

]-6=FREOUENCY OF
CAPTURE

 

 

 

II‘HIIH dawn-lama I.
r. . . .I.

 

Figure 6.

Grid III: Capture sites and frequencies of
capture of four representative meadow voles.
The water's edge lies along the right border
of each map. Below, sex, total number of
captures and parasites found upon autopsy
are given for each animal.

(a) Female: 15 captures

1 guingueserialis
guingueserialis

(b) Male: 1 captures
Schistosomatium douthitti

g. guingueserialis

captures
8. douthitti

g. guingueserialis

captures
parasites found

 

(c) Male:

(d) Male:

O\l r—‘Noo l—‘HV

42

A

X=CAPIURE snas
l-9=FREQUENCV or CAPTURE

 

 

43

TABLE 8

AVERAGE DISTANCE OF CAPTURE IN METERS FROM
THE WATER'S EDGE OF "PARASITIZED"
AND "UNPARASITIZED" VOLES

 

 

 

Parasitized Unparasitized

Grid II

27.7 53.6

13.7 40.0

2.7 33.8

1.1 20.7

-- 8.0

x = 11 3 x = 31 2

Grid III

39.5 73.6

34.2 66.7

23.3 59.7

23.2 58.3

17.8 43.7

8.5 42.4

8.0 24.7

0.0 10.1

__ 6.0

x:
H
H
\o
to
x:
ll
4.\
N
00

 

 

44

mean capture distance away from water is greater for
unparasitized animals than for parasitized animals. On
each grid, a statistically significant difference resulted
in the rejection of the null hypothesis of no differences
(Grid II, U = 3, P < .056; Grid III, U = 14, P < .025).

It appears therefore that there is a correlation between
the location of the center of activity of an individual as
indicated by its average distance of capture from the
water's edge and the composition of its parasite fauna.

In addition, information was desired on the distance
of closest approach to water by each animal as indicated by
capture location on the grid. This was considered to be
important because even if the majority of captures occur
far from water, a single contact with water may be suffi—
cient to cause infection. In order to examine the rela-
tionship between closest approach to water and the composi-
tion of an animal's parasitic fauna, animals captured at
least once in the two rows of traps closest to the water
on each grid (a distance of approximately eight meters
from the water's edge) were scored as "positive" while
those never captured in these rows were scored as "nega—
tive.” The parasite categories from the previous experiment
were retained and a Fisher exact probability test was per—
formed to examine the alternative hypothesis that animals
captured at least once close to the water's edge had a

greater probability of being infected with trematodes than

 

    

Fin! Eli-filialéfl'd ‘1' fl 3!“

  

”PM 4'"
"a

‘13-‘13” * _

_ ,.
w.

    

if: '3 '-- 1"

   

-=-.-r

45

those animals not captured in the first two rows of traps.
A significant difference resulted in the acceptance of the

alternative hypothesis (1 df, P = .03).

 

 

DISCUSSION

Distribution of Parasites

 

The results of the parasitological examinations showed
that the habitat in which a vole lived strongly influenced
the composition of its parasitic fauna. Trematode infec-
tions were entirely restricted to voles from the two water
edge sites and consisted mainly of guingueserialis

quinqueserialis and Schistosomatium douthitti. The inter-

 

mediate hosts of these two species, the snails Gyraulus
parvus and Lymnea elodes, respectively,werefound in abun—
dance in the ponds adjoining these sites. Infection levels,
as mentioned earlier, were low relative to previous year's
data from the same area. This may be due to the series of
dry summers which preceded and included this study, during
which the ponds dried up in late summer and transmission
cycles were most likely interrupted. This, coupled with the
relatively short life spans of voles under natural condi—
tions (Hamilton, 1941), could contribute to the low levels
of infection observed.

No distinct relationship to habitat type was noted in
the occurrence of nematode and cestode infections. The

pinworm, Syphacia obvelata, was the most frequently

46

 

 

47

encountered parasite during this study and its distribution
appeared to be random. This parasite possesses a direct
life cycle in which frequent contact with other small mam-
mals, rather than the presence of a specialized intermediate
host,wouldbe required for the completion of the life cycle.
These results are consistent with those of Rausch and Tiner
(1949) who noted no difference in the occurrence of this
parasite in voles collected in dry and more mesic habitats.
In contrast, Mollhagen (1978) observed the highest inci—

dence of Syphacia sigmodontis from Sigmodon hispidus to

 

occur in mesic habitats. One reason for this may be that
the viability of the free living stages of this parasite
may have been negatively influenced by the aridity of the
xeric habitat sampled in much of this study. The occur-
rence of the three species of cestodes was sporadic and
appeared to follow no distinct pattern, although the rela-
tively small number of infections observed may have contri—
buted to this conclusion.

Bush et a1. (1978) stated that ”one current view of
community ecology is that similar habitats are occupied by
an essentially constant primary community of species
adapted to those habitats and a more variable secondary
community. The former provides a basis for similarity, the
latter for diversity.” A population of definitive hosts is
considered to be the equivalent of a community of

trophically-similar organisms. Using this framework, a

_ .I .' _. -. :__.-... .Vy'pn
__flga'qé user It; 9.“?! “if” "i’lfltfl‘

1,4. - ' ‘ i} I

 

_fi-'I

 

48

population of voles may be infected with a primary com—
munity of parasites which occur in a variety of habitats
over a wide geographical area. This primary community is
represented in this study by Syphacia obveleta and may also
include one or more of the species of cestodes. The wide
distribution of these species is noted in the studies of
Erickson (1938) and Rausch and Tiner (1949) and an exami—
nation of these works indicates that cestodes of the genus
Andrya and Taenia as well as certain nematodes may be
included in this community.

Superimposed upon this community is a secondary com-
munity of parasites whose components are derived from a
certain environmental habitat within the overall geographi-
cal distribution. In this case, a secondary community of
parasites whose components are of fresh water origin may be
seen in the form of the trematode species whose distri—
bution is restricted to voles inhabiting pond edges. Bush,
Holmes and Humphrey (personal communication, 1979) also
discussed the presence of a tertiary community of para-
sites, the occurrence of which is restricted to a specific
region within the overall habitat. This may be related to
microclimatic site variation which may affect the parasites
directly or influence the distribution of various inter-
mediate host species. This tertiary community of parasites
is not clearly represented in this study. A larger sample

size may be needed to reveal this community, if present.

 

49

The low incidence of protozoan infections observed in
this study does not allow for a detailed analysis of their
distribution. The presence of the toxoplasma—like proto-
zoan,Frenkelia microti in M. pennsylvanicus appears to be
the second record for this species (Kirmse, 1965). Dubey
(1977), in a recent review, noted that a high incidence of
this parasite has been reported to occur in a number of
microtine species, but few authors reported the presence of
debilitating clinical symptoms. The occurrence of F.
microti in only one of the 42 animals examined is curious
in that an extensive portion of the brain was involved and
cysts were grossly visible on its surface. Histological
examinations of all other specimens revealed no further
infection. In this case involving such a massive infec-
tion, the behavior of the one parasitized animal is of
interest. This vole, an adult male, was captured a total
of nine times from 25 July to 16 September 1978 and was in
reproductive condition during that whole period. No aber-
rant behavior was noted at the time of removal. These
observations serve only to increase our interest in the
effects of this poorly—known protozoan upon microtine
biology.

In contrast with data obtained from M. pennsylvanicus,
two of the 14 specimens of Zapus hudsonius examined from
the upland grid sites contained infections of the water-

borne trematode, S. douthitti. This was surprising since

 

50

these two animals were captured on upland Grid IV, over 40
meters from the nearest free standing water. This is con—
sistent with the observation that movements of the meadow
jumping mouse are more extensive than those of the meadow
vole. The home ranges of meadow jumping mice are generally
larger than those of the meadow vole (Quimby, 1951;
Hamilton, 1937). Townsend (1935) suggested that meadow
jumping mice tend to wander, and felt that the observed
movement was a result of the animals seeking moist areas
during the dry part of the summer. Quimby (1951) suggested
that the movement is due to a relatively unstable home
range, the shape of which is determined by the terrain.
Patterns of movement and thus home range size of the meadow
jumping mouse may also be strongly influenced by the
dietary habits of this species. In contrast with the
herbivorous meadow vole which is continually surrounded by
its food supply, the meadow jumping mouse is primarily
granivorous, utilizing resources which occur in a patchy
distribution both in time and in space. Whatever the
proximal cause of this movement may be, this activity
appears to place these mice in frequent contact with
sources of infection by water borne parasites. Involvement
of this host species may play a significant role in the

maintenance of S. douthitti within certain habitats.

 

51

Behavior of Vole Populations

 

The behavior of vole populations from two distinct
types of habitats was examined in relation to their asso-
ciated parasitic faunas. With the exception of upland Grid
IV, all grids housed active populations of Microtus

pennsylvanicus along with populations of other small mam-

 

'mals. Densities of voles on the two water-edge grids fol-
lowed a similar pattern throughout this study (20 June to
19 September 1978), while those from the two upland sites
showed widely disparate fluctuations. Since the upland and
lowland populations were more or less continuous, it seems
improbable that the observed differences were related to
the various phases of microtine cycles (i.e., increase
phase, decline, etc.). These differences were most likely
related to the local variation of the habitat. Getz (1963)
and other authors have noted that the meadow vole appears
to have a high moisture requirement and is characteristic
of moist grasslands and marshes, although it has been
recorded from both wet and dry habitats. In a study of
vole populations in Michigan, Getz (1960) found higher den-
sities of voles in marshes when compared with old fields.
Pond edge sites perhaps provide voles with a highly
optimal and somewhat predictable or constant habitat. This
may be reflected in the similar behavior of the two water
edge populations of voles in this study. Some variation in

the environmental conditions did exist between these two

._ II.

51353 ' 91%

‘ =5! 21513: I

 

52

grids: Standing water remained in the pond adjoining Grid
III while the pond adjoining Grid II dried up by early
August. Nonetheless, the pond bed adjoining Grid II
remained more moist than the surrounding habitat until
autumn rains again filled it. The critical factor influ-
encing vole behavior at these sites may be the constant
source of moisture (Getz, 1960) which directly affects
plant growth. The presence of actively growing plant
material may positively affect reproductive output by voles
in these areas in a similar fashion as has been demonstrated
by Negus and Berger (1979) to occur in Microtus montanus.
It was noted during the present study that plant growth
essentially ceased in midsummer on the upland sites which
were dominated by brome grass. The effects of the mid-
summer drying were particularly pronounced on Grid IV and
on this grid the vole population declined consistently.
Grid I was set up in a grassy depression and on this grid
population levels stayed high, although the factors contri-
buting to the observed high density may differ from those
in operation on the two water edge grids as already noted.
On a local scale, yearly variation in the levels of
precipitation could influence the demography of voles liv-
ing in dry, marginally suitable habitat. Conversely,
highly suitable pond edge habitats may provide voles with a
somewhat stable and predictable environment. This stabil-

ity is perhaps reflected in terms of reproductive output as

 

53

maintained through compounds (Negus gt g1., 1977) found in
actively growing plant material. The data show that male
reproductive activity is definitely higher on the two water
edge grids than on the two upland grids, but female repro-
ductive indicators do not show this trend. The observation
that, in comparison with upland Grid I, nearly four times
as many pregnancies were noted on Grid II and nearly three
times as many on Grid III indicates that the hypothesis of
differential reproductive output from wet and dry grids
deserves further testing. The failure to find a difference
between wet and dry habitats may be due to the relatively
small sample size.

We may speculate on the influence of differential
reproductive output upon parasitic relationships: In cer-
tain dry seasons, the majority of reproduction within a
local area may arise from voles inhabiting favorable moist
habitats. This hypothesized reproductive effort may have a
strong influence upon the fixation within local vole popu—
lations of genetically controlled resistance to the high
parasitic assault experienced in water edge areas. The
local effects of habitat on vole populations will be con-
sidered further in the following section concerning para-

sitic interactions.

r

         
 

nap-#1,.-

,’_.J‘ '__ ‘I ‘ r
_ __I_ a,
r‘. val-1'3"} 3' _. 1,.

H: am an *

     

. Iii???

  
   

..:-:.-=.-.-.;-':'.5'-iéai:':-'.-.-. Le"! ' {um-'2'. 2 9" ' . ' ' ' """J ”'13

.- ‘ '- ' ' - ‘
.,__.... . - .

 

“fir

54

Relationship Between the Meadow Vole
and its Parasitic Fauna

 

 

One intention of this study was to try and gain some
information concerning the impact of a naturally-occurring
parasite complex upon its host population. In order to
examine the influence of parasitic infection, the preva-
lence of helminth parasitism of meadow voles was compared
between the two habitat types. A significantly higher
prevalence of parasitism was shown to occur on the water
edge grids when compared with the upland site. It has
already been noted that reproductive activity appeared to
be higher on the two water edge grids than on the upland
grids when evaluated on the basis of at least one indicator,
andVfiu;not significantly reduced. Meadow voles living near
water may achieve a higher reproductive output and incur a
higher parasite burden relative to voles living in dryer
upland sites. This is consistent with the assumption that
in a coevolved host—parasite system, little or no damage to

the host will be incurred by the ”prudent parasite.‘ Fur-
ther aspects of the coevolutionary nature of microtine
host-parasite systems will be considered in an upcoming
section. It should be stressed that although these data
imply that high reproductive output occurs in areas of high
parasitic infection, the actual impact of the parasite popu-
lation upon the host population cannot be clearly defined

from this sort of field study. Certain environmental

factors appear to enhance reproduction in the vole and it

 

55

is possible that this may mask detrimental effects exerted
by the parasites. It is also possible that parasitic infec-
tion negatively influences juvenile survivorship and that
this effect remained undetected in this study. It could be
argued that increased reproductive output on water edge
grids may result as a response to increased mortality due

to parasitism. Detrimental effects which might lead to
mortality have not been demonstrated for at least one common

parasite of the meadow vole, Schistosomatium douthitti.

 

Laboratory studies are needed to properly address this con-
tention.

The observation that reproduction in meadow voles
remained high in areas of frequent parasitism implies two
important points: First, that some degree of coordination
of life cycles and resistance occurs between the parasite
and host populations, and second, that high reproductive
potential coupled with a rapid population turnover rate in
the face of major parasitic assault might allow for
genetic selection of immunological resistance to parasitic
damage.

Two final notes of caution in interpreting these
results should be mentioned. First, it is unlikely that
all parasite species had an equal effect upon the host as
was assumed in this analysis. Also, for managability, the
effects of arthropod and protozoan parasites were not con-

sidered. Second, different results might possibly have

 

v2;-
‘3

 

56

been obtained if this study had been conducted in a year of
higher parasitic infection as was seen by Zajac (1978). A

controlled experiment which involved artificial infections

would give a more accurate view of the impact of naturally—
occurring parasites upon their host species, at least par-

tially freeing the investigator from the confounding influ-
ence of environmental effects.

Statistical tests showed an apparent correlation
between the location of the center of activity of an indi-
vidual vole as indicated by average distance of capture from
the water'sedgeand the composition of its parasitic fauna.
The average distance of capture from the water's edge of
voles infected with water borne trematodes was significantly
smaller than that of animals lacking these infections. This
indicates that relatively little movement by resident voles
occurred away from the site of infection during the three-
month course of this study, although it does not reflect
upon the behavior of dispersing animals. This observation
is consistent with that of Getz (1961) who found relatively
little movement of young voles away from their birth site
and noted that many female offspring constructed nests
within the home ranges of their mothers. These findings are
of particular interest in that they incorporated a temporal
as well as spatial element into our knowledge of the distri-
bution of a parasite population within a population of one

host species. A clearer definition of the behavior and

‘45 Juli- uswsat 91¢

situate”! .:-.r-. .;=..e. .~ - I: .ar;*;'za'r-3-.? gut

 

 

57

movements of infected host individuals aids our understand-
ing of the functioning of naturally-occurring\host-parasite
systems in that these factors determine the continued main—
tenance and dispersal of the parasite population.

The final statistical analysis performed involved an
examination of the helminth fauna of an animal in relation
to its closest approach to the water's edge, as indicated by
capture location on the grid. As was stated earlier, this
was considered to be important because even if the majority
of captures occurred far from the water's edge, a single
contact with water may be sufficient to cause infection with
a water borne trematode. The results show that voles cap-
tured at least once in the first two rows of traps closest
to the pond edge had a significantly greater chance of being
infected with water borne trematodes than did voles cap—
tured elsewhere on the grid. The previous analysis showed
that the prevalence<xfinfection with trematodes within the
vole populations under study dropped off rapidly as the dis—
tance from the water's edge increases (Table 8). This
analysis relates the probability of infection by trematodes
to the amount of dispersion of a vole's home range as well
as the location of that home range.

It appears that certain aspects of the biology of the
meadow vole have strongly influenced the nature of the
parasitic relationships associated with this species.

Rausch and Tiner (1949) attempted to examine the effects of

 

1

H.-

v;l
." "i 7

.. - .‘ —. .. - "' '..1 I
. . I. a .- =-' TI... .- ' _--" ' ‘_ ,H .
, “.5139“ .. ' ' '-:u ,.

- J

I - ,C‘
at: "is icrt‘lffiib " 1.3.

It

i..,' _ ' '- IIIILRI‘I '5"? l;-

. i.

 

 

58

microtine population fluctuations upon the population densi-
ties of associated parasitic species but found no definite
connection between population densities of voles and para-
site density. They felt that both quantitative and quali-
tative differences in helminth infections were seasonal or
geographic in nature. The present study has demonstrated
the effects of local habitat variation upon the composition
of the parasitic fauna of the meadow vole. The preference
for moist habitat by this species often places these

animals in direct contact with a major source of parasitic
infection. In relatively constant pond edge habitats, sur—
vival of meadow voles appears to be improved (Getz, 1960)
and reproductive output may be enhanced. An increase in the
already high fecundity of this species coupled with a fre—
quent parasitic assault in what appears to be a highly
favorable habitat may contribute to the formation of highly
coordinated and somewhat stable host-parasite systems.

Schistosomatium douthitti and Microtus pennsylvanicus as a
Host-Parasite System: Synthesis and Speculation

 

In the final section of this discussion, the relation-
ship between the meadow vole and one of its naturally—
occurring parasites, the blood fluke, Schistosomatium
douthitti, will be examined. Studies in the literature
combined with data from the present study provide the basis

for this consideration. Ecologically-significant parameters

 

 

59

along with selective pressures which have shaped this system
will be discussed.

The blood fluke, S. douthitti, is found in the
mesenteric veins of its mammalian hosts and appears to be
primarily a parasite of microtine rodents. Malek (1977)
gives a comprehensive review of the literature available on
the biology of this species. As with all schistosomes,
infection of the mammalian definitive host occurs by direct
penetration of the skin by the cercarial stage. For this to
be accomplished, the host must actually enter water contain-
ing cercaria. Although it is generally not considered to be I
a semiaquatic animal, the meadow vole frequently enters the
water and inhabits marshes and pond borders (Getz, 1961;
Blair, 1939). Activity patterns of the vole appear to be
coordinated with the time of cercarial release from the
intermediate molluscan host in that maximum cercarial out-
put occurs at dusk (Oliver, 1951) when rodent activity is
high (Hamilton, 1957). Cercarial shedding also occurs at
this time in the rodent strains of the blood fluke,

Schistosoma japonicum (Kennedy, 1975). In contrast, the

 

cercarial shedding of at least one human schistosome, S.
mansoni, occurs around mid-day when the chances of human
water entry are high.

The coordination of the life cycle of this parasite
with that of its host may also be seen in the time of maxi-

mum annual shedding of cercaria from infected snails.

41.5,

-.-+ -“
a J

‘ ‘2 i" I' 1.115;; “1123*“ "'
39111.3. “fife 1! '

91f

_ .‘b
. mm 1‘

'.---'F’{

 

 

60

Bournes (1961) and Blankespoor (personal communication,
1979) report that shedding of cercaria reaches a peak in
mid-summer. High cercarial shedding at this time may be
correlated with two aspects of host population biology.
First, populations of voles reach an annual high point at
this time following the first major reproductive bout in
spring and early summer (Figure l) which would allow for a
maximum number of potential host individuals to be exposed
to infection. Second, during spring when rainfall is fre-
quent and flooding can be expected, both snails and cercaria
would stand the chance of being highly dispersed as a
result of variations in water level. By mid-summer, the
pond edges have receded and snail populations, and thus
cercaria, are concentrated within a relatively small area
at the pond border which experiences frequent vole activity.
Also it might be speculated that as the overall habitat
dries out in mid-summer, densities of the water—limited
meadow vole may increase in the thick vegetation along the
pond borders relative to the rest of the habitat. Once
again, a large number of host individuals would be exposed
to a source of infection.

The high levels of infection achieved by S. douthitti
in the meadow vole once again indicate that some degree of
coordination exists between these two organisms. Zajac
(1978) has reported worm burdens ranging from eight to 236

adult parasites recovered from wild-caught voles. Tissue

 

. .-. -' " . v-
. I

._--= . _ _ . " '1" :- .' "I .4"... . .
.‘- 1 b81313!” ‘ _ 125;. f.
I I :- é

.,

.w,¢-'u'I 11:61” '9.-:. 53°15‘42" 1'51 a“. h,

iisinnuq

 

 

61

response to ova produced by these parasites is minimal.
Heavily-infected animals appear healthy and Zajac notes that
in light of the heavy predation pressure experienced by
voles (Burt, 1945), any reduction in an animal's fitness
would be expected to result in its removal from the popula-
tion. The author speculates that the parasite and its
associated tissue reaction do not affect the vole's perfor—
mance adversely. In striking contrast to this, experimental
studies have shown that a challenge of only 20 cercaria was
sufficient to kill the non-natural host, the house mouse,
Mtg musculus.

These observations point to a high degree of compata-
bility between the vole and parasite and suggest a long
evolutionary association between the two species. Zajac
(1978) also noted that subadult and adult voles have higher
levels of infection along with heavier worm burdens than do
juvenile voles. The presence of large worm burdens only in
older animals suggested to her that reinfection may occur
during the animal's lifetime. This appears to be in con—
trast with the situation seen in human infections by
schistosomes in which some degree of acquired resistance to
reinfection is presumed to occur (Kennedy, 1975).

It seems likely that the short life expectancy of M.
pennsylvanicus would have some impact upon the maintenance
of S. douthitti infections within a given habitat. The

average survival time of voles in the field has been

 

 

agalfiu'm

 

62

calculated as 2.7 months (Getz, 1960), about 4.2 months
(Blair, 1948), and a maximum as much as 16 months (Hamilton,
1941). These low expectancies would still allow enough time
for schistosome development and egg production, in that
Price (1931) observed egg production approximately 30 days
after infection. While other mammalian schistosomes are
restricted to tropical and subtropical regions, pronounced
seasonality severely limits the time span over which this
parasite can be cycled. The impact of seasonal restriction
upon the life cycle of S. douthitti combined with the rela—
tively short life expectancy of the meadow vole imply that
maintenance of the infection in vole populations throughout
the winter is unlikely. In years of high prevalence, some
infected voles may survive to continue the cycle the follow-
ing spring, but in years of environmental stress and thus
low infection levels as observed in this study, the infec—
tion has a fair chance of declining to extinction in vole
populations.

This speculation brings into question the role of
other host species in maintaining S. douthitti infections
within a given habitat. Malek (1974) found that in certain
areas, infections are maintained over the winter in the
intermediate molluscan host, Lymnea elodes. Blankespoor
(personal communication, 1979) is currently studying other
aspects of the role of the molluscan imtermediate host in

this cycle.

 

 

 

 

63

The other principal mammalian host of S. douthitti, the
muskrat, Ondatra zibethicus, is likely to play an important
role in cycling this parasite, although the nature of this
role is poorly understood. Penner (1942) felt that this
species was the most important definitive host of S.
douthitti. In contrast with the high infections level of 70
percent from M. pennsylvanicus found by Zajac (1978), Penner
(1938) found only 10 percent of the 330 muskrats which he
examined to be infected. This prevalence rate seems low and
may reflect the author's recovery techniques (Penner, per-
sonal communication, 1979). The specimens had been cap-
tured by trappers for their pelts, and clotted blood may
have made the recovery of worms from the extensive cecal
venous system difficult. Penner (personal communication,
1979) also observed thehighestprevalence of infection to
occur in young muskrats which may imply the presence of
acquired resistance or simply reflect behavioral patterns
which determine the amount of contact with infective stages.

Although findings in the literature are in no way con-
clusive, the muskrat may serve as a long distance disperser
of S. douthitti infections. The relatively larger terri—
torial requirements of the muskrat result in a more exten-
sive movement by this animal. Shanks and Arthur (1952)
reported that muskrats living in pond habitats tended to
move from pond to pond, and Errington (1939) reported that

during spring and fall periods of movement, muskrats may

, ”EM 1311f! ,, . H

. ’-.-I. . . ' : rI‘J
lit-F: "Baum-m . 'D‘.;Ii'-n.-'l ~111on _ Ii-

-' "Fl-VI. lw-r' a.

 

64

travel overlandumre than 20 miles, presumably in search of
more favorable habitat. These movements may serve to
inoculate new sites as well as reestablish the infection
where local extinctions have occurred.

It is also possible that the muskrat may maintain
infections within an area when hypothesized local extinc-
tions occur in populations of M. pennsylvanicus. This is
based on the assumption that muskrats are relatively longer
lived, although the findings of Mathiak (1966) make this
difficult to interpret since he reported an 87 percent
mortality in muskrats the first year and a 98 percent
removal by the second season. These data may reflect the
influence of trapping rather than natural removal, thus
confounding any interpretation.

The involvement of the meadow jumping mouse, nggg
hudsonius, as a definitive host of S. douthitti has already
been considered to some extent. It is interesting to note
that during this study in which the level of S. douthitti
prevalence in the meadow vole was low (7 percent overall),
a similar prevalence of 10 percent was observed in jumping
mice collected from all study sites combined. Carmichael
and Muchlinski (in press) demonstrated that S. douthitti
survives hibernation in the meadow jumping mouse and egg
production by worms was noted in animals which had recently
been aroused from hibernation. The meadow jumping mouse

may serve as a long-term reservoir of S. douthitti,

 

 

65

maintaining the infection within an area over the winter
while in hibernation or when populations of M.
pennsylvanicus undergo drastic fluctuations in numbers.
Also the relatively longer lived meadow jumping mouse
(Quimby, 1951) may maintain infections within an area for a
longer time following the disruption of the cycle due to
drought and temporary elimination of intermediate host
habitat. It should be noted, however, any proposed role of
the meadow jumping mouse in maintaining the life cycle of S.
douthitti is purely speculative until it has been demon-
strated that these mice actually pass the eggs of this
fluke.

The previous considerations represent only a very few
of the factors which contribute to the successful function—
ing of a highly coordinated host-parasite system and which
convey the complexity and dynamic nature of this inter—
action. As with most naturally-occurring host-parasite
systems, further work is needed both in the laboratory and
in the field if we are to understand more fully the main-

tenance of this unique system.

Summary
The data collected in this study indicate that popu-

lations of voles living near water incur a higher parasite
burden when compared with local populations of voles
inhabiting drier upland sites. Increased moisture along

pond edges presumably provides voles with a continual

 

ff-h 7 III:'-I'LI' I

.l-r. I .
I .
,-.
II

it. _
um..-&n'13 r. -'

 

 

66

source of an actively growing food supply which may be
favoring increased reproductive output. Population concen-
trations along the water's edge bring voles in direct con-
tact with a major source of parasitic infections. This may
lead to parasite burdens which differ both in composition
and intensity from those of other local vole populations.
The life cycle of at least one trematode, S. douthitti,
appears to be highly coordinated with the activity of M.
pennsylvanicus, and these two organisms may represent a
coevolved host-parasite system.

The tendency of voles to inhabit moist areas appears to
have a strong impact upon this system and a selective
regime resulting in resistance to parasitic damage in the
vole as well as a high degree of coordination between the
population dynamics of both species may be functioning.
These selective forces may tend to stabilize the system,
but as Kennedy (1975) points out, "Parasite populations are
still liable to large fluctuations because of their depen-
dence on climatic factors." He notes that climate influ—
ences the prevalance of infection, while host response
controls the level of infection within the host, and thus
introduces stability.

The findings of this study point toward a number of
areas of further research if we are to more fully understand
the dynamics of this and other host—parasite systems. A

laboratory study would be useful in determining the actual

 

 

.' . . f- .
#:1ch '.'I that-w '.

 

67

impact which S. douthitti has upon the meadow vole, and this
might be measured in terms of reproductive output and juve-
nile survivorship. Much work is needed in evaluating the
.role of other host species in maintaining this cycle. A
more precise knowledge of the population processes of the
intermediate host species in relation to parasitic infection
would aid in any attempt to model the dynamics of this
system. Also, the role of the muskrat in this parasitic
system deserves further study and reevaluation.

This study may aid in our overall understanding of the
functioning of host-parasite systems. The occurrence of S.
douthitti in local populations of the meadow vole provides
us with a readily available model with which to examine the
ecological constraints upon host—parasite systems involving
schistosomes. This investigation may have application to
studies concerning the ecology of human schistosomiasis,
particularly due to the involvement of wild rodents in most
schistosome life cycles. Cohen (1977) summarized the need
for studies of this sort when he said, "The control or
eradication of schistosomiasis is a truly ecological as
opposed to a purely medical or technological problem.” We
are still far from understanding the ecology of the schisto—
somes, and this group represents one of the most inten—
sively studied families of parasites. Further research is

needed on all phases of parasite ecology.

 

 

BIBLIOGRAPHY

 

 

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