PHOTOPERIODIC RESPONSES of a SUBTROPICAL MIGRATORY FINCH, the BLACK-HEADED BUNTING (,?34Ll,%Iza Mel4ivocephm,A)

Condor84:168-171 0 The CooperOrnithological Society 1982

PHOTOPERIODIC RESPONSES OF A SUBTROPICAL MIGRATORY FINCH, THE BLACK-HEADED BUNTING (,?34ll,%IzA MEL4iVOCEPHM,A)

PRABHA D. TEWARY

AND VINOD KUMAR

ABSTRACT. -Groups of photosensitive male Black-headed Buntings (Emberiza melunocephala) were exposed to long (1 SW9D) and short (8W 16D) daily pho- toregimes for a period of 120 days. Another group of buntingswas simultaneously exposed to normal day lengths and served as a control. Birds were weighed and laparotomized at intervals of 30 days during the treatment period. The buntings exhibited photoperiodic responsessimilar to those of many north temperate birds from mid- and high latitudes. Long days caused complete gonadal development followed by rapid testicular regressionand photorefractoriness,whereas short days inhibited testicular development. Premigratory fattening followed by metabolic photorefractoriness also developed in photostimulated birds.

Day length regulatesthe annual cyclesof many buntings to long and short daily photoperiods species of birds (for reviews see Farner and in the laboratory. The present experiments Follett 1966, Lofts and Mm-ton 1968, Farner were designedto further our understandingof and Lewis 197 1). However, most of the abun- the environmental factors that control the an- dant literature concerning avian photoperi- nual cycles of birds residing at low latitudes, odism pertains to mid- and high latitude since so few of them have been studied. forms. The variation in day length at low latitudes may in fact be too small to provide birds MATERIALS AND METHODS with reliable cues for the timing of seasonal Adult male buntings were caught locally at events (Farner and Lewis 197 1). Nonetheless, Varanasi during fall 1978 and kept in an out- some tropical species are photoperiodic and door aviary. They were housedin small groups exhibit testicular development if exposed to in wire-net cages(50 X 35 X 30 cm). In early long daily photoperiods (Disney et al. 196 1, December, two groups were brought indoors Thapliyal and Saxena 1964a, Thapliyal and and allowed to acclimate to laboratory con- Tewary 1964, Epple et al. 1972, Lewis et al. ditions for 15 days. Here, they were exposed 1974). to natural variations of photoperiod and tem- The Black-headed Bunting (Emberiza mel- perature. Acclimated buntings were then put anocephalu)is a sexually dimorphic migratory on a short daily photocycle consisting of 8 h finch found in the subtropics.It arrives in Va- light and 16 h dark (8L/ 16D; lights on begin- ranasi, India (25”18’N, 83”01’E), in the fall ning at 06:OO) for eight weeks so that they (September/October), overwinters, and then would become photosensitive. Laparotomy at returns to breeding grounds in southwestern the end of this period showed that all birds Asia and eastern Europe (ca. 25-40”N) during had testesof minimal size (combined testicular the late spring (March/April;’ Ali and Ripley weight = 5-8 mg); they also had little subcu- 1974). It has distinct annual cycles of body taneous fat and weighed ca. 30 g. weight, fat deposition, and gonadal size. In One group of thesebirds (n = 8 initially) was nature, buntings undergo gonadal recrudes- then photostimulated with 15 h light daily cence and gain weight during the summer (15W9D; lights on beginning at 06:OO)for the (May/June) as day length increases,but their next 120 days. The other group (n = 7 initially) testes regressand weight diminishes in July, continued on 8W 16D. A third group of adults although the days are still quite long (unpubl. (n = 7 initially) having testes of minimal size observ.). These data suggestthat the Black- (combined testicular weight = 5-8 mg) was headed Bunting is photoperiodic and has pe- also brought indoors and subjectedto normal riods of reproductive and metabolic photore- day lengths (NDL) for the same 120-day pe- fractoriness in its annual cycles. We sought, riod. These birds received unrestricted natural therefore, to determine experimentally if the light through the northeast-facing windows of seasonalchanges exhibited by this finch in the the laboratory. A few birds died during the field were related to day length by exposing treatment period (see the group sizesin Table

[1@31 PHOTOPERIODIC RESPONSES OF BLACK-HEADED BUNTINGS 169

1). The artificial light to which birds in the first 500 - lSL/9D two groupswere exposed was provided by flu- I 0---06L/lSD orescent tubes and had an intensity of ca. 400 400- @--+NDL lx at perch level. Food and water were always freely available. We did not regulate the temperature of the photoperiodic chambersclosely, but it did not vary more than 2°C from the temperature of the bird room. 0 zoo- Birds were weighed and laparotomized at intervals of 30 days during the treatment period. The combined testicular weight of each was estimated visually by comparing the size of its testesin situ with a reference set of fixed gonads of known weight. (The error inherent in this method is ca. 20%.) Since the deposition of fat accounts for most of the weight gain of 0 30 60 90 120 photostimulated passerines(King and Famer DAYS 1959, Helms et al. 1967), we assumed that FIGURE 1. Gonadal responsesof Emberiza melano- variations in body weight reflected differences cephala to long (15U9D) and short (SL/ 16D) daily pho- in the fat content of the birds in this experi- toperiods, and to normal day lengths (NDL) at Varanasi, ment. India, between February and June. The vertical lines as- We performed statistical analyses on the sociatedwith the symbols are standard errors. data with simple t-tests, except when comparing the responsesof a single group of birds as a function of time, in which case we used ular size until 60 days of treatment (when day paired t-tests. length was 12.36 h). Testes were still growing and body weight was still increasing when we RESULTS terminated the study on day 120 (Table 1, Fig. When photostimulated (15L/9D), buntings 1). initially gained weight and exhibited testicular growth (days 30 and 60). Body and testicular DISCUSSION weight then declined (day 90) and were min- Our data indicate that the Black-headed Bunt- imal again on day 120 (Table 1, Fig. 1). In ing is photosensitive. Its photoperiodic re- contrast,buntings on a short daily photoperiod sponsesare similar to those of many north (SL/16D) failed to exhibit testicular recru- temperate birds, i.e., mid- and high latitude descence(Fig. 1). Although fattening (increases forms: long days cause full gonadal develop- in body weight) was not pronounced in these ment followed by rapid regression and pho- buntings, their average body weight on day torefractoriness, whereas short days inhibit 120 was significantly (P < 0.05) higher than testicular development (responses of north at the beginningof the treatment period (Table temperate forms are reviewed by Farner and 1). This weight gain was, however, relatively Follett 1966, Lofts and Murton 1968, and small compared with the increment that oc- Dolnik 1976). Such findings may mean that curred in the NDL group in the same period buntings use the length of the daily photope- (Table 1; NDL birds were experiencing day riod as a source of information for regulating lengths of ca. 13 h on day 120). their seasonalcycles, even though annual vari- Birds subjected to NDL did not exhibit a ations in day length at Varanasi are only about significant increasesin body weight or testic- 3 h 8 min.

TABLE 1. Changesin the body weight of Black-headed Buntings during exposureto long (15U9D) and short (8L/ 16D) daily photoperiods, and to the normal day lengths (NDL) of February through June at Varanasi, India.

Photoperiods’ I5U9D 8Ul6D NDL

0 29.25 f 0.73 (8) 28.14 2 0.40 (7) 28.28 + 0.49 (7) 30 a 41.87 -+ 0.81 (8)**** 28.66 ? 0.49 (6) 28.57 k 0.84 (7) ;: a 42.7534.80 f+ 2.06I .66 (8)****(5)** 29.6631.20 k2 1.691.65 (6)(5) a 47.0031.71 kf 0.741.89 (6)****(7)***

120 29.75 + 0.85 (4) 31.80 k 1.56 (5)* a 49.60 + 1.20 (5)****

1 Values m the table are X ? SEM (n). Asterisks in each column Indicate that the body weight differs from that on day 0 at a segnficance level of 0.05 (*) 0.02 (**) 0.01 (***), or 0.001 ( ****). The letter a on the left of a weght indicates that it differs significantly (P < 0.001) from the mean weight of the XL/ 16’D group dn that day. 170 PRABHA D. TEWARY AND VINOD KUMAR

As is true of many other migratory birds (see when exposed to short or long daily photo- King and Farner 1956, 1963; Farner 1960, periods (Thapliyal and Saxena 1964b, Pandha 1964; King 196 1; Dolnik 1975) premigratory and Thapliyal 1969). Spotted Munias (L. activities such as fattening are also induced in punctulata)respond to unnaturally short pho- buntingsby long daily photoperiods (Table 1). toperiods, but long photocycles retard or in- Short daily photoperiods usually fail to induce hibit gonadal development (Chandola et al. such events in migratory forms, but a small 1975). However, munias breed after the sum- significant (P < 0.05) increasein body weight mer solstice and their testicular cycles appear occurred when our buntings were kept on 8W to be regulated by environmental cues (e.g., 16D for about six months (including the pre- monsoons) other than those associated with treatment days; Table 1). It is immensely in- the photocycle. Yellow-vented Bulbuls (Pyc- teresting that these birds gained weight under nonotusgoiavier), which are also sedentary, conditions in which there was little (NDL) or appear to time bouts of reproductive activity no (8W16D) photostimulation. Response to by seasonalchanges in the food supply rather NDL and to long daily photoperiods suggests than day length (Fogden 1972). Red-billed that weight gain is in part related to the length Queleas (Quelea quelea)may also do this of the photocycle.However, the weight gain of (Jonesand Ward 1976) although they too are birds exposed to short days suggeststhat fat- photoperiodic and exhibit a brief refractory tening is also to some extent independent of period that dissipatesspontaneously irrespec- day length. Perhaps Black-headed Buntings tive of photoperiodic conditions (Lofts 1962). have a circannual rhythm in body weight; or, The photoperiodic responses of Black- perhaps the change was related to room tem- headed Buntings (Fig. 1) stand in contrast to perature which was not kept absolutely con- those presented above, but resemble those of stant. a related tropical migrant, the Red-headed Buntings on 15L/9D fattened initially, but Bunting (Emberiza bruniceps;Prasad 1980). then lost weight beginning sometime after 60 Both of these species are photoperiodic and days of photostimulation (Table 1). This sug- become refractory if retained on 15L/9D, re- geststhat they undergo metabolic refractori- sponsestypical of mid- and high latitude mi- ness when photostimulated, as do mid- and grants in the north temperate zone. However, high latitude migrants. Changes in the body it remains to be determined if exposure to a weight of our birds coincided remarkably with short daily photoperiod is necessaryto dissi- changes in their testicular size (compare the pate their refractory states, as it is in typical data in Table 1 with those in Fig. 1). This may north temperate migrants. indicate that gonadal steroids modify the intensity of such premigratory activities as hy- ACKNOWLEDGMENTS perphagia and fat deposition in Black-headed We thank A. van Tienhoven and M. D. Kern for their Buntings. Such effects have been reported oc- critical evaluation of this paper and suggestionsfor its casionally in other passerines(e.g., seeMorton improvement. The researchwas supportedby funds from and Mewaldt 1962, Weise 1967). However, the University Grants Commission of India. castrated buntings also fatten considerably when they are photostimulated (Tewary and LITERATURE CITED Kumar 198 1). ALI, S., ANDS. D. RIPLEY. 1974. Handbook of the birds Because the photoperiodic responsesof so of India and Pakistan. Vol. 10. Oxford Univ. Press, few tropical and subtropical passerineshave New York. CHANDOLA,A., J. PAVNASKAR,AND J. P. THAPLIYAL. been studied, it is still difficult to discern gen- 1975. Scoto/photoperiodicresponses of a subtropical eral patterns of photoperiodic responseamong finch (Spotted Munia) in relation to seasonalbreeding them. To illustrate, some sedentarylow-lati- cycle. J. Interdiscipl. Cycle Res. 6: 189-202. tude forms, including Baya Weavers (Ploceus DISNEY,H. J. DES., B. LOFTS,AND A. J. MARSHALL.196 1. An experimental study of the internal rhythm of re- philippinus)and Rufous-collared Sparrows production in the Red-billed Dioch, Quelea quelea, (Zonotrichiacapensis), show testicular recru- by means of photostimulation, with a note on mel- descencein responseto long daily photoperi- anism induced in captivity. Proc. Zool. Sot. Lond. ods, but do not become photorefractory 136:123-129. (Thapliyal and Saxena 1964a, Thapliyal and DOLNIK,V. 1975. Fotoperiodicheskiikontrol sezonnykh tsiklov vesatela, linki i polovoi aktivnosti u zyablikov Tewary 1964, Lewis et al. 1974). In thesecases, (Fringilla coelebs).Zool. Zh. 54:1048-1056. testicular activity ceaseswhen the natural day DOLNIK, V. 1976. Fotoperiodizm u ptits, p. 47-81. In length diminishes in autumn (but see Singh V. A. Zaslavsky [ed.], Fotoperiodizm zhivotnykh i and Chandola 198 1). However, other seden- rastenii. Akademiya Nauk S.S.S.R., Leningrad. EPPLE,A., G. H. ORIANS,D. S. FARNER,AND R. A. LEWIS. tary forms respond to long days in a more 1972. The photoperiodic testicular response of a complex fashion. Black-headed Munias (Lon- tropical finch, Zonotrichia capensis costaricensis. churamolucca) become reproductively active Condor 74: l-4. PHOTOPERIODIC RESPONSES OF BLACK-HEADED BUNTINGS 171

FARNER,D. S. 1960. Metabolic adaptationsin migration. of reproduction in an equatorial bird, Quelea quelea. Proc. XII Int. Omithol. Congr. (1958): 197-208. Ibis 104:407-4 17. FARNER,D. S. 1964. The photoperiodic control of re- LOFTS,B., AND R. K. MURTON. 1968. Photoperiodic and productive cyclesin birds. Am. Sci. 52: 139-l 56. physiological adaptations regulating avian breeding FARNER,D. S., AND B. K. FOLLETT.1966. Light and other cycles and their ecological significance. J. Zool. environmental factors affecting avian reproduction. 155327-394. J. Anim. Sci. 25:90-l 15. MORTON,M. L., AND L. R. MEWALDT. 1962. Some effects FARNER,D. S., AND R. A. LEWIS. 1971. Photoperiodism of castration on a migratory sparrow (Zonotrichia and reproductive cycles in birds, p. 325-370. In A. atricapilla). Physiol. Zool. 35~237-247. C. Giese [ed.], Photophysiology:current topicsin pho- PANDHA,S. K., AND J. P. THAPLIYAL. 1969. Light and tochemistry and photobiology. Vol. 6. Academic the gonadal cycle of the BlackheadedMunia, Munia Press, New York. malacca malacca. Endocrinol. Jpn. 16:157-l 6 1. FOGDEN,M. P. L. 1972. The seasonalityand population PRASAD,B. N. 1980. Photoperiodic control of reproduc- dynamics of equatorial forest birds in Sarawak. Ibis tion in some Indian birds. Ph.D. diss., BanarasHindu 114:307-342. Univ., Varanasi, India. HELMS,C. W., W. H. AUSSIKER,E. B. BOWER,AND S. D. SINGH, S., AND A. CHANDOLA.198 1. Photoperiodic con- FRETWELL.1967. A biometric study of major body trol of seasonalreproduction in tropical Weaver Bird. components of the Slate-colored Junco, Bunco /rye- J. Exp. Zool. 2 16:293-298. malis. Condor 69~560-578. TEWARY,P. D., AND V. KUMAR. 1981. Effect of castration JONES,P. J., AND P. WARD. 1976. The level of reserve on photoperiodically induced weight gain in a migra- protein as the proximate factor controlling the timing tory finch: BlackheadedBunting. Indian J. Exp. Biol. of breeding and clutch-size in the Red-billed Ouelea._ 19:469471. Quelea q&lea. Ibis 118:547-574. THAPLIYAL,J. P., AND R. N. SAXENA. 1964a. Absence of KING, J. R. 1961. On the regulation of vernal premigra- refractory period in common Weaver Bird, Ploceus tory fatteningin the White-crowned Sparrow.Physiol. philippinus.Condor 66:199-208. Zool. 34:145-157. THAPLIYAL,J. P., AND R. N. SAXENA. 1964b. Gonadal KING, J. R., AND D. S. FARNER. 1956. Bioenergeticbasis development of male BlackheadedMunia under con- of light-induced fat deposition in the White-crowned stant nine-hour (short) days. J. Exp. Zool. Sparrow. Proc. Sot. Exp. Biol. Med. 93:354-359. 156:153-156. KING, J. R., AND D. S. FARNER. 1959. Premigratory THAPLIYAL,J. P., AND P. D. TEWARY. 1964. Effect of changesin body weight and fat in wild and captive light on the pituitary, gonad and plumage pigmen- male White-crowned Sparrows.Condor 6 1:315-324. tation in the Avadavat, Estrilda amandava, and Baya KING, J. R., AND D. S. FARNER. 1963. The relationship Weaver, Ploceusphilippinus. Proc. Zool. Sot. Lond. offat depositionto Zugunruheand migration. Condor 142:67-71. 65:20&223. WEISE,C. M. 1967. Castration and spring migration in LEWIS,R. A., J. R. KING, AND D. S. FARNER. 1974. Pho- the White-throated Sparrow. Condor 69:49-68. toperiodic responsesof a subtropical population of the finch Zonotrichia capensishypoleuca. Condor Department of Zoology, Banaras Hindu University, Va- 761233-237. ranasi 221 005, India. Received 22 April 1981. Final ac- Lams, B. 1962. Photoperiod and the refractory period ceptance 19 November 1981.

Condor84:171 0 The CooperOrnithological Society 1982

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