escape gaits of white-tailed deer, mule deer, and their hybrids: body configuration, biomechanics,...

Escape gaits of white-tailed deer, mule deer, and their hybrids: body configuration, bion~echanics, and function

SUSAN LINGLE Faculty c.f En\ironmental Dc.sign, Urzi\,ersity of Ccrlgcrn, Ccrlgcrry Alter. , Ccrnuclcr T2N I N 4

Received June 5 , 1992 Accepted October 28, 1992

LINGLE, S. 1993. Escape gaits of white-tailed deer, mule deer. and their hybrids: body configuration, biomcchanics, and function. Can. J. Zool. 71: 708-724.

Characteristics of body configuration in the escape gaits of white-tailed deer, mule deer, and their hybrids were examined to evaluate mechanical features of these gaits that pertain to their function. Landing and takeoff angles. angles of limb and vertebral tlexion, and neck and back attitudes were calculated using data digitized from high-speed films. Galloping white- tailed deer had the most horizontally directed flexion in their necks. backs, and forclinibs. Combined with features of limb timing, the summation of velocities of these body segments results in a faster gallop for white-tailed deer than for galloping mule deer and hybrids. Stotting mule deer attain considerable horizontal velocity which may be conserved between strides. The bound. used by hybrids. appears to be a slow and mechanically inefficient gait for deer, primarily due to bioniechanical factors stemming from the coupled forelimb landing and associated steep body position. These limitations prcscnt the possibility that hybrids have ineffective responses to predators, which could lower their viability relative to that of white-tailed and mule deer.

LINGLE, S. 1993. Escape gaits of white-tailed deer, mule dcer, and their hybrids: body configuration. bionicchanics, and function. Can. J. Zool. 71 : 708-724.

Une comparaison des caracteristiques de la configuration du corps pendant les allures de fuite chez le Cerf de Virginie, le Cerf mulet et leurs hybrides a permis de mettre en relation les traits inecaniques de ces allures avec leur fonction. Les angles de chute et de depart, les angles de flexion des menibres ct des vertebres, ainsi que les positions du cou et du dos ont kt6 calcules B partir de donnees digitalisees tirees de films B haute vitesse. Le Cerf de Virginie au galop a la flexion du cou, du dos et des membres anterieures la plus orientee vers I'horizontale. La sommation des vitesses de ces parties du corps, combinee au reglage precis des mouvements des membres. donne au Cerf de Virginie une vitesse de galop plus grande que celle des deux autres groupes. Le Cerf iiiulet atteint des vitesses horizontalcs considerables, qu'il peut reussir B conserver entre les pas. Le bond, utilise par les hybrides, est une allure lente et peu efficace mecaniquement chez le cerf, principalement a cause de hcteurs biomecaniques dus aux membres anterieurs qui touchent le sol simultanement et B un fort angle du corps. Ces restrictions peuvent amcner les hybrides B avoir des reactions de fuitc inefficaces face aux predateurs et diminuent leur viabilite par comparaison aux cerfs de Virginie et aux cerfs niulets.

[Traduit par la redaction]

Introduction

The security behavior of white-tailed deer (Odocoileus virginianus) and mule deer (0 . hemionus) is one of the largest differences between these closely related species (Geist 198 1 ) . Whether captive-born or free-ranging, Alberta white-tailed deer (0 . v. dacotensis) gallop when most alarmed, whereas Rocky Mountain mule deer (0 . h. hemionus) stot (Lingle 1992). Hybrids, having white-tailed or mule deer mothers, tend to bound. These results indicate that differences between the gaits of white-tailed and mule deer have a genetic basis, and so may have evolved in response to different selective pressures.

Information on limb coordination was used to identify the gaits used by each type of deer (Lingle 1992). Some conclu- sions regarding the mechanics and adaptive value of a gait can be drawn from patterns of limb timing, but movements within the body or movement of the body in relation to the substrate need attention before these evaluations are taken very far. The same footfall pattern can be used to very different ends, depending on the trajectory of the body or its segments. Close examination of escape behavior is rarely used as a tool in ethology, despite widespread interest in antipredator behavior and the function of unusual movements such as stotting.

This paper compares aspects of body configuration in common escape gaits of white-tailed deer, Rocky Mountain mule deer, and reciprocal F, crosses, all from Alberta. Information on limb coordination (after Lingle 1992) is integrated with these results to evaluate opportunities for function conferred

by the mechanics of each gait. If hybrid gaits have mechanical disadvantages, these limitations may result in ineffective responses to predators in the deer's natural habitat. Hybrid inviability, due to inappropriate security behavior, could serve to restrict genetic exchange between white-tailed deer and mule deer. However interbreeding affects the behavior of hybrid progeny, it could affect populations of white-tailed and mule deer, for hybrids have been reported throughout the zone in which these species are sympatric (Oceanak 1977; Wishart 1980; Gavin and May 1988; Stubblefield et al. 1986; Derr 199 1). Hybrids are physically viable in captivity and females, but not males, are fertile (Wishart et al. 1988).

Methods

Subjects, study areas, and methods used to film deer gaits are described in detail elsewhere (Lingle 1992). In summary, the main subjects included two adult females and one adult male of the following types: white-tailed deer, mule deer, F l hybrids with white-tailed deer mothers (hybrid I ) , and Fl hybrids with mule deer mothers (hybrid 2). The animals were housed in a 1.6-ha enclosure owned by The Calgary Zoo. Data on body configuration were also obtained from films of a 5-month-old hybrid 1 born into the main group and an adult hybrid 1 born after the main study was concluded. Two adult and five juvenile mule deer from The Calgary Zoo's permanent deer pen were also filmed. All animals were raised in captivity.

Filming In the main enclosure, an assistant led a leashed dog into the pen to

induce the deer to flee down a 56 x 8 m "runway," which opened Pr~nt td In Canada I Ir~ipr~mt: au Carlada

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

LINGLE 709

into a large field at the end. The assistant and the dog chased the sub- ject for a few seconds until it moved through the filming area. which began 25 m into the runway. A Super-8-mm (at 150 framesls) or a 16-mm (at 64 framesls) camera was set outside the filming area to capture a lateral view of the deer. Trials were spread out to minimize the possibility of either harassment or habituation (for details see Lingle 1992). In The Calgary Zoo mule deer pen, an assistant (with no dog) herded the deer along a fence past the Super-8-mm and 16-mm cameras.

Whereas hybrids usually galloped in the runway, they tended to bound when alarmed by stray dogs that wandered near the pen (Lingle 1992); bounding hybrids were therefore filmed by panning the camera after them.

Film and data analysis Film images of deer were analyzed by identifying points on a deer's

body that could be digitized. The digitized data were used to calculate body angles. These measurements were used to compare characteristics of body movement for the different types of deer or for deer using different gaits.

Selection of body points Twenty-one points approximating particular joints or landmarks on

the deer's body were identified for use in measuring body angles (Fig. l a ; section A in the Appendix). It was important to select body points that were identifiable throughout an animal's range of motion. In some cases, a point was shifted from the skeletal feature under examination to a more visible location, but only when the alternative site adequately represented the character under examination. For example, the caudal end of the calcaneus was selected rather than the site of joint movement, the astragalus. Even though shifting a point affects measurement of an angle, measurements of all subjects would be similarly affected.

Differences between deer and more traditional subjects of movement studies influenced the selection of points. Skeletal features and muscular contours are in many cases less visible on long-haired animals like deer than on humans and horses. Researchers of human and domestic animal gaits can mark the skin or shave the fur of their subjects with ease (Fredricson and Drevemo 1971; Fredricson et al . 1972; Goslow eta l . 1973; Grieve et al . 1975; Deuel 1985) to enhance consistency when identifying points from one film frame to the next, and consistency among different persons who may analyze the films.

There are some drawbacks to using skin markers. They introduce a source of error insofar as skin movement varies from movement of skeletal structures that the markers are intended to represent (Fredric- son et al. 1972; Deuel 1985; van Weeren et al . 1988). Skin displacement over limb joints is more pronounced proximally (van Weeren et al. 1988). It is possible that certain proximal body sites can be identified more reliably by a trained eye than by using markers.

Digitizing films A 16-mm or Super-8-mm image analyzer was used to project film

images onto a digitizing table. Selected body points were digitized from one of every five frames (with 150 framesls film) or one of two frames (with 64 framesls films) in a sequence of film that represented one stride. In addition, film frames corresponding to the landings and takeoffs of the fore and hind limbs closest to the camera were digitized.

A computer program was developed to plot a set of "stick" deer representing the motion of an animal throughout each stride (Fig. 2). The computer program was then extended to calculate landing and takeoff angles, angles of limb and vertebral flexion, and neck attitude.

Landing and takeofl angles Landing angles of limb segments (Fig. 16) were measured from the

first film frame that showed a limb touching the ground following a suspension. Takeoff angles were measured from the last frame before a limb left the ground. Landing and takeoff angles were calculated for limbs closest to the camera. A known level line was visible in the film images on a grid stationed behind the deer. Two predetermined points on this line were digitized from each film frame. This reference line

was used in calculations of landing and takeoff angles (and neck and back attitude).

Angles of body configuration were measured for the purpose of comparing the gait groups involved in this study. The qualitative ways in which angle values were affected by the selection of points were considered (section B in the Appendix). These considerations may be useful for comparing the results with those from other studies.

Angles of limb jlfleuion Fle.uion is defined as movement that results in a decrease in the dis-

tance between adjacent longitudinal axes. Extension results in an increase in distance between these axes. Flexion around two joints on the forelimb and two joints on the hind limb were measured (Fig. 1c) (see section C in the Appendix for measurement considerations). Maximum values correspond to maximum extension; minimum values represent maximum tlexion. The excursion of an angle during one stride was calculated by subtracting the minimum from the maximum value.

Angles of vertebral jlexion and neck and back attitude Vertebral flexion was examined by measuring angles formed along

the animals' dorsal contour. When part of the spine bends forward, the movement is considered flexion. When the motion is backward, it is defined as extension. Maximum, minimum, and excursion of vertebral angles were calculated for each stride.

Sites of sacrolumbar and lumbar-thoracic articulation are not read- ily visible from films of deer, as would be necessary to distinguish lumbar from thoracic flexion precisely. Instead, movement in the lower back was distinguished from overall vertebral movement (Fig. Id). Muscular definitions on the body provided the points used in these measurements, although point 14 was identified as the midpoint between 13 and 15. Muscles may accentuate the external shape of the animal, so the measured angles may exceed the amount of flexion or extension that is actually accomplished by skeletal movement.

Neck attitude (Fig. 14) was calculated to determine neck positions during a stride; maximum, minimum, and excursion were calculated for each stride. A point on the dorsal outline of the deer (Fig. le, point 16) was used as the base of the neck for this calculation. Using this point would make values for neck attitude smaller than if a more ventral point, closer to the cervical vertebrae, were used.

The back attitude of galloping animals appears to be lowest about the time that the leading forelimb lands, and highest about the time the trailing hind limb departs from the ground. Back attitude (Fig. le) was measured at these two times, as well as when the trailing forelimb landed and as the leading hind limb departed from the ground.

During stotting, back attitude was measured as the first limb landed. as the forelimbs departed from the ground, and as the hind limbs departed. Back attitude of bounding hybrids was measured at landing and takeoff of both fore and hind limbs. Rather than adjust the computer program for these calculations, back attitude during galloping and stotting was measured with a protractor from the series of stick deer (Fig. 2). Consequently, this angle was measured from the same digitized points that were used in the computerized calculations of other angles.

Back attitude was occasionally measured directly from films of bounding hybrids that travelled laterally to the camera. I do not consider these measurements to be as accurate as those made of gait groups, but they provide initial information on body movements in the hybrid bound.

Digitizing error Film resolution, body proportions, and the position of an animal all

affect the ease with which body sites can be identified. It is important to examine measurement error from film images that vary in these respects. Ten film frames, varying in the ways mentioned, were each digitized 5 times to measure digitizing error. (After three of these frames were digitized 10 times each, it was evident that the range of values did not increase past the fifth measurement.)

Angles of limb and vertebral flexion were calculated from these

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

7 10 CAN. J . ZOOL. VOL. 71. 1993

FIG. 1 . Method of measuring body configuration. (a ) Points digitized for use in measurements, with resulting "stick" deer inside silhouette. See A in the Appendix for identification of points. (6) Landing and takeoff angles. h , horizontal. Landing angles were calculated by using horizontals caudal to the limb. Takeoff angles were calculated by using horizontals cranial to the limb. Landing angles are depicted for the forelimb and takeoff angles for the hind limb, but both were calculated for fore and hind limb segments. Arrows indicate increasing angles. (c) Angles of limb flexion. Arrows indicate extension and increasing values. Maximum values (maximum extension), minimum values (maximum flexion), and excursion of angles were used for comparing gait groups. ( d ) Angles of vertebral flexion. For explanation see c. ( e ) Neck and back attitude. h , horizontal. Arrows indicate increasing angles. Maximum, minimum, and excursion of values were used for comparing neck attitude. Back attitude was measured at selected limb landings and departures (see text).

19

(b)

(c)

Upper forelimb

Carpus- y 7

(dl

Overall back

.

(el

Neck attitude

Back attitude

')h

')h

"

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

FIG. 2. A series of "stick" deer generated by digitizing film images of a stotting mule deer. Dots represent left hooves. Numbers represent film frames (shot at 150 framesls) that were digitized. Frame 77 is included with frame 1 because they represent the same stage of successive strides.

repeated measurements and then plotted on scatter diagrams. Individ- ual measurements were distributed relatively equally within the range of values, indicating that error was unlikely to be biased. The range

and standard deviation of each set of five measurements were determined for each angle and averaged over the 10 data sets (Table 1). It was assumed that the amount of error in calculations of landing and

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

CAN. J . ZOOL. VOL. 71. 1993

TABLE 1. Digitizing error sis. Bullock (1982) found that takeoff and landing angles of the

Angle Mean SD

Tarsus 5.4 2.2 Stifle 6.2 2.6 Hip 7.6 3.6 Carpus 6.6 3.0 Upper forelimb 9.4 4.0 Lower back 6.6 2.5 Overall back 6.6 5.5

NOTE: The range (mean + SD) of limb and vertebral angles was calculated from five repeated measurements of 10 film frames.

takeoff angles was relatively similar to measurement error calculated for tarsus and carpus angles, because the same body sites were used for these calculations.

Sampling design The animals travelled a path perpendicular to the camera in films

that were made in the runway and in the mule deer pen at The Calgary Zoo. This filming angle allowed a lateral image of the deer to be digitized and measurements of body configuration to be made from these images. Although the deer use other gaits at times (Lingle 1992), body configuration was examined from films of their primary escape gaits: the four gallops (white-tailed deer, N = 7; mule deer, N = 9; hybrid 1, N = 15; and hybrid 2, N = 8) and the mule deer stot (N = 8). Because bounding hybrids were filmed by panning the camera, only limited measurements of body angles were made (e.g., back attitude, N = 6), and these only when the deer were filmed from a lateral viewpoint.

Visual and statistical comparisons showed that, unlike data on limb coordination, those on the body configuration of fawns differed from those collected from adult animals for the four gallops and the stot. Data on fawns were excluded from the adult gait groups. Stotting mule deer fawns were analyzed as a distinct gait group (N = 6).

No differences were detected between characteristics of body flexion for individual animals, including females and males: however, few films were made of males with large antlers. It is possible that the inflated necks and large antlers of rutting males affect their gait. One large mule deer carried his neck lower than other mule deer, but this was an isolated measurement. Individual variation is more apparent in alarm responses like tail flagging.

One goal of the study was to compare the gallops of purebred deer with each other and with the mule deer stot. Another goal was to compare the gallops of hybrids with the gallops of purebred deer. Sepa- rate Kruskal-Wallis tests were made for these two comparisons. Dunn's multiple comparison procedure (Zar 1984) was used for appropriate pairwise comparisons. The two-tailed Mann-Whitney test was used to compare data gathered for adult and juvenile stotting mule deer, and to compare the back attitude of bounding hybrids and stotting adult mule deer.

The small sample size, novelty of measurement techniques, and pooling of a small number of repeated measurements introduced experimental limitations (for more details see Lingle 1992). Differ- ences indicated by the statistical results were evaluated by reviewing films and by considering whether these features were consistent with other gait characteristics. The results are interpreted as indicating the direction of the relative differences between deer gaits rather than as precise numerical values that can be extended to wild deer populations.

Results: characteristics of body configuration

Detailed measurements were needed to build an understanding of the sequence of movement in each gait and to evaluate its mechanical capabilities.

Gallops that varied in speed were included in the gait analy-

- - limbs of galloping pronghorns became more acute at greater speeds. It is assumed that the range of angles measured from deer was larger than it would have been if the animals had travelled at more similar speeds when filmed. Unless otherwise specified, the mule deer stot is that of adult animals.

EfJhct of lirzzb order Data collected from leading and trailing limbs were distin-

guished to determine how limb order affects landing and takeoff angles and angles of limb flexion. Scatter diagrams as well as two-tailed Mann-Whitney comparisons were made to compare angles formed by leading and trailing limbs.

The vast majority of strides that were digitized had right hind leads, including 5 of 7 strides for white-tailed deer, 8 of 9 for mule deer, 12 of 15 for hybrid 1 's, and 5 of 6 for hybrid 2's. This meant that the leading hind limb and trailing forelimb were usually digitized, because the right side of the animal was filmed in all trials except one. Because so few trailing hind limbs and leading forelimbs were digitized, data for the four types of deer were combined to evaluate the effects of limb order on limb angles. Emphasis was placed on identifying the direction of differences that exist.

In respect to landing and takeoff angles, the largest difference was in the forelimb takeoff: trailing limb angles tended to be smaller than leading limb angles (Table 2). Hind-limb data for takeoff angles differed in the same direction, but the difference between leading and trailing limbs was small.

Conversely, leading fore and hind limbs formed smaller mean landing angles than did trailing limbs (Table 2). Gam- baryan (1974) also reported this tendency. Differences were negligible in the forelimb and only attained significance in the tibia.

Regarding limb tlexion, the leading forelimb tended to extend more (larger maximum values) and flex less (larger minimum values) than did the trailing forelimb (Table 2). Only differences in the upper forelimb extension attained significance. The extension of hind-limb segments was similar between trailing and leading hind limbs. Leading hind limbs, however, underwent more flexion (smaller minimum values) than did trailing limb segments.

Differences between leading and trailing limbs will be considered when pertinent to the following results. Inasmuch as the proportion of leading to trailing limbs was the same for each of the four groups, these differences should not have biased the results. The differences are, however, important to consider when comparing the results with those obtained from other studies.

Landing and takeof angles No significant differences were found among the landing

and takeoff angles of the four limb segments for the gallops of white-tailed deer, mule deer, and hybrids (Table 3) . Galloping mule deer had slightly larger average landing and takeoff angles for most limb segments. Considering the greater vertical displacement found elsewhere in the bodies of galloping mule deer, e.g., the forelimb, hip, and back attitude (see below), it is surprising that there was not a larger difference between the landing and takeoff angles of galloping white- tailed and mule deer.

Bullock (1982) found that fore and hind limb departure angles became smaller and more similar at greater speeds. Landing angles of the deer in this study were similar to those of pronghorns travelling at moderate to fast canters. The

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

LINGLE

TABLE 2. Effect of limb order on landing and takeoff angles and on angles of limb tlexion in the gallops of deer

Leading limb (deg.) Trailing limb (deg.)

Mean k S D N Mean f S D N Z P

Landing Metacarpals Radius and ulna Metatarsals Tibia

Takeoff Metacarpals Radius and ulna Metatarsals Tibia

Limb flexion Carpus

Minimum Maximum Excursion

Upper forelimb Minimum Maximum Excursion

Tarsus Minimum Maximum Excursion

Stifle Minimum Maximum Excursion

Hip Minimum Maximum Excursion

"Two-tailed Mann-Whitney comparison: *, P < 0.05: **. P < 0.01: ***. P < 0.001

departure angles of deer were much larger than those of pronghorns, even though the large proportion of trailing forelimbs measured should have resulted in smaller angles than if more leading forelimbs had been measured.

Although the takeoff angles of the metatarsals were somewhat elevated because the calcaneus was used as the proximal point, this would not account for the large differences between these and Bullock's results. Greater extension around the tarsus, flexion in the stifle, or plantar flexion in the digits must have caused the pronghorn's limbs to form smaller angles with the ground at limb departure than were recorded in deer. Per- haps this difference reflects an anatomical difference between deer and pronghorns.

No differences were detected between the landing angles of the mule deer stot and the gallops of the purebred deer (Table 3). Landing angles appeared to be influenced by diverse factors, such as: (i) absorbing forces of impact; (ii) providing support during contact; (iii) maintaining momentum; and (iv) positioning the limb so that it may exert force over a rea- sonable distance before departure. Inasmuch as the landing angles of the different types of galloping and even stotting deer were similar, it may be that biomechanical factors that influence landing angles are shared by these animals despite other differences in their gait.

The average takeoff angles of all four segments were larger for stotting than for galloping deer; however, this difference

only approached significance in the metacarpals, perhaps because of the large variation in the takeoff angles of stotting deer (Table 3). Given that the forelimbs of stotting deer visually appear more obtuse at takeoff, replicating these measurements would be worthwhile (see Fig. 4 for an illustration of galloping and stotting deer).

Mule deer fawns that stotted had obtuse fore- and hind-limb takeoff angles which resembled those of stotting adult mule deer. The limb landing angles of stotting fawns, unlike those of adults, exceeded the landing angles of galloping purebred deer. except for the tibia. Stotting mule deer fawns differed significantly from stotting adults in the landing angle of the metacarpals (P < 0.02). The difference in landing angles between fawns and adults could be an effect of body size or a matter of developing coordination through physical maturity or experience.

Placement of the trailing hind limb a t landing The most gathered body position of the white-tailed deer

gallop occurs when the leading forelimb departs from the ground and the trailing hind limb lands. Regardless of whether a gathered suspension occurs, the trailing hind limb of white- tailed deer tends to cross lateral and cranial to the spot where the leading forelimb is or had been in contact with the ground (Table 4).

The most gathered position of mule deer and hybrids also

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

7 14 CAN. J . ZOOL. VOL. 71. 1993

TABLE 3. Landing and takeoff angles (in degrees) of limb segments in the gallops of white-tailed deer, mule deer, and hybrids, and in the mule deer stot

Gallop Mule deer stot Kruskal -Wallis H-value

Mule deer Hybrid I t - Hybrid 2$ Adults Fawns White-tailed deer (N = 9. (N = 15, (N = 6. (N = 8. (N = 6, Adult purebred Adult Mann-Whitney (N = 7, 11 = 3) n = 5) 11 = 4) 11 = 2) t l = 5) 11 = 4) gaits$ gallops(( U-value1

Metacarpals Landing 52 + 10 57+8 50+5 53+6 50+8 62+7 1 .724 4.949 6.0 Takeoff 53 +5a 53+10u 53+6 48+7 64+1IO 68+9 6.646" 2.347 16.0

Radius and ulna Landing 41 + 10 45f6c 36+7d 43+5 44+9 52+8 0.823 8.566" 11.5 Takeoff 73 +5 79+9c 71+5 69+6d 85+11 86+4 4.552 8.054" 22.5

Metatarsals Landing 39+5 41+12 38+5 37+10 43+9 52+8 0.55 1 0.483 9.5 Takeoff 67 $6 70+7 67+3 66+6 72+13 75+14 0.997 1.586 19.0

Tibia Landing 115+ 12 117+11 111+7 110+6 11015 116+8 1.855 2.299 16.0 Takeoff 16+8 16+7 17+6 8+3 22+I i 21+15 2.001 7.745 22.5

NOTE: Angles are given as the mean + SD. N is the number o f strides and 11 is the number of individuals; N = 8 t'or the lnule deer gallop for nletacarpals and for radius and ulna landings: N = 5 li>r the hybrid 2 gallop for nletatarsals and tibia takeoffs. Within row\. (1 and h tlenotc. differences that cy~pr.oclc.lr .si~ri(fic~orrc~c~ ( P < 0 .10) I'or pairwise comparisons between the gaits ol'adult purebred deer. No pairwlae comparisons between the gaits of adult deer attained s~gnificance. Wlthln rows. t. and tl denote d~l'lkrences that upprout.h six- n$t.ance ( P < 0.10) for pairwise comparisons between gallops ol' adult deer.

* P < 0.05. PF, hybrid with white-tailed deer mother. $F, hybrid with mule deer mother.

#x;~ oS.21 = 5.591.

Ix;00~.,, = 7.815. TComparison between stotting adult and juvenile mule deer.

TABLE 4. Placement of the trailing hind limb at landing by galloping white-tailed deer, mule deer, and hybrids

Distance White-tailed Mule Hybrid Hybrid Position (cm) deer deer 1 2

Cranial > 24 3 0 0 0 10-24 4 0 0 1 1-10 0 1 3 1

Adjacent 0 1 0 0 Caudal 1 - 10 0 5 9 5

> 10 0 1 0 0

NOTE: The position and distance (in the cranial-caudal direction) of the hoof of the trailing hind limb are described relative to the spot where the leading forelimb contacted the ground. The distance was estimated from films, using the deer's distal l ~ l n b segments for scale. The hind limbs were placed lateral to the ipsilateral forelimbs.

occurs when the trailing hind limb lands; at this time, the trailing forelimb has usually left the ground but the leading forelimb is often in the middle of its step. Mule deer tend to place the trailing hind limb lateral and caudal to the spot where the leading forelimb contacts the ground (Table 4).

Hybrids are more similar to mule deer than to white-tailed deer in this respect (Table 4). The trailing hind limb usually lands lateral and caudal to the leading forelimb. In a few trials, hybrids set this hind limb down slightly cranial (1 - 10 cm) to the leading forelimb.

Limb flexion The largest differences among the limb flexion of the gait

groups were found in the proximal limb sites, the upper forelimb and hip (Table 5). The upper forelimb measurements may have differed more than the carpus measurements as a

and scapula, for movement of all three segments can affect measurement of upper forelimb flexion (section C in the Appendix).

The forelimb is almost fully retracted as it departs from the ground in the gallops. Galloping deer usually push the forelimb more caudally upon limb departure, resulting in maximum extension of the upper forelimb at that time. Stotting mule deer had the greatest extension of the upper forelimb (mule deer stot x mule deer gallop, P < 0.002), despite no additional retraction after takeoff. This result appears to be an artifact of the stotting mule deer's forebody orienting upward at forelimb departure. At that time, the point on the dorsal surface used as the proximal point of the upper forelimb angle (Fig. lc, point 15) is more caudal to the limb than it is during the forelimb departures of galloping deer.

White-tailed deer had the largest amount of flexion (smallest minimum angles) in the carpus and upper forelimb, whereas stotting mule deer had the least flexion in these angles (white- tailed deer gallop x mule deer stott: carpus minimum, P < 0.05; upper forelimb minimum, P < 0.001). Of the galloping groups, mule deer had the least flexion in the lower and upper forelimb (white-tailed deer x mule deer, P < 0.05 for upper forelimb minimum). Values for hybrids tended to be intermediate, although the minimum upper forelimb measurements for hybrid 2's were similar to those of mule deer (Table 5).

Maximum extension in the carpus and upper forelimb was slightly larger for the white-tailed deer gallop than for the other gallops. Combined with their pronounced forelimb flexion, galloping white-tailed deer had a greater excursion of both forelimb angles than did galloping mule deer ( P < 0.005 for upper forelimb excursion). Hybrids were again intermediate but more like mule deer. Stotting mule deer had notably

resilt of the summed action of the radius and ulna, humerus, limited excursion in the carpus compared with the galloping

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

TABLE 5. Angles of limb flexion (in degrees) in the gallops of white-tailed deer, mule deer, and hybrids, and in the mule deer stot

Gallops Mule deer stot Kruskal -Wallis H-value

Mule deer Hybrid 1 Hybrid 2 Adults Fawns White-tailed deer (N = 9, (N = 15, (N = 6, (N = 8, (N = 6, Adult purebred Adult Mann-Whitney ( N = 7 . n = 3 ) n = 5 ) n = 4 ) n = 2 ) n = 5 ) n = 4 ) gaits? gallops$ U-value$

Carpus Minimum Maximum Excursion

Upper forelimb Minimum Maximum Excursion

Tarsus Minimum Maximum Excursion

Stifle Minimum Maximum Excursion

Hip Minimum Maximum Excursion

-- -- --

NOTE: Angles are given as the mean SD. N ix the number of strides and n is the number of individuals; N = 7 Ibr the maxinlunl and excursion of the tarsus for the adult mule deer stot. Within rowx, u and h denote significant differencex ( P < 0.05) for pairwise comparisonx between the gaits o f adult purebred deer. Within rows, (. and (/denote significant differences ( P < 0.05) for pairwise comparisons between gallopb of adult deer.

* P < 0.05; **. P < 0.01; ***. P < 0.001. t y f ,,,,,,,, = 5.591. ~ X ~ , , 0 5 , 3 1 = 7.815. $Comparisons between stotting adult and juvenile mule deer.

groups, because there is little flexion of this joint (white-tailed deer gallop x mule deer stot, P < 0.02).

These differences indicate that galloping white-tailed deer raise their forelimbs closer to their chest and protract their forelimbs more horizontally during forelimb recovery than do galloping mule deer or hybrids. The forelimbs of stotting mule deer follow a trajectory farther below their body during recovery.

The differences among hind-limb values were larger for the hip than for distal sites, even though the range of motion in the hip is much smaller. Maximum hip extension of galloping and stotting deer occurs after departure of the leading hind limb (or both limbs in the case of stotting deer). White-tailed deer had the smallest angles of hip extension (Table 5 , maximum values) and differed significantly from galloping mule deer and hybrids in this characteristic (white-tailed deer x mule deer, P < 0.002; white-tailed deer x hybrid 2, P < 0.001 ; white-tailed deer x hybrid 1, P < 0.01). White-tailed deer had more flexion, on average, in their hips than did the other groups, but this difference did not attain significance.

Rather than being intermediate, tarsus flexion and hip extension and excursion were more extreme in hybrid 2's than in either parent and neck attitude showed the same tendency. It would be necessary to conduct trials with more animals to sub- stantiate these results. One subjective observation may bear on this. Hybrid 2's tended to delay fleeing from the dog (S. Lin- gle, in preparation). Films show them in positions that could be construed as showing panic, with the head lowered to an

extreme degree. Perhaps their slow departure affected their level of excitement and their gait form.

Vertebral flexion No differences were found among angles of vertebral flex-

ion for the gaits of adult purebred deer, although mule deer fawns had a somewhat larger range of motion in their backs than did stotting adults (Table 6).

Hybrid 1's had small values for flexion and extension of the lower back (Table 6). There is no corroborating evidence, from other body sites or reviews of films, that hybrids differ from purebred deer in these respects. It is possible that a characteristic of their external morphology led to a discrepancy in the manner of digitizing the lower back between hybrids and purebred deer. For these reasons, values for vertebral movement in hybrids are viewed cautiously.

Neck and back attitude One of the largest differences in body configuration occurred

among measurements of neck attitude, maximum values for galloping white-tailed deer being similar to minimum values for stotting mule deer (Table 6). Maximum and minimum measurements differed significantly between these groups ( P < 0.02 and 0.002, respectively). Galloping mule deer were intermediate but did not differ significantly from white-tailed deer or stotting deer, perhaps because of the large variation in their measurements. Values for hybrids were more similar to those for white-tailed deer than to those for mule deer,

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

716 CAN. J . ZOOL. VOL. 71. 1993

TABLE 6. Angles of vertebral flexion and neck attitude (in degrees) in the gallops of white-tailed deer. mule deer, and hybrids, and in the mule deer stot

Gallop Mule deer stot Kruskal -Wallis H-value

Mule deer Hybrid 1 Hybrid 2 Adults Fawns White-tailed deer (N = 9, (N = 15, (N = 6, (N = 8, (N = 6, Adult purebred Adult Mann-Whitney (N = 7. n = 3) n = 5) tz = 4) n = 2) t7 = 5) n = 4) gaitst gallops$ U-value$

Lower back Minimum Maximum Excursion

Overall back Minimum Maximum Excursion

Neck attitude Minimum Maximum Excursion

NOTE: Angles are given as the mean i SD. N is the number of strides and n is the number of individuals; Within rows. cr and h denote significant differences ( P < 0.05) for pairwise comparisons between the gaits of adult purebred deer. Within rows. c and ( 1 denote significant differences ( P < 0.05) for pairwise comparisons between gallops of adult deer.

* P < 0.05; **, P < 0.01.

= 5.591.

~ ~ ; [ ) . [ ) 5 , 3 ~ = 7.815. #Comparisons between stotting adult and juvenile mule deer.

TABLE 7. Back attitude (in degrees) at selected limb landings and departures in common gaits of white-tailed deer, mule deer, and hybrids

Gallop Mule deer stot Mann - Whitney U-value

White-tailed deer Mule deer Hybrid 1 Hybrid 2 Adults Fawns Hybrid 1 bound (N = 7, (N = 9, (N = 14, (N = 6, (N = 8, (N = 6, (N = 6, Kruskal-Wallis Adults vs. Stot vs. n = 3) n = 5 ) n = 4 ) n = 2 ) n = 5 ) t 7 = 4 ) n = 4) H-valuet juveniles$ bound$

Landing 1 - 3 f 5 - 1 - 4 f 4 - 3 f l Of2 - 3 f 1 -12f2 3.130 10.0 O.O*** 2 - 7 f 4 - 7 f 7 - 9 f 3 - 5 f 3 na na - 9 f 4 3.638 na na

Takeoff 1 5 f 4a 10f3b 7 f 3 8 f 1 8 f 4 7 f 3 l l f 3 10.800* 23.0 13.000 2 - 1 f 2 a 5 f 4 b Of3 l f 3 1 0 f 4 11f4 1 4 f 5 9.595* 22.0 16.000

Excursion 11f3 16f 5 16f5 1 3 f 3 11f4 14f3 2 6 f 7 6.339 12.0 O.O***

NOTE: For gallops, "landing I " refers to the trailing forelimb landing. "landing 2" to the leading forelimb landing. "takeoff I " to the trailing hind limb takeoff, and "takeoff 2" to the leading hind limb takeoff; "excursion" is takeoff 1 minus landing I . For mule deer stots. landing I refers to landing of the first limb. takeoff I to forelimb takeoff, and takeoff 2 to hind-limb takeoff; excursion is the larger of the two takeoff values minus landing I . For the hybrid bound, landing I refers to the forelimb landing, landing 2 to the hind-limb landing, takeoff 1 to forelimb takeoff. and takeoff 2 to hind-limb takeoff: excursion is the difference between the larger of the two takeoff values and the smaller of the landing values. Values are given as the mean i SD; na, not applicable: N is the number of strides and 11 is the number of individuals. Within columns, cr and h denote significant differences ( P < 0.05) between gallops of adults (Dunn's multiple comparison test). *. P < 0.05: ***. P < 0.001.

tComparisons among gallops of adults; xf[, 05 ,31 = 7.8 15. $Comparison between stotting adult and juvenile mule deer. #Comparisons between the adult mule deer stot and the hybrids' bound.

although hybrid 2's tended to carry their necks especially low. Hybrid 2's differed significantly from galloping mule deer in their minimum and maximum neck measurements ( P < 0.05). The excursion of the neck was similar for all gait groups.

The backs of galloping white-tailed deer, mule deer, and hybrids tend to orient somewhat below the horizontal when the trailing forelimb lands (Table 7, landing 1) and continue to decline until the leading forelimb lands (landing 2). Their backs start to rise to a level position when the animals are in a gathered position, and continue to rise following the landing of the trailing hind limb. The backs orient to their steepest upward position shortly before the trailing hind limb leaves the ground (takeoff 1). The backs of white-tailed and mule deer decline after the departure of the trailing hind limb (see

Fig. 4a for illustration of a gallop). There is variability in this pattern, however. The backs of mule deer remained relatively high throughout two strides in which the animals were acceler- ating, and also remained high when the animal were making a transition to another gait.

Galloping mule deer underwent a larger upward shift in back attitude during their hind limb contact interval than did white-tailed deer. As a result, the back attitude of mule deer was, on average, greater than that of white-tailed deer as the hind limbs left the ground ( P < 0.01 and 0.02 for first and second takeoff, respectively). Values for this trait tended to be intermediate in hybrids.

The backs of stotting adult mule deer were nearly level (back attitude: 0.4 + 2.4" (1 SD) as the first limb landed

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

(a) Mule Deer stot: forelimb

LINGLE

hind limb

limb contact 0.127s

TIME (s )

(b) Hybrid bound: forelimb

I I I I I I I

0 100 0.133 0.167 0.200 0.233 0.267

TlME (s)

‘,I hind limb

limb contact. 0.234 s

TlME (s)

TlME (s)

FIG. 3. Trajectories of fore and hind limbs before, during, and following contact for stotting mule deer ( u ) and bounding hybrid (b) . The trajectories of the neck and olecranon (elbow) are plotted for the forelimb. with the fetlock and hoof plotted during contact. The trajectories of the caudal end of the back and carpus are plotted for the hind limb, with the hoof plotted during contact. Each line represents 11150 s for the mule deer and 1/64 s for the hybrid. Timing tics, aligned with dorsal body points, are at approximately 0.03-s intervals. An attempt was made to draw the mule deer and hybrid to approximately the same scale, but their velocities should not be conlpared directly. Unconnected points for the mule deer hind quarters represent the carpus; the caudal end of the back was not visible in those film images. The neck-olecranon distance appears long between the hybrid's fore- and hind-limb landings because the body is hunched at this time. Back-carpus lengths on hind- limb trajectories vary because of flexion in the stifle. Small incongruities i n the trajectories occur as a result of error i n plotting the points. The trajectories illustrate the overall pattern of motion; they are not accurate enough for measuring instantaneous velocities or the precise angle of trajectory at specific times. The neck and olecranon of stotting deer continue to move forward following limb contact. Trajectories of the neck. olecranon. and lower back of stotting deer are smooth, with gradual changes. as in the case of galloping deer (not shown). The olecranon of bounding hybrids fixes i n place for about 0.03 s after landing. The shoulder is also held back at this time. The forebody stops its descent before the hind limbs land, but rises steeply immediately after they land. The trajectories of the neck, olecranon, and lower back are steeper and undergo more sudden changes in bounding hybrids than in stotting mule deer. The hind-limb trajectory i n hybrids is also steeper than that of mule deer as the animals approach takeoff.

(Table 7, landing 1)). At hind-limb departure (takeoff 2), the backs of stotting deer oriented upward about as steeply as the backs of galloping mule deer at the first hind-limb takeoff. Because of their limited downward back movement, the range of their back attitude was small, similar to that of galloping white-tailed deer.

Back attitudes were measured from six hybrid 1 bounding strides. The backs of these animals inclined steeply downward at the forelimb landing ( - 12 f 2"; Table 7, landing 1). The backs oriented less steeply downwards as the hind limbs landed (landing 2), then immediately reoriented to a steep upward attitude. By the time the forelimbs left the ground, the

back attitudes averaged 1 1 f 3" (takeoff 1) and became steeper until hind-limb departure (takeoff 2). Back attitudes at the initial landing and the excursion of back attitude differed significantly between stotting mule deer and bounding hybrids (P < 0.001).

Back attitude at limb landing and the excursion of back attitude during a stride are characteristics that distinguish stots from bounds. These characteristics are useful for identifying these gaits in the field, because it is much easier to track the motion of the back than to untangle the order of footfalls in fast-moving animals. Back attitude is also useful for distin- guishing stots from gallops in the field, because of the

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

718 CAN. J . ZOOL. VOL. 71, 1993

prolonged descent and period of limb contact during which a stotting deer's back is nearly level. This characteristic could be useful for classifying gaits.

Trajectories of selected body points The takeoff angle of the body's center of mass was estimated

for five stotting mule deer that were moving fast and for three bounding hybrids. A trajectory was determined by plotting the center of the image area from film frames showing hind-limb departure and successive images. Recognizing the deficiencies of this method (the density of body segments are not equal), the takeoff angle was about 10- 15" for fast-moving mule deer. Despite the visually striking height attained by stotting mule deer, the trajectory of the body's center of mass is relatively shallow. Hybrids departed at steeper angles, approximately 15-20".

Trajectories of the base of the neck, the forelimb, the caudal end of the back, and the hind limb during limb contact were plotted for two strides by stotting mule deer and three by bounding hybrids. Once the forelimb lands, the olecranon (elbow) and shoulder of galloping ungulates typically continue to move forward and down as they flex under the weight of the body (Gambaryan 1974). This pattern of progression was seen in stotting deer (Fig. 3a), with the elbow decelerating as it approached the vertical and the forebody pivoted over it. The forelimb began to extend as it prepared for limb departure. Changes in the trajectory of the neck and lower back were gradual for stotting deer.

The neck of bounding hybrids continued to move forward after the forelimb landing. A lag in the motion of the olecranon occurred immediately after forelimb contact and lasted for 0.03 -0.45 s (Fig. 3b). The shoulder was also held back at this time, visibly protruding from the body until it resumed its forward motion. The neck stopped its descent before the hind limbs landed, then rose steeply upon their landing. Like changes in back attitude, changes in trajectories of the neck and lower back were rapid and large.

The lower back pivots over the carpus and fetlock after the hind limbs land, while the stifle flexes and continues to move forward. The carpus and then stifle extend as they prepare for departure. This pattern of motion was used by mule deer and hybrids; however, the lower back and carpus of hybrids followed steeper trajectories than did those of galloping or stotting deer (Fig. 3b).

Tail position and tarsal tufts When alarmed, white-tailed deer often raise their tails, flare

the fur on the underside and haunches, and wave the tail from side to side as they flee. Individuals vary as to how commonly they flag their tails. When flagged, the tails tend to be taut or even arched forward (Fig. 4a).

Mule deer tend to carry their tails down when they are alarmed or fleeing. Their tails commonly swing out as the hind limbs land or depart. This swing ranges from a slight bounce to a movement reaching a point higher than the horizontal, but is so quick it is usually not noticed by the unaided eye.

At some time, all F l hybrids flagged their tails vertically and waved their flagged tails from side to side as they ran. Although the flagged tails were held taut at times, hybrids often appeared to have "loose" tails (visible on film) that swung up and down as well as laterally, or the tip hung limply on an otherwise raised tail. The tail fur was often flared.

White-tailed deer usually flare the white tarsal tufts during flight, so these are large and bright. Tarsal flaring was

observed in videos of a few hybrids and in one of mule deer. The flaring of tarsal tufts is difficult to detect in mule deer and in most hybrids because their tan tufts blend in with their leg color.

Discussion: biomechanics and function of deer gaits

Films and sets of stick deer were reviewed, first, to identify when differences in limb coordination (identified in Lingle 1992) and body configuration occurred and, second, to evaluate the biomechanical effects of these features. Further inte- gration of these results may be aided by plotting complete trajectories of body sites alongside indicators of the timing phases of the stride (e.g., Goslow et al. 1973; Wetzel et al. 1976; Bullock 1982). The Eshkol - Wachmann movement notation may also be used to track movements within the body in relation to temporal events and has been applied to ethologi- cal topics (Pellis 1983, 1985).

A biomechanical evaluation helps in understanding ways in which a particular gait enables an animal to achieve speed, height, maneuverability, stability, or mechanical efficiency. Although several researchers have examined mechanical aspects of gallops (Hildebrand 1959; Gambaryan 1974; Rooney 1977; Leach 1986), the stot and bound have not received similar attention. A qualitative approach that con- siders the motion of the body overall can guide researchers to specific locomotory or morphological features that merit detailed analysis.

Gallops Discussion of the gallop is restricted to characteristics that

differ among the types of deer. A description of the sequence of events is available elsewhere (Lingle 1989).

White-tailed and mule deer Even though the duration of contact by each limb pair is

about the same for galloping white-tailed deer as for galloping mule deer and hybrids, the limbs contact the ground during a greater proportion of the white-tailed deer stride. The hind- limb contact of white-tailed deer has little or no overlap with the forelimb contact when the animal is in a gathered suspension (Fig. 4a, 3). White-tailed deer also have fleeting suspensions when their bodies are suspended (Fig. 4a, 8). These features of timing enable white-tailed deer to apply forces to maintain or increase their velocity during a larger proportion of the stride than is possible for galloping mule deer (Lingle 1992).

The extended suspension enables white-tailed deer, mule deer, and hybrids to cover a horizontal distance greater than their actual body length before the forelimb landing (Hilde- brand 1959). The body of the white-tailed deer may also be suspended after forelimb departure, this time in a gathered position (Fig. 4a, 3). The hind hooves land further ahead than would be possible if the body's forward movement were restrained by a grounded forelimb.

The white-tailed deer's habit of crossing the trailing hind limb lateral and cranial to the leading forelimb (Fig. 4a, 2) also enables the hind limb to cover more horizontal distance than it could if placed caudal to the leading forelimb, as in mule deer. This is true whether or not white-tailed deer use a gathered suspension.

The prolonged suspensions of mule deer indicate that they attain more vertical velocity at hind-limb departure than do white-tailed deer (Lingle 1992). The large vertical displace-

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

LlNGLE 719

ments would make their gallop mechanically inefficient, unless this species is more able to utilize elastic strain energy at hind-limb departure. The long suspensions may be useful for traversing obstacles (Dagg and de Vos 1968; Gambaryan 1974).

Compared with mule deer, the backs and necks of white- tailed deer are low as the hind limbs depart from the ground (Fig. 4a, 4 and 5), This lowers the body's center of gravity and the trajectory it will follow when suspended. White-tailed deer had significantly greater forelimb flexion and excursion (Fig. 4a, 6), with a tendency to greater flexion in the hind limb. Larger flexion in limb joints during limb recovery results in a more horizontal trajectory that gains more distance. Increasing the limb flexion also lowers resistance to angular motion and tends to be associated with increased velocity (Kreighbaum and Barthels 1990).

Extension of the lower back and hip accompanies the thrust of the hind limbs at departure. White-tailed deer flex at the hip, stifle, and hock to begin limb recovery soon after limb departure. Mule deer extend further at the hip and appear to sustain this position before initiating limb recovery. The basis for their larger hip extension is not clear. Do they have a stronger hind-limb thrust or just more vertical displacement'?

Combined with features of limb timing (Lingle 1992), the summation of the more horizontal velocities of individual body segments (the neck, back, and limbs) should result in a longer stride and a faster and more efficient gallop for white-tailed deer than for mule deer. Limited data on velocity indicate that galloping white-tailed deer can travel faster than mule deer (Lingle 1992). The difference between the low and graceful gallop of white-tailed deer and the rockier motion of galloping mule deer is visible to careful observers in the field (Geist 1981).

Hybrids The gallop of hybrids has a mixture of features observed in

the white-tailed and mule deer gallops. In characteristics that differed significantly between white-tailed and mule deer, hybrids were usually intermediate but often more similar to one or the other parent species. No significant differences were found between F I hybrids having white-tailed or mule deer mothers. These results suggest that genetic traits which influence the characteristics of body configuration that differ between white-tailed and mule deer have additive and domi- nance effects, as was also found for characteristics of limb coordination. A tendency to tail flag was clearly dominant to a tendency not to flag, as it was employed by all F, hybrids. This trait requires more careful measurement to determine other aspects of its inheritance.

Values for limb coordination (Lingle 1992), hind-limb placement, and hip extension in hybrids were more similar to values for mule deer than to those for white-tailed deer. Values for back attitude at hind-limb takeoff and forelimb flexion and excursion in hybrids tended to be intermediate between those for white-tailed and mule deer. Hybrids had some white-tailed deer traits: they carried their necks low and they flagged their tails. The larger number of segments having more vertical trajectories and the pattern of limb coordination indicate that hybrids undergo more vertical displacement than do white- tailed deer.

The low neck position would affect the position of the animal's center of mass and so would interact with the length of suspension and tempo of limb recovery. More detailed

analysis of the gallop would be necessary to determine how these characteristics interact and affect the mechanics of the strides of hybrids.

Mule deer stot The following analysis indicates that the stot may be faster

and more efficient mechanically than is generally thought. At the same time, its advantages over the gallop appear to lie in its flexibility in application.

At the end of the long suspension of the mule deer stot, the hind limbs as well as the forelimbs are held forward in preparation to land (Fig. 4b; see Fig. 2 for a more detailed illustration of the stot). The back is nearly level at this stage of the stride. The hip and lower back are flexed, curving the rump. Although at its lowest position of the stride, the neck is much more vertical than the minimum neck attitudes of the gallops, and appears nearly vertical.

The hooves are nearly even; which one lands first seems to depend on slight differences in terrain or on slight tilts of the body forward or backward, right or left. If all four feet do not land simultaneously, one or both of the forelimbs land first more often than does one of the hind limbs. Nevertheless, differences in the order of landing of the fore and hind limbs are slight and are not essential to the stot as they are to the gallop.

The hind limbs probably receive a substantial portion of the animal's weight at landing. They land simultaneously with the forelimb and they lie under the body's estimated center of mass (Fig. 4b, 0.00 s), similar to their position at the hind- limb landing during the gallop. The role of the forelimbs at landing may be shifted from that of absorbing the shock imparted by the entire body in the gallop to that of receiving a lesser proportion of shock and offering some balance.

In the stot, the large vertical acceleration due to gravity should result in greater impact forces than occur during any single limb landing in the gallop. Nevertheless, the positioning of the mule deer's body and the synchronization of the hind limbs with the forelimbs may enable a stotting deer to conserve much of its forward momentum during limb contact and, subsequently, acquire speed beyond that which might be expected from casual observation of this jumping gait.

Mule deer have sufficient vertical velocity at takeoff to remain suspended for a longer time. Nonetheless, the takeoff angle of the center of mass (approximately 10 - 15 " for fast-moving animals) and the path followed by an animal as it descends (Fig. 4b, 0.29-0.50 s) indicate that the horizontal velocity of a stotting deer is much greater than its vertical velocity.

The body forms a level plane during descent, and this is maintained following limb landing. The hind limbs land simultaneously with the forelimbs and the center of mass quickly passes in front of them (0.04 s). At this stage, a smooth upward shift in back attitude betrays the application of forces used to propel the animal into its upcoming suspension. No dramatic adjustment in body position is necessary to prepare for limb departure. The stability of the body's axis following limb contact (Fig. 4b, 0.00-0.04 s) and the gradual change in attitude that leads to limb departure (0.04-0.12 s) suggest that considerable horizontal velocity is conserved throughout limb contact.

The trajectory and the level positioning of the mule deer's body facilitate continuity of motion between strides. Con- tinuity of motion enables an animal to devote force to acceler- ating beyond the speed attained during previous strides, rather than to merely rebuilding speed. Under the conditions of this

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

CAN. J . ZOOL. VOL. 71. 1993

TlME (s) 0.00 (%I 0

C ;qpg& 1- 1 I 1 I

TIME (s) 0.00 0.05 0.08 0.1 1 0.16 0 20 0.31 0.39 0.47 (O/o) 0 10 17 23 3 3 4 3 67 83 100

FIG. 4. Selected phases of the white-tailed deer gallop (a). the mule deer stot (b), and the hybrid bound (c). A continuous ground line is used when images are in correct spatial relationship (i.e., the trajectories of the stot and bound). The actual time (s) and percentage of stride duration are listed under the rump in each image. Longitudinal axes (---) are used to aid visual comparison of changes in body position during limb contact. Solid circles represent the estimated center of body mass and were detern~ined by finding the spatial center of each silhouette. The figures were traced from projected film images. (a) Numbers indicate characteristics that differ between white-tailed deer and mule deer gallops. WT, feature in which hybrids resemble white-tailed deer; MD, feature in which hybrids resemble mule decr. 1 , white-tailed deer and hybrids often flag their tails when alarmed. 2, the trailing hind limbs of white-tailed deer land cranial to the spot where the leading forelimb contacted the ground, whether or not the deer has a suspension at this stage. The trailing hind limbs of mule deer (stippled inset) and hybrids tend to land caudal to the leading forelimb. 3, only white-tailed deer have gathered suspensions. 4, the back attitude of white-tailed deer is lower than that of mule deer at hind-limb departure. Hybrids tend to be intermediate. 5 . the neck attitude of white-tailed deer and hybrids is low throughout the stride. 6, white-tailed deer have more flexion and a larger range of movement in the forelimb during limb recovery than do mule deer, enabling them to protract the limb more horizontally. Hybrids tend to be intermediate. 7, white-tailed deer have less hip extension after hind-limb departure than do mule deer or hybrids. 8, white-tailed deer have a brief suspension after hind-limb departure. Mule deer and hybrids tend to have a prolonged suspension at this phase of the stride. The longitudinal axis is determined as follows: point u lies at the indentation above the sternum. Point b lies at the caudal end of the animal's visible ventral surface. Lines u-d and b-c. are drawn to form a right angle, with point d bisecting segment b-(8. (b and c) The solid circle (estimated center of body mass) is intended to help the reader to visualize the approximate placement of the body's bulk relative to the limbs. The density of body segments is likely similar for the two types of deer, so a spatial estimation can be used for a rough comparison of effects arising from conspicuous differences in body position. See the text for a discussion of the mule deer stot and hybrid bound.

study, the maximum velocities of stotting mule deer were somewhat less than those of the galloping white-tailed deer but similar to those reported for galloping mule deer and hybrids (after Lingle 1992: white-tailed deer gallop, 10.93 m/s; mule deer stot, 9.26; mule deer gallop, 8.52; hybrid 1 gallop, 8.53; hybrid 2 gallop, 9.49).

Following hind-limb departure (Fig. 4b, 0.12 s), mule deer extend the hip and then flex at the hip, stifle, and tarsus. By these movements, the hind limbs are initially pushed further back, but are then lifted close to the rump. The back levels out as the hind limbs are raised. From then on, the hind limbs and forelimbs are synchronized in their recovery, in that they take

similar positions relative to the body and move at the same rate while they are slowly protracted. As long as the limb pairs are synchronized, the body remains nearly level with the ground.

Mule deer attain a height that is visually striking despite their shallow trajectory. The center of body mass is raised by extension of the body before takeoff (Fig. 4b, 0.12 s): a higher departure point increases the height and length of a jump. Lift- ing the limbs adds to the apparent height of the body and allows unimpeded travel over rough ground and low-lying obstacles (Dagg 1973). Given the animal's compact body position during the final stage of descent (Fig. 4b, 0.44-0.50 s), the center of mass passes below its takeoff height. Vertical dis-

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

LINGLE 72 1

placement is greater during the animal's descent than during its ascent.

The extent and continuity of horizontal velocity indicated by this analysis suggest that the mule deer stot is more efficient mechanically than has been generally thought. It is also possible that the use of elastic strain energy reduces the metabolic cost of the vertical displacement during the stot (e.g., Dawson and Taylor 1973). No differences have been found between the appendicular structure of white-tailed and mule deer (Eslinger 1976) or between the elastic properties of their hind- limb tendons (Pollock 1991). Mule deer may be more able to use elastic strain energy, not because of a morphological difference but because of mechanical advantages resulting from their type of gait.

Four features of their stride may put stotting mule deer in an excellent position to use elastic strain energy more than galloping deer do. First, the impact forces should be large because of the height from which the animals descend. Second, the hind limbs, largely responsible for subsequent propulsion, land following the descent: kinetic energy gained during descent is not dissipated during a prior forelimb contact. Third, the hind limbs are placed under the mass of the body (Fig. 4b, 0.00 s), SO the vertical component of the animal's velocity may act directly on these limbs. The back, another potential site of storage of elastic strain, is fully flexed at this time. Fourth, the rapid limb contact would enable elastic strain energy to be released soon after it was loaded. Until further morphological, metabolic or kinetic research has been conducted, it seems prudent to withhold judgment as to whether stotting is much more costly metabolically than galloping for deer.

The usefulness of the stot relative to the gallop has to be evaluated by considering how mule deer use this gait in their natural habitat (S. Lingle, in preparation). Mule deer can adjust their takeoff angle and velocity to vary the height and direction of their trajectory according to the intensity, prox- imity, and position of a disturbance. The stot can be used for travel at a larger range of speeds than the gallop (Lingle 1992). Mule deer regularly covered 4 or 5 m per stride when fleeing down the runway in gait trials. When they appear mildly alarmed or uncertain of the extent or direction of danger, mule deer may use short, vertical stots that gain little distance. (The back attitude itself was quite shallow at hind-limb departure in particularly slow stots.) A mule deer may also stot to the side or over a pursuer, rather than separate itself by sheer distance. The biomechanical features of this gait make it tremendously versatile in application, yet still relatively fast.

Hybrid bound The right and left limbs of a pair mirror each other in the

bound, giving the appearance of a two-legged gallop with an exaggerated rocking movement (Fig. 4c). The moderately long suspension may also remind casual observers of the stot. Hybrids bound when intensely alarmed or excited, but not in play or in routine social encounters. By contrast, mule deer frequently stot in both these situations. The hybrids' opportunities to practice and refine the bound may therefore be limited.

The relationship between the timing of the fore- and hind- limb events is one of the most critical differences among the gallop, stot, and bound. I suggest that for a rapid escape gait in large ungulates, the fore lead cannot be reduced until the forelimbs and hind limbs become synchronized (indicated by

a small midtime lag), as in the stot. Hybrids travel more slowly during limb contact than do stotting deer. This is evident because they take about twice as long to cover the same distance (Lingle 1992). The coupled forelimb landing and associated body position appear to restrict the horizontal displacement achieved by the hybrid bound.

The forelimbs contact the ground alone after landing. There is no forelimb available to receive the animal's weight, as in the gallops, if the momentum of the body were to carry it further forward. A stage equivalent to the forelimb contact is bypassed in the stot, because the hind limbs also contact the ground. Once the forebody of a stotting deer passes in front of the forelimbs, the animal prepares for limb departure.

Most animals that bound as a regular gait, e.g., some felids, mustelids, and sciurids, have a vertically mobile spine and the ability to move the spine through the forelimbs relatively freely (Gambaryan 1974). These anatomical features enable the forebody to move forward while the forelimbs are com- pressed below the body to slowly absorb the shock of landing (Gambaryan 1974). In bounding hybrid deer, the shoulder and olecranon briefly fix in place upon landing, after which they begin to move forward (Fig. 3b). The lag in the forelimb trajectory may reflect the sudden absorption of shock, perhaps because the forelimbs cannot move independently of the spine in order to absorb the shock slowly. Ground reaction forces received by the limbs should be large as a result of the animal's steep trajectory and because these limbs land alone.

The hybrid's body is angled downward as the forelimbs land. The body has to be reoriented upward to continue moving forward. Hybrids undergo the largest and most sudden change in body position during limb contact (e.g., Fig. 4c, 0.08 -0.1 1 s). By the time the forelimbs have left the ground, only about 0.01 -0.06 s after hind-limb landing, the back has risen 20°, on average. The energy and time applied to this rotation are likely to detract from that applied to horizontal displacement, limiting both the speed and efficiency of the stride.

The hybrid's forelimbs are ready, or nearly ready, to leave the ground when the hind limbs land (Fig. 4c, 0.08 s). This means that the hind limbs must apply downward forces immediately following their landing to facilitate forelimb departure. The hind limbs are situated under the animal's stomach at forelimb takeoff (Fig. 4c, 0.11 s). Application of forces by these limbs direct the animal more vertically than if the limbs were situated more caudal to the animal's center of mass. Accord- ingly, upon the landing of the hind limbs, the hybrid's forebody assumes a steep upward trajectory that persists until hind-limb departure (Fig. 3b).

Suspensions of bounding hybrids are shorter than those of stotting mule deer, indicating that hybrids do not travel as high as mule deer (according to laws governing the motion of pro- jectiles). The steep takeoff angles of hybrids, however, indicate that the proportion of their velocity that is applied to the vertical is larger than that of stotting deer. This means that bounding hybrids should have proportionately less horizontal velocity during their suspensions than stotting mule deer, and so would cover less distance. Hybrids appeared to gain 1.5 - 3 m in horizontal distance while suspended.

The prolonged suspension of the stot provides mule deer with an extended period for metabolic recovery, for there is little limb or body movement during that stage that requires energy. The turnover of events is quicker during the bound

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

722 CAN. J . ZOOL. VOL. 71. 1993

than during the stot, which means that a hybrid has little time to rest before having to undergo muscular work during the subsequent limb contact interval and departure.

Hybrids protract their forelimbs as, or immediately after, the hind limbs are lifted following their departure. Together, these motions appear to have the effect of rotating the hind- quarters upward and the forebody downward relative to the body's center of gravity. When the forelimbs land, the hind limbs may be in a flexed or hanging position caudal to the rump or carried under the abdomen, already in the middle of their recovery. These differences in coordination seem to depend on the length of suspension.

In some bounding strides, the right and left forelimbs land side by side; in others, one limb is placed in front of the other. The hind hooves may land behind the forehooves, or one but not the other may land adjacent or in front of the forehooves. The placement of hind limbs relative to the fore varied among successive strides made by the same individual. Variability in the position of limb placement was not seen in white-tailed deer or in mule deer that travelled in a straight direction at a distance from a pursuer (variation in limb coordination is seen during the initial acceleration). The variability seen in the limb placement of hybrids may have resulted from interference between the fore and hind limbs, which contact the ground in nearly the same spot.

In 1944, Howell stated that the "decelerating influence" of the coupled forelimb landing of the bound would be difficult to overcome, in order for a large animal to bound for rapid travel and, for this reason, most animals use the half-bound instead. Indeed, because of the necessary rotation of the body, the steep trajectories, and potential constraints on forward progression during forelimb contact, it appears that the bound is a slow and mechanically inefficient form of movement for deer. Because of differences imposed by scale (Thompson 1966; Maynard Smith 1968), small animals, particularly those with a flexible backbone, may bound to accelerate rapidly (Gambaryan 1974; Dagg 1977).

As a usual gait over level terrain and low vegetation, the biomechanical limitations of the hybrid's bound may result in ineffective responses to predators in the animal's natural habitat. Selection against hybrids could restrict genetic exchange between white-tailed deer and mule deer. To evaluate this possibility, it is necessary to consider how these animals use their gaits in the natural habitat (S. Lingle, in preparation), for behaviors that seem mechanically inferior may prove useful in specific environments or predation contexts. For instance, gazelles (Walther 1969) and white-tailed deer (Lingle 1992) bound in order to travel through tall vegetation.

Conclusion

Characteristics of body configuration in the escape gaits of deer were measured and considered in conjunction with characteristics of limb coordination to evaluate opportunities and limitations for use conferred by the mechanics of each gait. An understanding of these possibilities allows subsequent con- sideration of the ways in which these gaits serve white-tailed deer, mule deer, and hybrids in their natural habitats.

Galloping white-tailed deer had the most horizontally directed flexion in their necks, backs, forelimbs, and hips. Com- bined with features of limb coordination, the summation of

velocities of these body segments results in a faster and more mechanically efficient gallop for white-tailed deer than for mule deer or hybrids.

In characteristics in which galloping white-tailed and mule deer differed, values for F , hybrids tended to be intermediate but usually more similar to one parental species or the other. No significant differences were found between the body con- figurations of reciprocal hybrids.

Unlike the data on limb coordination, measurements of adult and juvenile body configuration differed. This difference could be an effect of body size or a matter of developing coordination through physical maturity or experience.

Stotting mule deer appear to conserve much of their momentum between strides, which stems from the simultaneous landing of fore and hind limbs, the level positioning of their bodies during limb contact, and a trajectory that is much more horizontal than vertical. As a result, the stot may be faster and more efficient mechanically than is generally thought. The stot is also flexible in application, in that mule deer can vary the direction, distance, or height of a stride by making slight adjustments in departure angle or takeoff velocity. The value of this gait must be considered in the context of the animal's natural habitat.

The bound, used by hybrids, seems to be a slow and mechanically inefficient gait for deer, primarily because of biomechanical factors stemming from the coupled forelimb landing and associated steep body position. The body of the hybrid undergoes a large rotation during limb contact and follows a steep trajectory, factors that limit the horizontal distance gained during the stride.

Interbreeding between white-tailed deer and Rocky Moun- tain mule deer appears to result in biomechanically limited gaits for the hybrid progeny. These limitations present the possibility that hybrids respond ineffectively to predators, which could lower their viability relative to white-tailed and mule deer.

Acknowledgements

This research was supported by the Natural Sciences and Engineering Research Council of Canada and by Alberta Recreation, Parks and Wildlife through grants to Valerius Geist. I am grateful to the Calgary Zoo and to Edmonton Fish and Wildlife for letting me work with their animals, and for providing animal enclosures, veterinary care, and materials needed for animal care. Many employees of The Calgary Zoo and Fish and Wildlife gave valuable assistance in transporting animals, animal care, and general advice. I am grateful to many people at The Human Performance Laboratory at the University of Calgary for letting me use their facilities to analyze films and for technical advice. Byron Tory wrote the computer program that was central to the data analysis. I appre- ciate the efforts of Clarence Gerla, Robert Peele, William Samuels, and William Wishart in overseeing logistics, and I thank Ralph Fuhrmann and 0. Lingle for devoted field assistance. I thank Finbarr Wilson for discussing the topic at length and for reviewing drafts of the manuscript. Max Bayer and Anthony Russell made valuable comments on the thesis upon which this work is based. Sergio Pellis and three anonymous reviewers made useful suggestions on the manuscript. I extend special thanks to Dr. J . B. Cragg, Dr. V. Geist, and Mr. W. D. Wishart for contributions throughout this project.

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

LINGLE

Appendix

A. Location of digitized points on contour of deer's body (Fig. 1 ) Hind limb

1. Hoof. 2. Middle of limb where phalanges articulate with metatarsals. 3. Caudal end of calcaneus (when animal stands). 4. Distal end of femur. 5. Hoof (side away from camera).

Forelimb 6. Hoof. 7. Phalanges (selected as was point 2. but in respect to metacarpals). 8. Middle of limb at carpus. 9. Olecranon process of ulna.

10. Hoof (side away from camera). Body, neck. and head

1 1 . Tip of tail. 12. Caudal end of back. Site immediately cranial to rump patch (on mule deer) or to tail base (on white-tailed deer and

hybrids). 13. Dorsal tip of crest of the illium. 14. Midback, halfway between points 13 and 15, determined manually. Site appears to lie above thoracic-lumbar

junction. 15. lndentation caudal to withers. 16. Base of neck. indentation cranial to withers on dorsal outline of animal. 17. Thoracic inlet, indentation dorsal to sternum. 18. Site immediately proximal to middle of base of ear. 19. Tip of nose. 20. Tip of ear. 2 1 . Midpoint between points 16 and 17, calculated by computer.

B. Landing and takeoff angles The proximal point used to define the metatarsals segment (Fig. lb) was the caudal end of the calcaneus. The calculated

landing angles of the metatarsals are more acute and the departure angles more obtuse than would have resulted if the proximal point lay on the astragalus, where the tibia meets the tarsus. The caudal end of the calcaneus was also used as the distal point to outline the tibia segment (Fig. lb). Consequently, the measured landing angles of the tibia are more acute, and the takeoff angles more obtuse, than would have resulted if the distal point of this segment lay on the astragalus.

The proximal point usesd to define the radius and ulna (Fig. lb) was the caudal end of the olecranon of the ulna. The resul- tant landing angles of the radius and ulna segment are smaller (more acute) and the takeoff angles larger (more obtuse) than would have resulted if the proximal point of this angle were digitized at the semilunar notch, where the humerus articulates with the radius and ulna.

Any flexion that occurs around the carpus upon landing would result in somewhat more acute landing angles for the radius and ulna than for the metacarpals. Flexion at the carpus, however, is more likely to occur at forelimb departure than at limb landing (Bullock 1982); this would result in a larger (more obtuse) angle for the radius and ulna than for the metacarpals at limb departure.

Both the selection of points and extent of forelimb flexion at limb departure or landing may have led to differences between the angles of the radius and ulna and the metacarpals. For either or both of these reasons, the landing angles of the radius and ulna were generally more acute than those of the metacarpals. whereas the takeoff angles of the radius and ulna were more obtuse than the takeoff angles of the metacarpals.

C. Angles of limb flexion Referents were selected on the dorsal body surface to use as proximal points for upper forelimb and upper hind limb angles.

The indentation caudal to the withers (Fig. lc , point 15) was used as the proximal point of an angle that indicates the relative amount of flexion in the upper forelimb. The movement it represents could result from tlexion around the head of the humer- ous, from flexion around the proximal end of the ulna, and from rotation of the scapula.

A spot cranial to the tail on the dorsal outline of a deer's body was used as the proxin~al point of the stifle angle (Fig. lc, point 12). A line extrapolated to the dorsal surface of the animal from the longitudinal axis of the femur intersects with this site when the animal stands upright, but not when the limb is protracted or retracted. When the hind limb is held caudal to the rump, the actual angle formed by the femur and tibia is larger than the measured stifle angle. When the limb is held cranial to the rump, the femur-tibia angle is smaller than the measured stifle angle. Nevertheless, the angle calculated to represent the stifle angle increases as an animal extends the stifle and decreases as the animal flexes this joint and so can be used to compare the relative amount of stifle flexion among the gait groups.

Point 12 was also used as the vertex for the angle that was measured to represent flexion around the head of the femur (or hip, Fig. lc). Point 12 lies dorsal and caudal to the head of the femur. The measured hip angle is smaller than the actual angle formed by the intersection of the illium and femur. The difference between these angles increases as the hind limb is increasingly retracted.

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

724 CAN. J . ZOOL. VOL. 71. 1993

Bullock, R. E. 1982. An analysis of locomotor body movements in pronghorn antelope. Can. J. Zool. 60: 187 1 - 1879.

Dagg, A. 1. 1973. Gaits in mammals. Mammal Rev. 3: 135- 154. Dagg, A. 1. 1977. Running, walking and jumping: the science of

locomotion. Crane, Russak & Co., New York. Dagg, A. I., and de Vos, A. 1968. Fast gaits of pecoran species.

J. Zool. (1965- 1984), 155: 499-506. Dawson, T. L., and Taylor, C. R. 1973. Energetic cost of locomo-

tion in kangaroos. Nature (London). 246: 3 13 -3 14. Derr, J. N. 199 1. Genetic interactions between white-tailed and mule

deer in the southwestern United States. J. Wildl. Manage. 55: 228 -237.

Deuel, N. R. 1985. A kinematic analysis of the gallop of the horse. Ph.D. thesis, Department of Animal Science, University of Illinois, Urbana -Champaign.

Eslinger, D. H. 1976. Form, function and biological role in the locomotory apparatus of the genus Odocoileus in Alberta (Mammalia: Artiodactyla). M.Sc. thesis, Department of Biology, University of Calgary, Calgary, Alta.

Fredricson, I., and Drevemo, S. 197 1. A new method of investigat- ing equine locomotion. Equine Vet. J. 3: 137 - 140.

Fredricson, I., Drevemo, S., Moen, K., Dandanell, R., and Anders- son, B. 1972. Equine joint kinematics and coordination: photo- grammetric methods involving high-speed cinematography. Acta. Vet. Scand. Suppl. No. 37.

Gambaryan, P. P. 1974. How mammals run. Halstead Press, New York.

Gavin, T. *., and May, B. 1988. Taxonomic status and genetic purity of Columbian white-tailed deer. J. Wildl. Manage. 52: 1 - 10.

Geist, V. 1981. Behavior: Adaptive strategies in mule deer. In Mule and black-tailed deer of North America. Edited by 0 . C. Wallmo. University of Nebraska Press, Lincoln. pp. 157 -223.

Goslow, G. E., Reinking, R. M., and Stuart, D. G. 1973. The cat step cycle: hind limb joint angles and niuscle lengths during unre- strained locomotion. J. Morphol. 14: 1 -4 1.

Grieve, D. W., Miller, D. I., Mitchelson, D., Paul, J. P., and Smith, A. J. 1975. Techniques for the analysis of human movement. Lepus Books, London.

Hildebrand, M. 1959. Motions of the running cheetah and horse. J. Mammal. 40: 481 -495.

Howell, A. B. 1944. Speed in animals. University of Chicago Press, Chicago.

Kreighbaum, E., and Barthels, K. M. 1990. Biomechanics: a qualitative approach for studying human movement. 3rd ed. Burgess Pub- lishing Co., Minneapolis.

Leach, D. H. 1986. Locomotion of the athletic horse. In Equine cxer- cise physiology 2. Edited by J. R. Gillespie and N. E. Robinson. ICEEP Publications, Davis, Calif. pp. 516-535.

Lingle, S. 1989. Limb coordination and body configuration in the fast gaits of white-tailed deer, mule deer, and their hybrids: adaptive significance and management implications. M.E. Des. thesis, Faculty of Environniental Design, University of Calgary, Calgary, Alta.

Lingle, S. 1992. Escape gaits of white-tailed deer, mule deer and their hybrids: gaits observed and patterns of limb coordination. Behaviour. 122: 153 - 18 1.

Maynard Smith. J. 1968. Mathematical ideas in biology. 2nd ed. Cambridge University Press, London.

Oceanak, C. P. 1977. Frequency of naturally occurring hybrids among mule deer, Odocoileits hemionus, and white-tailed deer, Odocoileus virginiunus, in portions of eastern Wyoming. M.Sc. thesis, University of Wyoming, Laramie.

Pellis, S. M. 1983. Development of head and foot coordination in the Australian Magpie Gymnorhina tibicen, and the function of play. Bird Behav. 4: 57-62.

Pellis, S. M. 1985. What is 'fixed' in a fixed action pattern'? A problem of methodology. Bird Behav. 6: 10- 15.

Pollock, C. M. 1991. The relationship between body mass and the capacity for storage of elastic strain energy in mammalian limb tendons. M .Sc. thesis, Department of Biology, University of Calgary, Calgary, Alta.

Rooney, J. R. 1977. Biomechanics of lameness in horses. (Reprint of 1969 ed.) Robert E. Krieger Publications, Malabar, Fla.

Stubblefield, S. S., Warren, R. J. , and Murphy, B. R. 1986. Hybridi- zation of free-ranging white-tailed and mule deer in Texas. J. Wildl. Manage. 50: 699-701.

Thompson. D. W. 1966. On growth and form. Abridged ed. Edited by J. T. Bonner. Cambridge University Press, Cambridge.

Walther, F. 1969. Flight behavior and avoidance of predators in Thomson's Gazelle (Guzellu thornson; Guenther 1884). Behaviour, 34: 184-221.

van Weeren, P. R., van der Bogert, A. J. , and Barneveld, A. 1988. Quantification of skin displacement near the carpal, tarsal and fetlock joints of the walking horse. Equine Vet. J. 20: 203 -208.

Wetzel, M. C. , Atwater, A. E., and Stuart, D. G. 1976. Movements of the hindlimb during locomotion of the cat. In Neural control of locomotion. Edited by R. M. Herman, S. Grillner, P. S. G. Stein, and D. G. Stuart. Plenum Press, New York. pp. 99- 135.

Wishart, W. D. 1980. Hybrids of white-tailed and mule deer in Alberta. J. Mammal. 61: 716-720.

Wishart, W. D., Hrudka, F. , Schmutz, S. M., and Flood, P. F. 1988. Observations on spermatogenesis, sperm phenotype and fer- tility in white-tailed x mule deer hybrids and a yak x cow hybrid. Can. J. Zool. 66: 1664- 1671.

Zar, J. H. 1984. Biostatistical analysis. 2nd. ed. Prentice Hall, Englewood Cliffs, N.J.

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

WA

ST

AT

E U

NIV

LIB

RA

RIE

S on

11/

25/1

4Fo

r pe

rson

al u

se o

nly.

escape gaits of white-tailed deer, mule deer, and their hybrids: body configuration, biomechanics,...

Documents