Noga Libhaber David Eilam The Meir I. Segals Garden for Social Vole Parents Force Zoological Research Department of Zoology Tel-Aviv University Their Mates to Baby-Sit 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 an unfamiliar type of parental behavior in which one parent aggressively forces its mate to stay in the nest 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, this behavioral 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. Published online in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/dev.10075

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

Parental care in animals is conceived of as protecting, mental tool in the study of mating systems, in which nourishing, and nurturing the young (Immelmann & special attention has been directed at voles since Beer, 1989). While parental behavior appears in all different species of voles possess different mating classes of vertebrates and some invertebrates (Klopfer, systems despite their similarity in morphology, anato- 1981), it takes an exclusive form in mammals, in which my, and phylogenetic ancestor (Carter & Getz, 1993). the female produces milk to nourish the pups. Accord- For example, the prairie vole (Microtus ochrogaster) ingly, maternal behavior is vital and obligatory in and the pine vole (Microtus pinetorum) are monoga- mammals whereas paternal behavior is relatively rare, mous whereas the meadow vole (Microtus pennsylva- characterizing less than 10% of mammalian species nicus) is polygamous. In these studies on the mating (Woodroffe & Vincent, 1994). Male investment usually systems in voles, comparison of maternal and paternal varies in correlation with the mating system of a investment has been the main criterion in classifying species, with significant male participation in monoga- the mating system. mous species and minimal participation in polygamous Except for gestation and lactation, components of species (Gubernick & Teferi, 2000; Immelmann & parental behavior of the male and the female may be Beer, 1989; McGuire & Novak, 1986; Oliveras & similarly categorized into direct and indirect invest- Novak, 1986). Paternal investment is indeed a funda- ment (Kleinman & Malcolm, 1981). Direct investment includes huddling with young, grooming and clean- ing them, retrieving them, and carrying or transporting Correspondence to: D. Eilam them. Indirect investment includes resource acquisi- E-mail: [email protected] tion, maintenance and defense, shelter construction Contract grant sponsor: Israel Science Foundation Contract grant number: 589-99 and maintenance, and defending from predators. In addition, while the female nurses the pups, the male ß 2002 Wiley Periodicals, Inc. may care for the female, for example, by bringing food. Forced Baby-Sitting in Social Voles 237

In the present study on the mating system of Guenther’s remained in this cage at all times until the end of social vole (Microtus socialis guentheri), we discover- observations. The first videotaping session took place ed a novel pattern which does not fall under the within the first 24 hr after delivery, and then every other classification of either direct or indirect investment. day until postnatal day 17. Each videotaping session Specifically, we found that one parent, typically the started by removing the bedding material (cloth) and male, tried to increase parental investment by forcing wiping the floor to provide a clear view of the parents its mate to babysit. and the pups. Behavior was then videotaped continu- ously for 40 min (nine sessions total). All observations MATERIALS AND METHODS took place 2 hr before dusk—a time of peak activity in this species (Mendelssohn & Yom-Tov, 1999). Animals The social (Guenther’s) vole (M. socialis guentheri) RESULTS 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 Social voles appear to be monogamous, with extensive green vegetation. Its eyes and external ears are small, participation of the male in parental care and each and its limbs are short (2–3 cm). Ten pairs (male and parent tending to the pups either alone or together with female) of voles were each housed in 120 63 its mate (Libhaber, 2001). However, parents in this vole 45-cm metal cages, which were located outdoors in species were observed not only controlling their own The Meir I. Segals Garden for Zoological Research at direct and indirect investment in parental care but also Tel-Aviv University under natural temperature and attempting to force their mate to stay in the nest with light conditions. Overturned ceramic pots and wooden the pups. In this behavioral pattern, one parent used its boxes were placed in each cage to provide shelter. incisors to grasp the fur of its mate and drag it toward Seeds and diced, fresh vegetables were provided daily. the nest. A sequence of snapshots of this behavioral The animals could therefore receive all their water pattern is shown in Figure 1, and an illustration of requirements form the vegetables. All the animals used another sequence is provided in Figure 2. in the study were in good physical condition and did not As shown in Table 1, of the 10 pairs of voles, this appear to be disturbed. behavior was observed frequently in 2 pairs (140 and 84 times), was less frequent in 4 other pairs (7, 4, 3, and Apparatus 1 times), and was not observed in 4 pairs. The male was usually seen to drag the female, but in 2 pairs the Observations were carried out using a cage (108 female dragged the male. Dragging was initiated when 46 50 cm) with a transparent glass floor, opaque one parent established contact with its mate outside the walls, and an open top. A mirror was tilted underneath nest, apparently independent of which had initiated the cage in a 45-degree angle, providing a bottom view contact. Grasping of the mate was not executed in any of the cage and the insides of the two overturned specific manner, with the tugged parent being pulled ceramic pots used by the voles as a shelter and a nest to from the head, pelvis, or side of the chest and either raise their litter (see Figures 1 & 2). A video camera dragged backwards toward the nest or pushed forward (S-VHS NV-M9500; Panasonic) in front of the cage (Eilam & Libhaber, 2002). In 142 of 239 observations, was used to videotape the behavior of the parents and the tugged parent seemed unaffected and did not pay pups. This arrangement allowed us to observe the be- attention to the pups, but left the nest almost immedia- havior with minimal interference. The parents obvio- tely and consequently was dragged back, until one of usly were larger than the pups, and when they were the parents gave up and stayed with the pups. While crouching above the pups, it was possible to observe being forced to the nest, the tugged parent either re- the pups and their behavior against the background of mained passive or aggressively tried to evade the the parents and their behavior. A cloth (used T-shirt) puller. In a few cases, the tugged individual acquiesced was provided as bedding material. The setup was and completed its own way to the nest after being placed in a quiet, air-conditioned room (25 C) with released in the middle. As shown in Table 1, dragging natural illumination. was not correlated with other parental behaviors, and therefore did not seem to result from low or high in- Procedure cidence of another behavior in the male or the female. A pair of voles was transferred to the observation cage In summary, these parent voles aggressively attempted on the day of delivery, or 1 to 2 days before delivery if it to force their mates to stay with the pups in the nest. We was possible to detect that the female was at term. They have termed this behavior ‘‘forced baby-sitting.’’ 238 Libhaber and Eilam

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 the offspring 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 1 Stills taken from videotaped dragging episode. The pups are inside an 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 walking forward 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.

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 DISCUSSION approach each other, and the male grabs the female (2), pushing her from the side (3) toward the nest entrance (4) and The observations reported show that one parent, typi- the pups (5). Then, when the female is crouching above the cally the male, aggressively attempted to force its mate pups, the male departs the nest (6). Forced Baby-Sitting in Social Voles 239

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* rp r p Dragging and ‘‘Staying’’ 0.236 0.391 0.582 0.099 Dragging and ‘‘Crouching’’ 0.494 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.)

induced by the offspring, for example, if the pups the male, physically imposes increased parental invest- emitted ultrasonic calls. Future observations are re- ment upon its mate by ‘‘forced baby-sitting.’’ quired to isolate the stimuli that induce and control this behavioral pattern. Parental behavior of the male and the female may NOTES be categorized into direct investment when based on contact with the offspring, and indirect investment We are grateful to the zoo keepers of the Meir Segals Center when based on resource acquisition, maintenance, for Ecological Zoology at Tel-Aviv University for main- defense from predators, and hoarding food (Kleinman tenance of the vole colonies, to Ms. V. Wexller for setting the & Malcolm, 1981). A parent may increase either its Figures, and to Ms. N. Paz for editing this manuscript. This own direct investment or indirectly facilitate the study was supported by Israel Science Foundation Grant 589- investment of its mate. For example, while the female 99 to D. E. Video clips of ‘‘forced babysitting’’ are viewable on nurses the pups, the male may care for the female by the journal’s website [www.interscience.wiley.com/dev/ hoarding food and defending the nest (Dewsbury, suppmat]. 1985; Kleiman, 1977; Lonstein & De Vries, 1999; Oliveras & Novak, 1986; Solomon, 1993; Thomas & Birney, 1979). In the social vole, the male shares REFERENCES parental care with the female, as is typical for monogamous vole species. However, the behavior Carter, C. S., & Getz, L. L. (1993). Monogamy and the prairie reported here is remarkable since it does not follow the vole. Scientific American, 268, 100–106. traditional classification to direct and indirect invest- Dewsbury, D. A. (1985). Paternal behavior in rodents. ment. Rather, it would appear that one parent, typically American Zoologist, 25, 841–852. 240 Libhaber and Eilam

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