A radiographic study of skeletal growth and development in fetal red deer

Br. vet . J. (1986). 142, 336

A RADIOGRAPHIC STUDY OF SKELETAL GROWTH AND DEVELOPMENT IN FETAL RED DEER G . WENHAM, C . L . ADAM and C . E . MOIR The Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB

SUMMARY Twenty-one linear measurements were taken from radiographs of the major skeletal components of 17 red deer fetuses with known gestational ages ranging from 72 to 224 days . Modified Gompertz equations were fitted to the data to relate fetal weight to age and, using that weight, to relate skeletal dimensions to age and weight combined . The weight of a fetus at 75 days gestation was approximately 44 g and increasing by about 6 . 9%/day . This specific growth rate (SGR) decreased with time so that at term (233 days) a fetus weighing 8 kg was growing at 1 . 23%/day . The bone dimensions increased exponentially with time and, because some of them had a higher SGR and/or reached their maximum growth rate at different times, the inter-skeletal relationships were changing . At 72 days gestation the skull length was approximately double the skull depth and both dimensions had similar SGR, but the SGR of depth declined much more rapidly and reached its maximum rate some 32 days before the growth in length, so the fetus at term had a skull length three times the depth contributing to the long shallow skull characteristic of red deer, particularly the hinds . The distal limb bones, metacarpus and metatarsus maintained a higher SGR than the proximal limb bones for three quarters of gestation, which contributed significantly to the long-legged appearance of the animals at birth . The ratios of bone breadths to bone lengths changed with age, so that the bones became relatively longer and thinner . Estimates were made of the ages at which the primary and secondary centres of ossification were first identified .

INTRODUCTION Studies of fetal growth and development have been carried out on many species, among which were those of Pomeroy (1960) and Ullrey et al. (1965) on the fetal pig, and Wallace (1948), Joubert (1956), Stephenson (1962) and Richardson, Hebert & Terlecki (1976) on the fetal sheep ; but no reference could be found for fetal red deer . The red deer (Cervus elaphus) is now well on the way to domestication as a meatproducing farm animal (Kay, 1981) . There is a need to understand its growth and relate it to that of conventional farm animals such as sheep and pigs . In this study, pregnant



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hinds with known dates of conception were slaughtered at different stages of pregnancy . The fetuses were weighed and radiographed, and linear measurements were made on the radiographs to establish patterns of growth and development of the skeleton . The measurements were made during the 1982-83 and 1983-84 breeding seasons and some comparisons were made with the data from the fetuses of sheep and pigs previously obtained at this Institute by the same methods (Wenham, McDonald & Elsley, 1969 ; Wenham, Fowler & McDonald, 1973 ; McDonald, Wenham & Robinson, 1977 ; Wenham, 1977, 1981) .

MATERIALS AND METHODS Animals

Seventeen red deer hinds were used . They were domesticated animals that had been raised on the hill pastures of the Glensaugh experimental deer farm . They were multiparous and their average live-weight was 80 kg . From October 1982 and 1983 they were penned together indoors and were mated on known dates . They received grass hay to appetite and a barley-based concentrate rationed at 0 . 5 kg/head daily until January and subsequently increased steadily to 0 . 9 kg/head daily by April . The estimated concentrations of metabolizable energy and crude protein per kg air-dry matter were respectively 8 . 5 MJ and 85 g for the hay and 12 MJ and 150 g for the concentrate feed . The hinds were randomly allocated to slaughter between 72 and 224 days gestation (Table I) . They were stunned by captive-bolt pistol, bled and the gravid uterus was Table I Ages, weights and stages of gestation of the hinds at slaughter from which the fetuses were taken Age years

10 11 10 11 10 3 11 10 11 10 11 14 10 10 11 11 11

Weight kg

74 . 0 66 . 5 67 . 5 78 . 0 82 . 0 77 . 0 79 . 5 82 . 0 73 . 5 71 . 0 101 . 5 85 . 0 79 . 5 90 . 0 83 . 5 79 . 5 89 . 0

Gestation days

72 90 101 116 118 128 143 155 159 175 180 191 200 205 214 224



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removed . All carried a single fetus . The fetus was weighted, X-rayed and then dissected to obtain the weights of the major organs . The total tissues were then minced for determination of body composition, a study which will be reported separately . Radiography The fetuses were routinely radiographed in the lateral position . The upper limbs were displaced to reduce superimposition and were supported on cotton-wool in a plane parallel to the film . The neck and nose were similarly supported to make the vertebral column and the skull straight and parallel to the film . Dorso-ventral or antero-posterior views were also taken when needed for anatomical clarification . The smaller fetuses were X-rayed in the cabinet of a Faxitron X-ray System (Hewlett-Packard), the larger fetuses on the table of a major X-ray unit using a Triplex Optimatic generator (Siemens Ltd) . The maximum focus-film distance available, 56 cm in the cabinet and 112 cm on the table, was used to reduce geometric distortion . Either Reproduction film 4566 or Industrial C film (Kodak Ltd) was used ; both are fine-grained, high-resolution films . Measurements The following measurements were made from the radiographs with a vernier microscope or a vernier gauge accurate to 0 . 1 mm : length and depth of the skull, diaphyseal length and breadth at mid-shaft of the humerus, radius, metacarpus, femur, tibia and metatarsus, the length and depth of the ilium and ischium, and the length of the vertebral bodies of C4, T5 and L4 . Note was also taken of which primary and secondary ossification centres were visible . Mathematical analysis The modified Gompertz equations used in the previous studies (mainly McDonald et al., 1977) were fitted to relate body weight to fetal age and the skeletal dimensions to age and weight combined . The specific growth rates (SGR), percentage increases per day, were also calculated using the same equations . The equation for fetal weight (Wg) at a given fetal age (t days from conception) was calculated to be : In W=10 . 131-14 . 341 exp(-0 . 01089t)

(1)

This equation may be transformed as : t=[-logn(A-logn W)+logn B]/C to find age when weight is known . The equations calculated for fetal bone dimensions (y cm) at any given fetal age (t days) and fetal weight (W g) were of the form : In y- A-B exp(-Ct)+D(ln w-ln W)

(2)

where A and B are fitted parameters and W is the estimated fetal weight at age t as calculated from equation (1), w is the actual weight of the fetus, C indicates the rate of exponential decay of the specific growth rate and D is an allometric coefficient .



SKELETAL GROWTH IN FETAL RED DEER

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RESULTS Weight gain Fetal body weight (kg) is plotted against fetal age (days) in Fig . 1 . The weights of two newly-born calves were included in the weight analysis to provide full term points and are shown in Fig . I only .

1 l 1 ∎ . 1 1 90 110 130 150 170 190 210 230 250

Fig 1 .

Foetal age (days)

Fig 2 .

Foetal age (days)

t . ∎ ∎ ∎ ∎ 1 03 05 .1 •2 .3 5 1 2 3 4 5 6 7 8

.

.

Foetal weight(kg) 15 É 13 V

11

L

N

E g

m C 9

V

L a1 C

d

_ 7

7 5

L E

3 1

= 0 50

Fig 3 .

70

90

∎ ∎ . ∎ 110 130 150 170

. ∎ ∎ 1 190 210 230 250

F . .

. . ∎ ∎ ∎ ∎ 1 1 2 3 4 5 6 7 8

.

0 3,05 .1 '2 3 '5

Foetal weight (kg)

Fig . 1 . Fig . 2 . Fig . 3 . Fig . 4 .

90

Foetal age (days)

.

1

110 130 150 170 190 210 230 250

Foetal age (days) I ∎ ∎ ∎ ∎ t I . 1 ∎ 1 -03 05 1 -23 '5 2 3 4

. .

∎ ∎ . 1 5 6 7 8

Foetal weight (kg)

The relationship between fetal weight and age . Skull length plotted against fetal age and the calculated weights . Diaphyseal length of the humerus plotted against fetal age and the calculated weights . Diaphyseal length of the metatarsus plotted against fetal age and the calculated weights .

Using equation (1) it was possible to calculate from the data the mean weight one might expect a fetus to attain at any given age, and estimate the specific and actual growth rates (%/day and g/day) . The figures at the bottom of Table III illustrate the exponential decay of the SGR ranging from 6 . 9%/day at 75 days to 1-23%/day at full term . The corresponding figures in Table IV show the actual growth rate increasing from 3 . 09 g/day to 100 . 64 g/day at term and increasing to reach a maximum, it is calculated, at 244 days after conception, 11 days after birth . A second base-line has been added to



BRITISH VETERINARY JOURNAL, 142, 4

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Figs 2, 3 and 4 showing the calculated weight below the appropriate age so that, using the regression lines, lengths may be expressed relative to age or weight for the average fetus .

Table II Estimates of the parameters A, B, C and D for the modified Gompertz equation Ln Y=A-B exp (Ct)+D(Ln w-LnW) relating fetal bone dimensions (Y cm) to fetal age (t days) and to fetal weight (W g) calculated from the weight equation . A and B are fitted parameters, C is the rate of exponential decay of the specific growth rate, and D is an allometric coefficient Estimate of parameters A

B

C

D

RSD

Humerus Radius Metacarpus Femur Tibia Metatarsus Ilium Ischium Vert . C4 Vert . T5 Vert . L4

3 . 063 3 . 049 2 . 999 3 . 189 3 . 195 3 . 303 3 . 169 2 . 241 2 . 071 0 . 977 0 . 554 0 . 638

-4 . 884 -6 . 968 -6 . 796 -8 . 091 -7 . 387 -7 . 385 -8 . 649 -6 . 570 -9 . 116 -6 . 695 -6 . 072 -5 . 843

0 . 014 0 . 010 0 . 011 0 . 012 0 . 010 0 . 011 0 . 013 0 . 011 0 . 014 0 . 012 0 . 011 0 . 011

0 . 216 0 . 295 0 . 239 0 . 294 0 . 255 0 . 272 0 . 213 0 . 167 0 . 316 0 . 294 0 . 308 0 . 267

0 . 0276 0 . 0599 0 . 0550 0 . 0521 0 . 0525 0 . 0582 0 . 0613 0 . 0912 0 . 0826 0 . 0922 0 . 0502 0 . 0496

Depth Skull

1 . 870

-5 . 174

0 . 020

0 . 207

0 . 0737

0 . 782 0 . 628 0 . 992 0 . 685 0 . 857 0 . 839 1 . 106 0 . 610

-5 . 959 -5 . 540 -6 . 494 -6 . 642 -6 . 145 -6 . 559 -5 . 670 -6 . 121

0 . 011 0 . 009 0 . 009 0 . 012 0 . 010 0 . 010 0 . 008 0 . 012

0 . 338 0 . 313 0 . 338 0 . 346 0 . 415 0 . 206 0 . 126 0 . 166

0 . 0690 0 . 0776 0 . 0621 0 . 0622 0 . 1426 0 . 0905 0 . 0900 0 . 0930

Length Skull

Breadth

Humerus Radius Metacarpus Femur Tibia Metatarsus Ilium Ischium

Skeletal growth Table II provides the estimates of the parameters for the equations used to calculate the changes in bone dimensions with increasing age and weight . As with the weight analysis these equations were also used to provide estimates of specific and actual growth rates which are tabulated in Tables III and IV . The specific growth rates illustrate how the relative growth of the bones changes over the period of gestation, a higher rate at 75 days gradually declining toward full term . But the actual growth rates increase at first reaching maxima (t max) at different ages, and



SKELETAL GROWTH IN FETAL RED DEER

34 1

then gradually decline . Those which reach their t max early are said to be earlier maturing that those which follow . The skull, generally considered to be early maturing was the first to reach t max in both depth and length, depth at 83 days and length at 115 days . The fact that t max for depth was earlier and that it had a lower SGR indicates that the head will be long and shallow, an observable characteristic in the adult. Table III Specific growth rates of fetal bone dimensions of deer estimated from the modified Gompertz equation (expressed as % day) Days of gestation

Length Skull

Humerus Radius Metacarpus Femur Tibia Metatarsus Ilium Ischium Vert . C4 Vert . T5 Vert . L4 Depth Skull

75

125

175

225

233

2 . 39 3 . 29 3-26 3 . 93

1 . 20 2-00 1 . 91

0 . 60 1 . 21 1-12

0 . 27 0 . 68 0 . 61

2-21 2-10 2-05 2 . 25 1-85 2-24 1-78 1-68 1-61

1-24 1-26 1 . 19 1-20 1 . 09 1-12 0-97 0 . 96 0 . 92

0 . 30 0 . 74 0 . 66 0-70

2-32

0-87

0 . 32

0-12

0-10

2 . 88 2-56 2-94 3-24

1-64 1-61 1 . 90 1-78

0-94 1 . 01 1-23 0-98

0-53 0-64 0-80 0-54

0-49 0-59 0-75 0-49

2-90 3-09 2-53 2-99 6-90

1-76 1-88 1-67 1-60 4-00

1-07 1-14 1 . 10 0-85 2-32

0-65 0-69 0 . 73 0-45 1-35

0-60 0 . 64

3-51 3-56 4-23 3-14 4 . 47 3-27 2-93 2-83

0-75 0-68 0-64 0-64 0-56 0-53 0 . 55 0 . 52

0-64 0 . 69 0 . 63 0-58 0 . 59 0-50 0 . 48 0-50 0 . 48

Breadth

Humerus Radius Metacarpus Femur Tibia Metatarsus Ilium Ischium Body weight g

0 . 68 0 . 41 1-23

At the earliest age examined, 72 days, the bones of the forelimb, shortest to longest, were in the order metacarpus, humerus and radius, and even though the humerus maintained a higher SGR than the radius this relationship between them was not reversed . The metacarpus had the highest SGR up to 175 days and overtook the other two so that at term the order had been changed, shortest to longest, to humerus, radius then metacarpus . This indicates that elongation of the forelimb is due mainly to growth of the metacarpus . In the hindlimb at 72 days the positions were similar to the forelimb, metatarsus



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shortest, femur in the middle and the tibia longest, and even though the metatarsus at this time had a significantly higher SGR which it sustained until 150 days, its actual growth rate was higher than that of the tibia for a short time only and, though at term the metatarsus was longer than the femur, it did not overtake the tibia . Thus elongation of the hindlimb was due primarily to the tibia, secondly to the metatarsus and least to the femur . Table IV Rates of growth (mm/day) of fetal deer bones, estimated from the modified Gompertz equations together with the ages (t max) at which the measured parameters attained their maximum rate of growth, i .e . the slope of the regression was steepest No . of days post-conception 75

125

175

225

233

t max

0 . 90 0-26 0-31 0-31 0-28 0-38 0 . 35 0-18 0-14 0 . 06 0-04 0-04

1-07 0-57 0-64 0-78 0-66 0-86 0 . 90 0-36 0-35 0 . 11 0-06 0 . 07

0 . 83 0-76 0-79 1-02 0 . 90 1-10 1 . 10 0-44 0-39 0 . 12 0-07 0 . 07

0-52 0-74 0-71 0-92 0-88 1 . 00 0 . 92 0-39 0-30 0 . 09 0-06 0 . 06

0-48 0-73 0 . 69 0-89 0-86 0-96 0-87 0-38 0-28 0-08 0-05 0-06

115 194 180 182 195 182 171 178 160 156 162 157

Skull

0-46

0-36

0-18

0-07

0 . 06

83

Breadth Humerus Radius Metacarpus Femur Tibia Metatarsus Ilium Ischium Body weight g/day

0-05 0-03 0-03 0 . 04 0-04 0 . 03 0 . 04 0 . 05 3-09

0-08 0-05 0-06 0 . 08 0-07 0 . 07 0 . 07 0 . 08 25-67

0 . 09 0-06 0-08 0 . 08 0 . 09 0 . 08 0 . 09 0-08 69-72

0-07 0 . 06 0 . 09 0 . 07 0 . 08 0 . 08 0 . 09 0-06 99-03

0 . 07 0-06 0-08 0 . 06 0 . 08 0 . 08 0 . 09 0-05 100-64

Length Skull Humerus Radius Metacarpus Femur Tibia Metatarsus Ilium Ischium Vert . C4 Vert . T5 Vert . L4 Depth

159 184 216 158 182 189 209 144 244*

*As calculated but beyond the data limits . Similar figures for the breadth measurements of the same bones tell a parallel story as to how the proximal bones become short but broad while the distal bones become long and slim . The long neck of the species was evident at 72 days with the cervical vertebrae being longest . This characteristic was enhanced with increasing age as these vertebrae sustained a high SGR until 175 days, after which the SGR for the three main vertebral



SKELETAL GROWTH IN FETAL RED DEER

343

groups were similar, though the actual growth rate of the cervical vertebrae was still higher . Table V provides ratios of the SGR of other bones to those of the femur and gives some indication as to how the inter-skeletal relationships are changing . Table VI provides the ratios of diaphyseal breadth to diaphyseal length, all are declining as endochondral growth exceeds periosteal growth . Table V Ratios of the specific growth rates of fetal deer bone dimensions to the specific growth rates of the femur Days of gestation 75

125

175

225

233

Humerus Radius Metacarpus Femur Tibia Metatarsus Ilium Ischium Vert . C4 Vert . T5 Vert . L4

0 . 68 0 . 94 0 . 93 1 . 12 1 . 00 1 . 01 1 . 21 0 . 89 1 . 27 0 . 93 0 . 83 0 . 80

0 . 57 0 . 95 0 . 91 1 . 05 1 . 00 0 . 98 1 . 07 0 . 88 1 . 06 0 . 85 0 . 80 0 . 77

0 . 48 0 . 96 0 . 89 0 . 99 1 . 00 0 . 94 0 . 95 0 . 87 0 . 89 0 . 77 0 . 76 0 . 73

0 . 40 0 . 98 0 . 87 0 . 93 1 . 00 0 . 91 0 . 85 0 . 85 0 . 74 0 . 70 0 . 73 0 . 69

0 . 39 0 . 98 0 . 87 0 . 92 1 . 00 0 . 90 0 . 83 0 . 85 0 . 72 0 . 69 0 . 72 0 . 69

Depth Skull

0 . 72

0 . 49

0 . 33

0 . 22

0 . 20

0 . 89 0 . 79 0 . 91 1 . 00 0 . 89 0 . 95

0 . 92 0 . 90 1 . 07 1 . 00 0 . 99 1 . 06

0 . 96 1 . 03 1 . 25 1 . 00 1 . 09 1 . 16

0 . 98 1 . 18 1 . 48 1 . 00 1 . 20 1 . 28

1 . 00 1 . 20 1 . 53 1 . 00 1 . 22 1 . 31

Length Skull

Breadth

Humerus Radius Metacarpus Femur Tibia Metatarsus

Ossification centres

Tables VII shows the ages at which primary and secondary ossification centres first became visible . The majority of the primary centres, except for the carpus, tarsus and phalanges were present and measurable at 72 days, though the terminal phalanx of each digit was only just visible . The skeleton was not considered to be complete from the radiographs of two fetuses at 224 days, there still being eight minor secondary centres not seen . It was not possible to see if there were any differences in the number of centres present in fetuses of the same age but differing weight as had been observed in the fetal sheep and pig (Wenham et al, 1969 ; Wenham, 1977) because, except for 224 days, there was only one fetus at each age point .



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It is possible from fetal weight, bone dimensions and skeletal development to estimate the age of a fetus to plus or minus five days between 72 and 160 days, and to plus or minus 10 days between 160 days and birth . Table VI Ratios of diaphyseal breadths, at mid-shaft, to diaphyseal lengths including the ratios for skull depths to skull lengths Days of gestation

Skull Humerus Radius Metacarpus Femur Tibia Metatarsus Ilium Ischium

75

125

175

225

233

0 . 50 0 . 21 0 . 12 0 . 11 0 . 16 0 . 12 0 . 12 0 . 25 0 . 54

0 . 47 0 . 18 0 . 10 0 . 08 0 . 14 0 . 10 0 . 09 0 . 21 0 . 33

0 . 40 0 . 15 0 . 09 0 . 08 0 . 12 0 . 09 0 . 08 0 . 20 0 . 26

0 . 36 0 . 13 0 . 09 0 . 08 0 . 11 0 . 08 0 . 08 0 . 20 0 . 24

0 . 35 0 . 13 0 . 09 0 . 08 0 . 10 0 . 08 0 . 08 0 . 21 0 . 24

Table VII Ages at which the primary and secondary ossification centres were first seen, given as fetal age (days), and the percentage that age represents of the total gestational length Days

%

72 128 72 205

30 . 9 54 . 9 30 . 9 88 . 0

Axial skeleton

Cervical vertebrae 2-7 bodies Atlas body Odontoid process 3-7 anterior epiphyses 2-7 posterior epiphyses Spinous processes

-

-

175

75 . 1

72 205 224 102

30 . 9 88 . 0 96 . 1 43 .8

72 205 224

30 . 9 88 .0 96 . 1

Thoracic vertebrae Bodies Anterior epiphyses Posterior epiphyses Spinous processes

Lumbar vertebrae Bodies Anterior epiphyses Posterior epiphyses



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Table VII Ages at which the primary and secondary ossification centres were first seen, given as fetal age (days), and the percentage that age represents of the total gestational length Days

%

72 224

30 . 9 96 . 1

72

30 . 9

72 143

30 . 9 61 . 4

72 72 118

30 . 9 30 . 9 50 . 6

72 72 72

30 . 9 30 . 9 30 . 9

72 191 200 175 205

30 . 9 82 . 0 85 . 8 75 . 1 88 . 0

72 191 175

30 . 9 82 . 0 75 . 1

72 224 205

30 . 9 96 . 1 88 . 0

175 159 175 155 155 205 214

75 . 1 68 . 2 75 . 1 66 . 5 66 . 5 88 . 0 91 . 8

Sacral vertebrae

Bodies Anterior epiphyses Posterior epiphyses Coccygeal vertebrae

Bodies Anterior epiphyses Posterior epiphyses Scapula

Body Tuber scapulae Os coxae

Ilium Ischium Pubes Hyoid Sternebrae Ribs Forelimb Humerus

Diaphysis Head Lat tuberosity Condyles Epicondyles Radius

Diaphysis Prox . epiphysis Dist . epiphysis Ulna

Diaphysis Prox . epiphysis Dist . epiphysis Carpus

Radial Ulnar Intermediate Fourth Third Second Accessory



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Table VII Ages at which the primary and secondary ossification centres were first seen, given as fetal age (days), and the percentage that age represents of the total gestational length Days

Metacarpus

Diaphyses Dist . epiphyses Sesamoids

72 175

30 . 9 75 . 1

90 200 90 200 72

38 . 6 85 . 8 38 . 6 85 . 8 30 . 9

72 224 159 225 200

30 . 9 96 . 1 68 . 2 96 . 6 85 . 8

72 175 191 205 224

30 . 9 75 . 1 82 . 0 88 . 0 96 . 1

90 142 142 142 175 224

38 . 6 60 . 9 60 . 9 60 . 9 75 . 1 96 . 1

72 175

30 . 9 75 . 1

90 200 90 200 72

38 . 6 85 . 8 38 . 6 85 . 8 30 . 9

Phalanges

Proximal phalanges Epiphyses Middle phalanges Epiphyses Distal phalanges Hindlimb Femur

Diaphysis Head Condyles Gtr trochanter Minor trochanter Patella Tibia

Diaphysis Prox. epiphysis Dist . epiphysis Tubercle Lat . malleolus (fib) Tarsus

Fibular Tibial Central Fourth 2nd + 3rd First Tuber calcis Metatarsus

Diaphysis Dist . epiphysis Sesamoids Phalanges

Proximal phalanges Epiphyses Middle phalanges Epiphyses Distal phalanges



347

SKELETAL GROWTH IN FETAL RED DEER DISCUSSION

Although the numbers were few the study provides a good base-line of skeletal growth and development in the red deer fetus against which any changes caused by nutritional or pathological influences may be compared . The use of the modified Gompertz equations has again been shown to be a sound method of estimating changes in fetal weight and bone dimensions, and of providing specific and actual growth rates . All the evidence from McDonald et al. (1977) and Robinson et al (1977) on fetal sheep, from Wenham et al. (1969 and 1973) on fetal pigs, and the present study show that fetal growth follows a smooth, even curve with no sudden changes toward accelerated growth such as those described by Joubert (1956) for the fetal skull at 70 days gestation, and for the bones of the appendicular skeleton at 80 to 90 days described by Stephenson (1962) . The specific growth rates given in Table III show how the bones grow at different rates to establish the inter-skeletal relationships for the species . The distal limb bones, the metacarpus and metatarsus, if they are similar to those of sheep (Wenham, 1981), begin the ossification process later than the proximal bones . They have a higher SGR up to approximately 150 to 175 days and so become a major contributor to limb length . The ratios of the rates of growth (mm/day) of skull depth to skull length at 75 days are approximately 1 :2, but at term are 1 :8 . This reflects the known fast rate of growth of the facial bones rather than the cranium, so that the skull becomes long and shallow . The time taken to reach t max for these two skull dimensions, length 115 days and depth 83 days, are in the reverse order of those found for the fetal sheep, length 69 days and depth 80 days . The figures do not adequately describe the eventual shape of the head per se because the depth measurement does not include the growth of the vertical ramus of the mandible . Tables III and IV also suggest that the bones of the hindlimb are growing slightly faster than those of the forelimb . In sheep it was clear that the limb bones matured, i .e . time to reach t max, in the sequence distal, proximal then middle, but in deer it was distal, middle then proximal in the hindlimb, and middle, distal then proximal in the forelimb .

Table VIII Percentage of gestation period required for fetal bones to reach 1/4, 1/2 and 3/4 of their estimated length at birth for deer (D), sheep (S) and pigs (P), taken from the Gompertz regressions Fraction of length at birth 1/4

Humerus Radius Metacarpus Femur Tibia Metatarsus Skull length

1/2

3/4

D

S

P

D

S

P

D

S

P

53 51 52 51 51 52 36

53 52 54 54 53 56 37

52 49 54 52 51 56 37

70 68 68 67 68 68 57

70 67 70 69 67 70 57

66 64 67 66 64 72 55

85 84 82 82 83 82 75

85 82 84 83 80 84 75

80 77 81 80 78 86 72

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For all the differences in size, weight and shape, the skeletons of fetal deer, sheep and pigs attained a given fraction, 1/4,1/2 or 3/4 (Table VIII), of their size at birth (Table IX) at remarkably similar percentages of their respective gestational periods . For example the three species reached 1/4 of humeral length at birth at 53%, 53% and 52% of gestation ; 1/2 at 70%, 70% and 66% ; 3/4 at 85%, 85% and 80%, respectively . So even though their gestation lengths differed considerably they were attaining a given proportion of their size at birth at similar stages of gestation . Table IX Estimated length (cm) of the diaphyses at birth derived from the Gompertz equations

Humerus Radius Metacarpus Femur Tibia Metatarsus Skull

Deer

Sheep

Pig

10 . 5 11-6 12 . 9

6 . 65 6-77 7 . 00

11-7 14 . 3

7-65 9 . 20 7 . 31

4-14 2 . 72 1 . 52 3 . 89

14-1 18-2

12-64

3-67 1 . 77 9 . 02

There were not enough fetuses of each sex to examine for any sex effects on skeletal growth in deer . It was found in sheep (McDonald et al., 1977) that males tended to be slightly heavier than females and had larger bones, but when the allometric factor was included along with age in the Gompertz equations then sex differences disappeared with the exception of males having a shorter ilium .

ACKNOWLEDGEMENTS The authors are grateful to Mr I . McDonald for the statistical analyses and advice, and to various colleagues for their editorial comments .

REFERENCES JOL :BERT, D . M . (1956) . Journal of Agricultural Science, Cambridge 47, 382 . KAY, R . N . B . (1981) . Rowett Research Institute 37, 125 . McDONALD, I ., WENHAM, G . & ROBINSON, J . J . (1977) . journal of Agricultural Science, Cambridge 89, 373 . POMEROY, R . W . (1960) . ,Journal of Agricultural Science, Cambridge 54, 31 . RICHARDSON, C ., HEBER I, C . N . & TERLECKI, S . (1976) . Veterinary Record 99, 22 . ROBINSON, J . J ., MCDONALD, I ., FRASER, C . & CROFTS, R . M . J . (1977) . ,Journal of Agricultural Science, Cambridge 88, 539 . SI EPHENSON, S. K. (1962) . Australian Journal of Agricultural Research 13, 733 .



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ULLREY, D . E., SPRAGUE, J . I ., BECKER, D. E . & MILLER, E . R. (1965) . Journal of Animal Science 24, 711 . WALLACE, L. R . (1948). Journal of Agricultural Science, Cambridge 72, 243 . WENHAM, G . (1977) . journal of Agricultural Science, Cambridge 88, 553 . WEN HAM, G ., FOWLER, V . R . & McDONALU, I . (1973) . Journal of Agricultural Science, Cambridge 80, 125 . WENHAM, G ., McDONALU, I . & ELSLEY, F. W . H . (1969) . Journal of Agricultural Science, Cambridge 72, 123 . WENHAMM, G . (1981) . Journal of Agricultural Science, Cambridge 96, 39 .

(Accepted for publication 21 May 1985)