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Effects of photoperiod and temperature on testicular and thyroid activity of the Japanese quail
GENERAL
AND
COMPARATIVE
ENDOCRINOLOGY
36, 250-2.54(1978)
Effects of Photoperiod and Temperature on Testicular Thyroid Activity of the Japanese Quail
and
T. OISHI~ AND T. KONHHI Kanebo Institute for Cancer Research, Misaki-cho, Hyogo-ku, Kobe 652, Japan Accepted May 29, 1978 The testes of Japanese quail (Cotmzix cotumix.juponicu) grow during a short photoperiod (8L: 16D) and reach maturation at IO to 12 weeks after hatching. When the ambient temperature was lowered from 23 to IO’ in this photoperiod, the size of the cloaca1 gland, a secondary sex character in Japanese quail, was significantly reduced. These involuted cloaca1 glands attained mature size after elevation of the ambient temperature to 23’. Mature cloaca1 glands during long photoperiods (16L:SD)remained unchanged by transferring birds to low temperature. These results indicate that ambient temperature as well as the length of photoperiod affect the testicular activity of Japanese quail and that the effect of the length of the photoperiod is predominant. Triiodothyronine (Ta) levels in serum were significantly increased by tow temperature and short photoperiod. Thyroxine (Td) levels were not different among the environmental conditions tested. The result suggests the existence of an inverse relationship between gonadal activity and TZ activity.
Compared to the intensive study of the effects of light on avian gonadal activity, investigation of the effects of other environmental factors is meager (Lofts, 197.5). Several papers reported that low ambient temperature retarded testicular growth and high temperature accelerated it (Burger, 1948, in starlings; Kendeigh, 1941, in English sparrows; Farner and Mewaldt, 1952, 1953, in white crowned sparrows; Engels and Jenner, 1956, in Juncos). However, Farner and Mewaldt (19.53) emphasized that elevation of environmental temperature has no effect when the photoperiod is below the stimulatory level. In Japanese quail, Konishi et a/. (1965) shotied that testes grew during short photoperiods when birds were kept at 2@, although the rate of growth was slow compared to that of birds subjected to long i Present address and address to which reprint requests should be sent: Department of Biology, Nara Women’s University, Kitauoyanishi-machi, Nara 630. Japan.
photoperiods. Maturation of testes in short photoperiods has been confirmed in our laboratory. However, Follett and Farner (1966) reported that the quail (Pullman strain) did now show gonadal development under 6L:lSD. Possible reasons for this discrepancy are discussed by Oishi (1978). The testes of mature birds in short photoperiods showed considerable regression when the birds were transferred to low ambient temperature (Kato and Konishi, 1968). Thyroid activity also seems to be affected both by photoperiod and temperature (Assenmacher, 1973). An inverse relationship between thyroid activity and gonadal activity has been reported in nonmigratory Indian finches (Thapliyal, 1969). The subject of this paper is an investigation of the effects of combinations of photoperiod and temperature on gonadal and thyroid activity. MATERIALS
250 00166480/78/0362-0250$01.00/0 Copyright @ I978 by Academic Press, Inc. All rights of reproduction in any form reserved.
AND METHODS
Japanese quail (Cotumi.x co&~G juponicu) origiUzura Co., Ltd. nally obtained from Nihon
PHOTOPERIOD
AND TEMPERATURE
(Toyohashi, Japan), and maintained in this institute for two generations were used. They were housed in individual cages, Sixteen hours of light and 8 hr of darkness (l6L:SD) and 8 hr of light and I6 hr of darkness (SL: l6D) were used as a long photoperiod and a short photoperiod, respectively. The intensity of the light was 180-450 lux (0,2-0.6 pW/cmZ at 600 nm) at the floor of the cages. The standard rearing temperature was 23 * 1.V. and the low temperature was IO % 1.0’. Water and food (pellet type, Nihon haigoshiryo Co., Ltd., Japan) were given ad /ibitum. Three experiments were conducted. In Experiment I. IO mature males which were reared under conditions of a short photoperiod at 23’ were exposed to low temperature (loo) from 39 weeks of age to 42 weeks. Birds which were kept under conditions of a short photoperiod and warm temperature served as controls (n = IO). In Experiment II, 30 quail which were maintained and matured under 8L:l6D at 23O for 20 weeks after hatching were divided into three groups. Group (I) was kept under the same conditions (8L:l6D, 23’). Group (2) was transferred to a low temperature condition (lp) and kept there for 7 weeks. Ciroup (3) was transferred to low temperature (IO”) and kept there for 3 weeks and then retransferred to high temperature (2Y) and kept there for 4 weeks. In Experiment III, quail kept under SL:l6D at 23’ for I4 weeks after hatching were divided into two groups. One group (n = IO) was kept under the same conditions. The other group (n = 20) was transferred to l6L:8D at 23’. After 4 weeks of the treatment, a subgroup of these was transferred to low temperature. In all the experiments, the size of the cloaca1 gland
a
251
(length x width x height), which is a convenient external indicator of testicular activity (Nagra er u/., 1959; Sachs, 1967: Siopes and Wilson. 1975) was measured. At the end of each experiment, testes weight was recorded, and blood was collected for the measurement of triiodothyronine (Td and thyroxine (T& Concentrations of Ts and Td in serum were measured by radioimmunoassay using TX RI,4 kits and ‘Ia RIA kits (Dainabot RI Laboratory, Tokyo, Japan). These kits measure total serum Ts and T+ The reliability of this radioimmunoassay was tested by several investigators (Mitsuma er a/., 1974; Nakajima et al.. 1977).
RESULTS AND I.?lSCUSSlON When mature birds kept under the short photoperiod and warm temperature condition were transferred to the low temperature condition, their cloaca1 glands showed considerable regression (Experiment I- Fig. la). The data of Experiment II confirmed the above results, in which birds were exposed to lowered temperature at 20 weeks of age (Fig. lb). Progressively regressing cloaca1 glands began SOgrow with an elevation of environmental temperature and attained mature size after 3 weeks. Cloaca1 glands of birds kept under conditions of a short photoperiod and law temperature remained small until the end of the experiment. The resuhs of Experiment I
b
-0
’
I
I
,
I
,
I
I
20
21
22
23
2&
25
26
27
AGE (WEEKS) FIG. I. Effect of temperature on the cloaca1 size in a short photoperiod. (a) Experiment I. White triangles and solid lines indicate SL: l6D at 23’. Black triangles and dotted lines indicate 8L: 16D at 10’. (b) Experiment II. White triangles and solid lines indicate 8L:l6D at 23’. Black triangles and dotted lines indicate 8L:l6D at tw.
252
OISHI
AND
r
10.0
~J--t
,;
’
’ 16 AGE
16
20
t
22
(WEEKS)
FIG. 2. Effect of temperature on the cloaca1 size in a long photoperiod. White circles and solid lines indicate 16L:SD at 23’. Black circles and dotted lines indicate 16L:SD at IO”. White triangles and broken lines indicate SL:l6D at 23”.
and II (Fig. 1) show that regression of cloaca1 glands under conditions of lowered temperature was not a temporary phenomenon and that shifting in ambient temperature per se influences testicular activity of quail in short photoperiods. However, low temperature did not induce regression of cloaca1 glands in mature birds in long photoperiods (Experiment III, Fig. 2). This suggests the effect of the TABLE
KONISHI
length of photoperiod on testular activity is predominant over ambient temperature. Dual control of testicular activity by photoperiod and temperature has been reported in the Cyprinid fish (Nufemigonus cv&eucus) (De Vlaming, 1975), in the Japanese quail (Kato and Konishi, 196S), and in golden hamsters (Me~~c~&&,s QUYQU.S, Waterhouse) (Hoffman et ul., 1965; Frehn and Liu, 1970). The combination of shortened photoperiod and cold temperature together produced additive effect on the testes of golden hamsters. This is interesting, because the results with Japanese quail reported here also showed additive effects of short photoperiod and low temperature on testicular involution. Triiodothyronine (T3) and thyroxine (T4) levels in the serum were measured at the end of Experiments I and III (Table I). Among the environmental conditions tested, birds kept under a short photoperiod and low temperature condition showed the highest level of T3. The difference between this group and birds kept under a warm temperature condition was highly significant (P < 0.01). In the long photoI
EFFECTS OF PHOTOPERIOD AND TEMPERATURE ON TESTES WEIGHT AND TRIIODOTHYRONINE (TJ AND THYROXINE (TJ LEVELS IN THE SERUMS
No. of Body weight birds Cd
Treatment Experiment SL: 16D 23= SL: 16D IO0
I
Experiment 16L:8D 23’ 16L:SD IO0 SL: 16D 23’
III
< 095. < 0.01. < 0.001.
Testes weight Cd
T3 (ng/lOO ml)
T4 (pg/ IO0 ml)
10
113.3 ? 4.1
3.43 k 0.42
2.493 5 0.223
163.9 2 23.6
2.38 T!Z0.03
IO
112.6 I? 2.2
0.61 k 0.05***
0.050 5 0.006***
228.8 k 8.7**
2.25 Z!I 0.03
IO
128.9 k 5.0
4.10 2 0.19
3.215 5 0.207
141.0 2 7.6
2.42 k 0.06
IO
118.6 * 3.4
4.14 k 0.22
3.437 5 0.176
195.5 ?x 12.8*
2.43 2 0.04
10
112.7 2 3.5
3.13 AI 0.50
2.812 2 0.504
179.3 zk 7.8*
2.38 2 0.05
u Results are given as means 2 SE. *P **P ***p
Cloaca1 size (cmS)
PHOTOPERIOD
AND TEMPERATURE
pe’riods, the Ta level was significantly higher with low temperature than that with warm temperature (p < 0.05). When the ambient temperature was 23O, the Ta level was also significantly higher in birds in the short photoperiod than in those in the long photoperiod (p c 0.0s). The values under SL:l6D and 23’ were almost the same in two experiments (I and III). An inverse relationship between the response of cloaca1 glands and that of Ts to photoperiod and temperature was clearly shown. The results suggest that short photoperiod and low temperature increase T13levels in the blood and that effects of photoperiod and temperature are additive. Intensive molting was observed in all the birds kept under conditions of a short photoperiod and low temperature. Radioimmunoassayable Te in the serum was not significantly different in birds under the different conditions of photoperiod and temperature tested, while Ts levels were shown to fluctuate depending on the environmental conditions. In this context, it is interesting to note the report by Bobek et a/. (1977), who showed that the coefficients of correlation between oxygen consumption and TZsand Th concentration in different age groups of chickens oscillated from 0.78 to 0.9s and 0.19 to -0.63, respectively. These results support the hypothesis that triiodothyronine is the active thyroid hormone and that thyroxine serves mainly as prohormone (Oppenheimer et ul., 1972). The effects of environmental factors on the thyroid gland of Japanese quail have been reported by several authors. Long-day treatment markedly depressed thyroidal ‘s’I uptake in female Japanese quail (Follett and Riley, 1967). There was a tendency for Japanese quail to show higher thyroid weight in short photoperiods in comparison with long photoperiods (Oishi and Lauber, 1974). McFarland et ui. (1966) measured a decrease in the half-life of radiothyroxine in Japanese quail under low temperature conditions. However, a combined effect of
253
photoperiod and temperature on thyroid activity has not been reported. The inverse relationship between testicular activity and Ts levels in the serum is consistent with following reports, although the relationship between thyroid gland and serum Ts level has to be clarified. Thapliyai (1969) reported that annual gonadal size and activity cycles of the nonmigratory Indian finches (La1 Munia and Spotted Munia) are inversely related to thyroid activity cycles. Furthermore, he showed that thyroidectomy induced gonadal recrudescence and thyroxine treatment reduced gonadal activity. Hypothyroidism induced by propylthiouracil and thyroidectomy produced a significant increase in the uptake of :%P by the testes of young chicks (Lehman, 1970; Lehman and Frye. 1976). Wieselthier and Van Tier&oven (1972) reported that thyroidectomy of the starling prior to exposure to a long photoperiod (17L:7D) re,sulted in a failure of the testes to regress after an initial size increase- Lowered plasma testosterone concentration and an enhanced metabolic clearance rate was induced by thyroxine administration (Jailageas and Assenmacher, 1974). Further experiments will determine whether the inverse relationship between testicular activity and Ts level of Japanese quail is due to the direct interaction of hormones, due to an effect involving feedback to the pituitary or hypothalamus, or due to a coincidental relationship. ACKNOWLEQGMENTS We are grateful to Dr. J. Vriend for the critical reading of the manuscript. We also thank Miss T. Minamino, Miss M. Nemoto and Mr. T. Himoto for the technical assistance.
REFERENCES Assenmacher. I. (1973). The peripheral endocrine glands. In .‘Avian Biology” (D. S. Farner and J. R. King, eds.), Vol. 3, pp. l83-2g6. Academic Press. New York and London. Bobek, S., Jastrzebski, M., and Pietras. M. (1977). Age-related changes in oxygen consumption and
254
OISHI
AND
plasma thyroid hormone concentration in the young chicken. Gen. Camp. Endocrinol. 31, 169-174. Burger, J. W. (1948). The relation of external temperature to spermatogenesis in the male starling. .I. Exp. Zool. 109, 259-266. De Vlaming, V. L. (1975). Effects of photoperiod and temperature on gonadal activity in the Cyprinid teleost, Notemigonus crysoleucas. Biol. Bull. 148, 402-415.
Engels, W. L., and Jenner, C. E. (1956). The effect of temperature on testicular recrudescence in Juncos at different photoperiods. Biol. Bull. 110, 129-137. Farner, D. S., and Mewaldt, L. R. (1952). The relative roles of photoperiod and temperature in gonadal recrudescence in male Zonotrichia ieucophrys gambelii. Anat. Rec. 113, 612. Farner, D. S., and Mewaldt, L. R. (1953). The relative roles of diurnal periods of activity and diurnal photoperiods in gonadal activation in male Zonotrichia leucophrys gambelii (Nuttall). Experientia 9, 2 19-22 I. Follett, B. K., and Farner, D. S. (1966). The effects of the daily photoperoid on gonadal growth, content, and neurohypophysial hormone nemosecretion in the hypothalamo-hypophyseal system of the Japanese quail (Cotarnix coturnix japonica). Gen. Comp. Endoerinol. 7, I I l-124. Follett, B. K., and Riley, J. (1967). Effect of the length of the daily photoperoid on thyroid activity in the female Japanese quail (Coturnix coturnix japonica). .I. Endocrinol. 39, 615-616 Frehn, J. L., and Liu, C.-C. (1970). Effects of temperature, photoperoid, and hibernation on the testes of golden hamsters. .I. Exp. Zoo/. 174, 317-324. Hoffman, R. A., Hester, R. J., and Towns, C. (1965). Effect of light and temperature on the endocrine system of the golden hamster (Mesocricetus aurams, Waterhouse). Comp. Biochem. Physiol. 15, 525-533. Jallageas. M., and Assenmacher, I. (1974). Thyroid gonadal interactions in the male domestic duck in relationship with the sexual cycle. Gen. Comp. Endocrinol. 22, 13-20. Kate, M., and Konishi, T. (1968). The effect of light and temperature on the testicular growth of the Japanese quail. Pot&. Sri. 47, 1052-1056. Kendeigh, S. C. (1941). Length of day and energy requirements for gonad development and egglaying in birds. Ecology 22, 237-248. Konishi, T., Ishiguro, T., and Kate, M. (1965). Photoperiodical studies on the testicular development of Japanese quail. Zool. Mug. 74, 54-62.
KONISHI
Lehman, G. C. (1970). The effects of hype- and hyperthyroidism on the testes and anterior pituitary glands of cockerels. Gen. Comp. Endocrinol. 14, 567-577. Lehman, G. C., and Frye, B. E. (1976). The effects of changes in thyroid function on testes zzP uptake and the response to gonadotropin in the chick. Gen. Comp. Endocrinol. 28, 446-453. Lofts, B. (1975). Environmental control of reproduction. Zn “Avian Physiology” (M. Peaker, ed.), pp. 117-197. Academic Press, New York. McFarland, L. Z., Yousef, M. R., and Wilson, W. 0. (1966). The influence of ambient temperature and hypothalamic lesions on the disappearance rate of thyroxine ‘s’J in the Japanese quail. L$e Sci. 5, 309-315. Mitsuma, T., Hirooka, Y., and Nihei, R. (1974). Radioimmunoassay of triiodothyronine (Ts)-test of Dinabot kits. Horumon To Rinshyo 22, 557562. Nagra, C. L., Meyer, R. K., and Bilstad, N. (1959). Cloaca1 glands in Japanese quail (Coturnix coturnixjaponica): Histogenesis and response to sex steroids. Anat. Rec. 133, 415. Nakajima, T., Yagi, Y., Yamamoto, T., Furuichi, Y., Nishikawa, Y., and Tsuchida, T. (1977). Test of T4-RIA (PEG). Rinshyo To Kenkyu 54, 13381341. Oishi, T. (1978). Effect of short days in the photoperiodic testicular response of Japanese quail. Environ. Control Biol., 16, 35-40. Oishi, T., and Lauber, J. K. (1974). Pineal control of photoendocrine response in growing Japanese quail. Endocrinology 94, 1731-1734. Oppenheimer, J. H., Schwartz, H. L., and Surks, M. I. (1972). Propylthiouracil inhibits the conversion of L-triiodothyronine; an explanation of the antithyroxine effect of propylthiouracil and evidence supporting the concept that triiodothyronine is the active thyroid hormone. J. Clin. Znvest. 51, 2493-2497. Sachs, B. D. (1967). Photoperiodic control of the cloaca1 gland of the Japanese quail. Science 157, 201-203. Siopes, T. D., and Wilson, W. 0. (1975). The cloaca1 gland-an external indicator of testicular development in Coturnix. Pouh. Sci. 54, 1225- 1229. Thapliyal, J. P. (1969). Thyroid in avian reproduction. Gen. Comp. Endocrinol. Suppl. 2, 111-122. Wieselthier, A. S., and Van Tienhoven, A. (1972). The effect of thyroidectomy on testicular size and on the photorefractory period in the starling (Starnus vulgaris L.). J. Exp. Zooi. 179, 331-338.
AND
COMPARATIVE
ENDOCRINOLOGY
36, 250-2.54(1978)
Effects of Photoperiod and Temperature on Testicular Thyroid Activity of the Japanese Quail
and
T. OISHI~ AND T. KONHHI Kanebo Institute for Cancer Research, Misaki-cho, Hyogo-ku, Kobe 652, Japan Accepted May 29, 1978 The testes of Japanese quail (Cotmzix cotumix.juponicu) grow during a short photoperiod (8L: 16D) and reach maturation at IO to 12 weeks after hatching. When the ambient temperature was lowered from 23 to IO’ in this photoperiod, the size of the cloaca1 gland, a secondary sex character in Japanese quail, was significantly reduced. These involuted cloaca1 glands attained mature size after elevation of the ambient temperature to 23’. Mature cloaca1 glands during long photoperiods (16L:SD)remained unchanged by transferring birds to low temperature. These results indicate that ambient temperature as well as the length of photoperiod affect the testicular activity of Japanese quail and that the effect of the length of the photoperiod is predominant. Triiodothyronine (Ta) levels in serum were significantly increased by tow temperature and short photoperiod. Thyroxine (Td) levels were not different among the environmental conditions tested. The result suggests the existence of an inverse relationship between gonadal activity and TZ activity.
Compared to the intensive study of the effects of light on avian gonadal activity, investigation of the effects of other environmental factors is meager (Lofts, 197.5). Several papers reported that low ambient temperature retarded testicular growth and high temperature accelerated it (Burger, 1948, in starlings; Kendeigh, 1941, in English sparrows; Farner and Mewaldt, 1952, 1953, in white crowned sparrows; Engels and Jenner, 1956, in Juncos). However, Farner and Mewaldt (19.53) emphasized that elevation of environmental temperature has no effect when the photoperiod is below the stimulatory level. In Japanese quail, Konishi et a/. (1965) shotied that testes grew during short photoperiods when birds were kept at 2@, although the rate of growth was slow compared to that of birds subjected to long i Present address and address to which reprint requests should be sent: Department of Biology, Nara Women’s University, Kitauoyanishi-machi, Nara 630. Japan.
photoperiods. Maturation of testes in short photoperiods has been confirmed in our laboratory. However, Follett and Farner (1966) reported that the quail (Pullman strain) did now show gonadal development under 6L:lSD. Possible reasons for this discrepancy are discussed by Oishi (1978). The testes of mature birds in short photoperiods showed considerable regression when the birds were transferred to low ambient temperature (Kato and Konishi, 1968). Thyroid activity also seems to be affected both by photoperiod and temperature (Assenmacher, 1973). An inverse relationship between thyroid activity and gonadal activity has been reported in nonmigratory Indian finches (Thapliyal, 1969). The subject of this paper is an investigation of the effects of combinations of photoperiod and temperature on gonadal and thyroid activity. MATERIALS
250 00166480/78/0362-0250$01.00/0 Copyright @ I978 by Academic Press, Inc. All rights of reproduction in any form reserved.
AND METHODS
Japanese quail (Cotumi.x co&~G juponicu) origiUzura Co., Ltd. nally obtained from Nihon
PHOTOPERIOD
AND TEMPERATURE
(Toyohashi, Japan), and maintained in this institute for two generations were used. They were housed in individual cages, Sixteen hours of light and 8 hr of darkness (l6L:SD) and 8 hr of light and I6 hr of darkness (SL: l6D) were used as a long photoperiod and a short photoperiod, respectively. The intensity of the light was 180-450 lux (0,2-0.6 pW/cmZ at 600 nm) at the floor of the cages. The standard rearing temperature was 23 * 1.V. and the low temperature was IO % 1.0’. Water and food (pellet type, Nihon haigoshiryo Co., Ltd., Japan) were given ad /ibitum. Three experiments were conducted. In Experiment I. IO mature males which were reared under conditions of a short photoperiod at 23’ were exposed to low temperature (loo) from 39 weeks of age to 42 weeks. Birds which were kept under conditions of a short photoperiod and warm temperature served as controls (n = IO). In Experiment II, 30 quail which were maintained and matured under 8L:l6D at 23O for 20 weeks after hatching were divided into three groups. Group (I) was kept under the same conditions (8L:l6D, 23’). Group (2) was transferred to a low temperature condition (lp) and kept there for 7 weeks. Ciroup (3) was transferred to low temperature (IO”) and kept there for 3 weeks and then retransferred to high temperature (2Y) and kept there for 4 weeks. In Experiment III, quail kept under SL:l6D at 23’ for I4 weeks after hatching were divided into two groups. One group (n = IO) was kept under the same conditions. The other group (n = 20) was transferred to l6L:8D at 23’. After 4 weeks of the treatment, a subgroup of these was transferred to low temperature. In all the experiments, the size of the cloaca1 gland
a
251
(length x width x height), which is a convenient external indicator of testicular activity (Nagra er u/., 1959; Sachs, 1967: Siopes and Wilson. 1975) was measured. At the end of each experiment, testes weight was recorded, and blood was collected for the measurement of triiodothyronine (Td and thyroxine (T& Concentrations of Ts and Td in serum were measured by radioimmunoassay using TX RI,4 kits and ‘Ia RIA kits (Dainabot RI Laboratory, Tokyo, Japan). These kits measure total serum Ts and T+ The reliability of this radioimmunoassay was tested by several investigators (Mitsuma er a/., 1974; Nakajima et al.. 1977).
RESULTS AND I.?lSCUSSlON When mature birds kept under the short photoperiod and warm temperature condition were transferred to the low temperature condition, their cloaca1 glands showed considerable regression (Experiment I- Fig. la). The data of Experiment II confirmed the above results, in which birds were exposed to lowered temperature at 20 weeks of age (Fig. lb). Progressively regressing cloaca1 glands began SOgrow with an elevation of environmental temperature and attained mature size after 3 weeks. Cloaca1 glands of birds kept under conditions of a short photoperiod and law temperature remained small until the end of the experiment. The resuhs of Experiment I
b
-0
’
I
I
,
I
,
I
I
20
21
22
23
2&
25
26
27
AGE (WEEKS) FIG. I. Effect of temperature on the cloaca1 size in a short photoperiod. (a) Experiment I. White triangles and solid lines indicate SL: l6D at 23’. Black triangles and dotted lines indicate 8L: 16D at 10’. (b) Experiment II. White triangles and solid lines indicate 8L:l6D at 23’. Black triangles and dotted lines indicate 8L:l6D at tw.
252
OISHI
AND
r
10.0
~J--t
,;
’
’ 16 AGE
16
20
t
22
(WEEKS)
FIG. 2. Effect of temperature on the cloaca1 size in a long photoperiod. White circles and solid lines indicate 16L:SD at 23’. Black circles and dotted lines indicate 16L:SD at IO”. White triangles and broken lines indicate SL:l6D at 23”.
and II (Fig. 1) show that regression of cloaca1 glands under conditions of lowered temperature was not a temporary phenomenon and that shifting in ambient temperature per se influences testicular activity of quail in short photoperiods. However, low temperature did not induce regression of cloaca1 glands in mature birds in long photoperiods (Experiment III, Fig. 2). This suggests the effect of the TABLE
KONISHI
length of photoperiod on testular activity is predominant over ambient temperature. Dual control of testicular activity by photoperiod and temperature has been reported in the Cyprinid fish (Nufemigonus cv&eucus) (De Vlaming, 1975), in the Japanese quail (Kato and Konishi, 196S), and in golden hamsters (Me~~c~&&,s QUYQU.S, Waterhouse) (Hoffman et ul., 1965; Frehn and Liu, 1970). The combination of shortened photoperiod and cold temperature together produced additive effect on the testes of golden hamsters. This is interesting, because the results with Japanese quail reported here also showed additive effects of short photoperiod and low temperature on testicular involution. Triiodothyronine (T3) and thyroxine (T4) levels in the serum were measured at the end of Experiments I and III (Table I). Among the environmental conditions tested, birds kept under a short photoperiod and low temperature condition showed the highest level of T3. The difference between this group and birds kept under a warm temperature condition was highly significant (P < 0.01). In the long photoI
EFFECTS OF PHOTOPERIOD AND TEMPERATURE ON TESTES WEIGHT AND TRIIODOTHYRONINE (TJ AND THYROXINE (TJ LEVELS IN THE SERUMS
No. of Body weight birds Cd
Treatment Experiment SL: 16D 23= SL: 16D IO0
I
Experiment 16L:8D 23’ 16L:SD IO0 SL: 16D 23’
III
< 095. < 0.01. < 0.001.
Testes weight Cd
T3 (ng/lOO ml)
T4 (pg/ IO0 ml)
10
113.3 ? 4.1
3.43 k 0.42
2.493 5 0.223
163.9 2 23.6
2.38 T!Z0.03
IO
112.6 I? 2.2
0.61 k 0.05***
0.050 5 0.006***
228.8 k 8.7**
2.25 Z!I 0.03
IO
128.9 k 5.0
4.10 2 0.19
3.215 5 0.207
141.0 2 7.6
2.42 k 0.06
IO
118.6 * 3.4
4.14 k 0.22
3.437 5 0.176
195.5 ?x 12.8*
2.43 2 0.04
10
112.7 2 3.5
3.13 AI 0.50
2.812 2 0.504
179.3 zk 7.8*
2.38 2 0.05
u Results are given as means 2 SE. *P **P ***p
Cloaca1 size (cmS)
PHOTOPERIOD
AND TEMPERATURE
pe’riods, the Ta level was significantly higher with low temperature than that with warm temperature (p < 0.05). When the ambient temperature was 23O, the Ta level was also significantly higher in birds in the short photoperiod than in those in the long photoperiod (p c 0.0s). The values under SL:l6D and 23’ were almost the same in two experiments (I and III). An inverse relationship between the response of cloaca1 glands and that of Ts to photoperiod and temperature was clearly shown. The results suggest that short photoperiod and low temperature increase T13levels in the blood and that effects of photoperiod and temperature are additive. Intensive molting was observed in all the birds kept under conditions of a short photoperiod and low temperature. Radioimmunoassayable Te in the serum was not significantly different in birds under the different conditions of photoperiod and temperature tested, while Ts levels were shown to fluctuate depending on the environmental conditions. In this context, it is interesting to note the report by Bobek et a/. (1977), who showed that the coefficients of correlation between oxygen consumption and TZsand Th concentration in different age groups of chickens oscillated from 0.78 to 0.9s and 0.19 to -0.63, respectively. These results support the hypothesis that triiodothyronine is the active thyroid hormone and that thyroxine serves mainly as prohormone (Oppenheimer et ul., 1972). The effects of environmental factors on the thyroid gland of Japanese quail have been reported by several authors. Long-day treatment markedly depressed thyroidal ‘s’I uptake in female Japanese quail (Follett and Riley, 1967). There was a tendency for Japanese quail to show higher thyroid weight in short photoperiods in comparison with long photoperiods (Oishi and Lauber, 1974). McFarland et ui. (1966) measured a decrease in the half-life of radiothyroxine in Japanese quail under low temperature conditions. However, a combined effect of
253
photoperiod and temperature on thyroid activity has not been reported. The inverse relationship between testicular activity and Ts levels in the serum is consistent with following reports, although the relationship between thyroid gland and serum Ts level has to be clarified. Thapliyai (1969) reported that annual gonadal size and activity cycles of the nonmigratory Indian finches (La1 Munia and Spotted Munia) are inversely related to thyroid activity cycles. Furthermore, he showed that thyroidectomy induced gonadal recrudescence and thyroxine treatment reduced gonadal activity. Hypothyroidism induced by propylthiouracil and thyroidectomy produced a significant increase in the uptake of :%P by the testes of young chicks (Lehman, 1970; Lehman and Frye. 1976). Wieselthier and Van Tier&oven (1972) reported that thyroidectomy of the starling prior to exposure to a long photoperiod (17L:7D) re,sulted in a failure of the testes to regress after an initial size increase- Lowered plasma testosterone concentration and an enhanced metabolic clearance rate was induced by thyroxine administration (Jailageas and Assenmacher, 1974). Further experiments will determine whether the inverse relationship between testicular activity and Ts level of Japanese quail is due to the direct interaction of hormones, due to an effect involving feedback to the pituitary or hypothalamus, or due to a coincidental relationship. ACKNOWLEQGMENTS We are grateful to Dr. J. Vriend for the critical reading of the manuscript. We also thank Miss T. Minamino, Miss M. Nemoto and Mr. T. Himoto for the technical assistance.
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