Role of gonadal feedback in annual reproduction of the weaver bird: Interaction with photoperiod

GENERAL

AND

COMPARATIVE

Role of Gonadal

ENDOCRINOLOGY

Feedback in Annual Reproduction Bird: Interaction with Photoperiod

SUSHAMA Department

45, 521-526 (1981)

SINGH NEE PAVGI

of Zoology,

Banaras

Hindu

of the Wea .ver

AND ASHA CHANDOLA University,

Varanasi-221

005, India

Accepted April 14, 1981 Involvement of gonadal steroids in the annual reproduction of the weaver bird has been demonstrated by castration experiments. Castration renders the pituitary acyclic, as observed by LH-dependent yellow nuptial plumage, indicating the role of gonads in seasonal decline of pituitary activity. It was also evident from the results of castration performed at different months that sensitivity of the hypothalamo- hypophyseal system to negative feedback of testicular hormones changes with the phase of the reproductive cycle. The initiation of pituitary activity in this bird seems to be direct effect of photostimulation and not a consequence of altered sensitivity of the pituitary or the hypothalamus to gonadal steroids. Gonadal steroids appear to interfere with/alter the photoresponse of this bird. The annual reproduction in the weaver bird seems to be a result of interaction between steroidal feedback and the day length.

In weaver birds, Ploceus philippinus, as in other photoperiodic birds (Follett, 1977, 1978) the hypothalamohypophyseal-gonadal system is stimulated by long day length and inhibited by short day length (Thapliyal and Saxena, 1964; Thapliyal and Tewary, 1964; Singh and Chandola, 1981). Experimental photoresponses suggest a definite photoperiodic requirement for gonadal growth in weaver birds which lies between 11 and 12 hr. Gonadal development does not occur until this threshold is reached whether naturally or under artificial conditions. Birds enter reproduction with the increasing day length of spring, indicating that day length might serve as a stimulus for annual gonadal development and activity. However, gonads regress soon after summer solstice when day length is decreasing but is still longer than the photoperiodic response threshold (Singh and Chandola, 1981). Obviously, for gonadal regression factors other than photoperiod are involved. In the present study the role of negative steroidal feedback in the annual reproductive cycle of weaver bird has been investigated. An interaction of photoperiodic effects and castration was also studied.

MATERIALS

AND METHODS

Weaver birds exhibit a sexual dimorphism during the breeding period, the male having a bright yellow nuptial plumage and a black beak. The yellow plumage in the weaver bird, as in many other finches (Witschi, 1955), is LH dependent (Thapliyal and Saxena, 1961) and seems to be a good indicator of increased LH release in circulation. Normal females lack the nuptial plumage. In the present study the appearance of yellow plumage was taken as an index of pituitary activity. Birds were captured from nature near Varanasi (longitude 83”l’ E; latitude 25”18’ N) and after acclimatisation for a fortnight were laparotomized and sexed. Initial observations on gonadal volume, plumage, and beak coloration were taken and birds then placed in experiments. The experiments were divided into three series. (I) Effect of castration in November on the subsequent plumage cycle of the weaver bird. Twenty male birds were divided into two groups. Birds in group 1 were castrated bilaterally, in November, group 2 served as intact controls. Monthly observations on plumage coloration and beak pigmentation were taken over a period of 12 months. performed at different (10 Elf ec t o f castration months on plumage coloration of weaver bird. Fifteen to twenty adult male birds were castrated bilaterally every month over a period of 1 year. Observations on regenerating plumage color and beak pigmentation were then made monthly. (ZZI) Interaction of castration and photoperiod. This experiment was performed at two phases of the

521 0016~6480/81/120521-06$01.00/O Copyright @ 1981 by Academic Press, Inc. All rights of reproduction in any form reserved.

522

PAVGI

AND

CHANDOLA

TABLE

I Treatment

Time of the year

May

September

No. of birds in each group A

B

Gonadal condition

Photoperiod (hr)

10 10 12 12 12 12

NDL NDL SDL SDL LDL LDL

(6L118D) (6W18D) ( 15L/9D) (15L/9D)

12 12 10 10 10 10

NDL NDL SDL SDL LDL LDL

(6Wl8D) (6L/18D) (15W9D) (lSL/9D)

reproductive cycle: May, when the birds were in breeding state, and September, when breeding had terminated and the birds were sexually quiescent. Birds were subjected to the following treatments (Table 1). Photoperiodic treatments were begun on the day of castration and monthly observations on regenerating plumage coloration and beak pigmentation made for the following 5 months. Light-treated birds were placed in light-proof chambers fitted with fluorescent tubes. The light intensity at perch level was approximately 300 lx. All the birds were provided with paddy (Oryza sativa) and water ad libitum. Data on plumage coloration were expressed as the percentage of birds regenerating yellow plumage.

RESULTS

(I) Effect of Castration in November on the Subsequent Plumage Cycle oj’the Weaver Bird Results are summarized in Fig. I. In castrated adult male birds dull-type plumage appeared through each regeneration from November to April. In may, however, yellow plumage appeared in 37% of the birds and by June all the birds regenerated a yellow plumage this was maintained through each successive regeneration until October when observations were terminated. Throughout no pigmentation of the beak took place. Intact birds exhibited dull plumage from November to March but in April 15% of the

(Normal day length)

birds regenerated yellow plumage. Appearance of yellow plumage occurred in all intact birds in May and was maintained in the next regeneration in June. In July the percentage of yellow plumage-regenerating birds was 72% and this decreased further to 62% in August. Dull plumage appeared in all the birds in September, and also in October. Beak pigmentation was initiated in May, intensified in June and the beak turned black. Lightening of the beak occurred in August and by September the beak had lost its pigment. (II) Effect of Castration Performed Different Months on Plumage Coloration

at

Figure 2 shows the mean percentage of birds regenerating yellow plumage. Birds castrated from November to April showed the first appearance of yellow plumage in May, though in May itself not all the birds regenerated yellow plumage. In June, yellow plumage appeared in all birds including those castrated in May. Among the birds castrated in June, when gonads attain or have already attained maximum activity, two types of responses were obtained. In those birds having gonads of largest size (initial mean testicular volume 40.64 ?

INTERACTION

OF GONADAL

FEEDBACK

WITH

PHOTOPERIOD

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1. Plumage cycle of intact and castrated male weaver birds in normal day length.

3.30), dull-type plumage appeared in the next regeneration but in those in which gonads were smaller (initial mean testicular volume 12.62 k 5.23), yellow plumage appeared. Castration in July or later caused regeneration of dull plumage. Once yellow plumage appeared it was maintained through successive regenerations.

(III) Interaction of Castration and Photoperiod Short day length @L/180). Intact

birds when subjected to 6LI18D in May or September regenerated dull plumage through each monthly regeneration (Fig. 3). Birds castrated in May when subjected to short photoperiod exhibited yellow plumage through each regeneration (Fig. 3a). How-

00 MONTHS

FIG.

2. Effect of castration on plumage of male weaver birds during different months.

524

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AND

CHANDOLA

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3 months to stimulate yellow plumage and ever, the response of castrates in September to 6L/18D was similar to that of in- blackening of beak in birds with intact tact birds and these castrates regenerated gonads (Fig. 3b). But in castrated birds dull plumage (Fig. 3b). maintained on 15L/9D yellow plumage apIn castrated as well as intact birds of both ’ peared in the first regeneration (within a months, i.e., May and September, the beak month) and was maintained thereafter. eventually turned straw colored. However, the beak turned straw colored in Long day length (15L/9D). The effects of the absence of the testes. long photoperiod upon plumage coloration DISCUSSION were similar in both castrated and intact birds in May (Fig. 3a). Both groups exhibResults of experiment I indicate that ited persistent yellow plumage through re- castration renders the pituitary acyclic by peated regenerations. abolishing seasonal decline of pituitary acThe beaks of the intact birds turned to- tivity, as demonstrated by persistent yellow tally black whereas those of castrated birds plumage. This indicates that steroidal feedlost all their pigment. back is involved in seasonal inhibition of In September long photoperiods required the hypothalamohypophyseal-gonadal

INTERACTION

OF

GONADAL

FEEDBACK

system of the weaver bird. It may be mentioned that yellow plumage is only a qualitative parameter, the possibility of a fall in LH levels remains. From the results of experiment II it is evident that the sensitivity of the hypothalamo- hypophyseal system to negative feedback of testicular hormones changes with the phase of the reproductive cycle. During the progressive phase (April/May) castration stimulated the yellow plumage, but it was ineffective once breeding was terminated. Yellow plumage, however, makes its appearance spontaneously in the next breeding season despite the absence of gonads. Apparently the initiation of pituitary activity in this case is not dependent on the gonadal steroids. This finding is significant in view of the fact that in birds held under normal conditions also nuptial plumage first makes its appearance in April when day length is increasing. The initiation of pituitary activity therefore appears to be a consequence of direct photostimulation and not a consequence of altered sensitivity of the pituitary or hypothalamus to gonadal steroids. Similar observations have been made in quail, red grouse, tree sparrow, and willow ptarmigan (Gibson et al., 1975; Sharp and Moss, 1977; Wilson and Follett, 1974; Stokkan and Sharp, 1980a,b). Results of experiment III demonstrate the interaction between castration and photoperiod. The birds castrated in May (breeding phase) when exposed to inhibitory short photoperiod of 6L/18D continued to regenerate LH dependent yellow plumage (Fig. 3). But in September (quiescent phase) the castrated birds exposed to 6L/18D did not show pituitary stimulation even after 6 months of treatment. Steroidal feedback overrides the nonstimulatory effects of short photoperiod if the pituitary has already been stimulated. But it can not restimulate the pituitary activity once gonads have regressed.

WITH

PHOTOPERIOD

525

The birds castrated in May and maintained in NDL or exposed to long photoperiod ( 15L/9D) continued to regenerate yellow plumage like that in the intact birds. When castration was performed in September, birds in NDL did not regenerate yellow plumage. Intact birds exposed to long photoperiod developed yellow plumage after a delay of 3 months (Fig. 3). This delay in photoresponse was abolished (yellow plumage regenerated within a month) when birds were castrated and exposed to long photoperiod. Obviously gonadal steroids interfere with/alter the photoresponse of this bird. This might also explain the failure of pituitary to respond to castration during postnuptial period when the day length is still stimulatory. The enhanced circulating sex steriods of breeding period might render the neuroendocrine unit less sensitive to light by setting the photoperiodic response threshold at a higher level. Decreasing photoperiod thus would be insufficient to stimulate the hypothalamohypophyseal complex having a higher photoperiodic requirement than the available photoperiod. This might explain the regression in the natural reproductive cycle also. In this bird initiation of the hypothalamo- hypophyseal gonadal system requires external photoperiodic stimulus. The increasing day length of spring would provide a constant stimulus to the hypothalamohypophyseal complex not allowing the negative feedback to be operative, resulting in complete gonadal development. Gonads attain maximum activity by summer solstice, when the day length at Varanasi is 13.34 hr and regression sets in soon after that. Apparently the longest day length at Varanasi may not be sufficient to check the feedback at high steriod level, as a result of which hypothalamo-hypophyseal activity terminates. Although the day length is still stimulatory the birds fail to respond most likely because the neuroen-

526

PAVGI

AND

docrine system is rendered less sensitive to light by steriods. Thus in nature the annual reproductive cycle may be a result of an interaction between steroidal feedback and day length. ACKNOWLEDGMENTS

REFERENCES Follett, B. K. ( 1977). The neuroendocrinology of photoperiodism in birds. In “Proc. First Int. Symp. Avian Endocrinol., Calcutta, 1977” (B. K. Follett, ed.), pp. 20-22. Bangor. Follett, B. K. (1978). Photoperiodism and seasonal breeding in birds and mammals. In “Control of Ovulation” (D. B. Crighton, G. R. Foxcroft, N. E. Haymes, and G. E. Lamming, eds.), pp. 267-293. Butterworths, London. Gibson, W. R., Follett, B. K., and Gledhill, B. (1975). Plasma levels of luteinizing hormone in gonadectomized Japanese quail exposed to short or to long daylengths. J. EndocrinoL 64, 87- 101. Sharp, P. J., and Moss, R. (1977). The effects of castration on concentrations of leuteinizing hormone in the plasma of photorefractory red grouse (Lagopus 289-293.

scoticus).

Con.

Comp.

Endocrinol.

Singh, S., and Chandola, A. (1981). Photoperiodic control of seasonal reproduction in tropical weaver bird. J. Exp. Zool. 216, 293-298. Stokkan, K. A. and Sharp, P. J. (1980a). The roles of day length and the testis in the regulation of plasma LH levels in photosensitive and photorefractory willow ptarmigan (Lagopus lagopus lagopus).

Financial support from U .G.C., INSA, D.A.E., and a Senior Research Fellowship of the Programme of Special Assistance, U.G.C. (to S.S.), are gratefully acknowledged.

lagopus

CHANDOLA

32,

Gen.

Comp.

Endocrinol.

41, 520-526.

St o kk an, K. A. and Sharp, P. J. ( 1980b). The development of photorefractoriness in willow ptarmigan (Lagopus lagopus lagopus) after the suppression of photoinduced LH release with implants of testosterone. Gen. Comp. Endocrinol. 41, 527-530. Thapliyal, J. P. and Saxena, R. N. (1961). Plumage control in Indian weaver bird (Hoceus philippinus). Naturwiss 24, 741-742. Thapliyal, J. P., and Saxena, R. N . (1964). Absence of refractory period in the common weaver bird. Condor 66, 199- 208. Thapliyal, J. P., and Tewary, P. D. (1964). Effect of light on the pituitary, gonad and plumage pigmentation in the Avadavat (Esrrildu amandava) and Baya weaver (Ploceus philippinus) Proc. 2001. Sot.

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Wilson, F. E., and Follett, B. K. pituitary luteinizing hormone trated tree sparrows (Spizella photoinduced gonadal cycle. crinol.

(1974). Plasma ahd in intact and casarborea) during a Gen. Comp. Endo-

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Witschi, E. (1955) Vertebrate gonadotrophins. Sot. Endocrinol. 4, 149.

Mem.