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Diagonal walking in captive infant vervet monkeys.

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American Journal of Pnmatology 2:211-213 (1982)
BRIEF REPORT
Diagonal Walking in Captive Infant Vervet Monkeys
JACK R. HUROV
Department of Anthropologx The Uriiuerwty of Texas, Austin
The frequency of use of diagonal walking by three motorically immature vervet
monkeys (Cercopithecus aethiops) is discussed. The subjects were housed at
The Balcones Research Center (Austin, Texas) and ranged from 15-105 days of
age. Mixed longitudinal data taken from film indicated that lateral walking was
the first gait employed by the infant vervets studied, but that diagonal walking
completely replaced lateral walking by 81 days of age. These data were compared with those of captive infant Macaca mulatta and feral infant Papio anubis. General agreement was found regarding onset and frequency of use of diagonal walking in the three genera.
Key words: vervet monkeys, lateral walking, diagonal walking, neural regulation of
locomotion
INTRODUCTION
I t has been established that the characteristic walking gait employed by motorically
mature, quadrupedal nonhuman primates is the diagonal sequence [Hildebrand, 1967;
Muybridge, 18871. Diagonal walking is shared by few other tetrapods [Hildebrand, 1967,
19761. I t consists of footfall of a given hindlimb followed by the footfall of the forelimb
on the opposite side of the body. Alternating contacts and noncontacts of diagonal limbs
are conveniently represented by the letters; LH-RF-RH-LF, where L and R indicate left
and right and H and F refer to hindlimb and forelimb, respectively.
Little information is available on the development of diagonal walking in nonhuman
primates. The purpose of this report is to describe several aspects of the ontogeny of
diagonal walking in captive vervet monkey infants (Cercopithecus aethiops) and to compare this information with data reported for infants of feral Papio anubis [Rose, 19771
and captive Macaca mulatta [Hildebrand, 19671.
MATERIALS AND METHODS
Three infant vervet monkeys, one male, (CY) and two females (MN) and (AM) were
filmed at The Balcones Research Center (Austin, Texas)at 15,56-75 and 81-105 days of
age, respectively. Films from each subject combined; the data derived from this temporal
continuum were of the mixed longitudinal type.
Received August 18. 1981; accepted September 8, 1981
Address reprint requests to Jack R. Hurov, Room 336 Rurdine, Department of Anthropology, University of
Texas, Austin, TX 78712.
0275-2565/82/0202-0211$01.500 1982 Alan R. Liss. Inc.
212
Hurov
Filming was done inside a fenced outdoor run 7 m by 14 m. The substrate was a mixture
of clay and loose pebbled aggregate with interspersed grass patches. It presented minimal filming obstructions. The term “locomotor cycle” used here refers to the locomotor
behavior of all four limbs occurring between successive footfalls (foot contact with the
ground) of the LH.
The raw material for this study was 290 ft of 16 mm black and white Tri-X reversal film,
ASA 200, exposed at 48 frames per second. A Paillard Bolex camera fitted with a pistol
grip and Pan Cinor 17-85 mm zoom lens were used. A hand-held Asahi Pentax exposure
meter was used to take light readings. Film was analyzed frame by frame on standard 35
mm microfilm viewers.
RESULTS
At 15 days of age, CY was capable of maintaining himself for brief intervals in a quadrupedal standing posture. Slow progression involved single limb movement but occasionally, diagonal limbs provided bipedal support. All seven locomotor attempts observed
were lateral stepping cycles (LH-LF or RH-RF).
From 56-75 days of age, MN used lateral walking in 6, and diagonal walking in 11 of 17
locomotor cycles filmed. Walk speeds were 0.21-0.48 d s e c (4 records). MN occasionally
altered the order of foot contacts to LH-LF-RF-RH. The body was supported by stable
combinations of three and four limbs, comprising up to 74% and 22% of observed locomotor cycles, respectively
AM consistently used the diagonal walk between 81-105 days of age (9 locomotor cycles). Walk speeds were 0.40 and 0.45 mlsec (2 records).
The earliest walking attempts by infant vervets were not characterized by adult patterns of mid-sagittal body support furnished by adducted diagonal limbs. Infants instead crossed their forelimbs during walking, producing mid-sagittal lines of support
with widely postured hindlimbs. In these postures, the infant’s body rolled and yawed,
which in turn elicited premature lift-off of a forelimb in order to regain mechanical equilibrium.
Altered limb contacts (as defined above) and noteworthy lateral excursion of forelimbs
and hindlimbs during protraction indicated the formative stages of infant walking. As
vervet infants acquired coordination and controlled application of muscular power, they
adducted their limbs nearer to the mid-sagittal axis and reduced lateral excursion of their
limbs during protraction, thus recalling the adult pattern.
DISCUSSION
Reliance on adult walk patterns suggested that AM was motoricdy mature by at least
81 days of age. MN was capable of using the diagonal sequence by at least 58 days of age
but she frequently relied on lateral walking between 58-76 days of age. Variation in
ipsilateral footfall timing within each walk sequence mode (that is, diagonal or lateral)
suggested that she was still in the formative stages of interlimb control.
Mixed longitudinal data derived from film documenting the frequency of use of diagonal walking in infant vervets were in general agreement with those of Hildebrand [1967]
for a captive female infant Macaca mulutta and Rose [1977] for feral Papio anubis infants.
From 14-42 days of age, as the infant macaque gradually gained muscular coordination, lateral walking was characteristically observed. From 52-196 days of age, the macaque relied primarily upon diagonal walking [Hildenbrand, 19673. Infant baboons relied
on both lateral and diagonal walking by 21 days of age [Rose, 19771. Like the baboon
infants, locomotor attempts by infant vervets were limited by maternal restraint and
interference by cage mates.
Lateral walking is the first gait employed by motorically immature C. aethiops and M.
mulutta The lateral sequence walk may be an obligatory locomotor mode with a genetically programmed basis. The program may involve innervation of ipsilateral brachial and
Diagonal Walking in Infant Vervet Monkeys
213
lumbar spinal regions during a premotile stage of embyronic life. This hypothesis is not
intended to imply that diagonal circuits are absent at birth, indeed, they may be present
but remain functionally quiescent until a future life stage [Landmesser, 19761.
Gait ontogeny is a subject inviting further study because most kinesiological investigations of nonhuman primates have relied on motorically mature subjects. We remain ignorant about how and when such locomotor behavior is developed ontogenetically in most
primate taxa. Additional field and laboratory studies are required to determine if other
nonhuman primate infants rely on the lateral sequence walk as a first gait. Future research should seek to elucidate the development of neural circuits that correspond to the
lateral and diagonal stepping sequences observed in nonhuman primates. Are neural
regulatory mechanisms involved in switching from the lateral to diagonal pattern? This
appears to be a problem involving changing patterns of interlimb coordination and the
appropriate order of motoneuron activity [Grillner, 19751. Diagonal neural programs,
once activated, might be superimposed over ipsilateral linkages during ontogeny. How
ever, the fact that motorically mature monkeys sometimes use lateral stepping sequences [Hildebrand, 1967, Hurov, 19791 indicates the plasticity of such
hindlimb-forelimb coordination.
CONCLUSIONS
1. Motorically immature, captive vervet monkeys relied on lateral walking as a first
gait. By 81 days of age, they relied exclusively on diagonal walking.
2. As vervet infants acquired coordination and controlled application of muscular power,
they adducted their limbs nearer to the mid-sagittal axis and reduced lateral excursion of their limbs during protraction.
3. Additional field and laboratory studies should be undertaken to determine if other
nonhuman primates rely on lateral walking as a first gait. Experimental manipulations will be required in order to investigate neural regulation of changing patterns of
interlimb coordination.
ACKNOWLEDGMENTS
I am indebted to Dr. Lawrence Abraham (Department of Physical and Health Education, University of Texas, Austin) for providing the high speed camera used in this study.
Drs. Abraham, Philip Grant and Claud Bramblett (Department of AnthropoloeT, University of Texas, Austin) offered thoughtful comments during the preparation of the manuscript.
This work was supported in part by University of Texas Research Institute Grant SRF835 awarded to Dr. Grant.
REFERENCES
Grillner, S. Locomotion in vertebrates: Central
mechanisms and reflex interactions. PHYSIOLOGICAL REVIEWS 55~247-304, 1975.
Hildebrand, M. Symmetrical gaits of Primates.
AMERICAN JOURNAL O F PHYSICAL
ANTHROPOLOGY 26:119-130, 1967.
Hildebrand, M. Analysis of tetrapod gaits: General considerations and symmetrical gaits. Pp.
203-236 in ADVANCES IN BEHAVIORAL
BIOLOGY, VOLUME 18, NEURAL CONTROL OF LOCOMOTION. R.H. Herman; S.
Grillner; R.S.G. Stein; D.G. Stuart, eds. New
York, Plenum Press, 1976.
Hurov. J.R. Analysis of symmetrical and asymmetrical gaits in a captive group of vervet mon-
keys (Cercopithecus aethiops). M.A. Thesis,
University of Texas, Austin, 1979.
Landmesser, L. The development of neural circuits in the limb movements of the spinal cord.
Pp. 707-733 in ADVANCES IN BEHAVIORAL BIOLOGY, VOLUME 18, NEURAL
CONTROL O F LOCOMOTION. R.H. Herman; S. Grillner; R.S.G. Stein; D.G. Stuart,
eds. New York, Plenum Press, 1976.
Muybridge, E. ANIMALS IN MOTION. New
York, Dover Publications, 1957.
Rose, M.D. Positional behavior of olive baboons
(Pupio anubis) and its relationship to maintenance and social activities. PRIMATES
18~59-116,1977.
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