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Social Vole Parents Force

Their Mates to Baby-Sit

Noga Libhaber

David EilamThe Meir I. Segals Garden for

Zoological ResearchDepartment of Zoology

Tel-Aviv University Ramat-Aviv 69 978, Israel

Received 9 October 2001; Accepted 4 November 2001

ABSTRACT: Parental care has been categorized into direct and indirect investment. The former includes direct contact with the offspring, as in lactation or huddling with the pups, and the latter includes activities such as nest building or hoarding food for the guarding mate. We report here anunfamiliar type of parental behavior in which one parent aggressively forces its mate to stay in thenest with the pups. In this ‘‘forced baby-sitting,’’ one parent grasps the fur of its mate and drags it toward the nest. The behavior was observed in 6 of 10 pairs of the social vole (Microtus socilalis

guentheri) and was typically executed by the male. Dragging the mate to the nest was not correlated with other parental behaviors; neither could we explain why/when it occurred. However, thisbehavioral pattern was eye catching, and its goal was obviously to enforce the mate to stay in the nest with the pups. ß 2002 Wiley Periodicals, Inc. Dev Psychobiol 41: 236–240, 2002. Publishedonline in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/dev.10075

Keywords: Microtus socilalis; parental behavior; maternal behavior; monogamy; paternalbehavior; parental investment; mating system

Parental care in animals is conceived of as protecting,nourishing, and nurturing the young (Immelmann &

Beer, 1989). While parental behavior appears in all

classes of vertebrates and some invertebrates (Klopfer,

1981), it takes an exclusive form in mammals,in which

the female produces milk to nourish the pups. Accord-

ingly, maternal behavior is vital and obligatory in

mammals whereas paternal behavior is relatively rare,

characterizing less than 10% of mammalian species

(Woodroffe & Vincent,1994). Male investmentusually

varies in correlation with the mating system of a

species, with significant male participation in monoga-

mous species and minimal participation in polygamousspecies (Gubernick & Teferi, 2000; Immelmann &

Beer, 1989; McGuire & Novak, 1986; Oliveras &

Novak, 1986). Paternal investment is indeed a funda-

mental tool in the study of mating systems, in whichspecial attention has been directed at voles since

different species of voles possess different mating

systems despite their similarity in morphology, anato-

my, and phylogenetic ancestor (Carter & Getz, 1993).

For example, the prairie vole ( Microtus ochrogaster )

and the pine vole ( Microtus pinetorum) are monoga-

mous whereas the meadow vole ( Microtus pennsylva-

nicus) is polygamous. In these studies on the mating

systems in voles, comparison of maternal and paternal

investment has been the main criterion in classifying

the mating system.

Except for gestation and lactation, components of parental behavior of the male and the female may be

similarly categorized into direct and indirect invest-

ment (Kleinman & Malcolm, 1981). Direct investment

includes huddling with young, grooming and clean-

ing them, retrieving them, and carrying or transporting

them. Indirect investment includes resource acquisi-

tion, maintenance and defense, shelter construction

and maintenance, and defending from predators. In

addition, while the female nurses the pups, the male

may care forthe female, forexample, by bringing food.

Correspondence to: D. EilamE-mail: [email protected] grant sponsor: Israel Science Foundation

Contract grant number: 589-99

ß 2002 Wiley Periodicals, Inc.



In the present study on the mating system of Guenther’s

social vole ( Microtus socialis guentheri), we discover-

ed a novel pattern which does not fall under the

classification of either direct or indirect investment.

Specifically, we found that one parent, typically the

male, tried to increase parental investment by forcing

its mate to babysit.

MATERIALS AND METHODS

Animals

The social (Guenther’s) vole ( M. socialis guentheri)

weighs 37 to 50 g and is 11 cm long, plus a 2-cm tail. It

is a burrow-dwelling rodent that feeds on seeds and

green vegetation. Its eyes and external ears are small,

and its limbs are short (2–3 cm). Ten pairs (male and

female) of voles were each housed in 120Â 63Â

45-cm metal cages, which were located outdoors inThe Meir I. Segals Garden for Zoological Research at

Tel-Aviv University under natural temperature and

light conditions. Overturned ceramic pots and wooden

boxes were placed in each cage to provide shelter.

Seeds and diced, fresh vegetables were provided daily.

The animals could therefore receive all their water

requirements form the vegetables. All the animals used

in the studywerein goodphysical condition and didnot

appear to be disturbed.

Apparatus

Observations were carried out using a cage (108 Â46Â 50 cm) with a transparent glass floor, opaque

walls, and an open top. A mirror was tilted underneath

the cage in a 45-degree angle, providing a bottom view

of the cage and the insides of the two overturned

ceramic pots used by the voles as a shelter and a nest to

raise their litter (see Figures 1 & 2). A video camera

(S-VHS NV-M9500; Panasonic) in front of the cage

was used to videotape the behavior of the parents and

pups. This arrangement allowed us to observe the be-

havior with minimal interference. The parents obvio-

usly were larger than the pups, and when they were

crouching above the pups, it was possible to observe

the pups and their behavior against the background of

the parents and their behavior. A cloth (used T-shirt)

was provided as bedding material. The setup was

placed in a quiet, air-conditioned room (25C) with

natural illumination.

Procedure

A pair of voles was transferred to the observation cage

onthe day ofdelivery, or1 to 2 daysbefore deliveryif it

was possible to detect that the female was at term.They

remained in this cage at all times until the end of

observations. The first videotaping session took place

within thefirst24 hr afterdelivery, and then every other

day until postnatal day 17. Each videotaping session

started by removing the bedding material (cloth) and

wiping the floor to provide a clear view of the parents

and the pups. Behavior was then videotaped continu-ously for 40 min (nine sessions total). All observations

took place 2 hr before dusk—a time of peak activity in

this species (Mendelssohn & Yom-Tov, 1999).

RESULTS

Social voles appear to be monogamous, with extensive

participation of the male in parental care and each

parent tending to the pups either alone or together with

its mate(Libhaber, 2001). However, parentsin thisvole

species were observed not only controlling their own

direct and indirect investment in parental care but also

attempting to force their mate to stay in the nest with

the pups. In this behavioral pattern, one parent used its

incisors to grasp the fur of its mate and drag it toward

the nest. A sequence of snapshots of this behavioral

pattern is shown in Figure 1, and an illustration of

another sequence is provided in Figure 2.

As shown in Table 1, of the 10 pairs of voles, this

behavior was observed frequently in 2 pairs (140 and

84times), was less frequent in 4 other pairs (7, 4,3, and

1 times), and was not observed in 4 pairs. The male was

usually seen to drag the female, but in 2 pairs the

female dragged the male. Dragging was initiated whenone parent established contact with its mate outside the

nest, apparently independent of which had initiated

contact. Grasping of the mate was not executed in any

specific manner, with the tugged parent being pulled

from the head, pelvis, or side of the chest and either

dragged backwards toward the nest or pushed forward

(Eilam & Libhaber, 2002). In 142 of 239 observations,

the tugged parent seemed unaffected and did not pay

attention to the pups, but left the nest almost immedia-

tely and consequently was dragged back, until one of

the parents gave up and stayed with the pups. While

being forced to the nest, the tugged parent either re-mained passive or aggressively tried to evade the

puller. In a few cases, the tugged individual acquiesced

and completed its own way to the nest after being

released in the middle. As shown in Table 1, dragging

was not correlated with other parental behaviors, and

therefore did not seem to result from low or high in-

cidence of another behavior in the male or the female.

In summary, these parent voles aggressively attempted

to forcetheir mates to stay with the pups in the nest. We

have termed this behavior ‘‘forced baby-sitting.’’

Forced Baby-Sitting in Social Voles 237



DISCUSSION

The observations reported show that one parent, typi-

cally the male, aggressively attempted to force its mate

to stay in the nest with the pups. We suggest that this is

an enforced parental behavior or ‘‘forced baby-

sitting.’’ This can be termed a parental behavior since,

at the least, such dragging results in one parent staying

in the nest with the pups, and staying in the nest (even

without grooming, nursing, or huddling with the pups)

has been previously suggested to be beneficial for theoffspring and thus categorized as parental behavior

(Elwood, 1975; McGuire & Novak, 1984; Solomon,

1993).

The observations did not reveal why the forced

baby-sitting occurred. One possibility is that this was

an overmotivated retrieve, when a parent mistakenly

took its mate for a pup and retrieved it to the nest.

However, forced baby-sitting did not correlate with

retrieving, which characterizes the end of the second

postnatal week. Rather, forced baby-sitting was scat-

tered over the course of postnatal development and did

not correlate with other parental behaviors. Moreover,

forced baby-sitting was most frequent in 2 pairs that

greatly differed in parental behaviors when compared

to the other pairs we studied. For example, 1 pair had a

short duration of lactation whereas the other pair had a

long duration (Libhaber, 2001). Therefore, we could

not find differences in the behavior of the parents that

displayed forced baby-sitting compared to those that

did not. It also is possible that forced baby-sitting was

FIGURE 2 Illustration made from a videotape of a male

(M) pushing the female (F) through the nest entrance (") to

the pups (P). While both parents are outside the nest (1), they

approach each other, and the male grabs the female (2),

pushing her from the side (3) toward thenestentrance(4) and

the pups (5). Then, when the female is crouching above the

pups, the male departs the nest (6).

FIGURE 1 Stills taken from videotaped dragging episode.

Thepups areinsidean overturned ceramic pot (‘‘nest’’) while

the parents are outside. The male (with light ventral fur)

grasps the female in the side of the pelvis (a) and drags the

female toward the nest (b). The male keeps on walkingforward while pulling the female backwards toward the nest

opening (c) where the female is released and stays alone with

the pups (d) while the male left the nest area.

238 Libhaber and Eilam



induced by the offspring, for example, if the pups

emitted ultrasonic calls. Future observations are re-

quired to isolate the stimuli that induce and control this

behavioral pattern.

Parental behavior of the male and the female may

be categorized into direct investment when based on

contact with the offspring, and indirect investment

when based on resource acquisition, maintenance,

defense from predators, and hoarding food (Kleinman

& Malcolm, 1981). A parent may increase either its

own direct investment or indirectly facilitate the

investment of its mate. For example, while the femalenurses the pups, the male may care for the female by

hoarding food and defending the nest (Dewsbury,

1985; Kleiman, 1977; Lonstein & De Vries, 1999;

Oliveras & Novak, 1986; Solomon, 1993; Thomas &

Birney, 1979). In the social vole, the male shares

parental care with the female, as is typical for

monogamous vole species. However, the behavior

reported here is remarkable since it does not follow the

traditional classification to direct and indirect invest-

ment. Rather, it would appear that one parent, typically

the male, physically imposes increased parental invest-

ment upon its mate by ‘‘forced baby-sitting.’’

NOTES

We are grateful to the zoo keepers of the Meir Segals Center

for Ecological Zoology at Tel-Aviv University for main-

tenance of the volecolonies, to Ms. V. Wexller for setting the

Figures, and to Ms. N. Paz for editing this manuscript. This

study was supportedby IsraelScience Foundation Grant 589-

99 to D. E.

Video clips of ‘‘forced babysitting’’ are viewable on

the journal’s website [www.interscience.wiley.com/dev/

suppmat].

REFERENCES

Carter, C. S., & Getz, L. L. (1993).Monogamy andthe prairie

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Dewsbury, D. A. (1985). Paternal behavior in rodents.

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Table 1. Behavior Description and Frequency of Occurrence Per Pair of Voles

Pair No.

Behavior Description Total 1 3 4 8 9 10

Pulling parent The male pulls the female 230 140 1 4 84 0 1

The female pulls the male 9 6 3

Behavior before dragging Puller approached the other parent and 126 75 7 4 38 2 0

dragged it toward the nest

Tugged parent approached the puller and 113 65 0 0 46 1 1

consequently was dragged

Both parents were outside the nest before 54 28 4 4 16 1 1

dragging

Puller in the nest or checked it before pulling 29 18 3 0 7 1 0

Behavior after dragging Tugged parent left the nest after being dragged 142 116 0 0 25 1 0

Tugged parent stayed in the nest 97 24 7 4 59 2 1

Puller left the nest after dragging 161 129 0 4 27 1 0

Puller joined the other parent in the nest 78 11 7 0 57 2 1

Male Female

Correlations* r p r p

Dragging and ‘‘Staying’’ À0.236 0.391 0.582 0.099

Dragging and ‘‘Crouching’’ À0.494 0.175 0.076 0.845

Dragging and ‘‘Retrieving’’ 0.107 0.783 0.185 0.632

Dragging and ‘‘Lactating’’ — — 0.081 0.836

*Correlations are presented for the frequencies of the behavior. Similarly, correlations were measured for the duration of each behavior;

however, none of these correlations was significant (Data not shown.) In addition, there was no correlation between these behaviors in the 2 pairs

with high frequencies (Other pairs were compared separately due to the low incidence.)

Forced Baby-Sitting in Social Voles 239



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240 Libhaber and Eilam

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