GENERAL

AND

COMPARATIVE

26, 248-252 ( 1975)

ENDOCRINOLOGY

The Effects of Testosterone Propionate on Secondary Sexual Characters and Testes of House Sparrows, Passer domesticus’ EBERHARD lnstitut

far

HAASE

Haustierkunde, Universitnt 40-60, Federal Republic Accepted

January

Kiel, 23 Kiel, of Germany 30,

Olshausenstr.

1975

Male house sparrows were captured in October and transferred to artificial short days of 8L 16D. Beginning on November 19th they were injected either with 0.4 mg testosterone propionate (group T) or with sesame oil only (group C) every other day. Within 24 days the androgen injections caused a change in the inner and outer surfaces of the bill from light brown to black (Figs. 1,2) and a pronounced enlargement of the glomus vesicles (Table 1). In group C bill coloration was unchanged compared with the start of the experiment. In contrast, therefore, to other recent findings the development of ornamental structures in Passer domesticus does not depend on gonadotropins. No significant differences were observed between the testes of the two groups which were all regressed and inactive.

Many sexually and/or seasonally dimorphic ornamental structures of the head region like bills, combs and wattles of several bird species have been shown to depend on gonadal steroids (Witschi, 1961; Haase, 1973). Melanin deposition in the bill of the house sparrow in response to androgens has been used as a sensitive specific and quantitative test for these hormones. Recently, however, Lofts, Mm-ton, and Thearle (1973) reported that relatively large doses of exogenous testosterone propionate had no significant effect on bill coloration in sexually regressed wild caught sparrows after a 4-wk treatment. Their results with gonadotropin and testosterone injections made them believe that bill pigmentation depends on a synergistic action of androgens and FSH. This possible involvement of a gonadotropic hormone is of interest for comparative endocrinologists since in other ploceids like Euplectes, Quelea, Steganura, ’ Dedicated 65th birthday.

and Passerina gonadotropins are known to cause the ornamental nuptial plumage while in Steganura paradisea the seasonal change in bill color is controlled by gonadotropins (Witschi, 1961). In Quelea quelea, another weaver finch, agressive behavior which in birds is generally attributed to androgens has been shown to depend directly on a gonadotropin (Lazarus and Crook, 1973). Therefore, it seems that some functions of gonadal steroids in birds are replaced by gonadotropins in certain weaver finches. However, the experiments of Lofts et al. ( 1973) left some methodological doubts and it seemed desirable to repeat the experiment using testosterone proprionate dissolved in oil instead of an aqueous suspension. Resorption of the hormone could be checked by measuring the diameter of the glomus tubules. It was also hoped that the experiments would throw some more light on the role of androgens in spermatogenesis. So far rather contradictory results have been reported. In some cases spermatogenesis

to Prof. Dr. 11.c. W. Herre on his 248

Copyright All rights

@ 1975 by Academic Press, Inc. of reproduction in any form reserved.

TESTOSTERONE

AND

BILL

was uninfluenced, depressed or retarded (Burger, 1944; Pfeiffer, 1947 ; Kumaran, and Turner, 1949; Lofts, 1962; Haase, 1973) by testosterone while in others it was stimulated (Lofts, 1962; Lofts et al., 1973). MATERIAL

AND METHODS

Twelve male house sparrows (Passer domesticus) were captured during the second half of October 1973 at Kiel. They were immediately transferred in pairs to wire cages (45 X 45 X 28 cm) and held on a short daylength (8L 16D) provided by 100 W incandescent lamps that produced 130-250 lx at the floors of the cages. Injections began on Nov. 19th. Six of the birds (group T) received 0.4 mg of testosterone propionate every other day by intramuscular or subcutanous injections in the pectoral region on alternating sides. During the first 2 wk the hormone was dissolved in 0. I ml sesame oil but since the birds seemed to have difficulties in resorbing this amount of oil, the solvent was later reduced to 0.05 ml. The other six birds were used as controls (group C) and received identical amounts of oil without hormone. The birds were killed after II injections. Their testes and glomi were weighed and fixed in Bouin’s mixture, embedded in paraffin, sectioned at 6 pm and stained with iron hematoxylin-orange G. PAS-hematoxylin, or Heidenhain’s azan. For determination of the width of the seminiferous tubules and of the glomus vesicles ten (testis) or five (glomus) cross-sectioned tubules from each specimen were measured.

RESULTS Bill color. At the start of the experiment most of the birds had bills with a dark (brown or black) tip and a lighter (light brown to pale yellow) base. There was, however, a considerable degree of variation: in a few birds even the tips were pale brown and in a single male the whole bill was black. This specimen (Cl) was put into the control group. By the fourth injection marked differences in bill color of the two groups could be observed. In the testosterone treated group the color of the tip had darkened and the dark area seemed to have extended. This was especially true for the lower jaw where a narrow black line could be detected. In the controls the bills showed no changes or a slight depigmentation. This could best be seen in

COLOR

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249

sparrow Cl which now had a narrow pale line at the base of the bill. After 2 wk of treatment the differences between the two groups were more pronounced. The testosterone treated birds had almost black ramphothecae, and some showed a relatively large lighter spot in the middle of the bill. In Cl the yellow line at the base of both jaws had extended to about 2 mm. At the end of the experiment (Fig. 1) the bills of group T were either completely black as in the natural breeding season, or black with brown cutting edges and a small dark brown spot in the middle. These latter males were the youngest birds of the group as judged by the incomplete pneumatisation of their frontal bones. Melanin deposition was not restricted to the external visible surfaces but included the interior parts of the bill (Fig. 2). In the controls a more or less pronounced depigmentation had occurred which was most obvious in those specimens which showed a relatively dark bill at the beginning of the experiment. Cl was no longer distinguishable from other animals of group C. Body wright. As can be seen from Table 1 testosterone did not result in an increase in body weight. Testes. Table 1 clearly demonstrates that testicular weight and diameter of the seminiferous tubules was not affected by

FIG. I. The beaks of all the birds at the end of the experiment. Upper half = group T. lower half = group C.

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EBERHARD

FIG. 2. Bills of a testosterone propionate treated (left) and a control male (right) cut open. to demonstrate the color change in the inner ramphothecea.

the testosterone treatment. In their histological appearance the seminiferous tubules of the two groups showed no differences. Generally the tubules were lined by Sertoli cells and one to two rows of spermatogonia. Spermatogonial mitoses were rare in both groups. A very small number of stage I spermatocytes were present in one testosterone treated and one control bird. Thus, a recrudescence of spermatogenetic activity was not observed. Within each group the interstitial tissue separating the tubules exhibited a high degree of individual variation in its thickness and it was impossible to detect clear differences between the two groups but typivoluminous Leydig cally differentiated, TABLE BODY WEIGHT, SEMINIFEROUS VESICLES

1

TESTES WEIGHT, TUBULES AND

OF

IN CONTROL AND TESTOSTERONE TREATED SPARROWS”

Group Body weight (g) Testes weight (mg) 4 Semin. tubules b-4 $J Glomus vesicles

(pm)

DIAMETER OF GLOMUS

C

Group

T

26.40 A 0.49 4.05 2 0.70

25.65 zt 0.58 3.52 k 0.79

39.13

t

1.39

41.65

-c 1.21

48.73

k 4.18

143.07

+ 6.026

n Mean and standard error of the mean. b Significantly different from control (P i

0.001).

HAASE

cells were absent. In the controls as well as in testosterone-treated birds some partially differentiated Leydig cells were observed. Compared to the most frequent small undifferentiated, fibroblast-like interstitial cells they were slightly enlarged and showed a less stainable cytoplasm and nudifferences cleus. Again no marked between the two groups could be found. Glomzzs. Testosterone treatment resulted in a highly significant increase in the diameter of the glomus tubules (Table 1). Moreover, the epithelium was activated and consisted of several rows of columnar cells. DISCUSSION

The present study confirms the earlier findings of Keck (1933, 1934), Pfeiffer et al. (1944), and Witschi (1961): bill color of the house sparrow is controlled by androgens. The negative results reported by Lofts et al. (1973) may be due to their method of steroid application. They used an aqueous suspension of testosterone propionate and the birds may have been unable to resorb the hormone from the crystals. Lofts et nl. did not appear to check the seminal glomus to make sure whether the androgen had reached the circulation. The positive results of these authors after a combined treatment with testosterone and FSH, or with the two gonadotropins, may possibly be explained on the basis of additive effects of these hormones on the circulating androgen level. On the other hand a number of observations leads to the contusion that in the birds used for the present study the plasma gonadotropin concentration must have been very low. From histochemical investigations of the pars distalis of Fringilla mont$ringilla it is known (Haase, 1973) that handling and injecting birds inhibits gonadotropin synthesis. The melanin deposition in the inner surfaces of the bill has to my knowledge not been described before. It may. however,

TESTOSTERONE

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BILL

be an important ethological mark in this species. House sparrows are known to frequently show the opened bill during aggressive and courtship behavior (Decker-t, 1969). As to the seminiferous tubules no differences were found between the control and testosterone injected birds, i.e., testosterone did not stimulate spermatogenesis of resting testes. Spermatogonial mitoses were rare and only a very low number of spermatocytes I could be detected in one control and one testosterone treated male. Differences in tubular diameter comparable to those described by Lofts et al. ( 1973) for control and androgen treated sparrows were seen within each group of the present study. These findings confirm the results of Pfeiffer (1947) and are in agreement with the thesis of Burger (1941X Pfeiffer (1947), and Lofts ( 1970) that androgens can stimulate spermatogenesis in birds only after the testes have attained a certain size and the germ cells a certain degree of maturation, the only valid exception being Q~rleu quelrn (Lofts, 1962). The stimulatory effect of testosterone propionate on the testes of hypophysectomized pigeons (Chu and You, 1946) has been shown in a small number of birds only and it is not certain whether pituitary regeneration occurred in these. BaylC. Kraus, and van Tienhoven ( 1970) could not confirm these results in the Japanese quail. Neither control nor testosterone-treated birds had mature Leydig cells in the interstitial tissue of their testes. A reduction of the interstitial cell nuclear size by testosterone treatment as it is described by Lofts et al. (1973) was not observed in the present study. This may be due to inhibitory effects of the control injections on the gonadotropin release of the control birds. The controls of Lofts et al. (1973) had not received any injections. According to my observations in Fringilla rnontijEngilla (Haase, 1973) an-

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other criterion for the activity of the testicular interstitial tissue, namely its expansion (Lofts et al. 1973, Murton, Lofts, and Westwood, 1970) is not reliable. The expansion of the interstitial tissue is inversely correlated to the diameter of the seminiferous tubules. In the spring the growing tubules compress the interstitial tissue and during the testicular regression in the summer the interstitial tissue expands. Bill color and glomus vesicle diameter clearly indicate that during its expansion phase the androgen production of the interstitial tissue ceases. REFERENCES Bayle.

J. D., Kraus. M., and Van Tienhoven, A. (1970). The effects of hypophysectomy and testosterone propionate on the testes of Japanese quail, Coturnix cofrurzix ,japonicu. J. Endocrinol. 46, 403-404. Burger, J. W. t 1944). Testicular response to androgen in the light-stimulated starling. EndwrinoloXy 35, 183-186. Burger, J. W. (194.5). Some effects of sex steroids on the gonads of the starling. Etldocrinology 37. 77-82. Chu. J. P. and You, B. S. (1946). Gonad stimulation by androgens in hypophysectomized pigeons. J. Etldocrinol. 4, 43 l-435. Deckert, G. t 1969). Zur Ethologie und Gkologie des Haussperlings (Pusser dornrsfic~ru L.). Beitr. Vogeikde. 15, I-84. Haase, E. ( 1973). Zur Kontrolle von Fortpflanzungszyklen bei Vogeln. Untersuchungen an Bergfinken. J. Camp. Physiol. 84, 375-43 I Keck, W. N. t 1933). Control of the bill color of the male English sparrow by injection of male hormone. Prw. Sot. Exp. Biol. Med. (NY) 30, 1140-l 141. Keck, W. N. (1934). The control of secondary sex characters in the English sparrow, Passer donzestic,m Linneaus. J. Exp. Zoo/. 67, 3 15-347. Kumaran, J. D. S. and Turner. C. W. ( 1949). The endocrinology of spermatogenesis in birds. II. Effect of androgens. Poult. Sci. 28, 739-746. Lazarus, J. and Crook, J. H. (1973). The effect of luteinizing hormone. oestrogen and ovariectomy on the agonistic behaviour of female Qrrelecr qu~,lecr. Anim. Belt. 21, 49-60. Lofts, B. ( 1962). The effects of exogenous androgens on the testicular cycle of the weaver-finch Quc~l~w qrrc/ru. Gen. Cotnp. Endocrinol. 2. 394-400.

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Lofts, B. (I 970). Cytology of the gonads and feedback mechanisms with respect to photosexual relationships in male birds. In “La Photoregulation de la Reproduction Chez les Oiseaux et les Mammiferes” (J. Benoit and I. Assenmacher, eds.), pp. 307-314. CNRS, Paris. Lofts, B., Murton, K. R.. and Thearle, R. J. P. (1973). The effects of testosterone propionate and gonadotropins on the bill pigmentation and testes of the house sparrow (Passer Jomeufic~s). Gen.

Comp.

Endocrinol.

21, 202-209.

Murton. R. K., Lofts, B., and Westwood, N. J. ( 1970). Manipulation of photorefractoriness in the house sparrow Passer domesticus by cir-

HAASE cadian light regimes. Gen. Comp. Endocrinol. 14, 107-l 13. Pfeiffer. A. C. ( 1947). Gonadotrophic effects of exogenous sex hormones on the testes of sparrows. Endocrinology 41, 92- 104. Pfeiffer. A. C.. Hooker. C. W., and Kirschbaum. A. (1944). Deposition of pigment in the sparrow’s bill in response to direct applications as a specific and quantitative test for androgen. Endocrinology

34, 389-399.

Witschi, E. ( 1961). Sex and secondary sexual chardcters. In “Biology and Comparative Physiology of Birds. II” (A. J. Marshall, ed.), pp. 1 15-168. Academic Press, New York.

The effects of testosterone propionate on secondary sexual characters and testes of house sparrows, Passer domesticus.

GENERAL AND COMPARATIVE 26, 248-252 ( 1975) ENDOCRINOLOGY The Effects of Testosterone Propionate on Secondary Sexual Characters and Testes of Hou...
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