David EilamGabi Shefer The Developmental Order ofDepartment of Zoology

Tel-Aviv UniversityRamat-Aviv 69 978, Israel Bipedal Locomotion in the

Jerboa (Jaculus orientalis):Pivoting, Creeping,Quadrupedalism,and Bipedalism

Received 5 January 1995; accepted 11 June 1995

ABSTRACT: This is a brief report on the postnatal development of locomotor behaviorin the jerboa, a bipedal kangaroo-like rodent. Observations on one litter revealed threeintriguing aspects of the postnatal development of the jerboa compared to other rodentspecies: (a) The weaning period is extended, (b) the developmental stage in which pivotingis the main locomotor activity is extended, and (c) locomotor performance is differentlyrelated to anatomical growth. Jerboa pups are born after a long pregnancy compared toother altricial rodents, but possess typical neonate morphology: The hindlegs and forelegsare of the same length, the tail is short, skin pigmentation and fur are absent, and theeyes and ears are closed. However, the neonate jerboa differs from other rodents inposture and activity: Its hindlegs extend laterally to the same side of the pelvis and itcreeps with stepping of only the forelegs that drag the trunk while the hindlegs remainpassive. Pivoting and creeping are preserved in the jerboa for 4 weeks, as compared toa few days in other species. Afterwords, quadruped locomotion emerges and the jerboapup walks while folding its long hindlegs to the same functional length as the forelegs.Bipedal locomotion is acquired only in postnatal Day 47. These observations illustratethat further studies of the development of the jerboa, as well as other bipedal rodentspecies, may provide new perspectives on anatomy, histology, physiology, and motorbehavior during postnatal development. 1997 John Wiley & Sons, Inc. Dev Psychobiol31: 137–142, 1997

Keywords: postnatal development; bipedal locomotion; quadrupedal locomotion; crawl-ing; creeping; pivoting; giant Egyptian jerboa; Jaculus orientalis

Correspondence to: D. EilamContract grant sponsor: Israel Institute for Psychobiology,

Charles E. Smith FoundationContract grant number: 10–96

1997 by John Wiley & Sons, Inc. CCC 0012-1630/97/020137-06

138 Eilam and Shefer

Bipedal locomotion is a specialized mode of loco-motion that is seen in a variety of tetrapods (Chris-tian, Horn, & Preuschoff, 1994; Dagg, 1973;Gambaryan, 1974). Among these there are severalrodent species, including the giant Egyptian jerboa(Jacullus orientalis), a bipedal rodent that resem-bles a kangaroo–rat and features a short and widetrunk with hindlegs six times the foreleg length(Mendelssohn & Yom-Tov, 1987). However, suc-cessful breeding of many wild mammals in captiv-ity is rare, and may occur only under conditionswhich prevent direct observation of the pups. Con-sequently, previous descriptions on the develop-ment of motor behavior in the jerboa or otherbipedal rodents are not available yet for the entireperiod from delivery to weaning. The presentstudy provides a brief report on the postnatal de-velopment of locomotion of the jerboa.

METHODS

Animals

FIGURE 1 Representative postures during the post-Several pairs of jerboas (2–6 pairs, varying withnatal development of the jerboa. Closed eyes are repre-death and further trapping) were kept in the re-sented by an empty circle, and opened eyes by a filledsearch zoo of Tel-Aviv University, each in a 1.5circle. The pup initially lies with both hindlegs to the3 1 3 2 m (length, width, height) cage with asame side of the trunk (Day 1), and maintains this pos-cement floor covered with a 5-cm layer of sand.ture until Day 30. During this period the hindlegs growA nesting box (0.4 3 0.4 3 0.2 m) was placed into three times the foreleg length, but locomotion is based

the cage, and the jerboas built a nest in this box, on foreleg stepping while the trunk and the hindlegsstuffing it with materials that were provided (wool, are dragged passively (Day 30). On postnatal Day 39,straw). The jerboas were fed ad lib with sunflower the hindlegs are flexed underneath the trunk, and theseeds and fresh alfalfa. In 5 years, only one litter pups then switch to quadruped walk and run (Day 41).of 3 pups survived. Five additional litters (2–5 pups On Day 45 they sit on the hindlegs, and then switch to

bipedal locomotion (Day 48).per litter) survived only 1–2 days because of theabsence of maternal care, as frequently occurs inwild species in captivity. Thus, the present obser-vations comprise only 3 pups of one litter. newborns of other rodent species such as rats (Alt-

man & Sudarshan, 1974; Blumberg-Feldman &Eilam, 1994; Eilam & Golani, 1988). Their hind-Procedure and Apparatuslegs were about the same length as the forelegs,

Behavior was observed every other day. For obser- the tail was short, and the skull was elongated, asvation, each pup was gently placed in the center opposed to the wide and short skull of the adultof a 1 3 1 m empty table with 25-cm walls and its jerboa (Figure 1, Day 1). However, their posturebehavior was videotaped continuously for 5 min. was substantially different as compared to otherAfter testing, the lengths of the trunk, hindleg, neonate rodents. Most altricial rodent newbornsforeleg, and tail were measured. first extend their hindlegs laterally, to the left and

the right of the pelvis, in order to prevent tumbling.In contrast, both hindlegs of the jerboa newbornwere aligned laterally to the same side of the trunk,RESULTS AND DISCUSSIONcausing them to tumble frequently. Although thisposture seemed peculiar with the relatively shortThe morphology of the jerboa neonates was sur-

prising, as it was hard to distinguish them from hindlegs of the neonates, it became apparent that,

Bipedal Locomotion in the Jerboa 139

FIGURE 2 (a) Mean length (in mm) of trunk, tail, forelegs, and hindlegs during postnataldevelopment. The righthand data points represent the adult length. As shown, hindleg,foreleg, and tail length are almost the same at delivery. Although foreleg length does notchange much, hindleg and tail length increase extensively. Error bars (SEM) are indiscerniblefor their values. (b) The mean (6 SEM) distance (in m) traversed by the pups in the 5min of observation by crawling or quadruped locomotion (filled diamond) and by bipedallocomotion (open circle). On postnatal Day 38, 1 of the pups traversed 32.5 m, as opposedto only 7.8 and 8.7 m for the other 2 pups.

while the hindlegs are growing rapidly, this posture and pivoting is solely based on alternate steppingof the forelegs to that side.allows them to keep the hindlegs extended later-

ally while the forelegs support the trunk (Figure In the bouts of forward progression, the pupscrept on their forelegs while dragging the hindlegs1, Day 1–30). During these first postnatal weeks

the jerboa pups barely displayed forward progres- that were extended passively (Figure 1, Day 30and Figure 3a). This mode is reminiscent of thesion. Pivoting around the pelvic region (Altman &

Sudarshan, 1974; Eilam & Golani, 1988) was the progression of spinalized animals. Adapted fortheir initial role in dragging the trunk and thetypical activity in the 1st week, until the 4th postna-

tal week when brief periods of forward progression passive hindlegs, the forelegs were well developedin the newborn in comparison with the hindlegs,were observed. The orderly transition from lateral

to forward locomotion was formerly described as tail, and trunk. This was reflected in their length,which in absolute terms had reached almost thethe ground plan for the development of movement

(Eilam, 1995; Eilam & Golani, 1988; Golani, 1992), adult length in 10-day-old pups. This implies thatin relation to body length, foreleg length in pupsbut although in other rodent species the incorpora-

tion of forward movements takes only days, in was greater in comparison to their relative lengthin the adult jerboa (Figure 2a). Thus, the forelegsthe jerboa pups it took 4 weeks. While rodents

typically use forward or backward stepping of the seem to undergo swift development early on, ac-cording to their role in locomotion at this stage.hindlegs in pivoting (Altman & Sudarshan, 1975;

Cools, Scheenen, Eilam, & Golani, 1989; Eilam, Indeed, stepping in pivoting and in creeping com-prises only alternate stepping of the forelegs, and1982; Szechtman, Teitelbaum, Ornstein, 1985), the

hindlegs of the jerboa are sprawled to one side, not the punting or synchronous action which was

140 Eilam and Shefer

FIGURE 3 Three bouts of forward progression at different ages of the same pup, represent-ing the use of only the forelegs (a), of all four legs (b), and of only the hindlegs (c). Eachrow stands for one leg (H 5 hindleg, F 5 foreleg, L 5 left leg, and R 5 right leg). Eachcolumn represents one frame in the videotape (25 frames/1 s; each bout comprises less than2 s). For each leg, 5 represents lift-off, and T represents touchdown. (a) The pup uses onlythe forelegs, and locomotion is relatively slow as indicated by the small number of steps(three steps/leg), and the relatively long (slow) steps. In (b) The pups uses all four legs, withsynchronous stepping of diagonal legs (trot). Locomotion is fast as indicated by the numberof steps (six steps/leg) and their shorter duration. (c) The pup uses only the hindlegs in fastbipedal locomotion.

described in the development of other species mote fast, traversing a respectable distance duringthe 5 min of the observation period (Figure 2b;(Altman & Sudarshan, 1975).

The sprawling posture of the hindlegs was main- Figure 3b). In other words, despite the large differ-ence in foreleg and hindleg length, jerboas weretained for more than 5 weeks. By the end of the

5th week, the laterally extended hindlegs began able to display quadruped walk by folding theirlong hindlegs to a functional length that approxi-to display successive strokes while being dragged

by the forelegs, as if stepping in air. On postnatal mated the foreleg length. This distinction betweenanatomical and functional length was previouslyDay 38, 1–2 days after eyes opening, the pups

flexed the hindlegs to the trunk, placing them un- shown to be critical in the study of the develop-ment of locomotion (Peters, 1983). Starting onderneath the trunk and rotating the hindquarters

to normal posture (Figure 1, Day 39). Once this Day 38, quadrupedal locomotion consisted en-tirely of lateral walk and trot (Dagg, 1973; Eilam,was accomplished, they started to display quadru-

ped walk (Days 39–46). At this stage hindleg 1996; Gambaryan, 1974; Hildebrand, 1989). Bipe-dal walk emerged as late as Day 46, consisting oflength was about three times that of foreleg length,

and the pups encountered difficulty in executing alternate stepping of the hindlegs (Figure 3c).During the first 6 postnatal weeks, jerboa pupsquadruped walk. To overcome this difficulty, they

folded the hindlegs so that the ankle was directed were not able to sit on their hindlegs while groom-ing but, rather, laid down on their back to groom asup, much in the way that crickets fold their long

hindlegs in walk, or the way that bats fold their also described in mutant mice (Coscia & Fentress,1993). This changed on postnatal Day 45, whenforelegs. In this posture, jerboas were able to loco-

Bipedal Locomotion in the Jerboa 141

they sat and groomed with the hindlegs in planti- Great care should be taken in drawing conclu-sions from observations on a single litter of 3 pups.grade posture (Figure 1 Day 45). From this pos-

ture, they embarked upon bouts of bipedal digiti- Nevertheless, the present observations revealthree features of the postnatal development of thegrade progression, which replaced the quadruped

locomotion (Figure 2b). The diagonal posture of jerboa, which seem to withstand a possible littereffect: the lengthy period of development, the pro-the trunk (Figure 1, Day 48), however, still differed

from the adult posture in which the trunk is hori- longation of the pivoting phase, and the possiblerelationship between locomotor performance andzontal (Figure 1, Adult). Whenever standing only

on the hindlegs, the distal part of the long tail that anatomical growth. The present observations areaimed at stimulating the study of the jerboa orfeatures a bushy, black-and-white brush was in

contact with the substrate, providing additional other bipedal rodent species which may have bet-ter breeding success in captivity in order to furthersupport as if it was a third leg. The long tail also

plays an important role in bipedal locomotion examine the ecological, anatomical, histological,physiological, and behavioral perspectives of such(Christian et al., 1994).

In summary, the postnatal development of loco- intriguing postnatal development.motion in the jerboa undergoes several stages: piv-oting, creeping on the forelegs, quadruped walk,

NOTESsitting on the hindlegs, and ultimately shifting tobipedal walk. This pattern has also been observed

We are grateful to Ms. Rona Shulman and Ms. Amirain another litter of the giant Egyptian jerboa (H.Tiran for their help in keeping, videotaping, and analyz-Mendelssohn, personal communication). A remi-ing the behavior of the jerboas, Irit Eilam for drawingniscent order in the usage of limbs was describedFigure 1; Ms. Nomi Paz for editing this manuscript, andin the development of swimming in rodents: Theythe zookeepers of the Meir Segals Center for Ecological

begin by using the forelegs only, then all four legs, Zoology in Tel-Aviv University.and ultimately hindlegs only (Bekoff & Trainer,1979).

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