Skeletal Effects of Prepubertal Castration in the Male Chimpanzee'

GEORGE CLARK2 AND JAMES A. GAVAN United States A m y Research Institute of Environmental Medicine, Natick, Massachusetts, Department of Anatomy, Medical College of the State of South Carolina, Charleston, South Carolina and Yerks Laboratories of Primate Biology, Inc. Orange Park, Florida

Fifteen years ago there was reported some data on the effects of prepubertal cas- tration in the chimpanzee (Clark, '45). At that time it was quite evident that, even though the normative data were limited, the expected overgrowth of long bones had not occurred. Since there was then in this laboratory an active project on growth in the chimpanzee it was decided to cas- trate a second male chimpanzee for com- parison with the normative data being accumulated. In the normative study there were periodic anthropometric measure- ments, complete x-rays, weight records, etc., as well as behavioral studies. Some of the reports on this comprehensive study have already appeared (Nissen and Riesen, '49; Gavan, '53). This second castrate has recently been sacrificed and along with further data on the original castrate forms the basis for the present report. It should be emphasized that these two chimpanzees are the only known prepubertally castrated male anthropoids. The literature on the human, as was stated in the original re- port, can hardly be considered definitive despite the fact that it has been widely accepted. In the intervening years there have been no additional data.

SUBJECTS

Don was born in May, 1934, castrated at the age of two years and died in Novem- ber, 1956. The cause of death was not determined. He had had a series of severe attacks of diarrhoea but no gross pathology was seen at autopsy. The body was wrapped in roofing paper and buried in the sandy soil at the laboratory and was ex- humed in November, 1960. After being exhumed the left tibia was x-rayed. The

length of this tibia was used in making an estimate of the probable sum of the leg and thigh lengths at age 22. During his life- time he had been the subject in many dif- ferent experiments some of which involved the use of androgens and estrogens. Full details of these particular experiments may be found in Clark and Birch ('45).

Dag was born in May, 1945, castrated in July, 1945, and killed in June, 1960. During his lifetime he served as subject in numerous psychological experiments and aside from several bouts with enteric infections had no particular health prob- lems. At autopsy no indications of testis remnants were found. This was expected since at the original operation the sper- matic cord had been ligated, cut and all peripheral elements removed. Except for Bill, Jim, Jack, Dick and Tom, all the con- trol animals listed in table 1 were mem- bers of the normative series.

RESULTS

The data are summarized in table 1, and figures 1, 2 and 3. In table 1 are listed the sitting heights, leg lengths and thigh lengths of 13 normal adult male chimpan- zees and of the two castrates. Also listed are the sums of the leg and thigh lengths and a ratio between lengths of long and short bones derived by dividing the sum of the leg and thigh lengths by the sitting heights. It will be seen that the ratio for Don at age 11 years is below the mean

1Partial support for the portion of this work done at the Yerkes Laboratory of Primate Biology was pro- vided by the Rockefeller Foundation the Carnegie Corporation and the National Heart Ins'titute (H-5691) of the National Institute of Health.

2 A portion of this work was completed at USARML, Fort Knox, Kentucky.

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180 GEORGE CLARK AND JAMES A. GAVAN

TABLE 1 Selected meusurements of normal and Castrates

~

Sum Ratio Age in Sitting Leg Thigh years height length length

cm cm cm

Ken 12 78.4 24.6 30.4 55.0 0.702 Art 12 75.8 26.2 30.3 56.5 0.745 Alf 14 82.7 26.2 31.3 57.5 0.695 Bard 12 76.7 23.9 29.3 53.5 0.698 Jed 12 80.6 26.0 31.5 57.5 0.713 Mars 12 77.1 24.2 29.8 54.0 0.700 Jent 12 79.9 26.9 32.5 59.4 0.743 Web 12 81.8 24.7 30.8 55.5 0.678 Bill 12 85.5 28.3 28.4 56.7 0.663 Jim 35 79.6 24.8 28.4 53.2 0.668 Jack 24 84.0 27.1 33.5 60.6 0.721 Dick 12 75.0 29.2 29.3 58.5 0.780 Tom 12 83.8 27.6 33.7 61.3 0.732

Normals ( 13)

Mean 0.7106

Castrates Dag 15 77.7 25.9 33.8 59.7 0.768 Don 11 77.3 24.4 29.6 54.0 0.699

22 77.3 (see text) (see text) 61.2 0.792

while that of Dag at age 15 years is within the range of variation seen in the normal animals. The ratio for Don at the age of 22 is, as was mentioned in his protocol, (1) an estimation based on the length of the grave cured tibia, (2) an assumption that length of tibia would have the same relation to leg length before epiphyseal closure and after almost complete closure, (3) an assumption that growth of the fe- mur would be proportional to that of the tibia and ( 4 ) that no change in sitting height occurred.

The total leg lengths of the normals (cir- cles) and of the castrates (squares) are plotted against sitting heights as ordinates in figure 1. In this graph a relative in- crease in total leg length as opposed to sit- ting height would result in points toward the top and left of the figure. The estimate for Don at age 22 is not plotted but i t would lie near that for Dag at age 15.

Figures 2 and 3 are outline sketches of x-ray plates of tibias. In figure 2 are shown those of Alf, a normal male chim- panzee, at the ages of 9, 10, 11 and 13 years. These are labeled 1, 2, 3 and A re- spectively in the figure. It is apparent that even at the age of nine years some indica- tion of closure of epiphyses is present and that closure was complete at age 11. The

0

0 0

I I I I I I I I I I I I

75 76 77 78 79 80 81 82 83 84 85 86

Fig. 1 Scatter diagram of sitting heights (abscissas) plotted against total leg lengths (ordi- nates). Those of normal males are shown as circles and those of castrates as squares.

corresponding knee lengths are 29.6, 30.7, 31.3 and 31.9 cm. In those four years there was thus a minimal increase in length. In figure 3 are diagrams of the left tibias of Alf at age 13 (A), of Dag at the age of 15 ( B ) and of Don at the ages of 11 ( C ) and 22 (D). In contrast to the normal where closure was virtually com- plete at the age of 11 and was complete at the age of 13 both Don and Dag show only slight signs of closure in the x-rays and even in the x-ray of Don at age 22 (although it could not be shown in the

CASTRATION IN CHIMPANZEE 181

diagram) there were indications that re- modeling was still not complete.

3 A I 2 Fig. 2 Outlines of x-rays of left tibia of Alf

at ages of 9 years (l), 10 years (2), 11 years (3), and 13 years (A) .

A B C D

Fig. 3 Outlines of x-rays of left tibia of Alf at age 13 years (A), of Dag at age 15 years (B) , and of Don at age 11 years (C) and at 22 years (D).

DISCUSSION AND CONCLUSIONS

It is apparent that, even though the epi- physes of the long bones of these two chim- panzees remained open long after the nor- mal time of closure, there was no marked overgrowth of their long bones. This sug- gests two questions. 1. In the presence of open epiphyses why did this overgrowth fail to occur? For this the available data can afford no answer. 2. How can this lack of overgrowth be reconciled with the usual textbook statement that such an overgrowth does occur as a result of pre- pubertal castration in the closely related Homo sapiens? It was previously reported (Clark, '45) that the evidence for this con- cept was highly questionable and in the intervening years no new evidence has been reported. It would appear that the concept is probably incorrect and that as a result the so-called eunuchoid habitus in man cannot be the result of a primary testicular deficiency.

LITERATURE CITED

Clark, G. 1945 Prepubertal castration in the male chimpanzee with some effects of replace- ment therapy. Growth, 9: 327-339.

Clark, G., and H. G. Birch 1945 Hormonal modifications of sexual behavior: I. The effect of sex-hormone administration on the social be- havior of a male-castrate chimpanzee. Psycho- som. Med., 7: 321-329.

Gavan, J. A. 1953 Growth and development OP the chimpanzee: a longitudinal and compara- tive study. Hum. Biol. ( a record of research)

Nissen, H. W., and A. H. Riesen 1949 Retarda- tion in onset of ossification in chimpanzee re- lated to various environmental and physiologi- cal factors. Anat. Rec., 105: 665-676.

25: 93-143.